MASARYKOVA UNIVERZITA
Přírodovědecká fakulta
Tomáš Bartonička
Parazitace štěnicemi u netopýrů a člověka
Habilitační práce
Brno 2015
Poděkování
Předkládaný soubor studií by pravděpodobně nikdy nevznikl bez přispění spoluautorů, ať již
se jednalo o zkušenější kolegy nebo studenty, kteří do svých diplomových a doktorských
prací dali nejen ducha, ale často i tělo. Velký dík patří zejména Zdeňku Řehákovi, který mě
jednak uvedl do motivujícího pracovního prostředí ÚBZ PřF MU, ale byl mi vždy ochoten
pomoci či poradit v nesnázích. Nemalý dík si zaslouží i Jiří Gaisler, kterého problematika
štěnic zaujala již v počátcích mých úvah a dovedl mě správně nasměrovat. Oběma kolegům
pak vděčím též za inspirativní mezioborový přístup, který si takové téma vyžádalo. Za mnohé
motivující diskuze vděčím i O. Balvínovi. Velké poděkování patří mé ženě, která měla
pochopení pro mé pozdní příchody domů, i mým rodičům, kteří mě podporovali od dětství.
Obsah
1. Struktura habilitační práce a její cíle...................................................................................... 4
2. Úvod....................................................................................................................................... 5
3. Problematika........................................................................................................................... 6
3.1 Model parazit a hostitel.................................................................................................... 6
3.2 Využívání a střídání úkrytů u netopýrů............................................................................ 7
3.3 Úkrytoví ektoparaziti netopýrů ...................................................................................... 11
3.4 Stručný přehled systematiky rodu Cimex ...................................................................... 12
3.5 Životní cyklus štěnic a přežívání v úkrytech netopýrů .................................................. 16
3.6 Štěnice, její šíření a jako vektor patogenů...................................................................... 19
3.7 Vliv štěnic na chování netopýrů..................................................................................... 22
3.8 Hostitelská specifita štěnic............................................................................................. 26
3.5 Transport štěnic netopýry............................................................................................... 30
4. Závěr..................................................................................................................................... 33
5. Použitá literatura .................................................................................................................. 33
6. Komentář k publikacím........................................................................................................ 43
7. Úroveň spoluautorství a hlavní přínos předkládaných studiích ........................................... 44
8. Seznam publikovaných vědeckým prací k tématu habilitační práce.................................... 49
8.1 Využívání a střídání úkrytů u netopýrů
(1) BARTONIČKA T. & ŘEHÁK Z., 2007: Influence of the microclimate of bat boxes
on their occupation by the soprano pipistrelle Pipistrellus pygmaeus: possible cause of
roost switching. Acta Chiropterologica, 9(2): 517–526. (IF=0,831)
(2) BARTONIČKA T., BIELIK A. & ŘEHÁK Z., 2008: Roost switching and activity
patterns in the soprano pipistrelle, Pipistrellus pygmaeus, during lactation. Annales
Zoologici Fennici 45(6):503-512. (IF=1,03)
8.2 Životní cyklus štěnic a přežívání v úkrytech netopýrů
(3) BARTONIČKA T. & GAISLER J., 2007: Seasonal dynamics in the numbers of
parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost switching in bats
(Chiroptera, Vespertilionidae). Parasitology Research, 100:1323–1330. (IF=2,327)
(4) BARTONIČKA T., 2010: Survival rate of bat bugs (Cimex pipistrelli, Heteroptera)
under different microclimatic conditions. Parasitology Research, 107:827–833.
(IF=2,327)
(5) BARTONIČKA T. & RŮŽIČKOVÁ L., 2013: Recolonization of bat roost by bat
bugs (Cimex pipistrelli): could parasite load be a cause of bat roost switching?
Parasitology Research, 112:1615–1622. (IF=2,327)
8.3 Vliv štěnic na chování netopýrů
(6) BARTONIČKA T., 2008: Cimex pipistrelli (Heteroptera, Cimicidae) and the
dispersal propensity of bats: an experimental study. Parasitology Research, 104:163–168.
(IF=2,327)
(7) BARTONIČKA T. & RŮŽIČKOVÁ L., 2012: Bat bugs (Cimex pipistrelli) and their
impact on non-dwelling bats. Parasitology Research, 111:1233–1238. (IF=2,327)
8.4 Hostitelská specifita štěnic
(8) WAWROCKA K. & BARTONIČKA T., 2013: Two different lineages of bedbug
(Cimex lectularius) reflected in host specificity. Parasitology Research, 112: 3897-904.
(IF=2,327)
9. Seznam dalších publikací k tématu
1. Struktura habilitační práce a její cíle
Předložená habilitační práce se skládá z osmi vědeckých publikací. Jednotícím tématem
habilitační práce je výzkum úkrytových strategií netopýrů s následným posunem k
antiparazitárnímu chování vůči jejich nejběžnějším úkrytovým ektoparazitům – štěnicím.
Habilitační práce má mezioborový vertebratologicko-parazitologický charakter a je doplněna
o úvod do problematiky. Shrnující úvod je koncipován jako představení zásadních poznatků
publikovaných v přiložených studiích, které jsou zasazeny do širšího kontextu problematiky
životních strategií a ekologicko-biologických charakteristik studovaného modelu štěnice -
netopýr.
Hlavní cíle habilitační práce:
1. U vybraných štěrbinových druhů netopýrů popsat změny v sezónním využívání
úkrytů.
2. Definovat faktory, které mohou hrát roli ve změnách využívání úkrytů.
3. V terénních i laboratorních podmínkách testovat vybrané faktory ovlivňující
využívanost úkrytů.
4. Popsat a sledovat antiparazitární strategie netopýrů s ohledem na jejich úkrytové
parazity.
5. Sledovat vliv dočasného opouštění úkrytů netopýry na denzity štěnic.
6. Zjistit rychlost rekolonizace netopýřích úkrytů štěnicemi.
7. Testovat hostitelskou specifitu štěnice domácí (Cimex lectularius) parazitující
na netopýrech a člověku.
4
2. Úvod
Studium vztahu parazit – hostitel patří nepochybně k vděčným biologickým tématům.
V tomto směru však netopýři nepatřili nikdy k typické modelové skupině hostitelů. Většina
studií věnovaná jejich ektoparazitům byla zaměřena spíše faunisticky a vzájemné interakci se
věnovala pouze okrajově. Tradičně studovaní ektoparazité netopýrů tráví na těle hostitele
většinu svého ontogenetického vývoje a na chování hostitele související s úkrytovými
strategiemi mají pouze omezený vliv. Zcela odlišná je však situace u štěnic, které na těle
hostitele tráví pouze krátkou dobu během sání krve a většinu života žijí mimo hostitele. Díky
rychlému vývoji a velkému reprodukčnímu potenciálu na jedné straně a značné mobilitě na
straně druhé patří štěnice nepochybně k významným ektoparazitům nejen netopýrů, ale i
člověka. Štěnice v úkrytech netopýrů však žijí skrytým způsobem a snad i proto jim byla
v minulosti věnována pouze malá pozornost. Štěnice si netopýři na svých tělech přenášejí
pouze ojediněle na rozdíl od ostatních permanentních ektoparazitů (např. muchulí a roztočů),
a to z nich činí jedinečný model při výzkumu adaptivních úkrytových strategií netopýrů.
Vztah netopýrů a úkrytových parazitů, jako jsou štěnice, byl doposud z velké části založen
pouze na předpokladech. Přiložené publikace, vycházející z terénního pozorování a
následných experimentů, objasňují, jak významným stresorem štěnice pro netopýry jsou,
jakým způsobem jsou provázány reprodukční cykly netopýrů a štěnic, a částečně také
objasňují hostitelskou specifitu štěnic ve vztahu k člověku.
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3. Problematika
3.1 Model parazit a hostitel
Podrobné studie o mezi- a vnitro-druhových mechanismech jsou nezbytné pro správné
pochopení celkové biodiverzity. Vzhledem k rozmanitosti a složitosti životních strategií a
vztahů k hostiteli jsou parazitické organismy velmi zajímavými a hodnotnými modely
v evolučně-ekologických studiích. Prezentují celou škálu různých typů speciace a koevoluce
(Huyse et al. 2005). Úroveň speciace a diverzifikace parazita pramení ze stupně závislosti na
hostiteli a jeho životních strategiích. Dále je pak závislá na počtu preferovaných hostitelů,
oblastí jejich výskytu, populační struktuře hostitelů a charakteru jejich rozptýlení v čase a
prostoru (Esch et al. 1975). V populacích parazita se pak setkáváme s určitými podjednotkami
- démy (populace parazita na sociální skupině hostitele více či méně izolovaná od jiných
hostitelských démů) a infrapopulacemi (populace parazita z jednoho hostitelského jedince),
které představují různý stupeň izolace mezi sebou (Mayr 1963). U štěnic parazitujících na
netopýrech nebo ptácích, kteří většinu života tráví mimo tělo hostitele, je však termín
infrapopulace obtížně použitelný. Je proto vhodnější u nich používat termín dém. Ten je zde
reprezentován populací parazita v jednom úkrytu nebo hnízdě.
Jestliže předpokládáme, že polymorfismus v populaci parazita souvisí s preferencí
určitých životních podmínek (určitá část těla hostitele nebo část jeho úkrytu), je
pravděpodobné, že parazit bude mít tendenci lépe přežívat jen v některých z nich.
V podmínkách, kde bude vykazovat vyšší fitness, bude hledat i svého sexuálního partnera a
bude se tedy pářit s dostupnými jedinci podobných genotypů. To však logicky povede ke
snížení genového toku mezi jednotlivými démy parazita. Schopnost parazita přežívat na
větším spektru hostitelských druhů vede nejen k vyššímu polymorfismu (Brooks &
McLennan 1993), ale též v případě dalšího omezování genového toku k sympatrické speciaci
(např. v případě adaptace jedné sub-populace parazita na jiný hostitelský druh), která následně
vede opět k obnovení úzké specificity vůči (novému) hostitelskému druhu (Combes & Théron
2000). Ačkoliv je sympatrická speciace (bez existence geografické bariéry) ekology tradičně
odmítána, podmínky ve vztahu parazit a hostitel ji umožňují a často je označována termínem
alloxenická speciace (Melhorn 2008).
Lokální diferenciace zdůrazňuje závody ve zbrojení (host races) mezi hostitelem a
parazitem (Drès & Mallet 2002). Koncept závodů ve zbrojení bývá často definován z více
směrů 1) střídání hostitelských druhů a z ní vyplývající různá věrnost a závislost na hostiteli,
2) soužití v sympatrii s jediným hostitelem nebo 3) vztah mezi vyhledáváním sexuálního
6
partnera a změnou hostitele (Funk 2012). Důsledkem toho jsou pak například genetické
diferenciace nebo obecné ovlivnění toku genů v rámci populace parazita či mezi nimi.
S ohledem na stupeň diferenciace mezi jednotlivými entitami parazitů, je pak
pravděpodobnost opakování těchto změn v časoprostoru vyšší. Na druhou stranu je
pravděpodobnost fixace nové charakteristiky parazita závislá na efektivní velikosti jeho
populace, jeho životním cyklu, plodnosti, stupni závislosti na hostiteli, migralitě hostitele či
kolonizaci nových hostitelských skupin (Gandon & Michalakis 2002, Barrett et al. 2008).
3.2 Využívání a střídání úkrytů u netopýrů
Věrnost úkrytům není u mnoha druhů savců příliš vysoká a v případě druhů netopýrů
využívajících úkryty ve stromech je dokonce poměrně nízká (Lewis 1995). Terénní
pozorování dokládají, že druhy netopýrů přes den využívající štěrbinové úkryty, je střídají
několikrát za reprodukční sezónu, dokonce i každých několik dní (Lausen & Barclay 2002,
Mazurek 2004, Rancourt et al. 2005). Takové chování bylo pozorováno právě u druhů
využívajících úkryty ve stromech (např. Myotis californicus, Barclay & Brigham 2001;
Eptesicus fuscus, Willis & Brigham 2004). Štěrbinové úkryty ve stromech využívá i řada
zástupců evropských rodů Nyctalus, Pipistrellus a Myotis; z posledně jmenovaného rodu pak
především malé druhy jako M. bechsteinii, M. daubentonii, M. nattereri, M. mystacinus a M.
brandtii (Meschede & Heller 2000, Kerth et al. 2001, Meschede 2001). K dalším druhům
netopýrů rodící svoje mláďata ve stromových úkrytech dále patří i Plecotus auritus a
Barbastela barbastellus.
Úkryty ve stromech jsou často různého typu, může jít o dutiny, vzniklé činností
některých datlovitých ptáků nebo vyhníváním, štěrbiny a pukliny v rozsochách větví nebo za
odchlípnutou borkou (Vonhof & Barclay 1996). Dnes existují již práce věnované tomu, jaký
typ dutin netopýři upřednostňují (teplota, vlhkost, velikost, tvar, výška a orientace vletového
otvoru, hloubka dutiny, mocnost stěny dutiny), aby byl pro netopýry atraktivní (Sedgeley &
O’Donnell 1999, Gibbons et al. 2002, Russo et al. 2004, Willis & Brigham 2005, Spada et al.
2008, Ruczyński et al. 2010).
U výše zmíněných druhů se však v řadě případů setkáme s letními koloniemi i v
náhradních typech antropogenních úkrytů (Russo et al. 2004). Situace, kdy jeden druh
netopýra využívá jak přirozené typy úkrytů, tak štěrbinové typy úkrytů v budovách, je stále
častější. S rostoucí synantropizací některých druhů roste jejich vazba na úkryty v budovách a
postupně klesá využívanost úkrytů ve stromech. Do této skupiny patří např. netopýr rezavý
(Nyctalus noctula) (Boonman 2000), ale i dvojice druhů Pipistrellus pipistrellus a Pipistrellus
7
pygmaeus (Thompson 1992, Park et al. 1996, Ceľuch et al. 2006). Netopýři využívají jak
dřevěné stavby (posedy, seníky, sruby), tak se mohou ukrývat za dřevěným obložením stěn,
za okenicemi nebo ve šterbinách pod střešní krytinou běžných lidských stavení. Ale některé
druhy využívají i štěrbiny mezi panely nebo větrací šachty v panelových domech (N. noctula,
P. pipistrellus, Ceľuch et al. 2006).
Řada z přirozených úkrytů má krátkou životnost (odchlípnutá kůra, Grindall 1996,
Grindall 1999) a nedává netopýrům jinou volbu, než úkryt změnit (Grindal & Brigham 1998).
Naopak úkryty v dutinách a zejména budovách jsou plně dostačující po více roků a přesto je
netopýři pravidelně střídají. Jarní osidlování úkrytů je dočasné a jsou využívány na cestě ze
vzdáleného zimoviště do místa reprodukce (Dzal et al. 2009). V létě jsou stromové dutiny,
půdy budov či různé štěrbiny využívány samicemi jako místo úkrytu reprodukční kolonie.
Shromažďují se v nich různě početné skupiny, které zde rodí a odchovávají svá mláďata.
Samci tráví letní období solitérně. Ve druhé polovině léta, kdy se po osamostatnění mláďat
rozpadají reprodukční kolonie, a počátkem podzimu, jsou dutiny ve stromech nebo obložení
domů využívány jako úkryty, kde se netopýři dočasně shromážďují při přesunu na místo
zimování (Dzal et al. 2009). Pohlavně dospělí jedinci některých druhů se v dutinách páří. U
některých z nich se projevuje teritoriální chování, kdy samci po obsazení dutiny hájí tento
úkryt před jinými samci. V té době vznikají i nestabilní harémové skupiny (např. netopýři
rodu Pipistrellus), tvořené nejčastěji jedním samcem a několika samicemi (Jahelková et al.
2000).
Dalším faktorem ovlivňujícím obsazenost úkrytu v určité části vegetační sezóny je
blízkost bohatého potravního stanoviště (Boonman 2000). Blízký výskyt vodního biotopu je
obvykle zárukou vysoké potravní nabídky. Ta je též vysoká na okrajích porostů a v úzkých
průletových koridorech (Kusch et al. 2004). Netopýři se také během reprodukční sezóny
mohou přesunout do jiného úkrytu v závislosti na změně potravní nabídky (Davidson-Watts
& Jones 2006).
Řada studií ukazuje, že samice některých druhů nejsou omezeny pouze na úkryt
v konkrétním stromě, ale jedna kolonie se může rozdělit do více úkrytů (Kerth & König 1999,
Willis & Brigham 2004). Tato sociální struktura, popsaná jako fission-fusion model, může
pomoci udržet řadu výhod spojených s životem ve velké kolonii a současně omezit některé
jeho nevýhody. Fission-fusion model byl u evropských netopýrů popsán detailně na druhu
Myotis bechsteinii (Kerth & König 1999). Podskupiny vzájemně velmi příbuzných samic
střídají úkryty na poměrně malém území velmi často, obvykle každý 2. - 4. den (Kerth &
König 1996). Podobné chování bylo zjištěno i u řady běžných severoamerických druhů
8
netopýrů jako např. Eptesicus fuscus nebo Myotis lucifigus (Barclay et al. 1979, Willis &
Brigham 2004). Rozptyl jediné kolonie mezi více úkrytů se může na první pohled jevit jako
intenzivní střídání úkrytů více koloniemi. U druhů tvořících početné kolonie v budovách
(např. M. myotis) dochází též k výměně jedinců. Samice se však nepřesouvají všechny naráz a
do stejného úkrytu. Nedochází tedy pravidelně k situacím, kdy všichni netopýři úkryt opustí
během jediné noci, jako je to pozorováno u štěrbinových druhů osidlujících stromy.
