MASARYKOVA UNIVERZITA
Přírodovědecká fakulta
Jana Schenková
Ekologie opaskovců: variabilita druhové skladby,
habitatové preference a odpovědi na gradienty
prostředí máloštětinatců a pijavic
Habilitační práce
Brno 2016
Poděkování
Podklady pro tuto práci vznikly jako výsledek tvůrčí součinnosti se spoluautory, protože
hydrobiologická práce není solitérní, ale většinou probíhá v úzce spolupracujícím týmu
kolegů i studentů, jejichž činnosti jsou propojeny a za tuto spolupráci jim moc děkuju. Nikdy
bych se taky neobešla bez kolegů zajišťujících technické zázemí pro jednotlivé výzkumy,
Marcelky Růžičkové a Standy Němejce. Můj dík pak patří Světlaně Zahrádkové, která mi
kdysi nabídla volnou „niku“ v podobě studia kroužkovců, Honzovi Helešicovi, jehož vedení
projektů, na kterých jsem pracovala, podporovalo samostatnost a tvůrčí úsilí. Také všichni
kolegové na ÚBZ, kteří se zde zasloužili o milou atmosféru, zahrnující i dnes už málo
vídanou altruistickou pomoc, přispěli k pohodě na práci. A nakonec moc děkuju celé rodině,
za vědeckou podporu tatínkovi, i novému členu rodiny Michalu Horsákovi, Verče za trpělivé
přečtení celého textu a kritické připomínky a za všeobecnou podporu manželovi Michalovi
(heslo: to dáš!), Robinovi, za to, že skládá krásnou hudbu, a mamince za vše.
Obsah
1. Struktura a cíle habilitační práce 6
2. Shrnující komentář 7
2.1 Úvod do problematiky 7
2.2 Biologie sladkovodních opaskovců (Clitellata) 9
2.2.1 Biologie máloštětinatých opaskovců („Oligochaeta“) 9
2.2.2 Biologie pijavic (Hirudinida) 13
2.3 Druhová diverzita opaskovců a její změny podél gradientů prostředí 16
2.3.1 Druhová diverzita opaskovců (Clitellata) 16
2.3.1.1 Máloštětinatí opaskovci („Oligochaeta“) na území České
republiky 16
2.3.1.2 Pijavice (Hirudinida) na území České republiky 18
2.3.2 Variabilita druhové skladby máloštětinatých opaskovců v tocích 21
2.3.3 Variabilita druhové skladby máloštětinatých opaskovců
na prameništních slatiništích 24
2.3.4 Změny společenstva opaskovců v otepleném toku 27
2.3.5 Variabilita druhové skladby pijavic v tekoucích a stojatých
vodách 29
2.4 Odpovědi vybraných druhů opaskovců na různé proměnné prostředí
– malá a velká škála 31
3. Závěr 36
4. Literatura 37
5. Seznam publikovaných vědeckých prací v ISI časopisech k tématu habilitační
práce 45
5.1 Druhová diverzita máloštětinatých opaskovců a její změny podél
gradientů prostředí 45
[1] Schenková, J., O. Komárek & S. Zahrádková, 2001. Oligochaeta of the
Morava and Odra River basins (Czech Republic): species distribution and
community composition. Hydrobiologia, 463, 235–240. (IF 2,21)
[2] Schenková, J. & J. Helešic, 2006. Habitat preferences of aquatic Oligochaeta
(Annelida) in the Rokytná River, Czech Republic – a small highland stream.
Hydrobiologia, 564, 117–126. (IF 2,21)
[3] Schenková, J., J. Helešic & J. Jarkovský, 2006. Seasonal dynamics of
Bythonomus lemani and Bothrioneurum vejdovskyanum (Oligochaeta,
Annelida) in relation to environmental variables. Biologia, 61, 517–523. (IF
0,7)
[4] Syrovátka, V., J. Schenková & K. Brabec, 2009. The distribution of
chironomid larvae and oligochaetes within a stony-bottomed river stretch: the
role of substrate and hydraulic characteristics. Fundamental and Applied
Limnology, Archiv für Hydrobiologie, 174, 43–62. (IF 1,0)
[5] Schenková, J., P. Pařil, K. Petřivalská & J. Bojková, 2010. Aquatic
oligochaetes (Annelida: Clitellata) of the Czech Republic: check-list, new
records, and ecological remarks. Zootaxa, 2676, 29–44. (IF 1,06)
[6] Křoupalová, V., J. Bojková, J. Schenková, P. Pařil & M. Horsák, 2011.
Small-scale distribution of aquatic macroinvertebrates in two spring fens with
different groundwater chemistry. International Review of Hydrobiology, 96,
235–256. (IF 1,01)
[7] Bojková, J., J. Schenková, M. Horsák & M. Hájek, 2011. Species richness
and composition patterns of clitellate (Annelida) assemblages in the treeless
spring fens: the effect of water chemistry and substrate. Hydrobiologia, 667,
159–171. (IF 2,21)
[8] Růžičková, S., J. Schenková, V. Weissová & J. Helešic, 2014.
Environmental impact of heated mining waters on clitellate (Annelida:
Clitellata) assemblages. Biologia, 69(9), 1179–1189. (IF 0,70)
[9] Schenková, J., M. Bílková & M. Horsák, accepted 27.1.2016. The response
of Clitellata (Annelida) to environmental gradients in spring fens.
Limnologica. (IF 1,80)
5.2 Druhová diverzita pijavic a její změny podél gradientů prostředí 186
[10]Schenková, J., J. Jarkovský & J. Helešic, 2007. Strategies of coexistence of
two species: Erpobdella octoculata and E. vilnensis (Hirudinea:
Erpobdellidae). International Review of Hydrobiology, 92(4–5), 527–538. (IF
1,013)
[11]Schenková, J., J. Sychra, V. Košel, N. Kubová & J. Horecký, 2009.
Freshwater leeches (Annelida: Clitellata: Hirudinida) of the Czech Republic
(Central Europe): check-list, new records, and remarks on species
distributions. Zootaxa, 2227, 32–52. (IF 1,06)
[12] Kubová, N., J. Schenková & M. Horsák, 2013. Environmental determinants
of leech assemblage patterns in lotic and lenitic habitats. Limnologica, 43,
516–524. (IF 1,66)
[13]Kubová, N. & J. Schenková, 2014. Tolerance, optimum ranges and
ecological requirements of free-living leech species (Clitellata: Hirudinida).
Fundamental and Applied Limnology, Archiv für Hydrobiologie, 185(2),
167–180. (IF 1,00)
6. Seznam dalších publikací a vystoupení k tématu habilitační práce 247
6
1. Struktura a cíle habilitační práce
Předkládaná habilitační práce se skládá z 12 vědeckých prací opublikovaných v ISI
časopisech a jednoho rukopisu přijatého do ISI časopisu. Všechny jsou zaměřeny na studium
ekologie dvou největších skupin opaskovců (Clitellata): máloštětinatých opaskovců
„Oligochaeta“ a pijavic Hirudinida. Jde o významné zástupce bentické fauny obývající
v našich podmínkách bahnité i kamenité substráty všech vodních ekosystémů od pramenišť,
toků, rybníků, jezer a nádrží až po hyporeické vody. Široký rozsah citlivosti ke znečištění
předurčuje tuto skupinu k využití jak v terénních výzkumech, tak v laboratorních pokusech.
Výsledky studií máloštětinatých opaskovců a pijavic jsou v předkládané práci souhrnně
představeny a doplněny současným fylogenetickým postavením studovaných skupin a
úvodem k jejich biologii. Práce se zabývají odpovědí opaskovců na gradienty prostředí a pro
konkrétní druhy vyhodnocují jejich ekologické valence. Rozšíření znalostí o této skupině
přispívá k jejich základnímu poznání a posouvá hranice možností bioindikace stavu
sladkovodních ekosystémů na základě jejich ekologických preferencí a umožňuje i lépe
chránit druhy vzácné.
Hlavní cíle habilitační práce:
1. Popsat diverzitu opaskovců na území České republiky a sestavit aktuální check-listy
pro máloštětinaté opaskovce a pijavice.
2. Popsat variabilitu druhové skladby máloštětinatců a pijavic v různých akvatických
biotopech, především v tekoucích vodách.
3. Najít hlavní gradienty prostředí, které ovlivňují tuto variabilitu a vyhodnotit indikační
potenciál skupiny.
4. Zjistit odpověď společenstva máloštětinatců na antropogenní ovlivnění lokalit
5. Vyhodnotit habitatové preference vybraných druhů máloštětinatců a pijavic
7
2. Shrnující komentář
2.1 Úvod do problematiky
Nejznámější skupiny opaskovců – máloštětinatci a pijavice nepatří mezi bezobratlými
živočichy ke skupinám oblíbeným laickou veřejností, snad vyjma rybářů. Žížaly mohou
vzbuzovat nepříjemné pocity, neboť vylučují na povrchu sliz a pijavic se lidé podvědomě
bojí, neboť jim evoluční zkušenost říká, že by je mohly napadnout a přenášet choroby. Přesto
představují fascinující skupiny kroužkovců (Annelida), které osídlily jak akvatické
(sladkovodní a mořské), tak suchozemské biotopy a dosáhly zde vysoké diverzity.
Skupina opaskovci (Clitellata) představuje druhově bohatý taxon, zahrnující téměř
třetinu z 15000 druhů kroužkovců (Annelida) (Erséus 2005). Název opaskovci je odvozen od
žláznaté epidermální struktury ve tvaru kruhu nebo sedla kolem těla nazývané opasek
(clitellum), který se vytváří v době rozmnožování a napomáhá přenosu pohlavních buněk a
později tvorbě kokonů. Jeho přítomnost je jedním z morfologických znaků potvrzujících
monofylii tohoto taxonu kroužkovců (Ferraguti & Erséus 1999, Purschke 1999, Westheide et
al. 1999), prokázanou i na základě sekvencí DNA (McHugh 1997, Siddall et al. 2001 a
Erséus & Källersjö 2004). Pozice opaskovců uvnitř kroužkovců (Annelida) zůstává stále
vysoce neurčitá, pravděpodobně leží někde mezi „mnohoštětinatci“ a stále není zcela jasná ani
její sesterská skupina (Jördens et al. 2004, Rousset et al. 2006). Také fylogenetické vztahy
uvnitř opaskovců jsou složitější, než by ukazovalo tradiční dělení opaskovců (Clitellata) na
základě morfologických znaků na Oligochaeta a Hirudinea, které se dále dělily na pravé
pijavice (Euhirudinea) a na pijavicím podobné („leech-like“) taxony štětinovky
(Acanthobdellida) a potočnice (Branchiobdellida) (Sawyer 1986, Brusca & Brusca 1990,
Rouse & Fauchald 1995). V současnosti, přesto že každá další molekulární analýza přináší
odlišnosti v detailech, nastala zásadní shoda ve zjištění, že Hirudinida (pravé pijavice),
Branchiobdellida (komenzálové nebo parazité raků) a Acanthobdellida (skupina
představovaná jediným reliktním druhem Acanthobdella peledina Grube, 1851 parazitujícím
na lososovitých rybách) představují samostatnou větev opaskovců, jejímž společným předkem
byl máloštětinatý červ blízce příbuzný žížalicovitým Lumbriculidae (Martin 2001, Erséus
2005, Marotta et al. 2008). Složitost situace dokresluje, že existuje podpora i pro
monofyletický taxon zařazující Lumbriculidae dovnitř tohoto taxonu společně s
Acanthobdellida, Branchiobdellida a Hirudinida (Rousset et al. 2008). Nicméně
máloštětinatci jako validní taxon definitivně zanikají a pro tuto parafyletickou část opaskovců
8
Clitellata se zavádí označení máloštětinatí opaskovci – „oligochaetous Clitellata“ či
„Oligochaeta“ s použitím uvozovek.
Studium evoluce habitatových preferencí skupiny Clitellata ukázalo, že společný předek
obýval původně akvatické bitopy (Erséus & Källersjö 2004), přesněji řečeno sladkovodní
biotopy (Rousset et al. 2008). Zástupci čeledi Naididae (sensu Erséus et al. 2008) s asi 800
popsanými druhy obývali nejprve sladké vody a sekundárně se pak rozšířili také do
brakických a mořských. I o monofylii této skupiny dnes zahrnující podčeledi Naidinae,
Pristininae, Tubificinae, Rhyacodrilinae (a Telmatodrilinae, Phallodrilinae a
Limnodriloidinae, které se u nás nevyskytují) ovšem existují určité pochybnosti (Rousset et
al. 2008). Část z nich pak opustila typický život v sedimentech dna a naučila se obývat jejich
povrch a povrch vodních rostlin (podčeledi Naidinae a Pristininae). K takovému životnímu
stylu jim napomáhá častá přítomnost očních skvrn a schopnost plavat. Někteří z nich (rody
Dero a Ripistes) si navíc staví na povrchu substrátu tenké trubičky, kterými se chrání. Ve
stojatých vodách s množstvím drobných bezobratlých se pak některé druhy z podčeledi
Naidinae uchýlily k získávání potravy predací, jako např. rod Chaetogaster (Obr. 1a).
Další skupina dnes především terestrických máloštětinatců skupiny Crassiclitellata
zahrnující 3000 validních druhů, u nás zastoupených čeledí žížalovití Lumbricidae, měla
pravděpodobně naopak předka terestrického. Jejich trávicí soustava je přizpůsobena ke
zpracování organického materiálu pohlceného současně s částicemi půdy přítomností baktérií,
hub a prvoků, které umožňují trávení celulózy a rozklad organické hmoty. Podle ekologie je
můžeme rozdělit na epigeické (žijící na povrchu půdy a v listovém opadu), endogeické (žijí
v půdě v horizontálních trubičkách) a anektické (žijící ve vertikálních trubičkách, do kterých
si zatahují listy, které zpracovávají) (Bouché 1977). Druhá dnes převážně půdní skupina
roupicovití Enchytraeidae čítající asi 650 druhů pak pochází z vodního prostředí a k osídlení
půdy došlo až sekundární invazí (Rousset et al. 2008). Dnes obývají většinou svrchní vrstvu
půdy, i když i mezi nimi najdeme sladkovodní (např. rod Cognettia) i mořské zástupce (např.
někteří zástupci rodů Marionina a Lumbricillus).
Pijavicím podobné skupiny (Acanthobdellida, Branchiobdellida a Hirudinida), ať už
s čeledí Lumbriculidae nebo bez ní, dnes obývají sladkovodní biotopy stejně jako jejich
předek (či předkové) (Rousset et al. 2008). Také v čeledi žížalicovití (Lumbriculidae) se
objevily druhy, které osídlily rostlinné habitaty místo sedimentů dna (např. Lumbriculus
variegatus (Müller, 1774) a i u nich se pak vyvinula schopnost plavat. Pijavicím podobné
9
skupiny se naopak přizpůsobily karnivornímu způsobu života. Vznikla u nich zadní přísavka,
sloužící k přichycení k substrátu či kořisti, došlo k redukci štětin, vytvořil se svalnatý hltan a
různý počet očních skvrn na přídě (předním konci těla), které umožňují orientaci (Obr. 1b).
Obrázek 1. Příklad volně žijícího máloštětinatého opaskovce Chaetogaster diastrophus (Gruithuisen, 1828) (a),
velikost 3 mm (preparát v Kanadském balzámu) a volně žijící pijavice Glossiphonia complanata (Linnaeus,
1758) (b), velikost 15 mm (živý jedinec). Foto J. Schenková
2.2 Biologie sladkovodních opaskovců (Clitellata)
Přesto, že některé znaky skupiny Clitellata jako přítomnost opasku, nepřítomnost
parapodií, omezení počtu gonád jen na několik článků a přímý vývoj juvenilních jedinců po
uvolnění z kokonů jsou pro celou skupinu shodné, celková biologie dvou hlavních skupin –
máloštětinatců a pijavic je natolik rozdílná, že si každá zaslouží samostatné pojednání.
2.2.1. Biologie máloštětinatých opaskovců („Oligochaeta“)
Stavba těla máloštětinatých opaskovců skupiny „Oligochaeta“ se podobá typickému
tělnímu plánu kroužkovců s homonomní segmentací těla. Odlišuje se jen první článek
(peristomium) s ústním otvorem a čelním lalokem (prostomium) na předním konci těla, který
se také nazývaná přída, a pygidium (poslední článek tvořený jedním nebo srůstem více
a b
10
článků) na jeho zadním konci. Počet tělních článků je variabilní od 7 po asi 200, pro
jednotlivé druhy je pak relativně stálý. Každý tělní článek kromě prvního je opatřen primárně
4 svazky chitinózních štětin, které napomáhají při pohybu. Máloštětinatci se vrtají v substrátu
či pohybují po jeho povrchu peristaltickými kontrakcemi podkožní svaloviny s oporou o
štětiny. Některé druhy mohou plavat (např. z rodu Stylaria a Pristina) hadovitým pohybem
těla. „Oligochaeta“ se živí primárně jako neselektivní detritofágové, zpracovávají detrit spolu
s bakteriemi a organickými zbytky, anorganické částice pak nestrávené odchází z těla análním
otvorem. Ovšem mýtus, že máloštětinatci se živí jakoukoli potravou, se kterou se setkají, byl
vyvrácen laboratorními pokusy na druhu Tubifex tubifex (Müller, 1774), který si dokáže
selektivně vybírat potravu s částicemi menšími než 25 µm a z bahnitého substrátu vyžírá ten,
který obsahuje nejvíce organické hmoty (Rodriguez et al. 2001). Některé druhy se živí na
uhynulých tělech ryb (zástupci čeledi Enchytraeidae). Drobní máloštětinatci z podčeledí
Naidinae a Pristininae žijící na rostlinách se živí detritem a nárostovými řasami, zejména
rozsivkami. Pomocí svaloviny hltanu vysouvaného z dutiny ústní přichytávají podtlakem
potravu a jejím zatažením zpět ji odtrhují od substrátu (Sperber 1948), takto dokážou do
trávicího traktu vtáhnout i vláknitou řasu. Velmi drobní zástupci rodu Chaetogaster se živí
jako predátoři, široce roztaženou přídou vychytávají z vody prvoky a drobné bezobratlé
živočichy – vířníky, korýše a larvy hmyzu, v jejich trávicím traktu se nachází i zástupci „své
skupiny“ tedy drobní máloštětinatci (Obr. 1a, v tělní dutině je vidět kořist, máloštětinatý
opaskovec z podčeledi Naidinae). V České republice velmi vzácný druh Ripistes parasita
(Schmidt, 1847) se živí jako pasivní filtrátor, který vychytává potravu z proudu vody pomocí
svazku dlouhých a hustých štětin v VI.–VIII. segmentu. V pravidelných intervalech pak otáčí
přídu k zadnímu konci těla a protaženým prostomiem vybírá nachytané částice potravy.
Vzácně se vyvinul i parazitický způsob života: druh Chaetogaster limnaei Baer, 1827 žije na
povrchu ulit a v plášťové dutině plovatek, kde se živí nejen drobnými prvoky a bezobratlými,
ale může ožírat i epitel plášťové dutiny hostitele.
Skupina máloštětinatí opaskovci („Oligochaeta“) vyvinula velmi úspěšné reprodukční
strategie. U podčeledí Naidinae a Pristininae probíhá nepohlavní rozmnožování formou tzv.
paratomie, kde mateřský jedinec na zadním konci tvoří řetízky dceřiných jedinců, tzv. zoidů,
kteří ještě před oddělením mají plně vyvinuté prostomium, včetně např. chobotku (proboscis).
Místa budoucího dělení jsou pevně dána a typická pro každý druh. Toto rozmnožování
probíhá především v jarním období. U poměrně vzácného druhu Pristina bilobata (Bretscher,
1903), který žije spíše v podhorských oblastech, se pak asexuální reprodukce posouvá do
11
letního období (Obr. 2) a k sexuálnímu nemusí docházet vůbec, jak bylo pozorováno na řece
Morávce (Schenková & Kroča 2007). Paratomické rozmnožování se může střídat s pohlavní
reprodukcí, většinou před zimním obdobím.
Obrázek 2. Sezonní změny
abundance u druhu Pristina
bilobata, reprodukujícího se
paratomií. Mapa jeho nálezů
v České republice. Více viz
Schenková & Kroča (2007),
odkud byl obrázek převzat a
upraven; do mapy byly doplněny
dva současné nálezy.
Druhým typem asexuální reprodukce je architomické dělení, kdy nejprve dochází
k fragmentaci dospělého jedince a teprve pak k diferenciaci koncových částí těla. Vyskytuje
se např. u podčeledi Tubificinae, u rodu Aulodrilus, podčeledi Rhyacodrilinae, u druhu
Bothrioneurum vejdovskyanum Štolc, 1886 a čeledi Lumbriculidae, kde je typické pro druh
Lumbriculus variegatus. Nepohlavní architomické rozmnožování probíhá opět nejčastěji
v jarním a na začátku letního období. Např. u druhu B. vejdovskyanum se mateřský jedinec
s asi 140 segmenty rozpadá v průměru na šest částí v období od poloviny dubna a
rozmnožování probíhá po celé letní období (Hrabě 1935). Podobně i v případové studii na
řece Rokytné byl zaznamenán vývojový cyklus se zvyšováním denzity v průběhu května a
Obrázek 3. Analýza časové řady průměrných denzit (a) a peridiogram, tj. graf počtu cyklů za rok (b)
architomicky se množícího druhu Bothrioneurum vejdovskyanum. Blíže viz Schenková et al. 2006, odkud byly
obrázky převzaty.
Bothrioneurum vejdovskyanum
V.99
VII.99
IX.99
XI.99
I.00
III.00
V.00
VII.00
IX.00
XI.00
I.01
III.01
0
20
40
60
80
100
120
18.4.03
16.5.03
8.6.03
11.7.03
2.8.03
1.9.03
22.9.03
20.10.03
20.11.03
12.03
12.1.04
17.2.04
3.04
6.4.04
1.5.04
9.6.04
16.7.04
-10
0
10
20
30
40
50
60
70
80
Průměrnáabundance(n)ateplota(°C)
teplota
Pristinella bilobata
Loučka
Morávka
Jasénka
Obidová
Bothrioneurum vejdovskyanum
0 1 2 3 4 5 6 7
cycles/year
0,0
0,2
0,4
0,6
0,8
1,0
1,2
1,4
1,6
1,8
2,0Bothrioneurum vejdovskyanum a Bothrioneurum vejdovskyanum b
12
maximem v červnu, ovšem jen v prvním roce pozorování (Obr. 3a), dvouleté období
pozorování bylo pravděpodobně nedostatečné (Schenková et al. 2006). Pohlavně dospělí
jedinci se vyskytovali jen zcela sporadicky; celkově byl u tohoto druhu vyhodnocen jednoletý
vývojový cyklus (Obr. 3b) (Schenková et al. 2006). Architomické rozmnožování se opakuje
pravidelně a nebylo prokázáno, že by jej ovlivňovaly některé z parametrů prostředí jako
teplota vody, průtok, rozpuštěný kyslík nebo množství organické hmoty v toku (Schenková et
al. 2006).
U některých druhů se také vyvinulo partenogenetické rozmnožování, kdy juvenilní
jedinci vznikají z neoplodněných vajíček, např. u čeledi Lumbricidae (Sims & Gerard 1999).
Nejvýznamnější způsob reprodukce máloštětinatých opaskovců ovšem představuje
rozmnožování pohlavní. Zástupci této skupiny jsou hermafrodité s přímým vývojem.
Kopulace probíhá spojením dvou jedinců proti sobě v opačném směru, tj. přída jednoho ke
kaudální části druhého. Opasky obou jedinců jsou přiloženy k sobě a sliz, který produkují,
umožňuje přenos pohlavních buněk. Vývod chámovodu jednoho jedince ústí do chámových
schránek (receptaculum seminis) druhého jedince (a naopak). Jedinci si předávají shluky
spermií (spermatozeugma) nebo spermatofory (shluky spermií s obalovou vrstvou). Přenos je
u některých druhů usnadněn přítomností různě dlouhých penisů, které mohou být vyztuženy
peniálními trubkami, jejichž tvar je druhově specifický a představuje dobrý determinační
znak. Obdobně štětiny, které mohou být v oblasti opasku u některých druhů upravené jako
spermatekální, jsou často lopatkovitě zakončené a slouží k přenosu spermatozeugmat při
kopulaci. K oplodnění vajíček dochází v hlenovém pouzdře, produkovaném buňkami opasku,
do něhož se vajíčka uvolňují a posunují směrem k přednímu konci jedince, při průchodu
kolem vývodu chámových schránek jsou oplodněna. Hlenové pouzdro s oplodněnými vajíčky
se svléká přes přídu jedince a vytváří kokon, jehož tvar, struktura a počet vajíček uvnitř je
specifický pro jednotlivé druhy/rody máloštětinatých opaskovců.
V současnosti je problematika pohlavního rozmnožování mnoha druhů zejména
z podčeledi Tubificinae, které se vyskytují ve znečištěných vodách, velmi dobře
prostudována, např. Tubifex tubifex, Limnodrilus hoffmeisteri Claparède, 1862 a L.
udekemianus Claparède, 1862, (Ladle 1971, Bonomi 1979, 1980, Pfannkuche 1981, Lazim &
Learner 1986, Lazim et al. 1989). Také další běžné druhy z této podčeledi jsou z hlediska
sezonní dynamiky dobře probádané: Potamothrix hammoniensis (Michaelsen, 1901)
(Thorhauge 1976, Risnoveanu & Vadineanu 2002), Psammoryctides barbatus (Grube, 1861)
and Spirosperma ferox Eisen, 1879 (Adreani et al. 1984). Podčeledi Naidinae a Prisitininae
13
jsou dobře zpracovány např. v rozsáhlé studii (Learner et al. 1978). Méně známé jsou
reprodukční cykly u druhů, které se vyskytují buď vzácně, nebo je jejich determinace spojena
s určitými obtížemi. U čeledi Lumbriculidae, kde je dobře prostudovaná sezonní dynamika u
druhů Stylodrilus heringianus Claparède, 1862 a S. parvus (Hrabě-Černosvitov, 1927)
(Dumnicka & Kukuła 1990, Petto & Humpesch 1992) najdeme i druhy z tohoto hlediska
velmi málo prostudované, jako např. Stylodrilus lemani (Grube, 1879). Tento druh se množí
pohlavně; v případové studii na řece Rokytné probíhal vývoj v jednoletém cyklu, kdy
v jarním období vzrůstající teplota stimulovala vývoj pohlavních orgánů a následně kopulaci
jedinců, v období srpna až listopadu narůstal počet juvenilních jedinců (Obr. 4) (Schenková et
al. 2006). Byla nalezena pozitivní korelace abundance tohoto druhu s teplotou vody s dvou
měsíčním posunem (lagem) a rozdílné habitatové preference juvenilních jedinců (příbřežní
partie) a dospělců (proudnice toku) (Schenková et al. 2006).
Obrázek 4. Analýza časové řady průměrných denzit (a) a peridiogram, tj. graf počtu cyklů za rok (b) pohlavně
se množícího druhu Stylodrilus lemani. Blíže viz Schenková et al. 2006, odkud byly obrázky převzaty.
2.2.2 Biologie pijavic (Hirudinida)
Tělo pijavic je dorzoventrálně zploštělé, výrazně uniformní, tvořené vždy 34 články, na
předním konci je opatřeno menší přísavkou s ústním otvorem, na zadním konci větší
přísavkou, vzniklou splynutím sedmi článků, sloužící k pohybu a přichycení k podkladu.
Stavba těla pijavic odráží jejich dravý či parazitický způsob života. Měkké tělo
máloštětinatých opaskovců, jehož oporou je hlavně hydrostatická kostra, je u této
specializované skupiny zpevněno mohutným svalovým vakem, který spolu
s parenchymatickou tkání zatlačil tělní dutinu. Pijavice ztratily přepážky mezi segmenty,
štětiny a segmentovanou célomovou dutinu se změnou způsobu pohybu od peristaltického
vrtání v substrátu k pohybu lezením a plaváním. Mohutná svalovina slouží ke kontrakci těla
Stylodrilus lemani
V.99
VII.99
IX.99
XI.99
I.00
III.00
V.00
VII.00
IX.00
XI.00
I.01
III.01
0
5
10
15
20
25
30
35
40
45
50
Stylodrilus lemani
0 1 2 3 4 5 6 7
cycles/year
0,0
0,2
0,4
0,6
0,8
1,0
1,2
1,4
1,6
1,8
2,0Stylodrilus lemani a Stylodrilus lemani b
14
při pohybu po podkladu, který se děje píďalkovitým pohybem pomocí obou přísavek, a
při plavání, které probíhá dorzoventrální undulací. Na rozdíl od máloštětinatých opaskovců,
kde jsou oční skvrny přítomny jen u podčeledi Naidinae a nemají podstatný vliv na nacházení
potravy, pijavice mají vždy na přídě několik párů očí sloužících k vyhledávání kořisti či
hostitele.
Pijavice se živí jako krevsající (hematofágní) parazité a predátoři. Ty, které se živí krví,
mají buď kutikulární čelisti se zoubky, jako např. pijavka lékařská (Hirudo medicinalis
Linnaeus, 1758) (Obr. 5) z řádu čelistnatky (Gnathobdellida) nebo sají krev z hostitele pomocí
chobotku jako zástupci řádu chobotnatky (Rhynchobdellida). H. medicinalis, která se
v České republice řadí ke kriticky ohroženým druhům (Schenková & Košel 2005), se živí krví
obratlovců. Sání krve umožňuje pijavkám přítomnost protisrážlivého enzymu hirudinu.
Drobné juvenilní pijavky nejsou schopny
prokousnout kůži savců, proto se živí na
obojživelnících (Sawyer 1986). Dospělci sají
krev obojživelníků, ptáků, případně ryb, ale
dominantním zdrojem potravy je savčí krev,
kterou potřebují jakožto energeticky
nejbohatší, aby mohly dosáhnout pohlavní
dospělosti (Mann 1955). Pijavky se zdržují na
hostiteli jen v době sání, kdy se jejich
hmotnost zvýší až 9x, protože bez další
potravy mohou vydržet až jeden rok (Davies &
McLoughlin 1996). Z čeledi Piscicolidae se
parazitické druhy náležících do rodů Piscicola
a Caspiobdella živí krví ryb, kterou sají pomocí vysouvatelného chobotku. Zatímco zástupci
rodu Piscicola tráví celý život přichycení na hostiteli, zástupci rodu Caspiobdella žijí na dně
tekoucích vod a rybího hostitele navštěvují jen kvůli sání. V čeledi Glossiphoniidae se
parazitické druhy živí ektoparaziticky sáním krve ryb – Hemiclepsis marginata (O. F. Müller,
1774) nebo ptáků – Theromyzon tessulatum (O. F. Müller, 1774), který parazituje v nosní
dutině kachen.
Ostatní zástupci pijavic naší fauny se živí jako predátoři bezobratlých. Haemopis
sanguisuga (Linnaeus, 1758) z řádu Gnathobdellida se živí vodními bezobratlými živočichy,
ale pomocí kutikulárních čelistí je schopna ulovit i rybí plůdek (osobní pozorování).
Obrázek 5. Hirudo medicinalis, adultní a juvenilní
jedinec, Foto J. Schenková.
15
Neparazitičtí zástupci čeledi Glossiphoniidae se živí likvidosomatofágní predací (sají tělní
tekutiny a měkké části těl) především měkkýšů (Mollusca). Zástupci řádu hltanovky
(Pharyngobdellida), u nás jen z čeledi Erpobdellidae se živí makrofágní predací, kořist
polykají celou, což jim umožňuje svalnatý hltan opatřený třemi lištami k drcení potravy.
Jejich kořistí jsou především zástupci máloštětinatých opaskovců („Oligochaeta“) a
pakomárovitých (Chironomidae), přičemž velikost kořisti je přímo úměrná velikosti predátora
(Schenková et al. 2007). Selektivní výběr potravy pro zástupce čel. Glossiphoniidae
(Mollusca) ani pro zástupce Erpobdellidae („Oligochaeta“ a Chironomidae) však nebyl
potvrzen na velké škále (studie na 109 lokalitách); na lokalitách s vyšším zastoupením
měkkýšů, máloštětinatců a pakomárovitých nebyly signifikantně více zastoupeny pijavice,
které se jimi živí (Kubová et al. 2013).
Reprodukce pijavic probíhá výhradně pohlavně, kopulací, a nejen, že se nejsou schopny
množit asexuálně, ale ani regenerovat poškozené články, což je u kroužkovců netypické.
Pijavice jsou protandričtí (varlata se vyvíjejí dříve než vaječníky) hermafrodité, při kopulaci
nalepují poblíž samičích pohlavních otvorů spermatofory. Vajíčka jsou odkládána v kokonech
a u čeledi Glossiphoniiidae byla zaznamenána péče o potomstvo (kokony v tenkém obalu a
následně juvenilní jedinci jsou nošeni na ventrální straně mateřského jedince). Většina pijavic
má jedno až dvouletý vývojový cyklus začínající kopulací v jarním či letním období, líhnutím
juvenilů během léta a dospíváním během dalšího roku (Ruppert et al. 2004). Reprodukční
strategie koexistujících druhů pak může být využita i k dělení nik. Například sympatricky
žijící druhy Erpobdella octoculata (Linnaeus, 1758) a Erpobdella vilnensis (Liskiewicz,
Obrázek 6. Průměrné denzity (s 25 a 75% kvartily) jednotlivých ročních tříd (1998, 1999, 2000) druhu
Erpobdella octoculata (a) a Erpobdlella vilnensis (b). Blíže viz Schenková et al. 2007, odkud byly obrázky
převzaty.
a b
16
1925) snižují vzájemný boj o potravu rozdílnou rychlostí vývojových cyklů (Obr. 6), kdy
ačkoli se líhnou z kokonů téměř ve stejnou dobu, pomalejší nárůst váhy u E. octoculata
umožní rozdělení potravních zdrojů, jak bylo zjištěno v případové studii na řece Rokytné
(Schenková et al. 2007).
2.3 Druhová diverzita opaskovců a její změny podél gradientů
prostředí
2.3.1Druhová diverzita opaskovců (Clitellata)
2.3.1.1 Máloštětinatí opaskovci („Oligochaeta“) na území České republiky
Pro území České republiky je v aktuálním check-listu uvedeno 95 vodních, případně
semiakvatických, druhů máloštětinatých opaskovců (Schenková et al. 2010). Check-list byl
sestaven z publikovaných dat, především významných monografií Hraběte (1954, 1981),
publikovaných nálezů druhů (Schenková 2005, Schenková & Kroča 2007) a pro čeleď
žížalovití (Lumbricidae) byly zařazeny vodní a semiakvatické druhy z monografie Pižl
(2002). V neposlední řadě pak zahrnuje současné nálezy všech spoluautorů. V České
republice žije 12 druhů z čeledi žížalicovitých (Lumbriculidae), 72 druhů z čeledi Naididae
sensu Erséus et al. (2008), které zahrnují 36 druhů z podčeledi naidkovití (Naidinae), osm
druhů z podčeledi Pristininae, 22 druhů z podčeledi nitěnkovití (Tubificinae), šest druhů
z podčeledi Rhyacodrilinae, po jednom druhu z čeledí Propappidae, kryodrilovití
(Criodrilidae) a pastrunovcovití (Haplotaxidae) a osm vodních/semiakvatických druhů
žížalovitých (Lumbricidae). Přesto, že je již známo, že někteří zástupci čeledi roupicovitých
(Enchytraeidae) žijí spíše akvatickým způsobem života (např. rod Cognettia), nebyla tato
čeleď vzhledem k obtížné dostupnosti ekologických údajů o druzích a celkově odlišné
metodice determinace do check-listu vodních máloštětinatců České republiky zařazena.
Většina máloštětinatých opaskovců představuje široce rozšířené euryvalentní druhy
schopné vyrovnat se s různými podmínkami prostředí. Jde především o zástupce podčeledi
Tubificinae, často až extrémně odolné k organickému znečištění. Do této kategorie náleží
z naší fauny 44 druhů (Schenková et al. 2010). Řadíme sem i některé nepůvodní druhy jako
Potamothrix moldaviensis Vejdovský & Mrázek, 1903 a Potamothrix bavaricus (Oschman,
1913) (Drake 2009). Ovšem vzhledem k jejich historickým nálezům, P. moldaviensis
zaznamenal Hrabě na začátku 20. století ve Vltavě a P. bavaricus ve 30. letech v Labi (Hrabě
17
1939), by tyto druhy mohly být i na našem území původní. Třicet osm druhů naší fauny se
jeví jako druhy vzácné (Schenková et al. 2010), neznamená to ovšem, že všechny jsou
ohrožené, protože na svých specifických habitatech mohou dosahovat vysokých abundancí,
jako např. Stylodrilus lemani, který dominuje v několika eutrofizovaných tocích jižní Moravy,
např. v řece Rokytné (Schenková & Helešic 2006), jinde se s ním ale nesetkáme. Naopak
nepůvodní teplomilný obyvatel velkých řek Branchiura sowerbyi Beddard, 1892, se zvolna
šíří Evropou pravděpodobně s lodní dopravou (Lišková 1964, Gruszka 1999), avšak od
prvního nálezu (Lišková 1964) byly získány pouze čtyři další. Třináct druhů historicky
náležejících do fauny České republiky bohužel nebylo od roku 1996, kdy se autoři check-listu
začali věnovat máloštětinatým opaskovcům, vůbec zaznamenáno (Schenková et al. 2010). Jde
o druhy specifických habitatů, které nespadají do běžných výzkumů, jako např. jeskynní druh
Stylodrilus absoloni (Hrabě, 1970), druh podzemních vod Trichodrilus pragensis Vejdovský,
1876 nebo parazit plžů (plovatek) Chaetogaster limnaei. Zaměření českých hydrobiologů na
tekoucí vody, především jejich monitoring pak také snižuje pravděpodobnost nalezení
některých vzácnějších druhů typických pro stojaté či dokonce vysychající vodní habitaty.
Takto nám zmizel například specialista na temporální tůně Lamprodilus mrazeki Hrabě, 1929
a některé druhy stojatých vod, jako Dero dorsalis Ferronière, 1899, Dero nivea Aiyer, 1929,
Dero obtusa Udekem, 1855 a Chaetogaster setosus Světlov, 1925. Jiné druhy zaznamenané
jen jedenkrát jsou pravděpodobně nesmírně vzácné nebo vyhynulé: Pristina amphibiotica
Lastočkin, 1927, Haber speciosus (Hrabě, 1931), Peipsidrilus pusillus Timm, 1977,
Potamothrix bedoti (Piguet, 1913) a Tubifex nerthus Michaelsen, 1908.
Tabulka 1. Seznam druhů máloštětinatých opaskovců navržených pro Červený seznam. Blíže viz Schenková et
al. 2010, odkud byla tabulka převzata a upravena. Jednotlivé kategorie dle (IUCN 1994).
ohrožený druh (EN) zranitelný druh (VU)
Arcteonais lomondi (Martin, 1907) Amphichaeta leydigi Tauber, 1879
Criodrilus lacuum Hoffmeister, 1845 Aporrectodea limicola (Michaelsen, 1890)
Haber speciosus (Hrabě, 1931) Pristina aequiseta Bourne, 1891
Lamprodrilus mrazeki Hrabě, 1929 Pristina bilobata (Bretscher, 1903)
Peipsidrilus pusillus Timm, 1977 Pristina jenkinae (Stephenson, 1931)
Piguetiella blanci (Piguet, 1906) Pristina longiseta Ehrenberg, 1828
Stylodrilus absoloni (Hrabě, 1970) Pristina osborni (Walton, 1906)
Trichodrilus pragensis Vejdovský, 1876 Nais behningi Michaelsen, 1923
Trichodrilus strandi Hrabě, 1936 Nais christinae Kasprzak, 1973
Nais stolci Hrabě, 1981
Rhyacodrilus subterraneus Hrabě, 1963
Specaria josinae (Vejdovský, 1884)
téměř ohrožený druh (NT) Stylodrilus lemani (Grube, 1879)
Apporrectodea georgii (Michaelsen, 1890) Uncinais uncinata (Øersted, 1842)
18
Přesto, že se jedná o skupinu vodních bezobratlých, u nichž je nesmírně obtížné zjistit,
z jakých příčin je její výskyt ojedinělý, některé druhy zasluhují ochranu. Tu je u
máloštětinatých opaskovců možné realizovat pouze pomocí ochrany jejich stanovišť, proto
byly některé druhy byly navrženy pro zařazení do Červeného seznamu, aby došlo k ochraně
biotopů, na nichž se vyskytují. Dosud publikovaný seznam chráněných máloštětinatých
opaskovců (Schenková 2005, Pižl 2005) byl modifikován a rozšířen (Tab. 1) (Schenková et
al. 2010), ale brzká doba jistě přinese další změny.
2.3.1.2Pijavice (Hirudinida) na území České republiky
Z taxonu pijavice (Hirudinida) je pro území České republiky v současnosti uváděno 24
druhů (Schenková et al. 2009). Data pro check-list byla získána z historických údajů,
především z prací Hrabě 1954, Koubková & Vojtková 1973, Lucký & Dyk 1964 a Košel
1998, 1999a, dále z údajů z projektů monitoringu tekoucích vod a vlastních nálezů všech
autorů. Nejbohatěji je v České republice zastoupena čeleď Glossiphoniidae, zahrnující 10
druhů převážně ze stojatých vod, většina z nich jsou predátoři, dva druhy jsou ektoparazité.
Čeleď Erpobdellidae je druhá nejpočetnější se sedmi druhy, kteří jsou predátoři tekoucích i
stojatých vod. V čeledi Piscicolidae, kde jsou všichni zástupci ektoparazité, je známo pět
druhů, v čeledi Haemopidae jeden druh (predátor) a Hirudinidae jeden parazitický druh.
Území České republiky je zajímavé tím, že jeho středoevropská poloha zahrnuje povodí
tří významných evropských toků – Labe, Dunaje a Odry, po nichž se některé pijavice mohou
šířit napříč Evropou. Z hlediska síly populací a původnosti pro naše území můžeme pijavice
žijící u nás rozdělit do tří skupin: druhy původní se stabilními populacemi, druhy původní,
jejichž populace jsou slabé a roztroušené a invazní druhy, nově se šířící našem území
(Schenková et al. 2009).
Do první skupiny řadíme evropské palearktické druhy, které historicky osidlují
nejrůznější vodní tělesa na našem území s vysokou frekvencí i abundancemi –
Alboglossiphonia heteroclita (Linnaeus, 1761), Glossiphonia complanata, Helobdella
stagnalis (Linnaeus, 1758), Hemiclepsis marginata, Theromyzon tessulatum, Piscicola
geometra (Linnaeus, 1758), Haemopis sanguisuga, Erpobdella octoculata a E. vilnensis. Tři
další druhy, považované dříve za vzácné – Glossiphonia concolor (Apáthy, 1888), G.
nebulosa Kalbe, 1964 a Erpobdella nigricollis (Brandes, 1900), byly pak do této skupiny
přiřazeny nově vzhledem k vysoké četnosti současných nálezů. U prvních dvou druhů mohlo
19
v minulosti docházet k záměně s G. complanata. Celkem je u nás 12 druhů původních pijavic
se stálými populacemi (Schenková et al. 2009).
Druhá skupina, do které řadíme druhy se vzácným výskytem, nezahrnuje jen skutečně
ohrožené druhy, ale i druhy, které jsou vzhledem k malé velikosti a nenápadnému vzhledu
častěji přehlíženy, jako Alboglossiphonia hyalina (O. F. Müller, 1774) a Alboglossiphonia
striata (Apáthy, 1888), které jsou velmi drobné (v prvním případě dokonce průsvitné) a
obývají stojaté vody. Navíc jako druhy byly poměrně nedávno odděleny od druhu A.
heteroclita (Trontelj 1997, Neubert & Nesemann 1999). K nejzáhadnějším druhům naší fauny
patří Glossiphonia slovaca (Košel, 1973), zranitelný druh (VU) dle Schenková & Košel
(2005), který byl nalezen pouze na území jižní Moravy v řece Dyji (Košel 1995, 1999b) a
později již nebyl zaznamenán. Ovšem odlišení tohoto druhu od ostatních zástupců rodu pouze
na základě počtu varlat a tvaru pohlavních vývodů činí determinaci velmi náročnou a přesto,
že velmi podobná pijavice byla z jediné známé lokality výskytu opět nalezena (leg. L. Mikl,
2015, det. J. Schenková), nebylo možné ji spolehlivě určit. Další zajímavý druh pro naši
faunu je Dina lineata (O. F. Müller, 1774), která žije sporadicky v drobných stojatých
vodách, prameništích a potocích v nížinách. Tyto biotopy jsou citlivé k různým zásahům a
malý počet nálezů vedl k návrhu zařadit tento druh mezi zranitelné VU (Schenková et al.
2009). Naprosto unikátní je také situace kolem našeho největšího druhu Trochaeta cylindrica
Örley, 1886, jehož lokality jsou jak v tůních jižní Moravy, tak v prameništích a potocích
v Beskydech, takže je i vzhledem ke zjištěným morfologickým rozdílům velká
pravděpodobnost, že se zde mohou ukrývat druhy dva (Bílková & Schenková 2015).
Nejvíce pozornosti ovšem přitahuje kriticky ohrožený druh CR Hirudo medicinalis
(Schenková & Košel 2005), neboť se jedná o krevsajícího ektoparazita s možností lékařského
využití, který měl rozsáhlý areál výskytu v povodí řeky Moravy i Labe (Hrabě 1936). Díky
přítomnosti protisrážlivého enzymu hirudinu a řady dalších enzymů, které vypouští do rány
při sání krve, byl v historických dobách využíván k „pouštění žilou“, dnes prožívá jeho
příbuzný laboratorně chovaný druh Hirudo verbana Carena, 1820 renesanci a je používán
v mikrochirurgii, k léčbě onemocnění lymfatického systému a řadě dalších chorob. Typickým
biotopem H. medicinalis jsou mělké rozsáhlé mokřady v zátopovém území řek pravidelně
zaplavované při jarních povodních, bohatě zarostlé makrovegetací, hojně osídlené
obojživelníky (zdroj potravy pro juvenilní jedince) a neosídlené žádnou nebo jen minimální
rybí obsádkou (Glombová & Schenková 2015). Takové biotopy jsou už dnes vzhledem
k regulaci říční soustavy a intenzivnímu zemědělskému využití krajiny v povodí velkých řek
20
velmi vzácné a většina z 18 současných lokalit výskytu (15 lokalit uvedeno v Glombová &
Schenková 2015, nově v roce 2015 Lesní tůň u Lanžhota, ústní sdělení J. Glombová a tůně
Lesní herda a Háček u Nejdku, ústní sdělení E. Lorencová) leží v oblastech, které jsou do
různé míry chráněné.
Dalšími vzácně nacházenými druhy jsou rybí parazité Piscicola respirans Troschel, 1850
a Piscicola fasciata Kollar, 1842 (jediný záznam Lucký & Dyk 1964) žijící trvale přichycené
na rybím hostiteli, což znemožňuje jejich nalezení během hydrobiologických výzkumů. Také
jediný nález druhu Erpobdella testacea (Savigny, 1822) svědčí o jeho velké vzácnosti (Košel
1999b). Opět se jedná o druh obývající u nás ohrožené biotopy, jako bažiny v litorální zóně
stojatých vod a velkých řek, který je navíc snadno zaměnitelný s E. nigricollis.
Poslední skupina zahrnuje druhy, které se u nás úspěšně šíří. Pro rybí ektoparazity jako je
druh ponto-kaspického původu Caspiobdella fadejewi (Epshtein, 1961), který se k nám
rozšiřuje z řeky Dunaje, je rychlé šíření umožněno na těle hostitelských ryb. Od prvního
výskytu v řece Moravě na soutoku s Dyjí (Košel 1998, 1999a) v devadesátých letech do
dneška osídlil celé území České republiky, a dostal se do povodí řek Moravy, Odry a Labe.
Z dalších druhů, jejichž počet nálezů postupně narůstá, lze uvést i druh Piscola haranti Jarry,
1960, který byl zaznamenán nejprve na třech (Schenková et al. 2009), následně na dalších
dvou lokalitách (Kubová & Schenková 2014). Vzdálenost jednotlivých lokalit a jejich
příslušnost k různým povodím (Labe, Morava) vedou ovšem i k alternativní hypotéze, že spíš
než pomalé šíření tohoto parazitického druhu do České republiky se jedná o jeho stálý vzácný
výskyt, který dříve nebyl zaznamenán vzhledem k jeho relativně nedávnému popisu a jeho
snadné záměně s Piscicola geometra. Velmi řídké jsou také nálezy dalšího šířícího se druhu
Dina punctata Johansson, 1927. Šíří se k nám z povodí Dunaje, kde je běžný, a takto se dostal
proti proudu Dyje až do Vranova. Jeho další nálezy v jižních Čechách v povodí Vltavy jsou
však těžko interpretovatelné. Vzhledem k tomu, že jde o druh semiakvatický, lze spekulovat o
přenosu vodním ptactvem.
Současný výzkum ukazuje, že oblast největší diverzity této skupiny se nachází na jižní
Moravě, především v oblasti soutoku řeky Moravy a Dyje. Většina ohrožených druhů pijavic
obývá nížinné mokřady v povodí velkých řek zarostlých vegetací a právě tyto jsou
nejohroženější negativními dopady lidské činnosti. Stejně jako u jiných bezobratlých
živočichů je péče o zachování přirozených habitatů a jejich zákonná ochrana jediným
účinným mechanismem k zachování vzácných druhů. Proto si habitaty hostící silné populace
21
Tabulka 2. Seznam druhů pijavic navržených pro Červený seznam. Blíže viz Schenková et al. 2009, odkud byla
data převzata a upravena. Jednotlivé kategorie dle (IUCN 1994).
vzácných druhů, např. H. medicinalis, zasluhují přísnou a dobře promyšlenou ochranu. Na
základě těchto zjištění byl proto seznam ohrožených druhů z roku 2005 (Schenková & Košel
2005) rozšířen o další druhy, takže určitá úroveň ochrany náleží celkem deseti druhům a
potažmo i jejich biotopům (Tab. 2, Schenková et al. 2009).
2.3.2 Variabilita druhové skladby máloštětinatých opaskovců v tocích
Máloštětinaté opaskovce nacházíme téměř ve všech akvatických biotopech, od pramenišť
po veletoky, stojaté i podzemní vody nevyjímaje, od čistých oligotrofních až po vysoce
eutrofizované. Tato skupina má vzhledem ke svému širokému zastoupení, vysokým denzitám
a velkému rozsahu tolerance ke znečištění u některých druhů, významný potenciál z hlediska
hodnocení kvality vod a jejich managementu, zejména vod tekoucích. Zatímco v minulosti se
zájem soustředil na hodnocení různých biotických indexů (např. Sládeček 1973, Chapman et
al. 1982, Milbrink 1983, Uzunov et al. 1988) se zaměřením především na vody znečištěné,
dnes se studium rozšiřuje o poznání všech faktorů, které podmiňují ekologii této skupiny,
o zjištění geografické distribuce, habitatových preferencí a požadavků na kvalitu vody nejen
u běžných, ale i vzácných a ojediněle se vyskytujících druhů.
Z hlediska významu pro člověka a zastoupení na našem území jsou středně velké tekoucí
vody převažujícím biotopem, proto byla jejich studiu věnována největší pozornost. Nicméně
v evropském měřítku nejsou studie máloštětinatých opaskovců tekoucích vod na velké škále
(tedy z mnoha toků pokrývající větší geografické území) příliš frekventované (MartínezAnsemil
& Collado 1996, Nijboer et al. 2004 a Verdonschot 2006). Na území České
republiky byl výzkum zaměřen na menší, pokud možno neznečištěné toky z povodí řek
Moravy a Odry (Schenková & Komárek 1999, Schenková et al. 2001a, Schenková et al.
2001b). Hlavním gradientem strukturujícím taxocen máloštětinatých opaskovců v tomto typu
toků v České republice je gradient nadmořské výšky úzce svázaný s charakterem substrátu:
skladba taxocenu máloštětinatých opaskovců se mění spolu se snižující se drsností dna
kriticky ohrožený druh (CR) zranitelný druh (VU)
Hirudo medicinalis Linnaeus, 1758 Alboglossiphonia hyalina (O. F. Müller, 1774)
Dina lineata (O.F. Müller, 1774)
ohrožený druh (EN) Glossiphonia slovaca (Košel, 1973)
Alboglossiphonia striata (Apáthy, 1888) Piscicola respirans Troschel, 1850
Erpobdella testacea (Savigny, 1822) Trocheta cylindrica Örley, 1886
22
(přechod od kamenitého k bahnitému substrátu), které doprovází klesající nadmořskou výšku
(Schenková et al. 2001a). Druhý gradient, který strukturuje skladbu a abundance
máloštětinatých opaskovců, má komplexní charakter, neboť je představován koncentrací
vápenatých a hořečnatých iontů, tedy chemismem a současně gradientem množství organické
hmoty vyjádřené chemickou spotřebou kyslíku COD (Obr. 7, Schenková et al. 2001a). Velmi
podobné výsledky s nejvýznamnějším gradientem přestavovaným substrátem a rychlostí
proudění, následovaným gradientem mineralizace vody pro máloštětinaté opaskovce
potvrzuje i práce z oblasti Pyrenejského poloostrova (Martínez-Ansemil & Collado 1996).
Parametry vázané na řád toku jako např. průtok jsou rozhodující proměnné pro strukturu
taxocenu máloštětinatí opaskovci, i v rovinatých oblastech Holandska, kde také reprezentují
nejvýznamnější gradient, charakterizovaný hloubkou a šířkou toku, jeho stálostí
(stálý/intermitentní); druhý gradient z hlediska vysvětlené variability představuje pH a další
chemické proměnné (Nijboer et al. 2004). Proměnná průtok, která u českých řek nebyla
měřena, byla zastoupena drsností dna a nadmořskou výškou, které klesají směrem od pramene
a byly prokázány jako signifikantní, význam zaznamenané hloubky a šířky toku prokázán
nebyl (Schenková et al. 2001a).
Získaná databáze výskytu máloštětinatých opaskovců na 57 téměř neznečištěných tocích
spolu s fyzikálně-chemickými parametry byla využita i k vyhodnocení kvality vody a nalezení
indikátorových druhů, které ji v malých tocích charakterizují. Na základě analýzy
hierarchické divizivní klasifikace TWINSPAN (Hill 1979) byly studované lokality rozděleny
do dvou velkých skupin zahrnující lokality zcela neznečištěných toků s indikátorovými druhy
Obrázek 7. Ordinační diagram kanonické
korespondenční analýzy (CCA) první a druhé
ordinační osy s pozicí všech druhů a
proměnných prostředí vybraných v postupném
výběru testovaným Monte Carlo permutačním
testem na hladině významnosti P = 0,01 (999
permutací). Zkratky názvů druhů a další detaily
viz Schenková et al. 2001a, odkud byl obrázek
převzat.
23
Nais alpina Sperber, 1948, N. communis Piguet, 1906 a N. simplex Piguet, 1906 a toky se
sníženou kvalitou vody, indikované druhem Tubifex tubifex. Skupinu čistých vod indikují
druhy spásající řasové nárosty a obývající kamenitá dna čistých toků, toky s více organickou
hmotou dobře indikoval nejodolnější euryvalentní druh T. tubifex (Obr. 8, Schenková et al.
2001b). Vodní máloštětinatí opaskovci pak mohou indikovat celkem čtyři skupiny čistých
Obrázek 8. Divizivní hierarchická klasifikace lokalit TWINSPAN s indikátorovými druhy. Zkratky lokalit a
druhů a další detaily viz Schenková et al. 2001b, odkud byl obrázek převzat.
toků (z leva): čisté meandrující se štěrkovým dnem (Stylodrilus parvus, Nais pseudoobtusa
Piguet, 1906), rychle tekoucí toky s vyšším sklonem (bez indikátoru), toky se štěrkopísčitým
dnem (bez indikátoru) a chladné pomalu tekoucí toky v oblasti Hercynika (Nais simplex,
Eiseniella tetraedra (Savigny, 1826), Stylodrilus parvus). A dále čtyři skupiny s různou mírou
znečištění: zemědělsky ovlivněné toky (bez indikátoru), toky na flyšovém podloží s přirozeně
vyšší konduktivitou (Tubifex tubifex), toky s vyšším obsahem organických látek COD (bez
indikátoru) a toky s nejnižší kvalitou vody v rámci studovaného souboru (Nais elinguis
Müller, 1774).
Indikace malých čistých až mírně znečištěných toků pomocí máloštětinatých opaskovců
je možná, přičemž úspěšnost klasifikace toků stoupá s mírou jejich znečištění. Avšak
indikátorové druhy jsou často běžné a je známo, že stejné druhy jako např. Spirosperma ferox,
Stylodrilus heringianus i Tubifex tubifex mohou charakterizovat jak oligotrofní podmínky, tak
eutrofizaci např. jezer, záleží jen na jejich denzitách (Milbrink & Timm 2002).
24
2.3.3 Variabilita druhové skladby máloštětinatých opaskovců na prameništních
slatiništích
Dalším biotopem tekoucích vod, jehož studiu jsme se věnovali, byla prameništní
slatiniště. Jedná se o jeden z nejohroženějších biotopů v Evropě, k jehož vymizení přispívají
především antropogenní vlivy, jako je odvodňování, eutrofizace a změny managementu
vedoucí k zarůstání a postupnému vysychání. Prameništní slatiniště představují roztroušené
mokřady, které se nacházejí v bezlesých místech, jsou syceny podzemní vodu a hostí živinami
limitovanou vegetaci. Většinou vyvěrají ve svažitém terénu, na našem území nejsou příliš
rozsáhlá a vzájemně jsou izolovaná. Mnoho zachovalých pramenišť se nachází v oblasti
Západních Karpat, proto byly naše výzkumy rozšířeny na Slovensko, kde se většina tohoto
pohoří nachází. Studované území zahrnovalo tři oblasti: Moravsko-slovenské pomezí na
flyšovém podloží (charakteristické střídajícími se vrstvami pískovce a jílovce), oblast Oravy,
která představuje východní výběžek flyšové zóny a oblast vnitřních Západních Karpat, jejíž
geologická struktura je složitější, tvořená jádrem paleozoických a krystalinních břidlic
překrytých mezozoickými pískovci a karbonátovými litofaciemi (odlišitelnými částmi
vrstevního sledu sedimentů).
Vzhledem k různému podloží je chemismus prameništních slatinišť značně variabilní a
vytváří tak gradient minerální bohatosti, který je pro ně typický, a byl popsán jako tzv. poorrich
gradient (Malmer 1986, Hájek et al. 2006). Na základě změny chemismu vyvěrající vody
a typu vegetace pak bylo možné klasifikovat pět základní typů prameništních slatinišť: typ 1 –
vápnitá pěnovcová, v nichž dochází ke srážení uhličitanu vápenatého ve formě pěnovce a
dominuje mech Cratoneuron commutatum; typ 2 – vápnitá bez srážení pěnovce, kde se
v chladnějších oblastech pěnovec již nesráží, na povrchu je rašelina, obsah živin je nízký,
dominují ostřice, suchopýry, mechy, zejména Drepanocladus revolvens agg.; typ 3 – mírně
vápnitá mechová, kde je koncentrace vápníku nižší a reakce vody není zásaditá nebo je příjem
vápníku snížen velkým obsahem železa, což umožňuje uchycení kalcitolerantních rašeliníků
(Sphagnum warnstorfii); typ 4 – kyselá přechodová rašeliniště, kde na prameništi je voda
spíše kyselá a mohou se zde vyskytnout i další druhy rašeliníků; typ 5 – druhově chudá kyselá
slatiniště s rašeliníky rodu Sphagnum (podrobněji viz Hájek et al. 2006).
Gradient minerální bohatosti, který významně strukturuje složení rostlinných
společenstev, ovlivňuje i další skupiny organismů, jako druhovou skladbu a bohatost
měkkýšů (Horsák & Hájek 2003), řas (Poulíčková et al. 2003, Fránková et al. 2009) nebo
25
krytenek (Opravilová & Hájek 2006). Situace u hmyzu je složitější, zatímco některé studie
ukazují jen slabý vztah hmyzích skupin (Virtanen et al. 2009) nebo pošvatek (Bojková &
Helešic 2009) k chemismu vody v silně mineralizovaných prameništích, u pakomárovitých na
celém poor-rich gradientu prokázán byl (Omelková et al. 2013). Tato situace nabízela dosud
nestudovanou otázku, zda skupina máloštětinatých opaskovců, která náleží k permanentní
fauně a žije v nejtěsnějším spojení se substrátem, je také ovlivňována měnícím se chemismem
vody.
Odpověď opaskovců na hlavní gradienty prostředí v tomto částečně zjednodušeném
systému (např. relativně malé kolísání průtoku a teploty vody) je však komplexnější.
Studujeme-li lokality v oblasti moravsko-slovenského pomezí, kde se nachází všechny
prameništní typy a jsou až na výjimky neovlivněné eutrofizací (17 lokalit), ukazuje se, že je
taxocen Clitellata strukturován mírou mineralizace pramenící vody a charakterem substrátu
(Bojková et al. 2011). Výměna druhů podél tohoto gradientu souvisí s měnícími se
vlastnostmi („traits“) dominantních druhů: na minerálně bohatých slatiništích dominuje
vzácný stygofilní (např. dle Dumnicka 2001) druh Trichodrilus strandi, který přímo preferuje
slatiniště, kde dochází ke srážení pěnovce. S klesající minerální bohatostí nastupuje čeleď
Enchytraeidae, která většinou zahrnuje půdní druhy schopné využívat i hlubších vrstev
sedimentů a tolerovat jeho vysychání, ale i vodní druhy jako např. Cognettia sphagnetorum
(Vejdovský, 1878) s širokou nikou, neboť se vyskytuje jak v minerotrofních rašeliništích
(např. van Duinen et al. 2006), tak v jehličnatých lesích (např. Graefe & Schmelz 1999).
Podobně vodní máloštětinatec Rhyacodrilus falciformis Bretscher, 1901 se kromě vodních
habitatů může vyskytnout i na loukách a v listnatých lesích (Graefe & Schmelz 1999,
Schlaghamerský & Kobetičová 2005). Minerálně chudá rašeliniště ležící na opačném konci
gradientu jsou osídlena běžnými euryvalentními druhy, jako Limnodrilus hoffmeisteri, Tubifex
tubifex, Stylodrilus heringianus a pijavicí Erpobdella vilnensis, která vyžaduje chladnější
vodu, ale je velmi tolerantní k organickému znečištění (Kubová & Schenková 2014). Druhová
bohatost opaskovců narůstá od minerálně bohatých směrem ke kyselým slatiništím, která
obsahují větší množství nerozložené organické hmoty, tedy v opačném směru než u cévnatých
rostlin, rozsivek nebo měkkýšů (Hájek et al. 2002, Horsák & Hájek 2003, Fránková et al.
2009). Ovšem odpověď opaskovců bude pravděpodobně spíše unimodální, neboť na
ombrotrofních vrchovištích, která nebyla předmětem našeho zkoumání, nalézáme
v nejkyselejších rašeliništích jen jediný acidotolerantní druh (van Duinen et al. 2006). Druhý
nejvýznamnější gradient strukturující opaskovce představuje gradient hydrologického režimu
spojený s produktivitou lokalit (více živin na jedné stran
vegetace na straně druhé) (Bojková
Jak ale reaguje tato skupina na mineráln
širokou geografickou oblast, s
různou mírou eutrofizace a rů
Moravsko-slovenského pomezí, Oravy a vnit
accepted). Výběr lokalit byl
skupiny, jsou silně ovlivňováni omezenou možností disperze na nové
2014a), která probíhá jen pasivním zp
polovinu lokalit starších než 2
daného typu prameniště mě
opaskovců na této škále, je
PCoA, Obr. 9a). Skladba opaskovc
s množstvím nerozložené organické hmoty
uhlíku – TOC), až po lokality s
vyvěrající vody. Nicméně shluková
Obrázek 9. (a) Analýza hlavních koordinát PCoA 54 lokalit s
do prostoru 1. a 2. osy, fit P < 0,05.
druhy frekventované (na 15ti lokalitách a více)
kolečka, skupina B; trojúhelníky, skupina C. (b) Shluková analýza Wardovou metodou na Bray
vzdálenostech. Čísla lokalit označ
2006). Zkratky názvů druhů a další deta
Obr. 9b) nám jednotlivé lokality uspo
prameništních slatinišť (oproti p
26
produktivitou lokalit (více živin na jedné straně, více vlhka
(Bojková et al. 2011).
Jak ale reaguje tato skupina na minerálně trofický gradient na velké škále,
širokou geografickou oblast, s jednotlivými typy pramenišť v oblastech s
různého stáří? Pro takovou studii bylo vybráno 54 lo
slovenského pomezí, Oravy a vnitřních Západních Karpat
r lokalit byl podmíněn zjištěním, že opaskovci, zejména specialisté z
ňováni omezenou možností disperze na nové lokality
probíhá jen pasivním způsobem, a proto nový soubor zahrnoval více než
polovinu lokalit starších než 2 500 let (Horsák et al. 2015), aby všichni potenciální obyvatelé
ě měli šanci ho osídlit. Hlavní gradient, který strukturuje taxoce
je opět gradient minerální bohatosti (analýza hlavních koordinát
Skladba opaskovců se mění od lokalit minerálně chudých, kyselých,
množstvím nerozložené organické hmoty (vysoké koncentrace celkového organického
až po lokality s vysokými koncentracemi Ca a Mg a vysokou vodivostí
shluková analýza skupiny opaskovců (Schenková
ch koordinát PCoA 54 lokalit s osmi proměnnými prostř
0,05. Zobrazeno 15 indikátorových druhů pro tři skupiny shlukové analýzy
druhy frekventované (na 15ti lokalitách a více). Symboly lokalit podle shlukové analýzy:
trojúhelníky, skupina C. (b) Shluková analýza Wardovou metodou na Bray
ísla lokalit označují typ prameništního slatiniště na základě vegetace a chemismu
a další detaily viz Schenková et al., accepted, odkud byly obrázky
notlivé lokality uspořádala částečně odlišně od čty
(oproti původnímu dělení na 5 typů, zde jsme použili dva nejkyselejší
a
A B
A
B
C
, více vlhka a nižší produktivita
trofický gradient na velké škále, zahrnující
oblastech s různým podložím,
studii bylo vybráno 54 lokalit v oblasti
ních Západních Karpat (Schenková et al.,
, zejména specialisté z této
lokality (Rádková et al.
a proto nový soubor zahrnoval více než
aby všichni potenciální obyvatelé
adient, který strukturuje taxocen
analýza hlavních koordinát
od lokalit minerálně chudých, kyselých,
(vysoké koncentrace celkového organického
vysokými koncentracemi Ca a Mg a vysokou vodivostí
ková et al., accepted,
nnými prostředí pasivně proloženými
i skupiny shlukové analýzy a
Symboly lokalit podle shlukové analýzy: čtverce, skupina A;
trojúhelníky, skupina C. (b) Shluková analýza Wardovou metodou na Bray-Curtis
a chemismu (Hájek et al.
y obrázky převzaty.
od čtyř základních typů
, zde jsme použili dva nejkyselejší
b
C
27
sloučené v jednu skupinu) vytvořených na základě vegetace a chemismu (Hájek et al. 2006).
Za tímto rozdílem stojí právě vliv substrátu ovlivňující druhovou skladbu podle přítomnosti
organické hmoty nebo naopak převážně anorganického substrátu. Substrát se spolu s teplotou
vody podílí na druhém nejvýznamnějším směru variability v datech. Tři skupiny opaskovců
nalezené shlukovou analýzou můžeme popsat podle indikátorových druhů (Analýza
indikátorových druhů, Dufréne & Legendre 1997): skupina A s indikátorovým druhem T.
strandi zahrnující minerálně bohaté lokality většinou se srážením pěnovce (typ 1), skupina B
s indikátorovým druhem Stylodrilus heringianus, vodním máloštětinatcem indikujícím
kamenitý substrát a vysychavost toků (Nijboer et al. 2004) a skupina C, s velkým počtem
euryvalentních indikátorových druhů (Erpobdella vilnensis, Limnodrilus hoffmeisteri,
Lumbriculus variegatus, Tubifex tubifex, Cognettia glandulosa (Michaelsen, 1888), Tubifex
ignotus (Štolc, 1886), zahrnující teplejší lokality s dostatkem organické hmoty (Schenková et
al., accepted). Skupiny B a C zahrnují směs všech typů pameništních slatinišť a skladba
skupiny opaskovci zde odráží jen charakter substrátu, organický vs. anorganický, vlhký vs.
vysychavý a teplotu, nikoli chemismus vody. Signifikantní vliv množství organického
substrátu na skladbu opaskovců zcela nezávislý na chemismu potvrdili také Rádková et al.
(2014b). Druhý gradient, který strukturuje společenstvo opaskovců, je podobně jako ve studii
na malé škále (Bojková et al. 2011) představován hydrologickým režimem, avšak podstatnou
měrou je navíc ovlivňován přítomností rozkládající se organické hmoty, která je zdrojem
potravy studované skupiny a rozhoduje o jejich výskytu bez ohledu na typ prameništního
slatiniště dle vegetace. Tak je možné přísunem organické hmoty, např. vlivem pastvy koní,
nevratně přeměnit jedinečné pěnovcové slatiniště s dominantním vzácným druhem T. strandi
na místo osídlené akvaristickými nitěnkami T. tubifex a L. hoffmeisteri, jejichž kvantita
indikuje znečištění lokalit (Hrabě 1954).
2.3.4 Změny společenstva opaskovců v otepleném toku
Výjimečné vlastnosti skupiny opaskovci (máloštětinatí i pijavice), která jak se potvrdilo,
zahrnuje citlivé druhy indikující čistotu a neovlivněnost stanoviště i druhy, které ukazují na
velkou míru dotace organické hmoty uváděné např. v Brinkhurst & Cook (1974), Uzunov et
al. (1988), ale i v našich výzkumech (Schenková et al. 2001b, Bojková et al. 2011), vedly
k možnosti studovat i ekosystémy lidskou činností silně pozměněné, jako jsou např. oteplené
důlní vody. Jedinečnou příležitost ke studiu vlivu změny teplotního režimu představuje řeka
Nedvědička protékající Českomoravskou vrchovinou, která je recipientem oteplených důlních
vod z posledního uranového dolu ve střední Evropě v Rožné. Tato řeka je vhodným
28
modelovým systémem, neboť teplá důlní voda nezvyšuje zásadním způsobem průtok a
nemění tak hydrologické poměry a neobsahuje ani významně zvýšené množství
radioaktivních látek. Nejen voda v řece Nedvědičce pod přítokem důlních vod s obsahem
uranu Unat = 0,010 mg l−1
, ale i sama důlní voda s hodnotou Unat = 3,4 mg l−1
splňuje limity
evropských norem a je pod hodnotou 24 mg l−1
vyžadovanou směrnicí „Directive
2008/105/EC of the European Parliament“ (Hudcová et al. 2012). Důlní voda se ovšem
vyznačuje nejen zvýšenou teplotou, ale i vodivostí (vysoká koncentrace síranů), pH a
sníženým obsahem kyslíku a živin (odstraněny v čističce odpadních vod), takže celý systém je
více komplexní (podrobněji viz Růžičková et al. 2014).
Pro případovou studii byla vybrána tři odběrová místa na řece Nedvědičce: nad přítokem
oteplené důlní vody (US), těsně pod přítokem (DS1) a níže po toku (DS2) a jako pozadí jedno
odběrové místo v přítoku oteplené důlní vody (MW); na každém z těchto čtyř míst byly
studovány dva habitaty: peřej a tůň (podrobněji v Růžičková et al. 2014). Silný dopad na
společenstvo opaskovců byl potvrzen; jak druhová diverzita, tak abundance opaskovců pod
přítokem oteplené důlní vody signifikantně poklesla v habitatech tůň i peřej (Obr. 10). Přesto,
že nebylo možné odlišit vliv chemických proměnných od vlivu změny teploty, je vysoce
pravděpodobné, že absence typického sezonního jevu, jako je zamrzání toku, také ovlivnila
skladbu opaskovců. Jedna z nemnoha studií vlivu změny teplotního režimu zahrnující i
skupinu Clitellata prokázala v industriální oblasti po oteplení vody jiný výsledek, a to nárůst
abundance máloštětinatců, ovšem při signifikantně zvýšeném průtoku (Nedeau et al. 2003).
Ochuzení společenstva opaskovců na řece Nedvědičce však mělo jiné příčiny. První je vliv
zvýšené vodivosti, k níž jsou různé druhy do různé míry citlivé (Generlich & Giere 1996),
např. výskyt druhu Propappus volki Michaelsen, 1916 je silně negativně korelován
s vodivostí (Dumnicka & Pasternak 1978), druhý je vliv zvýšené teploty, neboť v řece
Nedvědičce se za normálních okolností vyskytují i stenotermní druhy, např. Haplotaxis
Obrázek 10. Krabicové grafy druhové
diverzity (a) a abundance (b) opaskovců
na vzorkovacích místech na řece Nedvědičce:
nad přítokem oteplené důlní
vody (US), těsně pod přítokem (DS1) a
níže po toku (DS2); hodnoceno odděleně
pro peřej (tmavá) a tůň (bílá). Další
detaily viz Růžičková et al. 2014, odkud
byl obrázek převzat.
a b
29
gordioides Hartmann, 1821 a Stylodrilus heringianus (Dumnicka 2000), které se nedokážou
vyrovnat s oteplenou a v zimním období nezamrzající vodou. Tyto vlivy pak jsou různě
intenzivní v prokysličených peřejích, kde pod přítokem důlních vod chybí šest taxonů, a
v hlubších tůních, kde chybí tři. Peřeje jsou obývány rheofilními taxony, typickými pro horní
toky s méně živinami a vyšší koncentrací rozpuštěného kyslíku (Schwank 1981) a citlivějšími
na pokles kvality vody (Verdonschot 2006).
Změny v teplotním režimu vedou nejen k úbytku, ale i k výměně druhů (Živić et al.
2006), kdy právě na druhové úrovni je možné proniknout do podstaty změn v druhové
diverzitě a změn v abundancích taxocenu Clitellata. Oligostenotermní druhy, mezi něž patří
obyvatel podzemních vod a pramenišť Haplotaxis gordioides (Schwank 1981, Dumnicka
2000), se už pod přítokem oteplené vody neobjevují. Zástupci chladnomilného rodu
Stylodrilus reagují poklesem početnosti a následným návratem do původního stavu vzhledem
k jeho široké ekologické plasticitě (Syrovátka et al. 2009). Stejně tak reaguje Lumbriculus
variegatus, ovšem z jiného důvodu – vzhledem ke své vazbě na nižší hodnoty pH (Nijboer et
al. 2004) se přesouvá z místa přítoku důlní vody do oblasti s pro něj vhodnějším pH.
Nenáročné druhy rodu Limnodrilus tolerující různé teploty, množství kyslíku i různou
vodivost (např. Korn 1963, Dumnicka & Galas 2006), zůstávají v početnostech nad i pod
přítokem stejné. Byl nalezen i druh Aulodrilus japonicus, který na oteplení vody reaguje
nárůstem početnosti. Celkově lze shrnout, že i tato skupina permanentní fauny vodních
bezobratlých je vstupem oteplených důlních vod do toku do různé míry ohrožena, přičemž pro
některé druhy je tento vliv limitující.