Pravděpodobně nejčastěji uváděným důvodem střídání úkrytů jsou odlišné teplotní
preference a požadavky na prostor se zvyšujícím se počtem jedinců ve skupině v průběhu
roku (Whitaker 1998, Lefebvre et al. 2003). Teplotní a vlhkostní preferendum se liší jednak
podle druhu netopýra (Harmata 1969) a jednak podle fáze reprodukčního cyklu (gravidita,
laktace, postlaktační období, harémové úkryty) (např. Gaisler 1970, Lourenço & Palmeirim
2004). Netopýři si vybírají pro každé období úkryt s optimálními mikroklimatickými
podmínkami (Kerth et al. 2001, Lourenço & Palmeirim 2004). Nepochybně znají alternativní
úkryty, včetně jejich mikroklimatu v předstihu, jelikož pátrání po novém úkrytu až v případě
potřeby souvisí s dalšími energetickými náklady a mohlo by znamenat značné riziko např.
úhynu mláďat, potratu apod. (Lewis 1995).
V roce 2002 byl na PřF MU, PřF UK a AVČR zahájen výzkum komplexu hemisynantropních
netopýrů rodu Pipistrellus (projekty GAČR 206/06/0954 Intraspecific
variability of populations of two cryptic bat species of genus Pipistrellus in Central Europe,
GAČR 206/02/0961 „Situation Pipistrellus pipistrellus superspecies in Czech Republic“).
Výzkum byl zaměřen zejména na rozšíření a vztahy dvou středoevropských druhů Pipistrellus
pipistrellus a tehdy čerstvě popsaného Pipistrellus pygmaeus. Před rokem 2000 oba druhy
nebyly na území České republiky a většiny Evropy rozlišovány a v této práci i publikacích
následujících jsou u starších údajů uváděny jako P. pipistrellus sensu lato (s.l.). V souvislosti
s intenzivním výzkumem těchto netopýrů byla zjištěna i řada behaviorálně-ekologických
poznatků souvisejících zejména s obsazováním úkrytů. Z našeho pozorování (Bartonička
2004, Bartonička & Řehák 2007) vyplývá, že samice P. pygmaeus, podobně jako samice P.
pipistrellus, mění úkryty během letního období několikrát. Počátkem června gravidní samice
sledované úkryty opuštěly a vracely se do něj i se svými vzletnými mláďaty teprve v polovině
července. Thompson (1992) zjistil, že většina jím pozorovaných kolonií P. pipistrellus s.l.
během reprodukční sezóny využívá 2 až 3 úkryty a pouze 20% kolonií navštěvovalo úkrytů
více. Feyerabend & Simon (2000) sledovali pomocí telemetrie u jediné kolonie P. pipistrellus
s.l. přesuny mezi osmi úkryty během dvou let. Bartonička et al. (2008) telemetricky zjistili, že
označené kojící samice P. pygmaeus přeletovaly mezi 2-3 úkryty. Společné však většině
9
pozorování je, že samičí kolonie obou druhů několik dní před obdobím porodů opustí
dosavadní úkryt a přesunou se do hlavního porodního úkrytu (Swift 1980, Webb et al. 1996).
Bartonička et al. (2008) nikdy nezjistili, že by všechny samice opustily hlavní porodní úkryt
v budově v průběhu laktace, zatímco satelitní úkryty, kam se přesouvala vždy pouze část
kolonie, ano. Bohužel telemetricky byly samice sledovány pouze v průběhu laktace a není
tedy známo, zda změnily úkryty využívané v graviditě. Z výše uvedeného je tedy zřejmé, že
netopýři rodu Pipistrellus střídají úkryty častěji než synantropní druhy osidlující půdy budov
(např. M. myotis). Ačkoliv jsme v článku Bartonička et al. (2008) toto chování viděli jako
analogické s chováním definovaným výše jako fission-fusion model, pozdější naše studie
ukázaly, že netopýři rodu Pipistrellus využívají jeden úkryt na dobu výrazně delší než je
uváděna ve studii Kerth & König (1999).
Výše je nastíněno několik aspektů, které ovlivňují střídání úkrytů netopýry. Přestože je
zřejmé, že u různých druhů jsou důvody odlišné a všechny nejsou doposud uspokojivě
vysvětleny (Lewis 1995, Vonhof & Barclay 1996, Brigham et al. 1997), lze je dle dostupné
literatury shrnout do čtyř možných skupin:
 náhlé změny mikroklimatických podmínek související s omezenou cirkulací vzduchu
ve štěrbinovém úkrytu (Whitaker 1998, Lourenço & Palmeirim 2004) nebo změna
v nárocích na mikroklima úkrytu s ohledem na reprodukční cyklus (gravidita versus
laktace) (např. Thompson 1990, Hamilton & Barclay 1994, Kerth et al. 2001).
 vyhnutí se vzrůstající parazitaci s cílem udržení tělesné kondice nebo snížení rizika
postnatální mortality mláďat (Wolz 1986, Lewis 1996).
 rušení lidskou činností, predátorem nebo jiné neznámé vlivy (Lewis 1995).
 dostupnost potravní nabídky v blízkosti úkrytů (Willis & Brigham 2004, Fleischmann
& Kerth 2014)
V naší studii Bartonička & Řehák (2007) jsme testovali hypotézu, která předpokládala
střídání úkrytů v důsledku potřeby jiného mikroklimatu v průběhu gravidity, kdy se samice
snaží využívat maximálně stav denní strnulosti, a laktace, kdy naopak při častém kojení
mláďat samice upadat do strnulosti nemohou (Kerth et al. 2001). Ve vnitřní teplotě
zkoumaných netopýřích budek jsme nezjistili žádné rozdíly mezi budkami obsazenými a
neobsazovanými, jak v průběhu gravidity, tak během laktačního období. Vnitřní teplota
negativně korelovala s větším počtem netopýrů, zejména během gravidity (Obr. 1). V období
před odletem z obsazených budek (v období gravidity) nebyly zjištěny žádné extrémní
výkyvy ve vnější teplotě, které by mohly souviset s opuštěním úkrytu v souvislosti s jeho
10
přehřátím. Nebyly zjištěny ani rozdíly ve vnitřní teplotě mezi úkryty, které netopýři před
porody opustili a kde zůstali, přestože signifikantní rozdíly mezi reprodukčními obdobími
nalezeny byly. Naše výsledky potvrzují, že samice před porody nejsou motivovány k přesunu
výhradně mikroklimatickými podmínkami, přestože se mezi graviditou a laktací mění jejich
možnost využívat denní letargie. Důvod přesunu samic v období před porodem mláďat studií
spolehlivě objasněn nebyl.
Obr. 1. Negativní vztah mezi počtem netopýrů a vnitřní teplotou, grafický výstup
generalizovaného aditivního modelu. Šedá zóna označuje 95% intervaly spolehlivosti a číslo
v závorce na y ose udává stupně volnosti.
3.3 Úkrytoví ektoparaziti netopýrů
Obvykle jsou studována společenstva ektoparazitů různých druhů netopýrů bez ohledu
na jejich životní strategie (např. Whitaker & Mumford 1978, Morkel 1999, Whitaker et al.
2000, Ritzi et al. 2001, Ritzi & Whitaker 2003). Na netopýrech bylo zjištěno více než 680
druhů parazitujícího hmyzu (Arixeniidae, Cimicidae, Polyctenidae, Nycteribiidae, Streblidae,
Ischnopsyllidae, Tungidae) a dále především roztočů včetně klíšťat (Argasidae, Ixodidae,
Acaridae, Glycyphagidae, Sarcoptidae, Laelapidae, Macronyssidae, Spinturnicidae,
Demodecidae, Myobiidae a Trombiculidae) (Scheffler 2011). Většina výzkumů, které se
zabývaly ekologickými souvislostmi vztahu ektoparazit – netopýr, je však realizována na
ektoparazitech permanentních respektive takových, kteří tráví na těle netopýra většinu svého
života (např. Hůrka & Povolný 1968, Gannon & Willig 1995, Sasse & Pekins 2000, Moura et
al. 2003). Některé publikace řeší přímo problematiku koevoluce ektoparazita a hostitelského
druhu netopýra (např. Patterson et al. 1998). Specifita ektoparazita je závislá na historickofylogenetických,
fyziologických, biochemických nebo behaviorálně morfologických
11
faktorech (Ryšavý et al. 1988, Volf & Horák 2007). Extrémně dlouhá doba koexistence blech
(Ischnopsyllidae) a muchulí (Nycteribiidae) s netopýry je mezi savci ojedinělá a poskytla
oběma skupinám dostatek času na koadaptaci (Horáček 1986). Není tedy divu, že vysoká
úroveň závislosti na hostiteli byla opakovaně v centru zájmu výzkumníků (např. Grulich &
Povolný 1955, Rosický 1957).
Ektoparazitům trávícím na svém hostiteli pouze krátký čas potřebný k sání krve, tzv.
úkrytovým parazitům, však byla dosud věnována pouze omezená pozornost.
K nejvýznamnějším úkrytovým ektoparazitům netopýrů patří zástupci roztočů (Acari),
klíšťáci čeledi Argasidae (např. klíšťák netopýří Carios vespertilionis) a zejména štěnice
čeledi Cimicidae. Tito obligátní ektoparazité recentně téměř výhradně asociovaní s ptáky,
netopýry a člověkem mají dorzoventrálně zploštělé tělo a silně sklerotizovaný integument,
což snižuje poškození při pohybu ve štěrbinách a usnadňuje tak únik před hostitelem (Usinger
1966, Marshall 1980). Čeleď Cimicidae zahrnuje asi 110 druhů zařazených do 24 rodů a šesti
podčeledí (Henry 2009). Zástupci této čeledi jsou přítomni na všech kontinentech; pouze z
Austrálie nejsou známy původní druhy (Usinger 1966).
Omezení štěnic na letouny je poměrně úzké a netradiční ve srovnání s jinými
krevsajícími skupinami hmyzu. Navíc se zdá, že netopýři jsou pravděpodobně původní
hostitelé štěnic (Horváth 1913), zejména pak čeledi Vespertilionidae a Molossidae (Marshall
1982). Asi dvě třetiny z celkového počtu druhů uvedených výše, parazituje na netopýrech a
z nich některé příležitostně sají i na člověku. Nejméně tři taxony z podčeledi Cimicinae
parazitují však na lidech pravidelně a vytváří na nich stabilní populace: Cimex lectularius
(Linnaeus, 1758), Cimex hemipterus (Fabricius, 1803) a Leptocimex vespertilionis (Ferris &
Usinger, 1957) (Usinger 1966, Marshall 1981, Balvín 2013).
Vysoká mobilita a schopnost dlouhodobé existence mimo hostitele staví štěnice mezi
význačné modelové ektoparazity (Usinger 1966). Tělo hostitele využívají pouze k sání krve a
k transportu do dalších hostitelských úkrytů.
3.4 Stručný přehled systematiky rodu Cimex
V úvodu do problematiky je třeba zmínit, že kompletní systematika čeledi Cimicidae
dosud není zcela ujednocena a v literatuře se setkáváme s jejím různým pojetím. Druhy rodu
Cimex jsou podle tradičních morfologických kritérií děleny do čtyř skupin (Usinger 1966).
1. Skupina kolem druhu Cimex pilosellus (Horváth, 1910) zahrnuje několik druhů
žijících na netopýrech a občas i na člověku v Severní a Střední Americe.
12
2. Do skupiny druhů Cimex lectularius náleží druh Cimex lectularius (Obr. 2a, 3), který
parazituje na netopýrech, člověku, domestikovaných a (hemi)synantropních druzích
savců, a dále Cimex columbarius Jenyns, 1839 vyskytující se na drůbeži a holubech.
Posledním druhem skupiny je Cimex emarginatus známý pouze z netopýra brvitého
(Myotis emarginatus).
3. Skupina druhů kolem Cimex pipistrelli parazituje pouze na netopýrech (Obr. 2b, 3).
Přestože občas napadají i člověka, nejsou na něm schopny dlouhodobě přežívat.
Skupina zahrnuje tři druhy popsané z Evropy a tři druhy popsané z Asie.
4. Druh Cimex hemipterus je vázaný především na tropické oblasti a parazitující na
lidech, netopýrech a drůbeži.
Zde je však potřeba zmínit jisté nejasnosti v taxonomii štěnic parazitujících na
netopýrech (Wendt 1941, Povolný 1957, Usinger 1966, Péricart 1972, Péricart 1996).
V podmínkách střední Evropy se lze setkat jak s druhy skupiny Cimex lectularius, tak zde lze
najít zástupce všech druhů skupiny C. pipistrelli (Tab. 1). Příležitostně jsou nalézáni zřejmě i
zavlečení jedinci druhu Cimex hemipterus. O taxonomických nejasnostech v obou skupinách
v posledních letech vznikla řada studií, které za použití standardních morfometrických
přístupů i genetických znaků přehodnocují doposud publikované taxony. S ohledem na
středoevropskou problematiku vynikají zejména práce O. Balvína (Balvín 2005, 2008, 2010 a
2013).
Z Evropy (v rámci Palearktu) byly popsány tři druhy štěnic žijících na netopýrech (C.
pipistrelli, C. dissimilis, C. stadleri) (Tab. 1). Obvykle jsou shrnovány do skupiny C.
pipistrelli. Pro klasifikaci evropských štěnic vyskytujících se na netopýrech různí autoři
využívali omezený počet morfologických znaků či nedostatečný počet vyšetřených jedinců
bez ohledu na časoprostorovou distribuci štěnic (např. Povolný 1957, Lansbury 1961, Péricart
1972). Snaha o klasifikaci na základě morfologických znaků však nevedla k přílišnému
vyjasnění taxonomické problematiky. Navíc Usinger (1966) pomocí hybridizačních
experimentů popsal určitou reprodukční bariéru mezi štěnicemi Cimex pipistrelli s. str.
z Britských ostrovů a populace C. stadleri z tehdejšího Československa. Je však zjevné, že
právě tyto morfologické rozdíly, způsobené snad adaptacemi na úkrytové chování
jednotlivých hostitelských druhů netopýrů, vedly k popisu více druhů.
13
14
ba
Obr. 2. Portréty modelových druhů štěnic a) štěnice Cimex lectularius, adultní samice, b)
štěnice C. pipistrelli, adultní samec (foto V. Káňa).
C. pipistrelli
C. lectularius
Obr. 3. Srovnání tvaru štítu u druhu C. lectularius se zaoblenými výběžky a krátkými chlupy
a C. pipistrelli s výběžky ostrými a dlouhým ochlupením (foto N.T. Gallagher).
Teprve v současnosti Balvín et al. (2013) doložili, že rozdíly v mitochondriální DNA
neukázaly souvislost s morfologickými znaky ukazujícími značnou fenotypovou variabilitu
štěnic mezi jednotlivými hostitelskými druhy netopýrů (Balvín et al. 2013). V následujícím
textu se proto přidržím taxonomického označení druhů skupiny Cimex pipistrelli popsaných
z Evropy jako Cimex pipistrelli s. lat., které vidím jako historicky oprávněné, ačkoliv recentní
studie Balvín et al. (2013) již dokonce ukazuje i na neplatnost zbývajících dvou druhů (C.
dissimilis a C. stadleri).
Tab. 1.: Seznam druhů skupin Cimex lectularius a C. pipistrelli jak jej charakterizují
vybrané studie (převzato z Růžičková 2012).
V minulosti popsaná diverzita souvisí spíše s adaptacemi na konkrétního hostitele, než
se vznikem nových druhů. Patrně až na jedinou výjimku, která souvisí s významnou změnou
hostitele, z tradičního hostitele (netopýra) na velmi vzdáleného hostitele (člověka) a to u
druhu C. lectularius. Balvín et al. (2012a) popsali značnou divergenci v mitochondriální i
jaderné DNA a morfologii mezi C. lectularius parazitující na člověku a netopýrech a ukazují,
že se obě linie štěnic oddělily již před desítkami tisíc let v době posledního interglaciálu
v souvislosti s disperzí moderního člověka z Afriky (Armitage et al. 2011). Další studie
(Booth et al., in press), kdy autoři využili jaderné markery, mikrosatelity, nezjistila žádný
genetický tok mezi liniemi štěnic parazitujících na člověku a na netopýrech. Mohlo by se tak
jednat o případ sympatrické (alloxenické) speciace, pravděpodobně v důsledku dlouhodobého
využívání různých hostitelů. Obě linie jsou od sebe též rozpoznatelné morfologicky.
Balvín et al. (2012a) dokládají, že úkryty synantropních netopýrů jako M. myotis a M.
emarginatus poskytují v současnosti jediný typ úkrytu původním divokým populacím štěnice
C. lectularius na většině území Evropy. Synantropizace těchto druhů netopýrů, stará několik
století, umožnila štěnicím snadné šíření mezi lidskými příbytky. Lze předpokládat, že by se
obě hostitelské linie mohly opakovaně potkávat a opětovně se pářit. Na druhou stranu
opakovaná a stále se prodlužující oddělenost obou linií, prohlubovaná rostoucí
15
“civilizovaností” člověka (odstartovaná např. již používáním ohně v jeskyních, Maestre
2013), mohla vést k tvorbě pre- i post-kopulačních reprodukčních bariér již daleko dříve.
Zcela odlišné životní strategie obou hostitelů vedly k postupné adaptaci linií na
jednoho nebo druhého hostitele. Balvín et al. (2012a) uvádějí, že štěnice pocházející z
netopýrů jsou větší, vyznačují se větším počtem sét a mají relativně kratší tělní výběžky jako
tykadla, rostrum a končetiny. O tom, že obě linie vykazují značný stupeň potravní speciace,
pojednává studie založená na experimentech, kdy byly štěnice C. lectularius, sebrané
v úkrytech netopýrů, krmeny lidskou krví a naopak štěnice z lidí byly krmeny netopýří krví
(Wawrocka & Bartonička 2013).
Pro úplnost charakteristiky skupiny C. lectularius zbývá dodat, že Simov et al. (2006)
publikovali popis nového druhu štěnice Cimex emarginatus Simov, 2006. Populace této
štěnice byla objevena v Bulharsku již v roce 1998 v kolonii netopýra brvitého, Myotis
emarginatus (Geoffroy, 1806), od něhož je odvozen i druhový název štěnice. Její postavení
v systému zůstává pro nejednoznačnost morfologických a molekulárních dat prozatím
nevyjasněno, zdá se ale, že by mohlo jít o druh příbuzný C. lectularius s. stricto (O. Balvín,
ústní sdělení).
Mezi zástupci čeledi Cimicidae bylo v minulosti provedeno několik hybridizačních
experimentů testujících přítomnost reprodukčních bariér (např. Ueshima 1964, Usinger 1966).
V řadě případů byla u hybridů potvrzena snížená fitness. Hybridi byli získáni mezi blízkými i
vzdálenými druhy (Usinger 1966), což dokládá malý význam pre-kopulačních bariér.
V současnosti dokončujeme studii založenou na hybridizaci mezi hostitelskými liniemi
štěnice C. lectularius. Přestože sporadicky dochází mezi smíšenými rodičovskými páry ke
kopulacím a detekci spermatu v abdomenu samic, pářené samice nekladou vajíčka. To by
ukazovalo na přítomnost post-kopulační bariéry (Wawrocka et al., in prep.). V tomto případě,
kdy předpokládáme oddělení obou linií skrze prostorovou izolaci zapříčiněnou různým
hostitelem, je absence pre-kopulačních bariér pochopitelná (Balvín & Bartonička, in press).
3.5 Životní cyklus štěnic a přežívání v úkrytech netopýrů
Následující informace odpovídají specifikům skupiny druhů C. pipistrelli a C.
lectularius. Zástupci čeledi Cimicidae jsou oviparní. Všech pět nymfálních instarů i adultní
jedinci žijí v úkrytech netopýrů nebo člověka, nikoliv přímo na těle hostitele (Usinger 1966).
Samice jsou schopny klást vajíčka dokonce bez nasátí krve hostitele. Růst a vývoj štěnic je
velice rychlý, při teplotě mezi 18 a 25°C se larvy za 30 dní pětkrát svléknou (Obr. 4).
Poslední instary nepotřebují k dalšímu vývoji žádné speciální podněty a jsou-li přítomni
16
v úkrytu i samci, mohou dospělé samice produkovat první vajíčka již do 5 dní po pohlavním
dospění. V experimentálních chovech však k prvním snůškám dochází 14 – 20 dní po
metamorfóze na imago (T. Bartonička, vlastní pozorování). Rychlý vývoj umožňuje štěnicím
v úkrytu dosáhnout vysokých abundancí záhy po jeho osídlení netopýry. Samice je schopna
denní produkce 2 - 4 vajíčka. Celoživotní snůška pak přesahuje i 500 vajec (Davis 1964),
obvykle je to však méně. Štěnice sají v intervalu několika dní a jsou schopny několik měsíců
hladovět (až 1,5 roku), což jim umožňuje přečkat zimní období nebo nepřítomnost hostitele
v úkrytu (Johnson 1942, Povolný 1957, Overal & Wingate 1976, Marshall 1982). Při vhodné
teplotě a optimální dostupnosti hostitele se však štěnice dožívají kolem jednoho roku. Usinger
(1966) sledoval, že teplota a vlhkost úkrytu významně ovlivňuje přežívání všech vývojových
stádií a také ochotu ke kopulaci. Štěnice však preferují celkově nižší teplotu úkrytu než
většina ektoparazitů, neboť se na hostiteli zdržují pouze krátkodobě po dobu krmení (Usinger
1966). Mimo dobu krmení je lze najít v početných skupinách ve škvírach trámů nebo
v záhybech polstrování nábytku (Obr. 5). Vyšší teplota naopak může snižovat jejich fitness
(Reinhardt 2007). V současnosti existují pouze ojedinělé informace o tom, zda změny
mikroklimatických podmínek a délka hladovění působí odlišně na přežívání jednotlivých
vývojových stádií, popřípadě pohlaví (srv. Funakoshi 1977, Overal 1980). Dosavadní
informace o délkách hladovění (až 250 dní) dokládají značnou odolnost imág (Dubinin 1947,
Southwood 1954). Zdali jsou však schopny podobného hladovění i další instary, není známo.
Doba hladovění s následnou schopností sát krev po znovuobjevení se hostitele v úkrytu je
však zásadní pro predikci density štěnic při opětovném osídlení úkrytu hostitelem a je
klíčovým momentem pro pochopení souvislosti stupně parazitace úkrytu a následného střídání
úkrytů netopýry.
Bartonička & Gaisler (2007) zjistili, že absence hostitele v úkrytech, spolu s vysokými
teplotami, vede ke snížení počtu dospělých štěnic a jejich vývojových stádií na méně než
polovinu původního počtu. Na přežívání štěnic má bezesporu velký vliv teplota a vlhkost
(Usinger 1966). Nicméně až do současnosti jen málo výzkumů řešilo ekologické vztahy mezi
teplotou a přežitím jednotlivých instarů po různě dlouhém hladovění (Funakoshi 1977, Overal
1980). Předchozí studie ukázaly u štěnic na vysokou toleranci k dehydrataci (až 40 % ztráty
vody v těle) a odolnost vůči vysokým teplotám (35-40°C) (Dubinin 1947, Southwood 1954).
Rivnay (1932) testoval vliv vlhkosti v rozmezí 10-70% na ontogenezi C. lectularius.
Nezjistil však žádné signifikantní rozdíly v růstu ani svlékání nymf, vliv vlhkosti byl
zanedbatelný. Lze však očekávat, že zejména v korelaci s vysokou teplotou v přirozených
úkrytech budou mít první instary s vyšším obsahem vody v těle horší přežívání (Jones 1930,
17
Johnson 1960, Usinger 1966). Reinhardt et al. (2008a) porovnávali teploty v úkrytu kaloně
egyptského (Rousettus aegyptiacus) a v refugiu štěnice Afrocimex constrictus. Zjistili, že
štěnice se raději za kaloni každou noc přesouvají několik metrů, než by riskovali trávit celou
dobu v úkrytu s vyšší teplotou, která se negativně projevuje na úspěšnosti jejich reprodukce.
Z jejich výzkumu vyplývá, že i poměrně malý teplotní rozdíl může ovlivnit fekunditu
ektoparazita.
Obr. 4. Životní cyklus štěnice domácí (Cimex lectularius) (převzato z Usinger 1966).
Obr. 5. Úkryty štěnice C. lectularius v bytech najdeme často v záhybech polstrování nábytku
(foto T. Bartonička).
Přežívání štěnic (Cimex spp.) je daleko více ovlivňováno okolní teplotou než je tomu u
permanentních ektoparazitů. Délka ontogeneze štěnic je limitována mikroklimatickými
podmínkami v úkrytu hostitele a dobou, kdy je hostitel přítomen. Doba pobytu hostitele je
18
v úkrytu omezena zejména u štěnic parazitujících netopýry. Toto omezení by mohlo ovlivnit
abundanci štěnic v úkrytu a způsobit asynchronizaci mezi reprodukcí ektoparazita a hostitele.
Bartonička (2010) zjistil rozdílnou pravděpodobnost přežívání u jednotlivých
ontogenetických stádií v rozmezí teplot 5-35°C. Nejvyšší přežívání bylo zjištěno u samičích
imag a nymf 4. a 5. instaru. C. pipistrelli byla též tolerantnější k vyšším teplotám ve srovnání
s C. lectularius. Štěnice C. pipistrelli z netopýrů měly kratší ontogenetický cyklus než štěnice
C. lectularius parazitující na člověku. Schopnost lépe přežívat při vysokých teplotách (35°C)
u druhu C. pipistrelli je pravděpodobně důsledkem jejího dlouhodobého soužití s netopýry,
jejichž úkryty se v letních měsících snadno přehřívají. S druhem C. lectularius se lze
v netopýřích úkrytech setkat též a dokonce je u některých druhů častějším parazitem než C.
pipistrelli. Nedávné studie však ukazují, že štěnice druhu C. lectularius tvoří dvě oddělené
linie parazitující na lidech a netopýrech (Balvín et al. 2012a, Wawrocka & Bartonička 2013).
Zdali je tolerance k vyšším teplotám i u štěnic C. lectularius z lidí než těch z netopýrů, není
prozatím známo, lze to však předpokládat.
3.6 Štěnice, její šíření a jako vektor patogenů
V posledním desetiletí došlo k prudkému nárůstu počtu nového výskytu štěnic druhu
C. lectularius parazitujících na člověku (Reinhardt & Siva-Jothy 2007). Stejní autoři uvádějí,
že prudký nárůst incidence v posledních letech je charakteristický pro tzv. západní svět Ameriku
a Evropu. Příčina nárůstu je patrně velmi komplexní, ať již souvisí s novými
způsoby bydlení, zálibou ve starožitném a použitém nábytku, v němž mohou být štěnice
ukryty, účinnější klimatizací, novými způsoby oblékání, častější přítomnost domácích zvířat v
bytech, rozvojem letecké dopravy (Dogget et al. 2004) nebo prostě pouze se skutečností, že
dnešní lidé štěnice nepoznávají (Seidel & Reinhardt 2013). Např. v Angliii předkládanou
štěnici správně určilo pouze 10% dotázaných z 358 osob (Reinhardt et al. 2008b).
Za další možnou příčinou návratu štěnice domácí v posledních letech byly považovány
restrikce počtu insekticidů a používání insekticidů se specifickou účinností jen na určitý druh
hmyzu, jiný než štěnice. U štěnice domácí odchycené v lidských obydlích několika států USA
a ve Velké Britanii byla zjištěna extrémně vysoká rezistence k pyrethroidům, deltamethrinu,
cyhalothrinu, cypermethrinu a ke karbamátům, které se na celém světě k jejich hubení
používají nejčastěji. Publikované výsledky naznačují, že jde o fenomén rozšířený i v jiných
státech (Romero et al. 2007). Tato rezistence je ovládána několika neúplně dominantními
geny, takže současně se štěnicemi se šíří i jejich vysoká rezistence (Ledvinka et al. 2008).
19
Studie Balvín et al. (2012a) a Booth et al. (in press) ukázali, že nárůst štěnic C.
lectularius parazitujících na lidech v posledních letech, nesouvisí s přenosem štěnic
z netopýrů a obě linie jsou dobře odděleny. Štěnice na člověka přešly patrně z netopýrů, když
když společně obývali jeskyně (Sailer 1952, Usinger 1966, Usinger & Povolný 1966). Odtud
se štěnice s novými hostiteli přesunuly do lidských obydlí, která jim klimaticky vyhovovala
ještě lépe. V tomto kontextu je velmi zajímavá kombinace ztráty ochlupení u člověka a jeho
následná parazitace úkrytovými parazity jako roztoči nebo štěnicemi v souvislosti
s používáním oblečení a dlouhodobých úkrytů (Rantala 1999). K výstavbě trvalejších
příbytků docházelo v souvislosti s rozvojem zemědělství někdy mezi 5 - 8 tisíci lety př. n. l.
Štěnice se objevily jako ektoparazité člověka již v prvních psaných dokumentech. V průběhu
20. století napomohly jejich šíření obě světové války. Štěnice expandovaly díky přesunu
velkého množství lidské populace a rovněž díky pasivnímu přenosu různými dopravními
prostředky (Whitfield 1939). S masivním zavedením postřiků infestovaných bytů přípravky
DDT během 2. světové války a především po ní došlo k téměř úplné likvidaci štěnic, do té
doby zcela běžných v lidských obydlích. Navíc po 2. světové válce docházelo k nahrazování
dřevěných rámů postelí kovovými, což značně omezilo možnosti úkrytu štěnic a současně
usnadnilo jejich kontrolu (Potter 2008) a tedy včasné rozpoznání jejich přítomnosti a jejich
následnou likvidaci.
Hostitelé jsou obvykle štěnicemi pokousáni v noci během spánku. Štěnice probodávají
kůži a do ranky vpouštějí antikoagulanty a další látky jako hydraluronidázy, proteázy a
kinázy. Krev sají přímo z vlásečnic, ale mohou sát i krev z poškozených tkání. Protože sliny
štěnic obsahují anestetikum, je kousnutí prakticky bezbolestné a místo vpichu není cítit
mnoho hodin. V důsledku velmi pozdní reakce si lidé obvykle štěnice jako původce
nepřipouštějí, což významně usnadňuje jejich šíření (Reinhardt & Siva-Jothy 2007). Do rány
však při vpichu pronikají i další antikoagulační, vasodilatační (např. oxid dusnatý) a
proteolytické látky (např. apyráza), které obvykle způsobují prudkou alergickou reakci (Davis
et al. 2009).
Kolem vpichu se tvoří typické kožní léze - svědivé erytematózní maculopapuly, které
mají 5 mm až 2 cm v průměru, s centrálním hemorhagickým váčkem. Vícečetná kousnutí
štěnic často sledují přímky nebo křivky (Obr. 6). Počty vzniklých lezí se pohybují od několika
do mnoha desítek za noc, v závislosti na abundanci štěnic v úkrytu. Štěnice na tělech netopýrů
přednostně sají na neosrstěných blánách, u člověka na neoblečených zónách těla (Obr. 6). U
člověka někdy erupce napodobují kopřivku. Léze obvykle zmizí po 2-6 týdnech, ale lokální
hyperpygmentace může přetrvávat i déle (Kolb et al. 2009, Reinhardt et al. 2009). Klinický
20
obraz je závislý na imunokompetenci a předchozí expozici napadeného člověka. Komplikace,
vyplývající z případné sekundární bakteriální infekce jsou výsledkem rozškrabání a exkoriace.
Kolb et al. (2009) uvádí úplnou necitlivost k bodání štěnic bez následných reakcí i při
opakovaném napadení asi u 20% lidí. Ti pak mohou být spolehlivými hostiteli a úspěšnými
šiřiteli štěnic. V této souvislosti je jedinou spolehlivou diagnózou nález živých štěnic. Kromě
dlouhodobého svědění trpí napadení lidé často nespavostí a psychickým stresem.
a b
Obr. 6. Ukázka umístění vpichů a sání štěnicí domácí C. lectularius. a) u člověka na
nekrytých částech těla s jemnou kůží, obvykle v řadách za sebou (převzato z Delaunay et al.
2011) a b) štěnice sající na létacích blánách mláděte M. myotis (foto R. Lučan).
Štěnice, jakožto v minulosti běžný ektoparazit člověka, je tedy logicky i v centru
parazitologického výzkumu jako možný vektor významných onemocnění. Delaunay et al.
(2011) uvádí na 40 patogenů (bakterií, plísní a virů), které byly nalezeny v trávicím traktu,
výkalech, na povrchu těla či ve slinách štěnic z volné přírody nebo z laboratorních chovů.
Zajímavý je však rozpor ve zjištěných vysokých hustotách patogenů v těle štěnic po
jejich umělé infekci v laboratoři a současně velmi nízkých počtech přenášených patogenů při
sáních. Předpokládá se, že za tímto rozporem stojí zvláštní reprodukční biologie skupiny.
Štěnice jsou totiž jedinou skupinou krevsajících členovců, kteří mají traumatickou inseminaci.
Opakovaný vstup patogenů do těla štěnic sice souvisí s kratší délkou života samičího imága
(Reinhardt et al. 2005), ale současně může být selekčním faktorem pro optimalizaci imunitní
odpovědi opakovanou stimulací systému. Přestože většina starších studií (např. Burton 1963)
nedokládá, že by štěnice byly významným vektorem infekčních onemocnění, je nutno uvážit i
skutečnost, že se tyto studie zaměřovaly na patogeny obecně málo přenášené krevsajícími
členovci (např. HIV; methicilin-rezistentní Staphylococcus aureus – MRSA; hepatitis B, C, E;
Goddard & deShazo 2009, Doggett et al. 2012). Současně však bylo identifikováno pouze
21
minimum patogenů v reakci na propuknutí konkrétního lidského onemocnění. Studie na
arbovirech (Adelman et al. 2013) uvádí zjištění většiny druhů až teprve intenzivním
průzkumem (mezi)hostitelů. Je tedy zřejmé, že těžištěm dalších výzkumů musí být
identifikace a charakterizace enzootických přenosových cyklů.
3.7 Vliv štěnic na chování netopýrů
Vysoký počet ektoparazitů nalezených na samicích a mláďatech v období po porodech
může signalizovat synchronizaci populačního cyklu ektoparazit – hostitel, a tím snížení
komfortu ve stávajícím úkrytu. Lewis (1996) zjistila pozitivní korelaci počtu ektoparazitů
s nízkou váhou kojících samic. Na druhé straně je nutno efekt parazita chápat jako proměnnou
silně závislou na jeho populační hustotě v úkrytu a je zřejmé, že s počtem roste i
intraspecifická kompetice (Jaenike 1996). Obecně se proto předpokládá, že parazitace není
důvodem přímého úhynu hostitele, ale spíše jeho oslabení (srv. Zahn & Rupp 2004) a zvýšené
potřeby změny úkrytu vedoucí k vyššímu komfortu. Na druhou stranu tlak ze strany parazita
nebude zanedbatelný, jelikož řada experimentálních i terénních výzkumů ukázala, že
ektoparaziti mohou snížit hnízdní úspěšnost svých hostitelů (Loye & Carroll 1991, deLope &
Møller 1993, Richner et al. 1993, Christe et al. 1996).