2.3.5 Variabilita druhové skladby pijavic v tekoucích a stojatých vodách
Pijavice (Hirudinida) představují úžeji specializovanou skupinu parazitů a predátorů,
kteří se odlišují nejen morfologicky, ale i celou svojí biologií, proto obvyklou metodikou pro
studium makrozoobentosu, vhodnou pro vzorkování máloštětinatých opaskovců, zachytíme
jen malou část jejich diverzity (Koperski 2011). K podrobnějšímu studiu ekologických
parametrů stojících za strukturováním skupiny pijavic je zapotřebí použití odlišných
vzorkovacích metod (Kubová & Schenková 2012) a její hodnocení samostatně. Pijavice
obývají jak tekoucí, tak stojaté vody, přesto je většina prací věnována buď jednomu, nebo
druhému habitatu (např. stojatým vodám se věnují Young & Ironmonger 1981, Spelling &
Young 1987, tekoucím např. Grosser et al. 2001, Koperski 2005, 2010). Omezení existujících
souhrnných prací z tekoucích i stojatých vod spočívá ve spíše popisném zaměření na
30
distribuci druhů, charakteristiku preferovaných habitatů, případně vztah ke znečištění (např.
Bennike 1943, Elliott & Mann 1979, Košel 1988, 1989, van Haaren 2004, Schenková et al.
2009) nebo naopak jen na jejich vztah k chemismu vody (Mann 1955, Grosser et al. 2001).
Proto je velmi zajímavá otázka studia vlivu nabídky potravy i fyzikálně-chemických
parametrů současně se zohledněním rozdílných podmínek v tekoucích a stojatých vodách.
První předpoklad zjištěný také již v pracích autorů Mann (1953) a Koperski (2006)
o odlišnosti společenstev obývajících tekoucí a stojaté vody, se potvrdil. Nejsilnější gradient
strukturující taxocen pijavic představuje rozdíl v typu habitatu: tekoucí versus stojaté vody.
DCA analýza ukázala spolu s ním další významné morfologické a fyzikální proměnné, které
tyto habitaty odlišují: tekoucí – vyšší zastínění, stojaté – nižší drsnot dna, větší množství
makrofyt a vyšší teplota vody (Obr. 11, Kubová et al. 2013). Při porovnání variability
vysvětlené jednotlivými proměnnými prostředí v přímých analýzách tří datových souborů –
oba habitaty, jen tekoucí a jen stojaté vody – vykazují výsledky celkového souboru mnohem
větší podobnost s habitatem tekoucích vod. Gradienty proměnných prostředí v tekoucích
vodách jsou pro strukturování společenstva pijavic zahrnující oba habitaty rozhodující. Zcela
novým zjištěním, dosud pouze odhadovaným bez statistických důkazů, je význam dostupnosti
kořisti, který je prediktorem výskytu pijavic a to jak v tekoucích, tak ve stojatých vodách, tak
v souboru zahrnujícím oba typy (Kubová et al. 2013). Dosud studované zástupné proměnné
charakterizující úživnost ekosystému a vykazující signifikantní vliv na strukturu společenstva
pijavic jsou např. alkalinita, vodivost, koncentrace fosforečnanů nebo biotické indexy
charakterizující trofický stav (Bennike 1943, Mann 1955, Herrmann 1970, Koperski 2005,
2010). Přímý vliv těchto proměnných na společenstvo pijavic je silně nepravděpodobný,
celková úživnost systému vede k vyšším abundancím makrozoobentosu, jímž se pak pijavice
živí. Jiným neočekávaným výsledkem je význam zastínění pro výskyt pijavic, vysvětlující
Obrázek 11. Ordinační diagram DCA
společenstva pijavic na 109 lokalitách
v prostoru 1. a 2. ordinační osy. Všechny
nalezené druhy kromě odlehlé hodnoty pro
Hirudo medicinalis jsou znázorněny.
V diagramu jsou pasivně proložené proměnné
prostředí, které signifikantně korelovaly s 1.
až 4. ordinační osou; signifikantní i po
Bonferonniho korekci jsou tučně (P <
0,0026). Zkratky názvů druhů a proměnných
prostředí a další detaily Kubová et al. (2013),
odkud byl obrázek převzat.
31
vysoký podíl variability jak v tekoucích tak stojatých vodách, jejich vliv je však protichůdný
(Kubová et al. 2013). V tekoucích vodách narůstá druhová diverzita i abundance s vyšším
zastíněním, neboť pijavice jsou zde lépe chráněné před fluktuacemi teploty, a množství
kyslíku. Zastíněná místa představují pro chladnomilné druhy refugia (Aguiar et al. 2002,
Ebersole et al. 2003). Naopak ve stojatých vodách – v rybnících a nádržích – s nižším
zastíněním narůstá diverzita teplomilných druhů. Také přímo teplota vody a průměrná roční
teplota vzduchu jsou pro pijavice významným parametrem. Druhová bohatost ve stojatých
vodách vykazuje podél gradientu průměrné roční teploty unimodální průběh (Kubová et al.
2013), neboť ani nížinné lokality s vysokou zemědělskou produkcí na jednom konci gradientu
ani chladné podhorské rybníky a nádrže na druhém konci nepodporují diverzitu teplomilných
druhů žijících ve stojatých vodách, jak bylo obdobně pozorováno v britských jezerech (Young
& Ironmonger 1981).
Zajímavé je srovnání výsledku z tekoucích a stojatých vod u nás, kdy mezi stojatými a
tekoucími vodami nebyl nalezen rozdíl v abundancích (Kubová et al. 2013), avšak druhová
diverzita byla vyšší v tekoucích vodách, s polskými lokalitami, kde nejvyšší diverzita byla
v jezerech a nižší v řekách a rybnících (Koperski 2006). Relativně čistá jezera v Polsku, jaká
se na našem území bohužel nenacházejí (vyjma horských, která jsou tuto skupinu příliš
chladná), představují pro pijavice unikátní kombinaci ekologických parametrů s vysokými
počty vodních bezobratlých (makrozoobentosu) jako kořisti při relativně nízké trofii.
2.4 Odpovědi vybraných druhů opaskovců na různé proměnné
prostředí – malá a velká škála
Odpověď celého společenstva na různé gradienty prostředí je vždy souhrnem odpovědí
jednotlivých druhů, jejich prezencí či absencí a změnami jejich abundancí. Zatímco na malé
škále ve smyslu mezohabitatů (Armitage et al. 1995) se jedná především o hydraulické a
substrátové preference, na velké škále jsou druhy vodních bezobratlých determinovány
hydromorfologií toků, klimatickými podmínkami, chemismem a množstvím potravy (např.
Hynes 1970, Cummins et al. 1984).
Na malé škále na úrovni habitatů podmiňuje výskyt máloštětinatých opaskovců charakter
substrátu: velikost zrna podmiňující jeho drsnost, přítomnost makrofyt a přítomnost
hydraulicky klidných míst umožňujících akumulaci organické hmoty, která tvoří jejich hlavní
32
složku potravy (Verdonschot 2001, Křoupalová et al. 2011). Detailní studium prostorové
distribuce jednotlivých druhů na úrovni mezohabitatů lze nejlépe studovat srovnáním různých
mezohabitatů lišících se typem substrátu, hydraulicky i množstvím akumulované organické
hmoty v rámci jednoho toku. Tento náročný přístup ovšem omezuje počet studovaných druhů
na druhy dostatečně frekventované a vyskytující se ve vysokých abundancích. Takto byly ve
studii věnované skupinám „Oligochaeta“ a Chironomidae na řece Svratce zjištěny hydraulické
preference pro pět druhů máloštětinatých opaskovců a další druhy pakomárovitých (Obr. 12,
Syrovátka et al. 2009, upraveno). Dva taxony preferují velmi úzké rozpětí hydraulických
podmínek - Aulodrilus japonicus Yamaguchi, 1953 se vyskytuje pouze v tůních s nízkou
hodnotou Froudova čísla (výpočet zahrnuje rychlost proudění, hloubku a gravitační zrychlení)
a Nais stolci preferuje středně rychle proudící úseky bez turbulencí. Další druhy nevykazují
tak úzké preference, Nais alpina se optimálně vyskytuje v úsecích se středním prouděním, ale
v nízkých denzitách se vyskytuje i v tůních s nejnižší rychlostí proudění a peřejích s nejvyšší
rychlostí. Rod Stylodrilus preferuje peřeje, ale obývá i středně proudivé úseky a druh
Propappus volki silně preferuje peřeje, obývá i proudivé úseky, ale tůním se vyhýbá
(Syrovátka et al. 2009). Oba tyto druhy jsou pro obývání peřejí dobře adaptovány, Stylodrilus
si staví hlenové trubičky, které ochraňují při pohybu substrátu (Mrázek 1926), P. volki, který
je známým obyvatelem pohyblivých písků a intersticiálních prostor se přilepuje k substrátu
pomocí adhezivní látky (Bird 1982, Petto & Humpesch 1992).
Stanovení habitatových preferencí pro jednotlivé druhy opaskovců na velké prostorové
škále vyžaduje rozsáhlý datový soubor s vysokým počtem lokalit postihující celou škálu
proměnných prostředí měřených na všech lokalitách, což velmi limituje počet takových studií
v tekoucích vodách. Takto precizně byl stanoven vztah jednotlivých druhů k saprobitě
(Sládeček & Košel 1984, Uzunov et al. 1988), tekoucím vs. tůňovým habitatům a
minerálnímu substrátu vs. vegetaci (Martínez-Ansemil & Collado 1996), typu vodního tělesa
(Koperski 2006), eutrofizaci, nadmořské výšce a substrátu (Verdonschot 2006) a některým
chemickým proměnným (Mann 1955, Timm et al. 2001).
Propappus volki
Stylodrilus spp.
Nais stolci
Nais alpina
Aulodrilus japonicus
Obrázek 12. Hydraulické preference pěti
frekventovaných druhů máloštětinatých
opaskovců. Kolečka znázorňují medián,
silné linky horní a dolní kvartil, tenké 10%
a 90% kvantily Froudova čísla váženého
abundancí taxonu. Převzato a upraveno
pouze pro „Oligochaeta“ ze Syrovátka et
al. (2009), kde jsou uvedeny další detaily.
33
Bohatý datový soubor opaskovců (většinou máloštětinatých) z 54 prameništních slatinišť
spolu s proměřením celkem 17 proměnných prostředí na každé lokalitě představoval možnost
stanovit enviromnentální prediktory jejich výskytu. Po redukci počtu druhů na dvanáct
dostatečně početných a proměnných prostředí na osm vzájemně nekorelovaných, vybraných
na základě předchozích studií opaskovců (Martínez-Ansemil & Collado 1996, Timm et al.
2001, Verdonschot 2006, Bojková et al. 2011) byly spočítány zobecněné lineární modely
(GLM, McCullagh & Nedler 1989). Tyto modely vyjadřující abundance vybraných druhů
jako lineární funkci osmi proměnných prostředí byly spočítány s quasi-Poissonovým
rozložením korigujícím overdisperzi dat (Schenková et al., accepted, kde jsou uvedeny další
detaily analýzy).
Jako nejzajímavější se jeví vzácný druh Trichodrilus strandi, indikátor minerálně
bohatých pěnovcových slatinišť, která nejsou antropogenně ovlivněná – v našich analýzách na
základě taxocenu opaskovců typ pramenišť A (Obr. 9, Schenková et al., accepted). Jde o druh
prameništního specialisty, obývající čisté oligotrofní, chladné, vysoce mineralizované toky
(Hrabě 1981, Juget & Dumnicka 1986, Šporka 1998, Bojková et al. 2011). Jeho výskyt je
pozitivně korelován s koncentrací Ca a Mg natolik, že 50 % variability jeho abundancí lze
vysvětlit těmito proměnnými. Ke stejnému typu pramenišť je byť slaběji vázán i druh
Rhyacodrilus falciformis, který je znám jak vztahem k pramenným a podzemním vodám krenofilní
stygobiot (Schwank 1981, Juget 1987, Dumnicka 2000), tak vlhkým půdám
(Schlaghamerský & Kobetičová 2005). My jsme u něj zaznamenali unimodální odpověď ke
koncentracím Ca a Mg (vysvětlující 13 % variability) a preferenci habitatů s nízkým
množstvím organického substrátu.
Druh Stylodrilus heringianus, indikující druhou skupinu pramenišť (B) na základě
opaskovců (Obr. 9), je charakteristický pro kyselé slatiniště se 73 % variability vysvětlenými
negativním vlivem Ca a Mg (Schenková et al., accepted). Pro tento druh je typická schopnost
přežít i občasné vyschnutí toku (Nijboer et al. 2004). Pro další druh Cognettia sphagnetorum
vázající se ke skupině B (i když ne jako indikátor) je všechna zjištěná variabilita vysvětlená
negativním vztahem k Ca a Mg koncentracím (47 %) (Schenková et al., accepted) a i když u
nás nebyla statisticky významná, je pro jeho prezenci v této skupině důležitá i vazba na nižší
teploty vody, kterou se významně liší od zástupce stejného rodu C. glandulosa (Timm et al.
2001). Mesenchytraeus armatus, také se vztahem ke skupině pramenišť B, má veškerou
zjištěnou variabilitu danou právě vztahem k chladnějším vodám, mineralizace vody pro něj
není důležitá (Schenková et al., accepted), naopak jde o půdní druh s pozitivním vztahem
34
k vlhkosti (Graefe & Schmelz 1999), takže může lépe odolávat dočasnému prosychání
prameniště, pravděpodobně charakteristickému pro tuto skupinu pramenišť.
Pijavice Erpobdella vilnensis, živící se jako predátor, je nejsilnějším indikátorem třetí
skupiny pramenišť označenou C a charakteristickou vyšší trofií; z měřených proměnných pro
ni byla významná jen schopnost tolerovat nedostatek kyslíku (vysvětlující 23 % variability)
(Schenková et al., accepted). Další indikátorové druhy této skupiny Tubifex tubifex a
Limnodrilus hoffmeisteri, jsou charakteristickými indikátory znečištěných vod (např.
Brinkhurst & Jamieson 1971, Uzunov et al. 1988), neboť jejich abundance narůstají směrem
k vyšším teplotám a množství organického substrátu, respektive k celkovému organickému
uhlíku a nitrátům (Schenková et al., accepted). U silně acidofilního druhu Cognettia
sphagnetorum (van Duinen et al. 2006) bylo 47 % variability vysvětleno Ca a Mg (negativní
vztah), u acidotolerantního druhu Lumbriculus variegatus (Graefe & Schmelz 1999) jen 8 %,
silnější vztah byl zaznamenán k vyšším koncentracím celkového uhlíku (40 %) a teplotě vody
(15 %). Nerozložená rostlinná potrava v kyselých slatiništích je typickou potravou druhu
Lumbriculus variegatus (Moore 1978, Brinkhurst & Gelder 1991). Drobné fytofilní druhy
z podčeledi Naidinae Pristina bilobata a Nais communis vykazovaly vztah k nižším
koncentracím Ca a Mg, přičemž podhorský druh P. bilobata navíc vykazoval pozitivní vztah
k teplotě a organickému substrátu a euryvalentní druh N. communis negativní vztah
k anorganickému substrátu (Schenková et al., accepted).
Pro stanovení preferencí jednotlivých druhů pijavic byl také vyhodnocen široký datový
soubor 109 lokalit na území České republiky (Kubová & Schenková 2014). Prediktivní
modely bylo možné spočítat pro sedm dominantních a dostatečně frekventovaných druhů
pijavic (A. heteroclita, G. complanata, H. stagnalis, Hemiclepsis marginata, T. tessulatum, E.
octoculata a E. vilnensis) a 12 proměnných prostředí. Vzhledem k šíři variability různých
typů vzorkovaných lokalit je na rozdíl od máloštětinatých opaskovců pro pijavice velmi
významný typ habitatu, kdy kategoriální proměnná tekoucí vs. stojaté vody byla signifikantní
pro všechny studované druhy. Tekoucí vody preferuje pouze G. complanata, pro kterou je
důležitý i nízký obsah amonných iontů, a E. vilnensis, která je naopak k jejich vysokým
koncentracím signifikantně tolerantní (Kubová & Schenková 2014), což bylo nové zjištění;
pouze Van Haaren (2004) popisuje přítomnost druhu v téměř stojatých vodách holandských
kanálů. Také jeho přítomnost v nejvíce znečištěné skupině prameništních slatinišť a tolerance
nízkého množství kyslíku podporuje informace o jeho všeobecné odolnosti (Schenková et al.,
accepted). Ostatní sledované druhy signifikantně preferují vody stojaté (Kubová & Schenková
35
2014). Téměř všechny sledované druhy mají také významný vztah ke klimatickým
podmínkám, kde průměrná roční teplota je pro většinu z nich signifikantní, pro tři druhy E.
octoculata, E. vilnensis a G. complanata i v kvadratickém tvaru, jak ukazují odpovědní křivky
sestrojené pro tekoucí a stojaté vody zvlášť, u G. complanata jen pro tekoucí (Obr. 13). Stejně
jako pro máloštětinaté opaskovce, je i pro pijavice významný charakter substrátu. A. heteroObrázek
13. (a) Signifikantní odpovědní křivky (P < 0,05) běžných druhů pijavic k průměrné roční teplotě
založené na kvadratickém tvaru prediktivních modelů, — stojaté vody, – - – tekoucí vody. Převzato z Kubová &
Schenková (2014), kde jsou uvedeny další detaily.
clita, G. complanata a Helobdella stagnalis dávají přednost hrubšímu substrátu, který je pro
ně optimálním podkladem, pouze parazitický druh Hemiclepsis marginata preferuje bahnitý
společně s vyšším obsahem nitrátů – oba tyto faktory jsou významné spíše pro jeho rybí
hostitele. Také další druhy stojatých vod A. heteroclita a Helobdella stagnalis obývají spíše
vody znečištěné s vysokým obsahem fosforečnanů, respektive s vysokými hodnotami
celkového uhlíku (Kubová & Schenková 2014), což je v souladu s pracemi Mann (1955),
Sládeček & Košel (1984), van Haaren (2004) a odporuje to pouze výsledkům práce Koperski
(2005), kde byl studován velmi omezený datový soubor.
Závěrem kapitoly lze říct, že stanovit preference konkrétních druhů opaskovců je velmi
obtížný úkol zejména pro vzácné a málo početné druhy, které se vymykají možnostem
statistického zhodnocení dat. Avšak každý příspěvek do této mozaiky byť s limitovanou
platností v místních podmínkách přináší možnost vysvětlení chování celého společenstva a
tudíž i vysvětlení, jaké podmínky taková druhová skladba indikuje.
36
3. Závěr
V tomto shrnujícím úvodu bylo mým cílem představit šíři diverzity našich dvou
největších skupin opaskovců (Clitellata), máloštětinatých opaskovců a pijavic, často
pokládaných za pouhé indikátory organického znečištění. Tito kroužkovci však reagují na
celou škálu gradientů prostředí, zejména na chemismus vody a charakter substrátu, takže
jejich druhové složení a početnost pomáhají odhalit nejen jednotlivé antropogenní vlivy, od
různých typů znečištění, přes oteplení vod až po morfologické změny habitatů, ale indikují
nám i vlastnosti habitatů vzácných a čistých, jako jsou prameništní slatiniště. Zatímco výskyt
většiny vodních máloštětinatých opaskovců odráží změny v substrátu a v chemismu vodního
prostředí, zejména obohacení organickým materiálem, přímo, pijavice nám pomáhají
indikovat zvýšení abundance jejich kořisti, tedy početnost ostatních vodních bezobratlých.
V dnešní uspěchané době prací silně zaměřených na fylogenezi a „barcoding“ jednotlivých
druhů opaskovců se někdy nedostává základních informací o jejich ekologii, a proto jsou
předložené práce příspěvkem k doplnění této mezery v poznání zejména zjištěním odpovědí
jednotlivých druhů na konkrétní fyzikálně-chemické i biologické gradienty.
37
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5. Seznam publikovaných vědeckých prací v ISI časopisech
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5.1 Druhová diverzita máloštětinatých opaskovců a její změny podél
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235
Oligochaeta of the Morava and Odra River basins (Czech Republic):
species distribution and community composition
Jana Schenkov´a, Ond˘rej Kom´arek & Sv˘etlana Zahr´adkov´a
Masaryk University, Faculty of Science, Department of Zoology and Ecology, Kotl´a˘rsk´a 2, 611 37 Brno,
Czech Republic
Fax: +420-5-41211214. E-mail: schenk@sci.muni.cz
Key words: aquatic Oligochaeta, distribution, ordination, Czech Republic
Abstract
The oligochaete fauna of 57 small streams of the Morava and Odra River basins, Czech Republic, was studied
during 1997 and 1998. TWINSPAN and CCA (CANOCO) were used to characterize the relationship between
oligochaete species, habitat diversity and environmental variables. Chemical oxygen demand (COD), water hardness,
NO3
−–N, Ca2+, Mg2+, altitude, and substrate type were found to be the primary factors influencing the
distribution of aquatic Oligochaeta.
Introduction
The ecological requirements of aquatic Oligochaeta
(Clitellata) and their relationship to abiotic factors in
streams of the Czech Republic (central Europe) have
received little attention in previous studies. While extensive
taxonomic reports on oligochaetes have been
published by Hrab˘e (1979) and Li˘sková (1976), and
on the oligochaete family Enchytraeidae, by Chalupský
(1988), few ecological studies on this diverse
and often dominant group of lotic benthic organisms
have been conducted (Brinkhurst, 1978; Uzunov et al.,
1988; Hörner et al., 1995).
The objectives of this study were to determine
the distribution of oligochaete species in small, relatively
unpolluted streams in the Czech Republic,
and to evaluate the impact of environmental factors
on the composition of oligochaete taxocenoses using
multicriterial analyses.
∗ The paper is dedicated to the memory of Prof. Dr Sergej Hrab˘e,
on the 100th anniversary of his birth. Dr Hrab˘e, a major contributor
to aquatic oligochaete taxonomy during his extensive career in the
Department of Zoology and Anthropology at Masaryk University,
actively published from 1927 up to 1984.
Description of sites studied
Study sites were located on small streams in the
Morava River basin (sensu lato, which means the
Morava and Dyje River basins together) and in the
Odra River basin (Czech Republic) (Fig. 1). The
studied area represents an interesting region since
all biogeographical subprovinces found in the Czech
Republic, are present: Hercynicum, Pannonicum,
Carpathicum and Polonicum (Culek, 1996) (Fig. 1).
All sites were either unpolluted or moderately influenced
by treated and untreated domestic wastewater
effluent. Studied localities presented the following
characteristics: they were situated from 175 to 750 m
a.s.l.; the distance from the source was 0.7 to 16.8 km;
the mean width of the streams ranged from 0.93 to
4.25 m; and the mean depth of the streams ranged from
0.06 to 1.1 m.
Materials and methods
Samples of macrozoobenthos were collected from 27
localities during spring, summer, and autumn of 1997,
and from 30 localities during the same seasons in
1998. Sampling at each station was completed using
236
Figure 1. Map of the study area showing site localities and river basins. D – Dyje; M – Morava; O – Odra River basin. Biogeographical
subprovinces named according to Culek (1996). He – Hercynicum; Po – Polonicum; Ca – Carpathicum; Pa – Pannonicum.
a standard method of kick sampling for a period of 3
min (Kershaw & Frost, 1968).
During each sampling period, water temperature,
width and depth of the stream, hydrogen ion concentration
(as pH), conductivity and the substrate
composition were measured. The evaluation of the
substrate composition at each site followed Wright et
al. (1984) by expressing the weighted average of percent
presence of each particle size-classes (boulders,
cobbles, pebbles, granules, sand, mud and clay).
The mean value of phi, which is the negative logarithm
of the particle size in millimetres, characterised
each particle size-class. Laboratory analyses for important
ion components present at our sampling sites
were performed on samples collected during each
sampling period. Alkalinity, water hardness, oxygen
content, dissolved oxygen (DO), biochemical oxygen
demand (BOD5), chemical oxygen demand (COD),
total organic carbon (TOC), dissolved organic carbon
(DOC), NH4
+–N, NO2
−–N, NO3
−–N, total nitrogen
(N TOT), o-PO4
3−–P, total phosphorus (P TOT),
Cl−, SO4
2−, Ca2+ and Mg2+ were measured. Current
velocity was not included in the analyses; single measurements
obtained during sampling had no predicable
value because of the frequently changing water level
at the studied sites.
Samples of macrozoobenthos were fixed on site
with 4% formaldehyde. After the samples had been
sorted, oligochaetes were prepared for identification
by either mounting permanently on slides using
Canada balsam, or prepared as temporary mounts
using a glycerin-water (1:5) solution.
With the exception of taxa representing five genera
in the family Enchytraeidae, which were determined
using the keys of Nielsen & Christensen (1959, 1961,
1963), all oligochaetes were identified to the species
level using the keys of Hrab˘e (1954, 1979). Juvenile
forms or damaged individuals were determined only
to family level.
The resulting data were evaluated and interpreted
using TWINSPAN (Hill, 1979). All options were set
to default; maximum group size for division was five
and maximum level of divisions was six. Relationships
between oligochaete species and environmental
variables were evaluated by Canonical Correspondence
Analysis (CCA) using the CANOCO program
for Windows (Ter Braak & ˘Smilauer, 1998). The scaling
type was biplot and species data were not transformed.
With the exception of representatives of Enchytraeidae,
taxa unidentified to the species level were
omitted from the analyses. Statistical significance was
then determined by a Monte Carlo permutation test
(Ter Braak & ˘Smilauer, 1998). 27 environmental vari-
237
Figure 2. Divisive hierarchic classification (TWINSPAN) of species (for abbreviations see Table 1). 1TWINSPAN group, 2eigenvalue.
ables were tested in 999 permutations using automatic
forward selection.
Results
During the 1997 and 1998 sampling periods, 22 211
individuals of the class Oligochaeta representing eight
families, 27 genera and 36 species were collected
(Table 1). One species of Aeolosomatidae (Annelida,
Aphanoneura)was also collected. The abbreviation for
each identified taxon used in analyses is provided in
Table 1.
Hierarchical divisive classification of species
Hierarchical divisive classification of 51 taxa with
eigenvalues of divisions is apparent from Figure 2.
The eigenvalues express the level of distinction of
separated groups at each division. Oligochaeta were
separated into seven different groups. Group ∗00, further
division of which expressed eigenvalue 0.196
and hence was not significant, consists of representatives
of the family Naididae and other species from
sites characterized by a sandy bottom with plant detritus.
Group ∗010 includes the taxa Enchytraeus,
Mesenchytraeus and Eiseniella tetraedra (Savigny,
1826). Group ∗011 consists of the cosmopolitan species
Nais elinguis Müller, 1773 and Cernosvitoviella
(Enchytraeidae). Group ∗100 and group ∗101, with relatively
low eigenvalue of division, include species of
the genus Stylodrilus – inhabiting unpolluted brooks
and rivers with sandy bottom, the species Criodrilus
lacuum Hoffmeister, 1845 – common in pools, and
the genus Pristinella – which prefers pristine waters.
Group ∗110 includes species in the family Tubificidae,
and Uncinais uncinata (Ørsted, 1842) (Naididae).
Group ∗111 contains only unidentified Enchytraeidae
species.
Canonical correspondence analysis (CCA)
Canonical correspondence analysis (CCA) concerned
27 environmental variables and 46 species or genera,
respectively; five genera that might have included
more than one species were omitted (Fig. 3). The eigenvalue
for the first axis was 0.535, the second 0.335
and the third 0.255. The percentage variance of species
environment relation was 35.8 for the first axis, 22.5
for the second and 17.1 for the third axis.
The statistical significance of the data was evaluated
using the Monte Carlo permutation test. The
following environmental factors were found to be
statistically significant: COD, hardness, NO3
−–N,
238
Figure 3. Canonical correspondence analysis (CCA), ordination plot of species (for abbreviations see Table 1) and main environmental variables
on the first two CCA axes.
Ca2+, Mg2+, altitude, and substrate type (P < 0.01).
CCA analysis showed correlations (>0.5): positive for
COD, altitude and negative for hardness and the first
axis. The distribution of species along the first axis
reflects their requirements regarding organic matter
supply, altitude and hardness. A positive correlation
for Mg2+ was shown by the second axis, while positive
correlations for Ca2+ and Mg2+ were shown by the
third axis. The distribution of species along the second
and third axis can be explained by the water hardness.
Discussion
From the analyses performed, we determined that
COD and water hardness together with concentrations
of NO3
−–N, Ca2+, Mg2+, altitude, and substrate type
are the primary factors influencing the distribution of
Oligochaeta in small streams.
The distribution of the species of the family Tubificidae
can be explained by their preference for
substrates with higher organic content and fine particle
size (Fig. 3). The species are widespread in distribution,
from lower to higher altitudes. All species
collected are common and abundant, especially in
239
Table 1. List of oligochaete species from the Morava and Odra River
Basins in the Czech Republic and the abbreviation of each species
Species Abbreviation
Aeolosoma hemprichi Ehrenberg, 1831 Aeol hem
Aulodrilus pluriseta (Piguet, 1906) Aulo pur
Bothrioneurum vejdovskyanum ˘Stolc, 1886 Both vej
Bythonomus lemani Grube, 1880 Byth lem
Cernosvitoviella sp. Cern sp
Chaetogaster cristallinus Vejdovsk´y, 1883 Chae cri
Chaetogaster diaphanus (Gruithuisen, 1828) Chae dip
Chaetogaster diastrophus (Gruithuisen, 1828) Chae dis
Chaetogaster langi Bretscher, 1896 Chae lan
Cognettia sp. Cogn sp
Criodrilus lacuum Hoffmeister, 1845 Crio lac
Eiseniella tetraedra (Savigny, 1826) Eise tet
Enchytraeidae Ench ind
Enchytraeus sp. Ench sp
Fridericia sp. Frid sp
Haplotaxis gordioides (Hartmann, 1821) Hapl gor
Limnodrilus hoffmeisteri Clapar`ede, 1862 Limn hof
Limnodrilus udekemianus Clapar`ede, 1862 Limn ude
Limnodrilus sp. juv. Limn spj
Lumbricidae Lumb ind
Lumbriculus variegatus Grube, 1844 Lumb var
Mesenchytraeus armatus Levinsen, 1884 Mese arm
Mesenchytraeus sp. Mese sp
Nais alpina Sperber, 1948 Nais alp
Nais bretscheri Michaelsen, 1899 Nais bre
Nais communis Piguet, 1906 Nais com
Nais elinguis O. F. Müller, 1773 Nais eli
Nais pseudoobtusa Piguet, 1906 Nais pse
Nais simplex Piguet, 1906 Nais sim
Nais variabilis Piguet, 1906 Nais var
Nais sp. Nais sp
Ophidonais serpentina (O. F. Müller, 1773) Ophi ser
Potamothrix hammoniensis (Michaelsen, 1901) Pota ham
Potamothrix sp. juv. Pota spj
Pristinella menoni (Aiyer, 1930) Pris men
Pristinella rosea (Piguet, 1906) Pris ros
Pristinella sp. Pris sp
Propappus volki Michaelsen, 1905 Prop vol
Psammoryctides barbatus (Grube, 1861) Psam bar
Rhyacodrilus coccineus (Vejdovsk´y, 1875) Rhya coc
Rhyacodrilus falciformis Bretscher, 1901 Rhya fal
Slavina appendiculata (Udekem, 1855) Slav app
Stylodrilus heringianus Clapar`ede, 1862 Styl her
Stylodrilus parvus (Hrab˘e & ˘Cernosvitov, 1927) Styl par
Stylodrilus sp. juv. Styl spj
Trichodrilus sp. Tric sp
Tubifex ignotus (˘Stolc, 1886) Tubi ign
Tubifex tubifex (O. F. Müller, 1774) Tubi tub
Tubificidae juv. Tubi juv
Uncinais uncinata (Ørsted, 1842) Unci unc
Vejdovskyella comata (Vejdovsk´y, 1883) Vejd com
polluted waters (Brinkhurst, 1971). COD and the sediment
structure, as the most significant factors for
oligochaete occurrence, have been mentioned by other
authors (Brinkhurst, 1967; Uzunov, 1982).
The distribution of Limnodrilus hoffmeisteri
Claparède, 1862, Nais elinguis Müller, 1773, Chaetogaster
langi Bretscher, 1896, Ophidonais serpentina
(Müller, 1773) and Pristinella rosea (Piguet, 1906) is
positively correlated with water hardness, Ca2+, Mg2+
and NO3
−-N and negatively correlated with altitude
(Fig. 3). All are known to occur also in stagnant waters.
While the values for water hardness, and Ca2+
and Mg2+ ion concentration are readily influenced by
easily eroded bedrock, the presence of these ions also
depends also on the concentration of dissolved CO2,
which is related to water eutrophication.
Major changes in the structure of oligochaete
assemblages related to water mineralization, substrate
type, and current velocity were documented by
Martínez-Ansemil & Collado (1996), who studied Oligochaeta
inhabiting largely unpolluted watercourses
in Galicia (Spain) and Northern Portugal. Dumnicka
(1978), in her studies of Oligochaeta in the River Nida,
Poland, concluded that bottom type and current speed
as well as hardness or Ca2+ and Mg2+ content determine
the composition of oligochaete communities.
With the exception of the species noted above,
naidids are distributed in streams with the lower content
of organic matter and coarse substratum (Fig. 3),
which is typical for unpolluted waters. This group is
distributed both at low and high altitudes.
While oligochaete distribution in small streams
is determined by COD, water hardness (MartínezAnsemil
& Collado, 1996) or current velocity (Dumnicka,
1978), substrate type seems to be the most important
factor governing the presence of Oligochaeta
in large rivers (˘Sporka, 1998; Montanholi-Martins &
Takeda, 1999; Rempel et al., 2000). This could also be
influenced by the presence of a sufficient food supply.
The results of this study also suggest that oligochaetes,
a group which demonstrate a broad range of ecological
tolerance, are nonetheless more restricted at the family
level to certain types of environments.
Acknowledgements
This project was supported by grants from Masaryk
University No. 206/99/1522 and from Ministry
of Education No. 143100010. We wish to thank
our teacher Prof. F. Kubí˘cek for assistance with
240
macroinvertebrate identifications, advice and direction
throughout this study. We also thank first author’s
father Prof. J. Gaisler for critical review of the manuscript
and M. J. Wetzel (Illinois Natural History
Survey, Champaign, U.S.A.) for language help and
suggesting many helpful improvements.
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53
Schenková, J. & J. Helešic, 2006
Habitat preferences of aquatic Oligochaeta (Annelida) in the Rokytná River, Czech Republic
– a small highland stream. Hydrobiologia, 564, 117–126.
Habitat preferences of aquatic Oligochaeta (Annelida) in the Rokytna´ River,
Czech Republic – a small highland stream
Jana Schenkova´ * & Jan Helesˇ ic
Institute of Botany and Zoology, Masaryk University, Kotla´rˇska´ 2, 611 37 Brno, Czech Republic
(*Author for correspondence: Fax: +420541211214; E-mail: schenk@sci.muni.cz)
Key words: Oligochaeta, habitat preferences, distribution pattern, temporal variability, multivariate analysis
Abstract
Research was carried out to determine aquatic oligochaete habitat preferences in the Rokytna´ River (Thaya
River basin), a sixth order highland stream in the Czech Republic during the period of April 1999–April
2001. Quantitative samples were collected and current velocity and basic physico-chemical variables were
measured monthly in four typical habitats in the Rokytna´ River. During this study, 28, 842 individuals
representing 44 oligochaete species or higher taxa were collected. Temporal variability of proportional
occurrence of trophic groups found on selected habitats (gathering collectors and grazers) was analysed.
Habitat preferences of oligochaete species were evaluated by Canonical Correspondence Analysis
(CANOCO). Biochemical oxygen demand (BOD) and nitrate (NO3
)
) ion concentration were the most
important variables explaining the distribution of Oligochaeta along the first axis. Current velocity (at 40%
of the depth) and presence of oligochaetes associated with the habitat where gravel bars never formed were
the most important variables along the second axis. Both axes were correlated with the temperature,
reflecting the sampling in summer along the first axis and sampling in late spring along the second axis. The
amount of organic matter (BOD) and concentrations of NO3
)
ions represented both oligochaete food source
and decomposition products contributing to the growth of algae. Current velocity and preferred habitat
explained the spatial pattern of oligochaete distributions.
Introduction
A wide range of environmental factors permanently
influences aquatic ecosystems. Major
physico-chemical factors are mostly defined by
geology, geomorphology, and climate, and aquatic
ecosystems can also be affected significantly by
human activity. The oligochaete community composition
reflects the states and changes in these
variables. Even under natural conditions, a dynamic
process of disturbance and change in the
community composition occurs continuously
(Hynes, 1970; Williams, 1980). The influence of
stream hydrology, and physical and chemical
factors on aquatic Oligochaeta (Annelida) have
been studied by many authors (e.g., Korn, 1963;
Dumnicka & Pasternak, 1978; Prenda & Gallardo,
1992; Martı´nez-Ansemil & Collado, 1996;
Verdonschot, 2001).
A moderately polluted highland stream was
selected to study habitat preferences within the
aquatic oligochaete community. The first objective
was to follow the temporal variability of the
community composition over a 2-year study. Oligochaete
species were divided according to their
feeding habits (Moog, 1995) into two groups –
grazers and gathering collectors, and temporal
variability in their proportional occurrence was
evaluated. Such changes were followed separately
on four dominant habitats differing from hydrological
point of view.
The second objective was to evaluate, by means
of multivariate analysis, environmental variables
significant for the oligochaete distribution and
Hydrobiologia (2006) 564:117–126 Ó Springer 2006
P.F.M. Verdonschot, H. Wang, A. Pinder & R. Nijboer (eds), Aquatic Oligochaete Biology IX
DOI 10.1007/s10750-005-1713-0
thus to establish if selected habitats play an
important role in oligochaete community compo-
sition.
Study area
The oligochaete fauna was studied in the Rokytna´
River (Thaya River basin, Czech Republic), a sixth
order stream (Strahler, 1957). The Rokytna´ River
is 89.3 km long, with a catchment area of
585.4 km2
; the mean annual discharge at the
mouth is 1.27 m3
s)1
. The present study was conducted
in a 60 m reach of the river, located at river
km 9, at an altitude of 220 m and a slope of
3.2 m km)1
.
The hydrology at the study reach is characterised
by two (summer and winter) annual maximum
discharge levels: 1999 (14.6 and 6.0 m3
s)1
respectively), 2000 (3.8 and 24.3 m3
s)1
respectively),
and 2001 (2.2 and 7.5 m3
s)1
respectively).
Highly variable discharges are often associated
with agricultural landscapes – the catchment area
is not able to absorb either summer rainstorms or
winter snow-melt. The substrate of the stream
within this study area consists of pebbles, gravel,
and small amount of sand. For the studied river
stretch, an alternating of the straight and meander
parts is typical.
On the gravel substratum, periphyton developed
in spring, dominantly represented by Bacillariophyceae
(Marvan, 1998), but the character of
the river bottom did not enable a growth of macro-
phyta.
Materials and methods
Habitat types
Four major habitat types on two cross-sections
were sampled monthly, from April 1999 to April
2001. One sample was taken at cross-section A,
situated in the streamline. This part of the river
was chosen, as a representative of the natural
straight part of the river, where gravel bottom does
not form either gravel bars or islands. Three
samples were taken in a meander at cross-section B
to include all different habitats of this river stretch.
One in the littoral, drying up part (depositional
zone indicated as B littoral), one on the gravel bar
(indicated as B gravel bar) and one in streamline
(erosional zone: B streamline), respectively
(Fig. 1). Water depth, current velocity at the bottom
and at 40% of the depth characterised selected
habitats.
‘‘Freeze core’’ method (Bretschko & Klements,
1986) down to the depth of 0.1 m on each of the
selected habitats was used for sediment structure
evaluation twice – in October 2000 and June 2001.
Detailed results of the sediment analysis including
organic matter content down to the 0.7 m depth
were published by Helesˇ ic et al. (2005). The sediment
particles were sorted and percent representation
of individual particle sizes was calculated.
The roughness of the substrate of each habitat was
expressed by the phi value (Cummins, 1962) for all
selected habitats as a weighted average of phi
values for each particle size. The smallest value
()3.5) and hence the highest roughness was found
on B gravel bar, similar to that found on habitat A
streamline ()3.2), habitats B littoral and B
streamline had higher values ()2.4 and )2.5), all of
them in October 2000. The bottom roughness almost
did not change on habitats A streamline
()3.1), B gravel bar ()3.4) and B streamline ()2.6)
while in B littoral the bottom roughness increased
()3.6) at the end of investigation in June 2001.
Due to possible habitat damage it was refrained
from more frequent sampling of the substratum.
Although the Rokytna´ River is quite a dynamic
stream, the substratum did not change within a
year except in one of the selected habitats. The
substrate data were not included in analyses below,
but were used to describe the characteristics
of studied habitats.
Environmental variables
The following physico-chemical variables were
recorded during each sampling period: water temperature,
hydrogen ion concentration (as pH),
dissolved oxygen, conductivity, current velocity at
40% of depth, current velocity at bottom, water
depth, biochemical oxygen demand (BOD), chemical
oxygen demand (COD), ammonia and nitrate
nitrogen, and phosphate phosphorus (PO4
3)
). The
values of physico-chemical variables measured
were very similar between habitats, however, the
current velocity differed considerably. Mean daily
118
discharge values of the sampling dates were
obtained from the Czech Hydrometeorological
Institute (Table 1). One value per sampling date
was obtained, since the values did not differ among
studied habitats.
Oligochaeta
The macrozoobenthic populations were sampled
using a Kubı´cˇ ek sampler (0.1 m2
, mesh size
0.5 mm) (Helan et al., 1973). Oligochaete specimens
were fixed in formalin (4%) in the field, and
sorted under the stereomicroscope in the laboratory.
All oligochaete species were mounted in
Canada Balsam (Cranston, 1982) and determined
using keys by Hrabeˇ (1954, 1981), Brinkhurst &
Jamieson (1971), Sperber (1950), Timm (1999) and
Kathman & Brinkhurst (1999). Identification of
Bythonomus lemani was confirmed by microscopical
examination of mounted specimens that
had been embedded in paraffin, sectioned longitudinally,
then stained in haematoxylin (Jı´rovec,
1958).
After the Oligochaeta were divided into trophic
groups (Moog, 1995), the temporal variability in
proportional occurrence of trophic groups found
(gathering collectors and grazers) and their
occurrence on selected habitats was evaluated.
Data processing
Habitat preferences of oligochaete trophic groups
on selected habitats were compared using the
Wilcoxon Matched pair test, because the measured
data did not have normal distributions (Kolmogorov–Smirnov
test) and were dependent on
sampling date. The correlation of two trophic
groups and two environmental variables (temperature
and daily discharge) were evaluated using
the Spearman rank correlation coefficient (Zar,
1984).
Faunistic and environmental data were analysed
by Canonical Correspondence Analysis
(CCA), CANOCO (Ter Braak & Schmilauer,
2002). This method permits the construction of
theoretical variables (ordination axes) that best fit
the species data according to a unimodal method
A
B
width [m]
0
-0.5
-1.0
0
-0.5
-1.0
150
B littoral B gravel bar B streamline
105
50
A streamline
10
depth[m]depth[m]
width [m]
Figure 1. Cross-sections of habitats A and B on the Rokytna´ River, Czech Republic (5 April 2000), and the position of the sampling
points: A streamline, B littoral, gravel bar and streamline (arrows).
119
of ordination. In the canonical ordination these
axes are a linear combination of environmental
variables. The correlations between environmental
variables and the ordination axes are derived and
summarised in the eigenvalue of the ordination
axis. The result of CCA is a set of scores for both
sites and taxa, which can be presented as twodimensional
ordination diagram where points
represent sites or taxa and lines outgoing from the
origin expresses environmental variables (Ter
Braak & Schmilauer, 2002). The length of the lines
represents the importance of the respective vari-
able.
The data were not transformed and species
were not down-weighted. The statistical significance
of the relationship between all species and
all variables was tested by Monte Carlo permutation
test using 9999 permutations (Ter Braak &
Schmilauer, 2002).
Results
Oligochaeta
During this study, 28 842 individuals representing
36 species of the families Lumbriculidae, Naididae,
Tubificidae, and Lumbricidae were collected and
identified (Table 2). In addition, the family
Enchytraeidae was represented by unidentified
species in four genera. Psammoryctides barbatus
and Bothrioneurum vejdovskyanum (Tubificidae)
and Nais elinguis (Naididae) were the dominant
species.
Trophic groups
Most of the recorded species belong to two trophic
groups, gathering collectors and grazers. Species
with more trophic adaptations (Moog, 1995), the
dominant feeding habit was used for evaluating.
The third group, predators (only within the genus
Chaetogaster) represented only about 0.1% of the
total number of individuals and therefore was
omitted in the analyses. Though the proportion of
trophic groups (gathering collectors and grazers)
varied among habitats, these differences were
insignificant (p>0.05) (Wilcoxon Matched pair
test).
The occurrence of grazers was positively
correlated (Spearman rank correlation coefficient,
p<0.05) with the discharge and negatively with
temperature on habitat A streamline (Fig. 2a). The
grazers were also negatively correlated with temperature
habitat B streamline (Fig. 2b) and gathering
collectors were positively correlated with
temperature on habitat A streamline (Fig. 2c),
(Spearman rank correlation coefficient, p<0.05).
Table 1. Minimum, maximum, mean and median values of environmental variables of the Rokytna´ River over the period April 1999–
April 2001
Variable Min. Max. Mean Median
Water temperature (°C) )0.2 19.4 11.0 13.0
pH 4.4 9.0 7.6 7.7
O2 [mg l)1
] 6.59 18.20 10.4 9.43
Conductivity [lS cm)1
] 453 725 615 615
Current velocity at bottom [m s)1
] 0 0.87 0.34 0.30
Current velocity at 40% of depth [m s)1
] 0 1.46 0.67 0.68
Mean daily discharge [m3
s)1
] 0.13 3.95 1.36 1.08
Depth [m] 0.10 0.47 0.22 0.20
BOD [mg O2 l)1
] 1.9 15.8 5.4 4.5
COD [mg O2 l)1
] 26.1 51.1 27.8 32.2
NO3
)
[mg l)1
] 12.0 57.5 27.8 20.0
NH4
+
[mg l)1
] 0.25 1.10 0.60 0.60
PO4
3)
[mg l)1
] 0.05 1.80 0.85 0.90
120
Table 2. List of oligochaete taxa recorded, taxon code, frequency of occurrence, percentage of occurrence and trophic group (gat –
gathering collector, gra – grazer and pre – predator)
Taxon Abbreviation No. of individuals % Trophic group
Lumbricidae
Allolobophora chlorotica Savigny, 1826) Allo chl 28 0.10 gat
Eiseniella tetraedra (Savigny, 1826) Eise tet 26 0.09 gat
Enchytraeidae
Enchytraeus g. sp. div. Ench sp 64 0.22 gat
Fridericia g. sp. Div. Frid sp 54 0.19 gat
Cernosvitoviella g. sp. div. Cern sp 3 0.01 gat
Cognettia g. sp. div. Cogn sp 32 0.11 gat
Tubificidae
Aulodrilus pluriseta (Piguet, 1906) Aulo plu 2 0.01 gat
Bothrioneurum vejdovskyanum Sˇ tolc, 1886 Both vej 2604 9.03 gat
Limnodrilus claparedeanus Ratzel, 1868 Limn cla 3 0.01 gat
Limnodrilus hoffmeisteri Claparede, 1862 Limn hof 167 0.60 gat
Limnodrilus udekemianus Claparede, 1862 Limn ude 6 0.02 gat
Limnodrilus g. sp. div. juv. Limn sp 2292 7.95 gat
Moraviodrilus pygmaeus Hrabeˇ , 1935 Mora pyg 386 1.34 gat
Potamothrix hammoniensis (Michaelsen, 1901) Pota ham 7 0.02 gat
Psammoryctides barbatus (Grube, 1861) Psam bar 5482 19.01 gat
Psammoryctides moravicus (Hrabeˇ , 1934) Psam mor 5 0.02 gat
Rhyacodrilus coccineus (Vejdovsky´ , 1875) Rhya coc 41 0.14 gat
Rhyacodrilus falciformis Bretscher, 1901 Rhya fal 1395 4.84 gat
Rhyacodrilinae juv. with hair chaetae Rhya juv 1634 5.67 gat
Spirosperma ferox Eisen, 1879 Spir fer 1 0.003 gat
Tubifex tubifex (O. F. M}uller, 1774) Tubi tub 50 0.17 gat
Tubificidae juv. with hair chaetae Tubi juv 957 3.32 gat
Naididae
Chaetogaster diaphanus (Gruithuisen, 1828) Chae dip 21 0.07 pre
Chaetogaster diastrophus (Gruithuisen, 1828) Chae dis 7 0.02 pre, gat, gat
Nais alpina Sperber, 1948 Nais alp 461 1.60 gra, gat
Nais barbata O. F. M}uller, 1773 Nais bar 108 0.37 gra, gat
Nais bretscheri Michaelsen, 1899 Nais bre 857 2.97 gra, gat
Nais communis Piguet, 1906 Nais com 144 0.50 gra, gat
Nais elinguis O. F. M}uller, 1773 Nais eli 5580 19.34 gra, gat
Nais pardalis Piguet, 1906 Nais par 6 0.02 gra, gat
Nais pseudobtusa Piguet, 1906 Nais pse 48 0.17 gra, gat
Nais simplex Piguet, 1906 Nais sim 20 0.07 gra, gat
Nais variabilis Piguet 1906 Nais var 1 0.003 gra, gat
Ophidonais serpentina O. F. M}uller, 1773 Ophi ser 4 0.01 gra, gat
Pristina aequiseta Bourne, 1981 Pris aeq 56 0.19 gra, gat
Pristina bilobata (Bretscher, 1903) Pris bil 19 0.07 gra, gat
Pristina rosea (Piguet, 1906) Pris ros 323 1.12 gra, gat
Stylaria lacustris (Linnaeus, 1767) Styl lac 2 0.01 gra, gat
Vejdovskyella intermedia (Bretscher, 1896) Vejd int 22 0.08 gra, gat
Continued on p. 122
121
Habitat preferences
Canonical correspondence analysis (Fig. 3) was
used to extract species–environment relationships;
44 taxa and 13 environmental variables and 8
nominal variables in 84 samples were evaluated.
Four nominal variables represented selected habitats
– A streamline, B littoral, B gravel bar, and B
streamline, and four nominal variables represented
seasons – spring (March–April), spring/summer
(May–June), summer (July–August), and autumn/
winter (September–February). These sampling
periods correspond more closely with temporal
changes in oligochaete community composition
than the four ‘standard’ seasons (e.g., winter=21
December through 20 March). The statistical significance
of environmental variables was assessed
by Monte Carlo permutation test. Ranked from
the most to the least: BOD, temperature, habitat A
streamline, NO3
)
, current velocity at 40%, habitat
B streamline, summer sampling and conductivity
were significant.
The eigenvalues for the four axes are 0.325,
0.171, 0.084, and 0.075, respectively. According to
the weighted correlation matrix, the first axis
(40.8% variance of the species–environment relation)
is related to BOD (0.592) and NO3
)
(0.350)
and thus represents the food source (NO3
)
as
indicator of a nutrient source for algae and diatoms).
The second axis (21.6% of variance) is
correlated with current velocity at 40% of the
depth (0.400) and presence on habitat A streamline
()0.408), explained spatial variability. Both axes
are negatively correlated with temperature
()0.334, )0.396 respectively), which reflects the
summer sampling along the first axis ()0.518) and
the spring/summer sampling ()0.421) along the
second axis respectively (Fig. 3). The third
ordination axis (10.6% of variance) is positively
correlated with the presence of oligochaetes
on habitat B streamline (0.391), BOD (0.376),
temperature (0.360) and negatively with NO3
)
()0.401).
In the ordination diagram representatives of
the family Naididae were in right upper corner
showing development at lower temperatures, in
spring. Most of Tubificidae representatives were
negatively correlated with current velocity in 40%
of the depth and occurred on habitat A streamline.
Discussion
Most oligochaete species found in the Rokytna´
River occurred within a wide range of environmental
conditions, demonstrating a large temporal
and spatial variability. Oligochaete composition
on four selected habitats did not differ significantly
when comparing proportion of two feeding
groups. We suggest that density changes of grazers,
which were negatively correlated with the
temperature and positively with discharge, were
directly caused by periphyton growth. The grazers
represented by members of the family Naididae
have maximal development in winter and spring
(Pfannkuche, 1981) when sufficient light enables
the development of periphyton, also Sˇ porka (1996)
have found that the abundance of the family
Naididae is dependent on the quantity of periphyton.
The positive correlation of gathering collectors
and the temperature again correspond with
availability of food sources. They reach maximal
densities in summer (Lazim & Learner, 1986),
when decaying organic matter is available. Most
significant relationships were associated with a
very stable habitat A; the fact that gravel bars
never form there enhance oligochaete growth.
Table 2. (Continued)
Taxon Abbreviation No. of individuals % Trophic group
Lumbriculidae
Bythonomus lemani (Grube, 1879) Byth lem 1401 4.86 gat
Lumbriculus variegatus O. F. M}uller, 1774 Lumb var 14 0.05 gat
Stylodrilus parvus (Hrabeˇ & Cˇ ernosvitov, 1927) Styl par 813 2.82 gat
Stylodrilus heringianus Claparede, 1862 Styl her 49 0.17 gat
Stylodrilus g. sp. div. juv. Styl juv 3647 12.64 gat
Total 28 842 100.00
122
2.
0.0
0.5
1.0
1.5
2.0
5
3.0
IV.99
V.99
VI.99
VII.99
VIII.99
IX.99
X.99
XII.99
II.00
III.00
IV.00
V.00
VI.00
VII.00
VIII.00
IX.00
X.00
XII.00
II.01
III.01
IV.01
date
-5.0
0.0
5.0
10.0
15.0
20.0
log(n+1)ofdensities[indm
-2
]
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
IV.99
V.99
VI.99
VII.99
VIII.99
IX.99
X.99
XII.99
II.00
III.00
IV.00
V.00
VI.00
VII.00
VIII.00
IX.00
X.00
XII.00
II.01
III.01
IV.01
date
-5.0
0.0
5.0
10.0
15.0
20.0 log (n+1)
discharge [m3 s-1]
temperature [˚C]
grazers on habitat A streamline
grazers onhabitat B streamline
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
IV.99
V.99
VI.99
VII.99
VIII.99
IX.99
X.99
XII.99
II.00
III.00
IV.00
V.00
VI.00
VII.00
VIII.00
IX.00
X.00
XII.00
II.01
III.01
IV.01
date
-5.0
0.0
5.0
10.0
15.0
20.0
gathering collectors on habitat A streamline
(a)
(b)
(c)
Figure 2. The temporal variability of grazers on habitat A streamline, positively correlated with the discharge and negatively with
temperature (a) The temporal variability of grazers on habitat B streamline, negatively correlated with temperature (b) The temporal
variability of gathering collectors on habitat A streamline, positively correlated with temperature (c) (Spearman rank correlation
coefficient, p<0.05).
123
Variability of current velocities in different habitats
of cross-section B resulted in either the
movement of worms between habitats or their
downward burrowing into hyporheic layers.
Habitat preferences of various species were
evaluated using CANOCO. Oligochaete community
composition was dependent upon organic
matter input (BOD) and sources of inorganic ions
NO3
)
(aerobic degradation product and secondary
periphyton nutrient source) along the first axis.
The second axis was correlated with current
velocity and presence on habitat A streamline. The
most important variable determining oligochaete
community composition in habitats assessed during
this study was habitat A streamline in which
little if any shifting of substrate occurred – it offered
stable conditions for oligochaete occurrence,
especially permanent availability of organic matter
in substratum. Both axes, however, were also
correlated with temperature and seasons of
sampling, thus representing temporal variability.
The values for chemical variables monitored during
this study indicate that the Rokytna´ River
varies from slightly to strongly polluted stream
within a year. Detecting the habitat preferences of
species in polluted waters is problematic. Some
authors (Dumnicka & Pasternak, 1978; Culp
et al., 1983; Prenda & Gallardo, 1992) showed that
certain oligochaete species were not habitat selective.
In CCA analysis, two of the four selected
habitats (B littoral and B gravel bar) showed only
small reaction with the oligochaete distribution.
Although both were differing in environmental
conditions with respect to velocity and depth, the
oligochaete composition was quite similar there.
The position of these environmental variables is
similar in the diagram (Fig. 3), although they are
not correlated. CCA analysis showed that certain
habitats are vital for oligochaete occurrence
(habitat A streamline was the third most impor-
0.8
-1.0 1.0
-0.8
Aulo plu
Allo chl
Both vej
Byth lem
Cern sp
Chae dip
Chae dis
Cogn sp
Eise tet
Ench sp
Frid sp
Limn cla
Limn hof
Limn ude
Limn juv
Lumb var
Mora pyg
Nais alp
Nais bar
ais bre
Nais com
Nais eli
Nais par
ais pse
Nais sim
Nais var
Ophi ser
Pota ham
Pris aeq
Pris bil
Pris ros
Psam bar
sam mor
Rhya juv
Rhya coc
Rhya fal
Spir ferStyl lac
Styl her
Styl par
Styl juv
Tubi tub
Tubi juv
Vejd int
A
BL
BG
BS
spring
spring/summer
summer
autumn/winter
temperature
conductivity
velocity at 40%
BOD
NO3
Figure
3. CCA diagram of the axis 1 and 2 of oligochaete taxa (for abbreviations see Table 2) in relation to environmental variables
(arrows), seasons (diamonds) and sampled habitats (points): A = A streamline, BL = B littoral, BG = B gravel bar, BS = B
streamline – recorded in the Rokytna´ River.
124
tant environmental variable); other variables were
less important. Results were significantly influenced
by temporal variability – oligochaete community
composition differed both in time and in
space.
We conclude that, at least in the lower reaches
of a highland stream, habitats do not play as an
important role as has been demonstrated in high
order streams (Korn, 1963; Montanholi-Martins
& Takeda, 1999, 2001). Although some authors
(Montanholi-Martins & Takeda, 1999) applied a
very similar sampling scheme, they found spatial
distribution to prevail over the temporal one. Our
conclusions are similar to those of Verdonschot
(2001), who studied the influence of different
substrates in lowland rivers. There were no significant
relationships with the habitats if the most
of the study streams included them. According to
Verdonshot (2000) the disturbance caused by
agricultural activities in the catchment area can
cause that only ubiquists without habitat preferences
settle the bottom. Most of the oligochaete
species show wide ecological valences and habitat
preferences are not significant when comparing
relatively close sampling points in streams particular
in agricultural areas. Relatively natural
character of the stream is why we found two
(stable) habitats important for oligochaete occurrence.
On the other hand, the impact of agriculture
causes extreme discharges and this promotes
ubiquist species whose community composition
and abundance, therefore, varies with time rather
than with habitat.
Acknowledgements
The authors would like to thank Prof. J. Gaisler
(Institute of Botany and Zoology, Masaryk University)
and Mr. M. J. Wetzel (Illinois Natural
History Survey, Champaign, U.S.A.) for their
critique of this manuscript and assistance in
improving the English. We are also grateful to our
team of co-workers in field and laboratory for
their helpful assistance. Financial support was
kindly granted by Masaryk University (No. 206/
01/0902) and Ministry of Education of the Czech
Republic (No. 0429).
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64
Schenková, J., J. Helešic & J. Jarkovský, 2006
Seasonal dynamics of Bythonomus lemani and Bothrioneurum vejdovskyanum (Oligochaeta,
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Biologia, Bratislava, 61/5: 517—523, 2006
Section Zoology
DOI: 10.2478/s11756-006-0085-x
Seasonal dynamics of Bythonomus lemani
and Bothrioneurum vejdovskyanum (Oligochaeta, Annelida)
in relation to environmental variables
Jana Schenková1
, Jan Helešic1
& Jiří Jarkovský2
1
Masaryk University, Faculty of Science, Institute of Botany and Zoology, Kotlářská 2, CZ–61137 Brno, Czech Republic;
e-mail: schenk@sci.muni.cz
2
Masaryk University, Centre of Biostatistics and Analyses, Faculty of Medicine and Faculty of Science, Kamenice 126/3,
CZ–62500 Brno, Czech Republic
Abstract: The seasonal dynamics of Bythonomus lemani (Lumbriculidae) were studied for the first time and the knowledge
of Bothrioneurum vejdovskyanum (Tubificidae) was extended based on four quantitative samples of oligochaetes taken
monthly in the Rokytná River (Czech Republic) during a two-year study (April 1999 – April 2001). The influence of water
temperature, velocity, depth, discharge, pH, conductivity, dissolved oxygen amount and biochemical oxygen demand (BOD)
on their life cycles was evaluated. Habitat preferences of the juvenile and adult stages were recorded. Time series analysis
was used to determine the worm densities, seasonality and trends. For Byth. lemani one distinct reproduction cycle per
year was found and this was regulated by temperature, while Both. vejdovskyanum showed a one-year cycle not significantly
dependent on measured environmental variables. The overall trend was an increase in density for Byth. lemani and a decrease
in density for Both. vejdovskyanum. Byth. lemani showed a significant negative correlation between the trend of its density
and BOD concentration.
Key words: Bythonomus lemani, Bothrioneurum vejdovskaynum, aquatic Oligochaeta, seasonal dynamics, time series
analysis.
Introduction
The knowledge on the seasonal population dynamics
of certain aquatic oligochaetes is limited. As early as
in the first half of the last century, Hrabě (1935a,
b) studied the reproduction of Bothrioneurum vejdovskyanum
Štolc, 1888 (Tubificidae) and described
its asexual reproduction, at that time not known
in any representative of this family. Brinkhurst &
Kennedy studied other tubificid species in the second
half of the last century (Brinkhurst & Kennedy,
1965; Brinkhurst, 1966; Kennedy, 1966). The best
known are the life cycles of Tubifex tubifex (M¨uller,
1774), Limnodrilus hoffmeisteri Clapar`ede, 1862 and L.
udekemianus Clapar`ede, 1862 (Ladle, 1971; Bonomi,
1979, 1980; Pfannkuche, 1981; Lazim & Learner,
1986; Lazim et al., 1989) because of their high abundance
in polluted waters. Other species of this family
which have been studied include Potamothrix hammoniensis
(Michaelsen, 1901) (Thorhauge, 1976; Risnoveanu
& Vadineanu, 2002), Psammoryctides barbatus
(Grube, 1861) and Spirosperma ferox Eisen, 1879
(Adreani et al., 1984).
Freshwater species of the family Lumbriculidae and
Propappidae represented by Stylodrilus heringianus
Clapar`ede, 1862, S. parvus (Hrabě-Černosvitov, 1927)
and Propappus volki Michaelsen, 1916 were studied
by Dumnicka & Kukula (1990) and Petto &
Humpesch (1992). Some species from the family Naididae
were also studied (e.g., Learner et al., 1978;
Dumnicka, 1982).
Recently there has been a shift from studies following
only changes in the numbers of worms to more
sophisticated techniques such as modelling of seasonal
dynamics. In this study we aim to evaluate the seasonal
dynamics of Bythonomus lemani (Grube, 1879) (Lumbriculidae)
and Bothrioneurum vejdovskyanum (Tubificidae)
because they are very rare and rare species,
respectively, in the Czech Republic and information
about their natural reproduction strategy is scarce (especially
for Byth. lemani). Distribution of the Palaearctic
species Byth. lemani covers S and C Europe and
the study area lies on its northern margin. The conservation
of this rare species requires more knowledge
about its ecological demands. Whereas some authors
(Brinkhurst, 1978; Hrabě, 1981) considered Byth.
lemani to be a stagnant water (lakes) species, others
(Rodriguez & Armas, 1983) considered it an inhabitant
of running waters; certain authors have considered
it as a species of oligosaprobic waters (Uzunov et al.,
c 2006 Institute of Zoology, Slovak Academy of Sciences
518 J. Schenková et al.
1988). The second species, Both. vejdovskyanum, with
a cosmopolitan distribution, is remarkable for its reproduction
by architomy (fission followed by development
of the rest of the body), which is quite rare in the Tubificidae
family.
The species studied represent two different forms
of life strategies, for Byth. lemani sexual reproduction is
typical, while Both. vejdovskyanum reproduces by the
above mentioned architomy. The aim of our study was
to describe and compare their life cycles, to evaluate
which environmental variable(s) regulate them and to
find habitat preferences of juvenile and adult stages of
Byth. lemani.
Material and methods
Study area and sampling
The sixth order Rokytná River (the Thaya River Basin,
Czech Republic), which is influenced relatively little by human
impact, was chosen for this study. The sampling site
was situated on the ninth river km near Moravský Krumlov
(49◦
03 N, 16◦
19 E), with 3.2% slope at 220 m a.s.l. (Fig. 1).
The river bottom mainly consisted of small pebbles, gravel,
sand and, locally, silt. During late winter and in spring periphytic
algae covered the substratum; from the beginning
of May the river channel was shaded and water showed high
turbidity.
Oligochaetes were sampled along two cross-sections (A
and B) across a 60 m long river reach. Cross-section A was a
straight part of the channel, while B was a meandering one;
they differed from one another in the variability of their
width during the year (Tab. 1). Four typical habitats were
sampled at the same time, one on cross-section A and three
on B (Fig. 1). The habitat on cross-section A was located in
the middle of the channel, where small pebbles (20–40 mm)
comprised 40% of bottom substratum and gravel bars did
not form there. This is hereafter referred to as ‘streamline
A’. The habitats on cross-section B were: ‘littoral’, located
close to the right bank of an inner river bend, ‘gravel bar’,
located in the middle of the channel and ‘streamline B’, on
the left side with the strongest water current up to 1.46 [m
s−1
] and the most coarse substratum. Small pebbles (20–
40 mm) formed on cross-section B: 13%, 12% and 17% of
the bottom substrata of littoral, gravel bar and streamline
habitats, respectively. The river channel in cross-section A
remained stable during the two-years sampling period, but
on cross-section B the substratum was continually shifting,
although the general shape of the river channel and character
of the three studied habitats remained approximately
the same.
Oligochaeta
Oligochaeta were sampled monthly from April 1999 to
April 2001 within each habitat except in winter, when
two monthly sampling was used. Quantitative samples were
taken using a Kubíček’s sampler (HELAN et al., 1973) (mesh
size 0.5 mm) from a triangular area of 0.1 m2
. Sampled animals
were stored in 4% formalin in the field and sorted in
the laboratory. Oligochaeta were identified to species level
using the keys of HRABĚ (1954, 1981). The specific identification
of Byth. lemani was tested using cross sectioning.
Abundance of juvenile and adult individuals of Byth. lemani
AS
BS
BG
BL
CZECH REPUBLIC
0 50 100 km
0 10 20 m
Rokytná
River
Fig. 1. Map showing the study site and selected river stretch with
the sampling points. AS – streamline; BL – littoral; BG – gravel
bar; BS – streamline.
and Both. vejdovskyanum were counted. Identification of juvenile
Byth. lemani was possible because they were the only
lumbriculids with simple pointed setae present in the area.
Environmental characteristics
On each sampling date one sample of water for chemical
analysis was taken on cross-section A and biochemical oxygen
demand (BOD) was evaluated in the laboratory. Considering
the dimensions of the river, values of BOD on crosssection
B were considered the same as from A. The water
temperature, velocity at 40% of the depth and velocity close
to the bottom, depth, pH, conductivity and dissolved oxygen
were measured at each of the four habitats. Mean daily
discharges were obtained from the hydrological station situated
6 km downstream from the sampling site.
Statistical analysis
The presence of species in different parts of the stream and
differences in their abundance were evaluated using χ2
test
with a null hypothesis of equal distribution of worms among
habitats. The proportion of adults and juveniles of Byth. lemani
was determined by contingency table analysis. Proportions
of their densities were weighted by the total number
of worms.
Time series analysis was used to evaluate trends in
worm abundance, based on the mean of worm densities and
the means of abiotic parameters. Twenty-five dates were
used in the time series of species density analysis; 21 sampling
events and four missing values (taking into account
two monthly samplings in winter) estimated from adjacent
points in the time period. Data were log transformed. Moving
average smoothing (3 numbers) was applied for visualization
of the time series.
The time series analysis enables division of the total
trend in oligochaete densities into two components: ‘smooth’
– representing a particular trend (increasing/decreasing)
during the whole sampling period and ‘cyclic’ – following
Seasonal dynamics of Bythonomus lemani and Bothrioneurum vejdovskyanum 519
Table 1. Physico-chemical characteristic of the selected sites, cross-sections A and B and habitats AS, BS, BG and BL.
A B
Cross-section
Mean Min.–Max. Mean Min.–Max.
Width (m) 10.35 9.56–14.42 13.02 9.06–18.14
AS BS BG BL
Habitat
Mean Min.–Max. Mean Min.–Max. Mean Min.–Max. Mean Min.–Max.
Temperature (◦C) 11.0 −0.1–19.4 11.0 −0.2–19.4 11.0 −0.2–19.4 11.0 −0.2–17.6
pH 7.5 4.4–9.0 7.7 5.9–9.0 7.6 5.9–8.8 7.5 5.9–8.3
Dissolved O2 (mg L−1) 10.2 6.9–12.4 10.6 7.3–17.5 10.3 7.3–14.2 10.4 7.3–14.2
Conductivity (µS cm−1) 620 468–700 617 479–725 612 536–725 612 536–725
Velocity close to the bottom (m s−1) 0.36 0.16–0.64 0.37 0.13–0.92 0.29 0–0.98 0.35 0.0–0.76
40% velocity (m s−1) 0.70 0.29–1.10 0.84 0.53–1.46 0.57 0.11–0.94 0.55 0.03–1.35
Depth (m) 0.26 0.11–0.47 0.27 0.11–0.42 0.16 0.02–0.36 0.20 0.06–0.38
Mean Min.–Max.
BOD (mg L−1) 5.4 1.9–15.8
COD (mg L−1) 27.8 26.1–51.1
NO−
3 (mg L−1) 27.9 12.0–57.5
NH+
4 (mg L−1) 0.60 0.25–1.10
PO3
4 (mg L−1) 0.85 0.05–1.80
Discharge (m3 s−1) 1.36 0.13–3.95
regularly repeating changes in densities over the course of
time. The smooth component of time series was evaluated by
Daniel’s test (DANIELS, 1950) which in fact is the Spearman
rank correlation between oligochaete densities and their
rank in the time series. For the subsequent analysis of cyclic
component of the time series, the time series was detrended
(i.e., the smooth component was removed) by linear regression.
The cyclic component was computed by two methods;
(i) autocorrelation of abundances and (ii) spectral analysis
of seasonality.
Relationships between abundances and abiotic parameters
were computed by cross-correlation (i.e., correlation
of densities with values of environmental variables shifted
in time) and the lag between them was evaluated (BOX &
JENKINS, 1970). The Spearman rank correlation coefficient
was used also to compare trends between species densities
and environmental parameters.
The analyses were performed using Statistica 7 for
Windows (STATSOFT, 2004).
Results
Environmental variables
Seasonal changes of physico-chemical variables in the
studied river stretch over two years were recorded
(Tab. 1). All values were calculated from the same number
of measurements (n = 21). In the highland river water
quality became near oligosaprobity during the winter,
while in the summer sufficient autochthonous and
allochthonous organic matter sources created a status
close to β-mesosaprobity (ČSN 75 7358, 1997).
Oligochaeta
Of the total number of 28,842 oligochaetes (36 species),
100 µm
at
ov
sp
vdte
ffsf
te
pe
pr
IX X XI
sf
Fig. 2. Bythonomus lemani. Schematic drawing of reproductive
organs, IX, X, XI segment, lateral view: at – atrium; ff – female
funnel; ov – ovarium; pe – penis; pr – prostate gland; sf – sperm
funnel; sp – spermatheca; te – testes; vd – vas deferens.
900 juvenile and 506 adult individuals of Byth. lemani
and 2,590 juvenile and 14 adult individuals of Both.
vejdovskyanum were found. In Byth. lemani, the following
identification characters were revealed: the clitellum
began in the half of segment IX and extended
into segment XIII, the paired mushroom-like spermatecae
were situated in segment IX, two pairs of testes
were in the IX and X segment, atria entered into small
penes in segment X (Fig. 2). Adults of Byth. lemani
were observed throughout the year. Adults of Both. vejdovskyanum
occurred only rarely because of asexual reproduction,
with seven individuals found in May 1999,
four in May 2001 and three in June 2001. Mean density
of Byth. lemani was 220 ind. m−2
while that of Both.
vejdovskyanum was 370 ind. m−2
.
520 J. Schenková et al.
Bothrioneurum vejdovsk ya num habitat A s tre am line
0
50
100
150
200
250
300
350
400
density[ind.0.1m-1
]
Bothrioneurum vejdovsk yanum habitat B littoral
Bothrioneurum vejdovsk ya num habitat B graveBothrioneurum vejdovsk ya num habitat B s tre am line
100
150
200
250
300
350
400
Bythonomus lemani habitat A s tre am line
0
20
40
60
80
100
120
140
160
180
200
density[ind.0.1m-1
]
Byth lem juv
Byth lem ad
Bythonomus lemani habitat B littoral
Bythonomus lemani habitat B grave l bar
V.99
VII.99
IX.99
XI.99
I.00
III.00
V.00
VII.00
IX.00
XI.00
I.01
III.01
Bythonomus lemani habitat B s tre am line
0
20
40
60
80
100
120
140
160
180
200
IV.99
VI.99
VIII.99
X.99
XII:99
II.00
IV.00
VI.00
VIII.00
X.00
XII.00
II.01
IV.01
Fig. 3. Bythonomus lemani. Seasonal changes in densities of juvenile and adult individuals in four selected habitats.
Bothrioneurum vejdovsk ya num habitat A s tre am line
0
50
100
150
200
250
300
350
400
density[ind.0.1m-1
]
Bothrioneurum vejdovsk ya num habitat B littoral
Bothrioneurum vejdovsk ya num habitat B grave l bar
V.99
VII.99
IX.99
XII:99
III.00
V.00
VII.00
IX.00
XII.00
III.01
Bothrioneurum vejdovskya num habitat B s tre am line
0
50
100
150
200
250
300
350
400
IV.99
VI.99
VIII.99
X.99
II.00
IV.00
VI.00
VIII.00
X.00
II.01
IV.01
Fig. 4. Bothrioneurum vejdovskyanum. Seasonal changes in densities in four selected habitats.
Habitat preferences
Numbers of Byth. lemani differed between the four
habitats (Fig. 3) whereas habitat preference was less
marked for Both. vejdovskyanum (Fig. 4). Significant
inter-habitat differences were found for both Byth. lemani,
(P < 0.01; χ2
= 598; df = 3) and Both. vejdovskyanum,
(P < 0.01; χ2
= 454; df = 3). Byth. lemani
preferred stream line B, a dynamic stretch of the
river with the fastest current (mean water velocity at of
depth 40% was 0.84 m s−1
). Both. vejdovskyanum preferred
stream line A, a relatively straight and shallow
river stretch with less fluctuating water level, with no
shifting of substratum (mean water velocity at of depth
40% was 0.70 m s−1
).
Significant differences in densities of adult and juvenile
Byth. lemani were found among habitats (χ2
=
24.5, P < 0.01). The adults predominated in the habitat
stream line A while juveniles were mostly in littoral
Seasonal dynamics of Bythonomus lemani and Bothrioneurum vejdovskyanum 521
Bothrioneurum vejdovskyanum
V.99
VII.99
IX.99
XI.99
I.00
III.00
V.00
VII.00
IX.00
XI.00
I.01
III.01
0
20
40
60
80
100
120
Bythonomus lemani
V.99
VII.99
IX.99
XI.99
I.00
III.00
V.00
VII.00
IX.00
XI.00
I.01
III.01
0
5
10
15
20
25
30
35
40
45
50
Fig. 5. Time series of Bythonomus lemani and Bothrioneurum vejdovskyanum based on mean densities, moving average smoothing
was applied.
Fig. 6. Peridiograms of Bythonomus lemani and Bothrioneurum vejdovskyanum after extraction of smooth component.
of B. In habitat B stream line, the one generally preferred
by this species, the ratio of adults to juveniles
was balanced.
Time series analysis
The evaluation of smooth components showed significant
trends for both species (Fig. 5). The density of
Byth. lemani was increasing with Daniel’s test value
0.51 (P = 0.017), while that of Both. vejdovskyanum
was decreasing with Daniel’s test value 0.54 (P =
0.011). None of the selected environmental variables
showed a significant trend (using Daniel’s test).
The evaluation of cyclic components using autocorrelation
showed certain cyclic trends, but they were insignificant.
Peridiograms showed one distinct cycle per
year in both species (Fig. 6).
The cross-correlations for the density of Byth. lemani
and Both. vejdovskyanum and environmental variables
showed significant positive cross-correlation of
Byth. lemani with water temperature (two-month lag).
No other significant relationships between either species
or environmental parameters were found. Comparison
of trends of species densities and environmental parameters
revealed some significant trends; a negative correlation
between abundance of Byth. lemani and BOD
(rs = 0.59; P < 0.05).
Discussion
Although Oligochaeta are generally considered as ubiquists
that live in various habitats, significant habitat
preferences were found in the two selected species. Byth.
lemani preferred sites with the highest water velocity
(0.53–1.46 m s−1
), hence we can confirm it as a running
water species (Rodriguez & Armas, 1983) requiring
a sufficient level of dissolved oxygen. Other habitats
were colonised with significantly lower densities – the
straight part of the stream was preferred by adults, the
littoral by juveniles. The arrangement of sexual organs
in this species corresponds to that found by Rodriguez
(1988), but we did not record prostate cells in discrete
masses as stated by Brinkhurst & Jamieson (1971).
Both. vejdovskyanum as a typical tubificid inhabited
the straight part of the stream, the substratum of
which did not shift for most of the year. This distribution
decreased the competition between Byth. lemani
and Both. vejdovskyanum, which were the dominant
species at this site.
Based on worm densities in the Rokytná River during
a two-year study, a model of the reproductive cycle
of Byth. lemani was created. The spectral analysis was
computed and its peridiogram showed one distinct reproduction
cycle per year. Although some adults were
522 J. Schenková et al.
present throughout the year, main breeding activity
started in April. The correlation with water temperature
indicates that increasing temperature in March
may have triggered the development of sexual organs
and the subsequent copulation of worms. Increasing
abundances of juveniles between August and November
indicates that worms were hatching from cocoons
at that time. The juvenile oligochaetes had probably
grown during the winter months and matured during
the spring or summer of the next year. Such a life cycle
is comparable with that of another lumbriculid, Stylodrilus
heringianus (Petto & Humpesch, 1992). These
authors also found a one-year cycle and significant correlation
with water temperature. A similar one-year life
cycle was recorded for S. parvus, with numerous adults
in May and the highest percentage of juveniles in October
(Dumnicka & Kukula, 1990).
The significant negative correlation of Byth. lemani
densities and BOD values can be explained by ecological
adaptation of this species to changing conditions
within the stream. According to Uzunov et al. (1988),
it is an oligo- (80%) or β-mesosaprobic (20%) water
species preferring a small amount of organic pollution
in water. During the part of the year when concentrations
of the dissolved organic matter are highest, most
adults die after deposition of cocoons and the development
of juveniles inside the cocoons takes place. Juveniles’
hatching and growth start in the autumn after
BOD values have decreased. The total trend showing
an increase in the abundance of the oligosaprobic
water species Byth. lemani and a decrease in the βmesosaprobic
species Both. vejdovskyanum (Uzunov et
al., 1988) probably reflected overall changes in water
quality at the site. Our data, however, are insufficient
to specify the impact of particular environmental vari-
ables.
The reproductive strategy of Both. vejdovskyanum
(Tubificidae) is different. The species reproduces by architomy,
and adults are found only sporadically. Our
peridiogram showed a one-year developmental cycle.
These results can be compared with a one year study
by Hrabě (1935a, b) who found worms, with up to 140
segments in winter, whose fission started in the second
half of April, continued during summer, declined
in autumn and completely stopped in winter. Similarly,
in laboratory experiments, Both. vejdovskyanum reproduce
by fragmentation without any marks of degeneration
for several years (Timm, 1984).
When looking at the asexual reproduction of the
Naididae family, we can find the numbers increasing
with temperature in the genus Nais (e.g., Poddubnaya,
1968; Pfannkuche, 1981; Dumnicka, 1982),
except for Nais elinguis M¨uller, 1773 (Learner et al.,
1978). No periodic cycle as a result of asexual reproduction
was found in the genus Chaetogaster (Petto
& Humpesch, 1992).
We can conclude that the life history of the sexually
reproducing lumbriculid Byth. lemani consists of a
one-year reproduction cycle regulated by temperature;
further knowledge of its seasonal dynamics could be obtained
by sampling the smallest juveniles and cocoons.
Under the same conditions asexual reproduction of the
tubificid Both. vejdovskyanum was not affected by temperature,
although it also showed a one-year reproduction
cycle. For this species, a longer study period in the
field will be necessary to find out which environmental
parameter(s) regulate reproduction.
Acknowledgements
We would like to thank A. PINDER (Dept. Conservation and
Land Management, Wanneroo, Australia) and J. GAISLER
(Masaryk University, Brno, Czech Republic) for reviewing
the manuscript and K. TAYLOR for proofreading. The
project was supported by grants from the Grant Agency of
the Czech Republic (No. 206/02/0902) and from the Ministry
of Education, Youth and Sports of the Czech Republic
(MSM0021622416 and MSM0021622412).
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THORHAUGE, F. 1976. Growth and life cycle of Potamothrix hammoniensis
(Tubificidae, Oligochaeta) in the profundal of eutrophic
Lake Esrom. A field and laboratory study. Arch. Hydrobiol.
78: 71–85.
TIMM, T. 1984. Potencial age of aquatic Oligochaeta. Hydrobiologia
115: 101–104.
UZUNOV, V., KOŠEL, V. & SLÁDEČEK, V. 1988. Indicator value
of freshwater Oligochaeta. Acta Hydrochim. Hydrobiol. 16:
173–186.
Received June 23, 2005
Accepted December 13, 2005
72
Syrovátka, V., J. Schenková & K. Brabec, 2009
The distribution of chironomid larvae and oligochaetes within a stony-bottomed river stretch:
the role of substrate and hydraulic characteristics. Fundamental and Applied Limnology,
Archiv für Hydrobiologie, 174, 43–62.
eschweizerbartxxx author
DOI: 10.1127/1863-9135/2009/0174-0043 1863-9135/09/0174-0043 $ 5.00
© 2009 E. Schweizerbart’sche Verlagsbuchhandlung, D-70176 Stuttgart
The distribution of chironomid larvae and oligochaetes
within a stony-bottomed river stretch:
the role of substrate and hydraulic characteristics
Vít Syrovátka*, Jana Schenková and Karel Brabec1
With 9 figures, 4 tables and 1 appendix
Abstract: The taxonomic and functional structure of oligochaete and chironomid communities in a stony-bottomed
river reach was investigated with respect to substrate and hydraulic conditions. Combined oligochaete and chironomid
data were analyzed to search for main gradients and the separate data sets were analyzed to identify the most
important variables determining the structure of the communities. Preferences for particular hydraulic conditions,
expressed as Froude number, were calculated for 29 most abundant taxa. The results of Correspondence Analysis
(CA) indicated that the main gradient in the data could be explained by hydraulic conditions and, inversely, by the
amount of sedimented particulate organic matter (POM). The second CA axis probably reflected the quantity of the
available food and space resources. Canonical Correspondence Analysis (CCA) showed the amount of sedimented
POM as the most important variable explaining 21 and 24 % of the variance in the oligochaete and chironomid data,
respectively. Among the other variables, the occurrence of aquatic vegetation, variability of near-bottom current
velocity and substrate roughness were the most important. In the case of chironomids, the proportions of functional
feeding strategies changed along the gradient of hydraulic conditions: the proportions of predators, active filterfeeders
and collectors/gatherers decreased with the increasing hydraulic stress, while the proportion of grazers/
scrapers increased. Nevertheless, in the case of oligochaetes, the proportions of functional feeding strategies did
not follow the gradient of hydraulic conditions. Although the total abundance of both oligochaetes and chironomids
was independent of hydraulic conditions, only few oligochaete taxa were able to succeed in hydraulically rough
conditions and most oligochaete taxa were found only in pools. On the other hand, chironomids showed high taxa
richness, which seemed to be limited by the quantity of the available food and space resources rather than hydraulic
stress.
Key words: chironomidae, oligochaeta, distribution, substrate, hydraulic conditions, stream.
Introduction
Hydromorphological features of rivers reflecting longterm
climatic and geomorphological processes are being
influenced by anthropogenic impacts and global
changes. The knowledge of distributional patterns of
river biota and its habitat preferences is fundamental
to effective assessment of possible effects of climate
fluctuations and/or anthropogenic impacts on fluvial
ecosystems. In this respect, the following paper aims
to contribute to the knowledge of aquatic macroinvertebrate
distributional patterns.
Physical factors, food availability and biological
interactions are generally proposed as determinants
of spatial variation in the stream community structure
(e.g. Hynes 1970, Cummins et al. 1984, Statzner et
al. 1988). At a larger scale (e.g. catchment) the main
changes in the benthic macroinvertebrate community
structure are usually found along the longitudinal gradient
from source to mouth of a stream and the influAuthors’
address:
1
Department of Botany and Zoology, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic.
* Author for correspondence; e-mail address: syrovat@sci.muni.cz
Fundamental and Applied Limnology
Archiv für Hydrobiologie
Vol. 174/1: 43–62, February 2009
© E. Schweizerbart’sche Verlagsbuchhandlung 2009
eschweizerbartxxx author
44 V. Syrovátka et al.
ence of particular physical and chemical factors is difficult
to separate because all the factors usually change
along with the distance from the source (Lindegaard &
Brodersen 1995).
At a finer scale (mesohabitat – sensu Armitage et
al. 1995) hydraulic and substrate conditions are the
major factors influencing the benthic macroinvertebrate
community structure. These factors are highly
interrelated and each in part depends on the other. The
substrate grain size is determined by past and present
flows (Leopold 1994, Allan 1995) and the grain size
determines surface roughness which, in turn, creates
fine-scale patterns of near-bed flow that influence organic
matter retention and the distribution of benthic
organisms (e.g. Culp et al. 1983, Quinn et al. 1996,
Bouckaert & Davis 1998, Hoover et al. 2006). Some
studies emphasize the importance of substrate – especially
its organic components – in determining the
density, taxa richness, and overall structure of benthic
invertebrate community (Ward 1975, Death & Winterbourn
1994, Way et al. 1995, Beisel et al. 1998, Habdija
et al. 2004, Ortiz et al. 2006) but most of the recent
studies are in agreement that the hydraulic conditions
play the major role (Quinn & Hickey 1994, Rempel et
al. 2000, Doisy & Rabeni 2001, Mérigoux & Dolédec
2004, Brooks et al. 2005).
The mean flow velocity is not an adequate descriptor
of the flow conditions. Therefore, some complex
hydraulic parameters incorporating the velocity, depth
and eventually substrate characteristics were proposed
(Davis & Barmuta 1989). These hydraulic parameters
(e.g. Froude number, boundary Reynolds number,
roughness shear velocity) have proved to be better predictors
of the benthic invertebrate community structure
than the measured current velocity not only in
cases when the substrate roughness and depth varied
within the studied locality (e.g. Qiunn & Hickey 1994,
Doisy & Rabeni 2001, Fesl 2002, Mérigoux & Dolédec
2004, Brooks et al. 2005). Moreover, easily accessible
Froude number (incorporates only the velocity,
depth and acceleration due to gravity) was found to
be strongly related to invertebrate abundance in many
other studies (e.g. Orth & Maughan 1983, Wetmore
et al. 1990, Jowett et al. 1991, Benbow et al. 1997).
Froude number was also identified as a good hydraulic
parameter for objective identification of pool, run, and
riffle habitats (Jowet 1993).
Oligochaeta (sensu oligochaetous Clitellata; Erséus
2005) and chironomid larvae often comprise a large
proportion of benthic macroinvertebrate communities
but due to their small body size and difficulties associated
with their identification, their habitat preferences
and distributional patterns at the mesohabitat scale are
not well known. For chironomid larvae only the works
of Ruse (1994) and Fesl (2002) deal with the spatial
distribution with regard to hydraulic conditions, and
some other studies focus on the preferences of particular
species to particular hydraulic conditions (Collier
1993, Benbow et al. 1997). Only few studies bring any
information about meso- or microhabitat preferences
of oligochaete taxa (Verdonschot 1999, 2001).
Oligochaetes and chironomid larvae differ in many
ways (their physique, life cycle, reproduction), but
they are similar in their relatively small, prolonged and
flexible body. Their body proportions together with the
locomotion type – sprawling/walking, and the absence
of legs enable them to inhabit bed sediments into notable
depths (Schmid 1993, Rulík 1995). Some taxa of
both groups are able to survive in low-oxygen to anoxic
conditions. Collecting/gathering and grazing/scraping
predominate within these groups, though they differ in
feeding mechanisms: contrary to the oligochaetes, chironomids
use chitinous mouthparts such as mandibles
and mentum to graze. Moreover, some chironomid larvae
can utilize particulate organic matter (POM) using
active or passive filtration which is very rare within the
oligochaetes (Learner et al. 1978).
In this study, spatial distribution of oligochaetes
and chironomid larvae at the mesohabitat scale was
investigated. The two groups were chosen because of
their high abundance in benthic stream communities
and their ecological similarity. Sampling was carried
out simultaneously at a single river reach which enabled
elimination of temporal variability and of factors
associated with the longitudinal stream zonation.
The objectives were to i) determine the main gradients
in the structure of oligochaete and chironomid
communities, ii) identify the most important factors
influencing the taxonomic structure of these communities,
iii) identify oligochaete and chironomid community
types and relate them to particular environmental
conditions, and iv) determine habitat preferences of
frequent taxa.
Study site
The Svratka River (Czech Republic) is a rather stable
simple channelled stream, which drains the Czech-
MoravianHighlandswithsiliceousbedrock.Thecatchment
area of about 354 km2
is dominated by coniferous
forests (42 %) and arable land (32 %), followed
by agricultural areas with significant areas of natural
vegetation (14 %), pastures (6 %), urban fabric (3 %)
and transitional woodlands-shrubs (2 %). Mean annual
rainfall in the catchment is about 746 mm year–1
.
eschweizerbartxxx author
Chironomids and oligochaetes in a river 45
The samples were taken from an approx. 300 m
long reach located in the Czech-Moravian Highlands,
480 m above sea level (49° 36′ 51″ N, 16° 13′ 59″ E).
The Svratka is a mid-sized river of the 5th Strahler’s
order at this site. The mean slope of the sampled reach
is 0.28 % and the mean channel width is 12.5 m. Both
river banks are bordered by willows and shrubs that
pass further to a coniferous forest on the left and arable
land on the right side. The median annual discharge in
2002 was 1.9 m3
s–1
(10 % and 90 % quantiles were
1.1 m3
s–1
and 8.2 m3
s–1
, respectively). The mean annual
water temperature in 2002 was 6.9 °C with the
summer maximum of 20.2 °C.
On the sampling date, water conductivity 164 µS
cm–1
and pH 7.36 were recorded. The stream-bed
substrate was dominated by cobbles (mesolithal) but
ranged from sand (psammal) to boulders (macrolithal).
The mineral substrate was covered with fine particulate
organic matter (FPOM) in the deposition areas
with low current, where also patches of leaf accumulation
occurred. Living parts of terrestrial plants (grass
leaves, roots) were observed at the margins. Patches
of aquatic mosses (Fontinalis antipyretica Hedw. and
Hygrohypnum ochraceum (Turn. ex Wils.) Loeske)
and Ranunculus sp. were recorded in the streamline
and the “bare” mineral substrate was usually overgrown
with diatoms.
Methods
Sampling and physical measurements
The sampling was carried out on one occasion (3–4 October
2002) during stable and low flow conditions (1.25 m3
s–1
). The
closest high flow event was recorded 50 days before sampling,
which ought to be sufficient time for stream recovery and recolonization
of habitats.
Mesohabitats (visually distinct areas) were initially visually
assessed according to surface flow characteristics, current
velocity, depth and substrate, and their proportions within the
studied river reach were estimated (± 5 %). In total, 27 samples
were taken. Twenty macroinvertebrate sampling points
were distributed among the mesohabitats proportionally to their
share (one sampling point was assigned for each 5 % of the
river reach). Within each mesohabitat the sampling points were
randomly positioned. Additional 7 macroinvertebrate sampling
points were randomly positioned at mesohabitats represented
by less than 5 % in order to collect samples from the majority of
hydraulic conditions available throughout the study site.
A short underwater video sequence was taken prior to sampling
at each sampling point. It was used to estimate the amount
of organic matter at the sampling points. The dominant and
subdominant substrate was visually classified into categories
according to Hering et al. (2004) and the presence of aquatic
vegetation at the sampling point was recorded. The depth was
measured using a simple mechanic device (Fig. 1a,b) at 25
points arranged in a matrix of 5 by 5 points with 5 cm distance
intervals. Although this procedure was very fast (a few seconds)
it might have disturbed the benthic organisms. A sampling net
was therefore placed downstream the investigated area before
the depth measurements, and the sample was taken immediately
afterwards.
Samples were taken using a hand net (mesh size 250 µm)
from an area of 0.0625 m2
(25 × 25 cm) where the depth was
measured. During sampling the substrate was disturbed by
hands into the depth of approx. 5 cm. Samples were preserved
in 4 % formaldehyde solution.
Current velocity was measured after the sampling (portable
water flow meter, The Marsh-McBirney Model 2000 FlowMate)
in 4 depths (2 cm from the bottom and in 0.2, 0.4 and 0.8
depth from the bottom) at 5 points distributed along the right
and upper edge of the disturbed sampled area.
Water temperature and discharge data were obtained from
the nearest gauge station (Dalečín, approx. 3 km downstream).
There are no major tributaries between the gauge station and
the study site.
Laboratory procedure
The samples were sorted under dissecting microscope in the
laboratory. All the macroinvertebrates were picked up and
stored in 75 % ethanol. Only oligochaetes and chironomid
larvae were identified under microscope and counted for this
study. Small oligochaete specimens (genera Nais and Pristina)
were slide-mounted in the glycerine-water solution (1:5), larger
oligochaetes and all chironomid head capsules in the Canada
balsam. Oligochaetes were identified according to Hrabě (1954,
1981), Brinkhurst & Jamieson (1971), Timm (1999) and Timm
& Veldhijzen van Zanten (2002) and chironomid larvae according
to Cranston (1982), Fittkau & Roback (1983), Nocentini
(1985) and Schmid (1992).
Calculated and estimated environmental
parameters
For the data analyses averages of the five measured values of
the current velocity for each depth were calculated and their
standard deviations were used as a measure of the current velocity
variability in particular depths. Depth was calculated as
the median value of the 25 measured depths.
A smooth inclined plane may provide high substrate roughness
if calculated as an ordinary standard deviation of the measured
depths. Therefore, a plane was fitted linearly through the
25 measured depths (arranged in the matrix of 5 × 5 points) and
the residues of the measured depths from the plane were calculated.
The standard deviation of these residues was used as the
measure of substrate roughness within each sampling area.
The amount of particulate organic matter (POM) was estimated
using the underwater video sequences. Values 0–3 were
assigned to each sampling area according to the quantity of visible
POM (0 – no visible sedimented organic particles (usually
riffles), 1 – some sedimented organic particles present, 2 – fine
organic particles covering most of the mineral substrate, and
3 – the substrate composed mainly of organic parts).
Substrate types were coded according to the estimated particle
size of the dominant mineral substrates. Values 0–6 were
assigned for each substrate type: organic substrate (0), psammal
(1), akal (2), microlithal (3), mesolithal (4), macrolithal (5) and
megalithal (6). For the description and the particle size of the
eschweizerbartxxx author
46 V. Syrovátka et al.
substrate types see Hering et al. (2004). Hydraulic parameters
that were calculated included:
Froude number (Fr) = U/(gD)1/2
Reynolds number (Re) = (UD)/v
roughness shear velocity (U*) = U/ (5.75 log10(12 D/kv))
inferred boundary Reynolds number (Re*) = (U* kv)/v
where D = depth, g = acceleration due to gravity, kv = substrate
roughness, U = current velocity at 0.4 depth and v = kinematic
viscosity of water (1.394 × 10–6
m2
s–1
at 7.8 °C). All the measured
and calculated environmental variables and their ranges
are listed in Table 1.
Community parameters
As the measure of the oligochaete and chironomid diversity,
number of taxa standardized according to Heck et al. (1975) to
50 individuals of each taxonomic group per sample was used. If
there were fewer individuals in a sample, the taxa richness was
not calculated and the sample was omitted.
The proportions of particular feeding strategies within
samples (further in text as proportions of collectors/gatherers,
predators etc.) were calculated using species traits characteristics
listed in the autecological database used in software ASTERICS
(AQEM consortium 2002; see also www.aqem.de and
Fig. 1. The device used for substrate roughness measurements. Two plastic boards are perforated in the middle (25 holes, Ø 11 mm)
and fitted in the metal frame equipped with four adjustable legs. 25 aluminium tubes (Ø 10 mm) go through the holes in both boards
and are blocked on the upper board’s surface by two 300 mm long L-shaped aluminium sticks tight together with two rubber bands.
A 5 mm thick cellular plastic strip is glued to the inner surface of each aluminium stick to adhere better to the surface of the tubes.
Each pair of the aluminium sticks operates 5 tubes. After the positioning of the device at the sampled area, the boards were set
horizontally using the adjustable legs. Then the pairs of the aluminium sticks were pulled apart, so that the tubes could slide down
to the stream-bed. The aluminium sticks were then released again and locked the tubes in their position. As soon as all the tubes
were locked, the whole device was removed from the stream and the tubes were measured on the bank. a) the whole device; b) a
detail of the aluminium sticks in the open position.
eschweizerbartxxx author
Chironomids and oligochaetes in a river 47
www.freshwaterecology.info/). Species traits characteristics of
related taxa were used when the characteristics of the respective
taxon were not available (6 chironomid taxa).
To compare the success of two most frequent feeding strategies
(collecting/gathering and grazing/scraping) all taxa were
classified into the following feeding groups: pure collectors/
gatherers (col), partial collectors/gatherers and partial grazers/
scrapers (col/gr), pure grazers/scrapers (gr), and others (other).
Taxa richness and abundance of particular feeding categories
were computed for each sample from 100 random selections
of 100 individuals. Random selections were performed using
MATLAB Version 6.1.0.450. The classification of taxa is given
in Appendix 1.
Data analyses
For multivariate analyses the species data were log (x+1) transformed.
Detrended Correspondence Analysis (DCA) was used
to identify the length of the main gradient in the faunal data. In
all cases the gradient lengths were between 1.5 and 3.0 standard
deviation units (2.3, 2.0, and 1.9 SDU in the oligochaete,
chironomid, and combined data respectively) indicating that
both the linear and unimodal models were suitable (Ter Braak
& Prentice 1988).
Correspondence Analysis (CA) was used to search for the
main gradients in the combined faunal data and Spearman
rank correlation coefficients of the sample scores with the environmental
and the community parameters were computed to
explain those gradients. Canonical Correspondence Analysis
(CCA) (Ter Braak 1986) using stepwise forward selection was
performed to identify environmental parameters which could
account for the maximum variation in the oligochaete and chironomid
data separately. All environmental variables were used
in this analysis and the significance of each variable was tested
by 999 unrestricted Monte Carlo permutations.
CANOCO for Windows version 4.5 was used for all ordinations.
Correlations were performed using STATISTICA for
Windows version 7.
In the next step, two cluster analyses and subsequent two
Indicator Species Analyses (Dufrene & Legendre 1997) were
performed to group communities according to the oligochaete
and chironomid taxonomic structure separately, and to identify
the taxa characteristic of the community types obtained by the
cluster analysis. Bray/Curtis (Sørensen) dissimilarity index was
used as the distance measure and the grouping was done using
the Flexible Beta linkage method with beta value set at -0.4.
The significance of indicator taxa was tested by 999 Monte
Carlo permutations. Only the taxa with the Indicator Value
higher than 50 were considered good indicators. Clustering and
Indicator Species Analysis were performed using PC-ORD for
Windows Version 4.17.
Hydraulic conditions were identified as the major factor influencing
the structure of the oligochaete and chironomid communities,
and therefore the preferences of particular taxa for
particular hydraulic conditions expressed as the Froude number
were assessed. Medians and 10, 25, 75, and 90 % quantiles of
the Froude number weighted by the abundance of a given taxon
were calculated for each taxon and the values were used to
demonstrate different hydraulic preferences of the taxa. Only
the taxa represented by at least 50 individuals were analyzed.
The result of this analysis might be affected by the irregularity
in the distribution of Froude numbers within the data set.
As there were more samples from habitats with low Froude
number than from habitats with high Froude number, eight
samples were removed to obtain as even distribution of Froude
numbers as possible.
Results
Faunal data
In total 6,275 specimens of 35 oligochaete taxa and
10,272 specimens of 56 chironomid taxa were collected.
The abundance of oligochaetes and chironomid
Table 1. Ranges of measured and calculated environmental variables.
Variable Abbreviation Range of values
Water depth (cm) depth 12.4–50.1
Substrate roughness (SD of 25 water depths) roughness 0.66–5.77
Current velocity in 2 cm from the bottom (cm s–1
) cur_2 0.0–54.8
Current velocity in 0.2 depth from the bottom (cm s–1
) cur_0.2 0.2–65.2
Current velocity in 0.4 depth from the bottom (cm s–1
) cur_0.4 0.2–95.8
Current velocity in 0.8 depth from the bottom (cm s–1
) cur_0.8 3.2–132.0
Variability of current velocity in 2 cm (SD) SDvel2 cm 2.55–37.44
Variability of current velocity in 0.2 depth (SD) SDvel0.2 2.05–32.28
Variability of current velocity in 0.4 depth (SD) SDvel0.4 1.41–47.25
Variability of current velocity in 0.8 depth (SD) SDvel0.8 1.79–26.27
Froude number Fr 0–0.56
Reynolds number Re 0–2061
Roughness shear velocity U* 0–40.35
Inferred boundary Reynolds number Re* 0–52.56
Presence of aquatic vegetation VEG 0/1
Category of the amount of particulated organic matter POM 0–3
Category of mineral substrate particle size mineral 0–6
eschweizerbartxxx author
48 V. Syrovátka et al.
larvae in samples ranged from 21 to 558 (median =
195) and from 65 to 957 (median = 258) individuals
respectively. The number of oligochaete taxa ranged
between 3 and 21 (median = 6), the number of chironomid
taxa ranged between 15 and 32 (median =
23) and the taxa richness of both taxonomic groups
combined ranged between 18 and 50 (median = 28).
Total abundances and frequencies of all taxa are listed
in Appendix 1.
Abundance and taxa richness patterns
The total abundance and diversity of chironomid
communities were independent of hydraulic conditions
(Fig. 2c). Nevertheless, the taxa richness of
chironomids was logarithmically dependent on their
total abundance (Linear regression model, Adjusted
R-squared = 0.9836, p < 0.001) (Fig. 2b), suggesting
their high diversity (Fig. 2a) and their ability to find
favourable conditions in different environments within
the sampled river section. Both chironomid total abundance
and taxa richness were limited by the availability
of food and space resources rather than hydraulic
conditions.
The total abundance of oligochaetes was also independent
of hydraulic conditions but their diversity was
negatively related to the Froude number (Spearman
Rank Correlation, R = 0.47, p < 0.05) (Fig 2c). Many
oligochaete taxa occurred in pools of the studied river
section but only few were able to succeed and reach
high densities in habitats with Froude number higher
than 0.1.
Fig. 2. Scatter plots showing the relationships between a) the diversity and total abundance of the oligochaete and chironomid communities,
b) their taxa richness and total abundance, c) their diversity and Froude number. Only the communities with more than
50 individuals are displayed.
eschweizerbartxxx author
Chironomids and oligochaetes in a river 49
Main gradients in the combined data
The first four CA axes explained almost 48 % of the
variance in the faunal data and the sum of all eigenvalues
was 1.223 (Table 2, Fig. 3).
The sample scores on the first CA axis were correlated
most with the amount of POM (positively) and
with hydraulic parameters (negatively) such as the
inferred boundary Reynolds number, Froude number,
roughness shear velocity, current velocity and the current
velocity variability in different depths (Table 2).
Considering the community parameters, the first CA
axis correlated positively with the proportion of predators
and active filter-feeders and with the taxa richness
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Table 2. Eigenvalues of the CA axes and Spearman rank correlations between the CA axes and environmental and community
parameters. Only parameters that significantly correlated with at least one CA axis are included. Stars indicate the significance
of the correlations (*** – p < 0.001, ** – p < 0.01, * – p < 0.05). S – total taxa richness, S_chir – chironomid taxa richness, chir
diversity – chironomid diversity, N_chir – chironomid abundance, S_olig – oligochaete taxa richness, olig diversity – oligochaete
diversity, COL_S – the taxa richness of collectors/gatherers, GR_S – taxa richness of grazers/scrapers, GR_N – abundance of
grazers/scrapers, %GA – proportion of collectors/gatherers, %AF – proportion of active filter-feeders, %PF – proportion of passive
filter-feeders, %PR – proportion of predators, %GR_chir – proportion of grazers/scrapers within chironomids, %GA_chir – proportion
of collectors/gatherers within chironomids, %AF_chir – proportion of active filter-feeders within chironomids, %PF_chir –
proportion of passive filter-feeders within chironomids, %PR_chir – proportion of predators within chironomids. For abbreviations
of environmental variables see Table 1.
eschweizerbartxxx author
50 V. Syrovátka et al.
of collectors/gatherers, and negatively with the taxa
richness and abundance of grazers/scrapers (Table
2). This axis correlated also with the proportions of
collectors/gatherers (positively) and grazers/scrapers
(negatively), but only if calculated from chironomid
data alone (Table 2, Fig. 3).
The sample scores on the second CA axis were
positively correlated with the presence of aquatic vegetation
and weakly with the current velocity variability
in different depths. Of the community parameters, the
second CA axis correlated most with the taxa richness
and total abundance of chironomids (positively) (Table
2). These parameters separated habitats rich in chironomids
from poorer ones so that the vegetated riffles
and runs together with pools rich in POM appeared in
the upper part of the CA ordination diagram, while the
habitats with bare mineral substrate in the lower part
(Fig. 3). The second CA axis correlated also with the
proportion of the passive filter-feeders, and with the
abundance of grazers and weakly with the total taxa
richness (positively) and the proportion of the collectors/gatherers
(negatively) (Table 2, Fig. 3).
The sample scores on the third CA axis were negatively
correlated with the current velocity variability in
different depths and with the presence of aquatic vegetation.
These correlations were stronger than those
between the second CA axis and the same parameters
(Table 2). The third CA axis also weakly correlated
with the Froude number, current velocity in 0.8 depth,
water depth and the category of the mineral substrate
particle size (Table 2). Of the community parameters,
the third CA axis correlated with the abundance and
taxa richness of grazers and the proportion of the passive
filter-feeders (negatively) and the active filterfeeders
(positively) (Table 2).
It is difficult to interpret the directions of the second
and the third largest variability in the data using
the available parameters. Both the second and the third
CA axes were correlated with similar parameters and
most of these correlations were rather weak. Nevertheless,
it seems that the direction of the second largest
variability might be explained by the taxa richness and
abundance of chironomids, while the direction of the
third one by the presence of aquatic vegetation and the
associated variability in current velocity, though the
presence of aquatic vegetation influences also the taxa
richness and abundance of chironomids.
The fourth ordination axis weakly correlated only
with the particle size of the mineral substrate (Table
2).
Oligochaete community structure in relation
to environmental parameters
The CCA suggested that the amount of POM followed
by hydraulic parameters were the most significant parameters
explaining the highest portion of variability
within the oligochaete data. Using stepwise forward
selection the amount of POM, category of the mineral
substrate particle size, the substrate roughness and the
presence/absence of aquatic vegetation, explaining
21.36, 7.51, 6.35, and 5.2 % of the total variance in the
oligochaete data respectively, were selected as statistically
significant parameters influencing the oligochaete
community structure (Fig. 4).
Fig. 3. CA ordination diagram showing
the position of samples on the first and
second CA axes. The area of samples
reflects the total chironomid abundance
and the symbols’ grey tones indicate
Froude number. Proportions of chironomid
feeding strategies are displayed as
passive variables. (%AF proportion of
active filter-feeding, %GA collecting/
gathering, %GR grazing/scraping, %PF
passive filter-feeding, %PR predation,
ᮀ samples from habitats with aquatic
vegetation, ᭺ the other samples)
eschweizerbartxxx author
Chironomids and oligochaetes in a river 51
Oligochaete community types
Cluster analysis identified three types of oligochaete
communities (Fig. 5), though Stylodrilus sp. and N.
alpina comprised the majority (from 60 % to 98 %)
of the oligochaete community at almost all sampled
patches:
The first type included communities from pool
habitats with mineral substrate and from riffles with
aquatic mosses (10 patches). The communities of
these quite different habitats were grouped probably
because of their low diversity and total abundance
(Fig. 6). Only the most common taxa occurred at these
habitats. The communities were dominated by N. alpina
followed by Stylodrilus sp. or N. stolci that was
found in runs and riffles with vegetation only (Fig. 4).
Of the other taxa, Propappus volki was the only one
occurring within these communities in considerable
proportions. As all these taxa were common in other
samples as well, no indicator taxa were identified for
this community type.
The second type included communities from run
and riffle habitats with mineral substrate and usually
with aquatic vegetation (10 patches). The diversity
was similar to the previous type. The communities
were dominated by Stylodrilus sp. followed by N. alpina
and P. volki. The proportions of Stylodrilus sp.
and P. volki were higher than within the previous community
type and P. volki was identified as a good indicator
species (Table 3) (Fig. 4).
The third community type was characteristic of
pools (Fig. 6) with high amount of POM (7 patches)
and also living parts of terrestrial plants (grass leaves)
occurred at three patches. It had almost twice as high
taxa richness as both the previous types (Fig. 6). N.
alpina dominated followed by Stylodrilus sp., Aulodrilus
japonicus, Tubificidae with hairs, Specaria josinae
and Limnodrilus sp. occurred in considerably high
abundances and were identified as indicators of this
community type (Table 3) (Fig. 4).
Chironomid community structure in relation
to environmental parameters
Similarly to the oligochaetes, the CCA suggested that
the variability in the chironomid data was best explained
by the amount of POM followed by hydraulic
parameters. Using stepwise forward selection, the
amount of POM, the current velocity variability near
the bottom and the particle size of the mineral substrate,
explaining 23.72, 8.63 and 4.31 % of the total
variance respectively, were selected as statistically
Fig. 4. CCA ordination diagram
(the first and second axes) showing
the positions of oligochaete taxa in
relation to environmental variables
significantly influencing the oligochaete
community structure. Only
the taxa with species fit and species
weight > 10 % are displayed. Froude
number is displayed as a passive
variable. (mineral – the category of
mineral substrate grain size, POM
– the category of the amount of particulate
organic matter, roughness
– substrate roughness, VEG – the
occurrence of aquatic vegetation, Fr
– Froude number, ᮀ indicator taxa
of the second community type, ᭡ indicator
taxa of the third community
type, + other taxa).
Fig. 5. Dendrogram showing the clustering of oligochaete communities
into the three oligochaete community types.
eschweizerbartxxx author
52 V. Syrovátka et al.
Table 3. Indicator taxa of the oligochaete community types. Indicator value (Ind. value), p-value (p) and median abundance within
each community type are shown for each taxon. Values in grey refer to the habitat type of which the taxa are indicative.
Fig. 6. Box-plots of the diversity, total abundance, and Froude number of the three oligochaete and four chironomid community
types (square – median, box – quartiles, whiskers – ranges).
eschweizerbartxxx author
Chironomids and oligochaetes in a river 53
significant parameters influencing the structure of the
chironomid community (Fig. 7).
Chironomid community types
In general, the taxonomic composition of chironomid
communities was similar across all sampled patches.
Most taxa occurred in the majority of habitat types
but their proportions differed. Four different types of
chironomid communities were identified using cluster
analysis (Fig. 8). These community types may be
interpreted in terms of different hydraulic conditions
(Fig. 6).
The first community type occurred at three sampled
patches with minor current (Fig. 6) and high amount
of POM. The total chironomid abundance was high
(Fig. 6) and Microtendipes pedellus-Gr. dominated.
Further characteristics of this community type were
high relative abundances of Prodiamesa olivacea,
Thienemannimyia/Conchapelopia-Gr., Corynoneura
sp. and taxa from the Tanytarsini tribe (Micropsectra
sp., Tanytarsus sp., Tanytarsus brundini/curticornis
and Cladotanytarsus sp.), and the presence of different
taxa from the subfamily Tanypodinae (Ablabesmyia
sp., Apsectrotanypus trifascipennis, Natarsia
sp. and Zavrelimyia sp.). In contrast to the other community
types, relative abundances of Synorthocladius
semivirens and Orthocladius species were low. Ten
good indicators of this group were identified (Table
4) (Fig. 7).
The second community type (9 patches) occurred
at habitats with low current (Fig. 6) and mineral substrate
sometimes covered with fine particulate organic
matter (FPOM). It was characterized by the dominance
of S. semivirens and high relative abundances
of Orthocladius cf. obumbratus and Orthocladius
cf. rubicundus. M. pedellus-Gr., Thienemannimyia/
Conchapelopia-Gr., Corynoneura sp. and taxa from
the Tanytarsini tribe (Tanytarsus sp., T. brundini/curticornis,
Micropsectra sp. and Cladotanytarsus sp.)
were again the most abundant taxa. If compared to the
first community type, the same taxa from the Tanypodinae
subfamily were present although in lower densities.
Most of the taxa were common in other community
types. S. semivirens was identified as a single
indicator with low indicator value (Table 4) (Fig. 7).
The third community type occurred in runs and
riffles (Fig. 6) with mineral substrate sometimes with
aquatic mosses (8 patches). The lowest total chironomid
abundances were observed (Fig. 6). O. cf. obumbratus,
S. semivirens and O. cf. rubicundus were the
most dominant taxa, together accounting for 50 – 80 %
of the entire community. No Tanypodinae taxa were
present except for Thienemannimyia/ConchapelopiaGr.,
and practically no individuals of M. pedellus-Gr.
Similarly, the relative abundances of Corynoneura sp.
and the Tanytarsini taxa were lower. On the contrary,
the proportions of Orthocladius rivicola-Gr., Eukiefferiella
and Tvetenia species and Rheotanytarsus sp.
were higher than in the previous community types.
One good and two weak indicators were identified
(Table 4) (Fig. 7).
The last community type was characteristic of
runs and riffles (Fig. 6), often with aquatic vegetation.
Similarly to the first community type, high total chironomid
abundances were observed (Fig. 6). Rheotanytarsus
sp. and both Tvetenia species dominated at the
expense of O. cf. obumbratus, O. cf. rubicundus and
Fig. 7. CCA ordination diagram (the
first and the second axes) showing the
positions of chironomid taxa in relation
to environmental variables significantly
influencing the chironomid
community structure. Only the taxa
with species fit and species weight
> 10 % are displayed. Froude number
is displayed as a passive variable.
(mineral – the category of mineral substrate
grain size, POM – the category
of the amount of particulate organic
matter, SDvel2 cm – the current velocity
variability 2 cm above the bottom.
Fr – Froude number, ᭿ indicator taxa
of the first community type, ᭺ indicator
taxa of the second community type,
᭡ indicator taxa of the third community
type, ᮀ indicator taxa of the fourth
community type, + other taxa)
eschweizerbartxxx author
54 V. Syrovátka et al.
S. semivirens, whose proportions decreased. Conversely,
the proportions of Eukiefferiella species and Potthastia
longimana increased to their observed maximum.
The proportions of Corynoneura sp. and the
Tanytarsini taxa were similar to those observed in the
previous community type. Seven good indicators were
identified (Table 4) (Fig. 7).
Hydraulic preferences of selected taxa
Hydraulic preferences of 6 oligochaete and 23 chironomid
taxa were assessed (Fig. 9). The taxa showed different
preferences for hydraulic conditions expressed
as the Froude number. Generally, it was possible to
identify i) taxa occurring only in pools with very low
Froude number, ii) taxa occurring only in riffles and
runs, and iii) taxa occupying most of (or all) the samTable
4. Indicator taxa of the chironomid community types. Indicator value (Ind. value), p-value (p) and median abundance within
each community type are shown for each taxon. Values in gray refer to the habitat type of which the taxa are indicative.
Fig. 8. Dendrogram showing the clustering of chironomid communities
into the four chironomid community types.
eschweizerbartxxx author
Chironomids and oligochaetes in a river 55
pled habitats and having low or no preferences for hydraulic
conditions.
Among the oligochaetes, three taxa preferred narrow
ranges of Froude number: A. japonicus and Tubificidae
with hairs occurred only in pools with very low
Froude number, while N. stolci preferred runs (Fig. 9).
The other three oligochaete taxa did not show such
strong preferences: N. alpina was almost evenly distributed
across all the sampled patches, Stylodrilus sp.
slightly preferred runs and riffles and only P. volki occurred
almost exclusively in runs and riffles (Fig. 9).
Among the chironomids, only M. pedellus Gr. and
P. olivacea showed strong preferences for particular
hydraulic conditions. They occurred only in pools
with low Froude number (Fig. 9). Some taxa showed
rather strong preferences for riffles (Tvetenia bavarica/
calvescens, T. discoloripes/verralli, Eukiefferiella devonica/ilkleyensis,
Polypedilum laetum-Gr. and Rheotanytarsus
sp.) or runs and riffles (O. rivicola-Gr., E.
lobifera, Cricotopus bicinctus-Gr. and P. longimana)
(Fig. 9). The other chironomid taxa occurred more or
less across the whole range of the available hydraulic
conditions and usually showed weak preferences
for pools or runs: e.g. taxa from the Tanytarsini tribe
except for Rheotanytarsus sp. (Cladotanytarsus sp.,
Micropsectra sp. and both the Tanytarsus sp. and T.
brundini/curticornis) preferred pools, but occurred
also in runs and riffles (Fig. 9).
Discussion
The importance of hydraulic conditions
The major influence of hydraulic conditions on the
structure of benthic macroinvertebrate communities
has already been reported (e.g. Orth & Maughan
1983, Jowett et al. 1991, Lancaster & Hildrew 1993,
Quinn & Hickey 1994, Benbow et al. 1997, Mérigoux
& Dolédec 2004). Also in this study, hydraulic
conditions, inversely related to the amount of sedimented
POM, best explained the main gradient in the
combined data, along which both the taxonomic and
functional structure of the communities changed. Surprisingly,
of the measured and calculated hydraulic
Fig. 9. Hydraulic preferences of frequent taxa. Medians (circles), lower and upper quartiles (thick lines) and 10 % and 90 % quantiles
(thin lines) of Froude number are weighted by the abundances of taxa. The area of the circles reflects the total abundance of
particular taxa. Tick marks pointing upwards indicate the position of the samples on the gradient of the Froude number. Pool, run
and riffle habitats are identified according to Froude number (Jowett 1993).
eschweizerbartxxx author
56 V. Syrovátka et al.
variables, current velocity in 0.8 depth (from bottom)
was the best explanatory variable of this gradient, although
it was closely followed by the inferred boundary
Reynolds number, current velocity in 0.2 and 0.4
depth, Froude number and roughness shear velocity.
The substitutability of the simple current velocity for
complex hydraulic variables might be caused by a relatively
low heterogeneity in water depth and substrate
roughness (Quinn & Hickey 1994, Brooks et al. 2005)
in the Svratka River.
It is also surprising that the amount of sedimented
POM, estimated from underwater video sequences
and classified into only four categories, was identified
as a more important variable, explaining the
structure of both separate oligochaete and chironomid
communities better than the measured and calculated
hydraulic variables. Nevertheless, already Rabeni &
Minshall (1977) demonstrated the influence of POM
on the structure of macroinvertebrate community, and
the spatial distribution of chironomid larvae in gravels
of the River Pank was also most correlated with
fine detritus (Ruse 1994). In this study, the amount of
POM explained about 21 and 24 % while the hydraulic
variables about 14 and 20 % of the variance in the
oligochaete and chironomid data respectively. In the
case of oligochaetes, the samples seemed to be divided
into organically rich with many oligochaete taxa and
poor containing only few common taxa. Within the
organically poor samples the substrate roughness and
the occurrence of aquatic vegetation played the major
role and hydraulic conditions were less important. In
the case of chironomids the amount of POM seemed
to be replaceable by some hydraulic variables and the
community structure changed more gradually along
the gradient of the amount of sedimented POM (hydraulic
conditions).
Potential influence of substrate
characteristics
A part of the variability within the data could be explained
by some substrate characteristics. In the case
of oligochaetes, the substrate characteristics might
have represented the thickness of the colonisable substrate
layer (Stanford & Ward 1988). It is quite curious
that both the substrate particle size and substrate
roughness were chosen by the CCA, which indicates
that these two variables probably expressed different
substrate qualities.
In the case of combined data, the second largest
variability could be best explained by chironomid
taxa richness and abundance that seemed to reflect the
quantity of available food and space resources across
the whole range of hydraulic conditions. The quantity
of available food and space resources could be probably
interpreted in terms of different substrate characteristics.
In this respect, aquatic vegetation in runs and
riffles and large quantities of sedimented POM in pools
provided the most favourable conditions. Aquatic vegetation
highly enlarges the substrate surface and may
also alter near-bed hydraulic conditions and promote
sedimentation of fine particles (Glime & Clemons
1972, Sand-Jensen & Mebus 1996). Higher abundance
and taxa richness of chironomids at vegetated habitats
was reported earlier e.g. by Wright et al. (1983), Nolte
(1989) and Schmid (1993). On the other hand, pools
rich in POM offer plenty of food to collecting/gathering
and active filter-feeding taxa with low oxygen demands
and are likely to satisfy food demands of large
numbers of individuals (e.g. Culp et al. 1983).
Functional feeding strategies
As well as the taxonomic structure, also the functional
structure of macroinvertebrate communities changes
and reflects the spatial variability within a stream
(Poff & Ward 1990, Scarsbrook & Townsend 1993,
Townsend & Hildrew 1994, Resh et al. 1994, Wohl et
al. 1995, Lamouroux et al. 2004). The taxa richness
of collectors/gatherers and grazers/scrapers changed
along the main CA axis. Negative association of collectors/gatherers
with hydraulic variables was recently
reported e.g. by Quinn & Hickey (1994), Rempel et al.
(2000), Doisy & Rabeni (2001) or Mérigoux & Dolédec
(2004). Lower current velocities enable sedimentation
of fine organic particles and therefore support collectors/gatherers.
On the other hand, higher velocities
benefit periphyton in nutrient-poor streams (Horner et
al. 1990) and therefore support grazers/scrapers – the
consumers of periphytic algae.
The taxa richness of collectors/gatherers and grazers/scrapers
changed along the gradient of hydraulic
conditions, and therefore similar changes in the proportions
of collectors/gatherers and grazers/scrapers
were expected. Nevertheless, the proportions of these
feeding strategies significantly correlated with the first
CA axis only if calculated from chironomid data alone.
This was the case because the two most abundant oligochaete
collectors/gatherers (Stylodrilus spp. juv.
and P. volki) preferred riffles and runs, while the most
abundant oligochaete species, a partial grazer/scraper
N. alpina did not show any preference for particular
hydraulic conditions. In this respect it seemed that the
proportions of functional feeding groups within the oli-
eschweizerbartxxx author
Chironomids and oligochaetes in a river 57
gochaete community did not follow the gradient of hydraulic
conditions as was observed in the chironomid
community (with two exceptions of uncommon predators,
all the oligochaete taxa were classified either as
pure collectors/gatherers or partial collectors/gatherers
and partial grazers/scrapers). This can probably be explained
by different behaviour of oligochaetes versus
chironomids. Oligochaetes usually exploit interstitial
spaces hidden from the rough hydraulic conditions
(Usseglio-Polatera et al. 2000), while tube-building
chironomids can stand quite rough hydraulic conditions
in the upper layer of the substrate, where the food
resources are influenced most by hydraulic conditions.
Similarly to the course of collecting/gathering strategy
within chironomid community, also the proportions
of active filter-feeders and predators decreased
along with the increasing hydraulic stress. Active
filter-feeders feed on sedimented POM and therefore
are favoured at habitats with high sedimentation rates.
Predators in pools can probably move about on the
substrate without the danger of being swept away by
the current. In contrast, Doisy & Rabeni (2001) found
no relationship between hydraulic variables and the
proportion of predators, while in the study of Rempel
et al. (2000) predators were even positively associated
with Reynolds number. This disagreement was probably
caused by different fractions of the macroinvertebrate
communities that were analyzed (only a part
of the macroinvertebrate community, e.g. without
predatory stoneflies, was analyzed in this study) and
by different identification levels (chironomids were
identified at the family and subfamily level in Doisy &
Rabeni (2001) and Rempel et al. (2000) respectively).
It is also possible that the proportion of predators differ
in different rivers.
The proportion of passive filter-feeders, attributable
only to a chironomid Rheotanytarsus sp., was possibly
influenced by the occurrence of aquatic vegetation. It
can be explained by the benefit of passive filter-feeders
from the unimpeded velocities and turbulence transmitted
through the open plant stands (Wallace 1980,
Iversen et al. 1985, Sand-Jensen & Pedersen 1999).
This hypothesis is supported by Schmid (1993), who
found Rheotanytarsus nigricauda Fittkau, 1960 in
distinctly higher densities in the epilithic moss Fontinalis
antipyretica than in the neighbouring mineral
substrate.
Notes on the ecology of frequent taxa
The oligochaete taxa richness patterns confirmed the
general preference of most oligochaete taxa for hydraulically
smooth conditions promoting creation
of patches rich in sedimented POM (Schmedtje &
Colling 1996). Nevertheless, the most abundant oligochaete
Stylodrilus sp., accounting for 40 % of the
whole oligochaete community, preferred runs and riffles
where it dominated. P. volki even indicated runs
and riffles. Both these taxa were able to succeed in hydraulically
rough conditions because of their adaptation
to living in floating sands and gravel bars: P. volki
is able to exploit interstitial spaces in the substrate and
it can attach itself to the substrate surface by adhesive
substance (Bird 1982, Petto & Humpesch 1992). Stylodrilus
sp. can form relatively firm mucous tubes into
which it hides during disturbances (Mrázek 1926).
N. stolci preferred runs too and was strongly associated
with aquatic vegetation though it is referred to
be a typical species of stony substrates (Learner et al.
1978, Verdonschot 1999). In contrast, N. alpina could
be considered a very adaptive species since it occurred
in all samples and dominated in most of them. Chironomids
S. semivirens, O. cf. rubicundus and O. cf.
obumbratus showed similar plasticity. All these taxa
are classified as partial collectors/gatherers and partial
grazers/scrapers (AQEM consortium 2002) and feeding
on both the FPOM and algae probably enables them
to succeed in wide range of hydraulic conditions.
Unlike the oligochaetes, habitat preferences of
most chironomids reflected their feeding behaviour.
Collectors/gatherers and active filter-feeders (primarily
taxa from the Chironomini tribe) preferred pools,
while grazers/scrapers (Tvetenia and Eukiefferiella
species) and the passive filter-feeder Rheotanytarsus
sp. preferred riffles and runs.
Conclusions
Even though a limited number of samples were analyzed,
large spatial variability in the taxonomic and
the functional structure of the investigated communities
was observed and it was further possible to relate
this variability to environmental variables. The sampling
design was set up to reduce the temporal and
large-scale spatial variation. The results of this study
are therefore associated with the studied river section
and the sampling season, but nevertheless contribute
to the knowledge of lotic macroinvertebrates spatial
distribution patterns. Although further work is needed
to understand the spatial variability in the macroinvertebrate
communities and the hydraulic preferences of
particular taxa at more general level, it was shown that
the investigated communities clearly reflected environ-
eschweizerbartxxx author
58 V. Syrovátka et al.
mental conditions. This indicates that any alteration of
physical habitat induced for example by human activities
or global changes (see Pedersen 2009 in this issue)
might influence both the taxonomic and the functional
structure of the macroinvertebrate communities in
whole river segments.
Acknowledgements
We are indebted to Marcela Růžičková and Petr Pařil for their
assistance in the field work and to Lenka Tajmrová for language
corrections. Thanks also to two anonymous reviewers for valuable
comments on the manuscript. This study was supported by
the grant from the Ministry of Education of the Czech Republic
(MSM 0021622416), grant from the Czech Science Foundation
(GA CR 524/05/H536) and by international projects Euro-limpacs
(GOCE-CT-2003-505540) and STAR (EVK1-CT
2001-00089).
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Chironomids and oligochaetes in a river 61
Appendix 1. Abundances and frequencies of taxa (in all samples / in the subset of 19 samples used for the analysis of hydraulic
preferences of selected taxa) and their classification to feeding groups (col – collectors/gatherers, col/gr – partial collectors/gatherers
and partial grazers/scrapers, gr – grazers/scrapers, other – others.
Abbrev. Taxon Abundances Frequenices Trophic
group
OLIGOCHAETA
NAIDIDAE
chaediap Chaetogaster diaphanus (Gruithuisen, 1828) 3 3 other
chaedias Chaetogaster diastrophus (Gruithuisen, 1828) 1 1 other
naisalpi Nais alpina Sperber, 1948 2,305/1,621 27/19 col/gr
naisbret Nais bretscheri Michaelsen, 1899 4 3 col/gr
naiscomm Nais communis Piguet, 1906 27 9 col/gr
naiselin Nais elinguis O. F. Műller, 1773 3 2 col/gr
naispard Nais pardalis Piguet, 1906 27 2 col/gr
naispseu Nais pseudoobtusa Piguet, 1906 2 2 col/gr
naisstol Nais stolci Hrabě, 1981 308/302 12/10 col/gr
ophiserp Ophidonais serpentina (O. F. Műller, 1773) 1 1 col
prisrose Pristina rosea (Piguet, 1906) 10 3 col
prisaequ Pristina aequiseta Bourne, 1891 12 6 col
prisbilo Pristina bilobata (Bretscher, 1903) 5 3 col
slavappe Slavina appendiculata (D’udekem, 1855) 10 5 col
specjosi Specaria josinae (Vejdovský, 1883) 72 9 col
styllacu Stylaria lacustris (Linnaeus, 1767) 13 4 col/gr
TUBIFICIDAE
aulojapo Aulodrilus japonicus Yamaguchi, 1953 177/156 9/5 col
auloplur Aulodrilus pluriseta (Piguet, 1906) 1 1 col
limnodsp Limnodrilus spp. juv. 78 7 col
rhyachair Rhyacodrilinae juv. with hair chaete 6 3 col
spirferx Spirosperma ferox (Eisen, 1879) 1 1 col
tubiigno Tubifex ignotus (Štolc, 1886) 2 2 col
tubihair Tubificidae with hairs juv. 163/131 7/4 col
PROPAPPIDAE
propvolk Propappus volki Michaelsen, 1916 484/408 23/17 col
HAPLOTAXIDAE
haplgord Haplotaxis gordioides (Hartmann, 1821) 5 5 col
ENCHYTRAEIDAE
achasp. Achaeta sp. 1 1 col
cognglan Cognettia glandulosa (Michaelsen, 1888) 1 1 col
cognsp. Cognettia sp. 3 1 col
enchsp. Enchytraeus sp. 1 1 col
fridsp. Fridericia sp. 1 1 col
LUMBRICIDAE
eisetetr Eiseniella tetraedra (Savigny, 1826) 5 4 col
luicussp Lumbricus sp. 1 1 col
LUMBRICULIDAE
lumbvari Lumbriculus variegatus O. F. Műller, 1774 1 1 col
stylbrac Stylodrilus brachystylus Hrabě, 1929 2 2 col
stylodsp Stylodrilus spp. juv. 2,539/2,117 27/19 col
CHIRONOMIDAE
TANYPODINAE
ablabesp Ablabesmyia sp. 6 4 other
apsetrif Apsectrotanypus trifascipennis (Zetterstedt, 1838) 25 8 other
natasp. Natarsia sp. 4 4 other
nilodubi Nilotanypus dubius (Meigen, 1804) 24 12 other
thiegrge Thienemannimyia/Conchapelopia - Gr. 495/312 25/17 other
zavyiasp Zavrelimyia sp. 5 5 other
eschweizerbartxxx author
62 V. Syrovátka et al.
Appendix 1. Continued.
Abbrev. Taxon Abundances Frequencies Trophic
group
DIAMESINAE
pottgaed Potthastia gaedii (Meigen, 1838) 1 1 col/gr
pottlong Potthastia longimana (Kieffer, 1922) 57/55 14/12 col/gr
PRODIAMESINAE
prodoliv Prodiamesa olivacea (Meigen, 1818) 147/142 4/3 col
ORTHOCLADIINAE
brilmode Brillia bifida (Kieffer, 1909) 31 11 col
brilflav Brillia flavifrons Johannsen, 1905 12 3 col
corysp. Corynoneura sp. 408/271 26/19 gr
cricannu Cricotopus annulator Goetghebuer, 1927 7 5 gr
cricbici Cricotopus bicinctus (Meigen, 1818) 8 7 col/gr
cricbigr Cricotopus bicinctus-Gr. 68/57 16/13 col/gr
crictrgr Cricotopus tremulus-Gr. 32 12 gr
critriia Cricotopus trifascia Edwards, 1929 5 3 col/gr
diplcult Diplocladius cultriger Kieffer in Kieffer & Thienemann, 1908 1 1 col
eukibrev Eukiefferiella brevicalcar (Kieffer, 1911) 30 11 gr
eukicoer Eukiefferiella coerulescens (Kieffer in Zavrel, 1926) 22 13 gr
eukideil Eukiefferiella devonica/ilkleyensis 94/91 13/10 gr
eukigrgr Eukiefferiella gracei-Gr. 2 1 gr
eukilobi Eukiefferiella lobifera Goetghebuer, 1934 69/55 19/14 gr
eukimino Eukiefferiella minor (Edwards, 1929) 3 2 gr
eukisimi Eukiefferiella similis Goetghebuer, 1939 1 1 gr
hetemarc Heterotrissocladius marcidus (Walker, 1856) 3 2 col
nanoreag Nanocladius rectinervis-Agg. 202/168 21/15 col
orthrigr Orthocladius rivicola-Gr. 124/116 15/11 gr
orthrubi Orthocladius cf. rubicundus (Meigen, 1818) 695/530 24/16 col/gr
orthfrig Orthocladius frigidus (Zetterstedt, 1838) 4 3 gr
orthobum Orthocladius cf. obumbratus Johannsen, 1905 1,167/903 27/19 col/gr
orththie Orthocladius thienemanni Kieffer in Kieffer & Thienemann, 1906 13 9 gr
paracrsp Paracricotopus sp. 2 2 col
parastyl Parametriocnemus stylatus (Kieffer, 1924) 9 6 gr
pararufi Paratrichocladius rufiventris (Meigen, 1830) 16 9 col/gr
rheofusc Rheocricotopus fuscipes (Kieffer, 1909) 199/162 23/16 col/gr
synosemi Synorthocladius semivirens (Kieffer, 1909) 1,575/809 27/19 col/gr
thellasp Thienemanniella sp. 266/178 24/16 col/gr
tvetbaca Tvetenia bavarica/calvescens 632/606 22/15 gr
tvetdive Tvetenia discoloripes/verralli 480/461 22/17 gr
CHIRONOMINAE-Tribus Chironomini
cromussp Cryptochironomus sp. 56 9 other
demisp. Demicryptochironomus sp. 1 1 col
micrchgr Microtendipes pedellus-Gr. 836/503 14/7 col
paraalgr Paratendipes albimanus-Gr. 3 2 col
phaepssp Phaenopsectra sp. 6 2 col/gr
polyconv Polypedilum convictum (Walker, 1856) 17 5 col
polylagr Polypedilum laetum-Gr. 299/283 18/13 col
polyscgr Polypedilum scalaenum-Gr. 75 10 col
xenoxeno Xenochironomus xenolabis (Kieffer in Thienemann & Kieffer, 1916) 1 1 other
CHIRONOMINAE-Tribus Tanytarsini
cladotsp Cladotanytarsus sp. 214/105 17/11 col
mictrasp Micropsectra sp. 455/383 26/18 col
paratasp Paratanytarsus sp. 4 2 col/gr
rheotasp Rheotanytarsus sp. 897/874 23/15 other
stembrgr Stempellinella brevis-Gr. 3 3 col
tanybrun Tanytarsus brundini/curticornis 201/130 24/16 col/gr
tanytasp Tanytarsus sp. 260/162 24/17 col
93
Schenková, J., P. Pařil, K. Petřivalská & J. Bojková, 2010
Aquatic oligochaetes (Annelida: Clitellata) of the Czech Republic: check-list, new records,
and ecological remarks. Zootaxa, 2676, 29–44.
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ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN 1175-5334 (online edition)Copyright © 2010 · Magnolia Press
Zootaxa 2676: 29–44 (2010)
www.mapress.com/zootaxa/ Article
Aquatic oligochaetes (Annelida: Clitellata) of the Czech Republic:
check-list, new records, and ecological remarks
JANA SCHENKOVÁ1
, PETR PAŘIL2
, KARLA PETŘIVALSKÁ3
& JINDŘIŠKA BOJKOVÁ4
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic.
E-mail: 1
schenk@sci.muni.cz; 2
paril@sci.muni.cz; 3
karlap@sci.muni.cz; 4
bojkova@centrum.cz
Abstract
This study contributes to the knowledge of central European clitellates by creating a check-list of Oligochaeta (sensu
oligochaetous Clitellata; Erséus 2005) of the Czech Republic, exclusive of taxa in the family Enchytraeidae. In total, 95
aquatic oligochaete species representing 43 genera are reported for the Czech Republic. Rare species are highlighted and
associated with the categories for threatened species as outlined by the International Union for the Conservation of
Nature. The first records of Trichodrilus strandi Hrabě, 1936, Pristina jenkinae (Stephenson, 1931), Pristina osborni
(Walton, 1906), Rhyacodrilus subterraneus Hrabě, 1963, Aulodrilus limnobius Bretscher, 1899, and Aulodrilus pigueti
Kowalewski, 1914 in the Czech Republic are presented. Their ecology, morphology, and distribution are discussed.
Key words: Oligochaeta, Trichodrilus strandi, Pristina jenkinae, Pristina osborni, Rhyacodrilus subterraneus,
Aulodrilus limnobius, Aulodrilus pigueti, habitat preferences, first records, red list, alien species
Introduction
Aquatic Oligochaeta (sensu oligochaetous Clitellata; Erséus 2005), are typical inhabitants of bottom
sediments, forming communities whose species composition is a relevant information source for water quality
assessment (Brinkhurst & Cook 1974; Chapman 2001; Verdonschot 2006). Hence, reliable species
identification and a complete knowledge of their ecology are essential. Since the turn of the 20th
century many
phylogenetic changes and taxonomic shifts in Oligochaeta have been made. Therefore, the monographs
published by renowned Czech oligochaetologists in the 20th
century have become insufficient for valid
identification. The list of oligochaete species of the Czech Republic is scattered among old monographs,
mostly written in Czech, and recent papers that have documented distributional records for particular species.
Furthermore, the territory of the present Czech Republic was previously a part of several different countries,
so its records of oligochaete fauna formed a subset of data published on larger territories.
Taxonomic surveys on aquatic oligochaetes have a long tradition in the Czech Republic. Many worldfamous
taxonomists, whose names have been assigned by patronymy to oligochaete species and genera, came
from the Czech territory. At the end of the 19th
century, when the Czech Republic was a part of AustriaHungary,
František Vejdovský (1849–1939) and Antonín Štolc (1863–1917) published numerous works
dealing with the classifications and morphology of Oligochaeta (e.g. Vejdovský 1876, 1883, 1884, 1892; Štolc
1886, 1888). At the beginning of the 20th
century, Alois Mrázek (1868–1923) and Lev Černosvitov (1902–
1946, born in Russia) continued their works with studies on anatomy and reproduction (e.g. Mrázek 1913a,
1913b), and morphology and faunistics (e.g. Černosvitov 1928, 1930, 1935). Fundamental research on this
group was made by Sergěj Hrabě (1899–1984), who was born in Russia where he lived with his Czech parents
until the October Revolution. After the revolution, during the civil war and under difficult circumstances, he
moved back to what was then Czechoslovakia. He published an admirable volume of almost 100 scientific
papers and monographs, in which he (and other authors), among others, described 11 new species to science
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from Czechoslovakia and 15 genera new for science and 77 new species of oligochaeta from other countries.
Both fundamental monographs by Hrabě (1954, 1981) still serve as the list of Czech oligochaetes and remain
the major source of information on the morphology of many species. These works were published prior to
1992, when the former Czechoslovakia was split into the Czech Republic and Slovakia, and therefore include
species from both countries irrespective of the new political boundaries. This list was supplemented by
species documented by Eva Lišková (1964, 1976), and more recently by species documented in faunistic
studies (e.g. Wohlgemuth & Schenková 1999) and ecological studies (e.g. Uzunov et al. 1988; Schenková et
al. 2001a, 2001b; Schenková 2005; Schenková & Kroča 2007). Aquatic and semiaquatic species of the family
Lumbricidae were treated in the monograph by Pižl (2002), which dealt with predominantly terrestrial
species. Up to now, aquatic species of the family Enchytraeidae have been investigated insufficiently (cf.
Hrabě 1954) or even omitted (cf. Hrabě 1981). Extensive studies focusing on the terrestrial and semiaquatic
Enchytraeidae occurring in terrestrial habitats were published by Chalupský (1988, 1991, 1994). New records
for the Czech Republic were recently reported by Jiří Schlaghamerský (e.g. Schlaghamerský 2007;
Schlaghamerský & Kobetičová 2005, 2006; Šídová & Schlaghamerský 2007; Schlaghamerský & Pižl 2009).
With respect to taxonomic development, the distribution of the family Enchytraeidae in the Czech Republic
needs detailed investigation of both freshwater and terrestrial habitats, and a revision of the published
historical data.
The objectives of this study are (i) to summarise and update the check-list of aquatic oligochaete species
for the Czech Republic, (ii) to evaluate the frequency of all species occurrences in the Czech Republic and
update the Red list and (iii) to discuss new records with extended information on their distribution, preferred
habitats, ecological requirements, and morphological characteristics. Six oligochaete species reported herein
as new for the Czech Republic—Trichodrilus strandi (Lumbriculidae), Pristina jenkinae and Pristina osborni
(Naididae: Pristininae), Rhyacodrilus subterraneus (Naididae: Rhyacodrilinae), and Aulodrilus limnobius and
Aulodrilus pigueti (Naididae: Tubificinae)—were studied in detail.
Material and methods
The check-list of aquatic oligochaetes (exclusive of taxa in the family Enchytraeidae) was compiled from
published records (Hrabě 1954, 1981; Schenková 2005; Schenková & Kroča 2007; Pižl 2002) and from
unpublished material determined and/or revised by the authors. Semiaquatic species of the family
Lumbricidae were selected based on the data published in the monograph by Pižl (2002), after personal
communication with the author. Nomenclature for species discussed in this paper follows Erséus et al. (2008)
and a synonymy of species (according to Timm 2009) is presented for the six species reported as new records
for the Czech Republic.
Each species discussed herein was given a category for its frequency of occurrence in the Czech Republic
based upon published data and unpublished records. The unpublished records were compiled from those
discussed in running water quality assessments and other projects in which the authors have participated since
1996. This dataset includes approximately 1300 sites across the whole of the Czech Republic. Species were
sorted into four categories: F1—scarce (up to 10 sites), F2—medium frequent (10–100 sites), F3—very
frequent (more than 100 sites) and A—absent (i.e., not recorded from the Czech Republic since 1996). For
scarce or rare species, a category of threat in the Czech Republic according to the International Union for
Conservation of Nature 1994 was recommended. As we applied the IUCN criteria at national level, we used
guidelines prepared by the IUCN/SSC Regional Applications Working Group (Gärdenfors et al. 2001, IUCN
2003, Miller et al. 2007). A national and regional category for a particular species may not be the same as its
global category, because at global level the whole range of a species is evaluated.
Because many oligochaete species dwell in different freshwater habitats, they were sampled by various
methods. The conservation and processing of samples and species identification were the same.
Trichodrilus strandi was collected quantitatively using a metal frame of 25 × 25 cm2
in spring fen habitats.
Vegetation and upper bottom layer were gathered to the depth of 5 cm and this substrate was elutriated
through a 250 μm mesh net.
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Zootaxa 2676 © 2010 Magnolia Press · 31CHECK-LIST OF OLIGOCHAETES OF THE CZECH REPUBLIC
Pristina jenkinae, Rhyacodrilus subterraneus, and Aulodrilus limnobius were collected in reaches of the
river (20–100 m in length) using a three-minute kick-sampling of all visually distinguishable habitats, which
were sampled proportionally to their occurrences in the reach of the river using a hand net (25 × 25 cm2
, mesh
size 500 μm) (Kokeš et al. 2006).
Aulodrilus pigueti was collected using the same type of hand net (25 × 25 cm2
, mesh size 500 μm) in the
bottom substrate of a fishpond and in submerged littoral vegetation.
Pristina osborni was collected in a large river from a depth up to 3 m using an “air lift” vacuum sampler
designed for sampling in large, fast-flowing rivers (Pehofer 1998) and the grab “van Veen” (Lie & Pamatmat
1965). The samples were elutriated through the 250 μm mesh net.
Samples obtained by all these methods were fixed by 4% formaldehyde in the field and then sorted under
a stereomicroscope in the laboratory. Oligochaetes were picked up, permanently mounted in Canada balsam
and identified under a light microscope using the keys by Hrabě (1954, 1981), Timm & Veldhijzen van Zanten
(2002) and Timm (2009).
New records of selected species included the following information associated with specimens: name of
the water body, name of the settlement (town, village, city), closest site from which the specimen(s) was/were
collected, latitude and longitude coordinates for the collecting site, name(s) of the person(s) who collected
and/or identified the species and date of collection. Abbreviations for the names of collectors and persons who
identified the species are presented below: IS—Ivan Skála, JB—Jindřiška Bojková, JK—Jiří Kokeš, JSc—
Jana Schenková, JSy—Jan Sychra, JZ—Jiří Zahrádka, KB—Karel Brabec, KP—Karla Petřivalská, LO—
Libuše Opatřilová, PH—Pavel Horák, PP—Petr Pařil. Data on habitat characteristics - abiotic and chemical
parameters, water saprobity (Kolkwitz & Marsson 1909), ecology, morphology (if new or untypical features
were recorded) and distribution of species are noted.
Results and discussion
The check-list of 95 aquatic/semiaquatic oligochaete species for the Czech Republic comprises the families
Lumbriculidae (12 species), Naididae sensu Erséus et al. (2008) (a total of 72 species)—which includes the
Naidinae (36 species), Pristininae (eight species), Tubificinae (22 species), and Rhyacodrilinae (six species),
Propappidae (one species), Criodrilidae (one species), Haplotaxidae (one species) and Lumbricidae (8
species) (Table 1).
The majority of the evaluated species (44) were moderately or widely distributed (F2 and F3) in the Czech
Republic. They are mostly ubiquitous and euryecious species (e.g., several species of Tubificinae inhabiting
running and stagnant waters) and many species can tolerate high organic matter content and pollution. There
were also two species, Potamothrix moldaviensis Vejdovský et Mrázek, 1903 and Potamothrix bavaricus
(Oschman, 1913) (both in the subfamily Tubificinae), that are considered alien species in Europe (Drake
2009). However, their non-indigenous status in central Europe is questionable because they were recorded
historically from areas within the border of today's Czech Republic. P. moldaviensis has previously been
described in the Vltava (Moldau) River (the Elbe basin) in the beginning of 20th
century and P. bavaricus was
recorded in the Elbe basin in the 1930s (Hrabě 1939). Both species recently occur in moderately polluted
rivers—P. moldaviensis prefers larger rivers, while P. bavaricus prefers smaller streams.
Thirty-eight species were considered rare (F1). Some of these species are not necessarily endangered,
since they can be locally abundant in either restricted areas or particular habitats. For instance, Stylodrilus
lemani (Grube, 1879) is abundant in a few eutrophic streams in southern Moravia (located in the south-eastern
part of the Czech Republic) and Haemonais waldovogeli Bretscher, 1900 is dominant in the bottom fauna of
small fishponds in the Czech-Moravian Highland Mountains. By contrast, one species, Branchiura sowerbyi
Beddard, 1892, is a non-indigenous thermophilic species which has been spreading throughout Europe, most
likely via water transport (Lišková 1964; Gruszka 1999). However, its invasion is very slow because of a lack
of suitable habitats (warmer waters). We have documented four records of B. sowerbyi since 1964, when it
was found (Lišková 1964) for the first time in Czechoslovakia. Two other species, Psammoryctides moravicus
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(Hrabě, 1934) and Paranais frici Hrabě, 1941—both considered aliens of Ponto-Caspian origin in Europe
(Drake 2009)—were recently found sporadically in the Labe and Morava Rivers that serve as immigration
gateways into Czech waters.
TABLE 1. Aquatic Oligochaeta of the Czech Republic. Lumbriculidae, Naididae (Naidinae, Pristininae, Rhyacodrilinae,
Tubificinae), Propappidae, Haplotaxidae, Criodrilidae, and Lumbricidae. Frequency of occurrence since 1996: F1—
scarce (up to 10 sites), F2—medium frequent (10–100 sites), F3—very frequent (more than 100 sites) and A—absent.
Lumbricidae, affinity to wet habitats and frequency of occurrence refers to Pižl (2002, and personal communication).