Synchronizace reprodukčního cyklu roztočů, nejběžnějších ektoparazitů netopýrů,
byla opakovaně publikována s ohledem na různé hostitelské druhy (např. Christe et al. 2000,
Lučan 2006). Podobná synchronizace byla zjištěna mezi netopýrem velkouchým (M.
bechsteinii) a muchulí Basilia nana (Reckardt & Kerth 2006). Metamorfovaní dospělci této
muchule přetrvávají v pupáriu týdny v úkrytech netopýrů a čekají na návrat hostitele. Po
obsazení úkrytu netopýry dochází k jejich rychlému uvolnění z obalu a takřka okamžitému
přichycení na těle nového hostitele. Samice netopýrů však rozpoznávají vícekrát obsazené
úkryty s vysokou pravděpodobností výskytu kukel a vyhýbají se jim (Reckardt & Kerth
2007). Imága jsou už pak permanentními ektoparazity netopýrů a tělo hostitele s výjimkou
kladení vajíček vůbec neopouštějí. Podobná synchronizace vývojových cyklů byla zjištěna i u
blech hlodavců nebo netopýrů. Po opuštění kukly se imago blechy stejně jako muchule
zdržuje ještě nějakou dobu v pupáriu a čeká na mechanický stimul ukazující na blízkost
nového hostitele. Na vibrace reaguje opět velmi rychle, opouští kokon během jedné minuty a
dokáže se přichytit na hostiteli až ve vzdálenosti 20 m (Rosický 1957). Schopnost vyhnout se
infestovaným hnízdům byla zjištěna i u některých často ve skupinách či koloniálně hnízdících
druhů ptáků (Opplinger et al. 1994, Rendell & Verbeek 1996).
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V práci Bartonička & Gaisler (2007) jsme se věnovali sledování cyklu štěnic
v umělých úkrytech netopýrů, v netopýřích budkách, v průběhu vegetační sezóny.
Modelovými druhy byl Pipistrellus pygmaeus a štěnice Cimex pipistrelli. Po příletu
gravidních samic netopýrů v květnu byly v budkách pozorovány především imága štěnic a
pouze několik jedinců 1. - 3. instaru. Na začátku června netopýři některé budky opouštěli
těsně před porody a období laktace většina samic trávila v kolonii v nedaleké budově
(Bartonička et al. 2008).
Obr. 7. Změny v počtu imág, 1. - 3. a 4. - 5. instarů štěnic s ohledem na reprodukční fáze
hostitele. Body v box-plotech označují průměry a boxy směrodatnou odchylku.
Během období absence hostitele v netopýřích budkách došlo k významnému snížení
počtu všech vývojových stádií, na více jak 50% původního počtu (Obr. 7). Páté instary
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metamorfovaly v imága během července předchozího roku, a jelikož se obvykle dožívají
pouze jednoho roku (Usinger 1966), jejich úbytek koresponduje s přirozeným vymíráním. Za
početní redukcí nymf, zejména 1. - 3. instarů, však stojí zjevně nepřítomnost hostitele. Rané
instary metamorfují do dalších stádií během 4-7 dnů a v každém stádiu potřebují na hostiteli
sát (Usinger 1966).
Ukázalo se, že krátkodobá nepřítomnost netopýrů v budkách významně omezí
abundanci štěnic, ať již důvodem pro opuštění dočasných úkrytů jsou klimatické výhody
prostornějšího úkrytu v budově v průběhu laktace nebo přímo antiparazitární chování. Období
absence hostitele přežívají pouze vajíčka a několik jedinců starších vývojových stádií.
Opětovné zvýšení počtu štěnic bylo zjištěno až po příletu samic netopýrů a čerstvě
odstavených mláďat. Na počátku srpna už v budkách nebyla nalezena žádná nová vajíčka. Je
tedy zřejmé, že nepřítomnost štěrbinových netopýrů v laktaci v úkrytech intenzivně
využívaných během gravidity a v postlaktačním období zabrání masivnímu namnožení štěnic
známému z kolonií netopýrů využívajících prostorné půdy budov (Bartonička & Růžičková
2012).
Je pochopitelné, že antiparazitární chování založené na střídání úkrytů má význam
pouze u hostitelských druhů, které mohou úkryt snadno změnit (např. jsou schopni snadno
přenést různě stará mláďata). Toto chování efektivně napomáhá přerušit nejen životní cyklus
úkrytových parazitů, jako jsou štěnice, ale i permanentních parazitů, je-li přesun do nového
úkrytu realizovan před dokončením jejich vývoje (např. Hausfater & Meade 1982; Lewis
1995, 1996; Roper et al. 2001; Kunz & Lumsden 2003; Peinke & Brown 2005). Frekvence
střídání úkrytů signifikantně korelovala s abundancí parazita i u jiných savců, např. Meles
meles (Butler & Roper 1996) nebo Parotomys brantsii (Roper et al. 2002). U netopýrů byla
stejná korelace zjištěna např. i u druhu Antrozous pallidus (Lewis 1996).
Potřebu změny úkrytu v souladu s rostoucím počtem ektoparazita v úkrytech by měly
doprovázet další typy chování. Takovým výrazným chováním ve vztahu k parazitaci je
bezesporu grooming. Velmi málo je však známo o úrovni groomingu vyvolaným úkrytovým
parazitem. Bartonička (2007, 2008) se proto věnuje významu auto a allogroomingu u
netopýrů v uměle infestovaných úkrytech v experimentálních podmínkách. Ve voliéře byly
instalovány dvě netopýří budky, jedna s různým počtem štěnic a druhá bez štěnic sloužící
jako náhradní úkryt. Byly zjištěny významné rozdíly v úrovni autogroomingu, ve frekvenci
přesunů jednotlivých netopýrů v budce a netopýrů, kteří budku opustili. Allogrooming byl
pozorován pouze v několika málo případech (Obr. 8). Štěnice po nějakou dobu (přibližně 20
minut) po zahájení experimentu nejsou schopny na netopýrech sát, a to z důvodu nízké
24
tělesné teploty hostitele. Sání je možné až tehdy, když teplota alespoň jednoho hostitele ve
skupině dosáhne hodnoty, která je pro ektoparazita atraktivní. Experiment též ukázal, že
štěnice napadají prvního netopýra, který se probouzí z denního torporu, a ten ve snaze zbavit
se ektoparazita budí ostatní hostitele v úkrytu. Netopýři, vyrušení sáním většího počtu štěnic,
kdy autogrooming a přesun v úkrytu nevede k setřesení ektoparazita, infestovaný úkryt
opouštěli. Z takových úkrytů odlétali významně častěji, než z budek kam štěnice nebyly
přidány.
Obr. 8. Úroveň auto- a allogroomingu, počet přesunů jednotlivých netopýrů v budce a počet
netopýrů, který budku opustil ve srovnání s kontrolou, kdy do budek nebyly aplikovány
štěnice. (**) ukazuje signifikantní rozdíl (p < 0,001) mezi experimenty s odlišným počtem
ektoparazitů a (*) rozdíl ve sledovaných proměnných mezi experimenty s aplikací
ektoparazita a bez něj. Body v box-plotech značí průměry, boxy směrodatné odchylky a
„whiskers“ min-max hodnoty.
25
26
Nebyla zjištěna spolupráce dospělých samic při groomingu ani snaha zbavit vlastní
mláďata štěnic, a to dokonce navzdory jejich vyšší parazitaci. Na mláďatech je však vysoký
počet ektoparazitů nalézán opakovaně (např. Criste et al. 2000). Na druhé straně neexistuje
přímá korelace mezi počtem ektoparazitů v úkrytu v průběhu laktace a pravděpodobnosti
přežití prvního roku. Proto bude v budoucnu vhodné porovnat délku odstavu mláďat, která se
obvykle používá jako hlavní ukazatel fitness (u ptáků např. Brown & Brown 1998), mezi
infestovanými a neinfestovanými úkryty.
3.8 Hostitelská specifita štěnic
V případě čeledi Cimicidae nelze mluvit o výraznější hostitelské specifitě čeledi a
často ani jednotlivých druhů. Spektrum štěnicemi parazitovaných druhů je obecně dosti
široké. Tradičně však chybí dostatek údajů pro stanovení kompletního výčtu hostitelů
konkrétního druhu. Přestože monoxenní druhy štěnic existují (např. Primicimex cavernis
Barber, 1941 parazitující zřejmě pouze na netopýrovi Tadarida mexicana), daleko častěji se
setkáme s druhy využívajícími více než jednoho hostitele.
Častěji však jeden druh štěnice preferuje jednoho hostitele jako hlavního a pouze
příležitostně tvoří populace (démy) na jiných hostitelských druzích. Takovým příkladem je
třeba štěnice Cacodmus vicinus Horváth, 1934, parazitující především na netopýrovi jižním
Pipistrellus kuhlii (Quetglas et al. 2012). Naopak modelové druhy skupiny druhů Cimex
lectularius a C. pipistrelli parazitují řadu druhů netopýrů zejména z čeledi Vespertilionidae,
dále pak člověka, hlodavce, lasicovité šelmy a několik druhů ptáků (Wawrocka & Bartonička
2013). V čeledi Cimicidae je však obtížné najít úplné hostitelské generalisty. Jako druhy
parazitující na více čeledích či dokonce řádech lze uvést Haematosiphon indorus Dugès, 1892
(ptáci, Usinger 1966) nebo Stricticimex antennatus Ferris and Usinger, 1957 (netopýři, Overal
& Wingate 1976).
Jelikož v dílčích studiích habilitační práce není detailně prezentováno hostitelské
spektrum studovaných štěnic C. lectularius a C. pipistrelli s.l., ale studie Bartonička &
Růžičková (2012) a Wawrocka & Bartonička (2013) se spektrem hostitelů dále pracují, proto
předkládám seznam hostitelských druhů netopýrů zde.
Tab. 2. Seznam hostitelských druhů netopýrů Cimex lectularius a skupiny C. pipistrelli.
Vychází z literární rešerše a zahrnuje i údaje v tisku.
Druh netopýra Literární zdroj
Cimex lectularius
Pipistrellus kuhlii Abul – Hab 1979 podle Lanza 1999
Pipistrellus pipistrellus Rybin et al. 1989
Vespertilio murinus Dubinij 1947 in Povolný 1957
Nyctalus leisleri Walter 1996
Nyctalus noctula Heise 1988
Eptesicus serotinus Baagoe 2011
Myotis myotis např. Povolný 1957, Usinger 1966
Myotis oxygnathus (blythii) Usinger 1966 (Tagiľcev 1971 jako Cimex sp.)
Myotis mystacinus Poppius 1912 in Usinger 1966
Myotis daubentonii Wagner 1967, Bogdanowicz 1994
Myotis emarginatus Protić & Paunović 2006, Balvín et al. 2012
Plecotus auritus Balvín et al. 2012b
Cimex pipistrelli s.l.
Pipistrellus kuhlii Abul-Hab & Shihab 1990 podle Lanza 1999
Pipistrellus pipistrellus Jenyns 1839
Pipistrellus pygmaeus Bartonička 2007, Bartonička & Gaisler 2007
Pipistrellus nathusii Heise 1988, Dietz & Walter 1995, Walter 1996
Vespertilio murinus Horváth 1935
Nyctalus noctula Povolný 1957, Southwood & Leston 1959, Dietz & Walter 1995
Nyctalus leisleri Nelson & Smiddy 1997, Morkel 1999, Krištofík & Kaňuch 2006
Nyctalus lasiopterus Balvín et al. 2012b
Eptesicus serotinus Southwood & Leston 1959, Heise 1988
Myotis myotis Lederer 1950, Usinger 1966
Myotis oxygnathus (blythii) Tagiľcev 1971 jako Cimex sp.
Myotis bechsteinii Morkel 1999
Myotis brandtii Heise 1988, Dietz & Walter 1995, Walter 1996
Myotis daubentonii Heise 1988, Dietz & Walter 1995, Walter 1996
Myotis dasycneme van Rooij et al. 1982, Walter 2004
Myotis mystacinus Kerzhner 1989
Myotis nattereri Balvín et al. in press.
Myotis emarginatus Usinger 1966
Rhinolophus ferrumequinum Usinger 1966
Rhinolophus euryale Balvín et al. in press.
27
V případě obou druhů vrápenců byly štěnice nalezeny ve smíšených reprodukčních
koloniích se samicemi druhů Myotis myotis a/nebo M. emarginatus. Samice vrápenců si
v koloniích udržují vzájemnou vzdálenost několik centimetrů (Dietz et al. 2007). Jedinou
výjimkou jsou dny s nízkou teplotou v době, kdy mláďata ještě nemají vyvinutu schopnost
termoregulace. Pak je možno vidět samice nahloučené ve skupině podobně jako u druhů
čeledi Vespertilionidae (T. Bartonička, osobní pozorování). Rozvolněné kolonie zřejmě
neposkytují dobré životní podmínky k rozvoji populací štěnic. Je tedy vysoce pravděpodobné,
že štěnice byly nalezeny ve smíšených koloniích právě díky přítomnosti druhů Myotis, u
kterých se naopak samice opakovaně shlukují. Navíc první nálezy štěnic na těchto druzích
však nepocházejí přímo z kolonie, ale z letících jedinců odchycených do harfové pasti (Protić
& Paunović 2006).
Podobně nevyjasněná situace je s parazitací netopýrů rodu Plecotus. Teprve nedávno
byla nalezena štěnice na jedinci Plecotus auritus odchyceném mimo úkryt (Balvín et al.
2012b) (Tab. 2). Středoevropské druhy Plecotus auritus a Plecotus austriacus tvoří obvykle
kolonie o několika kusech a přestože u nich byly štěnice systematicky hledány, nebyly
v koloniích samic nalezeny (Heise 1988, Rupp et al. 2004). Pětina letních úkrytů netopýrů,
každoročně monitorovaných na území České republiky, je sdílena druhy rodu Plecotus i
druhy, které běžně štěnice hostí jako M. myotis a M. emarginatus (Bartonička & Gaisler
2010). Přesto však nebyla dosud zaznamenána opakovaná parazitace netopýrů Plecotus a
Rhinolophus spp. a lze je tedy považovat pouze za příležitostné a spíše nevhodné hostitele
štěnic. Nelze však vyloučit, že se zde potýkáme pouze s nedostatkem informací z terénu, na
což mohou ukazovat výsledky diplomové práce Zedníkové (2010). Autorka prováděla
experimenty hostitelské specifity štěnic skupiny C. pipistrelli a ukázala, že štěnice jsou
schopny sát i na netopýrech rodu Plecotus a vrápencích Rhinolophus hipposideros.
I přes poměrně malou hostitelskou specifitu štěnic je zřejmé, že řada druhů netopýrů
slouží štěnicím pouze jako občasní hostitelé, na kterých štěnice mohou přežívat snad i řadu
generací. Odlišné přežívání parazita mezi hlavním a vedlejším hostitelem je dokladováno
opakovaně z různých skupin parazitů. Jejich populace jsou schopny na vedlejších nebo
příležitostných hostitelích přežívat, přestože ti jsou částečně imunní nebo jinak omezují
natalitu parazita (Pulliam et al. 2007). Podobná situace pravděpodobně nastává u
hostitelských druhů, které tvoří málo početné reprodukční kolonie, obvykle pod 20 jedinců
(např. právě Plecotus spp., Rhinolophus spp.). Pokud se nízká početnost kolonie navíc
kombinuje s častou změnou úkrytu, je pro časné instary štěnic dostupnost potravy velmi
28
omezená. Efektivitu sání na hostiteli významně redukuje i disperze samic po půdních
prostorech. Snaha dosáhnout hostitele aktivním vyhledáváním na větší vzdálenosti často
selhává (Bartonička & Růžičková 2012). Z tohoto důvodu jsou štěnice nuceny vyčkat příletu
hostitele zpět, do míst, které tradičně využívá. To dokládají i četná podzimní pozorování, kdy
v říjnu a listopadu jsou v úkrytech pozorována převážně imaga a 4. a 5. instary ve větších
počtech pouze v místech tradičního výskytu kolonie, případně přímo pod ním. Na strategii
dlouhého vyčkávání jsou zjevně imága štěnic dobře vybavena a nespářené samice bez příjmu
potravy přežívají až 2 roky (Usinger 1966). Tato skutečnost má zásadní význam pro ochranu
kolonií netopýrů. Pokud je mi známo, doposud totiž nebyl pozorován případ, kdy by štěnice
(zejména C. lectularius) osidlující úkryt netopýrů na půdě jinak obydlené budovy, napadaly
lidi využívající další blízké prostory, a to ani v době dlouhodobé nepřítomnosti netopýrů (září
- březen).
Situace v případě druhu C. pipistrelli je poněkud komplikovanější v souvislosti
s vazbou na druhy netopýrů využívající štěrbinové úkryty. V posledních desetiletích jsou
známy početné reprodukční kolonie hostitelských druhů netopýrů jako N. noctula a P.
pipistrellus z panelových domů. Ty jsou však v současnosti plošně revitalizovány a původní
úkryty v mnoha případech zanikají bez náhrady. Tato situace vede ke stále častějšímu výskytu
netopýrů v nových často klimaticky suboptimálních úkrytech, které jsou navíc v těsné
blízkosti prostor využívaných člověkem. Stav je navíc komplikován opakovanou
nepřítomností hostitele v úkrytu v letním období a štěnice jsou nuceny vyhledávají
alternativního hostitele. Přestože Southwood & Leston (1959) zjistili omezenou schopnost
reprodukce C. pipistrelli krmené lidskou krví, tyto štěnice na člověku sají a dovedou založit
početnou populaci (T. Bartonička, J. Šafář, osobní pozorování). To pochopitelně vede ke
snaze blízký úkryt netopýrů znepřístupnit. Eradikace štěnic je však z podobných prostor
obvykle nemožná a komplikuje praktickou ochranu netopýrů, jako zvláště chráněných druhů.
Dalším aspektem hostitelské specifity je přítomnost dvou reprodukčních cyklů v roce
u štěnic vázaných na netopýry (zejména u druhu C. pipistrelli). Druh C. lectularius, populace
vázané na jiné hostitele, zejména člověka, se rozmnožuje v průběhu celého roku bez omezení.
Tato cyklicita se u linií parazitujících na netopýrech přenáší i do chovných skupin držených
ve standandardních mikroklimatických podmínkách s dostatkem potravy (T. Bartonička, L.
Růžičková, K. Wawrocka, osobní pozorování). Neochota samic snášet vajíčka v podzimním
období byla opakovaně pozorována u dospělých samic odchycených přímo v netopýřích
úkrytech. U instarů pak byla zjištěna neochota sát.
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3.5 Transport štěnic netopýry
Disperze štěnic mezi úkryty hostitelů je nezbytná pro zachování genetické diverzity
v jednotlivých úkrytech i diverzity celé populace. Logickou snahou štěnic je též disperze
do nových, doposud neparazitovaných úkrytů. Štěnice však nemají schopnost letu, proto
jejich přenos probíhá výhradně pasivním způsobem.
Na netopýrech odchycených mimo úkryty jsou štěnice zjišťovány velmi zřídka
(Bartonička & Růžičková 2013). Nálezy štěnic na tělech netopýrů mimo jejich úkryty se
týkají prakticky výhradně skupiny C. pipistrelli. Přestože byly publikovány pouze dva nálezy
C. lectularius na netopýrech, je pravděpodobné, že netopýři musí přenášet i tento druh (Heise
1988). Z údajů uvedených v publikaci Balvín et al. (2012a), je zřejmé že nálezy štěnic C.
lectularius na těle netopýrů na území Evropy souvisí téměř výhradně s rodem Nyctalus. Na
druhou stranu není doposud objasněno, zda a nakolik jsou dosavadní výsledky ovlivněny
nedostatkem informací. Je totiž jisté, že štěnice na svém těle přenášejí i jiní netopýři.
Bartonička & Růžičková (2013) dokumentovali rychlou kolonizaci stěnicemi u budek
obývaných netopýrem nejmenším (Pipistrellus pygmaeus). Tento druh je druhým v pořadí po
n. rezavém, na jehož těle jsou štěnice mimo úkryty nalézány opakovaně (Balvín et al. 2012b).
Přenos jinými druhy je však ojedinělý a v literatuře zmínky prakticky chybí. Další, avšak
velmi ojedinělé, literární záznamy přenosu štěnice jiným netopýrem než rodu Nyctalus
ukazují na transport štěnic netopýry druhu Vespertilio murinus (Orlova & Pervušina 2010) a
Myotis daubentonii (Heise 1988). Nově jsou štěnice mimo úkryt uváděny z druhů M.
dasycneme, M. myotis a Plecotus auritus (Balvín et al. 2012b). Posledním druhem, u něhož
byly štěnice mimo úkryt potvrzeny teprve nedávno, je také M. nattereri (A. Reiter, ústní
sdělení).
Přestože je obtížné vyčíslit frekvenci přenosů štěnic netopýry, je nepoměr nálezů mezi
druhy rodu Nyctalus a jinými druhy netopýrů jednoznačný. Heise (1988) uvádí nález 55 štěnic
ze vzorku 1631 jedinců netopýra rezavého a Rupp et al. (2004) dokonce na 15% jedinců
tohoto druhu (ze 221 zkoumaných jedinců). Obvykle je nalézána pouze jedna až dvě štěnice
na netopýrovi. Pravděpodobně nejvyšší publikovaný počet štěnic nalezený na jednom
netopýrovi je čtyři (Rupp et al. 2004). Bohužel ve většině prací není odlišeno, zda nálezy
štěnic byly uskutečněny mimo úkryt kolonie či u jeho vletového otvoru, kde je logicky
pravděpodobnost nálezu štěnice na odlétajícím netopýrovi vyšší než na lovišti.
Jak vyplývá z databáze soustředěné Českou společností pro ochranu netopýrů, netopýr
rezavý tvoří pouze 0,9% (170 ks) z celkového počtu 18388 odchycených netopýrů v letech
30
2006-2013 (databáze ČESON nepubl., Bartonička & Gaisler 2010). Nepatří tedy k pravidelně
odchytávaným druhům, spíše naopak.
Temperátní druhy netopýrů během dne upadají do torporu, kdy se teplota těla netopýra
srovnává s teplotou vzduchu (Stones & Wiebers 1965, Stawski et al. 2014). Výjimkou je
období laktace a krátké období péče o mláďata, kdy kojící samice sice upadají během dne do
torporu, ale pouze na krátkou chvíli (např. Klug & Barclay 2013). Je-li však tělesná teplota
netopýra nižší než 30°C (Rivnay 1930), což je teplota, nad níž je štěnice schopna hostitele
najít a sát na něm, hostitel štěnici nepřitahuje (Bartonička 2008) a štěnice tak mají minimální
šanci sát a být vyneseny ven z úkrytu. Tato úvaha se zdá být podpořena i zjištěním Balvína et
al. (2012b). Ti zjistili, že pouze osm z 41 netopýrů, kteří na sobě měli štěnice mimo úkryt,
byly kojící samice.
Jak ukázaly experimenty, netopýr nejmenší se pro štěnice stává atraktivním, když
odpoledne zvyšuje tělesnou teplotu. Teprve v tom okamžiku byly štěnice schopny netopýra
napadnout. K rychlému zvyšování teploty netopýrů však v experimentech docházelo až krátce
před jejich výletem z budky (Bartonička 2008). Velmi pravděpodobně lze očekávat podobné
chování i u netopýra rezavého. Není doposud známo, zda je probouzení z denní letargie u
těchto dvou druhů netopýrů nějak odlišné v porovnání s druhy, na kterých štěnice nejsou
mimo úkryt nalézány.
Dalším možným důvodem častých nálezů štěnic právě na druhu N. noctula, může
spočívat v jeho tělesné velikosti. Jelikož patří mezi největší evropské druhy netopýrů, je tedy
pravděpodobně pro štěnice více atraktivní. Může tedy záležet na velikosti plochy vhodné
k přichycení a následnému sání, např. při porovnání velkého druhu N. noctula a drobného
druhu P. pygmaeus. Velikost těla však pravděpodobně nebude rozhodující faktor, jelikož
např. druh M. myotis dosahuje podobné váhy jako N. noctula a štěnice na něm byly nalezeny
mimo úkryt pouze v jediném případě (Balvín et al. 2012b).
Významnou roli by mohla mít i tloušťka a pevnost létací membrány. Odolnost vůči
zátěži je mezi membránami křídel jednotlivých druhů netopýrů odlišná a u druhu N. noctula
byly zjištěny vysoké hodnoty momentu setrvačnosti (Thollesson & Norberg 1991). Ten
pozitivně koreluje se sílou létací blány. Jelikož hodnoty momentu setrvačnosti jsou u druhu N.
noctula dvojnásobné než u jiných druhů, lze předpokládat, že se druh vyznačuje obzvláště
pevnou křídelní blánou (Quay 1970, Schwartz et al. 2006). Právě při odchytech netopýrů do
sítě je dobře patrné, že je blána silnější než u velikostně srovnatelných druhů jako M. myotis
nebo M. dasycneme (T. Bartonička, osobní pozorování). Štěnice sají přednostně právě na
křídlech a uropatagiu. Proto lze předpokládat, že N. noctula může být méně citlivý na
31
přítomnost štěnic na svém těle a může vykazovat nižší míru groomingu ve snaze se štěnic
před výletem zbavit. To se v současnosti snažíme experimentálně otestovat.
Recentní studie zaměřená na genetickou strukturu populací štěnic C. pipistrelli navíc
ukazuje, že ač jsou pozorování transportu velmi vzácná, dochází k nim opakovaně a nový
dém je obvykle zakládán více samicemi (Wawrocka et al., in prep.). N. noctula, podobně jako
druhy rodu Pipistrellus, jsou jako vektor ideální, jsou tažné (např. Petit & Mayer 2000,
Huttere et al. 2005) a navíc opakovaně střídají úkryty i během reprodukční sezóny (Kaňuch &
Ceľuch 2004). Dokonce navštěvují více úkrytů během jediné noci (Feyerabend & Simon
2000). Naopak druhy rodu Myotis jsou ve volbě úkrytu reprodukční kolonie velmi tradiční a
vrací se na jediné místo řadu let. Na druhou stranu jaderné markery, mikrosatelity, neukazují
na žádnou strukturovanost populací podle hostitelského druhu (Wawrocka et al., in prep.).
Nedávno jsme však realizovali sérii experimentů ve voliéře, kde jsme testovali, zda štěnice C.
lectularius dlouhodobě parazitující na netopýrech, se nechají z umělých budek vynášet častěji
netopýry druhu N. noctula nebo netopýry druhu M. daubentonii, na kterých též parazitují. I
v experimentálních podmínkách se ukázalo, že si štěnice vybíraly významně více jedince
druhu N. noctula.
Je velmi nápadné, že jsou nalézány na netopýrech mimo jejich úkryty pouze imaga a
to především dospělé samice. S ohledem na signifikantně delší přežívání samic (Bartonička
2010) je pravděpodobné, že nymfy při opuštění kolonie mají mnohem menší perspektivu
kolonizovat nová stanoviště. Opakovaná přítomnost dospělých samic na netopýrech je zcela
nenáhodná. Doba sání navíc není u imag výrazně delší ve srovnání s nymfami, aby zvyšovala
pravděpodobnost jejich vynesení z úkrytu (Bartonička 2008, 2010). Úspěšná kolonizace
nového hostitelského úkrytu štěnicemi však předpokládá dvě skutečnosti. První z nich je
bezpochyby schopnost přečkat v úkrytu do doby příletu většího počtu hostitelů. Tento
předpoklad byl opakovaně potvrzen terénním pozorováním transportu dospělých samic, které
mají vyšší přežívaní než nymfy i dospělí samci. Druhou skutečností je potřeba přenosu
spářené samice. Spermie jsou pozorovatelné v těle samice pouze po dobu několika hodin, a
proto nebylo možno dostupný materiál na přítomnost spermatu vyšetřit (Balvín et al. 2012b).
V podmínkách voliéry byla testována i hypotéza, zda se z úkrytů nechávají častěji vynášet
spářené samice než samice dosud nepářené (Bartonička, in prep.). Nicméně významně vyšší
počty spářených samic na vyletujících netopýrech nebyly zjištěny. Zde bude patrně nutno více
uvážit variabilitu chování imag samic v průběhu sezóny.
Tyto experimenty a řada výše uvedených okolností potvrzují, že štěnice si, pokud
mohou, aktivně vybírají druh netopýra. K objasnění důvodu proč tak činí, bude ještě potřeba
32
provést řadu pokusů. Jedním z nich by mohlo například být srovnání rychlosti probouzení
z denního torporu u běžně parazitovaných druhů.
Závěrem kapitoly je však nutno pouzázat na v těchto detailech omezené znalosti v
chování netopýrů a štěnic vůbec. Úroveň poznání, která by potvrdila výše uvedená tvrzení,
nemusí být dostačující, a je nutno připustit jistou míru spekulativnosti. V každém případě je
v současnosti obtížné rozhodnout, zda rozdílná frekvence výskytu štěnic na různých druzích
netopýrů souvisí s aktivním výběrem štěnice anebo pouze s odlišným chováním a
úkrytovými strategiemi jednotlivých druhů netopýrů.
4. Závěr
Shrnujícím úvodem předkládaných publikací a prací, které s tématem habilitační práce
úzce souvisí, jsem se pokusil ukázat, že štěnice jsou dobrým modelem pro výzkum vztahů
parazit-hostitel zejména v proximátní rovině vzájemných behaviorálních odpovědí.
V posledních letech se štěnice těší nebývalé pozornosti právě díky jejich úspěšnému šíření u
lidí. Štěnice jsou však původními hostiteli netopýrů a na člověka přešly později, v době
využívání společných prostor. S intenzivním rozvojem laboratorních detekčních metod
různých patogenů se lze stále častěji v lékařské i veterinární literatuře setkat se studiemi, které
uvádějí letouny jako významné vektory a jejich populace jako refugia řady patogenů. Mnohé
studie jsou však čistě laboratorní a patrně tlak ze strany oponentů nebo editorů vedou
k doplňování spekulativních informací týkajících se jejich zoonotických cyklů. Tyto úvahy,
do jisté míry zneužívající informační deficity v biologii letounů, však nevedou k obecnému
poznání a hlubšímu pochopení závislostí ve volné přírodě, spíše naopak. Výsledkem jsou pak
často až poplašné tiskové zprávy vedoucí sice ke zvýšení atraktivity dané publikace, ale také
v jisté míře k matení veřejnosti. V dílčích studiích předkládané habilitační práce jsem se
pokusil ukázat, že řada drobných terénních i experimentálních studií může vést k postupnému
objasnění komplexní problematiky parazitace štěnicemi, od antiparazitárních strategií
netopýrů, přes hostitelskou specifitu štěnic, po jistou rehabilitaci netopýrů jako hlavního
přenašeče štěnic do lidských obydlí.
5. Použitá literatura
* Abul - Hab J., 1979: On the bed bugs (Hemiptera, Cimicidae) in Iraq. Iraq Bulletin of
Endemic Diseases, 19: 65-76.
* Abul - Hab J., Shihab B.A., 1990: Ectoparasites of some bats from Iraq. Bulletin of Iraq
Natural History Museum, 8: 59-64.
Adelman Z.N., Miller D.M., Myles K.M., 2013: Bed Bugs and Infectious Disease: A Case for
the Arboviruses. PLoS Pathogens, 9(8): e1003462. doi:10.1371/journal.ppat.1003462.
33
Armitage S.J., Jasim S.A., Marks A.E., Parker A.G., Usik V.I., Uerpmann H.P., 2011: The
southern route “out of Africa”: evidence for an early expansion of modern humans into
Arabia. Science, 331: 453–456.
Baagøe H.J., 2012: Bechsteins flagermus – ynglende bestand på Bornholm. Natur på
Bornholm, 10: 55-59.
Balvín O., 2005: Středoevropské druhy rodu Cimex (Heteroptera: Cimicidae): literární
přehled. Seminární práce, Katedra Zoologie, Přírodovědecká Fakulta Univerzity Karlovy v
Praze, Prague, 48 s.
Balvín O., 2008: Revize druhů rodu Cimex (Heteroptera: Cimicidae) ve střední Evropě.
Diplomová práce. Katedra Zoologie, Přírodovědecká Fakulta Univerzity Karlovy v Praze,
Prague, 94 s.
Balvín O., 2010: Evolution and ecology of the bat bugs of the family Cimidae (Heteroptera).
Pp. 268–269, In A tribute to Bats (Horáček I. & Uhrin M., eds.). Lesnická Práce, Kostelec,
400 pp.
Balvín O., 2013: Fylogeografie a ekologie štěnic rodu Cimex (Heteroptera: Cimicidae) v
Evropě; evoluce taxonů a hostitelské specializace. Doktorská práce, Katedra Zoologie,
Přírodovědecká Fakulta Univerzity Karlovy v Praze, Prague, 46 s.
Balvín O., Munclinger P., Kratochvíl L. & Vilímová J. 2012a. Mitochondrial DNA and
morphology show independent evolutionary history of bed bug Cimex lectularius
(Heteroptera: Cimicidae) on bats and humans. Parazitology Research 111: 457-469.
Balvín O., Ševčík M., Jahelková H., Bartonička T., Orlova M. & Vilímová J., 2012b:
Transport of bugs of the genus Cimex (Heteroptera: Cimicidae) by bats in western
Palaearctic. Vespertilio, 16: 43-54.
Balvín O., Vilímová J., Kratochvíl L., 2013: Batbugs (Cimex pipistrelli group, Heteroptera:
Cimicidae) are morphologically, but not genetically differentiated among bat hosts. Journal
of Zoological Systematics and Evolutionary Research, 51 (4): 287–295.
Barclay R.M.R., Brigham R.M., 2001: Year-to-year reuse of tree-roosts by California bats
(Myotis californicus) in southern British Columbia. American Midland Naturalist, 146: 80–
85.
Barclay R.M.R., Fenton M.B., Thomas D.W., 1979: Social behavior of the little brown bat,
Myotis lucifigus. Behavioral Ecology and Sociobiology, 31:137-146.
Barrett R.D.H., Rogers S.M., Schluter D., 2008: Natural selection on a major armor Gene in
threespine stickleback. Science, 322: 255-257.
Bartonička T., 2004: Letová aktivita a echolokační chování druhu Pipistrellus pygmaeus
(Leach, 1825) s přihlédnutím k Pipistrellus pipistrellus (Schreber, 1774). Disertační práce,
Katedra zoologie a ekologie, Přírodovědecká fakulta Masarykovy univerzity v Brně, Brno,
89 s.
Bartonička T., 2007: Bat bugs (Cimex pipistrelli, Heteroptera) and roost switching in bats.
Berichte der Naturforschenden Gesellschaft der Oberlausitz, Supplement zu Band, 15: 29–
36.
Bartonička T., 2008: Cimex pipistrelli (Heteroptera, Cimicidae) and the dispersal propensity
of bats: an experimental study. Parasitology Research, 104:163–168.
Bartonička T., 2010: Survival rate of bat bugs (Cimex pipistrelli, Heteroptera) under different
microclimatic conditions. Parasitology Research, 107: 827–833.
Bartonička T., Bielik A., Řehák Z., 2008. Roost switching and activity patterns in the soprano
pipistrelle, Pipistrellus pygmaeus, during lactation. Annales Zoologici Fennici, 45(6): 503–
512.
Bartonička T., Gaisler J., 2007: Seasonal dynamics in the numbers of parasitic bugs
(Heteroptera, Cimicidae): a possible cause of roost switching in bats (Chiroptera,
Vespertilionidae). Parasitology Research, 100: 1323-1330.
34
Bartonička T., Gaisler J., 2010: Summer monitoring of bat populations. Pp. 113-124, In A
tribute to bats (Horáček I., Uhrin M., eds.). Lesnická práce, Kostelec nad Černými lesy,
400 pp.