Taxon Author Reference Frequency
Lumbriculidae
Lamprodrilus mrazeki Hrabě, 1929 Hrabě 1954, 1981 A
Lumbriculus variegatus (Müller, 1774) Hrabě 1954, 1981 F3
Rhynchelmis limosella Hoffmeister, 1843 Hrabě 1954, 1981 F2
Stylodrilus absoloni (Hrabě, 1970) Hrabě 1981 A
Stylodrilus brachystylus Hrabě, 1929 Hrabě 1954, 1981 F3
Stylodrilus heringianus Claparède, 1862 Hrabě 1954, 1981 F3
Stylodrilus lemani (Grube, 1879) Hrabě 1954, 1981 F1
Stylodrilus parvus (Hrabě & Černosvitov, 1927) Hrabě 1954, 1981 F1
Trichodrilus allobrogum Claparède, 1862 Hrabě 1954, 1981 F1
Trichodrilus moravicus Hrabě, 1937 Hrabě 1954, 1981 F1
Trichodrilus pragensis Vejdovský, 1876 Hrabě 1954, 1981 A
Trichodrilus strandi Hrabě, 1936 new record F1
Naididae: Naidinae
Amphichaeta leydigi Tauber, 1879 Hrabě 1954, 1981 F1
Arcteonais lomondi (Martin, 1907) Hrabě 1954, 1981 F1
Aulophorus furcatus (Müller, 1773) Hrabě 1954, 1981 F1
Chaetogaster cristallinus Vejdovský, 1884 Hrabě 1954, 1981 F1
Chaetogaster diaphanus (Gruithuisen, 1828) Hrabě 1954, 1981 F2
Chaetogaster diastrophus (Gruithuisen, 1828) Hrabě 1954, 1981 F2
Chaetogaster langi Bretscher, 1896 Hrabě 1954, 1981 F2
Chaetogaster limnaei Baer, 1827 Hrabě 1954, 1981 A
Chaetogaster setosus Světlov, 1925 Hrabě 1954 A
Dero digitata (Müller, 1774) Hrabě 1954, 1981 F2
Dero dorsalis Ferronière, 1899 Hrabě 1954, 1981 A
Dero nivea Aiyer, 1929 Hrabě 1954 A
Dero obtusa Udekem, 1855 Hrabě 1954, 1981 A
Haemonais waldvogeli Bretscher, 1900 Hrabě 1954, 1981 F1
Nais alpina Sperber, 1948 Hrabě 1954, 1981 F3
Nais barbata Müller, 1774 Hrabě 1954, 1981 F2
Nais behningi Michaelsen, 1923 Hrabě 1954, 1981 F1
Nais bretscheri Michaelsen, 1899 Hrabě 1954, 1981 F2
Nais christinae Kasprzak, 1973 Hrabě 1981 F1
Nais communis Piguet, 1906 Hrabě 1954, 1981 F2
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Taxon Author Reference Frequency
Nais elinguis Müller, 1774 Hrabě 1954, 1981 F3
Nais pardalis Piguet, 1906 Hrabě 1954, 1981 F2
Nais pseudobtusa Piguet, 1906 Hrabě 1954, 1981 F1
Nais simplex Piguet, 1906 Hrabě 1954, 1981 F2
Nais stolci Hrabě, 1981 Hrabě 1954 F1
Nais variabilis Piguet, 1906 Hrabě 1954, 1981 F2
Ophidonais serpentina (Müller, 1774) Hrabě 1954, 1981 F2
Paranais frici Hrabě, 1941 Hrabě 1954, 1981 F1
Piguetiella blanci (Piguet, 1906) Schenková 2005 F1
Ripistes parasita (Schmidt, 1847) Hrabě 1954, 1981 F1
Slavina appendiculata (Udekem, 1855) Hrabě 1954, 1981 F2
Specaria josinae (Vejdovský, 1884) Hrabě 1954, 1981 F1
Stylaria lacustris (Linnaeus, 1767) Hrabě 1954, 1981 F3
Uncinais uncinata (Øersted, 1842) Hrabě 1954, 1981 F1
Vejdovskyella comata (Vejdovský, 1884) Hrabě 1954, 1981 F2
Vejdovskyella intermedia (Bretscher, 1896) Hrabě 1954, 1981 F1
Naididae: Pristininae
Pristina aequiseta Bourne, 1891 Hrabě 1954, 1981 F1
Pristina amphibiotica Lastočkin, 1927 Hrabě 1954 A
Pristina bilobata (Bretscher, 1903) Schenková & F1
Kroča 2007
Pristina jenkinae (Stephenson, 1931) new record F1
Pristina longiseta Ehrenberg, 1828 Hrabě 1954, 1981 F1
Pristina menoni (Aiyer, 1930) Hrabě 1954 F1
Pristina osborni (Walton, 1906) new record F1
Pristina rosea (Piguet, 1906) Hrabě 1954, 1981 F2
Naididae: Rhyacodrilinae
Bothrioneurum vejdovskyanum Štolc, 1886 Hrabě 1954, 1981 F3
Branchiura sowerbyi Beddard, 1892 Hrabě 1981 F1
Epirodrilus pygmaeus (Hrabě, 1935) Hrabě 1954, 1981 F2
Rhyacodrilus coccineus (Vejdovský, 1875) Hrabě 1954, 1981 F3
Rhyacodrilus falciformis Bretscher, 1901 Hrabě 1954, 1981 F2
Rhyacodrilus subterraneus Hrabě, 1963 new record F1
Naididae: Tubificinae
Aulodrilus japonicus Yamaguchi, 1953 Hrabě 1954, 1981 F2
Aulodrilus limnobius Bretscher, 1899 new record F1
Aulodrilus pigueti Kowalewski, 1914 new record F1
Aulodrilus pluriseta (Piguet, 1906) Hrabě 1954, 1981 F2
Haber speciosus (Hrabě, 1931) Hrabě 1954, 1981 A
Ilyodrilus templetoni (Southern, 1909) Hrabě 1954, 1981 F2
Limnodrilus claparedeanus Ratzel, 1868 Hrabě 1954, 1981 F3
Limnodrilus hoffmeisteri Claparède, 1862 Hrabě 1954, 1981 F3
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Thirteen species have not been recorded in studies conducted in the Czech Republic since 1996. Their
absence from more recent collections could be caused by various reasons. Firstly, particularly unique habitats
were not studied, thus species limited in distribution to these areas where not recorded—e.g., a cave species
Stylodrilus absoloni (Hrabě, 1970), a groundwater species Trichodrilus pragensis Vejdovský, 1876, and a
snail parasite Chaetogaster limnaei Baer, 1827. Secondly, most of the material discussed in this paper was
collected in running water habitats; stagnant waters were studied to a lesser extent. This could be the reason
for the absence of the temporal pool specialist Lamprodilus mrazeki Hrabě, 1929 and stagnant water
specialists such as Dero dorsalis Ferronière, 1899, Dero nivea Aiyer, 1929, Dero obtusa Udekem, 1855, and
Chaetogaster setosus Světlov, 1925. Other species that have not been reported since 1996 include Pristina
amphibiotica Lastočkin, 1927, Haber speciosus (Hrabě, 1931), Peipsidrilus pusillus Timm, 1977,
Potamothrix bedoti (Piguet, 1913), and Tubifex nerthus Michaelsen, 1908—each of these had previously been
reported only once in the country, and we consider them to be either very rare or regionally extinct in the
Czech Republic.
Taxon Author Reference Frequency
Limnodrilus profundicola (Verrill, 1871) Hrabě 1981 F1
Limnodrilus udekemianus Claparède, 1862 Hrabě 1954, 1981 F2
Peipsidrilus pusillus Timm, 1977 Hrabě 1981 A
Potamothrix bavaricus (Oschmann, 1913) Hrabě 1954, 1981 F2
Potamothrix bedoti (Piguet, 1913) Hrabě 1954, 1981 A
Potamothrix hammoniensis (Michaelsen, 1901) Hrabě 1954, 1981 F2
Potamothrix moldaviensis Vejdovský & Mrázek, 1903 Hrabě 1954, 1981 F2
Psammoryctides albicola (Michaelsen, 1901) Hrabě 1954, 1981 F2
Psammoryctides barbatus (Grube, 1861) Hrabě 1954, 1981 F3
Psammoryctides moravicus (Hrabě, 1934) Hrabě 1954, 1981 F1
Spirosperma ferox Eisen, 1879 Hrabě 1954, 1981 F2
Tubifex ignotus (Štolc, 1886) Hrabě 1954, 1981 F2
Tubifex nerthus Michaelsen, 1908 Hrabě 1981 A
Tubifex tubifex (Müller, 1774) Hrabě 1954, 1981 F3
Propappidae
Propappus volki Michaelsen, 1916 Hrabě 1954 F2
Haplotaxidae
Haplotaxis gordioides (Hartmann, 1821) Hrabě 1954, 1981 F2
Criodrilidae
Criodrilus lacuum Hoffmeister, 1845 Hrabě 1954 F1
Lumbricidae
Aporrectodea georgii (Michaelsen, 1890) Pižl 2002 F1
Aporrectodea handlirschi (Rosa, 1879) Pižl 2002 F1
Aporrectodea limicola (Michaelsen, 1890) Pižl 2002 F1
Eisenia fetida (Savigny, 1826) Pižl 2002 F2
Eisenia spelaea (Rosa, 1909) Pižl 2002 F1
Eiseniella tetraedra (Savigny, 1826) Pižl 2002 F3
Helodrilus oculatus Hoffmeister, 1845 Pižl 2002 F1
Octoclasion tyrtaeum (Savigny, 1826) Pižl 2002 F2
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TABLE 2. Proposal of the Red list of aquatic Oligochaeta of the Czech Republic. Two species from the family
Lumbricidae according to Pižl (2005) are included.
The Red List of aquatic oligochaetes of the Czech Republic (Schenková 2005, Pižl 2005) was modified on
the basis of the new extensive data by excluding Aulodrilus japonicus Yamaguchi, 1953, Ilyodrilus templetoni
(Southern, 1909), Epirodrilus pygmaeus (Hrabě, 1935), Psammoryctides albicola (Michaelsen, 1901), and
Slavina appendiculata (Udekem, 1855), which had been formerly considered endangered. The number of
recent records and distribution of these species within the Czech Republic indicate the stability of their
populations. On the basis of those new data, we changed the protection status of another three species—
Pristina bilobata (Bretscher, 1903), Pristina longiseta Ehrenberg, 1828, and Uncinais uncinata (Ørsted,
1842)—from endangered (EN) to vulnerable (VU). However, we now suggest that the status of endangered
species (EN) to be allocated to Trichodrilus strandi, Haber speciosus, Lamprodrilus mrazeki, Peipsidrilus
pusillus, and Stylodrilus absoloni with respect to their very restricted occurrence—not only in the Czech
Republic, but also in neighbouring countries. Vulnerable protection status (VU) was proposed for
Amphichaeta leydigi Tauber, 1879, Nais behningi Michaelsen, 1923, Nais christinae Kasparzak, 1973, Nais
stolci Hrabě, 1981, Pristina aequiseta Bourne, 1891, P. osborni, P. jenkinae, R. subterraneus, Specaria
josinae (Vejdovský, 1884), S. lemani and Vejdovskyella intermedia (Bretscher, 1896), based on their rare
occurrence and scattered distributions. The new Red list of Czech aquatic oligochaete species with suggested
changes is given in Table 2.
Six species collected during this present study are reported here as new records for the Czech Republic: Trichodrilus
strandi, Pristina jenkinae, P. osborni, Rhyacodrilus subterraneus, Aulodrilus limnobius and A.
pigueti. The extent of their physical and chemical characteristics of finding sites is summarised in Table 3.
Species accounts
Family: Lumbriculidae
Trichodrilus strandi Hrabě, 1936
Records. Bílé Potoky Spring Fen, Valašské Klobouky, 49°06'52"N / 18°01'40"E, lgt. JB, det. JSc (2006);
Hrubý Mechnáč Spring Fen, Lopeník, 48°56'27"N / 17°47'51"E, lgt. JB, det. JSc (2006); Kalábová Spring
endangered (EN) vulnerable (VU)
Arcteonais lomondi (Martin, 1907) Amphichaeta leydigi Tauber, 1879
Criodrilus lacuum Hoffmeister, 1845 Aporrectodea limicola (Michaelsen, 1890)
Haber speciosus (Hrabě, 1931) Pristina aequiseta Bourne, 1891
Lamprodrilus mrazeki Hrabě, 1929 Pristina bilobata (Bretscher, 1903)
Peipsidrilus pusillus Timm, 1977 Pristina jenkinae (Stephenson, 1931)
Piguetiella blanci (Piguet, 1906) Pristina longiseta Ehrenberg, 1828
Stylodrilus absoloni (Hrabě, 1970) Pristina osborni (Walton, 1906)
Trichodrilus pragensis Vejdovský, 1876 Nais behningi Michaelsen, 1923
Trichodrilus strandi Hrabě, 1936 Nais christinae Kasprzak, 1973
Nais stolci Hrabě, 1981
Rhyacodrilus subterraneus Hrabě, 1963
Specaria josinae (Vejdovský, 1884)
near threatened (NT) Stylodrilus lemani (Grube, 1879)
Apporrectodea georgii (Michaelsen, 1890) Uncinais uncinata (Øersted, 1842)
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Fen, Březová, 48°56'22"N / 17°44'39"E, lgt. JB, det. JSc (2006); Chmelinec Spring Fen, Vyškovec,
48°56'22"N / 17°51'20"E, lgt. JB, det JSc (2006); Hutě Spring Fen, Žítková, 48°59'27"N / 17°54'33"E, lgt. JB,
det. JSc (2006).
Characteristics of sites. T. strandi was recorded in 2006 in the Western Carpathian spring fens, which are
situated in the easternmost part of the Czech Republic, on the boundary with Slovakia (Fig. 1). We have
collected this species from altitudes 350–642 m a.s.l. in extremely mineral-rich spring fens with precipitation
of cold water travertine (tufa). The bottom substrate of spring fens was dominated by inorganic material
(gravel and sand) and coarse particulate organic matter (leaves and wood). Tufa precipitated on all submerged
surfaces forms either small incrustations or strong layers.
FIGURE 1. The distribution of Trichodrilus strandi, Pristina jenkinae, Pristina osborni, Rhyacodrilus
subterraneus, Aulodrilus limnobius and A. pigueti in the Czech Republic.
Ecology. T. strandi is well adapted for this rather hostile environment because of a tiny flexible body that
enables it to utilise small interstitial spaces, particularly those in tufa-covered substrates. In studied sites, it
represented the eudominant species followed by 16 additional oligochaete taxa, mostly taxa in the family
Enchytraeidae. Its main adaptation can be feeding on specific kinds of bacteria that colonise surfaces in
mineral-rich waters (Tarmo Timm pers. com.). Although the environment in spring fens is rather stable with
small temperature fluctuations, we recorded seasonal variations in the ratio between juveniles and adults from
50% of juveniles in spring to their prevalence (80%) in autumn. T. strandi is a monocyclic gatherer-collector
burrowing in sediments of xenosaprobic streams, and it is considered a K-strategist (Šporka 2003).
Morphology. This species can be distinguished from other taxa in that all chaetae are bifid with tiny
upper teeth, the male pores are located on conical porophores in IX, and spermathecal pores are present in X
(Fig. 2). The positions of sexual pores in T. strandi (porophores in X, spermathecal pores in IX) are opposite
of those in the genus Stylodrilus, with which young T. strandi can be confused. We have recorded variability
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in the spermathecae position of 200 individuals: 36% had spermathecae in X, 38% in between X and XI
(crossing the septa) and 26% in XI. We did not observe any lateral wings in the genital region, but we
identified only fixed individuals.
Distribution. The nearest known localities for T. strandi are in the Valča Brook—a tributary of the Turiec
River in the Malá Fatra Mts. (Slovakia) (Šporka 1996a), which is approximately 80 km from our sites (Šporka
1996a), and the spring outflow of an ice cave in the Tatra Mts.—approximately 150 km from our sites (Hrabě
1942). European distribution is highly scattered with records from karstic or flysh areas in France (Giani
1979; Juget & Dumnicka 1986), Croatia (Karaman 1987) and Italy (Brinkhurst 1963). According to Fauna
Europaea (Timm & Giani 2004), the species was found in the Czech Republic, but unfortunately no
additional information for this report was provided, nor is available. These data most likely represent records
reported from areas in what is now known as Slovakia prior to its split from the former Czechoslovakia. T.
strandi as the stygophilous species, representative of the Lumbriculidae, is more limited in global distribution
(Martin et al. 2008). This species is worth further investigation since its populations seem to be
geographically separated and there is even the question if they represent the same species.
FIGURE 2. Trichodrilus strandi. A: Schematic drawing of reproductive organs in IX, X, XI segment, lateral view. mp:
male pore on conical porophorus, sp: spermatheca, ov: ovarium. B: dorsal chaeta.
Family: Naididae
Subfamily: Pristininae
Pristina jenkinae (Stephenson, 1931)
Synonyms: Naidium jenkinae Stephenson, 1931; Pristina idrensis Sperber, 1948; Pristinella jenkinae (Stephenson,
1931)
Records. Teplá Brook, Věžná, 49°26'42"N / 16°16'33"E, lgt. PP, det. PP (2003); Bečva River, Lipník-Osek,
49°29'48"N / 17°31'06"E, lgt. KB, det. PP (2004); Gránický Brook, Znojmo, 48°51'60"N / 16°01'33"E, lgt.
PP, det. PP (2005); all specimens were immature.
Characteristics of sites. The species was found in two different habitats: epirhithral and hyporhithral
streams. The epirhithral habitat was represented by two small brooks (2nd
and 3rd
Strahler order) with
dominating stony-gravel substrates, natural channel morphology and forested catchments (catchment area up
to 20 km2
). The hyporhithral habitat was a 30 m wide shallow reach of the river of 7th
Strahler order
(catchment area 1,526 km2
) with cobble-pebble substrate, which flows through extensively used farmland. A
natural self-restoration of this reach of the river resulted from a big flood in 1997.
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Ecology. Pristina jenkinae, a detritophagous oligochaete, was recorded in different freshwater habitats
(Timm & Veldhijzen van Zanten 2002), including hyporheic zones (Strayer & Bannon-O’Donnell 1988; Giani
et al. 2001; Wetzel & Taylor 2001), and in wet soil of a tropical rainforest (Collado & Schmelz 2001). In
central Europe, it was reported from rhithral and potamal zones, with preferences from xeno- to betamesosaprobity
(Hörner et al. 2002). The absence of any historic records of this species from the Czech
Republic are likely attributed to difficulties in its identification (ecophenotypic variation in its chaetae, and
status as a valid taxon) and its rare to occasional occurrence (Wetzel & Taylor 2001).
Morphology. This species can be distinguished from related European Pristina species by none or slight
shortening of the upper teeth in ventral chaetae from the anterior to posterior end, parallel teeth of dorsal
needles with upper teeth slightly (anterior most) or distinctly (posterior bundles) shorter and thinner (from 1/2
to 2/3), smooth hair chaetae, and gradual intestinal dilatation from ½ VI to VII (Collado & Schmelz 2001;
Timm & Veldhijzen van Zanten 2002). A single spermathecal chaeta is present in VII in mature specimens,
but we unfortunately did not find any sexually active individuals during this present study.
Distribution. Pristina jenkinae has a cosmopolitan distribution (Timm & Veldhijzen van Zanten 2002)
and it has been reported from many other European countries: Germany, Poland, Slovakia, Moldova,
Romania, Italy, France, Spain, Portugal, Norway, Sweden, The Netherlands, the UK, Greece, and Finland
(Timm & Giani 2004). However, the absence of records in other European countries can be connected with
identification difficulties and the unclear taxonomical status of this taxon. P. jenkinae was at first
synonymised with P. idrensis by Kathman (1985) and recently redescribed and discussed as probably distinct
species by Collado & Schmelz (2001).
Pristina osborni (Walton, 1906)
Synonyms: Naidium osborni Walton, 1906; Naidium minutum Stephenson, 1914; Pristinella osborni (Walton, 1906);
Pristina minuta (Stephenson, 1914)
Records. Labe (Elbe) River, Děčín 50°42'34"N / 14°11'44"E, lgt. JK, det. PP (2008); all specimens were
immature.
Characteristics of site. The species was found in a single site, in the Labe (Elbe) River approximately 20
km far from the Czech/German boundary near Dečín (Tetschen). This river is the largest in the Czech
Republic (8th
Strahler order) and it is extensively used for shipping to the German port of Hamburg. The mean
depth of this reach of the river was 2.4 m, the bottom substrate was predominantly sand (45%) and gravel
(55%) and water quality is classified according to BOD (biochemical oxygen demand) in the betamesosaprobity
(Table 3).
Ecology. Pristina osborni inhabits freshwaters including hyporheic waters and caves (Giani et al. 2001)
and wet soil (Stout 1958). Its ability to inhabit also semi-terrestrial environments enhances the opportunity
for freshwater populations of this species to persist in intermittent wetlands (Montalto & Marchese 2005). In
tropical regions, P. osborni prefers areas with higher calcium content (Alves et al. 2008). Asexual
reproduction occurs most commonly via paratomy (Timm & Veldhijzen van Zanten 2002). The species is not
usually abundant within the oligochaete community (Giani et al. 2001; Alves et al. 2008).
Morphology. The species can be distinguished by the typical shape of its dorsal bifid chaetae, with the
teeth diverting in a wide angle and the presence of only one needle and one smooth hair seta in the dorsal
bundles. The budding zone begins from XII, and the stomach dilatation begins abruptly in segments VII–VIII.
The morphology of the genital organs was described in detail by Erséus and Grimm (1998).
Distribution. Pristina osborni has a cosmopolitan distribution (Timm & Veldhijzen van Zanten 2002),
and is absent only in the eastern Palaearctic region (Timm & Giani 2004). European records are limited to
southern and western countries (Portugal, Spain, Italy, France, The Netherlands, and Germany; Timm & Giani
2004). The Labe (Elbe) River, which flows through north-eastern Germany to the Baltic Sea, likely serving as
a migration corridor for this species—from its original distribution area in western Europe (as well as it was
documented for aliens) into the Czech Republic. P. osborni could spread into this reach of the river, probably
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from a lower part of the watershed via upstream migration or dissemination by shipping. However,
downstream dissemination into the Labe River—proven to be an alternative pathway of spreading of
epipotamal species (Pařil et al. 2008)—is rather improbable for P. osborni.
TABLE 3. Summary of the characteristics of the aquatic oligochaete species Trichodrilus strandi, Pristina jenkinae,
Pristina osborni, Rhyacodrilus subterraneus, Aulodrilus limnobius and A. pigueti sites in the Czech Republic.
Subfamily: Rhyacodrilinae
Rhyacodrilus subterraneus Hrabě, 1963
Records. Robečský Brook, Česká Lípa, 50°40'05"N / 14°30'27"E, lgt. IS, det. JS/PP (2007), immature
specimens; Svitava River, Brno, 49°08'43"N / 16°37'48"E, lgt. PH, det. PP (2006); one mature specimen.
Characteristics of sites. Although most published records refer to groundwater and hyporheic habitats
(Erséus et al. 1999; Wetzel & Taylor 2001), we found R. subterraneus in surface waters. These surface
habitats, however, likely receive groundwater influences. The Robečský Brook is situated in the north-western
part of the Czech Republic in semi-natural landscape with numerous wetlands and fishponds. The sample was
taken downstream of the Peklo Natural Reserve, where a brook flows through a narrow sandstone gorge with
substrate formed of mud (40%), sand (30%) and gravel (30%). On the contrary, the second sampling site is
situated downstream of Brno, the second largest city in the country, in the straightened and dyked Svitava
River stretch (substrate: 20% mud, 20% sand, 30% gravel and 30% stones), which also serves as a recipient of
sewage water from urban settlements.
Ecology. Rhyacodrilus subterraneus occurs in fresh and brackish water (Erséus et al. 1999); in reference
to its name, especially in interstitial hyporheic zones and wet soil. Many records were reported from deeper
hyporheic habitats (Strayer 2001) and caves (Wetzel & Taylor 2001; Ferreira et al. 2007); nevertheless, it was
Species Trichodrilus
strandi
Pristina
jenkinae
Pristina
osborni
Rhyacodrilus
subterraneus
Aulodrilus
limnobius
Aulodrilus
pigueti
Sites:
No of sites 5 3 1 2 7 1
No of records 15 3 1 2 8 1
River basin Morava Morava Labe Morava, Labe Morava,
Dunaj, Labe
Morava
Abundance >10% 1–2% 1–2% 1–2% 2.1–5% 1–2%
Water body spring brook/
helocrene
brook/river river brook/river brook/river fish-pond
Abiotic parameters
Min.-max.:
Altitude [m a.s.l.] 350–642 225–420 120 190–240 165–485 440
Strahler order 1 2–7 8 5–6 3–4 –
Ann. average discharge [m3
s-1
] – 0.001–15.3 309 1.2–5.2 0.01–0.8 –
Average stream width [m] – 0.9–33.0 100 7.2–12.0 1.9–5.0 –
Chemical parameters
Min.- max.:
pH 7.3–8.2 6.0–9.0 8.8 7.3–8.5 6.0–9.1 9.5–9.8
Conductivity [mS m-1
] 406–599 91–1180 427 333–737 118–921 414–434
Ann. average water temp. [°C] 7.0–14.5 10.6–10.7 14.3 10.2–10.9 8.1–11.8 –
BOD [mg O2 l-1
] – 1.0–6.6 4 1.2–20.8 0.8–9.4 –
Dissolved oxygen [mg l-1
] 2.4–12.7 7.1–14.7 8.9 6.9–14.1 5.4–13.7 6.9–15.4
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also found in species-rich oligochaete assemblages in eutrophic streams (Timm et al. 1997). Reproduction in
this species is sexual (Timm & Veldhijzen van Zanten 2002), but in some regions (United States) only
immature specimens have been found (Wetzel & Taylor 2001).
Morphology. Rhyacodrilus subterraneus can be distinguished from its congeners by straighter and two
times longer upper tooth of anterior dorsal chaetae with intermediate teeth, and two times longer upper tooth
in anterior ventral chaetae. Penial chaetae near male pores in XI segment of mature specimens are only single
with a simple curved tip (Timm & Giani 2004).
Distribution. Prior to records collected during this present study, this rare Holarctic species had been
found only in western European countries (France, Germany, Norway, Sweden, Spain, and The Netherlands;
Timm & Giani 2004), and in the eastern and Midwestern United States (Strayer & Bannon-O'Donnell 1988;
Strayer 2001; Wetzel & Taylor 2001; Kathman & Brinkhurst 1998).
Subfamily: Tubificinae
Aulodrilus limnobius Bretscher, 1899
Records. Gránický Brook, Znojmo, 48°51'60"N / 16°01'33"E, lgt. PP, det. PP. (2005); Drietomice River,
Starý Hrozenkov, 48°57'13"N / 17°52'29"E, lgt. PP, det. PP (2005); Trusovický Brook, Jívová, 49°42'27"N /
17°21'40"E, lgt. KB, det. PP; Olešná River, Zvole, 49°29'26"N / 16°09'44"E, lgt. KB, det. PP (2002); Nectava
River, Březinky, 49°39'24"N / 16°46'52"E, lgt. KB, det. PP (2002); Okluky River, Uherský Ostroh,
48°59'38"N / 17°24'07"E, lgt. H, det. PP (2002); Farský Brook, Trhové Sviny, 48°50'24"N / 14°37'55"E, lgt.
JZ, det. PP (2002); all specimens were immature.
Characteristics of sites. All records were from small and middle-sized brooks (3rd
and 4th
Strahler order,
river width up to 5 m) with a bottom substrate dominated by sand, gravel, and stones. Most of these highland
stretches had a natural morphology (with buffer strips) and extensively used (cropland, grassland), partially
forested catchments. The brooks have good water quality (from oligo- to beta-mesosaprobity), with one
exception of lowland stream (Okluky River, alpha-mesosaprobity).
Ecology. Being a detritophagous species, A. limnobius occurs from hyporhithral to potamal, and also has
been collected from standing water areas including deeper, profundal habitats (Hörner et al. 2002; Šporka
2003; Alves et al. 2008). It can tolerate intermediate eutrophication (Verdonschot 2006) and organic pollution
from oligo- to alpha-mesosaprobity (Hörner et al. 2002). Microhabitat preferences of fine substrates rich in
organic material (pelal, psamal and argylal) have been reported (Šporka 2003; Alves et al. 2008). Among
oligochaetes, A. limnobius belongs to K-strategists (Šporka 2003) with one reproductive cycle per year,
mostly realised by asexual reproduction (architomy); mature specimens are rare (Timm & Veldhijzen van
Zanten 2002). Worms burrow in sediment, where they build reinforced tubes of silt (Timm & Veldhijzen van
Zanten 2002).
Morphology. Aulodrilus limnobius has characteristic bifid crotchets, with up to 10 chaetae per bundle (all
with shorter upper teeth, and occasionally with wing-like dilations of the distal ends of the chaetae in posterior
segments), and an unsegmented tail, serving as a respiratory organ—typical for this genus. It can be
distinguished from its congeners known to occur in the Czech Republic—A. pigueti, A japonicus, and A.
pluriseta—by a lack of hair chaetae (Timm & Veldhijzen van Zanten 2002; van den Hoek & Verdonschot
2005).
Distribution. This cosmopolitan species has been recorded in most of European countries, absent only in
Austria, the UK, Croatia, Denmark, Greece, Slovenia, and Portugal (Timm & Giani 2004). According to
Fauna Europaea (Timm & Giani 2004), the species was found also in the Czech Republic, but unfortunately,
the source of this data is not available.
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Aulodrilus pigueti Kowalewski, 1914
Records. Štěpánek Pond, Pozďatín, 49°13'22"N / 16°02'25"E, lgt. JS, det. KP (2007); the single specimen
collected during this study was immature.
Characteristics of sites. Aulodrilus pigueti was found at a single locality, the Štěpánek fishpond in the
Czech-Moravian Highland Mountains (Českomoravská vrchovina), which is situated in the middle part of the
Czech Republic. This fishpond is a small shallow pond (2.2 ha) exploited by intensive fish farming. The
management of the fish stock composed of Cyprinus carpio Linnaeus and Tinca tinca Linnaeus involved
supplementary feeding and application of manure, which caused nutrient enrichment. Macrophytes, mostly
Glyceria maxima (Hartman) and Typha latifolia Linnaeus, covered only 5% of the littoral zone.
Ecology. Aulodrilus pigueti burrows in sediments where it forms tubes from detritus (Timm & Veldhijzen
van Zanten 2002). Finogenova and Arkhipova (1994), Schloesser et al. (1995) and Šporka (1996b) reported
that A. pigueti inhabits various freshwater environments, such as lakes, rivers, and marshes. It prefers water
quality from oligo- to alpha-mesosaprobic and substrate pelal (Šporka 2003), and tolerates a lower amount of
dissolved oxygen and acidification (Orciari & Hummon 1975; report EPA/600/3-90/073). The sample from
which this single specimen of A. pigueti was identified was dominated by Dero digitata (Müller, 1774), more
species in the genus Limnodrilus, and other Tubificinae.
Morphology. Aulodrilus pigueti can be distinguished from all other taxa by distal dilatations of bifid
crotchets with shorter upper teeth (typical for the genus Aulodrilus). Dorsal crotchets beginning from VI–IX
are replaced by oar-shaped pectinate chaetae with a rounded or sometimes slightly bifid tip. It is possible to
distinguish it from congeners and all other Tubificinae by the presence of oar-shaped chaetae in dorsal
bundles in its middle segments.
Distribution. Aulodrilus pigueti is a cosmopolitan species, often found in tropical countries (Timm &
Veldhijzen van Zanten 2002; Arslan & Sahin 2003). The nearest record to the Czech Republic is from
backwaters of the Morava River in Slovakia (Šporka 1996b); it has also been recorded from the neighbouring
countries of Germany and Poland (Timm & Giani 2004). While A. pigueti is widely distributed in many other
European countries it has not been reported from Austria, Hungary, Romania, Belgium, the UK, Denmark,
Latvia, Switzerland, and Slovenia (Timm & Giani 2004).
Conclusions
This updated check-list of aquatic oligochaetes of the Czech Republic, based on historical and recent records,
includes 95 species: Lumbriculidae (12 species), Naidinae (36 species), Pristininae (eight species),
Tubificinae (22 species), Rhyacodrilinae (six species), Propappidae (one species), Criodrilidae (one species),
Haplotaxidae (one species), and Lumbricidae (8 species). The Red list of Czech aquatic oligochaete species
has been corrected and updated, and now includes nine endangered species (EN), 14 vulnerable species (VU),
and one near threatened (NT). Special attention should be given to the protection and conservation of unique
habitats from which these endangered and vulnerable species have been reported. In addition, it is important
to establish and support monitoring programs for all aquatic habitats to document introduced and invasive
species that are known to be spreading throughout Europe and elsewhere worldwide.
Acknowledgments
We would like to thank K. Brabec, P. Horák, J. Kokeš, A. Krausová, L. Opatřilová, I. Skála, J. Sychra, J.
Zahrádka for kindly providing material and information about sampling sites, and J. Gaisler for English
proofreading. We are indebted to V. Pižl for consultation about the family Lumbricidae. We would also like to
thank M.J. Wetzel and C. Erséus for their critical reading of the manuscript with many useful comments.
Financial support was granted by the Ministry of Education, Youth and Sports of the Czech Republic
(MSM0021622416).
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© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/11/306-0235
Internat. Rev. Hydrobiol. 96 2011 3 235–256
DOI: 10.1002/iroh.201111307
VENDULA KŘOUPALOVÁ*, JINDŘIŠKA BOJKOVÁ, JANA SCHENKOVÁ, PETR PAŘIL
and MICHAL HORSÁK
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2,
CZ-61137 Brno, Czech Republic; e-mails: vkroupalova@seznam.cz, schenk@sci.muni.cz
Research Paper
Small-Scale Distribution of Aquatic Macroinvertebrates
in Two Spring Fens with Different Groundwater Chemistry
key words: springs, fens, macroinvertebrate assemblages, within-site heterogeneity,
seasonal variation
Abstract
We examined responses of macroinvertebrate assemblages to environmental and temporal variations
along spring source-spring brook transects in two fen habitats, sharply differing in groundwater
chemistry, and compared the patterns among individual taxonomical groups. We hypothesised a different
importance of environmental heterogeneity and seasonal changes primarily linked to strong tufa
precipitation, which causes stronger environmental filtering in the calcareous fen. In concordance, we
observed that assemblages of the more homogenous calcareous fen primarily changed over time, due to
seasonal shifts in source availability and favourable conditions. Their spatial distribution was determined
by the amount of CPOM, tufa crusts and temperature variation, but a substantial part of the assemblage
exhibited spatial uniformity (Plecoptera, Clitellata, and especially Trichoptera and Diptera). The
assemblages of the more heterogeneous Sphagnum-fen were primarily driven by water pH and substrate
and the season was a notably weaker predictor. We found that different macroinvertebrate groups can
display various responses to the measured variables shaping the overall pattern obtained based on the
whole community. Further, greater environmental heterogeneity can result in temporally stable species
distribution patterns even at very small spatial scales within a single site.
1. Introduction
Small-scale distributions of macroinvertebrates in springs have been studied mainly in
terms of the zonation patterns of assemblages along the springbrooks and spring sourcespringbrook
gradients. These studies looked at different lengths of the spring fen gradient
and different within-site heterogeneity and the composition of assemblages from different
studies reflected different environmental factors such as discharge (MINSHALL, 1968; CHERTOPRUD,
2006), temperature (WARD and DUFFORD, 1979; RESH, 1983; VON FUMETTI et al., 2007;
BARQUÍN and DEATH, 2011), and substrate (WARD and DUFFORD, 1979; FERRINGTON et al.,
1995; ILMONEN and PAASIVIRTA, 2005). The distance from a spring-source was commonly
* Corresponding author
236 V. KŘOUPALOVÁ et al.
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
interpreted as a proxy for rapid changes in the environment with decreasing influence of a
stable supply of groundwater (e.g., VON FUMETTI et al., 2007) and rapid changes of distributional
patterns of macroinvertebrates at the species level and at higher taxonomic levels.
These patterns have often been described by comparing the macroinvertebrate species occurring
at different distances from the spring-source (e.g., RESH, 1983; WILLIAMS and HOGG,
1988; BARQUÍN and DEATH, 2011). Beside substrate, discharge and temperature regimes,
groundwater chemistry may also influence macroinvertebrate distributions within a single
spring site. It can be expected to be important in heterogeneous springs, where the input of
groundwaters of different chemistry creates markedly different patches within a spring. Direct
effects of pH, bases and metal content in water can alter the suitability of these microhabitats
for macroinvertebrates since individual species and/or taxonomic groups are diversely sensitive
to these factors, mainly due to physiological reasons (cf. FORD, 1989; SUTCLIFFE and
HILDREW, 1989; VUORI, 1995). GLAZIER and GOOCH (1987) and GLAZIER (1991) reported that
alkalinity and pH had an important influence on spring assemblage compositions; similarly,
WILLIAMS et al. (1997) found that water chemistry parameters, describing different levels of
urbanisation, were important determinants of spring assemblages.
Benthic macroinvertebrate assemblages of springs are composed of species with different
strengths of the linkage to the spring environment (LINDEGAARD et al., 1998) and also with
different biological and ecological traits (WILLIAMS, 1991; WAGNER et al., 1998). Therefore,
the distribution of macroinvertebrates within a spring reflects not only the various habitat
preferences of species (e.g., ILMONEN and PAASIVIRTA, 2005) and their requirements for different
food sources (e.g., MCCABE and SYKORA, 2000; BARQUÍN and DEATH, 2006), but also
their life histories (cf. WILLIAMS and HOGG, 1988; BARQUÍN and DEATH, 2004). The responses
of invertebrate orders and/or taxonomic groups to measured factors describing spring habitats
can differ from one another (e.g., MINSHALL, 1968; RESH, 1983; WILLIAMS and HOGG,
1988); thus, the whole macroinvertebrate assemblage may comprise taxa with different, even
inverse, responses. However, there is a lack of studies directly comparing the responses of
whole macroinvertebrate assemblages with responses expressed by the individual taxonomic
groups comprising them.
In this study, we explored the within-site distribution of macroinvertebrates in two spring
fens that significantly differ in water pH and mineral richness. The first site was a calcareous
fen with differing degrees of tufa precipitation which provided an ecologically extreme
habitat. The second site was a Sphagnum-fen characterised by different pH levels, mineral
richness and different substrates. We aimed (i) to compare the spatial and temporal variations
between the two complete macroinvertebrate assemblages and among individual taxonomic
groups, namely Ephemeroptera, Plecoptera, Trichoptera, Diptera (except Chironomidae),
Chironomidae, and Clitellata, and (ii) to analyse the influence of the measured variables on
species composition of the assemblages. We hypothesised that temporal variation would be
more important in the calcareous fen since precipitations of tufa can constrain the number
of microhabitats and their diversity, while the spatial distribution of species would be more
important in the environmentally more heterogeneous Sphagnum-fen and would be predominantly
driven by gradients of pH and mineral richness.
2. Methods
2.1. Study Area and Sites
The studied spring fens are located in the Western Carpathian flysch zone, in the borderland between
the Czech Republic and Slovakia. Flysch is characterised by a serial alternation of sandstone and
claystone deposits with different calcium contents. Due to specific bedrock chemistry, spring fens with
different mineral richness of groundwater occur in this area. Two spring fens representing the opposite
Small-Scale Distribution of Macroinvertebrates 237
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
ends of the pH/calcium gradient were selected for this study. The first site is a calcareous fen with
strong tufa precipitation (the Bílé Potoky Nature Reserve; 49°06′47″ N, 18°01′24″ E) situated in the Bílé
Karpaty Mountains; the second site is a Sphagnum-fen (the Obidová Nature Monument 49°31′03″ N,
18°31′24″ E) situated in the Moravskoslezské Beskydy Mountains. Both spring fens are composed of
four helocrenes with springbrooks which drain the whole spring fen area and connect downstream. In
each site, we chose a ca. 400 m long spring source-springbrook transect comprising three helocrenes
of different groundwater chemistry and their springbrooks. The transect ran longitudinally through the
spring fen and covered the whole site’s heterogeneity.
The calcareous fen was situated on a steep meadow hillside which reaches an altitude between 380
and 500 m above sea level (m a.s.l.) and covers 8.8 ha. Great horsetail (Equisetum telmateia EHRH.) and
butterbur (Petasites hybridus LINNÉ) were the dominant vascular plants; brown mosses (family Bryidae)
dominated in the moss layer. However, no plants covered the bottom of the springbrooks. The pH of
the water was alkaline (mean = 8.3 ± 0.2) and conductivity was very high (mean = 480 ± 43.0 μS cm–1
).
The spring source-springbrook transect was characterised by an increasing discharge and an increasing
variation in water temperature downstream (Table 1). An intense precipitation of calcium carbonate
(tufa) formed strong crusts (mostly upstream) as well as small tufa grains (predominantly downstream).
Beside tufa incrustations, the dominant types of bottom substrate were stones and dead leaves. Dead
leaves dominated in the upper sections near the spring sources, while stones were mostly found in the
lowermost section of the spring fen (Table 1).
The Sphagnum-fen was situated in a meadow with moderate slopes between 710 and 750 m a.s.l.
and covered 7.3 ha. The spring source-springbrook transect was characterised by a sharp gradient in pH
and mineral richness. The uppermost part of the spring fen was classified as a mineral-poor Sphagnumfen
characterised by an acidic pH (mean = 5.2 ± 0.6) and a high iron concentration (2620 μg l–1
). The
remaining part of the Sphagnum-fen was classified as a mineral-rich Sphagnum-fen dominated by
calcitolerant Sphagna. The mean pH was higher here than in the mineral-poor part of the Sphagnumfen
(pH 6.6 ± 0.7); the iron concentration remained very high in the middle part of the spring fen
(mean = 2875 ± 650.9 μg l–1
) but this value decreased distinctly downstream (mean = 244 ± 72.7 μg l–1
).
The conductivity was rather low (mean = 60 ± 14.2 μS cm–1
) along the whole Sphagnum-fen. The discharge
was lower in the middle sections of the spring fen than in the upper and lower sections due to the
high retention of water by peat in the middle sections (Table 1). The substrate characteristics changed
considerably along the entire spring source-springbrook transect; fine detritus (FPOM) and Sphagna
prevailed near the spring sources, whilst a coarse inorganic substrate (coarse gravel) dominated in the
lower part of the Sphagnum-fen (Table 1).
2.2. Field Sampling and Explanatory Variables
Sampling was carried out three times: in spring (April–May), summer (July), and autumn (September)
in 2006. Benthic samples were collected in five (calcareous fen) and six (Sphagnum-fen) sections
of the springs which represented different abiotic conditions along the 400 m long transects from spring
sources to the springbrooks draining each fen. The length of each section was approx. 50 m, and the
distance between neighbouring sections was at least 20 m. In each section, a sample consisting of ten
sampling plots (25 cm × 25 cm), which represented all of the habitats along the sampled spring section,
was taken semiquantitatively with a hand net (mesh size 0.5 mm) by the kick-sampling method (FROST,
1971). After washing the sampled substrate several times in a bucket and removing the coarse inorganic
substrate, the sample was elutriated through a net of a 0.5 mm mesh size and the remaining material was
preserved in 4% formaldehyde. The samples were subsequently sorted and invertebrates were identified
in the laboratory, mostly to the species and genus levels.
Water temperature, pH, conductivity, and dissolved oxygen were measured in the field using portable
instruments (WTW Multi 340i/SET) in each sampling occasion. The annual variation of temperature
of each section was calculated from individual measurements as the difference between maximal and
minimal temperature values during the year. Discharge was estimated by sampling the spring water in
a vessel for a defined period of time in each sampling. We recorded the percentage cover of stones,
gravel, sand, coarse particulate organic matter (CPOM), fine particulate organic matter (FPOM), and
tufa crusts in each section. For statistical analyses, the relative proportions of stones, gravel, and sand in
each section were expressed by the phi coefficient (FURSE et al., 1986). In autumn, water samples were
collected and concentrations of soluble Na, K, Ca, Mg, Al, Fe, SO4, NO3, and PO4 ions were measured
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
238 V. KŘOUPALOVÁ et al.
Table1.MeanvaluesofthephysicochemicalvariablesmeasuredinthecalcareousfenandtheSphagnum-feninspring,summer,and
autumnin2006.TheamountofinorganicsubstrateandFPOMdidnotchangeduringtheyear,thereforeconcretenumbersofphicoef-
ficient,tufacrusts,andFPOMareshowninthetableinsteadofmeanvalues.Thesamplesarenumberedfrom1to5and1to6and
describetheincreasingdistanceofthesampledsitesawayfromthesourceofthefens.Var.intemperature–variationintemperature;
CPOM–coarseparticulateorganicmatter;FPOM–fineparticulateorganicmatter.
pHVar.in
temperature
(°C)
Con-
ductivity
(μScm–1
)
Dissolved
oxygen
(mgl–1
)
Discharge
(mls–1
)
phi-
coefficient
Tufa
crusts
(%)
CPOM
(%)
FPOM
(%)
Ca
(mgl–1
)
Fe
(μgl–1
)
Distance
fromhelo-
crenes(m)
Calcareous-fen
18.1±0.123.7523±54.08.3±1.9377±441–3.23043.3±4.701055341
28.3±0.054474±27.09.2±2.3377±239–1.93053.3±4.7075.98310
38.2±0.124.8497±9.48.9±2.2767±525–3.12033.3±4.7093.7279120
48.5±0.087.4495±32.09.1±2.5933±556–0.7752030092.9130220
58.47483±7.59.9±3.2933±556–2.952010082.5164300
Sphagnum-fen
15.2±0.6655±16.73.1±3.0233±94–1.4100609.326201
26.1±0.6574±2.65.4±1.363±916.2500906.836601
36.5±0.5658±4.36.8±1.873±61–1.7500705.4209010
46.6±0.7465±16.27.5±1.9933±634–5.01003010311170
57.0±0.3547±2.68.3±2.0300±284–3.5500406.3143200
66.8±0.8463±14.57.8±1.81067±680–4.8300510.4278300
Small-Scale Distribution of Macroinvertebrates 239
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
in an accredited laboratory. These samples were collected in late autumn because of the relative stability
of water chemistry in this period (cf. HÁJEK and HEKERA, 2004).
2.3. Statistical Analyses
We analysed responses of the entire benthic community first (i.e., all taxa from all samples) and then
from the whole array we chose the following taxonomic groups, which were the most species rich and
abundant in studied sites: Ephemeroptera, Plecoptera, Trichoptera, Diptera except Chironomidae, and
Clitellata. These datasets were analysed separately. The individual species-by-sample matrices were
subjected to principal components analysis (PCA) due to the low species turnover within the studied
transects. The length of the main gradient in the detrended correspondence analysis (DCA) did not
exceed 3 units, indicating that ordination techniques based on the linear response model were most
appropriate (LEPŠ and ŠMILAUER, 2003). The relationships between explanatory variables and site scores
on the first four ordination axes of PCA were assessed using Spearman’s rank correlations (rs) for
continuous variables and the Mann-Whitney U test for nominal variables. Partial redundancy analysis
(pRDA) with the season as a covariable was used for testing the amount of variability explained by
each physicochemical variable with a forward selection for each tested taxonomic group. The MonteCarlo
permutation test was used to test the significance of variables (P = 0.01; 1999 permutations).
Prior to PCA and RDA, the species abundance data were log (x + 1) transformed to reduce the effect
of dominant taxa. The variation partitioning approach (BORCARD et al., 1992) was used to determine
the relative amounts of variation in species data explained by two different constraining groups of variables
(physicochemical variables and season) in separate RDAs. Since the explained variation was also
influenced by the number of explanatory variables (PERES-NETO et al., 2006), we only used the three
most powerful predictors in each group of variables that were significant in the separate RDAs. The
CANOCO 4.5 software package (TER BRAAK and ŠMILAUER, 2002) was used for computing the ordinations
and STATISTICA 8 (HILL and LEWICKI, 2007) was used for the univariate analyses. Sequential
Bonferroni corrections of the significance levels (HOLM, 1979) were applied for multiple comparisons
of explanatory variables.
3. Results
3.1. Macroinvertebrate Diversity and Abundance
Altogether, 138 and 163 taxa were represented by 54,424 and 45,988 individuals recorded
in the calcareous fen and in the Sphagnum-fen, respectively (Appendix 1). An abundance of
non-insect taxa prevailed at both sites. The amphipod Gammarus fossarum KOCH accounted
for 73% and 30% of all individuals in the calcareous fen and in the Sphagnum-fen, respectively.
After G. fossarum, the clitellate Trichodrilus strandi HRABĚ was the most abundant
species in the calcareous fen and the snail Bythinella austriaca (FRAUENFELD) was the most
abundant species in the Sphagnum-fen (Fig. 1). In contrast, insect fauna was more taxon
rich than non-insect fauna with a high dominance of Diptera, which was particularly rich in
the calcareous fen and comprised nearly 65% of all taxa recorded there (Fig. 2). There were
large proportions of other insect taxa in the Sphagnum-fen (Trichoptera and Plecoptera) and
Clitellata were also characteristic for this site (Fig. 2).
3.2. Differences in the Proportions of Spatial and Temporal Variations
between Spring Fens
The PCA and variation partitioning in partial RDAs revealed significant differences in the
role of physicochemical variables and season for structuring of assemblages in the study of
spring fens (Table 2, Fig. 3). When looking at the whole benthic assemblage in the calcare-
240 V. KŘOUPALOVÁ et al.
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
ous fen, the first PCA axis (28% of the explained data variation) reflected the difference
between spring, summer, and autumn samples, whereas the second ordination axis (18%
of the explained data variation) expressed changes in physicochemical variables along the
transect (Fig. 4). On the contrary, Sphagnum-fen assemblages revealed the opposite pattern;
the first ordination axis (24.5% of the explained data variation) displayed the grouping of
samples along the transect and the second PCA axis (17% of the explained data variation)
was associated with the season (Fig. 5). The variation partitioning method revealed that
physicochemical variables had a substantially greater influence (38%) than season (19%) in
the Sphagnum-fen, while the difference in the variation explained by physicochemical variables
and season was not so high in the calcareous fen (28.5% and 17%, respectively) when
considering the whole assemblage (Fig. 3).
Furthermore, the differences in the effect of physicochemical variables and season between
the individual taxonomic groups were also recorded. In the calcareous fen, the relative part
of the species data variation explained by season was the highest for Trichoptera and Diptera
(except Chironomidae) (32% and 28.5%, respectively), which corresponded well with the
high significance of season in these groups in the PCA analysis (Table 2). Ephemeroptera
was the group with the largest part of the variation explained by physicochemical variables
in the calcareous fen (45.5%). In the Sphagnum-fen, the greatest influence of physicochemical
variables (66%) and the lowest influence of season (3.7%) were characteristic for
Ephemeroptera. The second highest proportion of the variation explained by physicochemical
variables (43%) was recorded in the Trichoptera data set. Simultaneously, Ephemeroptera
and Trichoptera were the only taxonomic groups in the Sphagnum-fen where the season was
not significant on the first PCA axis (Table 2). In contrast, the smallest proportion of variFigure
1. The relative abundance of macroinvertebrates at the studied sites.
Figure 2. The taxonomic structure of macroinvertebrate assemblages at the studied sites.
Small-Scale Distribution of Macroinvertebrates 241
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Table2.RelationshipsbetweenPCAordinationsitescores(firsttwoaxes),explanatoryvariables,andnumberoftaxaandindividuals
inthecalcareousfenandtheSphagnum-fenusingSpearman’srankcorrelations(rs)andtheMann-WhitneyUtest.UsingBonferroni
correctionsthecurrentcutlevelforSpearman’scorrelationswasP<0.003(inbold).ValuesatthesignificancelevelofP<0.01arein
normalprint.Dipteraex.Chir.–DipteraexceptChironomidae;var.intemperature–variationintemperature;CPOM–coarseparticulate
organicmatter;FPOM–fineparticulateorganicmatter;ns–notsignificant.
calcareousfenEphemeropteraPlecopteraTrichopteraDipteraexc.Chir.ChironomidaeClitellataAlltaxa
1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis
Explainedvariance0.7980.1570.3640.2910.3010.2110.3090.2400.3060.2350.5310.2100.2790.178
rsrsrsrsrsrsrs
pHnsnsnsnsnsnsnsnsnsnsnsnsnsns
Var.intemperaturensnsnsnsnsnsnsnsnsnsnsnsns0.775
Conductivitynsnsnsnsnsnsnsnsnsnsnsnsnsns
Dissolvedoxygennsns0.793ns0.647nsns0.832ns0.705nsnsnsns
Dischargensnsnsnsnsnsnsns–0.790ns–0.721nsnsns
phi-coefficientnsnsnsnsnsnsnsnsnsnsnsnsnsns
Tufacrustsnsnsnsnsnsnsnsnsnsnsnsnsns–0.692
CPOMnsnsnsnsnsnsnsnsnsnsnsnsns–0.705
Cansnsnsnsnsnsnsnsnsnsnsnsnsns
Fensnsnsnsnsnsnsnsnsnsnsnsnsns
Distancefromhelocrenesnsnsnsnsnsnsnsnsnsnsnsnsns0.772
Numberoftaxa0.885ns–0.539nsnsns0.686nsnsnsnsnsnsns
Numberofindividuals0.974nsns–0.75nsns0.900ns0.964ns0.985ns0.703ns
P(Utest)P(Utest)P(Utest)P(Utest)P(Utest)P(Utest)P(Utest)
Season0.03ns0.007ns0.005ns0.0070.0050.040.030.014ns0.002ns
Sphagnum-fenEphemeropteraPlecopteraTrichopteraDipteraexc.Chir.ChironomidaeClitellataAlltaxa
1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis1.axis2.axis
Explainedvariance0.6060.2480.3580.1970.2590.2070.3930.1510.3050.2010.3240.2270.2450.171
rsrsrsrsrsrsrs
pHnsns0.733nsnsnsns0.6620.621nsns0.788nsns
Var.intemperature–0.882nsnsns–0.866nsnsnsns–0.64nsns–0.629ns
Conductivitynsnsnsnsnsnsnsnsnsnsnsnsnsns
Dissolvedoxygennsnsnsnsnsnsnsnsnsns–0.604nsnsns
Discharge0.739nsnsns0.769ns0.679nsnsnsnsns0.634ns
phi-coefficient–0.894nsnsns–0.699nsnsnsns–0.642ns–0.636–0.674ns
FPOM–0.914nsnsns–0.825nsnsns–0.636nsns–0.605–0.887ns
Ca0.673nsnsns0.712nsnsnsnsnsnsnsnsns
Fe–0.733nsnsns–0.636nsns–0.843nsnsns–0.724–0.761ns
Distancefromhelocrenes0.886nsnsns0.863nsns0.683nsnsns0.7230.889ns
Numberoftaxa0.968nsnsnsnsnsnsnsns0.770nsnsns–0.589
Numberofindividuals0.96ns–0.834nsns0.5950.721nsns0.746nsns0.607ns
P(Utest)P(Utest)P(Utest)P(Utest)P(Utest)P(Utest)P(Utest)
Seasonnsns0.020.050ns0.0400.0100ns0.008ns0.0090.05ns0.03
242 V. KŘOUPALOVÁ et al.
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ation explained by the physicochemical variables was detected in the Plecoptera (30%) and
Diptera (28%) assemblages (Fig. 3).
3.3. Responses of Individual Taxonomic Groups to Environmental Gradients
Calcareous fen. According to the PCA, the main changes in the species composition of
taxonomic groups were significantly associated with dissolved oxygen (Plecoptera and to
a lesser degree Trichoptera) and discharge (Chironomidae and Clitellata) (Table 2). Numbers
of individuals significantly correlated with the first PCA axes of all taxonomic groups
(except Plecoptera and Trichoptera) (Table 2). Using the season as a covariable in partial
RDA, variation in water temperature explained a large part of the variation in the whole
Figure 3. Comparison of the variance explained by physicochemical variables and season between the
taxonomic groups of the calcareous fen (A) and the Sphagnum-fen (B) using the variation partitioning
approach in separate RDAs.
Small-Scale Distribution of Macroinvertebrates 243
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
assemblage data set. Looking at the whole assemblage, the most significant factors in the
individual taxonomic groups were the amount of CPOM (Ephemeroptera), variation in temperature
and Ca concentration (Plecoptera), and tufa crusts (Chironomidae) (Table 3). In the
Clitellata assemblage, the pRDA results confirmed the importance of discharge, indicating its
significant influence on this taxonomic group. However, no significant predictor was found
in the Diptera assemblage (which did not include Chironomidae) (Table 3).
Sphagnum-fen. Changes in physicochemical variables along the spring source-springbrook
transect played a more important role in the structuring of macroinvertebrate assemblages in
the Sphagnum-fen than in the calcareous fen. Changes along the longitudinal transect were
best displayed by the first PCA axis of the Ephemeroptera and Trichoptera assemblages,
which were significantly correlated with nearly all of the physicochemical variables, reflecting
changes along the transect (Table 2). Water pH was the only physicochemical variable
that correlated with the first PCA axis of Plecoptera, reflecting a seasonal variation in this
assemblage. However, the remaining three taxonomic groups showed a different pattern;
they were more closely related to the physicochemical variables obtained on the second
PCA axis of each taxonomic group (Table 2). On the basis of partial RDA analysis, FPOM
was identified as the most important predictor and pH as the second most important when
looking at the whole assemblage (Table 3). Likewise, the amount of FPOM controlled a
large part of the variation in the Ephemeroptera, Plecoptera, and Chironomidae data sets.
The main changes in species composition of the remaining groups were explained by Fe and/
Figure 4. Principal component analysis (PCA) of all species data in the calcareous fen: ordination plot
of sampled sites on the first two PCA axes with posteriori plotted abiotic variables. Only the variables
significantly associated with the PCA axis at the level P < 0.01 are shown. The most important species
which were characteristic of upstream and downstream sections are displayed. • – springbrooks in the
upper part of the fen connected to their spring sources; – downstream springbrooks formed by the
joining of upstream springbrooks. Numbers from 1 to 5 before the slash describe the increasing distance
of the sampled sites from the spring source of the fen; numbers behind the slash describe the month
of sampling. Var. in temperature – variation in temperature; CPOM – coarse particulate organic matter;
distance – distance from helocrenes.
244 V. KŘOUPALOVÁ et al.
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Figure 5. Principal component analysis (PCA) of all species data in the Sphagnum-fen: ordination plot
of sampled sites on the first two PCA axes with posteriori plotted abiotic variables. Only the variables
significantly associated with the PCA axis at the level P < 0.01 are shown. The most important species
which were characteristic of upstream and downstream sections are displayed. • – springbrooks in the
upper part of fen connected to their spring sources; – downstream springbrooks formed by the joining
of upstream springbrooks. Numbers from 1 to 6 before the slash describe the increasing distance of the
sampled sites from the beginning of the fen; numbers behind the slash describe the month of sampling.
Var. in temperature – variation in temperature; FPOM – fine particulate organic matter, distance – distance
from helocrenes.
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Small-Scale Distribution of Macroinvertebrates 245
Table3.ResultsoftheforwardselectionprocedureinpRDAusingtheseasonasacovariableforspeciesdatainthecalcareousfen
andtheSphagnum-fen.Thenumbersfrom1to9expresstheorderoffactorsaccordingtotheproportionofexplainedvariationineach
taxonomicgroup.VariablessignificantatP=0.01(Monte-Carlotest)wereincludedinthemodel;thesevariablesareinbold.Significance
levels:***,P<0.001;**,P<0.01;*,P<0.05.Dipteraex.Chir.–DipteraexceptChironomidae;var.intemperature–variationin
temperature;CPOM–coarseparticulateorganicmatter;FPOM–fineparticulateorganicmatter.
calcareousfenEphemeropteraPlecopteraTrichopteraDipteraexc.Chir.ChironomidaeClitellataAlltaxa
Var.intemperature52%211%**83%27%64%55%116%**
Dissolvedoxygen37%**43%65%113%74%64%36%
pH62%62%74%64%46%46%55%
Conductivity81%35%*38%84%36%72%27%
Discharge43%82%46%45%26%114%*83%
phi-coefficient90%52%90%74%84%81%65%
Tufacrusts71%72%55%54%113%**211%46%
CPOM130%***90%29%90%90%90%74%
Ca28%*119%**110%36%90%37%90%
Fe90%90%90%90%56%90%90%
Totalvariance54%46%50%47%49%50%52%
Sphagnum-fenEphemeropteraPlecopteraTrichopteraDipteraexc.Chir.ChironomidaeClitellataAlltaxa
FPOM150%***117%***37%83%120%***73%122%***
Var.intemperature47%*37%*120%***54%27%210%**46%
pH71%28%*216%***91%83%45%211%**
Conductivity90%73%83%73%74%54%83%
Dissolvedoxygen81%45%75%44%*92%93%73%
Discharge211%**54%92%34%65%64%93%
phi-coefficient64%92%56%63%46%36%*37%**
Ca57%*64%66%*210%***37%*83%56%**
Fe38%**83%47%*114%***56%119%***65%
Totalvariance89%53%72%46%60%57%66%
246 V. KŘOUPALOVÁ et al.
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
or Ca concentrations (Diptera except Chironomidae and Clitellata), water pH (Trichoptera),
and variation in water temperature (Trichoptera and Clitellata) (Table 3).
4. Discussion
4.1. Spatio-Temporal Variations in Macroinvertebrate Assemblages
In the calcareous fen, the assemblages primarily changed in response to the changing
seasons (Fig. 4, Table 2), whereas in the Sphagnum-fen, they were primarily influenced by
substrate and water chemistry (Fig. 5, Table 2). On one hand, this could be connected to the
different within-site heterogeneity of environmental conditions between the two spring fens,
and/or on the other hand to seasonal shifts in available sources and favourable conditions.
Strong tufa precipitation in the calcareous fen created a rather uniform environment, thus
the main microhabitat differentiation was caused by discharge and the presence of leaf packets,
which varied seasonally. In contrast, the seasonal variation was overridden by a sharp
gradient of physicochemical variables (substrate structure, pH and mineral richness) in the
Sphagnum-fen. This demonstrates the importance of spatial heterogeneity for the distribution
of macroinvertebrates in springs, which was also previously pointed out by WARD and
DUFFORD (1979), who recorded a significant effect of substrate heterogeneity on macroinvertebrate
diversity and abundance in a springbrook-pond system. The pronounced shared
effect of physicochemical variables and season expressed in the calcareous fen (Fig. 3) can
be attributed in particular to the seasonal variability in discharge and the amount of leaf
packets (cf. significant correlations of physicochemical variables in the PCA analysis and
their non-significant contribution after including the season as a covariable in pRDA; Tables
2 and 3). It also suggests an important role of seasonal shifts in the sources and periods of
favourable environmental conditions in the calcareous fen. Harsh conditions in the calcareous
fen may mean that aquatic fauna is strongly dependent on the allochthonous input of
organic matter in the form of leaves and wood. A substantial part of the assemblages was
formed by univoltine species (especially many plecopterans and dipterans) with early spring
and spring emergence. This is obvious because the life cycles of many shredders in temperate
regions are synchronised with the input of riparian leaves in the autumn (e.g., MALICKY,
1989; WILLIAMS, 1991). They showed a major growth period in late autumn and winter when
they reached high abundance and species richness in the samples (Table 2). On the contrary,
the Sphagnum-fen was not influenced by the seasonal input of organic matter since it was
surrounded by coniferous forest and was rich in organic matter due to the continual strong
formation of peat. We recorded equal numbers of individuals collected during the seasons
and the numbers of taxa recorded even decreased towards autumn (Table 2).
4.2. Spatial Distribution of Macroinvertebrates in the Calcareous Fen
The spatial distribution of macroinvertebrates was primarily determined by factors linked
with the distance from the helocrene spring sources: tufa precipitation, organic matter input
and temperature variation (Tables 2 and 3). The sections directly following the helocrenes
were inhabited by unique crenophilic species from all macroinvertebrate groups that were
not present downstream, whereas some species occurred exclusively in downstream sections.
The contribution by particular groups to the total composition of the macroinvertebrate
assemblages differed. A relative spatial uniformity of species composition (and the
dominant influence of seasonal variation) was particularly observed for Trichoptera, Diptera
(except Chironomidae), Plecoptera, and Clitellata. The spatial uniformity of the Trichoptera
assemblage was most likely attributable to the tufa substrate, which is extremely unsuitable
Small-Scale Distribution of Macroinvertebrates 247
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for many species. It forms small particles similar to sand grains, which are known to be an
unstable and nutrient-poor substrate for caddis flies (SOLUK, 1985; COBB and FLANNAGAN,
1990; PHILLIPS, 2003), and/or strong compact crusts which hinder access to the deeper parts
of the bottom substrate (ZOLLHÖFER et al., 2000). Moreover, Trichoptera assemblages, even
if they included many species restricted to springs, did not show fixed zonation patterns in
a spring source-springbrook gradient, but these patterns had a strong seasonal component
(MCCABE and SYKORA, 2000). Similarly, spatially uniform Diptera (except Chironomidae)
assemblages varied more distinctly during the season, most likely because they consisted of
many eurytopic taxa which are able to colonise a wide range of habitats (cf. BRINKMANN,
1991; WAGNER et al., 1998; DE JONG et al., 2008). On the other hand, there were several Trichoptera
and Diptera taxa dominating in tufa zones which either have mechanisms to cope
with tufa deposition or may actually benefit from tufa formation (MARKS et al., 2006). We
found several calciphilous species of Trichoptera and Diptera (e.g., Rhyacophila pubescens
PICTET, Plectrocnemia brevis MCLACHLAN, Pericoma calcilega FEUERBORN, Thaumastoptera
calceata MIK) which could favour these conditions. However, they were evenly distributed
along the studied transect. For Plecoptera, we found an effect of Ca concentration, which
was difficult to interpret. The species composition of the Plecoptera assemblage was similar
along the studied transect, but their abundance was higher in sections with lower Ca concentrations.
We observed strong calcium carbonate encrustations on the thorax and tergites
of Nemoura and Protonemura larvae sampled in the places with the strongest tufa precipitation.
These encrustations might have adverse effects similar to those of Fe precipitates
which cause the inhibition of motion and the smothering of aquatic invertebrates in humic
waters (VUORI, 1995). A similar situation was observed in clitellate assemblages which were
locally negatively affected by discharge and the presence of strong tufa crusts, because
they are sensitive to physical disturbances (BARQUÍN and DEATH, 2004) and the reduction
of interstitial spaces in the stream bed caused by tufa deposition (cf. RUNDIO, 2009).
Clitellates assemblages have been documented as not being as closely related to seasonal
changes as insect fauna in springs (BARQUÍN and DEATH, 2009). However, in our study, the
seasonal variation was distinctive owing to the seasonal dynamics of the dominant species
Trichodrilus strandi, which is monocyclic with spring-summer copulation, lying cocoons in
summer (ŠPORKA, 2003; SCHENKOVÁ et al., 2010), with juveniles in autumn increasing the
number of individuals in samples.
A comparably lower influence of seasonal variation was observed in Ephemeroptera and
Chironomidae assemblages. Their species composition was significantly associated with
coarse organic matter and tufa crusts. They formed discrete assemblages in places near
helocrenes (Chironomidae) or in the springbrook (Ephemeroptera). This pattern resulted
from the dominance of crenobiontic and madicolous Chironomidae such as Neostempellina
thienemanni REISS, Krenopelopia sp., Krenosmittia cf. camptophleps (EDWARDS) and
Parachaetocladius abnobaeus (WULKER) (LINDEGAARD, 1995) near the helocrenes and rheophilous
mayflies (Ecdyonurus subalpinus KLAPÁLEK, Electrogena ujhelyii (SOWA)) dwelling
predominantly in the springbrook section of the fen.
4.3. Spatial Distribution of Macroinvertebrates in the Sphagnum-Fen
The spatial distribution of macroinvertebrates along the transect was governed by a joint
influence of pH/mineral richness and substrate. Particular taxa were more or less sensitive to
variations in pH and iron concentrations along the transect and/or the preferred substrate of
different volumes of fine detritus. Water chemistry varying along the studied transect influenced
Clitellata and Diptera (except Chironomidae) assemblages by the effects of acidity
and high iron concentrations (Table 3). Clitellates showed a shift from acidotolerant speciesdominated
assemblages (Enchytraeidae) to eurytopic aquatic species-dominated assemblages
248 V. KŘOUPALOVÁ et al.
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(Naididae and Lumbriculidae). Diptera (except Chironomidae) were characterised by an
increased abundance of acid-benefiting Ceratopogonidae (SOMMER and HORWITZ, 2001) and
by a very rare occurrence of species from the families Tipulidae and Limoniidae, which were
documented as being limited by pH and heavy metals (SASAKI et al., 2005).
Two groups, Chironomidae and Plecoptera, were predominantly associated with substrate,
regardless of acidity and the distance from the helocrenes (Table 3). Many Chironomidae
species showed clear preferences for either spring sections with a dominance of FPOM or
with a high amount of inorganic substrate. These results correspond well to the findings of
FERRINGTON (1998), who emphasised the importance of a predominant substrate type for the
chironomid assemblage composition in springs. A joint influence of pH/mineral richness and
substrate was observed in the Ephemeroptera and Trichoptera assemblages. As the mayflies
are the most acid-sensitive aquatic insects (BRAUKMANN, 2001), they were completely missing
in the most acidic parts of the fen. Under episodically slight acidic and circum-neutral
conditions, they were less abundant in sections with organic substrate and abundant in sections
with a higher discharge and coarse sediment. This response was caused by the different
degrees of acid sensitivity of mayflies. Baetis vernus CURTIS, an “acid-benefitting” species,
which can even increase their densities with increasing acidity (TIXIER et al., 2009), and
the “slightly acid-sensitive” species Baetis niger (LINNAEUS), which tolerates episodically
acid events (BRAUKMANN, 2001; PETRIN et al., 2007), inhabited sections with circum-neutral
conditions that were episodically weakly acidic. In sections with neutral conditions, i.e.,
springbrooks, the number of mayflies significantly increased and the assemblage included
“acid-sensitive” species. The distribution in these sections was governed by the substrate,
namely by the proportions of FPOM (preferred by, e.g., Baetis niger) and stones and gravel
(occurrence of Ecdyonurus subalpinus and Habrophlebia lauta EATON and higher abundance
of Baetis vernus). Contrary to Ephemeroptera, the Trichoptera taxa richness and abundance
remained constant along the Sphagnum-fen. However, some species occurred exclusively
in acidic sections (i.e., acid-tolerant and/or crenophilous species, according to BRAUKMANN,
2001; GRAF et al., 2008) or in acid-neutral sections (i.e., slightly acid-sensitive and acidsensitive
lotic species; BRAUKMANN, 2001; GRAF et al., 2008). Spring-dwelling species are
generally more tolerant to low pH levels than rhitrobiontic species (see also BRAUKMANN,
2001; SASAKI et al., 2005), which appears to be an adaptation to special crenal conditions
(HAHN, 2000). Simultaneously, the Trichoptera assemblage dwelling in this site comprised
many species with pronounced substrate preferences which were distributed in relation to
the fine detritus/inorganic particle proportions in the bottom substrate (e.g., Silo pallipes,
Odontocerum albicorne, and Hydropsyche saxonica).
5. Conclusions
Spatial heterogeneity in environmental conditions can be an important factor that controls
macroinvertebrate within-site distribution. Higher heterogeneity can result in temporally stable
species distribution patterns even at very small spatial scales, contrary to environmentally
more homogeneous habitats where seasonal changes are of higher importance. Environmentally
more heterogeneous habitats also promote variation in individual taxa responses to the
measured variables, shaping the overall pattern obtained based on the whole community.
In the more heterogeneous habitat, the response of the whole assemblage was a complex
of different group responses, contrary to analogical or non-significant responses in a less
heterogeneous habitat. This study stresses the importance of segregating the responses of
individual macroinvertebrate groups when studying species distribution patterns even within
a single habitat. Responses of individual groups can be highly variable or even reverse at
environmentally more heterogeneous sites.
Small-Scale Distribution of Macroinvertebrates 249
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6. Acknowledgements
This study was supported by the long-term research plan of Masaryk University (MSM 0021622416),
specific research of Masaryk University (MUNI/A/0976/2009) and research projects of the Czech Science
Foundation (P505/10/P302 and P505/11/0779).
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WARD, J. V. and R. G. DUFFORD, 1979: Longitudinal and seasonal distribution of macroinvertebrates and
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Manuscript submitted November 23rd, 2010; revised May 30th, 2011; accepted May 30th, 2011
252 V. KŘOUPALOVÁ et al.
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Appendix 1. The list of taxa collected in the calcareous fen and Sphagnum-fen in 2006.
calcareous fen Sphagnum-fen
Platyhelminthes
Dugesia gonocephala (DUGÉS, 1830) ×
Polycelis felina (DALYELL, 1814) ×
Mollusca
Ancylus fluviatilis O. F. MÜLLER, 1774 ×
Bythinella austriaca (FRAUENFELD, 1857) × ×
Galba truncatula (O. F. MÜLLER, 1774) × ×
Pisidium personatum MALM, 1855 × ×
Pisidium casertanum (POLI, 1791) × ×
Radix peregra (O. F. MÜLLER, 1774) ×
Annelida
Achaeta sp. ×
Cernosvitoviella sp. ×
Cognettia glandulosa (MICHAELSEN, 1888) ×
Cognettia sphagnetorum (VEJDOVSKÝ, 1878) ×
Eiseniella tetraedra (SAVIGNY, 1826) × ×
Enchytraeus sp. × ×
Erpobdella octoculata (LINNAEUS, 1758) ×
Erpobdella vilnensis LISKIEWICZ, 1927 ×
Fridericia sp. × ×
Haplotaxis gordioides (HARTMANN, 1821) ×
Henlea cf. perpusilla FRIEND, 1911 ×
Limnodrilus hoffmeisteri CLAPARÉDE, 1862 ×
Lumbriculus variegatus (O. F. MÜLLER, 1774) ×
Marionina sp. ×
Mesenchytraeus armatus (LEVINSEN, 1884) × ×
Nais communis PIGUET, 1906 ×
Pristina rosea (PIGUET, 1906) ×
Rhyacodrilus falciformis BRETSCHER, 1901 × ×
Stylodrilus heringianus CLAPARÉDE, 1862 ×
Tubifex tubifex (O. F. MÜLLER, 1774) × ×
Trichodrilus strandi HRABĚ, 1936 ×
Crustacea
Gammarus fossarum KOCH, 1835 × ×
Ephemeroptera
Baetis niger (LINNAEUS, 1761) ×
Baetis rhodani (PICTET, 1845) ×
Baetis vernus CURTIS, 1834 ×
Ecdyonurus subalpinus KLAPÁLEK, 1907 × ×
Electrogena ujhelyii (SOWA, 1981) ×
Habrophlebia lauta EATON, 1884 ×
Paraleptophlebia submarginata (STEPHENS, 1835) ×
Rhithrogena sp. ×
Odonata
Aeshna cyanea (O. F. MÜLLER, 1764) ×
Cordulegaster boltonii (DONOVAN, 1807) ×
Pyrrhosoma nymphula (SULZER, 1776) ×
Plecoptera
Amphinemura standfussi (RIS, 1902) ×
Diura bicaudata (LINNAEUS, 1758) ×
Isoperla cf. tripartita ILLIES, 1954 ×
Small-Scale Distribution of Macroinvertebrates 253
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Appendix 1. (continued)
calcareous fen Sphagnum-fen
Leuctra braueri KEMPNY, 1898 × ×
Leuctra inermis KEMPNY, 1899 ×
Leuctra nigra (OLIVIER, 1811) ×
Leuctra prima KEMPNY, 1899 ×
Nemoura cf. avicularis MORTON, 1894 ×
Nemoura cambrica STEPHENS, 1836 × ×
Nemoura cinerea (RETZIUS, 1783) ×
Nemoura marginata PICTET, 1835 × ×
Nemoura sciurus AUBERT, 1949 ×
Nemurella pictetii KLAPÁLEK, 1900 ×
Protonemura lateralis (PICTET, 1835) × ×
Heteroptera
Velia caprai TAMANINI, 1947 ×
Megaloptera
Sialis fuliginosa PICTET, 1836 ×
Neuroptera
Osmylus fulvicephalus (SCOPOLI, 1763) ×
Coleoptera
Anacaena globulus Ad. (PAYKULL, 1798) ×
Anacaena sp. Lv. × ×
Agabus guttatus Ad. (PAYKULL, 1798) ×
Agabus paludosus Ad. (FABRICIUS, 1801) ×
Agabus sp. Lv. ×
Deronectes platynotus Ad. (GERMAR, 1834) ×
Deronectes sp. Lv. ×
Elmis aenea Ad. (O. F. Müller, 1806) ×
Elmis maugetii Ad. (LATREILLE, 1798) ×
Elmis sp. Lv. ×
Elodes sp. Lv. × ×
Esolus angustatus Ad. (O. F. MÜLLER, 1821) ×
Eubria palustris Lv. GERMAR, 1818 ×
Hydraena gracilis Ad. GERMAR, 1824 ×
Hydraena morio Ad. KIESENWETTER, 1849 ×
Hydraena nigrita Ad. GERMAR, 1824 ×
Hydraena saga Ad. d’ORCHYMONT, 1930 × ×
Hydrobius fuscipes Lv. (LINNAEUS, 1758) ×
Laccobius striatulus Ad. (FABRICIUS, 1801) ×
Limnius perrisi Ad. (DUFOUR, 1843) ×
Limnius perrisi Lv. (DUFOUR, 1843) ×
Limnebius truncatellus (THUNBERG, 1794) ×
Oreodytes sanmarkii Ad. (C. R. SAHLBERG, 1834) ×
Platambus maculatus Ad. LINNAEUS, 1758 × ×
Platambus maculatus Lv. LINNAEUS, 1758 ×
Trichoptera
Beraea pullata (CURTIS, 1834) ×
Beraea sp. ×
Ernodes articularis (PICTET, 1834) ×
Ernodes articularis/vicinus ×
Chaetopteryx fusca BRAUER, 1857 ×
Chaetopteryx fusca/villosa ×
Chaetopteryx major MCLACHLAN, 1876 × ×
254 V. KŘOUPALOVÁ et al.
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Appendix 1. (continued)
calcareous fen Sphagnum-fen
Crunoecia irrorata (CURTIS, 1834) ×
Hydatophylax infumatus (MCLACHLAN, 1865) ×
Hydropsyche saxonica MCLACHLAN, 1884 ×
Limnephilus cf. ignavus MCLACHLAN, 1865 ×
Limnephilus cf. sparsus CURTIS, 1834 ×
Notidobia ciliaris (LINNAEUS, 1761) ×
Odontocerum albicorne (SCOPOLI, 1763) ×
Oligotricha striata (LINNAEUS, 1758) ×
Parachiona picicornis (PICTET, 1834) ×
Plectrocnemia brevis MCLACHLAN, 1871 ×
Plectrocnemia conspersa (CURTIS, 1834) × ×
Potamophylax nigricornis (PICTET, 1834) × ×
Rhyacophila philopotamoides MCLACHLAN, 1879 ×
Rhyacophila pubescens PICTET, 1834 ×
Rhyacophila sp. × ×
Sericostoma personatum (KIRBY et SPENCE, 1826) × ×
Silo pallipes (FABRICIUS, 1781) ×
Wormaldia occipitalis (PICTET, 1834) × ×
Diptera
Tipulidae Nigrotipula nigra (LINNAEUS, 1758) ×
Tipula bosnica STROBL, 1898 ×
Tipula fulvipennis DE GEER, 1776 ×
Tipula goriziensis STROBL, 1893 ×
Tipula lateralis MEIGEN, 1804 ×
Tipula maxima PODA, 1761 ×
Tipula rufina MEIGEN, 1818 ×
Tipula unca WIEDEMANN, 1817 ×
Limoniidae Cheilotrichia sp. ×
Eloeophila sp. × ×
Ellipteroides alboscutellatus (VON ROSER, 1840) ×
Gonomyia lucidula MEIJERE, 1920 ×
Gonomyia sp. ×
Helius sp. ×
Molophilus sp. ×
Neolimnomyia filata (WALKER, 1856) × ×
Orimarga sp. ×
Scleroprocta sp. × ×
Thaumastoptera calceata MIK, 1866 ×
Pediciidae Dicranota sp. × ×
Pedicia sp. × ×
Tricyphona sp. × ×
Ptychopteridae Ptychoptera lacustris MEIGEN, 1830 ×
Psychodidae Berdeniella sp. ×
Jungiella sp. ×
Pericoma calcilega FEUERBORN, 1923 ×
Pneumia sp. ×
Psychoda sp. ×
Threticus sp. ×
Ulomyia sp. × ×
Dixidae Dixa maculata MEIGEN, 1818 × ×
Dixa submaculata EDWARDS, 1920 ×
Small-Scale Distribution of Macroinvertebrates 255
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Appendix 1. (continued)
calcareous fen Sphagnum-fen
Thaumaleidae Thaumalea sp. × ×
Ceratopogonidae Atrichopogon sp. × ×
Ceratopogoninae × ×
Dasyhelea sp. × ×
Chironomidae Apsectrotanypus trifascipennis (ZETTERSTEDT, 1838) × ×
Brillia bifida (KIEFER, 1909) × ×
Chaetocladius piger GR. × ×
Conchapelopia sp. × ×
Corynoneura cf. lobata EDWARDS, 1924 × ×
Diamesa cf. tonsa (HALIDAY, 1856) × ×
Eukiefferiella cf. brehmi GOUIN, 1943 ×
Eukiefferiella brevicalcar (KIEFFER, 1911) ×
Eukiefferiella cf. fuldensis LEHMANN, 1972 × ×
Heleniella serratosioi RINGE, 1976 × ×
Heterotanytarsus apicalis (KIEFER, 1921) ×
Heterotrissocladius marcidus (WALKER, 1856) ×
Krenopelopia sp. × ×
Krenosmittia cf. camptophleps (EDWARDS, 1929) ×
Limnophyes sp. × ×
Macropelopia cf. nebulosa (MEIGEN, 1804) ×
Metriocnemus hygropetricus GR. × ×
Metriocnemus fuscipes GR. × ×
Micropsectra sp. × ×
Microtendipes chloris GR. ×
Nanocladius parvulus/rectinervis ×
Natarsia sp. × ×
Neostempellina thienemanni REISS, 1984 ×
Orthocladius lignicola KIEFFER, 1914 ×
Orthocladius rivicola GR. × ×
Orthocladius rivulorum KIEFER, 1909 ×
Paramerina sp. ×
Parametriocnemus stylatus (SPARCK, 1923) × ×
Paraphaenocladius sp. × ×
Paratendipes nudisquama (EDWARDS, 1929) ×
Phaenopsectra sp. ×
Polypedilum convictum GR. ×
Polypedilum laetum GR. ×
Polypedilum scalaenum GR. × ×
Prodiamesa olivacea (MEIGEN, 1818) × ×
Parachaetocladius abnobaeus (WÜLKER, 1959) × ×
Rheocricotopus atripes (KIEFER, 1913) × ×
Rheocricotopus effusus (WALKER, 1856) × ×
Rheocricotopus fuscipes (KIEFER, 1909) × ×
Rheocricotopus sp. ×
Smittia sp. ×
Stempellinella ciliaris/flavidula × ×
Synorthocladius semivirens (KIEFER, 1909) × ×
Tanytarsus sp. ×
Thienemanniella clavicornis/vittata ×
Trissopelopia sp. ×
Tvetenia bavarica GR. × ×
Zavrelimyia sp. × ×
256 V. KŘOUPALOVÁ et al.
© 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Appendix 1. (continued)
calcareous fen Sphagnum-fen
Simuliidae Simulium argyreatum MEIGEN, 1838 ×
Simulium cf. carpathicum (KNOZ, 1961) × ×
Simulium costatum FRIEDERICHS, 1920 × ×
Simulium ornatum MEIGEN, 1818 ×
Simulium trifasciatum CURTIS, 1839 ×
Simulium vernum GR. × ×
Sciaridae × ×
Cecidomyidae × ×
Stratiomyidae Beris clavipes (LINNAEUS, 1767) ×
Beris vallata (FORSTER, 1771) ×
Nemotelus pantherinus (LINNAEUS, 1758) ×
Oxycera meigenii STAEGER, 1844 ×
Oxycera pardalina MEIGEN, 1822 ×
Oxycera pygmaea (FALLEN, 1817) ×
Tabanidae Chrysops caecutiens (LINNAEUS, 1758) ×
Hybomitra sp. ×
Tabanus autumnalis LINNAEUS, 1761 ×
Tabanus sp. ×
Rhagionidae Chrysopilus sp. ×
Athericidae Ibisia marginata (FABRICIUS, 1781) ×
Empididae Chelifera sp. × ×
Clinocera sp. ×
Dolichocephala sp. ×
Dolichopodidae ×
Syrphidae Melanogaster hirtella (LOEW, 1843) ×
Sciomyzidae Pherbellia sp. × ×
Drosophilidae Scaptomyza sp. ×
133
Bojková, J., J. Schenková, M. Horsák & M. Hájek, 2011
Species richness and composition patterns of clitellate (Annelida) assemblages in the treeless
spring fens: the effect of water chemistry and substrate. Hydrobiologia, 667, 159–171.
PRIMARY RESEARCH PAPER
Species richness and composition patterns of clitellate
(Annelida) assemblages in the treeless spring fens: the effect
of water chemistry and substrate
Jindrˇisˇka Bojkova´ • Jana Schenkova´ •
Michal Horsa´k • Michal Ha´jek
Received: 6 February 2010 / Revised: 20 January 2011 / Accepted: 13 February 2011
Ó Springer Science+Business Media B.V. 2011
Abstract Spring fens are isolated treeless wetlands
of a high conservation value. Their environmental
conditions are strongly related to their groundwater
chemistry, which controls species distribution within
various groups of organisms. Clitellates, a dominant
group of non-insect aquatic fauna, however, have
never been studied in these habitats. It is unclear from
previous studies to what extent the distribution of
aquatic non-insect taxa reflects water chemistry rather
than the substrate structure. We studied 34 spring fens
sampled in 17 isolated sites in the Western Carpathian
Mountains to determine mainly the effects of water
chemistry and substrate structure on variation in
species richness and composition of clitellate assemblages
as examples of the non-insect fauna. A total of
34 taxa were found, with 3–15 taxa collected per
sample. Species richness was negatively correlated
with water mineral concentration measured as water
electric conductivity (r = -0.57, P \ 0.001) and
positively with TOC (r = 0.60, P \ 0.001). Surprisingly,
the lowest number of taxa was found in
calcareous fens and richness increased towards Sphagnum-fens.
There was a species turnover related to
changes in mineral richness and substrate characters.
The main change of species composition was promoted
by changes in substrate structure. The second gradient
of species composition was linked with the amount of
nutrients, moisture, and dominance of sphagna, and
was associated with an increase of eurytopic species in
fens with high nutrient availability. It was difficult to
separate the effects of water chemistry and substrate on
clitellate species distributions owing to the fact that
variation in tufa precipitation and vegetation was
driven by water chemistry changes. This study presented
the first quantitative data on fen clitellate
assemblages, which appear to have an unusual pattern
of species richness. In contrast to plants and molluscs,
calcareous fens appeared to be a harsh environment for
clitellate species. Only few specialized species, mainly
Trichodrilus strandi, were able to establish viable
populations. The significant effect of water chemistry
on clitellate distribution patterns raises questions about
the direct influence of water chemistry on non-insect
aquatic taxa, which have previously been considered to
be mostly determined by substrate characteristics.
Keywords Spring fens Á Oligochaeta Á Hirudinida Á
Poor–rich gradient Á Diversity pattern
Introduction
Identification and explanation of non-random patterns
of species richness and composition is one of the key
Handling editor: Stuart Anthony Halse
J. Bojkova´ (&) Á J. Schenkova´ Á M. Horsa´k Á M. Ha´jek
Department of Botany and Zoology, Faculty of Science,
Masaryk University, Kotla´rˇska´ 2, 61137 Brno,
Czech Republic
e-mail: bojkova@centrum.cz
123
Hydrobiologia
DOI 10.1007/s10750-011-0634-3
factors in understanding the underlying processes of
community ecology. However, the patterns observed
can vary between different habitats and they are also
dependent on the length of the gradient and the
groups of organisms studied. Thus, it is usually not
possible to apply results of studies in one type of
habitat or taxonomical group directly to another
habitat or group. Knowledge of the ecology of
particular taxonomical groups is often highly uneven
across different habitat types.
For example, clitellates (sensu Erse´us, 2005),
which include oligochaetes and leeches, have been
studied in detail in various types of running waters,
lakes, and artificial habitats (e.g. Sˇporka, 1998;
Verdonschot, 2001; Nijboer et al., 2004; Dumnicka
& Boggero, 2007; Dumnicka et al., 2007). However,
there are only few studies of this group in mire
habitats. These studies dealt with oligochaetes of
ombrotrophic bogs and moorlands (i.e. mires that
receive all of their water and nutrients from precipitation)
and bog streams (Svendsen 1957a, b; Cragg,
1961; Smith, 1986; Smith & Kaster, 1986; van
Duinen et al., 2006), which showed to have very low
species richness. The only abundant species inhabiting
these nutrient-poor and acidic mires, Cognettia
sphagnetorum, is also the only thoroughly studied
species in terms of growth, survival, and feeding
habits (e.g. Springett & Latter, 1977; Latter &
Howson, 1978). Habitats slightly influenced by
alkaline groundwater (lagg zones, transitional mires,
and bog brooklets) tend to have higher species
richness because of higher availability of nutrients
(van Duinen et al., 2006).
There is only sketchy information on clitellate
assemblages of treeless spring fens (i.e. minerotrophic
mires, wetlands supplied by mineral-rich groundwater).
Available studies on fens deal with the
production of soil oligochaetes (Erman & Erman,
1975) and species composition of assemblages in
degraded fenland area in the Netherlands affected by
eutrophication (Verdonschot, 1984) and in ditches
and canals of drained fens in Germany (Langheinrich
et al., 2004). Clitellates of undisturbed, nutrientlimited
spring fens have never been studied.
The habitat diversity of well-preserved fens is
primarily determined by the chemistry of the groundwater
supplying them, especially the calcium concentration
and water pH (e.g. Ha´jek et al., 2006). A sharp
gradient of mineral richness from acid mineral-poor
fens to extremely mineral-rich calcareous fens was
originally described in relation to vegetation as the
poor–rich gradient (e.g. du Rietz, 1949; Malmer,
1986; Ha´jek et al., 2006). Five vegetation types of
increasing complexity along the gradient clearly
describe the diversity of fens (for details, see Ha´jek
et al., 2006). Three of the vegetation types are
Sphagnum-fens (mineral-poor, moderately mineralrich,
and mineral-rich fens) and two are brown-moss
fens (extremely mineral-rich and calcareous fens).
Conspicuous changes in species richness and composition
have also been observed along this gradient
in molluscan (Horsa´k & Ha´jek, 2003), algal (Poulı´cˇkova´
et al., 2003; Fra´nkova´ et al., 2009), and
testacean (Opravilova´ & Ha´jek, 2006) assemblages.
However, the question whether aquatic macroinvertebrates
respond significantly to this ecological
gradient is yet to be studied, because most existing
ecological studies have not covered the entire length
of the gradient (e.g. Erman & Erman, 1975; van
Duinen et al., 2006; Suren et al., 2008).
Previous studies that have included water chemistry
were restricted to rather uniform mire habitats,
which is the probable reason why these studies found
that the variation in macroinvertebrate assemblages
was governed by physical habitat attributes at the
within-site scale and by various basic ecological
differences among wetland types at the between-site
scale. Glazier (1991) assumed there was an influence
of mineral richness and pH on the composition of
macroinvertebrate assemblages of springs, because
non-insect taxa highly dominated in assemblages of
hard-water springs and insect taxa dominated in softwater
springs, whereas insects usually prevail in other
lotic habitats regardless of their pH or alkalinity
(Glazier & Gooch, 1987; Glazier, 1991). Glazier
(1991) proposed a complex influence of the adverse
effects of low pH and alkalinity on crustaceans and
molluscs and the benefits of physical constancy in the
habitats he studied which favoured non-emergent
species with high population densities. Subsequent
research confirmed the importance of habitat stability,
especially in terms of minimal fluctuation in flow
and temperature fluctuations (Barquı´n & Death,
2004), and supported the existence of a weak
association between aquatic insects and spring water
only in hard-water springs (Virtanen et al., 2009) and
tufa-forming spring fens (Bojkova´ & Helesˇic, 2009).
However, the influence of water chemistry on the
Hydrobiologia
123
distribution patterns of the aquatic non-insect fauna
has not been studied to date in mires.
The aims of this study were to (i) determine the
effect of water chemistry on species richness and
composition of clitellate assemblages, (ii) show the
pattern of species distribution along the main environmental
gradients, and (iii) provide the first quantitative
data on aquatic and semi-aquatic oligochaetes
and leeches of spring fens. We have chosen the
Western Carpathian flysch zone (Czech Republic and
Slovakia) as our study area because they vary from
calcium-poor acidic fens with a tendency towards
ombrotrophy (about 2 mg l-1
of calcium) to extremely
calcium-rich tufa-forming fens (up to 300 mg l-1
of
calcium).
Materials and methods
Study area and sites
The study area was located on the western margin of
the Western Carpathians (48°560
–49°320
N, 17°440
–
18°510
E), in the border region between the Czech
Republic and Slovakia (Fig. 1). It was chosen
because of the variable chemistry of the local aquifers
and, therefore, the groundwater supplying the wetlands
within it, as well as because of the overall the
similarities in hydrological characteristics, origin, and
age of spring fens within the area (Rybnı´cˇkova´ et al.,
2005). The bedrock of this area is formed by
alternating claystone and sandstone with variable
chemistry, especially differing in calcium and magnesium
content. Marls, claystone, limestone, and
calcareous sandstone prevail in the south-western part
of the study area, where groundwater is extremely
rich in calcium and magnesium, which causes
formation of cold water travertine (tufa) in most
cases. Towards the north-east, the groundwater is still
rich in calcium, but has a lower content of magnesium
and higher contents of sodium, potassium, and
iron. The northern part of the study area is characterised
by decalcified, iron-cemented sandstone. It
has the lowest calcium concentration within the entire
study area (Rapant et al., 1996; Ha´jek et al., 2002).
Seventeen sites of treeless, mostly sloping fens
supplied by permanent springs, were chosen to cover
the complete mineral-richness gradient (Fig. 1). The
sites were selected on the basis of previous comprehensive
studies of spring fen vegetation in order to
cover all main vegetation types that mirror main
ecological types of spring fen habitats (Poulı´cˇkova´
et al., 2005; Ha´jek et al., 2006). To obtain a balanced
set of these structural habitat types, six sites were
selected within calcareous fens with a different
degree of calcium carbonate precipitation (Caricion
Fig. 1 Location of the study area and sites
Hydrobiologia
123
davallianae), six within mineral-rich fens without
calcium carbonate precipitation (Caricion davallianae),
and five sites within Sphagnum-fens of
different mineral richness and acidity of water
(Sphagno warnstorfii–Tomenthypnion, Caricion fuscae,
and Sphagno recurvi–Caricion canescentis).
The altitudes of the studied fens varied from 450 to
750 m a.s.l.
Field sampling and explanatory variables
Samples of clitellates were collected three times a
year (May, July, and September 2006), from 17 sites
in two different habitats (altogether 102 samples), i.e.
the part of the spring fen with strongest flow and the
part with slow-flowing or almost standing water. For
statistical analyses, samples from individual seasons
were merged to provide 34 samples from two habitats
at 17 sites. Each sample was a plot delimited by a
metal frame of 25 9 25 cm (625 cm2
), where vegetation
and bottom sediment were gathered to the
depth of 5 cm. It was elutriated through a net of
250 lm mesh size, and substrate was kept in 4%
formaldehyde solution. Clitellates were extracted by
hand-sorting under a stereomicroscope in the laboratory.
Oligochaetes were permanently mounted on
microscope slides. The keys of Hrabeˇ (1954, 1981),
Nielsen & Christensen (1959, 1961, 1963), Timm
(1999), and Timm & Veldhijzen van Zanten (2002)
were used for identification of oligochaetes. Hirudinida
were identified according to Neubert & Nesemann
(1999) and Kosˇel (2001). Species nomenclature
follows Siddall et al. (2001), Erse´us (2005), and
Erse´us et al. (2008).
Water conductivity, temperature, dissolved oxygen,
and pH were measured in situ by portable
instruments (WTW Multi 340i/SET). Water conductivity
represents the approximation of total water
mineral concentration; it strongly correlates with
Ca ? Mg concentration (Ha´jek et al., 2005) and it
can be used as a reliable proxy of the calcium
concentration (Sjo¨rs & Gunnarsson, 2002; Horsa´k,
2006). At each sampling date, 100 ml of substrate
was extracted from next to each sampling plots for
measuring total organic carbon (Shimadzu TOCVCPH).
For characterising each site, a one-shot
sample of substrate and water was taken in August
2006. Substrate samples were sampled from a plot of
25 9 25 cm to the depth of 5 cm. These plots always
lay next to the places where samples of clitellates
were taken and reflected the same structural microhabitat
type. Particulate organic matter (POM) was
elutriated from these samples using an elutriation
apparatus (Omesova´ & Helesˇic, 2004), sieved
through a net of 1 mm mesh size, and dried at
70 °C. Coarse particulate organic matter (CPOM;
fraction [1 mm) was sorted according to the origin
(sphagna, brown mosses, vascular plants, and wood/
leaves). All fractions were weighed and described as
the proportions of the total weight of CPOM.
Remaining inorganic substrate was dried at 80 °C
and used for grain size analysis. Median diameter of
particle size (D50) was used for describing the
substrate particle size (Giere, 1993). Water samples
were collected in autumn due to relative stability of
water chemistry (Ha´jek & Hekera, 2004) and the
content of ions Ca2?
, Mg2?
, Fe, NO3
,
and PO4
3were
measured (Table 1).
Two environment characteristics of sites (moisture
and nutrients) were estimated based on the vegetation
composition using the Ellenberg indicator values
(EIV) in the JUICE program (Tichy´, 2002). The
indicator value for nutrients referred to the availability
of three major nutrients (N, P, K) to plants and it
strongly correlated with plant biomass production
(Schaffers & Sy´kora, 2000). There is a general lack
of correlation between soil or water nutrient concentrations
and Ellenberg value for nutrients (Schaffers
& Sy´kora, 2000). The species composition of vascular
plants was recorded in the 4 9 4 m (16 m2
) plots
placed in the central part of each site. The cover of
each plant species was estimated using the BraunBlanquet
nine-grade scale (van der Maarel, 1979),
and an EIV for plant species was calculated (for
details see Schaffers & Sy´kora, 2000; Horsa´k et al.,
2007). EIVs have proved to be very useful in studies
of animal ecology, yielding accurate estimates of
variables difficult to measure directly in the field
(Horsa´k et al., 2007).
Statistical analyses
All explanatory variables were subjected to the
Principal Components Analysis (PCA) on the correlation
matrix (centred and standardised) to reveal the
main gradients of environmental variation and to
show the relations among variables. The species
abundance data were log-transformed as Y = log
Hydrobiologia
123
(n ? 1) to reduce the undue influence of dominant
species. Detrended Correspondence Analysis (DCA)
was used to study relationships between species
composition and explanatory variables. Spearman
rank correlations (rs) and Mann–Whitney U test were
used to examine possible relationships between
explanatory variables and site scores on the ordination
axes. Bonferroni corrections of the significance level
were used for multiple comparisons of explanatory
variables (Holm, 1979).
The variation partitioning approach (Økland,
1999) was used to determine the relative amount of
variation in clitellate data explained by two different
constraining groups of variables (water chemistry and
substrate characteristics) in separate Canonical Correspondence
Analyses (CCA) using the forward
selection procedure and the Monte Carlo test with
1,999 permutations (Lepsˇ & Sˇmilauer, 2003). Since
explained variation is also influenced by the number
of explanatory variables (Peres-Neto et al., 2006), we
used only variables that were significant in two CCAs
where all water chemistry variables and all substrate
characteristics were included (not shown in the
Results). The CANOCO 4.5 package (ter Braak &
Sˇmilauer, 2002) was used for ordination techniques
and STATISTICA 8 (Hill & Lewicki, 2007) for the
other (uni-dimensional) analyses.
Results
Major environmental gradients and relationships
among measured variables
Many of the explanatory variables were inter-correlated,
as shown in the PCA of 18 explanatory
variables (Table 2). PCA found one important environmental
gradient within a set of explanatory
variables, and the majority of these variables were
significantly associated with the first PCA axis. This
axis reflected the gradient of mineral richness (conductivity,
Ca2?
, Mg2?
), pH, NO3
-
concentration,
substrate structure (D50, TOC, POC, wood/leaves,
sphagna), moisture, and discharge (Table 2). The
second PCA axis was significantly correlated with
nutrients, Fe concentration, and vascular plants. The
third PCA axis was correlated with PO4
3-
concentration
and brown-mosses. The fourth axis explained
a very small part of the total variation, and no
significant correlations with the analysed variables
were observed.
Major gradients of species composition
A total of 34 taxa of clitellates of 7,299 specimens
were found in the studied spring fens (Table 3).
Table 1 Descriptive statistics for the variables used in the analyses
Calcareous fens Mineral-rich fens Sphagnum-fens
MEAN MAX MIN SD MEAN MAX MIN SD MEAN MAX MIN SD
pH 7.9 8.2 7.3 0.3 7.3 8.4 6.3 0.6 5.4 6.9 2.8 1.1
Conductivity (lS cm-1
) 485.8 600.0 406.0 60.3 288.3 599.0 48.0 169.8 62.9 114.0 30.0 19.5
Discharge (ml s-1
) 188.3 533.3 46.7 162.5 78.9 130.0 43.3 30.7 120.0 433.3 23.3 157.7
TOC (g kg-1
) 18.9 65.8 0.0 18.0 103.0 271.8 18.4 68.8 214.6 319.0 76.3 81.0
PO4
3(mg
l-1
) 0.1 0.5 0.0 0.2 0.2 0.3 0.0 0.1 0.3 0.7 0.0 0.3
NO3
(mg
l-1
) 9.3 20.5 0.2 6.2 1.0 2.5 0.1 0.9 0.5 1.3 0.1 0.4
Fe (lg l-1
) 305.7 816.0 40.0 280.3 2925.5 3600.0 169.0 846.4 1400.4 3660.0 46.0 2327.6
Ca (mg l-1
) 88.8 112.0 60.6 19.8 48.7 107.0 9.3 33.2 6.0 9.2 3.7 1.9
Mg (mg l-1
) 11.7 18.6 2.4 5.8 9.3 15.5 1.2 5.5 1.9 3.1 0.7 0.9
D50 (mm) 3.4 11.6 0.2 3.8 0.3 0.9 0.1 0.3 0.1 0.1 0.1 0.0
POM (%) 9.8 42.1 0.2 11.1 28.0 82.2 1.6 24.4 58.3 99.1 30.2 19.0
Leaves/wood (%) 58.8 100.0 20.0 36.3 46.5 90.0 3.0 43.5 0.0 0.0 0.0 0.0
Vascular plants (%) 18.0 24.0 14.0 4.3 48.8 72.0 6.0 25.3 54.0 80.0 24.0 23.0
Brown-mosses (%) 64.3 80.0 55.0 11.1 48.0 94.0 10 28.5 14.0 26.0 2.0 12.0
Sphagna (%) 0.0 0.0 0.0 0.0 24.0 24.0 24.0 0.0 62.0 100 18.0 28.7
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123
Numbers of taxa ranged from 3 to 15 per sample and
from 6 to 27 per site; the median number of species
per sample and site was 7 and 15, respectively. The
clitellate assemblages consisted mostly of taxa
belonging to families Enchytraeidae (14 taxa) and
Naididae (11 taxa). Both Lumbriculidae and Lumbricidae
were represented by three taxa and Haplotaxidae
by a single species. Two species of
Hirudinida were recorded. Dominant oligochaete
species, Trichodrilus strandi and Stylodrilus heringianus
(both Lumbriculidae), represented 31.7 and
28.7%, respectively, of all specimens recorded
(Table 3).
In the DCA, the first axis accounted for 22.4%, the
second for 8.2%, the third for 5.6%, and the fourth
3.3% of the total variance of species data. This
analysis revealed two major gradients in species data;
the first gradient expressed on the first ordination axis
reflected the influence of mineral richness and
substrate characteristics on the composition of clitellate
assemblages (Fig. 2). Variables displaying significant
correlation (P \ 0.002) with the sample
scores on the first DCA axis were those describing
chemistry of spring fen water (i.e. pH, conductivity,
NO3
,
Ca2?
, and Mg2?
) and characteristics of the
bottom substrate (i.e. D50, TOC, proportions of POM
and wood/leaves in substrate sample) (Table 4). Flow
parameters (water discharge and depth) were not
significantly correlated with the first DCA axis
(Table 4). The first DCA axis showed the shift in
species composition from calcareous fens with
different degree of tufa precipitation towards Sphagnum-fens
and, in several cases, towards mineral-rich
fens (Fig. 2). This gradient represented the compound
effect of mineral richness and substrate character.
According to the position of individual species on
the first DCA axis (Fig. 3), a stygophilous species
T. strandi was the only species with a strong affinity
to calcareous fens. In the middle part of the axis,
semiaquatic taxa Fridericia spp., Eiseniella tetraedra,
Mesenchytraeus armatus, Cognettia sphagnetorum,
and Rhyacodrilus falciformis were present.
Common aquatic oligochaete species, as well as a
leech Erpobdella vilnensis, had the highest scores on
the first axis. The second ordination axis expressed
the second important gradient in species data, the
gradient of moisture and nutrients as indicated by
EIV values and the dominance of sphagna. Along this
gradient, the group of Sphagnum-fens (upper right
part of the diagram) and mineral-rich fens (lower
right part of the diagram) were clearly separated
(Fig. 2). Cognettia sphagnetorum, C. glandulosa, and
Lumbriculus variegatus were associated with Sphagnum-fens,
which was indicated by their higher scores
on the second axis. Predominantly, eurytopic aquatic
species (e.g. Limnodrilus hoffmeisteri, Tubifex tubifex,
and Erpobdella vilnensis) were characteristic of a
group of mineral-rich fens on the opposite side of the
axis (Fig. 3). The number of taxa was significantly
correlated with sample scores on the first DCA axis
that reflects main changes in species composition
(Table 4). Abundance did not significantly vary along
both axes. Species richness significantly increased
with decreasing conductivity (r = -0.57, P \ 0.001)
and with increasing TOC (r = 0.60, P \ 0.001). The
number of taxa was lowest in calcareous fens and
Table 2 PCA of 18 explanatory variables
PCA 1 PCA 2 PCA 3 PCA 4
rs rs rs rs
Eigenvalues 0.413 0.143 0.108 0.078
Water chemistry
pH 20.922 -0.004 -0.044 0.149
Conductivity 20.817 -0.025 -0.323 0.049
Fe 0.465* 0.555 -0.127 0.288
Ca2?
20.819 0.199 -0.242 0.179
Mg2?
20.736 0.031 0.142 -0.217
NO3
-
20.758 -0.404 -0.017 -0.008
PO4
3-
0.278 0.071 20.529 0.450*
Substrate
TOC 0.865 0.230 0.148 -0.166
Moisture 0.609 -0.002 -0.466* 0.093
Nutrients -0.246 0.620 -0.042 0.083
D50 20.777 -0.335 0.012 0.118
POM 0.802 0.305 0.078 -0.317
Leaves/wood 20.806 -0.498* -0.285 0.201
Vascular plants 0.323 0.612 -0.183 -0.471*
Brown-mosses 0.099 0.447* 0.662 0.454*
Sphagna 0.721 -0.364 0.057 -0.178
Others
Average discharge 20.606 -0.222 0.342 -0.081
Depth 0.275 0.436 -0.009 -0.287
Eigenvalues of axes and correlations of explanatory variables
with the first four PCA axes (rs) are shown. Significant
correlations at the level of P \ 0.01 are marked by asterisks
and those significant after Bonferroni correction (P \ 0.002)
are in bold
Hydrobiologia
123
Table 3 List of recorded taxa
Names of taxa Calcareous fens (12) Mineral-rich fens (12) Sphagnum-fens (10)
Oligochaeta
Enchytraeidae
Buchholzia sp. 0 0 0.02/1
Cernosvitoviella sp. 0.21/1 0.05/1 0.09/4
Cognettia glandulosa (Michaelsen, 1888) 0.09/1 0.56/3 2.71/7
Cognettia sphagnetorum (Vejdovsky´, 1878) 1.03/3 7.67/5 10.03/10
Enchytraeus albidus Henle, 1837 0 0.05/1 0
Enchytraeus cf. buchholzi Vejdovsky´, 1879 0.15/1 0 0
Enchytraeus spp. 0.96/3 0.38/1 0.19/4
Fridericia spp. 10.22/7 3.19/8 2.91/7
Henlea spp. 1.09/5 0.12/2 0
Marionina argentea (Michaelsen, 1889) 0.04/1 0 0
Marionina sp. 0.10/2 0.27/2 0
Mesenchytraeus armatus (Levinsen, 1884) 0.31/3 1.86/4 0.48/5
Mesenchytraeus sp. 0 0 0.03/5
Stercutus niveus Michaelsen, 1888 0.17/1 0 0
Naididae (sensu Erse´us et al. 2008)
Aulodrilus limnobius Bretscher, 1899 0 0.18/1 0
Limnodrilus udekemianus Clapare`de, 1862 0.05/1 0.88/4 0.14/2
Limnodrilus hoffmeisteri Clapare`de, 1862 0 1.10/5 0.66/3
Nais communis Piguet, 1906 0 0.34/4 1.26/3
Pristina bilobata (Bretscher, 1903) 0 0.23/2 0.43/4
Pristina rosea (Piguet, 1906) 0 0 0.02/1
Rhyacodrilus coccineus (Vejdovsky´, 1875) 0 0 0.05/1
Rhyacodrilus falciformis Bretscher, 1901 0.26/2 1.54/6 0.09/3
Tubifex ignotus (Sˇtolc, 1886) 0 0.05/1 0
Tubifex tubifex (Mu¨ller, 1774) 0.38/3 0.95/1 1.71/3
Tubificidae juv. 0.39/3 1.64/3 1.35/5
Lumbriculidae
Lumbriculus variegatus (Mu¨ller, 1774) 0 4.09/3 12.77/7
Stylodrilus heringianus Clapare`de, 1862 0.09/1 13.64/8 59.88/10
Trichodrilus strandi Hrabeˇ, 1936 77.55/12 8.13/2 0
Lumbricidae
Eisenia fetida (Savigny, 1826) 0 0 0.07/1
Eiseniella tetraedra (Savigny, 1826) 6.41/12 22.67/12 1.52/6
Lumbricidae juv. 0 0 0.06/2
Haplotaxidae
Haplotaxis gordioides (Hartmann, 1821) 0.50/2 0.38/1 0
Hirudinida
Erpobdlellidae
Erpobdella vilnensis (Liskiewicz, 1925) 0 29.62/8 3.54/4
Trochaeta bykowski O¨ rley, 1886 0 0.40/2 0
The average abundance per sample/the frequency in samples are given. Numbers of samples are given in parentheses
Hydrobiologia
123
increased towards Sphagnum-fens. The number of
specimens per sample was significantly correlated
with moisture (r = 0.54, P \ 0.001).
The position of samples from two different
habitats (flowing and almost still water) differed in
the ordination only in the case of calcareous fens,
where sample scores differed significantly on the first
axis (Mann–Whitney U test, P \ 0.05); samples
collected in the higher flowing habitats were situated
on the left part of the DCA diagram. These flowing
water samples were the most species poor of all
samples (highly dominated by T. strandi), probably
because the formation of tufa was the strongest in
these habitats. Samples taken in slow-flowing habitats
had a high portion of enchytraeids and therefore
they were placed along the first axis close to samples
from mineral-rich fens.
Individual effects of two different variable groups
In the CCA, which included all explanatory variables,
conductivity, vascular plants, moisture, TOC,
and PO4
3were
the variables explaining the most
variation in species data (Table 4). It suggested the
importance of both water chemistry and substrate,
although conductivity was the strongest single
predictor of assemblage structure. Flow characteristics
(mean discharge and depth) were not significant
in the model. The variation partitioning revealed
that water chemistry explained slightly more variability
in species data than characteristics of the
substrate did (Fig. 4). Of the 16% of variation
explained by water chemistry alone, 10% was
explained by conductivity and PO4
3.
Moisture
and TOC were responsible for the majority (9%)
of the variability explained by substrate characteristics
(13%). The amount of shared variability (18%)
was higher than each partial effect, showing a strong
correlation between bottom substrate character and
mineral richness. Conductivity, that directly reflects
the mineral richness of water, was significantly
correlated with TOC (rs = -0.73, P \ 0.001), D50
(rs = 0.62, P \ 0.001), and proportions of wood/
leaves and sphagna in the substrate sample
(rs = 0.64 and rs = -0.67, P \ 0.001). Conductivity
was not significantly correlated with vascular
plants (rs = -0.26).
Discussion
Putting aside the widely studied effects of pollution
on clitellates (e.g. Brinkhurst & Cook, 1974; Uzunov
et al., 1988; Lang, 1998), main factors controlling the
species richness and composition of clitellate assemblages
in different freshwater habitats are linked with
substrate composition, organic matter content, food
quality of the organic component, current velocity
(e.g. Montanholi-Martins & Takeda, 1999; Verdonschot,
1999, 2001; Dumnicka, 2006; Syrova´tka et al.,
2009). To date, there have been only two studies
examining the effect of mineral richness of water on
clitellate assemblages (Martı´nez-Ansemil & Collado,
1996; Schenkova´ et al., 2001). Both reported a
significant influence of water mineral richness on
clitellate assemblages on a large geographical scale.
However, the reported patterns showed different
regional diversity of clitellates, partly interfering
with different geology, rather than real effects of
water chemistry. In both studies, some doubt
remained about the direct effect of mineral richness
on aquatic clitellate assemblages.
Our results suggest that both mineral richness and
substrate are important influences of the species
richness and composition of clitellate assemblages in
the Western Carpathian spring fens. Flow conditions
of these sites were less important (Table 4). The
Fig. 2 DCA ordination plot of samples on the first two
ordination axes. Variables that significantly correlated with the
first and the second ordination axes were posteriori plotted.
Classification of investigated sites was based on the vegetation
units: rectangles calcareous fens, circles mineral-rich fens,
triangles Sphagnum-fens
Hydrobiologia
123
influences of both factors were complex, owing to
direct as well as indirect influence of mineral richness
on particular substrate characteristics. The precipitation
of tufa on all submerged objects directly changes
the environment, creating harsh conditions for clitellates.
Thus, the sites with the strongest tufa formation
were the most species poor. The effect of mineral
richness was often indirectly mediated by vegetation,
the structure, and composition of which are strongly
influenced by mineral richness (Ha´jek et al., 2002;
Rozbrojova´ & Ha´jek, 2008). Along the major mineral
richness gradient both the amount and the quality of
organic matter in fen substrates changed (Tables 1,
2), which created different habitat conditions for
species strongly preferring specific substrates.
Species turnover clearly reflected the traits of
species that dominated particular assemblages along
the mineral richness gradient: a stygophilous species,
semiaquatic sediment burrowers, aquatic sediment
burrowers, and surface active species (Fig. 3). A very
rare stygophilous species Trichodrilus strandi (cf.
Dumnicka, 2001) occurred exclusively on tufa-forming
(calcareous) fens and reached high abundance also
in sites with such strong tufa precipitation that the
occurrence of other species was constrained. Tufa
habitats are in direct contact with groundwater due to a
weak formation of peat and stable high inflow of
groundwater (Ha´jkova´ et al., 2004). Further along the
gradient of decreasing mineral richness, weaker tufa
precipitation (leading to its absence) changed
Table 4 Spearman correlations (rs) between explanatory variables and sample scores on the first three DCA axes
DCA CCA
DCA 1 DCA 2 DCA 3 DCA 4 Order in forw. sel. Explained variation
rs rs rs rs % P
Water chemistry
pH 20.780 -0.500* -0.411 0.514 11 3 n.s.
Conductivity 20.837 -0.390 -0.376 0.406 1 21 \0.001
Fe 0.424 0.104 0.014 20.528 10 3 n.s.
Ca2?
20.750 -0.447* -0.316 0.357 8 3 n.s.
Mg2?
20.512 -0.498* -0.386 0.487* 12 2 n.s.
NO3
-
20.612 -0.309 -0.053 0.421 6 4 n.s.
PO4
3-
0.062 0.191 0.395 20.658 5 4 \0.05
Substrate
TOC 0.610 0.410 0.346 -0.411 4 5 \0.01
Moisture 0.195 0.532 0.013 -0.346 3 7 \0.01
Nutrients -0.279 20.610 -0.209 -0.042 7 4 n.s.
D50 20.649 -0.347 -0.110 0.492* 16 1 n.s.
POM 0.623 0.372 0.123 -0.248 13 2 n.s.
Leaves/wood 20.795 -0.164 -0.035 -0.141 16 1 n.s.
Vascular plants 0.371 -0.304 -0.061 -0.313 2 7 \0.01
Brown-mosses 0.166 -0.075 -0.043 0.028 15 2 n.s.
Sphagna 0.501* 0.702 0.108 0.456* 17 1 n.s.
Others
Discharge -0.165 -0.438* -0.461* 0.313 9 4 n.s.
Depth 0.197 -0.139 0.097 0.247 14 2 n.s
Number of species 0.660 0.200 0.247 -0.294 – – –
Number of specimens 0.084 0.410 -0.271 -0.076 – – –
Significant correlations at the level of P \ 0.01 are marked by asterisks and those significant after Bonferroni correction (P \ 0.002)
are in bold. Percentages of species data variance explained by all variables. Orders of variable selection in forward selection in CCA
and the significance (Monte Carlo test) are given
Hydrobiologia
123
assemblage composition towards species not restricted
to surface sediments (mostly Enchytraeidae; Fig. 3).
The wider vertical distribution of enchytraeids is
connected with the ability to penetrate to deeper
sediment layers, especially during periods of drought
and/or higher water temperature, and to inhabit
substrates of variable moisture (e.g. Springett et al.,
1970; Lundkvist, 1982). These sediment-burrowing
species have been reported from sediments in various
freshwater and terrestrial habitats as well. For example,
Cognettia sphagnetorum occurs in coniferous
forest soils (e.g. Lundkvist, 1982; Graefe & Schmelz,
1999; Schlaghamersky´, 2002), as well as in ombrotrophic
and slightly minerotrophic mires (e.g. Erman
& Erman, 1975; van Duinen et al., 2006). Rhyacodrilus
falciformis inhabits mainly different running water
habitats (Juget, 1987), but there were also several
records from terrestrial habitats—moist soils in grasslands,
meadows, and deciduous forests which were not
permanently waterlogged (Graefe & Schmelz, 1999;
Schlaghamersky´ & Kobeticˇova´, 2005). These species
from the middle part of the gradient of mineral
richness are likely not fully confined to the aquatic
environment. In contrast, the end of the mineral
richness gradient was characterised by the dominance
of aquatic sediment burrowers and surface dwellers
(e.g. oligochaetes Limnodrilus hoffmeisteri, Tubifex
tubifex, Stylodrilus heringianus, and a leech Erpobdella
vilnensis) which were not recorded in the previous
fen types or were scarce there.
The species richness of clitellates increased
towards more acidic sites and increasing organic
matter content, which is the opposite pattern than
other organisms strongly responding to the mineral
richness gradient. Species richness of vascular
plants, diatoms, and molluscs increased towards
mineral-rich fens (Ha´jek et al., 2002; Horsa´k &
Ha´jek, 2003; Fra´nkova´ et al., 2009). Chiefly, clitellates
were species-poor at sites where the abovementioned
organisms reach their high or maximal
species diversity. However, it should be stressed that
this study did not include extremely mineral-poor
and permanently acidic sites, simply because they
are not present in the study area. These types of
acidic mires are known to be the most species-poor
due to a low-nutrient availability for clitellates (van
Duinen et al., 2006). If these sites are included, a
skewed unimodal response of clitellate species
richness towards Sphagnum-dominated acidic mires
is expected, because the highly acidic conditions of
bogs were proved to limit the occurrence of many
clitellate species.
Beside mineral richness, the pattern of clitellate
occurrence also reflected different hydrological
regimes and productivity of the fen habitats because
clitellate assemblages were influenced by moisture
and fertility of the substrate (Fig. 2; Table 4). The
seasonal decrease of water level and desiccation of
the upper soil layer causes nutrients to mineralise. For
that reason, the species composition of the vegetation
shifts from sedge-moss dominance to forb-rich vegetation
with plant species that use more nutrients
(Ha´jek et al., 2006; Rozbrojova´ & Ha´jek, 2008).
Fig. 3 Position of species along the first two ordination axes.
Only species with a fit in the model above 10% are shown
Fig. 4 Variation partitioning. Independent and shared variability
of water chemistry and substrate characteristics were
expressed as percentages of the total inertia in partial CCAs.
Only significant variables were included (see Table 2).
Significance of independent variability explained was tested
by the Monte Carlo test
Hydrobiologia
123
Consequently, the formation of peat is lower, and the
structure of organic sediments is different in nutrientenriched
sites. It was observed that these changes
caused the decrease of plant and mollusc fen
specialists and their simultaneous replacement by
ubiquitous species (Ha´jek et al., 2006). In clitellates,
we observed a similar effect with an increase of
eurytopic aquatic species resulting in their dominance
in the assemblage. The species change could be
explained by the influence of different peat amount
and its structure. Nutrient-poor sites (associated with
the presence of sphagna and higher moisture) were
dominated by oligochaete species fed on decomposing
leaves and vegetation (Lumbriculus variegatus;
Moore, 1978; Brinkhurst & Gelder, 1991) and on
older decomposing litter of Eriophorum and Calluna
(Cognettia sphagnetorum; Latter & Howson, 1978).
As these oligochaetes are acidotolerant and reproduce
by fragmentation, they often reach high densities in
nutrient-poor ombrotrophic mires and coniferous
forest soils (Springett & Latter, 1977; Schlaghamersky´,
2002; van Duinen et al., 2006). On the other
hand, nutrient-rich sites were dominated by detritovorous
oligochaetes (Tubificinae and Rhyacodrilinae)
because the higher availability of nutrients leads to
greater production of plant biomass amounts of
decomposing organic matter in than in nutrient-poor
sites.
Conclusion
The results of our study showed the importance of
mineral richness, substrate, and nutrient availability
in constituting the clitellate assemblages in the spring
fens. The effect of water chemistry was roughly
equivalent to the effect of substrate as proportions of
an independent variation in species data explained by
water chemistry and substrate characteristics were
significant and comparable. However, water chemistry
and substrate characteristics are inter-correlated.
This is the result of tufa precipitation in calcareous
fens and vegetation changes along the mineralrichness
gradient, as well as related to seasonal
decrease of water level in some fens. These factors
determined the substrate character by the formation
of peat and the structure of organic sediments. We
also showed that response of species richness to the
same ecological gradient may be reversed for
different taxonomic groups. Contrary to previous
studies on various taxonomic groups in fens, the
species richness of clitellates increased towards more
acid sites owing to more favourable substrate conditions.
Nevertheless, when including the most acidic
sites into the study, a unimodal response could be
expected.
Acknowledgments This study was supported by the Czech
Science Foundation (526/09/H025 and P505/11/0779) and the
Ministry of Education, Youth and Sports (MSM 0021622416).
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147
Růžičková, S., J. Schenková, V. Weissová & J. Helešic, 2014
Environmental impact of heated mining waters on clitellate (Annelida: Clitellata)
assemblages. Biologia, 69(9), 1179–1189.
Biologia 69/9: 1179—1189, 2014
Section Zoology
DOI: 10.2478/s11756-014-0424-2
Environmental impact of heated mining waters on clitellate
(Annelida: Clitellata) assemblages
Sylvie Růžičková, Jana Schenková, Veronika Weissová & Jan Helešic
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137 Brno, Czech Republic;
e-mails: sylvie.ruzickova@gmail.com; schenk@sci.muni.cz; veronika.weissova@centrum.cz; helesic@sci.muni.cz
Abstract: Mining is a relatively highly monitored industry. While chemical pollutants (toxic ions, radionuclides, etc.) have
mostly been eliminated from mining waters, other types of environmental pollution (temperature regime alterations, high
concentrations of various anions, etc.) can affect benthic invertebrates. In this study, we focused on the effect of mining
water effluent on the diversity and density of aquatic Clitellata. Four sampling sites were selected. Three sites in a natural
stream (the Nedvědička River, Czech Republic), one upstream and two downstream from the mining effluent, and one
site on the mining waters were sampled monthly during 2008–2009. Environmental variables were recorded in and samples
were collected from two types of habitats – riffles and pools. The response of clitellate assemblages was evaluated using
principal component analysis and generalised estimating equations. The results indicated that the mining effluent caused
partial species exchange and had negative effects on clitellate taxa richness and abundance. These responses were specific
to both the habitat (riffle/pool) and species sampled. In each of the different taxa studied, we observed one of four typical
clitellate responses: (a) elimination of stenotherm species; (b) reduction of clitellate species followed by quick recovery;
(c) neutral response; or (d) positive influence. We found that aquatic clitellates, which are considered to be eurytopic with
broad ecological valences, are also sensitive to even slight environmental pollution.
Key words: aquatic Clitellata; oligochaeta; thermal pollution; mineralised heated water; pool and riffle habitats
Introduction
Freshwater ecosystems are threatened by various human
activities. Among the strongest reported threats
are alterations of temperature regime and water pollution.
Unlike global climate changes, heated mining
waters can cause a high, stable, and long-term increase
in water temperature, which is often accompanied by
increases in various ion concentrations.
Temperature influences the metabolism and life
history of organisms through its effect on both physical
and chemical processes, and it is a key determinant
of invertebrate community composition in most environments
(Hogg & Williams 1996; Živi´c et al. 2006;
Haidekker & Hering 2008). Thermal water effluent
causes disturbances in the natural state and can lead to
the elimination of stenothermic species and the establishment
of thermophilous species (Nedeau et al. 2003).
The second aspect of mining or general industrial water
inflow is the increase in the concentration of heavy
metals and various ions, which change water pH, conductivity,
and hardness (Maret et al. 2003; Nedeau et
al. 2003; Miliša et al. 2010). The final stress factor for
benthic organisms downstream from the operations is
elevated radiation; radionuclides accumulate primarily
in bottom sediments and can alter the life histories of
benthic invertebrates. However, in common conditions
where radiation doses in the vicinity of a mine are under
local government control, the direct effect on benthic invertebrates
has not yet been shown (Thomas & Liber
2001).
In the Czech Republic, a unique opportunity to
study the environmental impact of heated waters exists
in the Nedvědička River, which is a recipient of
treated mining water from the last underground uranium
mine in Central Europe. Fortunately, the discharge
into the Nedvědička River does not significantly
increase downstream from the effluence, which enables
the study of the effect of only the heated mining water,
without changes in stream morphology. Besides temperature,
mining water differs from stream water in
that it has higher pH, conductivity, and inorganic carbon
values, as well as lower oxygen and nutrient values,
which makes the influence on stream biota more
complex. The concentration of uranium, which is another
chemical variable that could affect benthic invertebrates,
was very low in the Nedvědička River at the
point of the mining water inflow (Unat = 3.4 mg L−1
),
and it decreased rapidly towards the most distant downstream
sampling point (Unat = 0.010 mg L−1
). Both
values were well below 24 mg L−1
, as required by Directive
2008/105/EC of the European Parliament (Hudcová
et al. 2012). As the mutagenicity of the water
sediments analysed by the Ames Test (Ames et al.
1975) was not previously recorded in either the mining
waters or the Nedvědička River (Hudcová et al.
c 2014 Institute of Zoology, Slovak Academy of Sciences
1180 S. Růžičková et al.
2012), this variable was not recorded in the presented
study.
Of the variables we studied, water temperature
was expected to have the greatest effect on local benthic
communities. A moderate increase in water temperature,
similar to those observed in the Nedvědička
River, was tested by Hogg & Williams (1996) on benthic
arthropods. They reported decreases in their densities,
as well as alterations in their life cycles. Other parameters
in our study, pH and oxygen concentration, are
supposed to have a lower impact when altered. In such
cases, when pH varies within a relatively small range
around neutral (6.8–8.9) and oxygen concentrations are
relatively high (6.5–12.2 mg L−1
), their influence on the
composition of the benthic community is not significant
(Quinn & Hickey 1990). In contrast, higher water conductivity,
which reflects an increase in total ionic content,
was associated with decreased invertebrate community
diversity (Batty et al. 2005). Unfortunately, recent
reports on the effects of altered thermal regime
and changes in ion concentration on benthic macroinvertebrates
have focused either on Ephemeroptera, Plecoptera,
and Trichoptera (EPT) taxa (Voelz et al. 1994;
Lakly & McArthur 2000) or on arthropods (Lehmkuhl
1972; Hogg & Williams 1996; Wellborn & Robinson
1996). Even if all components of the benthic community
are considered, clitellates are treated as a single
taxon or its several families (Saltveit et al. 1994; Batty
et al. 2005; Taylor & Dykstra 2005, Miliša et al. 2010),
due to difficulties associated with their identification.
For our study, we selected clitellate (Annelida:
Clitellata) assemblages, as oligochaetous clitellates are
generally considered to be the group of benthic invertebrates
most resistant to various disturbances, although
their sensitivity to disturbances still differs among
species. Oligochaetous clitellates represent a group of
permanent fauna, in which limited mobility is characteristic.
The slow, upstream movement of oligochaetous
clitellates such as Naidinae is accomplished by swimming
or burrowing into the substratum, as is the case
for non-swimming taxa, while their downstream movement
is accomplished by drift (e.g., Cellot & Juget
1998). Once present at a site with altered thermal
regime and water chemistry, they are continually exposed
to the new environment. Forasmuch as clitellate
species exhibit a wide range of ecological valences, including
eurythermic and stenothermic species, their assemblage
composition is likely to respond to thermal
alterations.
Surprisingly, there is no consensus in the literature
with respect to the response of the clitellates to
increased temperature. In running waters, where the
amount of dissolved oxygen is higher due to the continuous
movement, an increase in clitellate density under
an effluent of heated water was recorded, whether the
water was heated naturally (Taylor & Dykstra 2005;
Živi´c et al. 2013) or artificially (Nedeau et al. 2003).
However, in stagnant waters, the diversity of clitellates
was reduced to only a few of the most resistant species
in very low densities (Krodkiewska 2005). Conductivity
has been found to be one of the basic variables that induce
changes in clitellate assemblages, with a decrease
in diversity being caused by increasing conductivity
(Bojková et al. 2011). While results have been recorded
for conductivity resulting from Ca2+
and Mg2+
ion concentration,
there have been no previous reports about
the effect of SO2−
4 ion concentration on clitellate assemblage
changes. Although water mineralisation resulting
from the combination of various inorganic ion concentrations
is known to be a significant variable affecting
the structure of the clitellate community (MartínezAnsemil
& Collado 1996; Schenková et al. 2001), it
is not known if it has a positive or negative effect on
species diversity and density.
The poor understanding of the effect of heated
mineralised water effluence on clitellate assemblages
and their associated species, as well as discrepancies in
reported results regarding the effects (both positive and
negative) of thermal alteration on clitellate diversity
and abundance, led us to propose three null hypotheses.
First, the abundance and taxa richness of clitellates
as a group that generally tolerates environmental pollution
will not be influenced by the input of mining waters.
Second, any changes in clitellate assemblages due
to thermal and chemical alteration will be the same
for pool and riffle assemblages. Third, clitellates, as
a rather uniform group (e.g., feeding strategy, body
shape) of invertebrates, will show no species-specific answer
to thermal and chemical pollution.
Material and methods
Study site
The Nedvědička River is a second order stream with a length
of 28.5 km and an 84.3 km2
catchment area located in
the Bohemian-Moravian Highlands in the Czech Republic.
It runs through the village of Rožná, where uranium has
been mined since 1958. Decontaminated mining water is
used as a coolant in a chemical uranium ore processing plant.
The cooling water is discharged into the Nedvědička River
at 16.9 km from its spring (49◦
28 53 N, 16◦
14 00 E).
To evaluate the clitellate response to heated mining
water, four sampling sites were chosen, three on the Nedvědička
River and one on the mining water tributary. The
first site (US: upstream) is on the Nedvědička River about
200 m upstream from the mining water inflow, the second
site (MW: mining water) is on the mining water, the third
site (DS1: downstream1) is on the Nedvědička River immediately
downstream of this inflow, and the fourth site (DS2:
downstream2) is on the Nedvědička River about 800 m
downstream of the inflow site (Fig. 1). Sampling sites on
the Nedvědička River only (US, DS1, and DS2) are included
in all statistical analyses. The MW samples allowed us to
determine background information about the chemistry of
and the clitellate species pool in the mining water. The mining
water runs in a brook approximately 1.5 m wide with a
substratum composed of gravel in riffles and mud, and sand
and gravel in pools. All sampling sites were well canopied
with Alnus sp., Salix sp., Fraxinus sp., and Sambucus nigra.
Sampling sites DS1, DS2, and MW did not freeze over in
the winter due to the warm water inflow, in contrast to the
US site, which froze to the depth during the winter months.
Clitellata of heated mining waters 1181
Fig. 1. Location of sampling sites.
Species data
Samples of macroinvertebrates were taken monthly from
March 2008 to June 2009 (sampling in January was omitted)
at each of the four sampling sites. Macroinvertebrates
were collected quantitatively using a Hess stream bottom
sampler (0.08 m2
) fitted with a 256-µm-mesh collection net.
Two samples from each of the pools and two from each of
the riffles were pooled separately at each sampling site. A
total of 120 samples were obtained. The collected material
was fixed in 4% formaldehyde in the field. In the laboratory,
the clitellates were sorted and classified by species or genus
level (in the case of juveniles).
Physical and chemical measurements
Basic physicochemical parameters were recorded at each
of the sampling sites (Table 1). For each sampling site,
one value each of conductivity, pH, dissolved oxygen, and
oxygen saturation was measured (HACH HQ40d) during
each monthly sampling in the field. Concentrations of NH+
4 ,
NO−
3 , PO3−
4 (VIS spectrometer HELIOS δ), and SO2−
4 ions
(capillary electrophoresis) and total nitrogen (TN), total
carbon (TC), total inorganic carbon (IC), and total organic
carbon (TOC) (Shimandzu) were measured from each water
sample in the laboratory. During each sampling, two values
for depth, velocity at 40% of the depth from the bottom, and
substrate composition were recorded separately for pools
and riffles. Temperature data loggers were submersed at all
sampling sites, and water temperature was recorded every
15 minutes during the entire sampling period. To evaluate
the hydrodynamic characteristics of the sampling sites, the
Froude number (Fr) was calculated using Fr = U/
√
gD (D:
depth, g: acceleration due to gravity, and U: current velocity
at 0.4 depth). The phi value (Hynes 1970) was used to
evaluate substrate coarseness.
Statistical analyses
Principal component analysis (PCA) was used to search
for the main gradients in the environmental data and to
identify the relationships between the variables. Seasonal
changes in the environmental data were separated from differences
among sampling sites using special covariables that
represented relative seasonality (for details, see Straka et al.
2012). The collected temperature data were scaled by day
and month by means of these values and were used in the
PCA. Environmental data were fitted linearly into the twodimensional
ordination space, and only significant variables
(based on 999 permutations) were shown in the PCA diagram.
Variables (Froude number and phi) related to the
habitats were not included in the PCA because they were
measured twice, for riffles and pools separately, while only
one measurement per sampling site was taken for all the
other variables.
The differences in Froude number and phi among
the specific sampling sites were tested using the Wilcoxon
matched pairs test; habitats were treated separately. The
same test was used to find the differences in physicochemical
variables between US and MW.
PCA was also used to study the relationships between
species composition and explanatory variables. Seasonal
changes in species data were separated from differences
among sampling sites using the same covariables as in
PCA on environmental data (see above). The species data
were log(x + 1) transformed to reduce the undue influence
of dominant species. Samples containing fewer than five individuals
were excluded from the analysis. To explain the
ecological meaning of species data gradients, environmental
variables were fitted linearly into the two-dimensional ordination
space and only significant variables (based on 999
permutations) were shown in the PCA diagram.
Because the samples showed temporal dependence, we
used the generalised estimating equations (GEE) with autoregressive
(AR1) correlation structure and Poisson distribution
to evaluate differences in abundance and taxa richness
between particular sampling sites. The same method
and test was used for testing the mining water effect on
1182 S. Růžičková et al.
Table 1. Minimum, maximum, and median values of the measured environmental variables at sampling sites.
US MW DS1 DS2
Site
Min Median Max Min Median Max Min Median Max Min Median Max
Variable
Conductivity (µS cm−1) 202 318 410 987 1395 1580 400 604 930 415 583 789
pH 7.3 7.6 8.4 7.8 8.2 8.9 7.5 8.0 8.5 7.2 8.0 8.8
Dissolved O2 (mg L−1) 8.7 11.4 12.7 7.6 8.8 10.1 8.1 10.2 12.3 8.2 10.3 12.0
O2 saturation (%) 86 96 118 78 98 116 81 98 120 78 97 119
Mean monthly temperature (◦C) 2.9 11.7 15.4 12.6 17.9 19.9 4.8 13.4 16.4 4.8 13.3 16
Min. monthly temperature (◦C) 0.1 7.4 13.3 8.0 13.5 17.2 1.9 9.1 15.0 1.7 9.0 14.8
Max. monthly temperature (◦C) 5.8 15.0 19.0 18.1 21.2 24.1 7.4 16.8 20.6 7.4 16.3 20.7
NH+
4 (mg L−1) 0.4 0.7 1.6 0.0 0.6 1.6 0.0 0.5 1.1 0.0 0.5 1.3
NO−
3 (mg L−1) 8.6 29.5 41.9 0.4 12.9 30.5 13.8 22.0 41.1 13.6 21.3 41.5
PO3−
4 (mg L−1) 0.0 0.1 0.4 0.0 0.0 0.1 0.0 0.1 0.5 0.0 0.1 0.3
SO2−
4 (mg L−1) 44 48 66 430 500 690 80 170 280 81 145 270
TN (mg L−1) 0.6 7.8 15.5 0.2 1.7 8.4 0.2 6.0 14.6 0.8 5.7 14.6
TC (mg L−1) 11.8 21.3 64.8 16.9 32.8 63.9 12.9 20.5 38.9 12.7 20.5 37.9
IC (mg L−1) 4.4 11.3 23.2 11.2 23.6 46.1 7.6 13.3 27.8 6.4 15.9 27.3
TOC (mg L−1) 3.0 8.7 55.4 0.6 6.6 19.4 1.1 8.2 12.9 1.1 7.8 20.3
phi value (riffles) –7.0 –4.6 –1.7 –7.0 –3.4 –1.7 –7.4 –5.8 –3.2 –7.0 –4.4 –1.3
phi value (pools) –4.4 –0.7 2.4 –4.2 1.4 5.1 –5.1 –1.8 2.0 –4.5 –1.5 4.5
Froude number (riffles) 0.17 0.36 0.70 0.17 0.38 0.70 0.06 0.44 0.89 0.06 0.26 0.51
Froude number (pools) 0.01 0.08 0.17 0.01 0.11 0.17 0.01 0.05 0.12 0.01 0.06 0.14
Explanations: US – unaffected locality upstream from the tributary, MW – heated mining water, DS1 – first influenced locality
downstream from the tributary, DS2 – second influenced locality downstream from the tributary, TN – total amount of nitrogen, TC
– total amount of carbon, IC – amount of inorganic carbon, and TOC – total amount of organic carbon.
six of the most abundant and ecologically important taxa.
All analyses were performed in R (version 2.12.0; R
Development Core Team, 2010) using the ‘vegan’ (Oksanen
et al. 2011) and ‘geepack’ (Hojsgaard et al. 2006) packages.
Results
Environmental data
Mining water differs from water in the Nedvědička
River along several parameters, the most important
of which, for this study, are its elevated water temperature,
higher conductivity, and lower organic pollution
(Table 1). MW differed from the unaffected US
most significantly in water temperature (P < 0.001),
which ranged 8–24◦
C in MW. Heated mining water
caused an average increase of 1.8◦
C in water temperature
in DS1 when compared to US. Differences in temperature
between the downstream sites (DS1 and DS2)
were small (about 0.2◦
C; Fig. 2C). Significantly higher
conductivity (P < 0.001), which reached values above
1,000 µS cm−1
, was caused by increased SO2−
4 ions.
Inorganic carbon and pH were significantly higher in
MW compared to US (P < 0.01), and dissolved oxygen
and nutrients (NO−
3 and PO3−
4 ) were lower (P < 0.01).
Lower organic pollution in mining water (Table 1) was
due to the presence of the decanting plant, which processes
mining water upstream from its inflow into the
Nedvědička River.
Mining water is discharged continuously, without
fluctuation in volume (0.06 m3
s−1
). The Nedvědička
River displayed an unaltered character in the sampled
stretch, with a width of 2.7–3.5 m, a mean discharge
volume of 0.25 m3
s−1
, a mean pool depth ranging from
0.24 m (US) to 0.37 m (DS2), a mean riffle depth ranging
from 0.16 m (DS1) to 0.21 m (DS2), a mean velocity
in pools ranging from 0.12 m s−1
(DS1) to 0.14 m s−1
(US), and a mean velocity in riffles ranging from 0.41
m s−1
(DS2) to 0.54 m s−1
(DS1). Coarse gravel and
gravel were the dominating substratum in riffles, and
gravel and sand were the dominating substratum in
pools. Phi values were similar within particular habitats
(riffle/pool), especially in pools (Fig. 2A). In the
riffles, DS1 had significantly coarser substrate than that
found in DS2 and US (Wilcoxon paired test, P < 0.05).
In the pools, the US Froude number was significantly
higher than in both downstream sites (Fig. 2B). In the
riffles, DS1 had a significantly higher Froude number
when compared to DS2 (P < 0.05), but not when compared
to US.
The main gradients for the environmental data
were identified using PCA. The first PCA axis explained
34.3% of the variance. The main gradient represented
these measured variables (i.e., conductivity, temperature,
pH, and dissolved oxygen), which differed significantly
between the mining water tributary and the
natural water sites on the Nedvědička River. The unaffected
sampling site (US) was well separated from both
affected sites (DS1 and DS2; Fig. 3). The differences
between DS1 and DS2 were small; groups of points
highly overlapped each other in ordination space. The
second PCA axis explained 17% of the variance in the
data and was associated with the amount of nutrients,
specifically, total organic carbon and nitrate ions. General
differences among sampling sites along this nutrient
gradient were small.
Clitellate community
A total of 2,715 individuals representing 44 clitellate
Clitellata of heated mining waters 1183
Fig. 2. Box-plots of environmental variables: phi values (A),
Froude number (B) (habitats considered separately), and measured
temperature (C), lines join daily means. US – site upstream
from the mining water inflow, DS1 – first site downstream from
the mining water inflow, and DS2 – second site downstream from
the mining water inflow.
taxa were collected from the study sites in the Nedvědička
River. The numbers of taxa per sampling site
were 35 from US, 30 from DS1, and 24 from DS2. Total
abundance was 1,710 individuals from US, 279 from
DS1, and 942 from DS2. In the mining water tributary,
1,446 individuals from only 17 taxa were observed.
In PCA based on biological data, the first axis explained
33.9% of the variance (Fig. 4). Although points
of particular sampling sites overlap, the main gradient
in faunal data representing community change along the
extent of sampling site disturbance (from US through
DS2 to DS1) is clearly visible. This gradient was best
expressed by fitted environmental variables: increase of
conductivity, temperature, IC, and pH in the most affected
DS1 on the one side, and higher amount of dissolved
oxygen and organic carbon associated with unaffected
US on the other side. The second gradient, explaining
11.1% of variability, is related to the substrate
coarseness phi.
A comparison among sampling sites (both habitats
evaluated together) in the number of taxa showed
a significant (P < 0.05) decrease downstream from the
tributary (Fig. 5A). However, the difference in number
of taxa between DS1 and DS2 was insignificant.
In addition to detailing the elimination of some taxa
downstream from the effluent, species replacement was
also monitored. Some of the taxa we observed upstream
from the mining water effluent site were replaced either
by new taxa or by taxa coming from the mining waters
(Table 2). In addition, the number of individuals within
each taxa was significantly lower downstream from the
tributary (Fig. 5B) in both DS1 and DS2 (P < 0.05).
Separate evaluations of habitats revealed a significant
decrease in the number of taxa between the
pools in the US and both downstream sites (P < 0.05),
but no difference between DS1 and DS2. The DS1 riffles
had significantly fewer taxa compared to US and
DS2 (P < 0.005); there was no difference between US
and DS2. The number of individuals in pools was significantly
higher in US compared to both DS sites
(P < 0.05); DS1 had significantly fewer individuals
than DS2 (P < 0.05). Similarly, the DS1 riffles had significantly
fewer individuals compared to US and DS2
(P < 0.005), but there was no difference between US
and DS2.
Comparing the habitats (riffles/pools) within sampling
sites showed that they were populated differently
by clitellates. Significantly higher taxa richness in pools
was recorded for DS1 (P < 0.001; Fig. 5A), and significantly
higher abundances in the pools were recorded
for US and DS1 (P < 0.05).
Selected species responses
Genus Stylodrilus was the most abundant taxon found
in the three sample sites on the Nedvědička River
(US, DS1, and DS2), and genus Limnodrilus was the
most abundant in MW (Table 2). Other species that
were prevalent in particular sampling sites include
Haplotaxis gordioides in US, Nais bretscheri in DS1,
and Aulodrilus japonicus in DS2. Three species, Bothrioneurum
vejdovskyanum, Limnodrilus udekemianus,
and Psammoryctides albicola, were found exclusively
in MW. We focused our study on the response to
thermal and chemical alteration of six taxa (Aulodrilus
japonicus, Haplotaxis gordioides, Limnodrilus
spp., Lumbriculus variegatus, Spirosperma ferox, and
1184 S. Růžičková et al.
Fig. 3. PCA ordination plot of environmental variables. Circle – US, square – DS1, triangle – DS2. Black arrows represent fitted
variables. Only significant variables are shown (P < 0.05, based on 999 permutations).
Fig. 4. PCA ordination plot of species data. Samples are displayed. Circle – US, square – DS1, triangle – DS2. Black arrows represent
fitted variables. Only significant variables are shown (P < 0.05, based on 999 permutations).
Clitellata of heated mining waters 1185
Fig. 5. Box-plots of taxa number (A) and logarithmic transformed abundance values (B) for three sampling sites. The habitats were
treated separately. US – site upstream from the mining water inflow, DS1 – first site downstream from the mining water inflow, and
DS2 – second site downstream from the mining water inflow.
Fig. 6. Box-plots of logarithmic transformed abundances of selected species for three sampling sites; habitats treated separately. US
– site upstream from the mining water inflow, DS1 – first site downstream from the mining water inflow, and DS2 – second site
downstream from the mining water inflow.
Stylodrilus spp.) with the highest abundances and
regular occurrences in the sample sites from the
Nedvědička River. We observed four types of responses
by the species to the mining water effluent
(Fig. 6):
I) The decrease in abundance of Haplotaxis gordioides
in both DS sites was significant (P < 0.001).
In addition, this species was nearly eliminated downstream
of the tributary, with only a few occasional occurrences
(Fig. 6A).
1186 S. Růžičková et al.
Table 2. Total number of individuals of clitellate species recorded in sampling sites.
Site US-R US-P MW-R MW-P DS1-R DS1-P DS2-R DS2-P
Name
NAIDINAE
Nais alpina (Sperber, 1948) 3 5
Nais barbata (O.F. M¨uller, 1773) 69 3 8
Nais bretscheri (Michaelsen, 1899) 8 3 21 6 24 19
Nais communis (Piguet, 1906) 3 1 1
Nais elinguis (O.F. M¨uller, 1773) 6 7 3 2 27 2
Nais pseudobtusa (Piguet, 1906) 12 3 2
Nais simplex (Piguet, 1906) 2
Nais sp. juv. 74 23
Nais variabilis (Piguet, 1906) 2
Ophidonais serpentina (O.F. M¨uller, 1773) 2 2 1
Slavina appendiculata (d’Udekem, 1855) 2 1
Uncinais uncinata (Oersted, 1842) 8 5 2
PRISTININAE
Pristina jenkinae (Stephenson, 1932) 1
RHYACODRILINAE
Bothrioneurum vejdovskyanum (Štolc, 1888) 1 25
Rhyacodrilus falciformis (Bretscher, 1901) 5
TUBIFICINAE
Aulodrilus japonicus (Yamaguchi, 1953) 1 17 14 1 75
Aulodrilus limnobius (Bretscher, 1899) 1
Aulodrilus pluriseta (Piguet, 1906) 9 1 3
Limnodrilus claparedeanus (Ratzel, 1869) 15 1 6
Limnodrilus hoffmeisteri (Clapar`ede, 1862) 9 1 439 12 2 9
Limnodrilus udekemianus (Clapar`ede, 1862) 5
Limnodrilus sp. juv. 1 4 6 656 10 3 24
Psammoryctides albicola (Michaelsen, 1901) 2
Psammoryctides barbatus (Grube, 1861) 1 2 2
Spirosperma ferox (Eisen, 1879) 8 26 16 9 50
Tubifex tubifex (O.F. M¨uller, 1774) 2 36 1 15
Tubificidae juv. 1 4 2 153 3 11 53
ENCHYTREIDAE
Cognettia glandulosa (Michaelsen, 1888) 1 1 3
Enchytraeus albidus (Henle, 1837) 1
Enchytraeus sp. 1 1 1
Fridericia sp. 2 2 2 1 1 3
Henlea sp. 1 4 1 2 1
Mesenchytraeus armatus (Levinsen, 1884) 1
PROPAPPIDAE
Propappus volki (Michaelsen, 1922) 32
HAPLOTAXIDAE
Haplotaxis gordioides (Hartmann, 1821) 79 126 3 9 4
LUMBRICIDAE
Eiseniella tetraedra (Savigny, 1826) 5 20 24 6 7 1 4 16
LUMBRICULIDAE
Bythonomus lemani (Grube, 1880) 1
Lumbriculus variegatus (O.F. M¨uller, 1774) 14 46 3 31 1 11 5 26
Stylodrilus brachystylus (Hrabě, 1928) 38 157 4 67 18
Stylodrilus heringianus (Clapar`ede, 1862) 8 13 3
Stylodrilus sp. juv. 156 803 6 5 12 359 84
ERPOBDELLIDAE
Erpobdella octoculata (L., 1758) 2 5 1 3 1
Erpobdella vilnensis (Liskiewicz, 1927) 2 4
Erpobdella sp. juv. 2
GLOSSIPHONIIDAE
Glossiphonia complanata (L., 1758) 1
Glossiphonia concolor (Apathy, 1888) 1
Glossiphonia nebulosa (Kalbe, 1964) 1
Helobdella stagnalis (L., 1758) 1
Total 427 1283 45 1401 131 148 527 415
Explanations: US – site upstream from the mining water inflow, MW – heated mining water inflow, DS1 – first site downstream from
the mining water inflow, DS2 – second site downstream from the mining water inflow, R – riffles, P – pools.
II) While Stylodrilus spp. and Lumbriculus variegatus
abundances decreased in DS1, further downstream
in DS2, they increased again to almost the quantity
found in US (Fig. 6B, C). The decrease of abundance
in DS1 and the increase in DS2 were significant in
both Stylodrilus spp. and Lumbriculus variegatus (P <
0.001). Furthermore, an exchange of preferred habitat
for Stylodrilus spp. was observed. It showed a preference
Clitellata of heated mining waters 1187
for pools in US and DS1, while it showed a preference
for riffles in DS2.
III) A neutral response to the mining water effluent
was observed in two taxa, Spirosperma ferox and
Limnodrilus spp.; abundances in all sampling sites were
almost the same.
IV) An increase of abundance in Aulodrilus japonicus
was observed in the downstream sites (Fig. 6D).