Bartonička T., Růžičková L., 2012: Bat bugs (Cimex pipistrelli) and their impact on nondwelling
bats. Parasitology Research, 111: 1233–1238.
Bartonička T., Růžičková L., 2013: Recolonization of bat roost by bat bugs (Cimex
pipistrelli): could parasite load be a cause of bat roost switching? Parasitology Research,
112: 1615–1622.
Bartonička T., Řehák Z., 2007: Influence of the microclimate of bat boxes on their occupation
by the soprano pipistrelle Pipistrellus pygmaeus: possible cause of roost switching. Acta
Chiropterologica, 9(2): 517–526.
Bogdanowicz W., 1994: Myotis daubentonii. Mammalian Species, 475: 1-9.
Boonman M., 2000: Roost selection by noctules (Nyctalus noctula) and Daubenton’s bats
(Myotis daubentonii). Journal of Zoology, London, 251: 385–389.
Brigham R.M., Vonhof M.J., Barclay R.M.R., Gwilliam J.C., 1997: Roosting behaviour and
roost-site preferences of forest-dwelling California bats (Myotis californicus). Journal of
Mammalogy, 78: 1231-1239.
Brooks D.R., McLennan D.A., 1993: Parascript. Parasites and the language of evolution.
Washington and London, Smithsonian Institution Press, 448 pp.
Brown C.R., Brown M.B., 1998: Fitness components associated with alternative reproductive
tactics in Cliff Swallows. Behavioral Ecology, 9: 158–171.
Burton G.J., 1963: Bedbugs in relation to transmission of human diseases. Review of the
literature. Public Health Reports, 78: 513–24.
Butler J.M., Roper T.J., 1996: Ectoparasites and sett use in European badgers. Animal
Behaviour, 52: 621-629.
Ceľuch M., Danko Š., Kaňuch P., 2006: On urbanisation of Nyctalus noctula and Pipistrellus
pygmaeus in Slovakia. Vespertilio, 9–10: 219–221.
Combes C., Théron A., 2000: Metazoan parasites and resource heterogeneity: constraints and
benefits. International Journal of Parasitology, 30: 299–304.
Davidson-Watts I., Jones G. 2006: Differences in foraging behaviour between Pipistrellus
pipistrellus Schreber, 1774 and Pipistrellus pygmaeus Leach, 1825. Journal of Zoology,
London 268: 55–62.
Davis M.T., 1964: Studies of the reproductive physiology of Cimicidae (Hemiptera). I.
Fecundation and egg maturation. Journal of Insect Physiology, 10: 947-963.
Davis R.F., Johnston G.A., Sladden M.J., 2009: Recognition and management of common
ectoparasitic diseases in travelers. American Journal of Clinical Dermatology, 10: 1-8.
Delaunay P., Blanc V., Del Giudice P., Levy-Bencheton A., Chosidow O., Marty P., Brouqui
P., 2011: Bedbugs and infectious diseases. Clinical Infectious Diseases, 52(2): 200-10.
deLope F., Møller A.P., 1993: Female reproductive effort depends on the degree of
ornamentation of their mates.Evolution, 47: 1152-1160.
Dietz M., Walter G., 1995: Zur Ektoparasitenfauna der Wasserfledermaus (Myotis
daubentonii Kuhl, 1819) in Deutschland unter der besonderen Berücksichtigung der
saisonalen Belastung mit der Flughautmilbe Spinturnix andegavinus Deunff, 1977.
Nyctalus, 5: 451–468.
Dietz C., von Helversen O., Nill D., 2007: Die Fledermäuse Europas und Nordwestafrikas.
Biologie, Kennzeichen, Gefährdung. Kosmos Verlag, Stuttgart. 399 s.
Doggett S.L., Dwyer D.E., Penas P.F., Russell R.C., 2012: Bed bugs: clinical relevance and
control options. Clinical Microbiology Reviews, 25: 164–192.
35
Drès M., Mallet J., 2002: Host races in plant-feeding insects and their importance in
sympatric speciation. Philosophical Transactions of the Royal Society of London, Series B,
357: 471-492.
Dubinin V.E., 1947: Ekologičeskije nabljuděnia nad krovososuščimi klopami sem. Cimicidae
ďaurskou stěpi. Entomologičeskoje obozrenie, 29: 232-246.
Dzal Y., Hooton L.A.,Clare E.L., Fenton M.B., 2009: Bat activity and genetic diversity at
Long Point, Ontario, an important bird stopover site. Acta Chiropterologica, 11: 307–315.
Esch G.W., Gibbons J.W., Bourque J.E., 1975: An analysis of the relationship between
stress and parasitism. American Midland Naturalist, 93: 339-353.
Fleischmann D., Kerth G., 2014: Roosting behavior and group decision making in 2 syntopic
bat species with fission-fusion societies. Behavioral Ecology, 25(5): 1240-1247.
Feyerabend F., Simon M., 2000: Use of roosts and roost switching in a summer colony of 45
kHz phonic type pipistrelle bats (Pipistrellus pipistrellus Schreber,1774). Myotis, 38: 51-
59.
Funakoshi K., 1977: Ecological studies on the bats fly, Penicillida jenynsii (Diptera.
Nycteribiidae), infesting the Japanese long-fingered bat, with special reference to their
adaptation to the life cycle of their hosts. Japanese Journal of Ecology, 27: 125-140.
Funk D.J., 2012: Of “Host Forms” and Host Races: Terminological Issues in Ecological
Speciation. International Journal of Ecology, Volume 2012, Article ID 506957, 8
pp.,doi:10.1155/2012/506957.
Gandon S., Michalakis Y., 2002: Local adaptation, evolutionary potential and host-parasite
coevolution: interactions between migration, mutation, population size and generation
time. Journal of Evolutionary Biology, 15: 451-462.
Gannon M.R., Willig M.R., 1995: Ecology of ectoparasites from tropical bats. Environmental
Entomology, 24(6): 1495-1503.
Gaisler J., 1970: Remarks on the thermopreferendum of Palearctic bats in their natural
habitats. Bijdragen tot de Dierkunde, 40: 33-35.
Gibbons P., Lindenmayer D.B., Barry S.C., Tanton M.T., 2002: Hollow selection by
vertebrate fauna in forests of southeastern Australia and implications for forest
management. Biological Conservation, 103: 1-12.
Gindal S.D., 1996: Habitat use by bats in fragmented forests. Pages 260–272 in R.M.R.
Barclay & R. M. Brigham (eds). Proceedings of Bats and Forests Symposium. Resources
Branch, Ministry of Forests, Victoria, British Columbia.
Goddard J., deShazo R., 2009: Bed bugs (Cimex lectularius) and clinical consequences of
their bites. The Journal of the American Medical Association, 301: 1358–1366.
Grindal S.D., 1999: Habitat use by bats, Myotis spp., in western Newfoundland. Canadian
Field-Naturalist, 113: 258–263.
Grindal S.D., Brigham R.M., 1998: Short-term effects of small-scale habitat disturbance on
activity by insectivorous bats. Journal of Wildlife Management, 62: 996–1002.
Grulich I., Povolný D., 1955: Faunisticko-bionomický nástin muchulovitých (Nycteribiidae)
na území ČSR. Zoologické a entomologické listy, IV.(XVIII), 2: 111-134.
Hamilton I.M., Barclay R.M.R., 1994: Patterns of daily torpor day roost selection by male and
female big brown bats (Eptesicus fuscus). Canadian Journal of Zoology, 72: 744-749.
Harmata W., 1969: The thermopreferendum of some species of bats Chiroptera. Acta
Theriologica, 14: 49-62.
Hausfater G., Meade B.J., 1982: Alternation of sleeping groves by yellow baboons (Papio
cynocephalus) as a strategy for parasite avoidance. Primates, 23: 287–297.
Heise G., 1988: Zum Transport von Fledermauswanzen (Cimicidae) durch ihre Wirte.
Nyctalus, 2(5): 469-473.
36
Henry T.J. 2009: Biodiversity of the Heteroptera. Pp. 223-263, In Insect Biodiversity: Science
and Society (Foottit R.G. & Adler P.H., eds.). Oxford, England: Wiley-Blackwell., 656
pp.
Horáček I., 1986: Létající savci. Academia, 156 s.
Horváth G., 1910: Species nova Europaea cimicum sanguisugarum. Annales Musei Nationalis
Hungarici, 7: 631-632.
Horváth G., 1913: Objev štěnice Cimex dissimilis Horv. v Čechách. Časopis České
společnosti entomologické, 10: 140-142.
Horváth G., 1935: Eine neue Fledermauswanze aus dem Spessart. Mitteilungen der Deutschen
Entomologischen Gesselschaft, 6: 14-15.
Hůrka K., Povolný D.,1968: Faunal and ecological study on the families Nycteribiidae and
Streblidae (Dipt., Pupipara) of the Nangarhar province (Eastern Afganistan). Acta
Entomologia Bohemoslovakia, 65: 285-298.
Hutterer R., Ivanova T., Meyer-Cords Ch., Rodrigues L., 2005: Bat migration in Europe. A
review of banding data and literature. Federal Agency for Nature Conservation, Bonn, 162
pp.
Huyse T., Poulin R., Théron A., 2005: Speciation in parasites: a population genetics approach.
Trends in Parasitology, 21: 469–475.
Christe P., Arlettaz R., Vogel P., 2000: Variation in intensity of a parasitic mite (Spinturnix
myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis
myotis). Ecology Letters, 3: 207–212.
Christe P., Richner H., Opplinger A., 1996: Of great tits and fleas: sleep baby sleep. Animal
Behaviour. 52: 1087–1092.
Jaenike J., 1996: Population-level consequences of parasite aggregation. Oikos, 76: 155-160.
Jahelková H., Lučan R. & Hanák V., 2000: Nové údaje o netopýru parkovém (Pipistrellus
nathusii) v jižních Čechách. Lynx, n.s., 31: 41–51.
Jenyns L., 1839: On three undescribed species of the genus Cimex, closely allied to the
common bed-bug. Annals and Magazine of the Natural History Museum, 3: 241-244.
Johnson C.G., 1942: The ecology of the bed-bug, Cimex lectularius L., in Britain. Journal of
Hygiene, 41: 345-361.
Johnson C.G., 1960: The relation of weight of food ingested to increase in body-weight
during growth in the bed-bug, Cimex lectularius L. (Hemiptera). Entomologia
Experimentalis et Applicata, 3: 238–240.
Jones R.M., 1930: Some effects of temperature and humidity as factors in the biology of the
bedbug (Cimex lectularius Linn.). Annals of the Entomological Society of America, 23:
105–119.
Kaňuch P., Ceľuch M., 2004: On the southern border of the nursing area of the noctule in
Central Europe. Myotis, 41–42: 125–127.
Kerth G., König B., 1996: Transponder and an infrared-videocamera as methods used in a
fieldstudy on the social behaviour of Bechstein’s bats (Myotis bechsteinii). Myotis, 34:
27-34.
Kerth G., König B., 1999: Fission, fusion and non random associations in female Bechstein´s
bats (Myotis bechsteinii). Behaviour, 136: 1187-1202.
Kerth G., Weissmann K., Konig B., 2001: Day roost selection in female Bechstein´s bats
(Myotis bechsteinii): a field experiment to determine the influence of roost temperature.
Oecologia, 126(1): 1-9.
Klug B.J, Barclay R.M.R., 2013: Thermoregulation during reproduction in the solitary,
foliage-roosting hoary bat (Lasiurus cinereus). Journal of Mammalogy, 94(2): 477-487.
Kolb A., Needham G.R., Neyman K.M., High W.A., 2009: Bedbugs. Dermatology and
Therapy, 22: 347-52.
37
Kerzhner I.M., 1989: Cimex pipistrelli aus der (Heteroptera, Cimicidae) Mongolei.
Mitteilungen aus dem Zoologischen Museum in Berlin, 65: 341–342.
Krištofík J., Kaňuch P., 2006: First record of Cimex pipistrelli (Cimicidae) in Slovakia.
Biologia, 61: 219–220.
Kunz T.H., Lumsden L.F., 2003: Ecology of cavity and foliage roosting bats. Pp. 3–89, Bat
Ecology (Kunz T.H., Fenton M.B., eds.) University of Chicago Press, Chicago, 798 pp.
Kusch J., Weber C., Idelberger S., Koob T., 2004: Foraging habitat preferences of bats in
relation to food supply and spatial vegetation structures in a western European low
mountain range forest. Folia Zoologica, 53: 113-128.
Lansbury I., 1961: Comments on the genus Cimex (Hem. Het. Cimicidae) in the British Isles.
The Entomologist, 94: 133-134.
Lanza B., 1999: I parassiti dei pipistrelli (Mammalia, Chiroptera) della fauna italiana. Museo
Regionale di Scienze Naturali, Torino. 318 pp.
Lausen C.L., Barclay R.M.R., 2002: Roosing behavior and roost selection of female big
brown bats (Eptesicus fuscus) roosting in rock crevices in southeastern Alberta. Canadian
Journal of Zoology, 80(6): 1069-1076.
Lederer G., 1950: Auftreten von Cimex hemipterus Fabricius 1803 = C. rotundatus Sign.
sowie anderer Cimexarten in Hessen (Heteropt. Cimicidae). Anzieger für Schädlingskunde,
23: 44-46.
Ledvinka J., Rupeš V., Vlčková J., 2008: Štěnice se vracejí. Nezvaný host v bohatých i
chudých bytech. Vesmír, 87(7): 477-479.
Lefebvre D., Menard N., Piere J.S., 2003: Modelling the influence of demographic
parameters on group structure in social species with dispersal asymmetry and group
fission. Behavioral Ecology and Sociobiology, 53: 402-410.
Lewis S.E., 1995: Roost fidelity of bat: a review. Journal of Mammalogy, 76: 481-496.
Lewis S.E., 1996: Low roost-site fidelity in pallid bats: associated factors and effect on group
stability. Behavioral Ecology and Sociobiology, 39: 335-344.
Lourenço S.I., Palmeirim J.M., 2004: Influence of temperature in roost selection by
Pipistrellus pygmaeus (Chiroptera): relevance for the design of bat boxes. Biological
Conservation, 119: 237-243.
Loye J.E, Carroll S.P., 1991: Nest ectoparasite abundance and cliff swallow colony site
selection, nestling development, and departure time. Pp. 222–241, In Bird–parasite
interactions. Ecology, behaviour and evolution (Loye J.E. & Zuk M., eds). Oxford
University Press, Oxford, 422 pp.
Lučan R.K., 2006: Relationships between parasitic mite Spinturnix andegavinus (Acari:
Spinturnicidae) and its bat host, Myotis daubentonii (Chiroptera: Vespertilionidae):
seasonal, sex– and age–related variation in infestation and possible impact of parasite on
the host condition and roosting behaviour. Folia Parasitologica, 53: 147-152.
Maestre R.H., 2013: The bed bug book: The complete guide to prevention and extermination.
Skyhorse Publishing Inc., 208 pp.
Marshall A.G., 1980: The comparative ecology of insect ectoparasitic upon bats in West
Malaysia. Pp. 135-142, In proceeding of the Fifth International Bat Research Conference.
(Wilson D.E. & Gardner A.L., eds.). Texas Tech Press, Lubbock, 434 pp.
Marshall A.G., 1981: The ecology of ectoparasitic insects. Academic Press, London, 459 pp.
Marshall A.G., 1982: The ecology of Eoctenes spasmae (Hemiptera: Polyctenidae) in
Malaysia. Biotropica, 14: 50-55.
Mayr E., 1963: Animal species and evolution. Cambridge, MA, Harvard University Press.
797 pp.
38
Mazurek M.J., 2004: A maternity roost of Towsend´s big-eared bats (Corynorhinus
towsendii) in coast redwood basal hollows in northwestern California. Northwestern
Naturalist, 85: 60–62.
Melhorn H., 2008: Encyclopedia of parasitology. 3rd ed. Berlin, Springer, 860 pp.
Meschede A., 2001: Bats in Forests - Information and Recommendations for Forest
Managers. Landschaft als Lebensraum 4. Bundesamt für Naturschutz, Deutscher Verband
für Landschaftspflege, Bonn, Ansbach, 18 pp.
Meschede A., Heller K.-G., 2000: Ökologie und Schutz von Fledermäusen in Wäldern.
Schriftenreihe für Landschaftspflege und Naturschutz 66. Budesamt für Naturschutz,
Bonn, 325 pp.
Morkel C., 1999: Zum Vorkommen von an Fledermäusen (Chiroptera) parasitierenden
Bettwanzen der Gattung Cimex Linnaeus 1758 in Hessen (Heteroptera, Cimicidae).
Hessische Faunistische Briefe, 18: 38-48.
Moura M.O., Bordignon M.O., Graciolli G., 2003: Host characteristics do not affect
community structure of ectoparasites on the fishing bat Noctilio leporinus (L., 1758)
(Mammalia: Chiroptera). Memorias do Instituto Oswaldo Cruz., 98 (6): 811-815.
Nelson B., Smiddy P., 1997: Records of the bat bug Cimex pipistrelli Jenyns (Hemiptera:
Cimicidae) from Cos Cork and Waterford. Irish Naturalists' Journal, 25: 344-345.
Oppliger A., Richner H., Christe P. 1994: Effect of an ectoparasite on lay date, nest-site
choice, desertion, and hatching success in the great tit (Parus major). Behavioral
Ecolology, 5: 130–134.
Orlova M.V., Pervušina E.M., 2010: Èktoparazity rukokrylyh Srednego Urala [Ectoparasites
of bats in the Middle Ural Mts.]. Plecotus et al., 13: 83–87 (in Russian, with a summary in
English).
Orlova M.V., Kapitonov V.I., Griror’ev A.K., Orlov O.L., 2011: Èktoparazity rukokrylyh
Udmurtskoj Respubliky [Bat ectoparasites of the Udmurtia Republic]. Vestnik
Udmurtskogo Universiteta, 2: 134–138 (in Russian, with a summary in English).