The increase in DS1 and DS2 compared to US was significant
(P < 0.05). A significantly higher abundance in
DS2 compared to DS1 was also observed (P < 0.05).
Discussion
The Clitellata assemblages in this study, represented
mainly by oligochaetes and partly by leeches, proved to
be a good tool for the evaluation of aquatic ecosystem
degradation caused by mineralised and heated mining
water. Their diversity and density strongly reflected the
changes in water environment.
The environmental variables that were altered the
most below the mining water tributary included conductivity,
temperature, pH, IC, and dissolved oxygen
concentration (arranged in order of goodness of fit in
the multivariate analysis), and we assume them to be
responsible for changes in the clitellate assemblage composition.
This assumption was confirmed when we fitted
all environmental variables into a species data ordination
plot. The main gradient of community changes
corresponded with the gradient of environmental variables
altered by MW inflow. There was no opportunity
to segregate the effects of individual variables, but their
combined impact was detectable. A significant decrease
in species richness and abundance below the mining water
tributary was observed (Fig. 4), despite the fact that
clitellates are considered to be the most tolerant group
to various ecological disturbances (e.g., Brinkhurst &
Cook 1974; Uzunov et al. 1988). Contrary to our results,
Nedeau et al. (2003) observed an increased abundance
of oligochaetes and chironomid larvae under heated industrial
effluence, but a simultaneous increase in water
current and resulting changes in the stream morphology
probably affected the results.
Two mechanisms likely explain the negative effect
of mining water input on clitellate assemblages. First,
the effect of changes in water chemistry and the resulting
increase in conductivity causes a clitellate osmoregulation
problem that is balanced by active seeking
of optimal osmotic conditions (Preston 2009) more
distantly downstream. Some species, such as Propappus
volki, show a strong negative correlation with water
hardness, which is often tightly associated with conductivity
(Dumnicka & Pasternak 1978), and we observed
that this species was completely eliminated below the
mining water tributary in our study (Table 2). Osmoregulatory
capacity differs among oligochaete species
(Generlich & Giere 1996), and Propappus volki is probably
highly sensitive to osmotic stress. Second, the effect
of increased water temperature was remarkable. A
small increase (1.8◦
C on average) resulted in water remaining
unfrozen during the winter, a feature to which
cold water species (e.g., Haplotaxis gordioides and Stylodrilus
heringianus; Dumnicka 2000), which naturally
inhabit part of the stream above the tributary, are not
adapted. The drop in their numbers below the tributary
was significant (Fig. 6A, B). Hence, we can reject the
hypothesis that running water clitellates are such a resistant
group of organisms that the mining water input
does not change their densities and taxa richness.
Stream morphology has been reported to be significant
for clitellate distribution (Neadeau et al. 2003),
which was confirmed by evaluating the riffle and pool
samples separately. The clitellate assemblage composition
of each habitat (riffle/pool) was distinctly affected
(Fig. 5). The decrease in the number of taxa
observed downstream from the mining water tributary
was higher in the riffles than in the pools. Six taxa
inhabiting only riffles upstream were excluded downstream
from the tributary, whereas the three taxa inhabiting
pools upstream were excluded downstream
(Table 2). Rheophilous taxa, which often inhabit the
upper parts of streams, for which low nutrients and
higher oxygen content are typical (Schwank 1981), are
often more vulnerable to decreased water quality (Verdonschot
2006). Contrary to our results, an identical
diversity with different qualitative and quantitative
composition was reported in another study below
thermal water inflow for all macroinvertebrates,
with only a decrease in overall abundance being reported
(Živi´c et al. 2006). Nevertheless, the species exchange
as the response to the thermal inflow (Živi´c et al.
2006) was analogous to our results. Similarly, changes
in water chemistry, which are often accompanied by a
higher trophic state, result not in decreased clitellate
species diversity, but in changeover of the proportion
of particular species with different ecological valences
(Krodkiewska & Michalik-Kucharz 2009). We recorded
species exchange below the mining water tributary and
changes in the abundance of particular taxa, but overall,
we observed a decrease in diversity and density. The
reason for this result might be the cumulative effect of
the simultaneous influence of high conductivity and increased
temperature. Nevertheless, all of these changes
were distinct for riffles and pools, and therefore, we can
also reject the hypothesis that species will respond in
the same manner to these changes in different habitats.
In our study, we observed habitat-specific responses of
the clitellates to the various disturbances.
The collective response of the entire clitellate community
to the mining water inflow can be explained
by analysing the responses of particular species to the
changes in their environment. We found that the level
of influence was not the same at the species level.
The elimination of the oligo-stenotherm species
Haplotaxis gordioides, one of the most abundant species
in the upstream site, explains its life strategy as stygobiont,
meaning that it inhabits cool water springs and
small streams (Schwank 1981; Dumnicka 2000). We believe
that the increased water temperature and absence
of winter freezing affected the downstream population
1188 S. Růžičková et al.
negatively. The reduction of Stylodrilus spp. abundance
was due to its preference for higher altitudes and, therefore,
lower temperatures and higher oxygen concentrations
(Dumnicka 2000; Verdonschot 2006). Its quick recovery
is due to its ecological plasticity, expressed by
a broad flow condition valence (Syrovátka et al. 2009).
However, the analogous response of Lumbriculus variegatus
is explained differently, by its preference for lower
pH (Nijboer et al. 2004), which can result in its movement
into parts of the stream with optimal pH values.
Some taxa with broad ecological valence, such as
Limnodrilus spp., were not influenced by changes in environmental
conditions because of their high tolerance
to low oxygen levels, increased temperatures, and high
levels of conductivity caused by sulphate ions (Korn
1963; Dumnicka & Galas 2006). The input of mining
waters was even favourable for Aulodrilus japonicus,
which is intolerant of water pollution (Dumnicka &
Pasternak 1978), especially nutrient loading and higher
conductivity. Therefore, it was found only in small numbers
in the mining water tributary and in riffles and
pools downstream (DS1), but its abundance increased
further downstream (DS2), where it found a compromise
between conductivity and water quality levels.
Other taxa of the 44 recorded clitellates would also
probably fit into one of these strategies, but they were
present in such low numbers that they showed random
distributions.
In contrast to the Nedvědička River, the mining
water assemblages showed distinctly lower species diversity,
comprising a subset of the species recorded in
the other sampling sites (Table 2). Only three species
that inhabited the mining water were excluded from the
other, “better” sites. These species were Bothrioneurum
vejdovskyanum, a rare species preferring either
large rivers or smaller streams in lowlands (Hrabě 1981;
Schenková et al. 2006);Limnodrilus udekemianus, which
prefers organically enriched sites, but not those under
poor conditions (Brinkhurst & Cook 1974); and Psammoryctides
albicola, a lowland stagnant water species
(Hrabě 1981).
To summarize, Clitellate assemblages, similar to
other aquatic invertebrate taxa, are threatened by mining
water pollution. This pollution not only lowers
their diversity and density, but also causes species
changeover. Therefore, analyses of clitellate assemblages
must always be conducted at the species level.
The problem is the exclusivity of the types of disturbances
discussed in this report under natural conditions
and, hence, worse plausibility of their mutual compar-
isons.
Acknowledgements
We would like to thank V. Syrovátka for useful statistical
comments and recommendation, and M. Růžičková and S.
Němejc for their technical assistance. This study was supported
by the grant from the Ministry of Education of the
Czech Republic (MSM 0021622416) and the specific research
of Masaryk University (MUNI/A/0888/2013).
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Received September 4, 2013
Accepted July 27, 2014
159
Schenková, J., M. Bílková & M. Horsák, accepted 27.1.2016
The response of Clitellata (Annelida) to environmental gradients in spring fens. Limnologica.
Accepted Manuscript
Title: The response of Clitellata (Annelida) to environmental
gradients in spring fens
Author: Jana Schenkov´a Martina B´ılkov´a Michal Hors´ak
PII: S0075-9511(16)00009-8
DOI: http://dx.doi.org/doi:10.1016/j.limno.2016.01.004
Reference: LIMNO 25492
To appear in:
Received date: 27-8-2015
Revised date: 18-1-2016
Accepted date: 27-1-2016
Please cite this article as: Schenkov´a, J., B´ilkov´a, M., Hors´ak, M.,The response of
Clitellata (Annelida) to environmental gradients in spring fens, Limnologica (2016),
http://dx.doi.org/10.1016/j.limno.2016.01.004
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The response of Clitellata (Annelida) to environmental gradients in spring fens
Jana Schenková*, Martina Bílková, Michal Horsák
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2,
61137 Brno, Czech Republic
*Corresponding author. Tel.: +420 549496959. E-mail address: schenk@sci.muni.cz
(J. Schenková).
Abstract
Patterns in aquatic Clitellata assemblage composition are known to be driven by several
environmental gradients, with water chemistry and substratum characteristics being
particularly important. In this study we explored 54 isolated spring fens across the eastern
Czech Republic and Slovakia. These fens varied in calcium and magnesium concentrations,
forming a sharp and well defined environmental gradient running from calcium-poor acidic
fens to extremely calcium-rich tufa-forming fens. We found that the main changes in
clitellate species composition were controlled by this gradient, and/or total organic carbon
content, over a wide area, including fen sites differing in other environmental conditions and
historical development. However, this pattern was weakened in sites with a high organic
matter content, which represented a second driver of change in assemblage composition
along with water temperature. Three main types of fens were determined using cluster
analysis based on clitellate assemblage composition. However, only the first type, which
included tufa-forming fens, was found to fit with the previously established spring fen types
based on vegetation (i.e. extremely mineral-rich fens with a tufa, brown-moss mineral-rich
fens, mineral-rich Sphagnum fens and mineral-poor Sphagnum fens). The second clitellate
type included sites with low temperatures and occasional desiccation, while the third type
was characterised by high temperatures and trophy. Using eight environmental predictors,
we were able to significantly explain changes in the population abundances of all 12
common species (i.e. recorded at 15-plus sites). The results from individual species
modelling also suggests that an increase in organic matter content can trigger compositional
shifts towards assemblages of common eurytopic tubificid species. Thus, human-induced
eutrophication and negative changes in spring fen hydrology, mainly drying up, can
represent a serious threat for species-specific assemblages of aquatic clitellates, especially at
alkaline sites due to their isolated and spatially limited nature.
Keywords: Clitellata, spring fens, environmental gradients, indicator species, species
responses
*Manuscript
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1. Introduction
Spring fens represent scattered treeless wetlands fed by groundwater that host
nutrient-limited vegetation (Hájek et al., 2006). Helocrene wetlands are characterised by
highly stable environments, less prone to natural disturbances than other types of aquatic
environments (Lake, 2000). They also tend to include various habitat types, both lotic and
lentic, forming heterogeneous mesohabitat complexes (Lindegaard, 1995). They vary in
water chemistry from calcium-poor acidic fens with a tendency towards ombrotrophy to
extremely calcium-rich tufa-forming fens, thus forming a so called poor-rich gradient
(Malmer, 1986; Hájek et al., 2006). The water chemistry of wetlands is generally extremely
important for clitellates, with very acidic sites inhabited only by asexually reproducing
species (van Duinen et al., 2006), while high mineral richness can favour spring fen
specialists (Bojková et al., 2011). Spring fens also cover a broad variety of substrate types,
known to be one of the most important environmental gradients determining clitellate
species distribution (e.g. Šporka, 1998; Montanholi-Martins and Takeda, 1999; Verdonschot,
2001; Syrovátka et al., 2009).
As existing studies on aquatic clitellate assemblage diversity have shown, their broadscale
patterns can be explained mainly by water chemistry, substrate characteristics and
organic pollution (Martínez-Ansemil and Collado, 1996; Schenková et al., 2001; Nijboer et al.,
2004; Verdonschot, 2006). As such, spring fens seem to be an appropriate model system for
deepening our understanding of the main responses of clitellate assemblages, as well as
individual species responses. Further, there currently exists only limited data dealing with
clitellates in headwater habitats, covering acidic conditions of ombrotrophic peatlands (van
Duinen et al., 2006), bog streams (Smith, 1986; Smith and Kaster, 1986), limnocrene karstic
springs (e.g. Dumnicka, 2006; Mori and Brancelj, 2006) or cave springs (e.g. Dumnicka, 2000;
Achura and Rodriguez, 2008; Achurra et al., 2015). Some studies have explored several
spring fens over a relatively spatially limited area (Erman and Erman, 1975; Bojková et al.,
2011). However, virtually no data exist on clitellate diversity patterns from wetland
headwater habitats over a broader spatial scale. Patterns of response in individual species
have also been mostly neglected. Only a few studies have addressed this topic, exploring a
species response to a single or only a few variables. For instance, organic matter content
(Uzunov et al., 1988), current velocity and substratum (Martínez-Ansemil and Collado, 1996;
Syrovátka et al., 2009), ecological quality, altitude and total phosphorus (Verdonschot, 2006)
and other chemical variables (Timm et al., 2001) have been studied in running waters.
In this study we aim to analyse the effect of water chemistry and physical variables on
the diversity of clitellate assemblages over a large spatial scale using an extensive dataset,
collected from 54 isolated hydrologically uniform fen sites in the Western Carpathians
Mountains (Czech Republic and Slovakia). Low variation in water temperature, as well as
discharge makes water supply across the spring fens comparable (Rádková et al., 2014). We
made sure to explore a high number of sites, covering a wide variety of ecological settings
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along several environmental gradients. The study sites belong to four main types based on
water chemistry and vegetation (Hájek et al., 2006): (i) extremely mineral-rich fens with a
tufa formation dominated by the moss Cratoneuron commutatum, (ii) brown-moss mineralrich
fens without a tufa formation dominated by the moss Drepanocladus revolvens agg., (iii)
mineral-rich Sphagnum fens with calcitolerant Sphagnum species and (iv) mineral-poor
Sphagnum fens dominated by S. recurvum agg. Each of the four spring fen types were spread
throughout the entire study area with none of them locally aggregated. As various groups of
invertebrates are strongly determined by the poor-rich gradient (Testacea: Opravilová &
Hájek, 2006; Mollusca: Horsák & Hájek, 2003; Clitellata: on small scale, Bojková et al., 2011;
Diptera: Omelková et al., 2013), we focused on spring fen clitellate assemblages inhabiting a
large number of localities. Clitellates form neither cases nor solid cuticle structures to
protect their soft and flexible bodies. Therefore, the effect of the calcium and magnesium
concentration gradient is considered to be indirect (Martínez-Ansemil and Collado, 1996).
Nevertheless, we expect to see a different species composition at sites with high inorganic
particles compared to sites dominated by organic materials, such as wood, leaves and
particulate organic matter (Verdonschot, 2001; Bojková et al., 2011). It has been shown that
organic substrate is used by clitellates as a source of food (e.g. Lafont, 1984; Verdonschot,
2006) and can serve as a shelter.
The objectives of this study are to (i) determine the main gradients of clitellate
assemblage composition at isolated fen sites distributed over a broad spatial scale, (ii)
identify the main fen types based on clitellate assemblage composition and compare these
clitellate-based types with the types defined based on chemistry and vegetation and (iii)
determine the habitat preferences of common species using predictive models of species
abundance as a linear function of environmental variable(s).
2. Material and methods
2.1. Study area
The study area was located in the Western Carpathian Mountains of the Czech and
Slovak Republics (Fig. 1), covering an area of 223 km west to east and 74 km north to south.
The area consists of three main parts: the Moravian-Slovakian borderland on flysh bedrock
(i.e. alternating claystone and sandstone layers), the Orava region, which is the eastern
extension of the flysh zone, and the Inner Western Carpathians with geological structures
formed by cores of Paleozoic and crystalline schists overlaid by Mesozoic shale-sandstone
and carbonate lithofacies (Poprawa and Nemčok, 1988; Hájek and Hekera, 2005; Horsák et
al., 2007). This area was selected for this study because of the frequent occurrence of wellpreserved
spring fens with contrasting water chemistry, spanning from calcareous fens to
acidic Sphagnum fens, within each of the three geologically distinct parts.
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Fifty four permanent treeless spring fens, fed by groundwater and developed mostly on
gentle slopes, were chosen for this study to cover as wide a gradient of groundwater
chemistry (pH 3.6–8.4) as possible. The study sites can be classified into four main types
based on water chemistry and vegetation (Hájek et al., 2006): (i) extremely mineral-rich fens
with tufa (25 sites), (ii) mineral-rich fens without tufa (15 sites), (iii) mineral-rich Sphagnum
fens (7 sites) and (iv) mineral-poor Sphagnum fens (7 sites). The uneven representation of
the site types corresponds with the variation in the bedrock chemistry and a high frequency
of alkaline sloping fens. The elevation of the study fens varied from 400 to 800 m a.s.l.
2.2. Field sampling
From 2006 to 2012, samples of aquatic macroinvertebrates were collected in spring and
autumn from each study site. To cover the whole spring fen habitat heterogeneity, samples
from three contrasting mesohabitats were collected at each site. Two types of mesohabitats,
i.e. with flowing and standing water, were sampled from the spring mouth, each from a
quadrate defined by a metal frame (25x25 cm). All the material taken up to the depth of 5
cm was elutriated using a hand net (mesh size 500 µm). A spring brook was the third type of
mesohabitat, sampled using a hand net (mesh size 500 µm) from 10 25x25 cm sampling plots
distributed along an approximately 20 m long stretch starting immediately downwards of
the spring mouth. Altogether, 324 samples were obtained. To cover the whole seasonal and
spatial variability of clitellate assemblages we merged samples from both seasons and from
three mesohabitats into a single sample per site. Samples were preserved by 4%
formaldehyde in situ and clitellates were hand-sorted in the laboratory under a
stereomicroscope and identified after mounting into the Canadian Balsam. For the
identification of oligochaetous clitellates, keys from Hrabě (1954, 1981), Timm (2009), Pižl
(2002) and Schmelz and Collado (2010) were used, and for leeches keys from Neubert and
Nesemann (1999) and Košel (2001) were used. Current taxonomy of clitellates follows Siddall
et al. (2001), Erséus (2005) and Erséus et al. (2008).
2.3. Environmental variables
The following eight variables were established for each study site, as they have already
been proven, or are likely to be, important drivers of aquatic clitellate assemblages and
species population size (Martínez-Ansemil and Collado, 1996; Timm et al., 2001;
Verdonschot, 2001; Verdonschot, 2006; Bojková et al., 2011; Rádková et al., 2014). Water
temperature and dissolved oxygen were measured in the field using portable instruments
(WTW Multi 340i/SET) at each sampling occasion. GPS positions were directly measured in
the field and used to determine mean annual air temperature by using overlays of plot
locations with a digital elevation model and climatic maps, based on Tolasz (2007), in the
ArcGIS 8.3 program (ESRI, 2003). Of the intercorrelated variables altitude and mean annual
air temperature, we selected the latter because of the independence of geographical
position. Water samples for the laboratory analysis of Ca2+
and Mg2+
(combined, Ca+Mg) and
NO3
ion
concentrations were taken in autumn, when the chemistry of spring fens is the
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most stable (Hájek and Hekera, 2004). Total organic carbon (TOC) was measured from a 100
ml sample of substrate (Shimadzu TOC VCPH), which was taken next to the sample of the
clitellates. This variable is closely bound to spring fen type categorisation, reaching only 5%
in extremely mineral-rich fens, but significantly increasing in fens of low mineral content
(poor fens) (Hájek et al., 2002). Substrate samples were collected during the autumn
sampling from a 25x25 cm plot up to the depth of 5 cm. Substrate was collected from
patches adjacent to the plots used for clitellate sampling and reflected the same structural
microhabitat type. Organic matter (ORG) was obtained from substrate samples by elutriation
(Omesová and Helešic, 2004), using a net with a mesh diameter of 100 µm, dried at 80 °C
and weighed. The remaining inorganic substrate was dried at 80 °C and used for the grain
size analysis (Giere, 1993), from which the amount of inorganic particles smaller than 500
µm was determined (INORG) and expressed as a percentage of the total weight of inorganic
matter.
2.4. Statistical analyses
Relationships among explanatory variables were inspected using Spearman correlations
and multi-panel scatter plots. The environmental variables were not found to be highly
intercorrelated (rho<0.50), except for total organic carbon (TOC) and Ca+Mg concentration
(rho=-0.57). These two variables were; however, used as they are likely to constitute
ecologically different responses of clitellate species. Under a high Ca+Mg concentration, in
alkaline sites, a strong precipitation of calcium carbonate notably changes substrate
conditions, while TOC increases in both acidic and productive sites. Descriptive statistics of
the eight explanatory variables used in the statistical analyses are summarised in Table 1.
Principal Coordinate Analysis (PCoA), also known as MDS (Metric Multidimensional
Scaling), on Bray-Curtis distances was used to explore and visualise variation in the species
composition of clitellate assemblages (command “cmdscale” in the “vegan” package).
Species abundances were transformed as y=ln(x+1) prior to the analysis to reduce the effect
of dominant species. The importance of ordination axes was evaluated using a broken-stick
model (Peres-Neto et al., 2003), which is a permutation-based technique comparing the real
eigenvalues of ordination axes with those eigenvalues generated randomly by the model.
Based on this method, only the first and second axes were selected as important and
meaningful for further interpretation of assemblage compositional variances. To associate
the main changes in species composition with the environmental predictors, we used
multiple regressions between the predictors and site scores on the first and second
ordination axes. The significance was tested by 9999 permutations using the “envfit”
function in the “vegan” package. Distance based Redundancy Analysis (dbRDA) using BrayCurtis
distances was performed to test the significance of the effect of each predictor on the
species composition variance and to identify a parsimonious set of environmental predictors
which could account for the maximum variation in the clitellate species data. Forward
selection procedures and Monte Carlo permutation tests with 4999 runs were used.
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Procrustes analysis with 9999 permutations (Gower, 1975; Jackson, 1995) was used to test
the congruence between site scores on the first two PCoA and dbRDA axes.
Cluster analysis, followed by Indicator Species Analysis (Dufréne and Legendre, 1997),
was performed to determine the main types of fens based on clitellate assemblage
composition and to identify the clitellate species characteristics for these fen types. BrayCurtis
dissimilarity on log-transformed abundance data, y=ln(x+1), and Ward’s method were
used for the grouping. Indicator Species Analysis (Dufréne and Legendre, 1997) was
performed using the “multipatt” function from the “indicspecies” package (De Cáceres and
Legendre, 2009), with significance tested using a permutation test with 999 runs. Fen types
determined based on clitellates were compared with the main types of fens defined based
on vegetation (Hájek et al., 2006). Differences in environmental variables among the three
main clitellate types of fens were compared using a one-way ANOVA, and a Tukey post hoc
test (multiple comparison tests) was used to determine the significant differences between
group pairs.
Generalized Linear Models (GLM; McCullagh and Nelder, 1989) with quasi-Poisson
distribution of errors, i.e. corrected for overdispersion, were used to model related clitellate
species abundances as a linear function of the eight environmental variables. Prior to
modelling, we assessed the distribution of all variables to look for potential outliers. We
transformed some of the predictors to straighten up their left-skewed distribution and to
linearise the relationships between response variables and predictors. Ca+Mg, inorganic
particles and total organic carbon were square root transformed, nitrate concentration and
water temperature were transformed by natural logarithm, while the other variables were
kept untransformed. Modelling was performed only for the 12 common species, i.e. those
recorded at 15 or more sampling sites. First, the response of species abundance to eight
predictors was searched visually in case of a potential unimodal response (found only for
Ca+Mg and annual air temperature) we also tested the effect of the quadratic term along
with a linear term, included for all predictors. To find the best model for each species we
used a guided step-wise forward selection with F statistic. We started with a null model and
the predictors were sequentially added into the model and at each step the current model
was tested against a set of more complicated and simpler models. The selection process
stopped once the inclusion of another term did not cause a significant improvement in the
current model and, simultaneously, the omission of any term would lead to a significant
worsening of the model. For all final models we examined residuals for residual patterns
with respect to fitted values and to individual predictors and we also checked residuals for
normality, homogeneity of variance and identified influential observations using Cook’s
distances (Cook, 1977).
All statistical analyses were performed in R (R Core Team, 2014) using the “vegan”
(Oksanen et al., 2011), “PerformanceAnalytics” (Carl and Peterson, 2010) and “indicspecies”
(De Cáceres and Legendre, 2009; De Cáceres, 2013) packages.
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3. Results
3.1. The response of clitellate assemblages to environmental gradients
A total of 34,122 individuals collected from 54 study sites, were assigned to 42 clitellate
taxa (mostly species, except for some genera of the family Enchytraeidae). On average 632
individuals and 13 species were collected per site. The highest abundances were obtained
for Lumbriculidae, in contrast the highest taxa-richness was found for Naididae sensu Erséus
et al. (2008) (Table 2).
Using Principal Coordinate Analysis (PCoA), we observed two main gradients of species
composition variance, which covered 31.1% and 16.0% of the entire variation respectively.
The main compositional change, expressed on the first PCoA axis, was related mainly to the
variation in total organic carbon (TOC) in the substratum and also partly to Ca+Mg
concentration and annual air temperature (Table 3, Fig. 2). Mineral poor Sphagnum fens,
having a high content of poorly decomposed organic matter (recorded as a high TOC), were
occupied by Cognettia glandulosa, Lumbriculus variegatus and Nais communis, plotted in the
right part of the diagram. In contrast, extremely mineral-rich fens with a tufa formation and
very low TOC in the substratum were inhabited by a rich population of Trichodrilus strandi
(left part of the diagram). The second main direction of species compositional variance was
mostly associated with the amount of organic matter vs. inorganic matter and the gradient
of water temperature (Table 3, Fig. 2). Fen sites with a high amount of food and a high water
temperature were plotted in the upper part of the diagram, harbouring rich populations of
generalist species (e.g. Tubifex tubifex and Limnodrilus hoffmeisteri) and predators
(Glossiphonia nebulosa, G. concolor, Erpobdella vilnensis and Haemopis sanguisuga). Several
variables, such as concentration of calcium and magnesium, dissolved oxygen concentration
and mean annual air temperature, expressed almost an equal association to both PCoA axes.
The distance based Redundancy Analysis (dbRDA) showed very similar results as the
PCoA (Table 3), with TOC, Ca+Mg ions and annual air temperature being the most important
environmental predictors of clitellate assemblages. Each of these variables separately
explained more than 10% of the total variance in the species data and two of them were
included in the most parsimonious model in the forward selection (Table 3). The Procrustes
analysis showed a strong significant correlation between the position of samples in the
ordination spaces of the PCoA and dbRDA (Procrustes R=0.854, P<0.001).
3.2. Clitellate assemblage types
Based on the cluster analysis we determined three main types of fens differing in
clitellate assemblage composition (Fig. 3). In the first division, the sites split up into
extremely mineral rich fens with a tufa precipitation (type A) and the other fens (type B and
C). However, the following division reflected more complex environmental differences (Table
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2, Fig. 3). The sites of the type A fens were characterised by high concentrations of Ca+Mg
ions, low TOC and high annual air temperature (Fig. 4) and Trichodrilus strandi was identified
as the indicator of this group. Based on field observations, all these sites were pristine
calcareous fens. Type B included spring fens with cold water and also the lowest
concentration of Ca+Mg ions and intermediate values of TOC (Fig. 2, Fig. 4). Stylodrilus
heringianus was found to be an indicator species of this fen type. This group included both
calcareous fens and the most acidic fens, defined as vegetation type 1-2 and 4. Type C was
the most broad fen type in respect of clitellate distribution, with 12 species characteristic for
this type of fen (Table 2). The sites of this fen type had the highest water temperatures and
were also enriched by organic matter, resulting in significantly lower oxygenation compared
with the other two types (Fig. 4). Their mineral richness was highly variable as they belonged
to all four types defined by vegetation (Fig. 3).
3.3. Environmental preferences of studied species
We succeeded in building a significant model between the abundances of all the 12
dominant species and the eight environmental predictors using a GLM (Table 4). Based on
the final parsimonious model, variables linked with mineral richness gradient (i.e. combined
Ca and Mg concentration and TOC in the substratum) were the most important predictors
for six species. Three of these species (all with a total explained variation >50%) were also
among those species selected based on Indicator Species Analysis as characteristic for one of
the three main fen types defined based on clitellate assemblage composition. The
abundance of these species increased mostly in acidic fens, but Trichodrilus strandi
increased in mineral-rich tufa fens as the indicator of type A. In contrast, Rhyacodrilus
falciformis abundances expressed a unimodal response to concentrations of Ca2+
and Mg2+
.
Water temperature, dissolved oxygen, organic matter and concentration of nitrates were
found to be the main drivers for the other five species. Responses to water temperature
both positively and negatively separated oligostenothermic species, such as Pristina bilobata
and Mesenchytraeus armatus, from those species preferring high temperatures, such as
Tubifex tubifex. Nevertheless, responses to high organic matter were positive not only for
Tubifex tubifex but also for Pristina bilobata populations. The other predictors were less
important in the models, yet significant responses were found in several species, having
both positive and negative effects on individual species abundances.
4. Discussion
4.1. The response of clitellate assemblages to environmental gradients
Based on an extensive dataset of spring fen habitats, distributed over a large spatial
scale and covering a broad ecological variety of spring fens, we found that nutrient limited
ecosystems harbour clitellate assemblages of relatively high species richness, with a total
number of 42 taxa (mostly species) and an average of 13 taxa per sampling site, recorded at
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54 sampling sites. In comparison with other spring ecosystems, the diversity in the studied
spring fens was almost as high as those of the karstic systems in southern Europe, with a
total of 47 species and a range of 2–19 taxa per sampling site (Achura and Rodriguez 2008).
Clitellate diversity in fenland areas and raised bogs appears to be even lower than that of
fens, as Verdonschot (1984) reported 33 species and van Duinen et al. (2006) only 7–13
species in acidic conditions. It seems that spring fens are well utilized by species of
Lumbriculidae, as they reached the highest mean abundances per sampling site in all three
clitellate fen types (Table 2). Trichodrilus strandi dominated in extremely mineral-rich fens
with tufa precipitation, Stylodrilus heringianus dominated in spring fens with cold water and
low Ca+Mg ion concentrations and Lumbriculus variegatus dominated in fens with a high
content of organic carbon in the substratum.
The importance of mineral richness on compositional variation of clitellate assemblages
at spring fens has already been observed in the data collected in the Outer Western
Carpathians (Bojková et al., 2011), which in many cases did not exceed 700 years (Hájková et
al., 2012). However, the distribution of passively dispersing clitellates was found to be highly
influenced by spatial processes, especially among habitat specialists (Milbrink, 1999;
Rádková et al., 2014) and it is likely that there was not enough time for all species to colonise
all the favourable sites studied by Bojková et al. (2011). Therefore, in this study we explored
a higher number of sites located across the entire Western Carpathians, half of which were
older than 2.500 years. There were several sites with continuous development over the
whole Holocene (Horsák et al., 2015). The gradient of mineral richness was still highly
significant for both compositional changes of clitellate assemblages and also for the
responses of individual species. However, the highest predictive power for the overall
variation in assemblage composition was found for TOC in the substratum. This can be
explained by the confounding effect of water chemistry and TOC in the substratum, due to
the accumulation of organic matter in acidic fens (Hájek et al., 2006). Further, several
clitellate species are known to prefer substrate with a high amount of organic matter (e.g.
Uzunov et al., 1988). Along this combined gradient of water chemistry and substrate
characteristics a complete species composition turnover was observed. Acidic fens, i.e. with
a high amount of accumulated organic carbon (TOC) in the sediment, were inhabited mainly
by Lumbriculus variegatus, Cognettia glandulosa, C. sphagnetorum and Nais communis,
which are known as acid-tolerant/acidophilus species (Graefe and Schmelz, 1999; van
Duinen et al., 2006) that feed mainly on plant remains. The opposite end of the gradient is
represented by alkaline sites with assemblages dominated by Trichodrilus strandi, a spring
fen specialist/stygophilous species (Hrabě, 1942; Dumnicka, 2001; Bojková et al., 2011). We
hypothesise that such harsh conditions at these preserved calcareous spring fens with tufa
precipitations can be linked to the reduction of the interstitial spaces. This change has a
negative effect on most oligochaetes (Rundio, 2009), but it is preferred by T. strandi, as it is a
stygophilous species (Dumnicka, 2001) that probably specialised on feeding on
microorganisms associated with a high calcium content (Timm, pers. com.).
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4.2. The clitellate assemblage types
Using the classification of the study sites based on vegetation (Hájek et al., 2006) only
the extremely mineral-rich fens with a tufa formations were fitted with a clitellate
assemblage type. Clitellate type A almost exclusively occurred in extremely mineral-rich fens
with a tufa formation (vegetation type 1), with only three sites containing brown-moss
mineral-rich fens (vegetation type 2). Trichodrilus strandi was proven to be a specialist of
pristine, oligotrophic, cold and highly mineralized spring and underground waters, as it was
found to be a significant indicator of clitellate type A. Similar habitat preferences have
already been reported for this species in the literature (Hrabě, 1981; Juget and Dumnicka,
1986; Giani et al., 2001; Achurra and Rodriguez, 2008; Bojková et al., 2011; Achurra et al.,
2015). This species showed the highest indicator value of all species analysed (Table 2).
Rhyacodrilus falciformis was also associated with type A, though not as an indicator, and is
reported both as a crenophilous stygobiont of running water as well as a soil species
(Schwank, 1981; Juget, 1987; Dumnicka, 2000; Schlaghamerský and Kobetičová, 2005). Such
a relatively wide habitat tolerance can be; however, explained by its unimodal relationship
to Ca+Mg concentrations, combined with a preference for low organic matter (Table 4),
which explained 23.8% of the variance in its abundance data.
The second fen type defined based on clitellate assemblage composition (type B)
included cold water fens with variable concentrations of Ca+Mg ions (Fig. 4). The high
abundance of Stylodrilus heringianus, which was the only indicator species from this fen
type, was explained by Ca+Mg ion concentration, which had a strong negative effect on
population densities. Likewise, Cognettia sphagnetorum is a typical inhabitant of acidic soils
(Graefe and Schmelz, 1999), and acidic wetlands up to ombrotrophic bogs (van Duinen et al.,
2006), and was associated with this fen type. This species strongly and positively responded
to decreases in Ca+Mg concentrations, which explained 47% of the variance in its abundance
data (Table 4). However, another species associated with type B, Mesenchytraeus armatus,
did not show any relationship to the poor-rich gradient and its abundances were predicted
mainly by mean annual temperature, with a preference for colder waters. The other two
dominant clitellate species from type B are characterised by their tolerance to desiccation;
Stylodrilus heringianus prefers habitats with stony substrates and intermittent stream flow
(Nijboer et al., 2004) and Cognettia sphagnetorum is able to survive 20 days of drought,
probably in a desiccation tolerant stage (Maraldo and Holmstrup, 2009). In addition, the
other species associated with this group were either Enchytraeidae (generally soil species) or
semiaquatic species (the leech Trocheta cylindrica). The presence of these species might
suggest an important common environmental feature of the fen sites included into type B,
which is occasional desiccation. This was partly observed in the field, but it was not directly
measured.
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The highest species diversity and highest number of indicator species was associated
with the third clitellate fen type, type C (Table 2). The presence of many generalist species
was in the accordance with low oxygenation, high water temperature, high variability, but
overall high TOC and also highly variable mineral richness. Tubifex tubifex and Limnodrilus
hoffmeisteri, whose dominance can indicate waters with high organic pollution (e.g.
Brinkhurst and Jamieson, 1971; Uzunov et al., 1988), were abundant in sites with either a
high amount of organic matter content or total organic carbon content and nitrate
concentration respectively. Another two indicator species, Lumbriculus variegatus and
Cognettia glandulosa, with 40% and 27% of their variation in abundance explained by TOC
were characteristic for most acidic sites in this group, preferring high water temperatures
and high inorganic substratum respectively. It is worth noting that several sites included in
this group showed vegetation classification favourable for Trichodrilus strandi. However, due
to a human-made increase in organic matter, as a result of horse or cow pasture (indicated
in the field), Trichodrilus strandi was most likely replaced by the eurytopic species Tubifex
tubifex and Limnodrilus hoffmeisteri. Therefore, Tubifex tubifex could have a hypothetical
competitive advantage, and also other eurytopic species, over the habitat specialists. This
might be supported by the fact that eurytopic species did not show any association with
characteristics of microhabitats, such as vegetation or substrate coarseness, if sufficient food
in form of organic matter was available (Prenda and Gallardo, 1992).
To summarise, we confirmed that clitellate distribution is strongly connected with the
gradient of spring fen groundwater chemistry, which remains the same across a large spatial
area including isolated fen sites of highly variable age. Although we expected a significant
imprint of dispersal, based on processed compositional variance (as found by Rádková et al.,
2014), it seems that the effect of environmental conditions is extremely important. Our
study also stresses that pristine and highly endangered spring fen habitats, hosting unique
species-rich clitellate assemblages, can be easily destroyed by an increase in organic matter,
either by human-made eutrophication or also negative changes in hydrological conditions
(Hájek et al., 2006). Our results, based on individual species response modelling, suggest that
these negative alterations in habitat conditions can trigger compositional shifts towards
assemblages of common eurytopic tubificid species. A higher risk is expected for
assemblages of calcareous spring fens, as acidic sites and their surroundings are less suitable
for pasture and require more space, while alkaline fens develop on spatially limited
groundwater outlets.
5. Acknowledgements
We are very grateful to Ondřej Hájek for the preparation of the map. Comments from two
reviewers have considerably improved the quality of the manuscript. This study was
supported by the Czech Science Foundation (P505/11/0779, GA15-15548S and GA16-
03881S) and the Masaryk University (MUNI/A/0788/2013).
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Table 1 Descriptive statistics of environmental variables for the three types of fens (A, B, C;
Fig. 3): Ca+Mg, the sum of concentrations of calcium and magnesium ions in the
groundwater; O2, dissolved oxygen; NO3
,
the amount of nitrate; TOC, total organic carbon;
ORG, total organic matter; INORG, % of inorganic particles smaller than 500 µm from total
weight of the inorganic particles.
Variable MIN MEAN MAX SD MIN MEAN MAX SD MIN MEAN MAX SD
Ca+Mg (mg l-1
) 25.40 70.29 120.60 29.08 4.40 32.27 79.10 21.84 8.50 40.30 101.40 26.86
O2 (mg l-1
) 2.91 6.85 10.00 1.74 2.50 6.85 10.00 1.88 1.43 4.90 7.83 1.70
NO3
(mg
l-1
) <0.01 3.51 12.00 3.65 <0.01 3.83 21.66 5.80 <0.01 1.83 12.64 3.21
TOC (mg l-1
) <0.01 51.58 137.00 43.62 2.12 131.00 266.80 82.48 30.32 169.00 327.40 98.14
ORG (g) 18.65 77.95 129.70 30.61 18.08 71.50 146.50 44.03 33.20 106.20 186.10 35.64
INORG < 500 µm (%) 13.00 33.50 59.00 12.34 11.00 40.44 71.00 14.52 15.00 40.44 53.00 10.49
Water temperature (°C) 8.8 12.9 23.5 3.3 7.7 10.9 15.0 2.0 11.8 14.5 20.2 2.4
Annual temperature (°C) 5.1 6.8 8.3 0.8 4.5 5.8 7.2 0.8 5.2 6.1 7.3 0.6
Type A Type B Type C
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Table 2 List of all recorded taxa arranged according to the results of the Indicator Species
Analysis. The indicator value of a species represents the maximal indicator value of the
species among the three types of fens (A, B, C; Fig. 3). Significant indicator species and P
values are in bold. The assemblage type, with the maximal indicator value, is highlighted in
grey for each of the indicator species. Average abundances per sample from the sites where
the species was found and the number of these sites are shown before and after the slash,
respectively. The total number of study sites for each fen type is given after the slash.
Type A/19 Type B/16 Type C/20
Taxon name Ind. value P
Trichodrilus strandi Hrabě, 1936 0.880 0.001 435.6/18 4/3 50.2/10
Henlea spp. 0.638 0.036 8/16 4.4/14 4.2/6
Eiseniella tetraedra (Savigny, 1826) 0.583 0.731 23.4/18 28.5/15 20.1/18
Rhyacodrilus falciformis Bretscher, 1901 0.528 0.146 12.2/10 4.1/9 9.5/4
Enchytraeus spp. 0.510 0.787 7.5/11 2.4/12 1.5/13
Stylodrilus heringianus Claparède, 1862 0.674 0.004 5.3/9 124.9/15 107.9/19
Cognettia sphagnetorum (Vejdovský, 1878) 0.622 0.080 17.3/9 117.8/14 75/18
Fridericia spp. 0.608 0.207 19.3/15 24/14 5.3/16
Mesenchytraeus armatus (Levinsen, 1884) 0.575 0.331 7.5/13 16.2/13 5.3/14
Henlea perpusilla Friend, 1911 0.410 0.390 2/5 8/5 3/4
Haplotaxis gordioides (Hartmann, 1821) 0.350 0.171 1.5/2 2/3 Trochaeta
cylindrica Örley, 1886 0.338 0.292 1.5/2 3.3/3 2/1
Marionina argentea (Michaelsen, 1889) 0.182 0.746 1/1 1/1 Erpobdella
vilnensis (Liskiewicz, 1925) 0.849 0.001 1.8/5 25/2 48.1/17
Limnodrilus hoffmeisteri Claparède, 1862 0.803 0.001 40.8/9 2.3/3 86.6/18
Lumbriculus variegatus (Müller, 1774) 0.766 0.001 12/6 20.6/11 223.7/18
Tubifex tubifex (Müller, 1774) 0.751 0.001 15.3/15 29.5/8 135.6/19
Cognettia glandulosa (Michaelsen, 1888) 0.694 0.002 6/2 16.2/12 89.5/15
Tubifex ignotus (Štolc, 1886) 0.655 0.002 1/1 - 15.7/9
Nais communis Piguet, 1906 0.650 0.019 2/2 48/11 94.1/15
Aulodrilus limnobius Bretscher, 1899 0.602 0.003 9/1 2/2 48.6/9
Haemopis sanguisuga (Linnaeus, 1758) 0.519 0.012 1/1 - 2.5/6
Cernosvitoviella spp. 0.500 0.338 3.1/7 18.9/7 11.2/11
Glossiphonia concolor (Apáthy, 1888) 0.500 0.004 - - 6.2/5
Pristina bilobata (Bretscher, 1903) 0.496 0.102 2.7/3 13/4 9.2/9
Limnodrilus udekemianus Claparède, 1862 0.462 0.074 5/1 1.5/2 1.7/7
Slavina appendiculata (Udekem, 1855) 0.447 0.036 - - 24/4
Glossiphonia nebulosa Kalbe, 1964 0.500 0.004 - - 4.8/4
Pristina jenkinae (Stephenson, 1931) 0.496 0.102 14.5/4 - 10.6/7
Limnodrilus claparedeanus Ratzel, 1868 0.424 0.077 61/1 - 15.6/5
Rhyacodrilus coccineus (Vejdovský, 1875) 0.402 0.304 12/4 1/1 3/7
Marionina sp. 0.388 0.441 3.4/5 1/2 3.5/6
Pristina aequiseta Bourne, 1891 0.387 0.112 - - 2.7/3
Spirosperma ferox Eisen, 1879 0.387 0.091 - - 28.7/3
Nais variabilis Piguet, 1906 0.332 0.334 - 13/2 5/4
Aulodrilus japonicus Yamaguchi, 1953 0.316 0.319 - - 130/2
Trichodrilus tatrensis Hrabě, 1937 0.316 0.342 - - 7/2
Trichodrilus sp. 0.316 0.342 - - 4.5/2
Mesenchytraeus spp. 0.246 0.786 - 1/2 3.5/2
Helobdella stagnalis (Linnaeus, 1758) 0.246 0.786 - 5/1 4/2
Pristina rosea (Piguet, 1906) 0.228 0.787 - 6/1 3.5/2
Nais bretscheri Michaelsen, 1899 0.217 0.756 4/1 1.5/2
Type of fen based on clitellate assemblage composition
Mean abundances from sites with species occurence
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Table 3
Summary results of the PCoA and dbRDA analyses. Regression coefficients for the multiple
linear regressions for the explanatory variables and the PCoA site scores on the first two axes
(PCoA 1 and 2), explained variation (R2
%) and its significance (P) based on 9999
permutations. Adjusted percentage of explained variation (AdjR2
) in species data by each
variable in separate dbRDA analyses (Gross effects) and in a single dbRDA model that
includes all variables (Pure effects). The order of the variables entering the single dbRDA
model was based on a forward selection procedure (FS). Significance (P) of explained
variation was tested using a Monte Carlo test with 4999 runs. For abbreviations of
environmental variables see Table 1.
PCoA dbRDA
Regression coefficients Explained variability Explained variability in FS
Variable PCoA 1 PCoA 2 R2
(%) P AdjR2
(%) P AdjR2
(%) P Order FS
TOC 1.000 -0.027 54.330 <0.001 18.09 0.005 16.46 0.001 1
Ca+Mg -0.787 0.617 55.210 <0.001 16.62 0.005 5.46 0.001 2
Annual temp. -0.764 0.646 36.610 <0.001 10.28 0.005 n.s. n.s. n.s.
O2 -0.711 -0.703 34.890 <0.001 9.20 0.005 1.89 0.005 4
Water temp. -0.014 1.000 42.230 <0.001 6.98 0.005 4.84 0.001 3
ORG 0.319 0.948 21.880 0.002 3.81 0.015 n.s. n.s. n.s.
NO3 -0.930 -0.367 11.050 0.047 3.79 0.015 n.s. n.s. n.s.
INORG<500 µm 0.507 -0.862 11.610 0.040 2.26 0.045 n.s. n.s. n.s.
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Table 4
Adjusted percentage of variance in the analysed species abundance explained by each
predictor included in the final generalized linear models with Poisson distribution. The gross
effect of the most important predictor for each taxa group (in bold) and the net effects of
the other predictors are listed sequentially and summed up to give the Total. The effect of
the linear term of each predictor and the quadratic term of the combined content of Ca+Mg
and annual temperature are denoted by (+) and (-) for a positive and a negative effect
respectively. Significance: ***, <0.001; **, <0.01; *, <0.05; <0.07 (marginally significant). For
the explanation of predictor abbreviations see Table 1.
Explained variance - pure effects
Total ORG
Stylodrilus heringianus 75.8 72.8 (-)*** 3.0 (-)*
Lumbriculus variegatus 62.8 7.9 (-)** 15.3 (+)*** 39.7 (+)***
Trichodrilus strandi 50.2 19.5 (+)*** 30.7 (+)***
Nais communis 34.7 24.4 (-)** 10.3 (-)**
Cognettia sphagnetorum 47.1 47.1 (-)***
Cognettia glandulosa 42.5 15.7 (+)** 26.9 (+)**
Pristina bilobata 36.8 8.9 (-)** 12.7 (-)* 10.6 (+)** 14.3 (-)**
Mesenchytraeus armatus 32.8 22.9 (-)*** <1.0 n.s. 9.9 (+)*
Tubifex tubifex 27.5 16.6 (+)** 10.9 (+)*
Rhyacodrilus falciformis 23.8 13.2 (+)* 10.6 (-)*
Erpobdella vilnensis 23.3 23.3 (-)**
Limnodrilus hoffmeisteri 17.9 10.2 (+)* 7.7 (+).
NO3 Annual
temp.
Annual
temp.^2Ca+Mg Ca+Mg^2 Water temp. O2 INORG
<500 µm
TOC
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Fig. 1 Location of the study area and sites.
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Fig. 2 PCoA ordination plot of the 54 clitellate assemblages with the position of 15 indicator
species (given in bold) and the eight the frequent species (found at least at 15 sites). Eight
environmental variables were fitted post-hoc into the ordination space of the first and
second axes (all variables had significant fit, P<0.05). The classification of sites is based on
the results of the cluster analyses (Fig. 3): rectangles, type A; circles, type B; triangles, type C.
Abbreviations of taxa–indicators of type A: TriStr, Trichodrilus strandi; HenSpp, Henlea spp.;
indicator of type B: StyHer, Stylodrilus heringianus; indicators of type C: ErpVil, Erpobdella
vilnensis; LimHof, Limnodrilus hoffmeisteri; LumVar, Lumbriculus variegatus; TubTub, Tubifex
tubifex; CogGla, Cognettia glandulosa; TubIgn, Tubifex ignotus; NaiCom, Nais communis;
AulLim, Aulodrilus limnobius; HaeSan, Haemopis sanguisuga; GloCon, Glossiphonia concolor;
SlaApp, Slavina appendiculata; GloNeb, Glossiphonia nebulosa; frequent taxa: CerSpp,
Cernosvitoviella spp.; CogSph, Cognettia sphagnetorum; EisTet, Eiseniella tetraedra; EncSpp,
Enchytraeus spp.; FriSpp, Fridericia spp.; MesArm, Mesenchytraeus armatus; PriBil, Pristina
bilobata; RhyFal, Rhyacodrilus falciformis. For the abbreviations of the environmental
variables see Table 1.
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Fig. 3 Result of the cluster analysis (Bray-Curtis distance, Ward’s method) of the 54 fen sites
based on clitellate assemblages into the three types (A, B, C). Classification of the sites based
on vegetation is shown by different numbers: 1, extremely rich fens with tufa; 2, rich fens
without tufa; 3, mineral-rich Sphagnum fens and 4, mineral-poor Sphagnum fens.
Fig. 4 Variation of five environmental factors among the three types of fens based on
clitellate assemblage composition (see Fig. 3).
mean value, box height indicates
(i.e. 1.5 times the interquartile range at each side), and
letters at the top indicate statistically significant
Tukey post-hoc test, P<0.05).
five environmental factors among the three types of fens based on
clitellate assemblage composition (see Fig. 3). The central line of each box refers to the
indicates the interquartile range, whiskers to the non
(i.e. 1.5 times the interquartile range at each side), and a small cross for
statistically significant differences between the types
five environmental factors among the three types of fens based on
The central line of each box refers to the
the interquartile range, whiskers to the non-outlier range
cross for an outlier. Small
differences between the types (ANOVA and
186
5.2 Druhová diverzita máloštětinatých opaskovců a její změny podél
gradientů prostředí
187
Schenková, J., J. Jarkovský & J. Helešic, 2007
Strategies of coexistence of two species: Erpobdella octoculata and E. vilnensis (Hirudinea:
Erpobdellidae). International Review of Hydrobiology, 92(4–5), 527–538.
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/07/4-508-527
JANA SCHENKOVÁ*, 1
, JIRˇÍ JARKOVSKY´2
and JAN HELESˇIC1
1
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlárˇská 2,
611 37 Brno, Czech Republic; e-mail: schenk@sci.muni.cz
2
Institute of Biostatistics and Analyses, Faculty of Medicine and Faculty of Science,
Masaryk University, Kamenice 126/3, 625 00 Brno, Czech Republic
Strategies of Coexistence of Two Species: Erpobdella octoculata
and E. vilnensis (Hirudinea: Erpobdellidae)
key words: seasonal dynamics, habitat preferences, diet
Abstract
Populations of Erpobdella octoculata and E. vilnensis were studied monthly over two years (May
1999–April 2001) at four sampling points on the river Rokytná (Czech Republic). The water depth and
velocity were measured and the Froude number for each sample was calculated to follow flow conditions
above the bottom. Temporal differences in biomass of the two species were studied by comparing
their wet weights and evaluated by the time series analysis; differences in their diets were evaluated
by gut content analyses. Significantly different hydrodynamic preferences for juvenile and adult
stages of E. octoculata and E. vilnensis were recorded. In E. vilnensis only, an annual cycle was recorded
with a one-month shift of mean weights compared to E. octoculata. This shift, together with the correlation
of the leeches wet weights with their prey sizes and their distinct habitat preferences are suggested
as mechanisms that explain their coexistence.
1. Introduction
The predatory species Erpobdella octoculata (LINNAEUS, 1758) (Hirudinea: Erpobdellidae)
seems to be one of the best-investigated organisms of the bottom fauna across different water
bodies. Its life cycle in stagnant and running waters is completed principally in one (e.g.,
MURPHY and LEARNER, 1982; DALL, 1979, 1983) or, rarely, in two or three years (e.g.,
MANN, 1953; ELLIOTT, 1973). Certain authors recorded both one-year and two-year cycles
but in different localities (ASTON and BROWN, 1975; MALTBY and CALLOW, 1986). Many
studies of the feeding habits of E. octoculata have been undertaken (e.g., YOUNG and IRONMONGER,
1979, 1980; DALL, 1983; TOMAN and DALL, 1997; KUTSCHERA, 2003), because the
prey is swallowed as a whole and remains in the gut for some time almost undamaged. Only
one study of Erpobdella vilnensis LISKIEWICZ, 1927 (former E. monostriata GEDROYC´), has
been published (MANOLELI, 1976). This species probably has a similar life strategy to
E. octoculata but is less common. In most populations of E. vilnensis, a one year cycle was
recorded with only few breedings in their second year.
The goal of our study was to reveal the mechanisms enabling the coexistence of E. octoculata
and E. vilnensis populations. These species are of similar size and weight, feed on
similar prey and are commonly found together in Czech streams. Competition for space was
assessed by the habitat preferences of individual juveniles and adults of the two species.
From the environmental variables recorded, we selected those which regulate the reproducInternat.
Rev. Hydrobiol. 92 2007 4–5 527–538
DOI: 10.1002/iroh.200610992
* Corresponding author
tion of leeches. The life cycles of E. octoculata and E. vilnensis, based on recording the
leeches wet weights, were compared and their synchronisation estimated. The food niches
were evaluated by the analysis of the leeches’ gut contents and by comparing the composition,
abundance and size of the prey.
2. Methods
2.1. Study Area
The study stream was the Rokytná (6th
order) which has a length of 89.3 km and a catchment area
of 585.4 km2
. It runs through an upland area in the southern part of the Czech Republic. In this area
the climate is warm and dry with a moderate winter and a mean annual temperature of 8 °C. During the
study period, the mean annual discharge varied from 1.0 to 1.3 m3
s–1
, with winter and summer floods.
The maximum discharge reached 24.3 m3
s–1
and the minimum was 0.08 m3
s–1
. The bottom substratum
consisting of small pebbles, gravel, and sand, was rather unstable, especially in meandering reaches. In
January and February, the river was frozen down to the bottom, in spring the substratum was colonized
by periphytic algae and in summer the stream was completely shaded and the water was highly turbid
because of organic pollution (ß-mesosaprobity). No macrophytes were observed on the river bottom during
the course of study year.
2.2. Sampling and Laboratory Methods
Four habitats in the River Rokytná were chosen with different hydrological characteristics and substratum.
These were situated on two cross-sections, A and B, 60 m distant (for details of sampling see
SCHENKOVÁ and HELESˇIC, 2006). The first sampling point was on cross-section A in the straight part of
the stream, here called A streamline (AS). In this part of the stream the substratum did not shift and did
not form gravel bars. The three remaining sampling points were on cross-section B in the meandering
part of the stream, here called B littoral (BL), B gravel bar (BG), B streamline (BS). At each sampling
point, quantitative macro-invertebrate samples were taken monthly from May 1999 to April 2001,
except for a two-month interval in winter. Samples were collected using a triangular sampling device
(HELAN et al., 1973) with an area of 0.1 m2
and a mesh size 500 µm.
Due to the unstable substratum on cross-section B, we did not evaluate preference of leeches for particular
sampling points but for particular hydrodynamic conditions. The values of Froude number (Fr)
were computed for each sample from water velocity and depth using the formula Fr = U¯/÷
–
g D, where
U¯ is mean current velocity, g is acceleration due to gravity and D is total water depth (DAVIS and BARMUTA,
1989). The Froude number as a descriptor of the main channel flow represents the ratio of inertial
forces to gravitational forces. The critical value of Fr is that at which the flow is changing from
tranquil to broken and turbulent. Samples were divided into four categories according to their Fr values.
Categories three and four were subsequently combined because of some anomalies with category
four samples (Table 1 shows the respective categories 1–3). From the environmental variables recorded
– water temperature, velocity, depth, discharge, pH, conductivity and biochemical oxygen demand
(Table 2) – we aimed to select those that regulate the life cycles of leeches.
Macrozoobenthos samples were fixed in the field using 4% formaldehyde. Samples were sorted and
leeches removed in the laboratory. These were stored in 70% ethanol and identified to species (Table 3).
E. octoculata and E. vilnensis represented the eudominant Hirudinea species. Adults of both species can
528 J. SCHENKOVÁ et al.
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Table 1. Categories of Froude number values.
Fr 0–0.3 0.31–0.6 0.61–0.9 0.91–1.23
Category 1 2 3
be identified by the position of their male and female ducts but juveniles only by colour. As result of
fixation with formaldehyde, the clitellum could not be observed (MURPHY and LEARNER, 1982). In
E. octoculata dark spots cover the whole dorsal part, while E. vilnensis has a light median stripe without
any spots. The smallest stages were colourless when fixed and their identification, unfortunately, was
impossible. All leeches of the two species were weighed to the nearest 0.01 mg after 15 minutes of drying.
According to their wet weights they were divided into six weight categories on a common logarithmic
scale (Table 4).
Strategies of Coexistence 529
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Table 2. Environmental variables recorded 1999–2001.
Variable Min. Max. Mean Median
Water temperature [°C] –0.2 19.4 11.0 13.0
Current velocity at 40% of depth [m s–1
] 0.00 1.46 0.67 0.68
Depth [m] 0.10 0.47 0.22 0.20
Mean daily discharge [m3
s–1
] 0.13 3.95 1.36 1.08
pH 4.4 9.0 7.6 7.7
Conductivity [µS cm–1
] 453 725 615 615
BOD [mg l–1
] 1.9 15.8 5.4 4.5
Table 3. List of Hirudinea species recorded.
List of Hirudinea species
Erpobdella octoculata juv. 315
Erpobdella octoculata ad. 49
Erpobdella vilnesis juv. 152
Erpobdella vilnesis ad. 191
Erpobdella spp. juv. 61
Glossiphonia complanata juv. 4
Glossiphonia concolor juv. 4
Glossiphonia nebulosa juv. 1
Piscicola geometra juv. 6
Helobdella stagnalis juv. 2
Hemiclepsis marginata juv. 1
Total 786
Table 4. E. octoculata and E. vilnensis wet weight categories, maximal, minimal and mean
prey width. Category 1 prey widths were not analysed in this study.
Weight Limits of wet Erpobdella octoculata Erpobdella vilnensis
category weight [g] Mean width Min. – Max. Mean width Min.–Max.
[µm] width [µm] [µm] width [µm]
1 0.0001–0.0003 – – – –
2 0.00031–0.001 172.0 129.5–220.4 190.3 132.5–248.0
3 0.00101–0.003 189.7 78.0–310.0 219.9 102.1–456.6
4 0.00301–0.01 210.8 76.2–616.2 245.4 103.4–676.2
5 0.01001–0.03 247.3 53.6–1021 321.9 104.2–673.0
6 0.03001–0.1 284.4 149.8–516.0 291.3 158.1–558.3
After being weighed, the gut contents of 48 individuals of E. octoculata and 51 of E. vilnensis were
examined. We selected leeches from all sampling months within the year 2000. These included specimens
from all weight categories except category one, which was too small for gut examination
(Table 4). The gut contents were obtained by cutting their ventral parts and removing prey items under
a stereomicroscope. Whole or fragments of invertebrates were identified to the most precise acheivable
level in glycerine-water (1:5 solution) under an upright microscope. The head capsules widths of insects
530 J. SCHENKOVÁ et al.
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Table 5. List of the prey taxa and their abundances from the analysed guts of E. octoculata
and E. vilnensis.
Taxon E. octoculata E. vilnensis
Oligochaeta
Bothrioneurum vejdovskyanum 2
Bythonomus lemani 3
Chaetogaster diastrophus 1
Limnodrilus spp. juv. 26 17
Nais alpina 1 1
N. bretscheri 5 1
N. communis 3 1
N. elinguis 9 7
Potamothrix hammoniensis 1
Psammoryctides barbatus 9 14
Rhyacodrilinae, with hair chetae 6
Rhyacodrilus coccineus 2
Stylodrilus spp. juv. 33 9
Tubifex tubifex 1
Tubificidae indet. 8
Crustacea
Gammarus roeselii 1
Ephemeroptera
Baetis rhodani 3 2
Trichoptera
Hydroptila sp. 1
Chironomidae
Chironomini gen. sp. 1
Eukiefferiella spp. 2 3
Micropsectra sp. 1 1
Microtendipes gr. pedellus 1
Nanocladius parvulus/rectinervis 1
Orthocladiinae gen. sp. 10 10
Orthocladius sp. 2
Parametriocnemus stylatus 1
Prodiamesa olivacea 1
Rheocricotopus chalybeatus 4 2
Rheotanytarsus sp. 2 3
Tanypodinae gen. sp. 1
Tanytarsus brundini/curticornis 1
Chironomidae indet. 2 1
unidentified taxa 7 5
empty gut 10 18
number of prey items 118 84
number of leeches analysed 48 51
mean number of prey items per ind. 3.8 3.3
and the mean body widths of other taxonomic groups (at least three measurements) were measured
under the microscope and recorded. When more than one fragment of a taxon was recorded, especially
for oligochaetes, we distinguished different individuals by their widths or, if this was not possible,
by counting only fragments with prostomial parts.
2.3. Statistical Methods
Seasonal changes of Fr number values were tested by auto-correlations for all particular habitats (AS,
BL, BG and BS) and no significant cyclic changes were found. The total trend of Fr number values was
evaluated by Daniel’s test (in fact Spearman correlation against their order) and no significant trend was
found either for total data (P = 0.718) or for particular habitats AS: P = 0.283, BL: P = 0.083, BG:
P = 0.351, BS: P = 0.117. Therefore samples from habitats were treated as independent and habitat preferences
of adults and juveniles of E. octoculata and E. vilnensis in places with different hydrodynamic
conditions were evaluated by chi square test. The null hypothesis, of equal distribution between habitats
represented by categories of Fr number, was rejected at the 5% significance level.
The relationships between the mean abundances of leeches and mean environmental variables were
computed by cross-correlation (BOX and JENKINS, 1970). The goal was to find correlations of values of
environmental variables with abundances, shifted in time, and to compute the lag between changes of
these values and the response in terms of the abundance of leeches.
Seasonal dynamics for both species were evaluated by time series analysis of the mean abundance
of leeches, after first excluding the extremely abundant samples from May 1999. Moving average
smoothing was applied for visualisation of the time series. The number of cycles per year and, thus, the
length of the cycle were evaluated by spectrum (Furier) analysis of seasonality (SHUMWAY, 1988).
Food niches of both species and their overlap were tested by Bray-Curtis Similarity Index (BRAY and
CURTIS, 1957), which was applied to invertebrate taxa found in leech guts (Table 5). The previous finding
that, in E. octoculata, the size of prey is positively correlated with the leeche’s wet weight (i.e.
YOUNG and IRONMONGER, 1979; DALL, 1983) was tested for both Erpobdella species by the Spearman
rank correlation coefficient (rs). Statistica 7 for Windows (STATSOFT, 2004) was used for all analyses.
3. Results
3.1. Habitat Preferences
In total, 786 individuals of eight Hirudinea species belonging to the orders Pharyngobdellida
and Rhynchobdellida were recorded in samples (Table 3). In this study, 315 juveniles
and 49 adults of E. octoculata and 152 juveniles and 191 adults of E. vilnensis were
recorded. As already mentioned, 61 individuals could not be identified to species and were,
therefore, excluded from all analyses.
Significantly different habitat preferences were found by the chi square test: juveniles of
E. octoculata preferred either the lowest flow (category 1, Fr 0–0.3) or the highest (category
3, Fr 0.6–1.23), juveniles of E. vilnensis preferred the middle flow (category 2, Fr
0.31–0.6). Densities of adults of E. octoculata increased significantly towards the lower
flow. No significant preferences of E. vilnensis adults were found.
3.2. Seasonal Dynamics
The life cycle of E. vilnensis was regulated by physical parameters of the environment.
The cross-correlations showed significant relationships with temperature, water depth and
velocity with the three-month shift. Seasonal changes in densities of both species, after curve
smoothing, are shown in Figure 1. While the densities of E. vilnesis followed significant,
Strategies of Coexistence 531
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
regular cyclic changes, the differences in densities of E. octoculata were not significant. The
same results were obtained by periodograms of both species (Fig. 2). Furier’s analysis
revealed approximately a one year cycle for E. vilnensis. The cross-correlation analysis of
temporal changes of mean wet weights revealed a one-month shift of E. octoculata weights
against E. vilnensis (Fig. 1). Therefore the two species differed in weight at any time of the
year. The mean monthly increase in wet weight was 0.0064 g for E. octoculata but only
0.0037 g for E. vilnensis, so that the difference in their size increased during their develop-
ment.
The life cycle of each species was visualised by frequency histograms of the mean densities
of juvenile and adult leeches in each of six weight classes. End of year classes were
estimated and marked (Fig. 3). The end of each year generation enabled three distinct gen-
532 J. SCHENKOVÁ et al.
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Plot of selected variables (series)
6/7/99
7/15/99
7/21/99
8/3/99
9/7/99
10/7/99
12/2/99
2/17/00
3/29/00
4/12/00
5/10/00
6/7/00
7/12/00
8/9/00
9/6/00
10/4/00
12/7/00
2/7/01
3/14/01
4/14/01
Erpobdella octoculata; trns. Erpobdella vilnesis; trns.
-5
0
5
10
15
20
25
30
35
meannumberofleeches[ind0.1m
-2
]
Figure 1. Seasonal changes in mean densities (a) and mean wet weights (b) of E. vilnensis and
E. octoculata.
a)
b) Plot of selected variables (series)
6/7/99
7/15/99
7/21/99
8/3/99
9/7/99
10/7/99
12/2/99
2/17/00
3/29/00
4/12/00
5/10/00
6/7/00
7/12/00
8/9/00
9/6/00
10/4/00
12/7/00
2/7/01
3/14/01
4/14/01
Erpobdella octoculata; trns. Erpobdella vilnensis; trns.
0.000
0.002
0.004
0.006
0.008
0.010
0.012
0.014
wetweight[g]
erations to be distinguished: year class 1998 (individuals born in 1998 and dying in spring
and summer 1999), year class 1999 and year class 2000. Mean wet weights of distinct yearclasses
are given for E. octoculata (Fig. 4) and E. vilnensis (Fig. 5). Though a one-year life
cycle for the latter species was not confirmed by spectral analysis, all adults died after breeding
and hence the reproduction was probably also annual.
Strategies of Coexistence 533
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Spectral analysis: Erpobdella octoculata
No. of cases: 20
1 2 3 4
frequency
0
100
200
300
400
500
periodogramvalues
Spectral analysis: Erpobdella vilnesis
No. of cases: 20
1 2 3 4
frequency
0
100
200
300
400
500
periodogramvalues
Figure 2. Periodograms of E. octoculata (a) and E. vilnensis (b).
a)
b)
534 J. SCHENKOVÁ et al.
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Figure 3. Frequency histograms of mean densities of E. octoculata and E. vilnensis. For ranges of
weight categories see Table 4. Black arrows indicate the borders between year classes.
Strategies of Coexistence 535
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Erpobdella octoculata
Median; Whisker: 25%-75%
class 1998
class 1999
class 2000
May-1999
Jun-1999
Jul-1999
Sep-1999
Oct-1999
Dec-1999
Feb-2000
Apr-2000
May-2000
Jun-2000
Jul-2000
Aug-2000
Sep-2000
Oct-2000
Dec-2000
Feb-2001
Mar-2001
Apr-2001
month
0.000
0.005
0.010
0.015
0.020
0.025
0.030
weight[mg]
Figure 4. Mean densities (with 25 and 75% quartile) of the 1998, 1999 and 2000 year-classes of
E. octoculata during the study period.
Erpobdella vilnensis
Median; Whisker: 25%-75%
class 1998
class 1999
class 2000
May-1999
Jun-1999
Jul-1999
Sep-1999
Oct-1999
Dec-1999
Feb-2000
Apr-2000
May-2000
Jun-2000
Jul-2000
Aug-2000
Sep-2000
Oct-2000
Dec-2000
Feb-2001
Mar-2001
Apr-2001
month
0.000
0.005
0.010
0.015
0.020
0.025
0.030
weight[mg]
Figure 5. Mean densities (with 25 and 75% quartile) of the 1998, 1999 and 2000 year-classes of E. vilnensis
during the study period.
3.3. Gut Content Analysis
In the guts of 48 individuals of E. octoculata and 51 individuals of E. vilnensis, we identified
202 individual specimens of invertebrate of 15 taxa of Oligochaeta, 14 of Chironomidae
and a single taxon each of Crustacea, Ephemeroptera and Trichoptera (Table 5).
Oligochaeta and Chironomidae were the dominant components of the food. A Bray-Curtis
similarity index was computed and the food composition of the two species had a high similarity
of 83.7%. E. octoculata was adjudged to be more effective at hunting because the
percentage of leeches with empty guts was higher for E. vilnensis (21.0%) than for E. octoculata
(8.4%). However, the mean number of prey per leech was similar 3.8 for E. octoculata
and 3.3 for E. vilnensis (leeches with empty guts not included). A significant Spearman
correlation between mean wet weight leeches and their prey size was recorded for both
E. octoculata, rs = 0.507 and E. vilnensis, rs = 0.519 at a significance level of 0.05. Figure 6
shows the increase in prey size with four leech weight categories; the fifth category (the
biggest leeches) was omitted because of low sample size. The size of E. vilnensis prey
seemed to increase more rapidly than that of E. octoculata.
4. Discussion
The present study of the coexistence of two sympatric populations of E. octoculata and
E. vilnensis revealed a complex of mechanisms enabling them successfully utilise the same
food niche. Based on time series analyses, no evidence of cyclic changes in densities were
confirmed for E. octoculata and none of the environmental variables tested were shown to
influence its life cycle. According to ASTON and BROWN (1975) breeding is regulated by a
day-length. In our study, E. octoculata seemed to have an annual cycle, as previously record-
536 J. SCHENKOVÁ et al.
© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com
Median; Whisker: 25%-75%
Erpobdella octoculata
Erpobdella vilnensis
<0.001 0.001-0.003 0.003-0.01 >0.01
w eight [mg]
120
140
160
180
200
220
240
260
280
300
320
340
360
380
400
preysize
Figure 6. Mean prey size for individual weight categories of E. octoculata and E. vilnensis.
ed by DALL (1983). However, the duration of our study was too short to confirm this. On
the other hand the annual life cycle of E. vilnensis, as previously recorded by MANOLELI
(1976), was confirmed, with reproduction significantly stimulated by changes of water temperature,
depth and velocity. Increasing temperature in early spring, together with high discharges,
trigged the development of the leeches clitella, followed by copulation and the
deposition of cocoons. The hatching time was approximately the same in both species –
juveniles occurred during July, but the mean wet weights of new-born leeches were slightly
higher in E. octoculata and increasing more rapidly than for E. vilnensis. Juvenile
E. octoculata were more successful in hunting the prey and they chose habitats with very
low or very high flow, which probably increased the variability of the food on offer. This
could have caused the one-month shift in the wet weights of the two species, which is another
mechanism lowering food competition. DALL (1979) observed similar behaviour in sympatric
populations of E. octoculata and E. testacea (SAVIGNY, 1822) but he recorded that
reproduction of E. testacea began a month earlier. We found that the size of the leeches’
prey is weight-specific (DALL, 1983) in both species. The analysis of leech gut contents
showed that their main food was comprised of Oligochaeta and Chironomidae, with an 83%
similarity in the taxonspecies composition of their diets which means that they were not
selective feeders. Two different life strategies of reproduction were observed. E. octoculata
as a typical r-strategist produced a huge number of juveniles with high mortality. In all samples
combined, juveniles represented 87% of individuals captured. For E. octoculata, high
fecundity (juveniles per adult) was typical. More than half of the specimens of E. vilnensis
found were adults and this would remain so even if all unidentified juveniles were of this
species. In the conditions pertaining in our study, E. vilnensis, produced less juveniles than
E. octoculata. Hence, E. vilnensis must have had a lower mortality resulting in low fecundity
for this species. We also observed rapid sexual development of E. vilnensis. Specimens
of E. vilnensis were also recorded in the winter months when individuals of E. octoculata
were hidden in bottom substratum, suggesting that E. vilnensis is better adapted to running
waters conditions.
In general, the life strategy of E. octoculata is based upon high cocoon production and
high food source utilisation, but also on high mortality of juveniles. In contrast, E. vilnensis
produces lower numbers of cocoons, its juveniles hunt for prey preferentially in mid-current
conditions, but with lower success, and its all-year mortality is small. As a result, populations
of the two species are able to co-exist to good effect.
5. Acknowledgements
We would like to thank our colleague V. SYROVÁTKA for identifying representatives of the family
Chironomidae and J. GAISLER and M. FURSE for checking the language and other improvements. The
project was supported by Long-term Research Plans from the Ministry of Education, Youth and Sports
of the Czech Republic (MSM0021622416 and INCHEMBIOL MSM0021622412).
6. References
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octoculata (L.) in a polluted river warmed by condenser effluents. – Hydrobiologia 47: 347–366.
BRAY, J. R. and J. T. CURTIS, 1957: An ordination of the upland forest communities of southern Wisconsin.
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Holden Day. 553 pp.
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DALL, P. C., 1979: Ecology and production of the leeches Erpobdella octoculata L. and Erpobdella testacea
SAV. in Lake Esrom, Denmark. – Arch. Hydrobiol./Suppl. 57: 188–220.
DALL, P. C., 1983: The natural feeding and resource partitioning of Erpodella octoculata L. and
Erpodella testacea SAV. in Lake Esrom, Denmark. – Int. Revue ges. Hydrobiol. 68: 473–500.
DAVIS, J. A. and L. A. BARMUTA, 1989: An ecologically useful classification of mean and near-bed
flows in streams and rivers. – Freshw. Biol. 21: 271–282.
ELLIOTT, J. M., 1973: The life cycle and production of the leech Erpobdella octoculata (L.) (Hirudinea:
Erpobdellidae) in a lake district stream. – J. Anim. Ecol. 42: 437–450.
HELAN, J., F. KUBÍČEK, B. LOSOS, E. SEDLÁK and M. ZELINKA, 1973: Production conditions in the trout
brooks of the Beskydy Mountains. – Folia Biologia. Univ. J. E. Purkyně, Brno, 105 pp.
KUTSCHERA, U., 2003: The feeding strategies of the leech Erpobdella octoculata (L.): A laboratory
study. – Internat. Rev. Hydrobiol. 88: 94–101.
MALTBY, L. and P. CALOW, 1986: Intraspecific life-history variation in Erpobdella octoculata
(Hirudinea: Erpobdellidae). II. Testing theory on the evolution of semelparity and iteroparity. – J.
Anim. Ecol. 55: 739–750.
MANN, K. H., 1953: The life history of Erpobdella octoculata (LINNAEUS, 1758). – J. Anim. Ecol. 22:
199–207.
MANOLELI, D., 1976: Ecological and biological observation on the species Erpobdella monostriata
(GODROYC, 1916). PAWLOWSKI, 1948 (Hirudinea, Erpobdellidae). – Trav. Mus. Hist. nat. “Gr. Antipa”
17: 1–8.
MURPHY, P. M. and M. A. LEARNER, 1982: The life history and production of the leech Erpobdella
octoculata (Hirudinea Erpobdellidae) in the River Ely, South Wales. – J. Anim. Ecol. 51: 57–67.
SCHENKOVÁ, J. and J. HELESˇIC, 2006: Habitat preferences of aquatic Oligochaeta (Annelida) in the
Rokytná River, Czech Republic – a small highland stream. – Hydrobiologia 564: 117–126.
SHUMWAY, R. H., 1988: Applied statistical time series analysis. – Englewood Cliffs, NJ: Prentice Hall.
STATSOFT, Inc. 2004: STATISTICA (data analysis software system), version 7. – www.statsoft.com.
TOMAN, M. J. and P. C. DALL, 1997: The diet of Erpobdella octoculata (Hirudinea: Erpobdellidae) in
two Danish lowland streams. – Arch. Hydrobiol. 140: 549–563.
YOUNG, J. O. and J. W. IRONMONGER, 1979: The natural diet of Erpobdella octoculata (L.) (Hirudinea:
Erpobdellidae) in British lakes. – Arch. Hydrobiol. 87: 483–503.
YOUNG, J. O. and J. W. IRONMONGER, 1980: A laboratory study of three species of leeches occuring in
British lakes. – Hydrobiologia. 68: 209–215.
Manuscript received March 17th, 2006; revised February 5th, 2007; accepted May 23rd, 2007
538 J. SCHENKOVÁ et al.
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200
Schenková, J., J. Sychra, V. Košel, N. Kubová & J. Horecký, 2009
Freshwater leeches (Annelida: Clitellata: Hirudinida) of the Czech Republic (Central Europe):
check-list, new records, and remarks on species distributions. Zootaxa, 2227, 32–52.
Accepted by B. Sket: 17 Aug. 2009; published: 10 Sep. 200932
ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN 1175-5334 (online edition)Copyright © 2009 · Magnolia Press
Zootaxa 2227: 32–52 (2009)
www.mapress.com/zootaxa/ Article
Freshwater leeches (Annelida: Clitellata: Hirudinida) of the Czech Republic
(Central Europe): check-list, new records, and remarks on species distributions
JANA SCHENKOVÁ1
, JAN SYCHRA1
, VLADIMÍR KOŠEL2
, NELA KUBOVÁ1
& JAKUB HORECKÝ3
1
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic.
E-mail: schenk@sci.muni.cz; dubovec@seznam.cz; Kubova.Nela@seznam.cz
2
Department of Zoology, Faculty of Science, Comenius University, Mlynská dolina B-1, 84215 Bratislava, Slovakia.
E-mail: kosel@fns.uniba.sk
3
Povodí Vltavy, s. p., Na Hutmance 5a, 158 00 Praha, Czech Republic. E-mail: horecky@centrum.cz
Abstract
Freshwater leeches (Annelida: Clitellata: Hirudinida) of the Czech Republic were studied on the basis of recent
literature, information in selected databases, and results of recent surveys conducted by the authors. The objectives of
this study were to summarize recent taxonomic information, and to update the check-list of leeches using records
collected during an eleven-year study (1998 through 2008). Altogether, twenty-four species representing 12 genera and
five families are reported for the Czech Republic, including the first reports of Piscicola cf. haranti Jarry, 1960 and Dina
punctata Johansson, 1927 for the country. A detailed description of the distributions of rare species and characterization
of localities from which they are reported are presented. Plausible modes of dispersal and propagation of species in
Central Europe are discussed.
According to recent records, leech species are divided into three groups: indigenous species with stable and strong
populations (12 species), indigenous species with weak populations known from a limited number of localities (9
species), and species only recently recorded in the Czech Republic (3 species). For scarce or rare species, a category of
threat in the Czech Republic according to the International Union for Conservation of Nature is recommended. Most of
threatened species are inhabitants of lowland wetlands and lowland larger rivers—habitats that are negatively impacted,
often catastrophically, by human activities throughout Central Europe. The protection of suitable habitats is the most
effective way to protect extant populations of endangered leech species. Six species of leeches are recommended for
permanent addition to the Red list of threatened species in the Czech Republic.
Key words: Annelida, Clitellata, Hirudinida, leeches, Glossiphoniidae, Piscicolidae, Haemopidae, Hirudinidae,
Erpobdellidae, Czech Republic, IUCN, Red List, habitat, distribution, Piscicola cf. haranti, Dina punctata, first record
Introduction
A check-list of freshwater leeches (Hirudinida) of the Czech Republic has long been in need of revision.
Available information on the distribution, taxonomy, and ecology of leeches in the Czech Republic has been
scattered throughout various historical as well as recent papers, but none of these have focused on the
country’s fauna as a whole.
Based on molecular phylogeny, leeches (Hirudinida), Branchiobdellida, and Acanthobdellida form a
monophyletic clade—with its common ancestor being an oligochaetous clitellate related to the family
Lumbriculidae (Siddall et al. 2001, Erséus 2005). While most leeches in the Czech Republic are
thermophilous freshwater species inhabiting stagnant as well as running waters, a few species are considered
to be amphibious. Leeches are common in eutrophic waters and often serve as indicators of pollution (e.g.,
Sládeček & Košel 1984, Košel 1988, Grosser et al. 2001, Koperski 2005). Although some of them have been
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Zootaxa 2227 © 2009 Magnolia Press · 33CHECK-LIST OF HIRUDINIDA OF THE CZECH REPUBLIC
studied extensively, (e.g., the medicinal leech, Hirudo medicinalis Linnaeus, 1758), research focusing on the
taxonomy and ecology of leeches occurring in the Czech Republic has been limited.
Several noteworthy papers presenting distributional information on leeches in the Czech Republic have
been published over the last 55 years: Hrabě (1954) recorded eleven leech species in his key to fauna; Švec
(1960) found only six species during a faunal study of southeastern Moravia, but one was a new record
(Alboglossiphonia hyalina (O. F. Müller 1774)—considered as a “form” at the time of Švec’s publication);
Lucký & Dyk (1964) recorded four species of leeches during their study of fish parasites in rivers and ponds
in Odra (Oder) and Dyje (Thaya) River catchment area, including a new record of Piscicola fasciata Kollar,
1842 (as Cystobranchus fasciatus Brumpt, 1900) for the Czech Republic; and Koubková & Vojtková (1973)
reported eleven species in their publication on the fauna of the Czechoslovak Socialist Republic. More
recently, Košel (1998 and 1999a) recorded nineteen and twenty species, respectively (Table 1). Unfortunately,
the record of P. fasciata was not included in the check-list (Košel 1998). Although, most of these papers were
published in the Czech or Slovak language, none provided a thorough review of the leech fauna known or
thought likely to occur in the country.
The objectives of this study are to summarize historical, recently published, and unpublished records of
leeches occurring in the Czech Republic, to present data resulting from our recently completed surveys for
leeches throughout the country (1998–2008), and to provide a current check-list of Hirudinida occurring in the
Czech Republic.
Methods and materials
The information and data summarized herein have been obtained from following sources: recent literature
records (Košel 1999a, Sukop 2004, Košel & Beran 2006); records in PERLA, a database prepared for the
assessment of running waters in the Czech Republic (Kokeš et al. 2006); records in a database of monitoring
of running waters provided by the T. G. Masaryk Water Research Institute (monitoring of reference
conditions, surveillance monitoring, Project Labe (Elbe) (Horecký et al. 2004), research projects and others);
records obtained during the monitoring of Hirudo medicinalis carried out by the authors and organized by the
Agency for Nature Conservation and Landscape Protection of the Czech Republic 2005–2008; records and
information included in the diploma thesis of N. Kubová (Kubová 2008); and data resulting from recent
collections by the authors, colleagues, and other personnel.
1. Košel (1999a), Sukop (2004), Košel & Beran (2006), Kubová (2008) and authors collected leeches with
tweezers and with hand strainers (mesh size 1 mm) from solid submerged inorganic and organic substratum,
e.g., gravel, stones, woody debris and vegetation. Leeches were then narcotized by graduating concentration
of ethanol to final 70%, and then fixed in 4% formaldehyde.
2. PERLA database and monitoring of running waters (1998–2008). Leeches were collected with a hand
net (mesh size 500 µm) during a 3-minute kick sampling period from running waters. All habitats (e.g., riffle,
pool, macrophytes, and woody debris) were sampled proportionally. Leeches were then fixed in 4%
formaldehyde.
3. Project Labe (1999–2005). Leeches were collected during a 3-min kick sampling period using a hand
net (mesh size 500 µm), which was supplemented by qualitative sampling from submerged substratum and insitu
picking of individuals from additional material taken by hand net during extended sampling and sorting
procedure. Samples were preserved in 80% ethanol.
All leech specimens collected by these methods were identified in a laboratory under a stereomicroscope
according to the keys of Neubert & Nesemann (1999) and Košel (2001).
4. Monitoring of Hirudo medicinalis (2005–2008). Specimens were collected by hand, removing from
both gumboots (waders) or from the bare legs of the collectors.
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Maps noting the distributions of leeches in the Czech Republic (with Bohemia to the west, and Moravia to
the east, see Figure 1) were prepared for most species discussed in this paper, with the exception of those
commonly collected throughout the country.
FIGURE 1. The geographical position of the Czech Republic in central Europe, including historical divisions within the
country—Bohemia (Čechy) to the west, and Moravia (Morava) to the east.
Unpublished records of selected species are presented in the accounts, below, and (if available) include
the following information associated with specimens: name of the water body, name of the settlement (town,
village, city) closest to the site from which the specimen(s) was/were collected, index number [in brackets] of
Central European map square (Pruner & Míka 1996) on which the collection site can be found, latitude and
longitude coordinates for the collecting site, name(s) of the person(s) who collected and/or identified the
species (collectors’ names, abbreviated in the accounts below), and date of collection. Published records are
presented in the same way, and include a valid citation. Typical habitats and species distribution in the Czech
Republic are briefly described. For scarce or rare species, a category of threat in the Czech Republic
according to the International Union for Conservation of Nature (IUCN) (1994) is recommended.
Abbreviations for the names of collectors associated with the species accounts presented below: A—
anonymous, EP—Eva Podborská, FK—František Kubíček, GČ—Gašpar Čamlík, IS—Ivan Skála, JB—
Jindřiška Bojková, JH—Jakub Horecký, JK—Jiří Kroča, JP—Jiří Procházka, JR—Jan Rucki, JSc—Jana
Schenková, JSy—Jan Sychra, JŠ—Jan Špaček, KK—Kateřina Kolářová, MB—Milan Boukal, ML—Marek
Liška, MS—Michal Straka, MŠ—Monika Štambergová, NK—Nela Kubová, NL—Natália Lapšanská, PK—
Petr Komzák, PP—Petr Pařil, SV—Stanislav Větříček, VK—Vladimír Košel.
Results and species accounts
In total, twenty-four species of Hirudinida representing five families (Table 1) are now reported to occur in the
Czech Republic based upon records in the literature and/or specimens collected during our eleven-year study
(1998 through 2008). Detailed accounts for leeches occurring in the Czech Republic are presented below.
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Zootaxa 2227 © 2009 Magnolia Press · 35CHECK-LIST OF HIRUDINIDA OF THE CZECH REPUBLIC
TABLE 1. Historical lists of leeches (Annelida, Clitellata, Hirudinida) and a new check-list of Hirudinida occurring in
the Czech Republic, based upon published and unpublished records, and specimens from collections by the authors
during the years 1998 through 2008.
Phylum: Annelida
Class: Clitellata
Order: Hirudinida
Hrab
ě
(1954),
Koubková&
Vojtková
(1973)
Švec(1960)
Lucký&
Dyk(1964)
Košel(1998)
Košel
(1999a)
thisstudy
(1998–2008)
Family: Glossiphoniidae
Alboglossiphonia heteroclita (Linnaeus, 1761) + + + +
Alboglossiphonia hyalina (O. F. Müller, 1774) + + +
Alboglossiphonia striata (Apáthy, 1888) + +
Batracobdella paludosa (Carena, 1824) misidentified
Glossiphonia complanata (Linnaeus, 1758) + + + +
Glossiphonia concolor (Apáthy, 1888) + + +
Glossiphonia nebulosa Kalbe, 1964 + + +
Glossiphonia slovaca (Košel, 1973) + + +
Helobdella stagnalis (Linnaeus, 1758) + + + + +
Hemiclepsis marginata (O. F. Müller, 1774) + + + + +
Theromyzon tessulatum (O. F. Müller, 1774) + + + +
Family: Piscicolidae
Caspiobdella fadejewi (Epshtein, 1961) + + +
Piscicola geometra (Linnaeus, 1758) + + + + + +
Piscicola cf. haranti Jarry, 1960 +
Piscicola fasciata Kollar, 1842 +
Piscicola respirans Troschel, 1850 + + +
Family: Haemopidae
Haemopis sanguisuga (Linnaeus, 1758) + + + + +
Family: Hirudinidae
Hirudo medicinalis Linnaeus, 1758 + + + +
Family: Erpobdellidae
Dina lineata (O.F. Müller, 1774) + + + + +
Dina punctata Johansson, 1927 +
Erpobdella nigricollis (Brandes, 1900) + + +
Erpobdella octoculata (Linnaeus, 1758) + + + + +
Erpobdella testacea (Savigny, 1822) + + + +
Erpobdella vilnensis (Liskiewicz, 1925) + + +
Trocheta cylindrica Örley, 1886 + + +
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Family: Glossiphoniidae
Alboglossiphonia heteroclita (Linnaeus, 1761)
Habitats and status: The species prefers lowland vegetated pools or slow running waters with riparian
vegetation. Because of both morphological and genetic differences, two new species—A. hyalina and A.
striata —were recently separated from this taxon (Trontelj 1997, Neubert & Nesemann 1999). Unfortunately,
only some of the older records are distinguished into forms ‘heteroclita’, ‘hyalina’ and ‘striata’, thus it is not
possible to separate their habitat preferences at this time. Alboglossiphonia heteroclita seems to be the most
common species occurring in the whole territory of the Czech Republic except at higher elevations (only
rarely over 500 m a.s.l.).
Alboglossiphonia hyalina (O. F. Müller, 1774)
Records: Chabařovice artifical lake, Chabařovice [5349], 50°39'05''N / 13°57'11''E, lgt. JŠ, det. JŠ (2005,
2006); concrete fire reserve, Jestřebice [5553], 50°27'49"N / 14°34'36"E (Košel & Beran 2006); Harasov
Pond, Janova Ves [5553] 50°24'43"N / 14°34'18"E, (Košel & Beran 2006); irrigation ditch, Rakvice [7166],
48°49'45''N / 16°48'58''E, (Košel 1999a); Kutnar Pond, Rakvice [7166], 48°50'11''N / 16°47'34''E, lgt. NK,
det. NK (2008); Milotický Pond, Milotice [7068], 48°57'52"N / 17°09'17"E, lgt. JSy, det. JSy (2008);
Štěpánek pond, Pozďatín [6762], 49°13'26"N / 16°02'19"E, lgt. JSy (2006), det. JSy (2008); Tužínský Brook,
Dřevěnice [5558], 50°26'33"N / 15°27'14"E, lgt. JŠ, det. JŠ (2008) (Figure 2).
Habitats: The species was found in heterogeneous stagnant or slow-running waters, often of artificial
origin, and all rich in organic material. The presence of submerged vegetation and aquatic snails also seems to
be important.
Status: Alboglossiphonia hyalina is a rare species with only few localities from southern Moravia, CzechMoravian
Highland and northern Bohemia. These records suggest that this leech is probably more common in
suitable habitats, most likely overlooked in previous collections due to its small size and translucent body.
Alboglossiphonia striata (Apáthy, 1888)
Records: Bažinka Pool, Lanžhot [7367], 48°38'05''N / 16°55'55''E, lgt. JSc, det. JSc (2006); pool, Ranšpurk
[7367], 48°40'27''N / 16°56'23''E, (Košel 1999a) (Figure 2).
Habitats: The species was recorded in natural lowland pools with aquatic vegetation. Its ecology is still
not well known.
Status: Alboglossiphonia striata is the rarest species in the genus known to occur in the Czech Republic,
to date having been recorded only in southernmost Moravia. However, it could have been confused with or
misidentified as A. heteroclita in previous studies.
Glossiphonia complanata (Linnaeus, 1758)
Habitats and status: Glossiphonia complanata represents a widely distributed species recorded from all
kinds of water bodies, stagnant as well as running, with the exception of fast flowing mountain rivers and
brooks. It is common throughout the Czech Republic. In past studies, this species was likely confused with or
misidentified as one or more other Glossiphonia species because of its variable coloration.
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Zootaxa 2227 © 2009 Magnolia Press · 37CHECK-LIST OF HIRUDINIDA OF THE CZECH REPUBLIC
FIGURE 2. The distribution of selected leech species (Annelida, Clitellata, Hirudinida: the families Glossiphoniidae and
Piscicolidae) in the Czech Republic recorded during the years 1998 through 2008, based upon published and unpublished
records, and specimens collected during this study.
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Glossiphonia concolor (Apáthy, 1888)
Records: Bílina River, Bílina [5448], 50°33'17"N / 13°46'25"E, lgt. JSy, det. JSy (2007); Bílina River,
Kozlíky [5355], 50°36'41"N / 13°52'59"E, lgt. JSy, det. JSy (2007); Bílina River, Lbín [5349], 50°36'20"N /
13°51'32"E, lgt. JSy, det. JSy (2007); Bílina River, Stadice [5349], 50°37'08"N / 13°58'02"E, lgt. JSy, det. JSy
(2007); Bílina River, Ústí nad Labem [5350], 50°39'27"N / 14°02'28"E, lgt. A, det. NK (2006); Blanice River,
Nový Mlýn [6255], 49°46'40"N / 14°55'53"E, lgt. A, det. FK (1998); Blažejovický Brook, Blažejovice
[6357], 49°36'46"N / 15°12'19"E, lgt. JH, NL, det. ML (2007); Bolíkovský Brook, Heřmaneč [6857],
49°07'07"N / 15°18'24"E, lgt. A, det. JSc (2007); Břevnický Brook, Břevnice [6359], 49°38'01"N /
15°35'36"E, lgt. A, det. FK (1998); Častava Brook, Chomoutov [7369], 49°37'54"N / 17°13'59"E, lgt. JSy,
det. JSy (2008); Čechtický Brook, Křivsoudov [6356], 49°38'26"N / 15°04'40"E, lgt. JH, NL, det. JH (2007);
Černý Brook, Meclov [6443], 49°30'36"N / 12°53'16"E, lgt. A, det. FK (1999); Dlažkovice Pond, Dlažkovice
[5549], 50°27'53''N / 13°58'02''E, lgt. NK, det. NK (2007); Dolní Bartošovický Pond, Bartošovice [6374],
49°40'52"N / 18°01'45"E, lgt. JSy, det. JSy (2005); Harasov Pond, Janova Ves [5553], (Košel & Beran 2006);
Hranečník Pond, Častotice [6762], 49°14'03"N / 16°04'24"E, lgt. JSy, NK, JSc, det. JSc (2008); Jihlava River,
Vladislav [6761], 49°12'24"N / 15°59'49"E, lgt. A, det. NK (2006); Káča Brook, Hořátev [5856], 50°08'33"N
/ 15°02'25"E, lgt. A, det. JSy (2006); Kozárovický Brook, Zálezlice [5652], 50°18'35"N / 14°25'29"E, lgt. A,
det. JSy (2006); Křišťanovický Pond, Křišťanovice [7049], 48°58'05"N / 13°56'45"E, lgt. JSy, det. JSy
(2007); Lišanský Brook, Rakovník [5948], 50°05'35"N / 13°45'06"E, lgt. JH, NL, det. JH (2007); Morava
River, Nové Zámky [6268], 49°42'58"N / 17°01'28"E, lgt. A, det. JSc (2007); Nový Častotický Pond,
Častotice [6762], 49°14'09"N / 16°05'57"E, lgt. JSy, det. PP (2002), lgt. NK, JSc, JSy, det. JSc (2008); Odra
River, Petřvaldík [6274], 49°43'30''N / 18°07'53''E, lgt. PK, SV, det. JSc (2007); Panenská Pool, Nové Mlýny
[7166], 48°50'41''N / 16°43'40''E, (Košel 1999a); Ploužnický Brook, Ploužnice pod Ralskem [5354],
50°38'10"N / 14°48'30"E, lgt. A, det. JSy (2006); Podhrázský Pond, Lkáň [5549], 50°26'55''N / 13°56'57''E,
lgt. NK, det. NK (2007); Pstružný Brook, Františkodol [6358], 49°39'22''N / 15°22'58''E, lgt. PK, SV, det. FK,
JSc (1998, 2007); Rakovec Brook, Hrušky [6867], 49°07'44"N / 16°50'24"E, lgt. PK, det. PK (2007); Rokytná
River, Moravský Krumlov [6963], 49°03'45"N / 16°19'31"E, (Schenková et al. 2007); Rokytná River,
Vémyslice [6963], 49°02'06''N / 16°11'47''E, lgt. PK, SV, det. JSc (2007); Řečička Brook, Jindřichův Hradec
[6856], 49°07'22"N / 15°00'02"E, lgt. JH, NL, det. JH (2007); Sázava River, Sázava [6155], 49°53'09"N /
14°52'26"E, lgt. A, det. FK (1998); Sázava River, Soběšín [6255], 49°47'55"N / 14°57'19"E, lgt. A, det. FK
(1998); Sázava River, Vlastějovice [6257], 49°44'07"N / 15°10'45"E, lgt. A, det. FK (1998); Sázavka River,
Sázavka [6258], 49°44'11"N / 15°23'15"E, lgt. A, det. FK (1998); Sekulská Morava (Morava River dead arm),
Lanžhot [7367], 48°37'39"N / 16°57'12"E, lgt. JSy, NK, JSc, det. JSy (2008); Skalička Brook, Práče [7163],
48°53'03"N / 16°12'56"E, lgt. SV, PK, det. PK (2007); Střela River, Žlutice [5944], 50°05'45"N / 13°04'11"E,
lgt. A, det. FK (1999); Šatava River, Nosislav [7065], 48°59'33"N / 16°38'48"E, lgt. A, det. JSy (2006);
Únětický Brook, Únětice [5852], 50°08'56"N / 14°21'33"E, lgt. JH, NL, det. JH (2007); Úslava River,
Vilémov [6447], 49°32'40"N / 13°36'08"E, lgt. A, det. FK (1999); Úslava River, Zdemyslice [6447],
49°35'58"N / 13°31'51"E, lgt. A, det. FK (2000); Vlára River, Svatý Štěpán [6974], 49°03'18''N / 18°01'19''E,
lgt. PK, SV, det. JSc (2007); Vltava River, Praha [5952], 50°03'21"N / 14°24'60"E, lgt. JH, NL, det. JH (2002,
2005), Vltava River, Zelčín [5652], 50°19'09"N / 14°23'56"E, lgt. JH, NL, det. JH (2002); Vsetínská Bečva
River, Bystřička [6573], 49°25'09''N / 17°57'10''E, lgt. PK, SV, det. JSc (2007) (Figure 2).
Habitats: Glossiphonia concolor prefers especially stagnant waters or slowly running rivers or brooks. It
occurs mainly in lowlands and moderate elevations (150–500 m, rarely up to 750 m a.s.l.).
Status: Glossiphonia concolor can be locally abundant. With the exception of the boundary mountain
areas, G. concolor is distributed throughout the entire Czech Republic.
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Glossiphonia nebulosa Kalbe, 1964
Records: Bačovka Brook, Velký Osek [5957], 50°05'43"N / 15°12'46"E, lgt. A, det. JSy (2006); Bílina River,
Bílina [5448], 50°33'17"N / 13°46'25"E, lgt. JSy, det. JSy (2007); Brodečka River, Víceměřice [6669],
49°20'35"N /17°10'29" E, lgt. SV, PK, det. PK (2007); Chomutovka Brook, Postoloprty [5648], 50°21'52"N /
13°42'10"E, lgt. JSy, det. JSy (2008); ditch, Lanžhot [7267], 48°42'42"N / 16°56'27"E, lgt. MS, det. JSy
(2006); Dlažkovice Pond, Dlažkovice [5549], 50°27'53''N / 13°58'02''E, lgt. NK, det. NK (2007); Dyje River,
Břeclav [7166], 48°48'40''N / 16°48'59''E, (Košel 1999a); Dyje River, Břeclav [7267], 48°46'22''N /
16°52'43''E, (Košel 1999a); Jihlava River, Vladislav [6761], 49°12'24"N / 15°59'49"E, lgt. A, det. NK (2006);
Káča Brook, Hořátev [5856], 50°08'33"N / 15°02'25"E, lgt. A, det. JSy (2006), Kozárovický Brook, Zálezlice
[5652], 50°18'35"N / 14°25'29"E, lgt. A, det. JSy (2006); Labe River, Němčice [5960], 50°05'38"N /
15°48'34"E, lgt. JH, NL, det. JH (2005); Labe River, Valy [5959], 50°01'58"N / 15°37'05"E, lgt. JH, NL, det.
VK (2003); Labe River, Verdek [5560], 50°26'47"N / 15°47'05"E, lgt. JH, NL, det. JH (2002, 2003); Lišanský
Brook, Rakovník [5948], 50°05'35"N / 13°45'06"E, lgt. JH, NL, det. JH (2007); Litava River, Vážany nad
Litavou [6867], 49°07'47"N / 16°51'02"E, lgt. SV, PK, det. PK (2007); Mlýnská strouha drain, Jaroslavice
[7263], 48°45'44"N / 16°15'06"E, lgt. SV, PK, det. PK (2007); Mnichovka Brook, Hrušov [6154], 49°53'36''N
/ 14°44'06''E, lgt. JH, NL det. JH (2006); Návesník Pond, Vortová [6261], 49°42'46"N / 15°55'43"E, lgt. JSy,
det. JSy (2007); Nový Častotický Pond, Častotice [6762], 49°14'09"N / 16°05'57"E, lgt. JSy, det JSy (2006);
Nový Pond, Mikulov [7266], 48°46'55''N / 16°40'32''E, (Košel 1999a); Okluky Brook, Uherský Ostroh
[7070], 48°59'37"N / 17°24'10"E, lgt. SV, PK, det. PK (2007); Oslava River, Náměšť nad Oslavou [6862],
49°11'55"N / 16°08'58"E, lgt. A, det. EP (2007); Ploužnický Brook, Ploužnice pod Ralskem [5354],
50°38'10"N / 14°48'30"E, lgt. A, det. JSy (2006); Podhrázský Pond, Lkáň [5549], 50°26'56''N / 13°56'57''E,
lgt. NK, det. NK (2007); Rakovec Brook, Hrušky [6867], 49°07'44"N / 16°50'24"E, lgt. PK, det. PK (2007);
Rokytná River, Moravský Krumlov [6963], 49°03'45"N / 16°19'31"E, (Schenková et al. 2007); Rouchovanka
Brook, Rešice [6962], 49°02'50"N / 16°08'47"E, lgt. SV, PK, det. PK (2007); Říčka River, Sokolnice [6866],
49°06'32"N / 16°43'16"E, lgt. SV, PK, det. PK (2007); Sendražický Brook, Velký Osek [5957], 50°05'26"N /
15°12'10"E, lgt. A, det. JSy (2006); Skalička Brook, Práče [7163], 48°53'03"N / 16°12'56"E, lgt. SV, PK, det.
PK (2007); Svratka River, Křižánky [6362], 49°41'52"N / 16°03'39"E, lgt. SV, PK, det. PK (2007); Svratka
River, Veverská Bitýška [6764], 49°16'45"N / 16°26'15"E, lgt. SV, PK, det. PK (2006); Šatava River, Nosislav
[7065], 48°59'33"N / 16°38'48"E, lgt. A, det. JSy (2006); Štemberský Brook, Slaný [5750], 50°13'29"N /
14°04'48"E, lgt. JH, NL, det. JH (2008); Tichá Orlice River, Kunčice [5965], 50°00'17"N / 16°32'44"E, lgt. A,
det. JSc (2007); Třebůvka River, Loštice [6267], 49°43'21''N / 16°53'48''E, lgt. PK, SV, det. JSc (2007);
Únětický Brook, Únětice [5852], 50°08'56"N / 14°21'33"E, lgt. JH, NL, det. JH (2007); Valová Brook,
Polkovice [6669], 49°23'42"N / 17°15'51"E, lgt. JSy, det. JSy (2008); Vltava River, Praha Podolí [5952],
50°03'21"N / 14°24'560"E, lgt. JH, NL, det. JH (2002) VK (2003); Vltava River, Zelčín [5652], 50°19'09"N /
14°23'56"E, lgt. JH, NL, det. JH (2002, 2005) (Figure 2).
Habitats: Glossiphonia nebulosa is considered typical of running waters, but some of the records are
from ponds at middle and higher elevations (about 600 m a.s.l.). Its ecological valences are probably broader
than have been documented to date.
Status: Prior to this study, Glossiphonia nebulosa had been recorded only from two localities in the
southernmost part of the country (Košel 1999a); more recently, this species has been reported as a common
species from additional localities in both Bohemia and Moravia. Most of localities are situated in southern
Moravia (Dyje (Thaya), Svratka, and Jihlava River basins) and middle Bohemia (Labe (Elbe), Vltava, and
Ohře River basins); no records have yet been reported from the southwestern part of the country. The species
was probably overlooked in previous studies, and perhaps may have been confused with or misidentified as G.
complanata in past studies.
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Glossiphonia slovaca (Košel, 1973)
Synonym: Batracobdella slovaca Košel, 1973
Records: Dyje River, Břeclav [7166], 48°48'40''N / 16°48'59''E, (Košel 1999a); Dyje River, Břeclav [7267],
48°46'22''N / 16°52'43''E, (Košel 1999a); Dyje River, Břeclav [7267], 48˚43'25''N / 16˚53'07''E, lgt. PK
(2006), det. PK (2008) (Figure 2).
Habitats: Limited information suggests that Glossiphonia slovaca occurs in larger lowland rivers.
Status: Both records of this species in the Czech Republic were collected from Dyje River in the
southernmost part of the country, which limit its northern range margin (Grosser & Nesemann 2004). Because
of its scarceness, G. slovaca was classified as vulnerable in the Red list of threatened species in the Czech
Republic (Schenková & Košel 2005).
Helobdella stagnalis (Linnaeus, 1758)
Habitats and status: Helobdella stagnalis is a very common species throughout the Czech Republic,
especially in stagnant and slowly running waters. Most of the records are from eutrophic water bodies; it is
absent only in brooks at the highest elevations in the country (over 800 m a.s.l.).
Hemiclepsis marginata (O. F. Müller, 1774)
Habitats and status: Hemiclepsis marginata is relatively abundant in stagnant water bodies, and usually
those with aquatic vegetation occurring in lowlands and mid-elevations (150–450 m a.s.l.). It is less frequent
in slowly running waters. Its distribution is scattered throughout the Czech Republic.
Theromyzon tessulatum (O. F. Müller, 1774)
Habitats and status: Theromyzon tessulatum is a locally abundant leech occurring in stagnant water bodies
with aquatic vegetation or in larger rivers and slowly running brooks. Its distribution is scattered throughout
the Czech Republic.
Family: Piscicolidae
Caspiobdella fadejewi (Epshtein, 1961)
Synonym: Piscicola fadejewi Epshtein, 1961
Records: Bakovský Stream, Vepřek [5651], 50°18'18"N / 14°18'58"E, lgt. JH, NL, det. JH (2005); Bečva
River, Choryně [6473], 49°30'12"N / 17°53'43"E, lgt. PK, SV, det. JSc (2007); Bílina River, Ústí nad Labem
[5350], 50°39'28"N / 14°02'31"E, lgt. A (2007), det. JSy (2008); Blanice River, Mladá Vožice [6454],
49°32'52''N / 14°49'02''E, lgt. JH, NL, det. NL (2007); Blanice River, Radonice [6155], 49°47'20''N /
14°55'58''E, lgt. JH, NL, det. JH, NL (2004, 2005, 2007); Doubrava River, Záboří nad Labem [5958],
50°01'34"N / 15°20'40"E, lgt. JSy, det. JSy (2008); Dyje River, Břeclav [7267], 48°46'22''N / 16°52'43''E
(Košel 1999a); Dyje River, Jevišovka [7164], 48°49'41"N / 16°28'24"E, lgt. A (2007), det. JSy (2008); Dyje
River, Podhradí [7159], 48°53'29''N / 15°38'30''E, lgt. JŠ, det. JŠ (2008); Chotýšanka Brook, Libež [6255],
49°45'32''N / 14°54'53''E, lgt. JH, NL, det. NL (2006); Dyje River, Podhradí [7159], 48°53'29''N /
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15°38'30''E, lgt. PK, SV, det. JSc (2007); Dyje River, Podhradí [7060], 48°54'12"N / 15°41'21"E, lgt. A
(2007), det. JSy (2008); Haná River, Bezměrov [6670], 49°19'53"N / 17°20'18"E, lgt. JSy, det. JSy (2008);
Jevanský Brook, Stříbrná Skalice [6155] 49°53'22''N / 14°51'26''E, lgt. JH, NL, det. JH (2006); Kozský
Brook, Sezimovo Ústí [6654], 49°22'57"N / 14°41'38"E, lgt. JH, NL, det. JH (2006); Labe River, Hřensko
[5151], 50°52'28"N / 14°14'08"E, lgt. JSy, det. JSy (2008); Labe River, Liběchov [5552], 50°24'08"N /
14°26'53"E, lgt. A (2007), det. JSy (2008); Labe River, Valy [5959], 50°01'59"N / 15°37'00"E, lgt. A (2007),
det. JSy (2008); Lužnice River, Bechyně [6752], 49°17'21''N / 14°28'11''E, lgt. PP, det. JSc, JSy (2007, 2008);
Lužnice River, Dobronice [6652], 49°19'07"N / 14°29'36"E, lgt. A, det. JSc (2007); Lužnice River, Veselí nad
Lužnicí [6854], 49°10'41"N / 14°41'51"E, lgt. A (2007), det. JSy (2008); Morava River, Černovír [6369],
49°36'44"N / 17°15'14"E, lgt. A (2007), det. JSy (2008); Morava River, Lhota [6368], 49°40'59"N /
17°08'59"E, lgt. A, det. JSc (2007); Morava River, Lobodice [6669], 49°23'48''N / 17°18'25''E, let. PK, SV,
det JSc (2007); Morava River, Nové Zámky [6268], 49°42'57"N / 17°01'27"E, lgt. A, det. JSc (2007); Morava
River, Větrovany [6569], 49°27'55"N / 17°18'19"E, lgt. JSy, det. JSy (2008); Moravská Dyje River, Písečné u
Slavonic [7058], 48°57'48"N / 15°27'50"E, lgt. A (2007), det. JSy (2008); Nežárka River, Veselí nad Lužnicí
[6854], 49°10'53"N / 14°42'33"E, lgt. A (2007), det. JSy (2008); Nučický Brook, Stříbrná Skalice [6155],
49°52'58"N / 14°51'33"E, lgt. JH, NL, det. JH (2007); Odra River, Petřvaldík [6274], 49°43'30''N /
18°07'53''E, lgt. PK, SV, det. JSc (2007); Oslava River, Nová Ves [6863], 49°07'21''N / 16°18'47''E, lgt. PK,
SV, det. JSc (2007); Oslava River, Skřípina [6863], 49°08'27''N / 16°12'30''E, lgt. PK, SV, det. JSc (2007);
Ostrovský Brook, Zruč nad Sázavou [6256], 49°44'31''N / 15°06'14''E, lgt. JH, NL, det. JH (2006); Sázava
River, Kamenný Přívoz [6153], 49°51'31''N / 14°31'49''E, lgt. A, det. JSc (2007); Sázava River, Nespeky
[6153], 49°51'27"N / 14°39'25"E, lgt. JH, NL, det. JH NL (2004, 2006, 2007); Sázava River, Pikovice [6152],
49°52'38''N / 14°26'11''E, lgt. A, det. JSc (2007); Sázava River, Sázava [6155], 49°52'51''N / 14°52'57''E, lgt.
PK, SV, det. JSc (2007); Sázava River, Smrčná [6358], 49°39'37''N / 15°20'39''E, lgt. PK, SV, det. JSc (2007);
Sázava River, Soběšín [6255], 49°47'35''N / 14°57'03''E, lgt. PK, SV, det. JSc (2007); Sázava River,
Vlastějovice [6257], 49°43'41''N / 15°10'31''E, lgt. PK, SV, det. JSc (2007); Sázava River, Zruč nad Sázavou
[6256], 49°44'32''N / 15°06'04''E, lgt. JH, NL, det. JH NL (2004, 2007), lgt. A (2007), det. JSy (2008);
Svratka River, Vranovice [7065], 48°57'02"N / 16°37'07"E, lgt. A (2007), det. JSy (2008); Třebůvka River,
Loštice [6267], 49°43'21''N / 16°53'48''E, lgt. PK, SV, det. JSc (2007); Valová Brook, Polkovice [6669],
49°23'42"N / 17°15'51"E, lgt. JSy, det. JSy (2008); Vlára River, Svatý Štěpán [6974], 49°03'18''N /
18°01'19''E, lgt. PK, SV, det. JSc (2007); Vltava River, Zelčín [5652], 50°19'09"N / 14°23'56"E, lgt. JH, NL,
JSy det. JH, JSy (2005, 2006, 2008); Zákolanský Brook, Kralupy nad Vltavou [5751], 50°14'22"N /
14°18'14"E, lgt. JH, NL, det. JH (2004) (Figure 2).
Habitats: Caspiobdella fadejewi occurs in large or medium size rivers with slow moving reaches. This
species is often found on substratum – in contrast to Piscicola geometra, which is more often collected
directly from its fish host. Based upon the distributional records of these two species, the higher number of
current records of C. fadejewi than of P. geometra probably reflects the differences in collecting
methodologies, rather than some other ecological factors.
Status: Prior to this study, Caspiobdella fadejewi was known only from southern Moravia. However, it
has been recently recorded at many additional localities in the Labe (Elbe), Odra (Oder), and Morava (March)
River basins. The main areas of its distribution in the Czech Republic are associated with the Vltava and
Morava River basins. Although it is likely that C. fadejewi has been confused occasionally with P. geometra,
an overall trend of rapid spreading of C. fadejewi along the rivers with suitable habitats has been observed
during our eleven-year study.
Piscicola fasciata Kollar, 1842
Synonym: Cystobranchus fasciatus Brumpt, 1900
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Habitats and status: Piscicola fasciata is a rare ectoparasitic species living most often on the catfish (Silurus
glanis Linnaeus, 1758) (Neubert & Nesemann 1999). In the Czech Republic it was reported only once from
the lower Dyje (Thaya) River (Lucký & Dyk 1964). During their survey, P. fasciata was found frequently on
catfish in spring period. This species is hence supposed to live in the Czech Republic, although by the
sampling method used it was not collected recently (1998 through 2008).
Piscicola geometra (Linnaeus, 1758)
Habitats and status: Piscicola geometra is the most common species of the family Piscicolidae; some
specimens found in Czech rivers and streams are quite variable in color. While this species inhabits stagnant
as well as running waters, it prefers slower flow conditions and the presence of various fish hosts.
Piscicola cf. haranti Jarry, 1960
Records: Bílina River, Ústí nad Labem [5350], 50°39'28"N / 14°02'31"E, lgt. A (2007), det. JSy (2008);
Mlýnský Brook, Litovel [6368], 49°41'58"N / 17°04'08"E, lgt. JSy, det. JSy (2008) (Figure 2).
Habitats: The species was recorded in slow running waters located in the lowlands of the country.
Status: Piscicola cf. haranti is reported in this paper to be a new record for the Czech Republic. The first
two records of this species in the country were collected from the Morava (March) and Labe (Elbe) River
basins, and indicate its possible wider distribution in the country. Over the last 20 years this species has likely
been slowly expanding its range throughout central Europe.
Piscicola respirans Troschel, 1850
Synonym: Cystobranchus respirans Brumpt, 1900
Records: Lukovský Brook, Luková [6165], 49˚52'10"N / 16˚37'39"E, lgt. SV (2007), det. PK (2008); Morava
River, Moravičany [6267], 49˚45'19"N / 16˚58'32"E, lgt. SV (2006), det. PK (2008); Vlára River, Svatý
Štěpán [6974], 49˚02’05”N / 18˚03’03”E, lgt. PK (2007), det. PK (2008) (Figure 2).
Habitats: Piscicola respirans has been collected from small to medium-sized rivers and brooks, located
in low or mid-elevations (250–400 m a.s.l.) of the country. Similar to P. geometra, P. respirans is most
commonly collected from its fish host; it is rarely present in general macrobenthic samples.
Status: Recent records for this species suggest that P. respirans is a rare species with a scattered
distribution in the Czech Republic. All recent records for P. respirans are from the Morava River basin.
Family: Haemopidae
Haemopis sanguisuga (Linnaeus, 1758)
Habitats and status: Haemopis sanguisuga has been found in small and medium sized running waters, small
shallow ponds and pools, and often on wet soil next to these water bodies. Preference for habitats in higher
elevations in Central Europe was reported by Košel (1982). Although infrequently collected in the Czech
Republic, the current distribution of this species likely has been under-estimated due to its semi-aquatic life
style and insufficient survey effort in its preferred habitats.
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Family: Hirudinidae
Hirudo medicinalis Linnaeus, 1758
Records: Černá jezera – Dyje River dead arm, Břeclav [7267], 48°43'09"N / 16°54'22"E, lgt. JP, det. JSy
(2008); Kačení Louka Pool, Moravičany [6267], lgt. MB, det. MB (1998, 2003), lgt. MŠ, det. MŠ (2008);
Kutnar Pond, Rakvice [7166], 48°50'11"N / 16°47'34"E, lgt. JSy, det. JSy (2006); Milotický Pond, Milotice
[7068], 48°57'47"N / 17°09'15"E, lgt. JSc, JSy, GČ, det. JSc (2008); Pastvisko Pool, Lednice [7166],
48°48'30"N / 16°47'53"E, (Sukop 2004), lgt. JSc, NK, det. JSc (2005), lgt. JSc, MŠ, NK, JSy, det. JSc (2006),
lgt. JSc, JSy, MS, det. JSc (2007), lgt. JSc, JSy, MS, det. JSc (2008); pond, Ostrovec [6550], lgt. MŠ, det. MŠ
(2008); pond, Varvažov [6550], lgt. MŠ, det. MŠ (2008); Sekulská Morava (Morava River dead arm), Lanžhot
[7367], 48°37'39"N / 16°57'12"E, lgt. JSc, JSy, NK, det. JSc (2008); Zámecký Pond, Lednice [7166],
48°48'46"N / 16°48'32"E, lgt. JSy, det. JSy (2006), lgt. JSc, JSy, MS, det. JSc (2008) (Figure 3).
Habitats: Hirudo medicinalis was found in shallow stagnant lowland water bodies with abundant
vegetation, stable water levels, and presence of amphibian and mammal hosts for juveniles and adults,
respectively. All localities were in rather temperate climatic conditions.
Status: Hirudo medicinalis is a critically endangered species in the Czech Republic (Schenková & Košel
2005) due to intensive agri- and aquaculture in the country, which has resulted in extensive destruction of
natural wetlands by drainage and flood-control management. Further loss of critical habitat for this species
has resulted from intensive fishery and recreation in the few remaining unaltered wetlands, ponds, and small
pools in the country. Based on authors’ monitoring experiences, the intensive mud removal by heavy
machinery in the Czech Republic has had destructive impact on H. medicinalis populations. Isolated pools
that historically supported populations of medicinal leeches have failed to yield specimens after mud removal
operations have been conducted. Recent distributional records for this species in the Czech Republic have
been limited to only a few localities in southern and middle Moravia and southern Bohemia.
Family: Erpobdellidae
Dina lineata (O.F. Müller, 1774)
Records: Dyje River dead arm, Břeclav [7267], 48°43'09"N / 16°54'22"E, lgt. JSy, det. JSy (2008); Myšník
Pond, Častotice [6762], 49°14'12"N / 16°06'13"E, lgt. JS (2006), det. JS (2008); Ohře River, Terezín [5450],
50°30'06"N / 14°09'39"E, lgt. IS, det. IS (2005); Opatovický Brook, Ústí [6472], 49°31'19"N / 17°45'48"E,
lgt. PK, SV, det. PK (2008); Panenská Pool, Nové Mlýny [7166], 48°50'41''N / 16°43'40''E, (Košel 1999a);
Radičeveská strouha Brook, Trnovany [5647], 50°19'00"N / 13°35'54"E, lgt. IS, det. IS (2006); Reslava
River, Pomezí nad Ohří [5939], 50°05'31"N / 12°15'07"E, lgt. IS, det. IS (2005); Soutěska Spring, Pavlovské
vrchy [7165], 48°51'39''N / 16°38'46''E, (Košel 1999a); Skluzavka Pool, Plošiny [7267], 48°44'17''N /
16°53'19''E, (Košel 1999a); Sviní Brook, Kozlíky [5349], 50°36'43"N / 13°53'11"E, lgt. IS, det. IS (2005)
(Figure 3).
Habitats: Dina lineata occurs in smaller or medium-sized stagnant and running water bodies or in springs
in lowlands (150–250 m a.s.l.); rarely also in pond or river littorals in mid-elevations (about 450 m a.s.l.).
Status: Dina lineata is a rare species in natural habitats and commonly collected only in some lowland
areas of the Czech Republic.
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Dina punctata Johansson, 1927
Records: Dyje River, Podhradí [7159], 48°53'29''N / 15°38'30''E, lgt. PK, SV, det. JSc (2007); Lužnice River,
České Velenice [7255], 48°45'53"N / 14°58'03"E, lgt. JR, det. JR (2007); Otava River, Katovice [6748],
49°16'22"N / 13°49'22"E, lgt. KK, det KK (2007) (Figure 3).
Habitats: Dina punctata lives in littoral zones of larger rivers and brooks.
Status: Dina punctata is reported in this paper to be a new species record for the Czech Republic. This
species likely has spread into the country from the Dunaj (Danube) River basin, where it is more common.
This is the case of the occurrence in the Dyje (Thaya) River. Its occurrences in southern Bohemia (in the
Vltava River basin) need additional documentation. Other new records can be expected, especially in the
southern part of the country.
FIGURE 3. The distribution of selected leech species (Annelida, Clitellata, Hirudinida: the families Hirudinidae and
Erpobdellidae) in the Czech Republic recorded during the years 1998 through 2008, based upon published and
unpublished records, and specimens collected during this study.
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Erpobdella nigricollis (Brandes, 1900)
Records: Bílina River, Brozánky [5349], 50°36'35" / 13°56'25", lgt. JSy, det. JSy (2007); Bílina River,
Hostomice [5448], 50°35'23"N / 13°49'36"E, lgt. JSy, det. JSy (2007); Bílina River, Kozlíky [5355],
50°36'41"N / 13°52'59"E, lgt. JSy, det. JSy (2007); Bílina River, Lbín [5349], 50°36'20"N / 13°51'32"E, lgt.
JSy, det. JSy (2007); Bílina River, Stadice [5349], 50°37'08"N / 13°58'02"E, lgt. JSy, det. JSy (2007); Bílina
River, Ústí nad Labem [5350], 50°39'27"N / 14°02'28"E, lgt. A (2007), det. JSy (2008), lgt. EP, det. EP
(2008); Dyje River, Břeclav [7166], 48°48'40''N / 16°48'59''E, (Košel 1999a); Dyje River, Břeclav [7267],
48°46'22''N / 16°52'43''E, (Košel 1999a); Holínková dead arm, Rakvice [7166], 48°50'08''N / 16°48'06''E,
(Košel 1999a); Káča Brook, Hořátev [5856], 50°08'33"N / 15°02'25"E, lgt. A, det. JSy (2006); Kamenice
River, Nekrasín [7053], 49°13'20"N / 15°04'29"E, lgt. A, det. FK (1998); Kyjovka River, Lanžhot [7367],
48°41'26"N / 16°57'07"E, lgt. A, det. NK (2006); Labe River, Děčín [5251], 50°46'09"N / 14°12'45"E, lgt.
JH, NL, det. VK (1999, 2003); Labe River, Hradec Králové [5760], 50°12'20"N / 15°49'29"E, lgt. A, det. EP
(2007); Labe River, Hřensko [5151], 50°52'24"N / 14°14'07"E, lgt. JH, NL, det. JH (1999); Labe River, Lysá
[5855], 50°10'49"N / 14°50'08"E, lgt. JH, NL, det. JH (2002); Labe River, Obříství [5652], 50°18'12"N /
14°29'08"E, lgt. JH, NL, det. JH (1999); Labe River, Obříství [5752], 50°17'54"N / 14°28'55"E, lgt. A, det.
EP (2007); Labe River, Valy [5959], 50°01'58"N / 15°37'05"E, lgt. JH, NL, det. JH (1999, 2002, 2005);
Lužnice River, Bechyně [6752], 49°17'29"N / 14°28'18"E, lgt. A, det. FK (1998); Lužnice River, Roudná
[6854], 49°18'59"N / 14°43'21"E, lgt. A, det. FK (1998); Lužnice River, Vlkov [6756], 49°09'41"N /
14°43'18"E, lgt. A, det. FK (1998); Moravice River, Opava [6073], 49°55'38"N / 17°56'44"E, lgt. A, det. NK
(2006); Mže River, Stříbro [6244], 49°45'14"N / 13°00'36"E, lgt. A, det. EP (2007); Odra River, Bohumín
[6075], 49°55'04"N / 18°19'27"E, lgt. A, det. EP (2007), lgt. A, det. EP (2008); Odra River, Ostrava [6175],
49°49'13"N / 18°13'03"E, lgt. A, det. EP (2008); Olše River, Kopytov [6076], 49°56'49"N / 18°20'07"E, lgt.
A, det. NK (2006); Opava River, Třebovice [6175], 49°49'57"N / 18°13'10"E, lgt. A, det. EP (2007); Oskava
River, Pňovice [6268], 49°43'11"N / 17°09'37"E, lgt. A, det. EP (2007); Ostružná River, Sušice [6747],
49°15'18"N / 13°33'01"E, lgt. A, det. FK (1998); Otava River, Topělec [6650], 49°21'00"N / 14°08'40"E, lgt.
A, det. NK (2006); Ploučnice River, Děčín [5251], 50°46'32"N / 14°12'30"E, lgt. A, det JSy (2006); Pšovka
River, Kokořín [5553], 50°26'47"N / 14°34'41"E, (Košel & Beran 2006); Rokytka River, Strašín [6054],
49°59'59"N / 14°41'12"E, lgt. A, det. JSy (2006); Sázava River, Soběšín [6255], 49°47'55"N / 14°57'19"E,
lgt. A, det. FK (1998); Sázava River, Utín [6360], 49°36'09"N / 15°40'01"E, lgt. A, det. FK (1998); Sázava
River, Zruč nad Sázavou [6256], 49°44'32"N / 15°06'06"E,lgt. A, det. NK (2006); Senice River, Leskovec
[6773], 49°16'52"N / 17°59'16"E, lgt. A, det. FK (2000); Smutná River, Bechyně [6654], 49°18'33"N /
14°27'38"E, lgt. A, det. FK (1998); Svratka River, Rajhrad [6965], 49°05'35"N / 16°37'10"E, lgt. A, det. EP
(2007); Šlapanka Brook, Věžnice [6460], 49°30'56"N / 15°41'06"E, lgt. JH, NL, det. JH (2006); Tichá Orlice
River, Kunčice [5965], 50°00'33"N / 16°32'15"E, lgt. A, det. FK (2000); Úhlava River, Dubová Lhota [6645],
49°20'10"N / 13°11'24"E, lgt. A, det. FK (1999); Úpa River, Jaroměř [5661], 50°21'24"N / 15°55'53"E, lgt. A,
det. EP (2007); Úslava River, Vilémov [6447], 49°32'40"N / 13°36'08"E, lgt. A, det. FK (1999); Vltava River,
Praha Podolí [5952], 50°03'21"N / 14°24'60"E, lgt. JH, NL, det. VK (2003) JH (1999, 2002, 2005); Vltava
River, Podolí [5952], 50°03'01"N / 14°24'47"E, lgt. A, det. EP (2007); Vltava River, Praha Trója [5951],
50°04'06"N / 14°15'00"E, lgt. JH, NL, det. JH (2006, 2007); Vltava River, Zelčín [5652], 50°19'09"N /
14°23'56"E, lgt. JH, NL, det. VK (2003) JH (1999, 2002, 2005); Zákolanský Brook, Kováry [5851],
50°11'27"N / 14°15'52"E, lgt. JH, NL, det. JH (2006, 2007) (Figure 3).
Habitats: Erpobdella nigricollis is an inhabitant of large- or medium-sized running waters, where it
occurs frequently with (although less abundantly than) Erpobdella octoculata.
Status: The distribution of E. nigricollis in the Czech Republic is scattered throughout the entire country,
especially in lowland habitats; however, it seems to be absent from habitats located at higher elevations (over
500 m a.s.l.).
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Erpobdella octoculata (Linnaeus, 1758)
Habitats and status: Erpobdella octoculata is a very common leech species in all types of both running and
stagnant waters throughout the Czech Republic. It is less abundant in running waters at higher elevations,
where Erpobdella vilnensis is more commonly collected.
Erpobdella testacea (Savigny, 1822)
Records: Nesyt Pond, Lednice [7266], 48°46'48''N / 16°43'25''E, (Košel 1999a) (Figure 3).
Habitats: The occurrence of Erpobdella testacea is restricted to lowland stagnant waters; to date, this
species had been recorded from only one pond located in the south-eastern part of Czech Republic.
Status: Although Erpobdella testacea is one of several species that are difficult to identify, it is
nonetheless considered to be very rare in the Czech Republic; thus, we recommend a certain degree of
protection for this species until further studies can establish its true status in the country.
Erpobdella vilnensis (Liskiewicz, 1925)
Habitats and status: Erpobdella vilnensis is common in the Czech Republic, especially in smaller brooks
and springs or in the littoral areas of ponds occurring in the mid and higher elevations (usually over 350 m
a.s.l.). It is distributed throughout the country and can be locally very abundant.
Trocheta cylindrica Örley, 1886
Synonym: Trocheta bykowskii Gedroyč 1913
Records: Blazický Brook, Loukov [6572], 49°24'23"N / 17°43'05"E, lgt. A, det. JSy (2006); Brook,
Halenkov [6775], 49˚16'33''N / 18˚10'43''E, lgt. JK (2006), det. JSy (2008); Brook, Trojanovice [6575],
49˚29'58''N / 18˚12'25''E, lgt. JK (2007), det. JSy (2008); Malše River, Straňany [7153], 48°53'14''N /
14°30'42''E, lgt. A, det. FK (1998) Bystrý Brook, Řeka [6377], 49˚37'16''N / 18˚36'09''E, lgt. JK, det. JSy
(2008); Javorový Brook, Rovné [6377], 49˚37'38''N / 18˚36'57''E, lgt. JK (2007), det. JSy (2008); Malá
Ráztoka Brook, Trojanovice [6575], 49˚29'57''N / 18˚15'56''E, lgt. JK, det. JSy (2008); Malá Tisová Brook,
Halenkov [6774], 49˚16'29''N / 18˚08'38''E, lgt. JK, det. JSy (2008); Moravská Sázava River, Rájec [6167],
49°51'43"N / 16°54'46"E, lgt. A, det. NK (2006); Oskava River, Pňovice [6268], 49°43'11"N / 17°09'38"E,
lgt. A (2007), det JSy (2008); Sázava River, Štukheilský Mlýn [6360], 49°36'09''N / 15°40'02''E, lgt. A, det.
FK (1998); Skluzavka Pool, Plošiny [7267], 48°44'17''N / 16°53'19''E, (Košel 1999a); springbrook, Bukovec
[6479], 49°32'51''N / 18°51'24''E, lgt. JB, det. JSy, (2005, 2006); Svitava River, Brno [6865], 49°08'35"N /
16°37'44"E, lgt. A., det. JSy (2008); Trnávka River, Hrobice [6772], 49°16'14''N / 17°49'30''E, lgt. A, det. FK
(2000); Vlára River, Brumov [6974], 49°02'16"N / 18°03'04"E, lgt. A, det. NK (2006); Vsetínská Bečva
River, Velké Karlovice [6675], 49°21'45"N / 18°18'09"E, lgt. A (2008), det. JSc (2009); Zaplavená Pool,
Lubeš [7167], 48°48'12''N / 16°50'14''E, (Košel 1999a); Žábronožková Pool, Lanžhot [7267], 48°46'05''N /
16°52'08''E, (Košel 1999a); Živkovský Brook, Břeclav [7267], 48°47'30"N/16°52'32"E, lgt. A, det. JSy
(2006) (Figure 3).
Habitats: Trocheta cylindrica has commonly been collected in the Czech Republic from springs, and
from small brooks at higher elevations (up to 900 m a.s.l.). Other records of this species were reported from
lowland pools and wetlands, and (although less frequently) from larger rivers.
Status: Trocheta cylindrica has a limited distribution in the Czech Republic; most of the records to date
are from localities in eastern Moravia. Although infrequently collected in the Czech Republic, the current
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distribution of this species likely has been under-estimated due to its semi-aquatic life style and insufficient
survey effort in its preferred habitats.
Discussion
Geographically, the Czech Republic is situated in the centre of Europe (Figure 1), on the watersheds of the
Labe (Elbe), Dunaj (Danube), and Odra (Oder) Rivers; each of these major watersheds serve as ‘avenues’ for
leech distribution. Elevations throughout the country range from 120 to 1600 m, with a mean elevation of
about 430 m.
Czech leeches (Hirudinida) can be classified into three groups according to population strength and
increasing or decreasing number of localities:
1) indigenous species with stable and strong populations – those with records from many sites throughout
the country;
2) indigenous species with weak populations – those known from only a limited number of localities in
the country; and
3) species recently recorded in the Czech Republic – those which have passively spread or have been
introduced (in one or more ways) into the Czech Republic.
Group 1. Various kinds of water bodies in the Czech Republic provide optimal conditions for most
species of leeches known to occur in the country—indigenous species representing the European, Palaearctic
fauna with historical records and stable populations. Alboglossiphonia heteroclita, Glossiphonia complanata,
Helobdella stagnalis, Hemiclepsis marginata, Theromyzon tessulatum, Piscicola geometra, Haemopis
sanguisuga, Erpobdella octoculata and E. vilnensis belong to this first group. Three other species are now
included in this group: Glossiphonia concolor, G. nebulosa, and Erpobdella nigricollis. Previously considered
to be rare in this country, these three species are now considered common due to the accurate identification of
specimens and presence in the diversity of localities that have been surveyed for the presence of leeches.
Group 2. The second group includes species considered historically extant in the Czech territory (mostly
those considered to be restricted to several finite areas or habitats based upon historical records), but now
considered to be a declining or more restricted species in the country based upon a limited number of records
and/or specimens collected during this and other recent studies. The most important region for thermophilous
leeches is the southernmost part of the Czech Republic, particularly in southern Moravia near the confluence
of the Morava (March) and Dyje (Thaya) Rivers; this area lies biogeographically within the Pannonian Basin.
In the cases of Alboglossiphonia hyalina and Alboglossiphonia striata, we have recorded an increase in
reports of these two species in the Czech Republic—likely attributable to their recent separation,
taxonomically, from Alboglossiphonia heteroclita (Trontelj 1997, Neubert & Nesemann 1999). In fact, A.
hyalina and A. striata are probably indigenous to Central Europe. Very little is yet known about their ecology,
but neither ever occurs in large populations. Because records of A. hyalina are limited in the Czech Republic,
we suggest that this species be considered for listing as vulnerable. The distribution records for A. striata in
this country are quite limited, and we believe this species to be threatened. Because we are aware of only two
recent records of A. striata from the southeastern part of the country, we believe this species should be
considered for listing as endangered.
Of the species restricted to the Southern Moravia, only Glossiphonia slovaca is considered vulnerable
(Schenková & Košel 2005). This species occurs mainly in running waters (all of our records come from the
lower reaches of the Dyje River), although its occurrence is also likely in river branches and ponds. We
believe this species to now be extirpated from the Morava River above its confluence with the Dyje River
(Košel 1995, 1999b). Southern Moravia represents the northernmost limit of the current known distribution of
G. slovaca (Grosser & Nesemann 2004).
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Dina lineata is another rare species with a limited distribution in the Czech Republic; recent records come
mainly from southern Moravia and western Bohemia. This species has only been recorded in smaller brooks,
in stagnant, often temporal bodies, and in springs. To date, the known distribution of Dina lineata in the
Czech Republic is based upon only a few specimens; most of these were recorded from unique and sensitive
habitats. The limited known distribution and restricted habitats in which this rare species seems to occur
provides plausible support for the listing of Dina lineata as vulnerable in the country.
Another amphibious species, Trocheta cylindrica, is known from only a few scattered localities, primarily
springs and small brooks, and (less frequently) from pools and slow running rivers. Although large
populations of T. cylindrica have been recorded in its preferred habitat, its apparent restriction to unique and
finite localities in the Czech Republic supports assignment of this species to vulnerable status.
Hirudo medicinalis represents a unique case. It is a critically endangered species (Schenková & Košel
2005), yet has a historical distribution covering larger areas in the Morava and Labe River basins —with
records of its broad distribution documented in several publications in the early and mid-20th
century (Zavřel
1923, Hrabě 1936, Blažka 1958, 1960). Intensive collection pressure on natural populations of Hirudo
medicinalis for use in a variety of medical applications has resulted in reductions—sometimes even
decimation—of previously strong, naturally occurring populations of this species in the Czech Republic and
elsewhere in Europe. The dramatic decrease in abundance of this species can also be attributed to the
significant increase in intensive agri- and aquaculture activities in the Czech Republic (especially widespread
and uncontrolled drainage of land) leading to the destruction of preferred habitats. This decrease in
populations of H. medicinalis in the Czech Republic is quite obvious when compared to populations of this
species in some other European countries, e.g., Poland (Buczyńsky 2003). During this present survey, H.
medicinalis was recorded at only nine localities in the Czech Republic, most of them restricted to the Morava
and Dyje River basins. Nevertheless, regular monitoring of H. medicinalis over the last five years—using
specific, quantifiable methods for surveying and capture of specimens—has resulted in additional
distributional information and new habitat preferences for this species. Our study of this critically endangered
species in the Czech Republic is continuing.
A closely related thermophilous species, Hirudo verbana Carena 1820, occurs in Austria and Hungary
(Neubert & Nesemann 1999), which are located (respectively) south and east of the Czech Republic. This
species, however, has not yet been recorded—either historically or during this and other recent studies—
within the Czech Republic. Several records of H. verbana, especially those from Western Europe, are likely
specimens that were obtained (or had escaped from) commercial cultures. Hirudo medicinalis and H. verbana
can easily be distinguished from one another by comparison of their ventral color patterns: dark spots are
present on H. medicinalis, but absent from H. verbana.
Another uncommon species, Piscicola respirans, was recorded sporadically from several medium-sized
rivers and brooks, within the Morava River basin only. Its preference for running water habitats at higher
elevations (Neubert & Nesemann 1999, Košel 2001) was not confirmed during this study. Because of its
scarceness, we believe this species should be considered vulnerable. The collection of P. respirans from fish
hosts would most likely provide additional information about its distribution.
Piscicola fasciata, a very uncommon species, to date, it has only been recorded in the Czech Republic by
Lucký & Dyk (1964). This species is probably more common in the country than presently known from
verifiable records, because it lives permanently attached to its catfish host, and thus has not been collected via
the methodologies used for most free-living leeches during this eleven-year study. We expect to document the
presence of P. faciata in the Czech Republic in the near future.
Erpobdella testacea represents a very rare species, based upon a single known record from the
southeastern part of the country. This species used to be reported from more stagnant water bodies in this area
(Vojtek et al. 1967, Koubková & Vojtková 1973); the reason for its recent low occurrence, however, is still
unknown. For this reason we suggest assignment of endangered status for Erpobdella testacea.
Group 3. The third group includes leeches only recently recorded in the Czech Republic, with an
increasing number of localities. For these species, there are no historical records from the Czech Republic.
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One species—Caspiobdella fadejewi—had been reported only once from the country prior to this study. Two
species are reported for the first time in the country—Piscicola cf. haranti and Dina punctata.
Caspiobdella fadejewi, non-indigenous species of Ponto-Caspian origin, is quickly spreading throughout
central Europe up the Dunaj River. It is a parasitic species that uses its hosts (several fish species) for
transport. Since the 1980s, this species has been recorded in Poland, Austria, Germany and the Netherlands
(Tittizer et al. 2000, Bij de Vaate et al. 2002, van Haaren et al. 2004). Today, C. fadejewi is the dominant
piscicolid species in the Austrian part of the Dunaj River, and it has also been reported from many localities in
the Dunaj and Rhein (Rhine) River basins in Germany. In the Czech Republic, it was initially recorded in the
1990s in the vicinity of the Morava-Dyje confluence (Košel 1998, 1999a) and it has recently spread into
various slow flowing larger rivers in the Morava, Odra, and Labe River basins. Caspiobdella fadejewi is often
more frequent than Piscicola geometra in macrozoobenthos samples, because it spends more time apart its
fish host. In the same habitats, these two species are probably mutually exclusive (Jueg et al. 2004).
Piscicola cf. haranti, reported here as a new record for the Czech Republic, is also thought to be spreading
throughout central Europe based upon recent records. The origin and mode of distribution of this species,
however, is still unclear. Recent records of this species are from Romania, Hungary, Austria, and Germany
(from the Dunaj River), and more recently from the Rhein River basin (Neubert & Nesemann 1999, Tittizer et
al. 2000, Jueg et al. 2004). Unfortunately, the original description of P. haranti by Jarry in 1960 was based
only on the external morphology of specimens collected from a single locality—a spring in southern France.
Given the dissimilarity of 1) the habitats in which populations of P. haranti (as originally described by Jarry in
1960) and P. cf. haranti (as reported from our surveys in the Czech Republic and from other records included
herein), and 2) the distance of these two populations from one another, it is possible that these two taxa could
in fact be different species. In consideration of its probable Dunaj basin origin, our record of this taxon from
the Labe River basin is remarkable. This species appears to be more widespread than previously thought.
Furthermore, there is the possibility of confusion with its congener, P. geometra.
Dina punctata, recently reported as a new species for the country, can be considered a non-indigenous
species that has been spreading into the Czech Republic from the west—likely from the Rhein River basin
(Germany) through the Main River and floating channel to the Dunaj River. From the Dunaj, D. punctata has
moved upstream into its tributaries, initially into the Slovak part of the Morava River (Košel 1999b), then
more recently into the Dyje River in Vranov. During the eight years since it was first recorded in Slovakia, the
species has moved about one hundred km upstream into the Dyje River. Two other Czech localities for D.
punctata were found in southern Bohemia— both in upper parts of the Vltava River basin. The occurrence of
this species in this region is still somewhat of a surprise. Because of its possible semi-aquatic life-style, we
can speculate about its terrestrial spread from near situated brooks in the Dunaj River basin, where this species
was previously recorded (Nesemann 1997). One possible explanation is that young D. punctata specimens are
transported by waterfowl. Additional specimens of D. punctata collected from the lower parts of the Vltava or
the Labe River basins may provide us with insight into this question. Its current northern distribution probably
extends into, but not north of, the Czech Republic. According to the observations of this species in Slovakia,
D. punctata seems to be an invasive and aggressive species, which can negatively influence the indigenous
leech community (personal observation), and thus we expect more specimens to be collected from areas in the
Czech Republic in the future.
In general, the most diverse leech fauna in the Czech Republic has been recorded in southern Moravia,
mainly in the vicinity of the Morava-Dyje confluence—an area into which some species (e.g., Glossiphonia
slovaca) are known to have spread from south-eastern Europe. Other species such as Batracobdelloides moogi
Nesemann & Csányi 1995 and Glossiphonia verrucata (Fr. Müller 1844) were found not far from the Czech
border, and likely will be collected in the country in the near future. We also expect a recently confirmed
species, Haemopis elegans Moquin-Tandon, 1846, to eventually spread into the Czech Republic; to date, H.
elegans has been reported from Austria, Hungary, Slovenia and Germany (Grosser 2004a, Grosser &
Neseman 2004).
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Most of the records for leeches discussed in this paper were collected during recent monitoring programs
of running waters in the Czech Republic, conducted over the last 11 years (1998 through 2008). Additional
research focusing specifically on wetlands and habitats associated with smaller stagnant water bodies is
necessary to increase our knowledge of leech distributions in the Czech Republic and elsewhere in Europe.
As is true for other invertebrates, the conservation and legal protection of critical habitats used by
threatened species is the most effective protection for leeches. Most of the threatened species of leeches are
inhabitants of lowland wetlands and larger lowland rivers, usually those with aquatic macrophytes. These
habitats are often heavily impacted by human activities throughout central Europe, usually with negative and
often irreversible results. Leeches are usually not very sensitive to moderate changes and fluctuations in water
quality; however, their populations have been declining steadily, often drastically, because of the destruction
of their preferred habitats, or because of other unsuitable or incompatible influences there. Therefore, habitats
with extensive and perennial populations of vulnerable, threatened, and/or rare leech species should be strictly
protected; only carefully designed, well-managed, and regularly monitored construction projects should be
permitted.
Conclusions
The check-list of leeches (Hirudinida) of the Czech Republic discussed in this paper and presented in Table 1
includes twenty-four species, reflecting historical and recent records published in the literature, unpublished
records, and specimens from collections by the authors during this eleven-year study (1998 through 2008).
Two of these—Piscicola cf. haranti and Dina punctata—are reported here as new records for the Czech
Republic. Two species—Hirudo medicinalis and Glossiphonia slovaca—are already considered to be
threatened species (Schenková & Košel 2005). The results of our research presented in this paper support our
recommendation that six additional species be added permanently to the Red list of threatened species in the
Czech Republic: four of these – Alboglossiphonia hyalina, Dina lineata, Piscicola respirans, and Trocheta
cylindrica—should be listed as “vulnerable”, and two—Alboglossiphonia striata and Erpobdella testacea –
should be listed as “endangered” according to IUCN Red List Categories and Criteria (IUCN 1994).
Acknowledgments
We would like to thank our colleagues J. Bojková, L. Opatřilová, J. Špaček and M. Štambergová and
institutions the Agency for Nature Conservation and Landscape Protection of the Czech Republic, the
Ministry of the Environment of the Czech Republic, and T. G. Masaryk Water Research Institute for providing
specimens and faunistic information from their research projects. We thank L. Tajmrová for checking the
language and other improvements. We are much indebted to both reviewers for constructive suggestions and
especially to M. J. Wetzel (Illinois Natural History Survey, USA) for improving the English text. The project
was supported by Long-term Research Plans from the Ministry of Education, Youth and Sports of the Czech
Republic (MSM0021622416) and by the Ministry of the Environment of the Czech Republic (no.
0002071101).
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222
Kubová, N., J. Schenková & M. Horsák, 2013.
Environmental determinants of leech assemblage patterns in lotic and lenitic habitats.
Limnologica, 43, 516–524.
Limnologica 43 (2013) 516–524
Contents lists available at SciVerse ScienceDirect
Limnologica
journal homepage: www.elsevier.com/locate/limno
Environmental determinants of leech assemblage patterns in lotic and
lenitic habitats
N. Kubová, J. Schenková∗
, M. Horsák
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotláˇrská 2, 61137 Brno, Czech Republic
a r t i c l e i n f o
Article history:
Received 27 November 2012
Received in revised form 27 April 2013
Accepted 2 May 2013
Available online 10 June 2013
Keywords:
Hirudinida
Species diversity and composition
Lotic and lenitic habitats
Environmental predictors
Prey availability
Response curves
a b s t r a c t
Leeches (Clitellata: Hirudinida) are abundant predators or ecto-parasites inhabiting various freshwater
habitats; however many biotic and abiotic drivers of their assemblage patterns have been deduced rather
than directly tested. To study species richness and composition changes in leech assemblages, 109 sites
of running and stagnant water bodies were sampled in three regions of the Czech Republic in 2007–2010,
together with several explanatory variables that are known or expected to be important predictors of
leech distribution. In total, 17 species of leeches were recorded, varying between 0–7 and 0–9 species
in lotic and lenitic sites, respectively. These differences in species richness of lotic and lenitic sites were
highly significant, contrary to the abundances, which varied between 0–283 and 0–295 individuals. The
main change in species composition was controlled by water temperature and morphological characteristics
(e.g. substrate and cover of macrophytes), mostly reflecting the differences between lotic and
lenitic habitats. We found the density of benthos (i.e. prey availability) to be the best predictor of species
composition in both lotic and lenitic sites, together with the percentage of canopy cover. However, the
other significant predictors (i.e. the substrate and water conductivity found to be significant in lotic sites,
and the mean annual temperature and PO4
3−
in lenitic sites), differed between these habitats. Other than
mean annual temperature and water temperature, which had different effects on species richness in lotic
and lenitic sites, there were no other differences between lotic and lenitic sites in terms of how species
richness and abundance responded to all other analyzed predictors. Our results stress the importance of
prey availability and canopy for leech distribution patterns. Differences in the significant predictors of
leech assemblage patterns between lotic and lenitic sites raise fundamental questions about the underlying
mechanisms and ecological constraints to leech distribution in these main types of aquatic systems.
© 2013 Elsevier GmbH. All rights reserved.
Introduction
The life strategies of leeches (Clitellata: Hirudinida), bloodsucking
ecto-parasites of vertebrates or predators of invertebrates,
determine their distribution patterns due to a tight relationship
between food availability and leech occurrence (Sawyer,
1974). The importance of prey availability has however only been
deduced from other habitat characteristics, such as the chemistry
and trophic status of the water, without quantification and/or a
detailed statistical evaluation (Pawłowski, 1936; Sandner, 1951;
Mann, 1955; Elliott and Mann, 1979). Specific data exist only
for some species of which the diet was explored in detail, with
the majority of studies being related to Erpobdella octoculata (e.g.
Young and Ironmonger, 1979; Dall, 1983; Toman and Dall, 1997;
Schenková et al., 2007). Substrate, water depth, type of aquatic
habitat and chemical parameters of the waterbody have also been
∗ Corresponding author. Tel.: +420 532146333.
E-mail address: schenk@sci.muni.cz (J. Schenková).
determined to be the other significant predictors of leech distribution
(Sawyer, 1974; Koperski, 2006). As leeches have adapted
to most aquatic environments, covering a rich variety of trophic
levels from dystrophic to eutrophic aquatic systems (Mann, 1955;
Sládeˇcek and Koˇsel, 1984), testing other environmental factors
can reveal some important determinants of their distribution patterns.
However, other biotic parameters of waterbodies, such as
the presence of a canopy or macrophytes, have only exceptionally
been considered in ecological studies to date. We are aware
only of the work of Koperski (2010) evaluating the effect of riparian
vegetation. Several hypotheses that are also unexplored relate
to the effect of temperature, which is expected to have a great
importance for leech distribution (Sawyer, 1974, 1986; Elliott and
Mann, 1979). In the conditions found in central European, leeches
are generally described as thermophilous organisms, but without
specifying whether higher importance should be given to seasonal
variations in water temperature within the habitat (which
differ between running and standing waters) or the variation
of temperature between sampling sites (mostly correlating with
altitude).
0075-9511/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.limno.2013.05.001
N. Kubová et al. / Limnologica 43 (2013) 516–524 517
Fig. 1. Map of the Czech Republic showing the position of study areas with all
109 sampling sites. Note that the Bohemian–Moravian Highlands (B–M Highlands)
include two distinct local sampling areas.
Previous ecological studies on leeches were focused either
solely on stagnant (e.g. Young and Ironmonger, 1981; Spelling and
Young, 1987) or running waters (e.g. Grosser et al., 2001; Koperski,
2005, 2010). Existing studies summarizing the response of the
whole assemblage in various types of water habitats are always
focused only on a part of all the potential environmental variables.