Overal W.L., 1980: Host-relations of the bat fly Megistopoda aranea (Diptera: Streblidae) in
Panama. Kansas University Science Bulletin, 52: 1-20.
Overal W.L., Wingate L.R., 1976: The biology of the batbug Stricticimex antennatus
(Hemiptera: Cimicidae) in South Africa. Annals of the Natal Museum, 22: 821-828.
Park K.J., Altringham J.D., Jones G., 1996: Assortative roosting in the two phonic types of
Pipistrellus pipistrellus during the mating season. Proceedings of the Royal Society B:
Biological Sciences, 263: 1495–1499.
Patterson B.D., Ballard J.W.O., Wenzel R.L., 1998: Distributional evidence for cospeciation
between neotropical bats and their bat fly ectoparasites. Studies on Neotropical Fauna and
Environment, 33 (2-3): 76-84.
Peinke D.M., Brown C.R., 2005: Burrow utilization by springhares (Pedetes capensis) in the
Eastern Cape, South Africa. African Zoology, 70: 37-44.
Péricart J., 1972: 7. Hémipterès Anthocoridae, Cimicidae ae Microphysidae de l´OuestPaléartique.
Faune de l´Europe et du Bassin Méditerranéen. Paris: Mason et Cue Éditeurs,
402 pp.
Péricart J., 1996: Family Cimicidae. Pp. 141-144, In Catalogue of the Heteroptera of the
Palearctic Region. (Aukema B. & Rieger C., eds.). Nederlandse Entomologische
Vereiniging, Wageningen. The Netherlands, Volume 2, Cimicomorpha I, 361 pp.
Petit E., Mayer F., 2000: A population genetic analysis of migration: the case of the noctule
bat (Nyctalus noctula). Molecular Ecology, 9: 683–690.
Povolný D., 1957: Kritická studie o štěnicovitých (Het. Cimicidae) v Československu. Folia
Zoologica, 6: 59-80.
Potter M. F., 2008: The business of bed bugs. Pest Management Professional, 76(1): 24–40.
39
Protić L., Paunović M., 2006: Bat bugs Cimex dissimilis (Horváth, 1910) (Heteroptera:
Cimicidae) – the first record from Serbia. Pp. 8–9, In 3rd Meeting of the International
Heteropterists Society (Aukema B., ed.), 18–21 July, Wageningen, Netherlands.
International Heteropterists’ Society, Washington, 31 pp.
Pulliam J.R., Dushoff J.G., Levin S.A., Dobson A.P., 2007: Epidemic enhancement in
partially immune populations. PLoS ONE, 2: e165.
Quay W.B., 1970: Integument and derivatives. Pp. 2–56, In Biology of bats (Wimsatt W.A.,
ed.). Academic Press, 406 pp.
Quetglas J., Balvín O., Lučan R., Benda P., 2012: First records of the bat bug Cacodmus
vicinus (Heteroptera: Cimicidae) from Europe and further data on its distribution.
Vespertilio, 16: 243–248.
Rancourt S.J., Rule M.I., O'Connell M.A., 2005: Maternity roost site selection of long-eared
myotis, Myotis evotis. Journal of Mammalogy, 86: 77–84.
Rantala M.J., 1999: Human nakedness: adaptation against ectoparasites? International Journal
for Parasitology, 29: 1987-1989.
Reinhardt K., 2007: Evolutionary consequences of sperm ageing. Quarterly Review of
Biology, 82: 375-393.
Reinhardt K., Harder A., Holland S., Hooper J., Leake-Lyall C., 2008b: Who knows the bed
bug? Knowledge of adult bed bug appearance increases with people's age in three counties
of Great Britain. Journal of Medical Entomology, 45(5): 956-958.
Reinhardt K., Kempke D., Naylor R.A., Siva-Jothy M.T., 2009: Sensitivity to bites by the
bedbug, Cimex lectularius. Medical and Veterinary Entomology, 23: 163-6.
Reinhardt K., Naylor R.A., Siva-Jothy M.T., 2005: Potential sexual transmission of
environmental microbes in a traumatically inseminating insect. Ecological Entomology,
30: 607–11.
Reinhardt K., Naylor R.A., Siva-Jothy M.T., 2008a: Temperature and humidity differences
between roosts of the fruit bat, Rousettus aegyptiacus (Geoffroy, 1810), and the refugia of
its ectoparasite, Afrocimex constrictus. Acta Chiropterologica, 10: 173–176.
Reinhardt K., Siva-Jothy M.T., 2007: Biology of the bedbugs (Cimicidae). Annual Review of
Entomology, 52: 351–374.
Reckardt K., Kerth G., 2006: The reproductive success of the parasitic bat fly Basilia nana
(Diptera: Nycteribiidae) is affected by the low roost fidelity of its host, the Bechstein’s bat
(Myotis bechsteinii). Parasitology Research, 98: 237–243.
Reckardt K., Kerth G., 2007: Roost selection and roost switching of female Bechstein’s bats
(Myotis bechsteinii) as a strategy of parasite avoidance. Oecologia, 154: 581–588.
Rendell W.B., Verbeek N.A.M., 1996: Old nest material in nestboxes of tree swallows:
Effects on reproductive success. Condor, 98: 145-155.
Richner H., Oppliger A., Christe P., 1993: Effect of an ectoparasite on reproduction in great
tits. Journal of Animal Ecology, 62: 703-710.
Ritzi C.M., Ammerman L.K., Dixon M.T., Richerson J.V., 2001: Bat ectoparasites from the
Trans-Pecos region of Texas, including notes from Big Bend National Park. Journal of
Medical Entomology, 38 (3): 400-404.
Ritzi C.M., Whitaker J.O.Jr., 2003: Ectoparasites of small mammals from the Newport
Chemical Depot, Vermillion County, Indiana. Northeastern Naturalist, 10 (2): 149-158.
Rivnay E., 1930: Host selection and cannibalism in the bed bug Cimex lectularius L. Annals
of the Entomological Society of America, 23: 758–764.
Rivnay E., 1932: Studies in tropisms of the bed bug Cimex lectularius L. Parasitology, 24:
121–136.
40
Rooij H.A. van, Voute A.M., Bronswijk J.E.M.H., 1982: De bloedzuigende insekten (vlooien,
wantsen en luisvliegen) van de Meervleermuis in Nederland. Natura (Hoogwoud), 79: 119-
121.
Romero A., Potter M.F., Potter D.A., Haynes K.F., 2007: Insecticide resistance in the bed
bug: a factor in the pest's sudden resurgence? Journal of Medical Entomology, 44: 175-
178.
Roper T.J., Jackson T.P., Conradt L., Bennett N.C., 2002: Burrow use and the influence of
ectoparasites in Brants’ whistling rat Parotomys brantsii. Ethology, 108: 557–564.
Roper T.J., Ostler J.R., Schmid T.K., Christian S.F., 2001: Sett use in European badgers
Meles meles. Behaviour, 138: 173-188.
Rosický B., 1957: Fauna ČSR (sv. 10): Blechy -Aphaniptera. Praha: Československá
akademie věd. 439 s.
Rupp D., Zahn A., Ludwig P., 2004: Actual records of bat ectoparasites in Bavaria
(Germany). Spixiana, 27(2): 185–190.
Ruczyński I., Nicholls B., MacLeod C.D., Racey P.A., 2010: Selection of roosting habitats by
Nyctalus noctula and Nyctalus leisleri in Białowieża. Forest-adaptive response to forest
management? Forest Ecology and Management, 259: 1633–1641.
Russo D., Cistronec L., Jones G., Mazzolenia S., 2004: Roost selection by barbastelle bats
(Barbastella barbastellus, Chiroptera: Vespertilionidae) in beech woodlands of central
Italy: consequences for conservation. Biological Conservation, 117: 73–81.
Růžičková L., 2012: Štěnice Cimex pipistrelli - její hostitelská specifita a rychlost
rekolonizace netopýřích úkrytů. Diplomová práce. Ústav botaniky a
zoologie,Přírodovědecká fakulta Masarykovy univerzity, Brno, 82 s.
Rybin N., Horáček I.,Červený J., 1989: Bats of southern Kirghizia: distribution and faunal
status. Pp 421–441, In European bat research 1987 (Hanák V., Horáček I., Gaisler J., eds).
Charles University Press, Prague, 718 pp.
Ryšavý B., Černá Ž., Chalupský J., Országh I., Vojtek J., 1988: Základy parazitologie. Státní
pedagogické nakladatelství, Praha. 216 str.
Sailer R., 1952: The bedbug: an old bedfellow that’s still with us. Pest Control, 20(10): 22-24.
Sasse D.B., Pekins P.J., 2000: Ectoparasites observed on northern long-eared bats, Myotis
septentrionalis. Bat Research News, 41 (3): 69-71.
Sedgeley J.A., O’Donnell C.F.J., 1999: Roost selection by the long-tailed bat, Chalinolobus
tuberculatus, in temperate New Zealand rainforest, and its implications for the
conservation of bats in managed forests. Biological Conservation, 88: 261-276.
Seidel C., Reinhardt K., 2013: Bugging forecast: unknown, disliked, occasionally intimate.
Bed bugs in Germany meet unprepared people. PLOS One, 8e51083,
doi:10.1371/journal.pone.0051083.
Scheffler I., 2011: Die Ektoparasiten der Fledermäuse Europas – Teil 1. Nyctalus, 16: 246-
263.
Simov N., Ivanova T., Schunger I., 2006: Bat-parasitic Cimex species (Hemiptera: Cimicidae)
on the Balkan Peninsula, with zoogeographical remarks on Cimex lectularius, Linnaeus.
Zootaxa 1190: 59-68.
Southwood T.R.E., 1954: The production of fertile eggs by Cimex pipistrelli Jenyns 1839
(Hem. Cimicidae) when fed on human blood. The Entomologist´s Monthly Magazine, 90:
35.
Southwood T.R.E., Leston D., 1959: Land and water bugs of the British Isles. Fr. Warne &
Co. Ltd., London. xi + 436 pp.
Spada M., Szentkuti S., Zambelli N., Mattei-Roesli M., Moretti M., Bontandina F., Arlettaz
R., Tosi G., Martinoli A., 2008: Roost selection by non-breeding Leisler’s bats (Nyctalus
41
leisleri) in montane woodlands: implications for habitat management. Acta
Chiropterologica 10(1): 81-88.
Stawski C., Willis C.K.R., GeiserF., 2014: The importance of temporal heterothermy in bats.
Journal of Zoology, 292(2): 86–100.
Stones R.C., Wiebers J.E., 1965: A Review of Temperature Regulation in Bats (Chiroptera).
American Midland Naturalist, 74(1): 155-167.
Swartz S., Bishop K., Aguirre M.-F. I., 2006: Dynamic complexity of wing form in bats:
implications for flight performance. Pp. 110-130, In Functional and Evolutionary Ecology
of Bats (Zubaid A., McCracken G.F., Kunz T.H., eds.). Oxford University Press, New
York, 360 pp.
Swift S.M., 1980: Activity patterns of pipistrelle bats (Pipistrellus pipistrellus) in north-east
Scotland. Journal of Zoology, London, 190: 285-295.
* Tagil'cev A.A. 1971: O členistonogich, sovrannych s nočnic v Zajsanskoj kotlovine.
Parazitologija, 5: 382-384.
Thollesson M., Norberg U.M., 1991: Moments of inertia of bat wings and body. Journal of
Experimental Biology, 158: 19–35.
Thompson M.J.A., 1990: The pipistrelle bat Pipistrellus pipistrellus Schreber on the Vale of
York. Naturalist, 115: 41-56.
Thompson M.J.A., 1992: Roost philopatry in female pipistrelle bats Pipistrellus pipistrellus.
Journal of Zoology, London, 228: 673-679.
Ueshima N., 1964: Experiments on reproductive isolation in Cimex lectularius and Cimex
columbarius (Hemiptera: Cimicidae). The Pan-Pacific Entomologist, 40: 47-53.
Usinger R.L., 1966: Monograph of Cimicidae (Hemiptera – Heteroptera). Entomological
Society of America. Thomas Say Foundation Vol. 7, New York, 585 pp.
Usinger R.L., Povolny D., 1966: The discovery of a possibly aboriginal population of the
bedbug (Cimex lectularius Linnaeus, 1758). Acta Musei Moroviae, 51: 237-242.
Volf P., Horák P., 2007: Paraziti a jejich biologie. Praha, Triton, 318 str.
Vonhof M.J., Barclay R.M.R., 1996: Roost-site selection and roosting ecology of forestdweling
bats in southern British Columbia. Canadian Journal of Zoology, 74: 1797-1805.
Wagner E., 1967: Wanzen oder Heteropteren II. Cimicomorpha, vol 55. Die Tierwelt
Deutschlands und der angrenzenden Meeresteile. Gustav Fischer, Jena.
Walter G., 1996: Zum Ektoparasitenbefall der Fledermäuse und den potentiellen
Auswirkungen. Myotis, 34: 85–92.
Walter G., 2004: Űberblick zum Vorkommen und zur Biologie von Ectoparasiten
(Siphonaptera; Cimicidae; Nycteribiidae; Calliphoridae) bei Fledermäusen in Deutschland.
Nyctalus, 9(5): 460–476.
Wawrocka K., Bartonička T., 2013: Two different lineages of bedbug (Cimex lectularius)
reflected in host specificity. Parasitology Research, 112: 3897-904.
Webb P.I., Speakman J.R., Racey P.A., 1996: Population dynamics of a maternity colony of
the pipistrelle bats (Pipistrellus pipistrellus) in north-east Scotland. Journal of Zoology,
London, 240: 777-780.
Wendt A., 1941: Cimicidae in guide´s. Die Wanzen Mitteleuropas, 8: 119-131.
Willis C.K.R., Brigham R.M., 2004: Roost switching, roost sharing and social cohesion:
Forest-dwelling big brown bats (Eptesicus fuscus) conform to the fission-fusion model.
Animal Behaviour, 68: 495-505.
Willis C.K.R., Brigham R.M., 2005: Physiological and ecological aspects of roost selection
by reproductive female hoary bats (Lasiurus cinereus). Journal of Mammalogy, 86: 85-94.
Whitaker J.O., 1998: Life history and roost switching in six summer colonies of eastern
pipistrelles in buildings. Journal of Mammalogy, 79(2): 651-659.
42
Whitaker J.O.Jr., Deunff J., Belwood J.J., 2000: Ectoparasites of neonate Indiana bats, Myotis
sodalis (Chiroptera: Vespertilionidae), with description of male of Paraspinturnix globosa
(Acari: Spinturnicidae). Journal of Medical Entomology, 37 (3): 445-453.
Whitaker J.O., Mumford R.E., 1978: Food and ectoparasites of bats from Kenya, east Africa.
Journal of Mammalogy, 59(3): 632-634.
Whitfield F.G.S., 1939: Air transport, insects and disease. Bulletin of Entomological
Research, 30: 365-442.
Wolz I., 1986: Wochenstuben-Quartierewechsel bei der Bechsteinfledermaus. Zeitschrift für
Säugetierkunde, 51: 65-74.
Zahn A., Rupp D., 2004: Ectoparasite load in European vespertilionid bats. Journal of
Zoology, 262: 383–391.
Zedníková K., 2010: Přežívání štěnic (Cimex pipistrelli) v různých mikroklimatických
podmínkách. Diplomová práce. Katedra zoologie a ornitologická laboratoř,
Přírodovědecká fakulta, Univerzita Palackého v Olomouci, Olomouc, 52 s.
Práce označené * nebyly k dispozici.
6. Komentář k publikacím
Studie v prvním tematickém celku byly vedeny spíše potřebou definovat specifické
chování netopýrů v různých souvislostech jejich časoprostorových strategií. Díky terénnímu
pozorování byly odhaleny specifické vzorce ve využívání úkrytů, které nebylo možno
uspokojivě vysvětlit na základě doposud publikovaných výsledků. Na modelu úkrytových
strategií netopýrů rodu Pipistrellus byly diskutovány tradičně přijímané příčiny vysvětlující
střídání úkrytů. Dvě studie v tomto tematickém celku (8.1) osvětlily a částečně rozporovaly
interpretace úkrytového chování běžných středoevroských netopýrů v souvislosti s dosud
publikovanou literaturou.
Za nejvýznamnější však považuji studie v druhém tematickém celku (8.2), které
upozornily na existenci nového mechanismu - parazitaci štěnicemi, vysvětlujícího adaptivnost
střídání úkrytů (studie 3). Třetí studie v tomto tematickém bloku (5) demostrovala střídání
dvou vzorců chování při přítomnosti a absenci spouštěcího faktoru, vysoké abundance štěnic
v úkrytu netopýrů.
Jelikož v terénních podmínkách působí současně větší množství faktorů, kdy každý
z nich může vést k velmi podobnému vzorci chování, bylo nutno připravit sérii experimentů
v kontrolovaných podmínkách a ty doplnit o další pozorování. Studie z dalších dvou
tematických celků více či méně potvrzují oprávněnost úvah o adaptivním významu
studovaného mechanismu a dokreslují detaily ve vztahu hostitel (netopýr) a úkrytový parazit
(štěnice).
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V třetím tematickém celku (8.3) si pravděpodobně nejvíce cením studie 7, ve které
jsme adaptivnost mechanismu střídání úkrytů potvrdili i u druhů netopýrů se značně
odlišnými úkrytovými nároky.