Descriptive studies summarizing leech data related to a certain geographical
area (e.g. Bennike, 1943; Elliott and Mann, 1979; Koˇsel,
1988, 1989; van Haaren, 2004; Schenková et al., 2009) cover mostly
habitat characteristics, pollution status and distribution of particular
leech species. Other studies emphasize the importance of
water chemistry (e.g. Mann, 1955; Grosser et al., 2001) or solely
the trophic status of the water (Sládeˇcek and Koˇsel, 1984). Particular
attention was given to various water types and their features
by Koperski (2006) in his meta-analysis, but unfortunately without
any evaluation of water chemistry. Some ecological studies refer
to a different geographical range, with only a small overlap with
European species (Herrmann, 1970; Moser et al., 2006).
In this study, we used a geographically extended data set, covering
both lotic and lenitic habitats, accompanied by the sampling
of macrozoobenthos as potential prey, in order to segregate the
influence of diet availability from the other environmental drivers.
Specifically we attempted to: (i) determine the main predictors
of species richness and composition of leech assemblages; and
(ii) compare the observed assemblage patterns between lotic and
lenitic habitats.
Methods
Study area
Sampling sites were located in three different areas (i.e.
Bohemian Uplands, the Bohemian–Moravian Highlands and the
South Moravia Lowlands), covering the main types of waterbodies
in the Czech Republic (Fig. 1). The majority of the waterbodies
occurring within these areas (total extent 4320 km2) were sampled.
In each area we tried to cover as much as possible of the
broad variety of waterbodies in respect to their size (stream width
in running waters, total area in stagnant waters), depth, substratum
composition, relative cover and composition of the riparian/littoral
vegetation.
The Bohemian Uplands Protected Landscape Area is characterized
by a patchy landscape, composed of fields, pastures and
deciduous forests, with the exception of the northern part, which
has been affected by brown coal mining. It represents a relatively
warm and medium-dry region of a broader range of elevation
(Table 1). The ˇZd’árské vrchy Hills (in the northern part of the
Bohemian–Moravian Highlands) are covered by spruce forests and
meadows, which are irrigated by numerous brooks and small rivers.
This region is rather cold and humid and has the highest elevation
of all the study sites. The Námˇeˇst’ nad Oslavou territory (the
southern part of the Bohemian–Moravian Highlands) is characterized
by an undulating landscape, covered by fields and pine forests.
Although brooks and rivers are often present there, the most frequent
waterbodies are ponds. It is warmer than the northern part
of the region, but drier and of lower elevation. The third region, the
South Moravia Lowlands, is an agricultural territory, dominated by
fields and arable lands; most of the waterbodies studied were to
a certain extent organically polluted. This region has the highest
mean annual temperature, the lowest elevation and is semi-dry.
Field sampling and laboratory work
The sampling was carried out from the end of April to the beginning
of June in 2007–2010. In total, 109 sites of lotic (51) and lenitic
(58) waters were explored. Leeches were collected for 30 min by
hand along 10 m of shoreline, including areas of bare shore and
riparian/littoral vegetation at each study site. The method applied
of collecting by tweezers or with bare hands (Elliott and Mann,
1979; Koˇsel, 1988) was used mainly because leeches were usually
tightly attached to the substratum. Leeches were identified
in the laboratory, after standardized fixation procedures (Koˇsel,
1988), according to Neubert and Nesemann (1999) and Grosser and
Nesemann (2004).
Several explanatory variables, which were known or expected
to be important predictors of leech distribution, were established
for each site: (i) water temperature, dissolved oxygen, water pH
and conductivity were measured in the field by portable instruments
(WTW Multi 340i/SET) two times in one week, and the
mean value was used in the analyses to reduce the effect of shortterm
variation; (ii) the concentration of nitrates, ammonia and
orthophosphates, total carbon and total nitrogen were determined
in the laboratory from water samples; (iii) the GPS position was
directly measured in the field and used to determine the altitude
and several climatic conditions (i.e. mean annual temperature,
mean January and July temperatures, and the annual precipitation),
obtained by using overlays of plot locations with a digital elevation
model and climatic maps, based on Tolasz (2007), in the ArcGIS 8.3
program (ESRI, 2003); and (iv) water depth was measured in the
field, the percentage of canopy and the percentage of the shoreline
with riparian/littoral vegetation (macrophytes) were estimated
and recorded in the field, and the substrate composition was estimated
as a percentage of particle size categories in the field and
converted using the phi scale (Hynes, 1970; Gordon et al., 1992).
Samples of the macrozoobenthos were collected by three
minute kick-sampling using a hand net with 250-␮m mesh size.
All mesohabitats at each site were sampled proportionally, i.e.
the sampling time given to each mesohabitat corresponded to
their proportional representation at the site (Kokeˇs et al., 2006;
Kubová and Schenková, 2012). The numbers of dominant taxa
of macrozoobenthos (i.e. “Oligochaeta”, Mollusca, Ephemeroptera,
Plecoptera, Trichoptera and Chironomidae) were counted and
entered into the analyses; other taxa with a very low abundance
were excluded from further evaluation. Invertebrate densities were
converted on a scale from 1 to 5 (1, up to 150 individuals; 2, 150–300
individuals; 3, 300–500 individuals; 4, 500–1000 individuals; 5,
more than 1000 individuals).
Data analyses
The preference of each species for either lotic or lenitic sites
was tested based on a comparison of recorded individuals between
the studied lotic and lenitic sites using a Mann–Whitney U test.
518 N. Kubová et al. / Limnologica 43 (2013) 516–524
Table 1
Climatic characteristics of the studied areas.
Area Altitude (m a.s.l.) Mean annual
temperature
(◦
C)
Mean January
temperature
(◦
C)
Mean July
temperature
(◦
C)
Precipitation
(mm year−1
)
Bohemian Uplands 135–667 6.1–9.1 −3.8 to −0.8 15.7–18.8 488–713
Bohemian–Moravian Highlands
ˇZd’árské vrchy Hills 553–719 6.0–6.8 −4.1 to −3.3 15.1–16.1 684–768
Námˇeˇst’ nad Oslavou territory 541–630 6.7–7.9 −3.5 to −2.8 16.5–17.8 355–586
South Moravia Lowlands 161–207 9.0–9.4 −1.9 to −1.5 19.0–19.4 480–504
Differences among number of species, total abundance and all
explanatory variables were compared between lotic and lenitic
sites using a t-test, as all these variables had a normal distribution
(Kolmogorov–Smirnov test, p < 0.05). As all the climatic variables
(altitude, temperature and precipitation) were strongly correlated
(Spearman’s rank correlations rs > 0.795, p < 0.001), only the mean
annual temperature was used in the analysis.
The species-by-site matrix was analyzed using Detrended Correspondence
Analysis (DCA; detrended by segments) to expose
the major compositional gradients in the data. The numbers of
individuals were transformed as log(x + 1) to exclude the effect
of dominant species; rare species were downweighted according
to the recommendations given by Lepˇs and ˇSmilauer (2003). The
length of the main gradient (3.31 SD) in the species data was
adequate for use in unimodal modelling (ter Braak and Prentice,
1988). To explain the gradients in the species data, the correlations
with climate and environmental variables were examined
using Spearman correlations (rs), with site scores on the first four
DCA axes; a Mann–Whitney U test was used for nominal variables.
Sequential Bonferroni corrections of the significance level
were used for multiple comparisons of continuous environmental
variables (Holm, 1979). Canonical Correspondence Analysis (CCA)
and Redundancy Analysis (RDA) with a forward selection procedure
and a Monte-Carlo test with 999 permutations were used to reveal
the environmental variables that were able to explain a significant
portion of variability in the leech data.
Generalized Linear Models (GLM; McCullagh and Nelder, 1989),
with Poisson family corrected for overdispersion (i.e. quasipoisson)
in the data, were used to determine the explanatory variables that
were significant for leech species richness and abundance. All variables
were entered into the analysis in linear and quadratic shape;
the interactions between variables were not included. The accuracy
of the final models was checked using distribution of residuals and
Cook’s distances. In the case of the existence of two good models
for one species, Akaike’s information criterion (AIC) and the number
of parameters were used as the deciding parameters (Guisan and
Zimmermann, 2000). In order to test dietary preferences, the total
abundance of macrozoobenthos and the numbers of “Oligochaeta”,
Mollusca, Ephemeroptera, Plecoptera, Trichoptera and Chironomidae
were entered stepwise into the analysis.
All analyses, except for the DCA, were computed separately
for lotic and lenitic sites. Species and environmental data were
analyzed using the statistical programs CANOCO (ter Braak and
ˇSmilauer, 2002), Statistica (StatSoft Inc., 2001) and R (version
2.10.1; R Development Core Team, 2010).
Results
In total, 4547 specimens of 17 leech species were collected
(Table 2). Table 3 shows the environmental differences between the
lotic and lenitic sites studied based on all the explanatory variables.
The total abundance per site varied from 0 to 283 and from 0 to 295
individuals at lotic and lenitic sites, respectively. There was no difference
between lotic and lenitic sites in terms of total abundance
(p = 0.176); however, the abundance of several species differed
significantly. Erpobdella vilnensis (p = 0.018) and Glossiphonia complanata
(p = 0.042) expressed a significantly higher population size
at lotic sites, contrary to Hemiclepsis marginata (p < 0.001) and
Theromyzon tessulatum (p < 0.001), which had a higher number
recorded at lenitic sites. In contrast to abundance, species numbers
differed significantly between lotic and lenitic sites (p < 0.001),
varying from 0 to 7 and from 0 to 9 species, respectively (Table 3).
The DCA analysis of leech assemblages significantly separated
lotic and lenitic sites along the first axis (Mann–Whitney U test,
p = 0.038) (Fig. 2). The sample scores on this axis were strongly
correlated with water temperature and several morphological
variables: phi, macrophytes (positively) and canopy (negatively)
(Table 4). The sample scores on the second axis were significantly
correlated with the nitrate content (negatively), which represented
the water chemistry gradient. The other correlations with the first
four DCA axes were weaker and not significant after Bonferroni
corrections (Table 4). The CCA analysis revealed significant relationships
between the variance in leech compositional data and
benthos densities (prey availability), water conductivity (water
chemistry) and phi (substratum characteristics) (Table 5). Single
RDA analyses, which were run separately for both habitat types,
showed that the largest part of the variability in species data was
also explained by benthos density: 24% in lotic and 15% in lenitic
sites (Table 5). However, other than the percentage of canopy the
other significant predictors differed between habitats, with phi and
water conductivity found to be significant at lotic sites, and the
mean annual temperature and PO4
3− at lenitic sites (Table 5).
The type of habitat, along with mean annual temperature,
water temperature, density of benthos, substratum composition
and canopy significantly affected the species richness of leeches in
the whole dataset (p < 0.001). The numbers of species in lotic sites
Fig. 2. DCA ordination diagram of study sites positioned on the first two ordination
axes, based on leech assemblages of 109 study sites. All species except Hirudo medicinalis,
which was an outlier in the ordination space, were plotted. Variables with a
significant correlation (p < 0.05) with at least one of the first four DCA axes are shown,
and those significant after Bonferroni corrections (p < 0.0026) are in bold. Nominal
variables (i.e. lotic or lenitic sites) are displayed as dark triangles. The first four DCA
axes explained 16.9, 10.9, 7.0, and 4.4% of the species data variance, respectively.
The sum of all eigenvalues was 3.31.
N. Kubová et al. / Limnologica 43 (2013) 516–524 519
Table 2
List of recorded leech species with total abundances, number of their records and relative abundance (%) in all sampling sites, with lotic and lenitic sites shown separately.
Species Both habitats (n = 109) Lotic habitats (n = 51) Lenitic habitats (n = 58)
No. of
individ.
No. of sites Relative
abund. (%)
No. of
individ.
No. of sites Relative
abund. (%)
No. of
individ.
No. of sites Relative
abund. (%)
Alboglossiphonia heteroclita (Linnaeus, 1761) 226 18 4.97 35 5 1.98 191 13 6.98
Alboglossiphonia hyalina (O.F. Müller, 1774) 6 3 0.13 4 2 0.22 2 1 0.07
Alboglossiphonia striata (Apáthy, 1888) 8 4 0.17 3 1 0.17 5 3 0.18
Glossiphonia complanata (Linnaeus, 1758) 188 34 4.13 136 21 7.65 52 13 1.87
Glossiphonia concolor (Apáthy, 1888) 31 10 0.68 13 4 0.73 18 6 0.64
Glossiphonia nebulosa Kalbe, 1964 33 6 0.72 30 4 1.68 3 2 0.10
Helobdella stagnalis (Linnaeus, 1758) 774 58 17.02 187 23 10.52 587 35 21.19
Hemiclepsis marginata (O.F. Müller, 1774) 99 29 2.17 5 5 0.28 94 24 3.39
Theromyzon tessulatum (O.F. Müller, 1774) 43 22 0.94 7 3 0.39 36 19 1.23
Piscicola geometra (Linnaeus, 1758) 22 8 0.48 2 1 0.11 20 7 0.72
Piscicola haranti Jarry, 1960 1 1 0.02 1 1 0.05 0 0 –
Haemopis sanguisuga (Linnaeus, 1758) 30 6 0.66 1 1 0.05 29 5 1.04
Hirudo medicinalis Linnaeus, 1758 12 1 0.26 0 0 – 12 1 0.43
Dina lineata (O.F. Müller, 1774) 1 1 0.02 1 1 0.05 0 0 –
Erpobdella octoculata (Linnaeus, 1758) 2552 78 56.12 873 27 49.12 1679 51 60.61
Erpobdella testacea (Savigny, 1822) 1 1 0.02 1 1 0.05 0 0 –
Erpobdella vilnensis (Liskiewicz, 1925) 520 41 11.43 478 25 26.89 42 16 1.51
Table 3
Descriptive statistics of environmental and response variables, recorded in lotic and lenitic study sites; differences between habitat types were tested by a t-test.
Variable p Lotic habitats Lenitic habitats
Min Median Max Min Median Max
Explanatory variables
Altitude (m a.s.l.) n.s. 136 318 719 135 263 708
Mean annual temperature (◦
C) n.s. 6.0 7.7 9.4 6.0 8.0 9.4
Mean January temperature (◦
C) n.s. −4.1 −1.9 −0.8 −4.1 −1.8 −0.9
Mean July temperature (◦
C) n.s. 15.1 17.6 19.4 15.1 17.7 19.4
Annual precipitation (mm) n.s. 485 552 768 480 554 759
Water temperature (◦
C) 0.001 10.5 14.3 22.9 13.3 18.4 26.7
Water pH 0.035 5.4 7.9 9.4 5.6 8.1 10.4
Water conductivity (␮S/cm) n.s. 50 424 2890 45 540 2014
Dissolved oxygen (mg/l) n.s. 3.4 9.8 15.7 2.3 8.9 21.8
Total carbon (mg/l) n.s. 0.5 35.0 290.4 0.7 41.0 125.1
Total nitrogen (mg/l) 0.001 0.7 7.0 20.0 0.1 2.2 18.0
Nitrates (mg/l) 0.001 0.0 13.5 38.4 0.0 1.8 28.1
Ammonium ions (mg/l) 0.046 0.0 0.6 28.5 0.0 0.7 9.4
Phosphates (mg/l) n.s. 0.0 0.2 1.9 0.0 0.1 5.9
Phi 0.028 −5.9 −1.3 8.0 −6.0 2.3 8.0
Water depth (cm) 0.004 15 28 60 21 45 85
Percentage of canopy (%) 0.001 0 30 95 0 10 80
Percentage of macrophytes (%) 0.001 0 0 80 0 20 100
Categorical density of benthos n.s. 1 3 5 1 3 5
Response variables
Total abundance n.s. 0 20 183 0 23 295
Species richness 0.001 0 2 7 0 3 9
Table 4
Eigenvalues of the first four axes of the DCA, Spearman’s rank correlations (rs) and the Mann–Whitney U test (M–W) between environmental factors and site scores on the
DCA axes.
DCA
AX1 AX2 AX3 AX4
rs rs rs rs
Eigenvalues 0.984 0.863 0.779 0.686
Morphological variables
Phi 0.38***
0.21*
n.s. n.s.
Macrophytes 0.44***
n.s. n.s. −0.27*
Canopy −0.42***
−0.22*
n.s. n.s.
Density of benthos n.s. n.s. −0.25*
n.s.
Water temperature 0.45***
n.s. n.s. −0.21*
Chemical variables
pH 0.25*
n.s. n.s. n.s.
Nitrates −0.26*
−0.34***
n.s. n.s.
Total carbon n.s. −0.23*
0.22*
n.s.
Phosphates −0.22*
n.s. 0.24*
n.s.
Only those factors that significantly correlated with at least one DCA axis are shown.
Significant correlations after Bonferroni corrections are in bold (the cut level was p = 0.0026); non-significant (n.s.) correlations are not shown.
*
Significance level: p < 0.05.
***
Significance level: p < 0.001.
520 N. Kubová et al. / Limnologica 43 (2013) 516–524
Table 5
Percentage variance in leech species data explained by each variable in separate canonical correspondence analyses (CCA, all sites) or redundancy analyses (RDAs, lotic or
lenitic sites), and the percentage of independent variation explained in a single CCA/RDA for all variables together using the forward selection procedure (FS).
Variable CCA – all sites RDA – lotic sites RDA – lenitic sites
Expl. var.
%
Order in FS Expl. var.
in FS %
Expl. var. % Order in FS Expl. var.
in FS %
Expl. var. % Order in FS Expl. var.
in FS %
Density of benthos 13.28*
1 13.28*
24.12**
1 24.12**
15.53**
1 15.53**
Conductivity 11.11*
2 11.38*
11.47*
4 11.76*
14.77**
7 n.s.
Phi 10.26*
3 10.57*
16.76**
2 11.47*
7.95 6 n.s.
Nitrates 10.02*
4 n.s. 1.76*
12 n.s. 6.43 5 n.s.
Water temperature 8.67 5 n.s. 11.17 5 n.s. 8.71 9 n.s.
pH 8.67 6 n.s. 7.06 8 n.s. 3.03 12 n.s.
Mean annual temperature 7.05 7 n.s. 10.0 6 n.s. 14.85**
2 14.77*
Canopy 7.32 8 n.s. 11.76*
3 17.9**
14.39**
3 10.22*
Phosphates 7.59 9 n.s. 5.59 10 n.s. 12.12*
4 9.85*
Total carbon 7.86 10 n.s. 11.47 7 n.s. 7.57 11 n.s.
Ammonium ions 7.05 11 n.s. 9.71 9 n.s. 7.19 8 n.s.
Total nitrogen 7.32 12 n.s. 5.0 11 n.s. 7.19 10 n.s.
The significance (p) of explained variation (expl. var.) was tested using the Monte Carlo test with 999 runs. The order of the variables during forward selection is shown.
*
Significance level: p < 0.05.
**
Significance level: p < 0.01.
were controlled by mean annual temperature, water conductivity
and canopy, contrary to lenitic sites, with species richness significantly
driven by benthos densities, water temperature, canopy
and the quantity of ammonium (Table 6). We found that the total
abundances of leeches in the whole dataset responded to the same
variables as species richness. However, the abundances of leeches
at the lotic sites were affected by water temperature, mean annual
temperature, substratum composition, concentration of nitrates
and canopy (Table 6). At the lenitic sites, the abundances were also
associated with mean annual temperature and substratum composition;
however, benthos density and the amount of total carbon
were revealed as additional significant variables (Table 6).
Using response curve modelling, we mostly found consistency
in the responses of species richness and abundances to those
environmental factors that had a significant effect on the analyzed
data (Fig. 3). Other than for mean annual temperature and
water temperature, which had different effects on species richness
in lotic and lenitic sites, there were no other differences
between lotic and lenitic sites in terms of the way in which
species richness and abundance responded to all the other analyzed
predictors.
Discussion
Assemblage patterns in the whole dataset
Using the whole dataset, we documented significant differences
in leech species composition between lotic and lenitic sites,
Table 6
Results of the GLM modelling for species richness and total abundance recorded in all sites and in lotic and lenitic sites analyzed separately.
Habitat Variable categorical Linear Quadratic p Value Var. expl. %
Species richness Positive/negative response Positive/negative response
All sites Habitat type 0.001 9.0
+ Mean ann. temp. − Mean ann. temp. 0.013 8.7
+ Water temp. − Water temp. 0.001 6.8
+ Dens. of benthos – 0.002 4.1
− Phi – 0.033 3.4
− Canopy – 0.046 2.9
Lotic sites + Mean ann. temp. − Mean ann. temp. 0.018 10.3
+ Conductivity − Conductivity 0.031 8.2
+ Canopy – 0.011 3.6
Lenitic sites + Dens. of benthos − Dens. of benthos 0.001 12.1
+ Water temp. − Water temp. 0.012 9.0
− Canopy – 0.041 6.5
− Ammonium – 0.047 3.1
Abundance
All sites Habitat type 0.024 8.5
+ Water temp. − Water temp. 0.001 7.8
+ Dens. of benthos – 0.002 5.5
+ Canopy − Canopy 0.021 4.3
+ Mean ann. temp. − Mean ann. temp. 0.025 4.2
− Phi – 0.034 3.1
Lotic sites + Water temp. − Water temp. 0.006 9.1
+ Mean ann. temp. − Mean ann. temp. 0.017 7.1
− Phi – 0.005 6.3
+ Nitrates − Nitrates 0.029 4.6
+ Canopy – 0.006 2.8
Lenitic sites + Mean ann. temp. − Mean ann. temp. 0.008 7.7
+ Dens. of benthos − Dens. of benthos 0.001 6.8
+ Phi − Phi 0.023 4.2
+ Total carbon – 0.036 2.8
Mean ann. temp., mean annual temperature; water temp., water temperature; dens. of benthos, density of benthos; var. expl., explained variation. In the cases of both linear
and quadratic term significant at p = 0.05 based on F test, a lower value of significance is shown.
N. Kubová et al. / Limnologica 43 (2013) 516–524 521
Fig. 3. Response curves of species richness and abundance in lotic and lenitic sites against selected significant environmental factors. Significance of curves based on F test:
***p < 0.001; **p < 0.01; *p < 0.05; n.s., not significant.
formerly also reported by Mann (1953) and Koperski (2006). Contrary
to Koperski (2006, 2010), who distinguished further habitat
types within lotic and lenitic waters, we only established these two
basic categories in order to obtain gradients of physical–chemical
and morphological characteristics that were as wide as possi-
ble.
Habitat type and several environmental factors, i.e. water temperature,
phi (substratum composition), presence of macrophytes,
percentage of canopy and nitrates, were found to be important
in driving the main compositional changes in leech assemblages
(Fig. 2). Variables connected with site morphology – phi value and
the presence of macrophytes – increased along the first DCA axis
towards lenitic sites, while the canopy variable increased towards
lotic sites. It has already been pointed out that the coarser substratum
in lotic habitats is generally preferred by leeches (Koperski,
2010). However, in lenitic habitats the fine substratum was
accompanied by the presence of macrophytes, which could substitute
for the lack of a coarse substratum (Sawyer, 1986). The direct
ordination analysis (CCA) confirmed the importance of substratum
composition and nitrates; significant effects of water conductivity
and prey availability were also determined. However, as most of
these important variables significantly differed between the two
habitat types (Table 3), it was not possible to segregate the effect of
habitat type and these variables based on the whole dataset. It can
be concluded that these variables rather serve to define ecological
differences between lotic and lenitic waters, which are also important
predictors of leech distribution. As leech species composition
was controlled by a combination of morphological, climatic, chemical
and biological variables, it was not possible to conclude which
of them was of higher importance. We therefore analyzed lotic and
lenitic sites separately to segregate the effects of these confounding
predictors.
522 N. Kubová et al. / Limnologica 43 (2013) 516–524
Comparison between lotic and lenitic habitats
We found several important differences in variables that significantly
shaped changes in the patterns of leech species composition,
as well as species richness and abundance in lotic and lenitic sites.
The results from lotic sites were more similar to those based on the
whole dataset, suggesting the overall patterns of species composition
to be mostly constrained by the lotic assemblages (Table 5).
In all three datasets the density of benthos (i.e. prey availability)
appeared consistently to be the best explanatory variable of leech
species composition. To test the causality of these relationships, we
ran separate CCA and RDA models, with all the significant environmental
variables (see Table 5) included in each respective model,
and tested the significance of benthos density for the residual variation
in the leech data. The effect of benthos density was significant
in all models (p < 0.05, data not shown).
Although this factor also possessed the highest predictive power
for changes in species richness at lenitic sites, no significant relationship
was found for lotic sites (Table 6). Similar results were
also found for the total abundances of leeches. Despite the great
importance of prey availability for structuring leech assemblages,
we did not determine any indicators of the specific food preferences
of leeches as a whole, as has been reported earlier for individual
genera, for example Erpobdella (e.g. Dall, 1983; Toman and Dall,
1997) or Helobdella (Davies et al., 1979). Moreover, leech abundance
at lenitic sites expressed a clear unimodal response, with
a significant decrease of leech abundance with increasing benthos
densities (Fig. 3b). This can probably be explained by a compounding
effect of organic pollution and high temperatures in lenitic
habitats. This was further indicated by a higher percentage of Chironomidae
larvae and “Oligochaeta”, suggesting a notable decrease
in water quality to levels at which even some of the most tolerant
species, Helobdella stagnalis and E. octoculata, were not able to
increase their densities. Rather low and non-significant changes
in both number of species and of individuals in lotic sites together
with changes in prey density (Fig. 3a and b) suggested a presumably
higher importance of abiotic variables in lotic habitats.
These observations on prey availability are in good concordance
with those previously published; however, they either give
broader support to these earlier findings or have revealed some
new underlying mechanisms. For example, Koperski (2005) found
a high influence of phosphates, but only for lotic habitats and on
the basis of only eleven sites in three relatively unpolluted rivers.
It has previously also been reported that several chemical variables,
closely connected with the trophic status of the water (e.g.
alkalinity, conductivity, concentration of phosphates, nitrates and
oxygen, and various direct indices of trophic status), are significant
for leech distribution (e.g. Bennike, 1943; Mann 1955; Herrmann,
1970; Koperski, 2005, 2010). However, it is rather unlikely that
these variables would exert a direct effect on the leeches as all of
them are more or less linked with prey density and availability. Similar
patterns were also obtained in our data, with water conductivity
having a significant influence on species composition changes in
all three datasets (Table 5). Phosphate content also explained a
significant and notable amount of the variations in leech species
composition, but only for lenitic sites. However, as mentioned
above, it would appear that prey availability is a more important
predictor of leech assemblage patterns in lenitic than in lotic sys-
tems.
We found the surrounding terrestrial vegetation (percentage of
canopy) to have an important and previously unreported role for
leech species distribution. It explained a high portion of the variations
in the species composition data for both lotic and lenitic sites
(Table 5). The surrounding terrestrial vegetation cover was also a
significant predictor for species richness, but the effects observed
in lotic and lenitic sites were opposite to each other. It is likely
that the higher canopy at lotic sites, on one hand, probably prevented
thermal fluctuations and offered patches of cold water as
refuges for running water species (Aguiar et al., 2002; Ebersole
et al., 2003), which are less tolerant of higher temperatures. On
the other hand, a low canopy can offer suitable warm-water conditions
for thermophilous/temperature-tolerant species in lenitic
habitats. In contrast to the canopy, the influence of macrophytes
was of lower importance, being significant only in the context
of the whole dataset (Fig. 2), and probably reflecting the difference
between lotic and lenitic habitats. In agreement with this,
Koperski (2010) observed no significant effect of riparian vegetation
on leech assemblages in running water. As most of the benthic
taxa observed in our study were found on the coarse substratum at
the bottom rather than on macrophytes, several explanations for
this behaviour can be proposed. The underside of stones can be a
suitable shelter, reducing the risk of fish predation and/or of being
washed away during high flow events (Young and Spelling, 1986).
We observed that these microhabitats can also provide rich sources
of food, as they supported the highest densities of prey recorded on
the river bottom during our sampling.
We found a compounding effect of mean annual temperature
and water temperature on leech assemblages, with importance differences
of these two variables for each habitat type as a result of
the different habitat features of lotic and lenitic sites. In lenitic sites,
the mean annual (air) temperature explained a significant proportion
of the variance in the leech composition data, and was more
important than the directly measured water temperature (Table 5).
In lotic sites, in contrast, both water and mean annual temperature
had almost the same importance, as water temperature was
probably more associated with stream morphology and substrate
character than it was in lenitic sites. The character of the substrate
was one of the most important predictors of compositional changes,
but only in lotic sites. When considering species richness, however,
opposite results were found for lotic and lenitic sites. There
was a significant, but rather flat, response to mean annual temperature
at lotic sites (Fig. 3c). In contrast, water temperature had a
significant effect on lenitic species richness, presenting a unimodal
response (Fig. 3e). Interestingly, we observed a rather narrow range
of higher species richness in lotic sites along water temperature,
with a maximum of 16 ◦C (based on water temperature range during
the sampling), though the response curve was not significant
(Fig. 3e). This can only suggest there are possible ecological limits to
having a higher number of species towards both ends of the temperature
gradient, as some leech species have a thermal threshold for
starting reproduction (Bennike, 1943). In warmer sites there was an
even sharper drop in species richness, starting from around 20 ◦C,
probably caused by a lack of thermophilous/high temperaturetolerant
species, which were represented only by E. octoculata,
G. complanata and H. stagnalis in our data (Madsen, 1963). Thus,
species that prefer simultaneously a higher water current and temperature
would appear to be very rare.
There is good ecological support for a unimodal response of
species richness in lenitic sites along the mean annual temperature
(Fig. 3c). Low temperatures are not favourable to most of the
species: a negative correlation with altitude in stagnant waters has
been reported for some leech species in British lakes (Young and
Ironmonger, 1981). In contrast, higher mean annual temperatures,
which were reached in the South Moravian sampling sites, are associated
with the negative influence of organic pollution (caused by
agricultural land-use in the surroundings). Similar limits can also
shape the response of leech density along mean annual temperature,
which expressed a significant unimodal pattern in both types
of waterbodies (Fig. 3d).
As reported previously by Koperski (2006), intensity of fish predation
is another important controller of leech assemblages; this
was not examined in detail in our study. We designed the present
N. Kubová et al. / Limnologica 43 (2013) 516–524 523
study to achieve a rather large and representative data set of various
freshwater bodies, which presented difficulties to obtain exact
data on fish stock for all the lotic and lenitic sites. Thus, we were
only able to estimate fish densities in the field (on a six-grade scale
from 0, no fish, to 5, high abundance of fish). Using these rather
coarse-scale estimates we were not able to determine any significant
relationships between leech assemblages and fish densities.
Habitat requirements and preferences of study species
Most of the central European leech species are often reported as
being rather generalist (Sawyer, 1974; Koˇsel, 1988, 1989; Neubert
and Nesemann, 1999). Despite the common occurrence of most of
the study species in both types of habitats, there were several statistical
preferences of some species for one habitat or the other.
We observed that four species, E. vilnensis, G. complanata, H. stagnalis
and T. tessulatum, significantly preferred only one type of site,
although they are able to inhabit either (Elliott and Mann, 1979;
Neubert and Nesemann, 1999). These preferences have already
been reported by Koperski (2006) for the former two species (which
prefer lotic habitats) and by Bennike (1943) for the latter two
species (which prefer lenitic habitats), but without an exact statistical
evaluation. The rare species Dina lineata and Erpobdella
testacea were found only in lotic habitats, though they are reported
elsewhere predominantly from lenitic habitats (Elliott and Mann,
1979). This was probably linked to the presence of suitable mesohabitats
in the study streams (e.g. muddy bottoms or shallow
banks) and favourable water chemistry. The choice of study sites
could be another possible explanation of this deviance from its
known habitat requirements. However, this seems of low importance,
as the observed habitat preferences of frequent species are
in good agreement with those previously reported. For example,
the common species E. octoculata and H. stagnalis were dominant
in both lotic and lenitic habitats, as is generally known. These two
species are the most dominant and frequent leech species in the
Czech Republic (Koˇsel, 1988) and Europe (Elliott and Mann, 1979;
Neubert and Nesemann, 1999).
We did not find any significant differences in total abundance
between lotic and lenitic sites, but significantly higher numbers of
species were recorded in lotic habitats. In contrast to this result,
Koperski (2006) recorded a higher diversity in lakes and a lower
diversity in rivers and ponds. As there are no natural lakes present
in our sampling area, it is difficult to compare these results. It is
likely that large and natural lakes can offer a combination of suitable
microhabitats and conditions characteristic of both lotic and
lenitic habitats. They also possess a unique combination of ecological
parameters: they are able to provide high prey availability, but
without having a high trophic status. Thus, in order to achieve a better
understanding of the processes driving local species richness, a
perspective for further research would be to study a broader variety
of water types, from springs and marches to large natural lakes.
Acknowledgments
This research has been supported by the Ministry of Education,
Youth and Sports (MSM 0021622416) and MUNI/A/0976/2009. We
want to thank Marcela R ˚uˇziˇcková and Stanislav Nˇemejc for their
technical assistance.
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232
Kubová, N. & J. Schenková, 2014
Tolerance, optimum ranges and ecological requirements of free-living leech species
(Clitellata: Hirudinida). Fundamental and Applied Limnology, Archiv für Hydrobiologie,
185(2), 167–180.
Tolerance, optimum ranges and ecological
requirements of free-living leech species (Clitellata:
Hirudinida)
Nela Kubová1,
* and Jana Schenková1
With 4 figures and 2 tables
Abstract: Deep knowledge of the ecology of aquatic invertebrate species has always been essential background
for water quality assessment and leeches (Clitellata: Hirudinida), which are at the top of the benthic invertebrate
food chain, are hence a group of principal importance. To study the biological and habitat requirements of freeliving
leeches, 109 sites of running and stagnant water were sampled in the Czech Republic, between 2007 and
2010. The morphological characteristics of the sampling site, chemical parameters of the water and climatic data
were available for each site. Leeches were collected by hand, counted and identified. In total, seventeen species
of genera Alboglossiphonia, Glossiphonia, Helobdella, Hemiclepsis, Theromyzon, Piscicola, Haemopis, Hirudo,
Dina and Erpobdella were recorded. Environmental and species data were used in the analyses. The optima of
twelve environmental variables for nine common species were compared using boxplots. The structure of the leech
data set was recognised by cluster analysis, where eurytopic species formed a distinct group, well separated from
all other species, which was further subdivided according to their ecology. Predictive models designed for seven of
the leech species, revealed significant variables, which determined species occurrence and the extent of the effect
of these variables. The most frequent significant variables were the type of habitat (lotic or lenitic) and the mean
annual temperature.
Key words: Hirudinida, cluster analysis, species optima, predictive models.
Fundam. Appl. Limnol.  Vol. 185/2 (2014), 167–180Article
published online September 2014
© 2014 E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany www.schweizerbart.de
DOI: 10.1127/fal/2014/0594 1863-9135/14/0594 $ 3.50
Introduction
Most of the Central European leech species are
adapted to lower water quality, and above all to higher
trophy, from beta-mesosaprobic to alpha-mesosaprobic
(water saprobity by Kolkwitz & Marsson 1909).
In such waters, hundreds of individuals of common
species, e.g., Erpobdella octoculata or Helobdella
stagnalis, inhabit one sampling site (Schönborn 1985,
Kutschera 2003). Hirudinida can therefore serve as
good indicators of organic pollution (Sládeček &
Košel 1984, Koperski 2005). Despite broad and systematic
research into this group, the ecology of some
of the rare species is poorly known. The life strategy
and life cycles of the common species are the moststudied
areas of leech biology (Mann 1957a, Mann
1957b, Elliott 1973, Learner & Potter 1974, Davies
& Reynoldson 1976, Maltby & Calow 1986a, Maltby
& Calow 1986b, Mason & Sayers 2005). Co-existence
or competition of related species in one family
(Calow & Riley 1982, Milne & Calow 1990) or in
one genus (Dall 1983, Schenková et al. 2007) are further
well-known research topics. In such studies, not
only rare, but also less abundant common species are
seldom covered and therefore their ecology on a large
scale is only partly known.
Authors’ address:
1  Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137 Brno, Czech Republic
* Corresponding author; kubova.nela@seznam.cz
E
eschweizerbart_xxx
 168 Nela Kubová and Jana Schenková
There are only a few ecological studies based in
the field, which summarise the response of Hirudinida
species to various environmental variables on
a larger scale (Bennike 1943, Mann 1955, Elliott &
Mann 1979, Sládeček & Košel 1984, Košel 1988,
Košel 1989, Koperski 2006, Moser et al. 2006); unfortunately,
these mostly refer to relatively small geographical
areas. Focusing solely on stagnant (Young &
Ironmonger 1981, Spelling & Young 1987) or running
water (Grosser et al. 2001, Koperski 2005, Koperski
2010) is a further limitation. Predictors of species
richness and composition of the leech assemblages
were revealed within a large-scale study on freshwater
leeches (Kubová et al. 2013), however, there was no
inclusion of species ecology.
To fill the gap in knowledge concerning the ecological
demands of leech species, we focused on leech
assemblages across the Czech Republic (Central Europe).
Twenty-four species from five families have
been reported in this territory: ten in the family Glossiphoniidae,
four in the Piscicolidae, seven in the Erpobdellidae,
one in the Haemopidae, and one in the
Hirudinidae (Schenková et al. 2009). The main object
of our study was therefore to evaluate the responses
of leeches to various physical, chemical and morphological
variables covering the lotic and lenitic habitats
and mutually compare their responses between lotic
and lenitic environments. To include the whole range
of selected variables, we extended our study sites beyond
the commonly sampled pool, to include those
where leeches do not usually occur, such as brooks at a
higher altitude. Appropriate mesohabitats were chosen
to cover the whole spectrum of preferences of freeliving
species. Using such a data set, we were able to
evaluate the response of single species to the gradient
of environmental variables.
Our main targets were (1) to evaluate ecological
valences in various environmental parameters for selected
species and (2) to test the response of species in
lotic and in lenitic habitats separately.
Material and methods
Study area
Leeches were sampled from April to June in 2007– 2010 in
109 sites from running (51) and stagnant (58) water; each
site was sampled once. With respect to leech occurrence, four
areas were selected: the Bohemian Uplands Protected Landscape
Area, the Žďárské vrchy Hills (the Bohemian-Moravian
Highlands), the Náměšť nad Oslavou territory (the Bohemian–Moravian
Highlands) and the South Moravian Lowlands
(Fig. 1). These represented the main types of landscapes in the
Czech Republic that are rich in water bodies and covered the
main environmental gradients, as well as the gradients of latitude
and longitude.
Field sampling and laboratory procedure
Within each area, sites were selected to sample the whole
gradient of altitude, stream width in running water, the total
area in stagnant water, depth, substratum composition, and the
composition and amount of the littoral/riparian vegetation. The
majority of water bodies in the study area (960 –1,440 km2
)
were sampled. At first, the type of habitat was determined at
each sampling site as categorical variable: lotic, i.e. water with
at least slow current (brooks, streams), and lenitic, i.e. water
with absence of current (ponds, reservoirs). At each site,
10 m of shoreline was chosen for sampling. This sampling
line included the different mesohabitats available at the site
(Kubová & Schenková 2012). The amount of littoral/riparian
vegetation was estimated as a percentage of shoreline covered
by macrophytes within the selected sampling line. Leeches
were collected manually according to the hand-collecting
method (Elliott & Mann 1979, Košel 1988). The coarse substratum,
macrophytes, wood and different submerged objects
were checked. We collected leeches for 30 min at each site, to
standardise sampling time (Kubová & Schenková 2012). Live
leeches were transported from the field to the laboratory, where
they were narcotised by a gradually increasing concentration of
ethanol to a final level of 70 % and, after their death, the mucus
was removed from their bodies. Leeches were then transferred
onto paper saturated with 4 % formaldehyde to strengthen their
bodies (Košel 1988) and stored in 4 % formaldehyde. They
were identified according to Neubert & Nesemann (1999) and
Grosser & Nesemann (2004). The abundances of adult leeches
only were used for all statistic analyses.
The GPS position was directly measured in the field and
used to obtain the altitude and the climatic conditions (i.e.,
mean annual temperature, mean January and July temperatures
and the annual precipitation) based on Tolasz (2007), in the
ArcGIS 8.3 program (ESRI 2003). The pH, conductivity, dissolved
oxygen and water temperature were measured in situ by
portable instruments (WTW Multi 340 i/SET) twice-weekly at
each site, and the mean values were used in analyses, to reduce
the effect of short-term excesses. The concentration of nitrates,
ammonium and orthophosphates, total carbon and total nitrogen
were evaluated in the laboratory from water samples. The
percentage of the canopy above the whole water body (lenitic
habitats) or above the sampling river stretch (lotic habitats) was
estimated in the field. The percentage of shoreline with littoral/
riparian vegetation was also estimated in the field.
Substrate composition was estimated as a percentage of
particle size categories in the field and converted on the phi
scale (Hynes 1970, Gordon et al. 1992); phi values were then
used for the respective statistic analyses.
The quantity of all benthic macroinvertebrates was recorded,
to obtain information concerning food availability.
Samples of the benthos were collected by three-minute kicksampling
using a hand net with 250 µm mesh size. All habitats
were sampled proportionally. The number of individuals from
the total macrozoobenthos, Oligochaeta (sensu oligochaetous
Clitellata; Erséus 2005), Mollusca, Ephemeroptera, Plecoptera,
Trichoptera and Chironomidae were counted and entered the
analyses; the other very low abundant taxa were excluded from
further evaluation.
eschweizerbart_xxx
169Tolerance, optimum ranges and ecological requirements of free-living leech species
Data analyses
Cluster analysis was used to arrange leech species into groups
of similar ecological requirements. After data (abundances of
all species) standardisation, Ward’s method with Manhattan
distances as the linking method was used to get the most objective
results.
Ecological preferences for leech species recorded at eight
and more sites were visualised using box plots. Box plots for
eight leech species and 12 selected environmental variables
were constructed, based on the originally measured values,
weighted by the abundance of each species at particular sites.
The median, minimum and maximum values and the upper and
lower quartile were depicted as box plots. The original values
were shown on the x-axis.
Predictive generalised linear models (GLM) based on an
assumed relationship between the mean response variable and
the linear combination of the explanatory variables was used
to determine the explanatory variables that were significant for
species with eight and more records. All variables were entered
into the analysis in linear and quadratic shape, the interactions
between variables were not included into the model formulae.
As all climatic variables (temperatures and precipitation) were
strongly correlated (Spearman’s rank correlations rs > 0.795, p
< 0.001), only mean annual temperature was used in the analysis.
For testing diet preferences, the total abundance of macrozoobenthos
and numbers of Oligochaeta, Mollusca, Ephemeroptera,
Plecoptera, Trichoptera and Chironomidae entered the
analysis stepwise. Two models were computed for each species:
one model based on the Poisson (quasipoisson in the case
of over-dispersion in the data) distribution, recommended for
the abundance data, and another model with logarithmic distributions.
Poisson models were tested by the Chi-squared test
at the p = 0.05 significance level, quasipoisson models by the
F-test and logarithmic models by the t-test at the same significance
level. The accuracy of final models was checked using
the distribution of residuals and Cook’s distances. In the case
when both models for one species complied with both criteria,
Akaike’s information criterion (AIC) and the number of parameters
were the deciding factors (Guisan & Zimmermann 2000).
Seven final models complied with all the criteria.
Based on the predictive models, graphs with selected leech
species and mean annual temperature were constructed. The
original discontinuous data were used to predict continuous sequences
within the observed range in the models, which were
depicted separately for lotic and lenitic habitats in the respective
graphs.
Species and environmental data were analysed using the
statistics program Statistica (StatSoft Inc. 2001) and program
R, version 2.10.1 (R development core team 2010).
Fig. 1. Map of the Czech Republic, showing all sampled sites.
eschweizerbart_xxx
 170 Nela Kubová and Jana Schenková
Results
Species composition
Overall, 4,547 individuals of 17 leech species were
found (Table 1). The maximum number of leeches
(295) was found at the stagnant water site in the Bohemian
Uplands, and the maximum abundance of one
species (208 specimens) was recorded for Helobdella
stagnalis. We counted the total abundance and frequency
of each species in lotic and lenitic habitats,
both separately and together (Table 1).
The structure of the leech data set was revealed
using cluster analysis, which divided the whole assemblage
into two main clusters (Fig. 2). The first
cluster (A) was composed of eight more or less common
species, which were recorded at ten or more sites.
Erpobdella octoculata, which was found at 71.6 % of
the observed sites (Table 1) was the last species to join
the cluster (Fig. 2). The remaining species of cluster A
formed two subgroups. The first group included three
species (E. vilnensis, Glossiphonia complanata and
G. concolor), which inhabited both lotic and lenitic
habitats, but preferred habitats where the mean annual
temperature did not exceed the mean values of the observed
range. The second subgroup included four common
stagnant water species. Two of these, Theromyzon
tessulatum and Hemiclepsis marginata, were almost
absent in lotic habitats and preferred less organically
polluted sites, whereas two other rather eurytopic species,
Alboglossiphonia heteroclita and H. stagnalis,
inhabited similar, but more polluted sites in both lotic
and lenitic habitats. The second cluster (B) included
nine species, formed again from the two smaller subgroups.
The first of these included free-living species
of genus Alboglossiphonia: A. striata and A. hyalina,
and the parasitic Piscicola geometra. Both species of
the genus Alboglossiphonia are quite rare in the Czech
Republic and prefer similar lenitic mesohabitats with
macrophytes. Piscicola geometra was not rare, but
with the sampling method used, their numbers should
Fig. 2. Cluster analysis diagram for all leech species with displayed link distances. Species abbreviations: AlbHete – Alboglossiphonia
heteroclita, AlbHyal – Alboglossiphonia hyalina, AlbStri – Alboglossiphonia striata, DinLine – Dina lineata, ErpOcto
– Erpobdella octoculata, ErpTest – Erpobdella testacea, ErpViln – Erpobdella vilnensis, GloComp – Glossiphonia complanata,
GloConc – Glossiphonia concolor, GloNebu – Glossiphonia nebulosa, HaeSang – Haemopis sanguisuga, HelStag – Helobdella
stagnalis, HemMarg – Hemiclepsis marginata, PisGeom – Piscicola geometra, PisHara – Piscicola haranti, TheTess – Theromyzon
tessulatum.
eschweizerbart_xxx
171Tolerance, optimum ranges and ecological requirements of free-living leech species
Table1.Totalabundancesandfrequenciesofspeciesatallsamplingsites:abundancesandfrequencies(displayedasthepercentageofsiteswithoccurrenceofeachspecies)ofspecies
inloticandlenitichabitatswererecordedseparately.
TotalLotichabitatsLenitichabitats
Speciesn
individuals
frequencyof
occurrence(%
ofsites)
minmaxmedianfrequencyof
occurrence(%of
loticsites)
minmaxmedianfrequencyof
occurrence(%of
leniticsites)
Alboglossiphoniaheteroclita(Linnaeus,1761) 22616.51 18 2 9.8 1 62 522.4
Alboglossiphoniahyalina(O. F. Müller,1774)   6 2.72  2 2 3.9 2  2 2 1.7
Alboglossiphoniastriata(Apáthy,1888)   8 3.73  3 3 1.9 1  3 1 5.2
Glossiphoniacomplanata(Linnaeus,1758) 18831.21 33 441.2 1 12 322.4
Glossiphoniaconcolor(Apáthy,1888)  31 9.21  5 3.5 7.8 1  7 2.510.3
GlossiphonianebulosaKalbe,1964  33 5.51 25 2 7.8 1  2 1.5 3.4
Helobdellastagnalis(Linnaeus,1758) 77453.21 52 545.1 1208 760.3
Hemiclepsismarginata(O. F. Müller,1774)  9926.61  1 1 9.8 1 12 241.4
Theromyzontessulatum(O. F. Müller,1774)  4320.21  3 3 5.9 1  6 132.8
Piscicolageometra(Linnaeus,1758)  22 7.32  2 2 1.9 1 12 112.1
PiscicolaharantiJarry,1960   1 0.91  1 1 1.9 0  0 0 0
Haemopissanguisuga(Linnaeus,1758)  30 5.51  1 1 1.9 1 20 1 8.6
HirudomedicinalisLinnaeus,1758  12 0.90  0 0 012 1212 1.7
Dinalineata(O. F. Müller,1774)   1 0.91  1 1 1.9 0  0 0 0
Erpobdellaoctoculata(Linnaeus,1758)255271.611351952.9 11522687.9
Erpobdellatestacea(Savigny,1822)   1 0.91  1 1 1.9 0  0 0 0
Erpobdellavilnensis(Liskiewicz,1925) 52037.61107 949 1  9 1.527.6
eschweizerbart_xxx
 172 Nela Kubová and Jana Schenková
have been underestimated when taking into consideration
its parasitic life. The second subgroup included
one rare species, G. nebulosa, and the species Haemopis
sanguisuga, both of which prefer colder habitats,
and four other species that are very rare in the Czech
Republic and were found only once during sampling.
Fig. 3. Environmental preferences for species with more than eight records and selected variables. Displayed values are weighted
by the abundance of a particular species. —– min, max (except the outlying values), ― 25 %–75 %, ‫׀‬ median. Tick marks pointing
upwards indicate the distribution of measured data.
eschweizerbart_xxx
173Tolerance, optimum ranges and ecological requirements of free-living leech species
Species environmental optima
For the visualisation of the differences between the
environmental optima of particular species, box plots
were used (Fig. 3). These were prepared for all available
variables, but only those where species responses
were different from each other were presented.
The mean annual temperature and altitude (Fig. 3a,
b) represent the climatic variables. The thermophilous
species (A. heteroclita and H. stagnalis) preferred
Fig. 3. Continued.
eschweizerbart_xxx
 174 Nela Kubová and Jana Schenková
Table2.ResultsoftheGLMmodelstestedbytheF-test(Poissonmodel)orChi-squaredtest(quasipoissonmodel)forsevenspeciesinbothhabitatsanalysedtogetherandseparately.
Forthequasipoissonmodels,thedispersionparameterisnoted.Fromtwohabitats(lotic/lenitic)onlythiswithhigherpredictedabundanceforeachspeciesisdisplayed.Abbreviations:
P–Poissonmodel;Q–quasipoissonmodel;meanann.temp.–meanannualtemperature;var.exp.–variabilityexplained.
SpeciesModelVariable
%var.exp.per
model
Categorical:
habitattype
Linear
positive/negativeresponse
Quadratic
positive/negativeresponse
AlboglossiphoniaheteroclitaQ:9.16lenitic–phi+phi47.9
+PO4
3 ––PO4
3 –
GlossiphoniacomplanataQ:5.13lotic–meanann.temp.20.3
–phi
–NH4
+
HelobdellastagnalisQ:33.26lenitic–phi21.1
+TC
HemiclepsismarginataPlenitic+meanann.temp.–meanann.temp.35.6
+phi
+NO3
 –
TheromyzontessulatumPlenitic+meanann.temp.26.4
–TN+TN
ErpobdellaoctoculataQ:1.18lenitic+meanann.temp.–meanann.temp.23.4
–TC
–canopy
ErpobdellavilnensisPlotic+meanann.temp.–meanann.temp.27.4
+NH4
+
eschweizerbart_xxx
175Tolerance, optimum ranges and ecological requirements of free-living leech species
warmer sites at lower altitudes, whereas G. complanata
and Theromyzon tessulatum had an optimum in
colder sites at higher altitudes. Other species are rather
eurytopic and the climatic variables were not limiting
for these.
Water temperature, substratum, canopy and vegetation
(Fig. 3c–f) are variables that characterise the type
of habitat. Water temperature was the most fluctuating
variable. The optimum of single species is connected
to their affinity to the habitat type (lotic, lenitic) and
partly to altitude. The substratum composition represented
by the phi value was also related to the habitat
type. Most of the leech species preferred a coarse substratum;
only the parasitic Hemiclepsis marginata and
T. tessulatum preferred sites with a fine substratum.
The canopy and vegetation represented the macrophytes
above and inside the water body, respectively.
The canopy had an influence on the stability of the water
temperature and was usually higher in lotic habitats
in contrast to water vegetation (macrophytes), which
was more abundant in lenitic habitats. The parasitic
species preferred sites with a higher percentage of
vegetation.
Among the chemical variables, dissolved oxygen
(Fig. 3g) is a variable that changes considerably in its
dependence on time, microhabitat, or water flow. All
the species, with the exception of A. heteroclita and
P. geometra had an optimum of dissolved oxygen of
about 10 mg l–1
.
The amount of phosphates (Fig. 3h) represented
the trophy of observed habitats and most of the species
preferred the mean concentrations. Erpobdella vilnensis
and two small species, H. stagnalis and mainly
A.heteroclita, were very tolerant and had optima at a
high concentration of phosphates. For this chemical
variable, we noted the highest range of species optima.
The species optima did not strongly differ according
to total carbon and ammonium ion concentrations,
contrary to total nitrogen and nitrates, higher values
of which were limiting for A. heteroclita, H. stagnalis
and P. geometra (Fig. 3i–l). Theromyzon tessulatum
only preferred very low concentration of nitrates
(Fig. 3k).
Predictive models
The most parsimonious predictive models for seven
selected leech species (A. heteroclita, G. complanata,
H. stagnalis, Hemiclepsis marginata, T. tessulatum,
E. octoculata and E. vilnensis) were computed (Table
2). Final models were computed from the Poisson or
quasipoisson distributions, and in quasipoisson, the
dispersion parameter was noted. Variables significant
for species distribution (p < 0.05) were selected from
all variables and the type of species response was recorded
(Table 2). The categorical variable, type of
habitat (lotic or lenitic), was significant for all selected
species and those habitat types for which the abundance
of each species was predicted to be higher is
shown in Table 2. Only G. complanata and E. vilnensis
preferred lotic habitats. For both of these species, the
mean annual temperature and ammonium ions were
the most decisive variables, together with the substratum
composition for G. complanata. All other species
were more abundant in lenitic habitats and the significant
variables were more diversified. In addition to the
mean annual temperature, we noted the importance of
substratum composition and water chemical param-
eters.
Species response curves to mean annual
temperature
Mean annual temperature was significant in the majority
of predictive models; hence, the response curves
of three common species (E. octoculata, E. vilnensis,
G. complanata) to this variable were constructed
(Fig. 4). The significant effect of mean annual temperature
was expressed for lotic and lenitic habitats
separately, to allow better comparison both within and
between species.
For two out of three dominant species (E. octoculata
and E. vilnensis), mean annual temperature was
significant for both linear and quadratic shapes in both,
lotic and lenitic habitats. These models were used for
creating species response curves and their quadratic
shapes were visualized (Fig. 4). Erpobdella octoculata
was more frequently recorded in lenitic habitats and
it had a lower temperature optimum in lenitic then in
lotic habitats. The temperature optimum of E. vilnensis
in both habitats was similar, although this species
preferred lotic habitats. In contrast to two previous
species, quadratic shape of mean annual temperature
for Glossiphonia complanata was significant only in
lotic habitats (Fig. 4). G. complanata was less abundant
than two previous species and preferred colder
sites in lotic habitats.
Response curves were not produced for the other
species, because of their relatively low abundances
and/or small numbers of records, which were further
reduced by division between the two habitat types.
The input data for creating predicted sequences were
weak and curves had a low predictive effect.
eschweizerbart_xxx
 176 Nela Kubová and Jana Schenková
Discussion
Factors determining leech assemblage
composition
In this study, 17 out of 24 species reported from the
Czech Republic (Schenková et al. 2009) were found.
The type of habitat (lotic/lenitic) was an important
determinant of leech occurrence (Table 2); generally,
we recorded higher abundances (of common species)
and lower total species diversity in lenitic than in lotic
habitats. Conversely, out of the total of seventeen species
found, sixteen were present in lotic habitats, with
only Hirudo medicinalis being absent, and only fourteen
were present in lenitic habitats.
The cluster analysis identified two main clusters
with eight common species in cluster A and nine less
common and rather rare species in cluster B (Fig. 2).
Such a division suggests species grouping according
to two main leech life strategies: broad ecological
valences for one part of leech species, where habitat
preferences of a particular species are rather a quantitative
function (Sawyer 1974), and alternatively, more
specific ecological requirements for another group of
leech species with special habitat preferences that enable
them to inhabit only a few suitable sites with a
certain combination of environmental characteristics.
The habitat requirement of seven out of eight species
from cluster A with the exception of G. concolor, were
described using predictor modelling (Table 2).
Habitat preferences of common leech species
(cluster A)
Erpobdella octoculata is the most common Central
European leech, although its occurrence was restricted
in hard water (Mann 1955). We found it at various site
types from clean brooks to eutrophic ponds. This species
is tolerant to the complete range of water quality
and chemical conditions (Elliott 1973, Elliott &
Mann 1979, Grosser et al. 2001) and has even been
considered a low water-quality indicator (Sládeček &
Košel 1984, Koperski 2005). We recorded the highest
abundances in water with sufficient, but not an overabundance,
of organic matter, which provided enough
available diet (indirectly via benthic invertebrates
feeding on it and later serving as a prey). A suitable altitude
with an optimum of 300 – 500 m a.s.l. in predictive
models, substituted by a mean annual temperature
with an optimum of about 7 °C in stagnant and 8 °C in
running water, respectively, was another crucial condition
for the occurrence of E. octoculata. A negative
correlation with the canopy in this model showed that
it preferred unshadowed waters, which created slightly
higher temperatures.
The most abundant and frequent running water
species, E. vilnensis, is common in Central European
running water (Košel 1989, Neubert & Nessemann
1999, Koperski 2006). At the intermediate altitudes,
E. vilnensis was syntopic with E. octoculata, however,
E. vilnensis was almost absent from the southern
Moravian territory (lower altitudes), where both
lotic and lenitic habitats had higher temperatures and
were more productive. On the contrary, E. vilnensis
was more frequent and abundant than E. octoculata at
higher altitudes. A surprising result was the tolerance
of E. vilnensis to high concentrations of all analysed
chemical variables. Considering its preference for
higher altitudes and lotic habitats, which are usually
less affected by chemical pollution, these results were
not expected. Van Haaren (2004) only indicated a spo-
Fig. 4. Significant curves (p < 0.05) of the common species response to the mean annual temperature, based on the quadratic predictive
models. — lenitic habitats, – - – lotic habitats.
eschweizerbart_xxx
177Tolerance, optimum ranges and ecological requirements of free-living leech species
radic occurrence of E. vilnesis in lowland brooks and
ditches, but the high tolerance of E. vilnensis to chemical
pollution has not been so far discovered. Erpobdella
octoculata and E. vilnensis niche portioning is
probably controlled by temperature, which rather than
chemical conditions, regulates differences in their life
cycles (Schenková et al. 2007).
Glossiphonia complanata is an evenly distributed
species in all types of water bodies: lakes, ponds,
marshes and running water (Bennike 1943). We recorded
G. complanata in both habitat types, with a
preference for lotic habitats. This species was syntopic
with G. concolor and G. complanata, which, however,
did not reach the same abundance. We found that
G. complanata preferably inhabited water at higher
altitudes and water with a sufficient amount of phosphates.
These preferences, together with tolerance to
a higher amount of nitrates and ammonium ions, also
reported by Grosser et al. (2001) and Koperski (2005),
enabled this species to colonise habitats with a high
supply of both oxygen and organic matter. Organic
matter was also essential for the occurrence of molluscs,
the main component of its diet (Elliott & Mann
1979, Neubert & Nesseman 1999).
Infrequent records of G. concolor confirmed its
previously reported preference for stagnant water or
slowly running water from lowlands to moderate elevations
(Košel 1989, Neubert & Nessemann 1999,
Koperski 2006, Schenková et al. 2009). Unfortunately,
its ecological requirements have not yet been statistically
evaluated, also based on insufficient frequencies
in previous studies. New information concerning its
ecological valences was the unusual combination of
preference for habitats with a coarse substratum, typical
for the genus Glossiphonia, and the high percentage
of canopy and littoral/riparian vegetation. Its preference
for shore covered with vegetation, separated its
optimum habitat from the other congeners, G. complanata
and G. nebulosa.
Theromyzon tessulatum was almost absent from
lotic habitats. Its preferred sites were ponds with
abundant water birds. Its chemical preferences (e.g.,
the amount of oxygen, phosphates or total nitrogen)
and saprobe status did not considerably differ from
those reported from the Czech Republic (Košel 1989)
and Germany (Grosser et al. 2001). Similar to Mann
(1955), we recorded distinct behaviour in different
size categories: small individuals were almost exclusively
attached to the vegetation, whereas large, adult
specimens were also found on the underside of stones.
Such a strategy enables young leeches to more easily
attach to birds for feeding and consequently grow
to mature size. Adult leeches that do not feed but are
breeding (Mann 1955), are safer under the stones
(Sawyer 1986).
Hemiclepsis marginata is a species that strongly
prefers lenitic habitats, often weedy ponds (Mann
1955, van Haaren 2004). We usually found H. marginata
on submerged vegetation, most often in eutrophic
ponds with a muddy bottom, higher water temperature
and sufficient fish stock. We recorded the importance
of fine substratum and nitrates in the predictive model.
In contrast to species with similar habitat preferences,
such as H. stagnalis or A. heteroclita, Hemiclepsis
marginata did not prefer high concentrations of chemical
variables, especially phosphates. An unexpected
finding was that this species was not abundant at the
southernmost sites (with the highest mean annual temperatures)
and at sites at the lowest altitudes with the
richest fish stocks. Higher values of chemical parameters
were probably limiting at these habitats. Such
ecological valence might be the cause of its recent
classification among high quality indicator species
(Koperski 2005).
The most common species of the family Glossiphoniidae
was H. stagnalis. The ecological status of
this species is still rather ambivalent. It occurs in heavily
organically polluted waters and is considered as
an indirect indicator of such conditions (Mann 1955,
Sládeček & Košel 1984, van Haaren 2004), whereas
in Poland, it belongs to a group of species that indicates
high quality water (Koperski 2005). The explanation
might be due to its tolerance of high content
of phosphates on the one hand, and to limiting total
nitrogen and nitrates on the other (this study, Grosser
et al. 2001). The latter limitation might cause an undesirable
increase in nutrients without any positive effect
on habitat conditions or the amount of available
diet, which is one of the most important parameters for
the occurrence of H. stagnalis (Elliott & Mann 1979,
Sawyer 1986).
Alboglossiphonia heteroclita is a eurytopic species
that often inhabits eutrophic sites with a high amount
of phosphates, a muddy bottom and a low amount
of oxygen (Mann 1955, Schenková et al. 2009), i.e.,
habitats which provide sufficient food, particularly
oligochaetes, chironomids and molluscs. The importance
of phosphates was confirmed by the predictive
model, which explained a high percentage of the variance.
The tolerance of A. heteroclita to water pollution
was much higher, and its oxygen requirements lower,
than those recorded in Germany (Grosser et al. 2001).
This discrepancy might be caused by differences in the
sampled habitat types; lotic habitats sampled in Sax-
eschweizerbart_xxx
 178 Nela Kubová and Jana Schenková
ony (Germany) might not be polluted to a similarly
high level as some of the lenitic habitats (fish ponds)
included in our study. As a species that prefers lenitic
habitats (Mann 1955, Košel 1989, Koperski 2006),
A. heteroclita cannot be evaluated on the basis of lotic
habitats only and the indication value and saprobe
optimum of A. heteroclita should be re-evaluated to
α-mesosaprobity, according to Košel (1989).
Habitat preferences of less common and rare
leech species (cluster B)
Alboglossiphonia striata and A. hyalina have not been
frequently reported from the Czech Republic (Schenková
et al. 2009). In this study, only a few specimens
were recorded, and therefore, it was impossible to better
describe their ecology.
Piscicola geometra is a common species in Central
Europe: the small number of specimens recorded in
this study was due to the sampling method used. Mann
(1955), who used a similar sampling method for stagnant
as well as running water, also reported P. geometra
as a comparatively rare leech. The small number
of our records might also have led to its positioning in
the cluster analysis near to the rare species A. striata
and A. hyalina, however, with a different ecology. Piscicola
geometra spends most of its life attached to its
fish host, and is therefore more frequently found during
fish catches. Water quality was not a limiting factor
for the occurrence of this leech, but recorded numbers
were probably underestimated in comparison to
its actual numbers (Grosser et al. 2001). In spite of few
records, our results were similar to those in Grosser’s
study (Grosser et al. 2001).
The remaining six species within cluster B were all
very rare during sampling. A small number of records
of G. nebulosa in lotic habitats and an even smaller
number in lenitic habitats, with the exception of the
dominance of 25 specimens at one site, enabled us to
calculate predictive models and visualise box plots.
Due to its semi-aquatic lifestyle, Haemopis sanguisuga
was usually found on the edge of water or
on the shore during sampling: the most typical habitat
was a pond with soft shores at higher altitudes.
Haemopis sanguisuga was always found as a single
specimen per site, except in one case, where 20 copulating
individuals at one site were found. Haemopis
sanguisuga was predominantly found in lenitic habitats,
not only during this sampling but also in previous
studies (Schenková et al. 2009, and unpublished
data). Concerning its altitude preferences, we recorded
this species preferentially at higher altitudes, similar
to findings by Košel (1982), rather than in lowlands
(Neubert & Nessemann 1999, Koperski 2006).
Piscicola haranti is a species only recently reported
from the Czech Republic (Schenková et al. 2009).
Three existing records are now supplemented by one
new record from this study. Since these records belong
to different river basins (Morava and Labe Rivers), the
distribution of P. haranti is probably wider; imprecise
determinations and confusion with P. geometra have
previously lowered its numbers.
Hirudo medicinalis is a critically endangered leech
species in the Czech Republic (Schenková & Košel
2005). The small populations are mostly weak and
mutually isolated by various barriers. One site with a
rather large population of H. medicinalis was included
in our sampling site set, but from this single record,
even general requirements could not be calculated.
Hirudo medicinalis populations were depleted by collecting
for medicinal purposes in the 19th century, and
later by the deterioration in water quality as a consequence
of industrial development at the beginning of
the twentieth century. Changes in the agricultural landscape,
such as the draining of pools, led to a decrease
in the number of amphibians, which are hosts for juvenile
leeches and H. medicinalis populations never recovered
from these dramatic changes. Currently, even
though water quality has improved and amphibians
are more numerous, the availability of suitable habitats,
irrespective of problems of leech dispersion, is
still too low (Elliott & Kutschera 2011).
Dina lineata and Erpobdella testacea from the
family Erpobdellidae are further species that are not
commonly found in the Czech Republic. Similar to
Haemopis sanguisuga, Dina lineata is the second species
that is almost amphibian and it inhabits mostly
shallow littoral areas or soft banks and is scarce in
the Czech Republic. Erpobdella testacea should be
expected in stagnant water (Neubert & Nessemann
1999), but our record from running water shows that
its distribution should not be solely associated with
this habitat type.
A few leech species whose occurrence could be expected
within the study area remained completely undiscovered
from various reasons. Caspiobdella fadejewi
(Epshtein, 1961) from the family Piscicolidae
and Erpobdella nigricollis (Brandes, 1900) from the
family Erpobdellidae are relatively frequent, but both
inhabit rather large rivers with slow current (Schenková
et al. 2009) which were not included in the sampling.
Absence of Piscicola fasciata Kollar, 1842 and
Piscicola respirans Troschel, 1850 (family Piscicolidae)
was probably caused by sampling method inap-
eschweizerbart_xxx
179Tolerance, optimum ranges and ecological requirements of free-living leech species
propriate to their collection (they live attached to the
fish host) and their relative rarity. Trocheta cylindrica
Örley, 1886 (family Erpobdellidae) was also not recorded,
as it is an infrequent species with semiaquatic
life. Nevertheless, gaining information about habitat
preferences of these species is a challenging task for
further research.
Conclusions
The results of this study show the fundamental importance
of the type of habitat (lotic versus lenitic).
Box plots visualising the preferred ranges of twelve
physico-chemical variables of nine medium-frequent
to frequent species, enabled a comparison between the
species ecological requirements. Predictive models
based on linear regression were produced for Erpobdella
octoculata, Erpobdella vilnensis, Glossiphonia
complanata, Helobdella stagnalis, Alboglossiphonia
heteroclita, Hemiclepsis marginata and Theromyzon
tessulatum. For each of the evaluated species, certain
morphological and also chemical variables were relevant.
For future surveys of the ecological demands
of rare species, special sampling that focuses on their
preferred habitats will be required.
Acknowledgements
The authors would like to thank two anonymous reviewers
for their constructive critique of this manuscript and Veronika
Schenková for assistance in improving the English. This research
was supported by the Ministry of Education, Youth
and Sports (MSM 0021622416) and MUNI/A/0888/2013. We
would like to thank Marcela Růžičková and Stanislav Němejc
for their technical assistance.
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Submitted: 20 November 2013; accepted: 17 July 2014.
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6. Seznam dalších publikací k tématu habilitační práce
Publikace v recenzovaných časopisech a monografiích
Horsák M., V. Rádková, J. Bojková, V. Křoupalová, J. Schenková, V. Syrovátka & J.
Zajacová, 2015. Drivers of aquatic macroinvertebrate richness in spring fens in relation
to habitat specialization and dispersal mode. J. Biogeogr. 42(11), 2112–2121.
Glombová, J. & J. Schenková, 2015. Habitat preferences and ventral color variability of
Hirudo medicinalis (Clitellata: Hirudinida). Ecologica Montenegrina, Podgorica
(Montenegro) 2(1), 51–61.
Kubová, N. & J. Schenková, 2012. A comparison of two semi-quantitative methods for freeliving
leeches (Clitellata: Hirudinida) collecting. Lauterbornia 75(3), 79–86.
Schenková, J. & J. Kroča, 2007. Seasonal changes of an oligochaetous Clitellata (Annelida)
community in a mountain stream. Acta Universitatis Carolinae: Environmentalica 21,
145–152.
Schenková, J. & V. Košel, 2005. Hirudinea (pijavice). In Farkač, J., D. Král & M. Škorpík.
Červený seznam ohrožených druhů České republiky. Bezobratlí. Red list of threatened
species in the Czech Republic. Invertebrates. Praha: Agentura ochrany přírody a krajiny
ČR, 67–68.
Schenková, J., 2005. Oligochaeta (máloštětinatci). In In Farkač, J., D. Král & M. Škorpík.
Červený seznam ohrožených druhů České republiky. Bezobratlí. Red list of threatened
species in the Czech Republic. Invertebrates. Praha: Agentura ochrany přírody a krajiny
ČR, 62–64.
Schenková, J., 2005. Polychaeta (mnohoštětinatci). In Farkač, J., D. Král & M. Škorpík.
Červený seznam ohrožených druhů České republiky. Bezobratlí. Red list of threatened
species in the Czech Republic. Invertebrates. Praha: Agentura ochrany přírody a krajiny
ČR, 60–61.
Schenková, J. & O. Komárek, 1999. Oligochaeta of the Morava River Basin: distribution
patterns, community composition and abundance. Scripta 1999, 33–52.
Schenková, J., O. Komárek & S. Zahrádková, 2001. The plausibility of using Oligochaeta to
evaluate running waters in the Czech Republic. Scripta 2001, 173–187.
Populární publikace
Schenková, J. & K. Tajovský. 2007. Kroužkovci. In Hudec, K., J. Kolibáč, Z. Laštůvka & M.
Peňáz et al. (eds), Příroda České republiky Průvodce faunou. 1. vydání. Praha,
Academia, 36–41.
Konferenční vystoupení
Schenková, J., M. Bílková & J. Schlaghamerský. Can oligochaete assemblages predict an
ecological type of treeless spring fens? In 13th International Symposium on Aquatic
Oligochaeta, 2015, Brno. (Přednáška).
Schenková, J., M. Horsák & M. Bílková, 2015. Máloštětinatí opaskovci a jejich odezva na
podmínky prostředí na prameništních slatiništích. In Zoologické dny 2015, Brno.
(Přednáška)
Schenková, J., M. Bartošová, V. Křoupalová & I. Přikryl, 2014. Bentická fauna pěnovcových
potoků na Velké podkrušnohorské výsypce. In Zoologické dny 2014, Ostrava. (Poster)
248
Schenková, J., V. Opravilová & J. Helešic, 2013. Diverzita mikro-meiofauny na řekách
Rokytné a Loučce. In Zoologické dny 2013, Brno. (Přednáška)
Schenková, J., M. Bílková & J. Bojková, 2012. Variabilita vodních opaskovců (Clitellata) na
slatiništích vnějších Západních Karpat. In XVI. Konferencia Slovenskej limnologickej
spoločnosti a České limnologické společnosti 2012, Jasná. (Přednáška)
Schenková, J., J. Sychra & N. Kubová, 2011. The freshwater leeches (Clitellata: Hirudinida)
of the Czech Republic – preference of different types of water bodies. In 4th
International Conference Hirudinea: biology, taxonomy, faunistics 2012, Wierzba,
Poland. (Přednáška)
Schenková, J., P. Pařil, K. Petřivalská & J. Bojková, 2011. Vodní máloštětinatci (Annelida:
Clitellata) České republiky. In Zoologické dny 2011, Brno. (Přednáška)
Schenková, J., J. Bojková, V. Křoupalová A M. Horsák, 2010. Variabilita opaskovců
(Annelida: Clitellata) na minerálně-trofickém gradientu prameništních slatinišť:
srovnání velké a malé prostorové škály. In Zoologické dny 2010, Praha. (Přednáška)
Schenková, J., V. Křoupalová, M. Horsák & J. Bojková, 2009. Comparison of clitellate
assemblages (Annelida: Clitellata) in two different mineral types of spring fens: the
response in permanent fauna abundance and species richness. In 11th International
Symposium on Aquatic Oligochaeta 2009, Alanya, Türkiye. (Přednáška)
Schenková, J., P. Pařil & K. Petřivalská, 2009. Od Hraběte po současnost - aneb co víme o
máloštětinatých červech v Čechách. In 15. konference České limnologické společnosti a
Slovenskej limnologickej spoločnosti 2009, Třeboň. (Přednáška)
Schenková, J., J. Sychra, V. Košel, N. Kubová & J. Horecký, 2009. Pijavice (Clitellata:
Hirudinida) České republiky: check-list, nové nálezy a poznámky k šíření druhů. In
Zoologické dny 2009, Brno. (Přednáška)
Schenková, J., J. Špaček & J. Sychra, 2007. Dva nové druhy pijavic (Hirudinida)
Alboglossiphonia hyalina (O. F. Müller, 1774) a Glossiphonia verrucata (Fr. Müller,
1844) pro Českou republiku. In Zoologické dny 2007, Brno. (Poster)
Schenková, J. & J. Kroča, 2006. Sezónní změny společenstva máloštětinatců (Oligochaeta,
Annelida) horského toku Moravskoslezských Beskyd. In 14. konference České
limnologické společnosti a Slovenskej limnologickej spoločnosti 2006, Praha.
(Přednáška)
Schenková, J., J. Helešic & J. Jarkovský, 2005. Life strategies and habitat preferences of two
competing species: Erpobdella octoculata and Erpobdella vilnensis (Annelida:
Hirudinea). In Symposium RIVER BOTTOM VI Brno. (Přednáška)
Schenková, J. & J. Helešic, 2004. Záleží akvatickým máloštětinatcům (Oligochaeta) na
prostředí ve kterém žijí? In Zoologické dny 2004, Brno. (Přednáška)
Schenková, J. & J. Helešic, 2003. Akvatická Oligochaeta - máloštětinatci a jejich habitatové
preference. In Zoologické dny 2003, Brno. (Přednáška)
Schenková, J. & J. Helešic, 2003. Habitat preferences of aquatic Oligochaeta in a small
highland stream (Czech Republic). In 9th International symposium on aquatic
Oligochaeta 2003, Wageningen, the Netherlands. (Poster)