Ve čtvrtém tematickém celku (8.4), který zahrnuje pouze jedinou publikovanou práci,
ale i několik již realizovaných experimentů zmíněných v úvodním textu, byl prostor věnován
problematice hostitelské specifity. Největší význam této studie spočívá v roli netopýrů jako
možných vektorů štěnice C. lectularius do lidských obydlí. Naše výzkumy prokázaly, že tyto
štěnice mohou na člověku úspěšně sát a založit dlouhobě fungující populace. Tato skutečnost,
bude-li nedostatečně citlivě sdělena široké veřejnosti, může již tak komplikované vztahy mezi
člověkem a netopýrem, ještě zhoršit. Lze očekávat, že pak veřejnost neuspokojí ani
informace, že prozatím takové populace (založené štěnicemi z netopýrů) nebyly v lidských
obydlích zjištěny (Balvín et al. 2013).
Závěrem bych chtěl poukázat na skutečnost, že publikace předkládané v habilitační
práci tvoří pouze necelou třetinu mé publikační aktivity a tak logicky i mnou (spolu)řešených
tematických okruhů. Práce však byly vybrány tak, aby tvořily logický tematický celek, který
je však současně značně odlišný od jiných publikovaných studií.
7. Úroveň spoluautorství a hlavní přínos předkládaných studiích
S výjimkou poslední práce (8) jsem vždy prvním autorem a tedy tím kdo provedl
statistické zpracování získaného materiálu a hlavním autorem textu. S výjimkou článků 1 a 2
jsem i jediným autorem nosné myšlenky konkrétní studie a navrhovatelem designu. U studií 1
a 2 jsem pak významně myšlenky studií pozměnil se zaměřením na publikaci vybraných
netriviálních poznatků.
(1) BARTONIČKA T. & ŘEHÁK Z., 2007: Influence of the microclimate of bat boxes on
their occupation by the soprano pipistrelle Pipistrellus pygmaeus: possible cause of roost
switching. Acta Chiropterologica, 9(2): 517–526.
V terénu jsem získal většinu dat samostatně, po konzultacích se spoluautorem (vedoucím mé
doktorské práce) je i samostatně vyhodnotil a jsem autorem textu článku.
Hlavní přínos práce: Studie porovnává mikroklimatické podmínky využívaných a nevyužívaných
umělých úkrytů netopýry v průběhu gravidity, laktace a postlaktace. S ohledem na odlišné klimatické
44
nároky reprodukujících se samic, jsme předpokládali, že podmínky budou mezi úkryty odlišné.
Překvapivě se však tato hypotéza nepotvrdila. V průběhu výzkumu nebyly zjištěny ani krátkodobé
výkyvy v teplotě (přehřívání, ochlazení), které by vysvětlovaly, proč reprodukující se samice netopýrů
úkryt na určitou dobu opouští. Výsledky studie připouští existenci dalšího doposud nezkoumaného
faktoru.
(2) BARTONIČKA T., BIELIK A. & ŘEHÁK Z., 2008: Roost switching and activity patterns
in the soprano pipistrelle, Pipistrellus pygmaeus, during lactation. Annales Zoologici Fennici,
45(6):503-512.
Jsem spoluautorem myšlenky a designu studie (se Z. Řehákem). Na terénním výzkumu se
intenzivně podílel s mnou podílel A. Bielik (diplomant Z. Řeháka), který pod mým a vedením
Z. Řeháka připravil podkladovou databázi. A. Bielik se rovněž podílel na části vyhodnocení
dat pro účely své diplomové práce, většinu výsledků jsem však vyhodnotil samostatně a jsem
hlavním autorem textu článku.
Hlavní přínos práce: V rámci výzkumu jsme zkoumali časoprostorovou aktivitu netopýra
Pipistrellus pygmaeus. K nejvýznamnějším zjištěním patřilo, že některé samice již koncem
laktace opakovaně navštívili teritoria samců v okolí úkrytu kolonie. Přestože některé samice
z původního úkrytu přenášely mláďata i do úkrytů jiných, po dobu laktace zůstala většina
jedinců v původním úkrytu kolonie. Po odstavu mláďat se však začala rychle rozpadat.
(3) BARTONIČKA T. & GAISLER J., 2007: Seasonal dynamics in the numbers of parasitic
bugs (Heteroptera, Cimicidae): a possible cause of roost switching in bats (Chiroptera,
Vespertilionidae). Parasitology Research, 100:1323–1330.
Jsem autorem myšlenky a designu výzkumu. Data v terénu jsem získal sám, zcela samostatně
je i vyhodnotil a jsem autorem text článku. Spoluautor text článku připomínkoval a upravil
jeho jazykovou stránku.
Hlavní přínos práce: Studie byla zaměřena na odhalení souvislosti střídání úkrytů u netopýrů
rodu Pipistrellus s abundancí štěnic v jejich úkrytech. Zjistili jsme, že netopýři opustili
sledované úkryty na období laktace. Během této doby uhynula většina raných instarů a období
nepřítomnosti netopýrů přežívala pouze vajíčka. Netopýři se do úkrytů vrátili s čerstvě
45
vzletnými mláďaty. Dočasné opuštění úkrytu netopýry efektivně potlačuje rozvoj populace
štěnic.
(4) BARTONIČKA T., 2010: Survival rate of bat bugs (Cimex pipistrelli, Heteroptera) under
different microclimatic conditions. Parasitology Research, 107:827–833.
Jsem autorem myšlenky článku a designu experimentu. Na laboratorních experimentech se
částečně podílela i K. Zedníková (moje diplomantka). Po částečných výsledcích (pro účely
diplomové práce) jsem objem laboratorní práce rozšířil asi na trojnásobek a dokončil ji
samostatně. Jsem autorem vyhodnocení dat a jediným autorem textu článku.
Hlavní přínos práce: Řada informací týkajících se přežívání v různých mikroklimatických
podmínkách v detailech ontogenetického vývoje je známa pouze od štěnice C. lectularius.
V experimentálních podmínkách jsem testoval přežívání štěnic C. pipistrelli, běžnějšího
druhu u netopýrů, v různých teplotách a následně jejich schopnost sání na hostiteli. Ukázalo
se, že na netopýry lépe adaptovaná štěnice C. pipistrelli lépe snáší vyšší teploty a má kratší
vývojový cyklus než štěnice C. lectularius.
(5) BARTONIČKA T. & RŮŽIČKOVÁ L., 2013: Recolonization of bat roost by bat bugs
(Cimex pipistrelli): could parasite load be a cause of bat roost switching? Parasitology
Research, 112:1615–1622.
Jsem autorem myšlenky výzkumu a jeho designu. Též jsem provedl většinu terénních šetření
samostatně. L. Růžičková se k terénnímu výzkumu připojila až v posledním roce. Provedl
jsem statistické zpracování výsledků a připravil text publikace.
Hlavní přínos práce: Z umělých netopýřích úkrytů byli opakovaně odstraňováni úkrytoví
paraziti. V letech, kdy byly úkryty infestovány vysokými populačními hustotami štěnic,
netopýři se v nich nerozmnožovali. Naopak v letech, kdy došlo k odstranění štěnic,
k porodům mláďat zde opakovaně došlo. Též bylo zjištěno, že štěnice kolonizují nové úkryty
hostitele poměrně rychle již v období jeho gravidity.
(6) BARTONIČKA T., 2008: Cimex pipistrelli (Heteroptera, Cimicidae) and the dispersal
propensity of bats: an experimental study. Parasitology Research, 104:163–168.
46
Jsem jediným autorem celého výzkumu.
Hlavní přínos práce: V kontrolovaných podmínkách voliéry jsem sledoval reakce netopýrů
na vysoké abundance štěnic v jejich úkrytech. Jednoduchý experiment ukázal, že netopýři
zvyšují grooming při vysokých denzitách štěnic, a pokud se nejsou schopni štěnic zbavit,
opouští takový úkryt záhy po probuzení z denního torporu. Přítomnost štěnic v úkrytu vede
k předčasnému opouštění úkrytu a tak změnám v úkrytovém chování hostitele.
(7) BARTONIČKA T. & RŮŽIČKOVÁ L., 2012: Bat bugs (Cimex pipistrelli) and their
impact on non-dwelling bats. Parasitology Research, 111:1233–1238.
Jsem autorem myšlenky i designu. L. Růžičková (moje diplomantka) se podílela zásadní
měrou na sběru dat v terénu. Společně jsme data vyhodnotili. Jsem autorem textu článku.
Hlavní přínos práce: Předchozí naše studie ukázala, že netopýři dočasným opuštěním úkrytu
mohou redukovat masivní gradaci štěnic ve štěrbinových úkrytech, proto jsme chtěli ověřit
podobnou strategii u netopýrů tradičně osidlujících pouze jediný, ale prostorný úkryt.
Sledovali jsme úkryt s vysokou abundancí štěnic. Zjistili jsme, že vysoce gravidní samice se
těsně před porody přesunou do předtím neobsazené části úkrytu, kde štěnice doposud nebyly.
Současně na opakovaně osidlovaném místě úkrytu poklesne abundance raných instarů štěnic,
které nemají dostatek potravy. Tímto způsobem mohou i netopýři osidlující dlouhodobě
rozsáhlé půdní prostory efektivně redukovat abundanci úkrytových parazitů jako jsou štěnice.
(8) WAWROCKA K. & BARTONIČKA T., 2013: Two different lineages of bedbug (Cimex
lectularius) reflected in host specificity. Parasitology Research, 112: 3897-904.
Jsem autorem myšlenky výzkumu a jeho designu. K. Wawrocka (moje doktorandka) odvedla
většinu práce v laboratoři. Společně s doktorandkou jsme získaná data vyhodnotili a oba jsme
se stejnou měrou podíleli na textu článku.
Hlavní přínos práce: V předchozích studiích bylo zjištěno, že se ve střední Evropě vyskytují
dvě hostitelské linie štěnice Cimex lectularius. Jedna parazituje převážně na člověku a druhá
na netopýrech. Laboratorní experimenty v chovech štěnic ukázaly na snížené přežívání skupin
47
krmených krví nespecifického hostitele. Výrazný rozdíl byl zjištěn především u linie
parazitující na člověku, kdy tyto populace nebyly schopny přežívat na netopýrech. Naopak
štěnice z netopýrů krmené lidskou krví měly dostatečně vysoké přežívání na udržení
populace. Toto zjištění má zásadní význam pro hodnocení netopýrů jako vektorů štěnic do
lidských sídel, zejména v souvislosti se současnou expanzí štěnic u člověka.
48
49
8. Seznam publikovaných vědeckým prací k tématu habilitační práce
8.1 Využívání a střídání úkrytů u netopýrů
(1) BARTONIČKA T. & ŘEHÁK Z., 2007: Influence of the microclimate of
bat boxes on their occupation by the soprano pipistrelle Pipistrellus
pygmaeus: possible cause of roost switching. Acta Chiropterologica, 9(2):
517–526. (IF=0,831)
(2) BARTONIČKA T., BIELIK A. & ŘEHÁK Z., 2008: Roost switching and
activity patterns in the soprano pipistrelle, Pipistrellus pygmaeus, during
lactation. Annales Zoologici Fennici 45(6):503-512. (IF=1,03)
8.2 Životní cyklus štěnic a přežívání v úkrytech netopýrů
(3) BARTONIČKA T. & GAISLER J., 2007: Seasonal dynamics in the
numbers of parasitic bugs (Heteroptera, Cimicidae): a possible cause of
roost switching in bats (Chiroptera, Vespertilionidae). Parasitology
Research, 100:1323–1330. (IF=2,327)
(4) BARTONIČKA T., 2010: Survival rate of bat bugs (Cimex pipistrelli,
Heteroptera) under different microclimatic conditions. Parasitology
Research, 107:827–833. (IF=2,327)
(5) BARTONIČKA T. & RŮŽIČKOVÁ L., 2013: Recolonization of bat
roost by bat bugs (Cimex pipistrelli): could parasite load be a cause of bat
roost switching? Parasitology Research, 112:1615–1622. (IF=2,327)
8.3 Vliv štěnic na chování netopýrů
(6) BARTONIČKA T., 2008: Cimex pipistrelli (Heteroptera, Cimicidae) and
the dispersal propensity of bats: an experimental study. Parasitology
Research, 104:163–168. (IF=2,327)
(7) BARTONIČKA T. & RŮŽIČKOVÁ L., 2012: Bat bugs (Cimex
pipistrelli) and their impact on non-dwelling bats. Parasitology Research,
111:1233–1238. (IF=2,327)
8.4 Hostitelská specifita štěnic
(8) WAWROCKA K. & BARTONIČKA T., 2013: Two different lineages of
bedbug (Cimex lectularius) reflected in host specificity. Parasitology
Research, 112: 3897-904. (IF=2,327)
8.1 Využívání a střídání úkrytů u netopýrů
BARTONIČKA T. & ŘEHÁK Z., 2007
Influence of the microclimate of bat boxes on their occupation by the soprano pipistrelle
Pipistrellus pygmaeus: possible cause of roost switching.
Acta Chiropterologica, 9(2): 517–526.
INTRODUCTION
Roost fidelity is low in many species, especially
among tree-dwelling bats (Lewis,
1995). Field observations (Lausen and Barclay,
2002; Mazurek, 2004; Rancourt et al.,
2005) suggest that species of bats dwelling
in holes and crevices switch their roosts
several times during a season, even every
few days. This behaviour was observed
mainly in species roosting in tree hollows
(Barclay and Brigham 2001; Kerth et al.,
2001; Willis and Brigham, 2004). However,
several studies suggest that roost switching
was registered even in Pipistrellus pipistrellus
s.l., usually roosting in buildings
(e.g., Thompson, 1992; Park et al., 1996).
Thompson (1990) or Feyerabend and Simon
(2000) found large numbers of roosts exploited
by one colony of pipistrelles. Small
groups of female pipistrelles often leave
their respective roosts and move into a main
nursery roost a few days prior to parturition,
probably to reduce costs associated with
thermoregulation (Swift, 1980; Webb et al.,
1996; authors’ personal observations).
Recent studies show that females of species
using tree cavities are not restricted to
individual trees and one colony may be
spread among multiple trees on a given
night, conforming with a fission-fusion
model (Kerth and König, 1999; Willis and
Brigham, 2004). The motivation underlying
roost switching and reasons why groups
Acta Chiropterologica, 9(2): 517–526, 2007
PL ISSN 1508-1109 © Museum and Institute of Zoology PAS
Influence of the microclimate of bat boxes on their occupation by
the soprano pipistrelle Pipistrellus pygmaeus: possible cause of
roost switching
TOMÁŠ BARTONIÈKA1, 2 and ZDENÌK ØEHÁK1
1Department of Zoology and Ecology, Masaryk University, Kotláøská 2, 611 37 Brno, Czech Republic
2
Corresponding author: E-mail: bartonic@sci.muni.cz
Between April and October 2003–2004, the changes in occupation of three bat boxes used by Pipistrellus
pygmaeus were studied using a passive IR monitors and data loggers. Bat boxes were situated in a floodplain
forest in south-eastern Moravia. Generalized additive models indicated that internal humidity described better
the fluctuation in bat numbers during pregnancy and lactation than did changes in the internal temperature.
Three variables (internal humidity, external temperature, and number of bats) described 87% of the variability
in internal roost temperature, while the number of bats described only 29% of the variability. A negative
correlation was found between the internal temperature and the number of bats roosting in a bat box the next
day during pregnancy and lactation. The number of bats was also positively correlated with the internal
humidity. The internal temperature of a roost with bats was biased by temperature strategies induced by the bats
during particular reproductive periods. Mean temperature of occupied bat boxes was higher during pregnancy
than during lactation. Females were able to go into torpor even during lactation period.
Key words: Pipistrellus pygmaeus, roost changing, microclimate, bat boxes
disperse among several roosts is not well
understood (Lewis, 1995; Vonhof and Barclay,
1996). This social structure may help
maintain a number of potential benefits
linked to living in a large colony. Roost
switching might force social relationships
among the small ‘subgroups’ that comprise
a larger group. However, dispersion of
colonies among tree cavities and bat boxes
may result from a complex of different constraints.
Roost switching and dispersion
may reflect differences in group size between
bats forming large colonies in caves
and buildings and those roosting in smaller
colonies in trees, perhaps due to thermal
differences or to competition for space
when the number of individuals is increasing
and one cavity is too small (Whitaker,
1998; Lefebvre et al., 2003). Roost switching
could be a good mechanism by which
bats select roost site with optimal microclimatic
conditions (Kerth et al., 2001; Lourenço
and Palmeirim, 2004). Bats may
know alternative roosts including their microclimate
in advance, since the search for
a new roost might be costly in terms of energy
output (Lewis, 1995). Benefits associated
with roost switching could also be positively
correlated with decreasing the mortality
of juveniles due to the impact of parasites
(Wolz, 1986; Lewis, 1996).
We attempted to answer the following
questions. (i) Are differences in microclimatic
parameters among bat boxes dependent
on particular parts of the reproductive
season? (ii) Do reproductive requirements
influence roost switching or roost sharing
behaviour? (iii) Can internal temperature or
other microclimatic parameters be used to
predict the presence of bats in a roost?
MATERIALS AND METHODS
Study Area and Data Collection
The changes in microclimate and occupancy
of bat boxes used by P. pygmaeus were studied in
a floodplain forest in south-eastern Moravia (Czech
Republic). The study was performed between April
and October of 2003 and 2004. Three wooden bat
boxes were studied, two of them were placed in trees
situated within the forest and its edge, the third was
placed on a hide at a forest edge. Altogether four boxes
were installed in the study area, but only three of
them were occupied periodically. The reproductive
season under study was divided into three periods:
pregnancy (until 7th June), lactation (8th June till 7th
July, 30 days after first parturition observed) and postlactation
(after 8th July — cf. Bartonièka and Zukal
2003). The time of first parturition was assessed in
a nearby (14 km) nursery colony of P. pygmaeus in
a building at Vranovice (T. Bartonièka et al., unpublished
data). There, the bats were captured, examined
and released. We also netted bats emerging from all
boxes during the years 2001 and 2002, but never captured
males. Therefore we suppose the absence of
adult males during the study in 2003 and 2004. All
captures were performed under the licence No.
922/93-OOP/2884/93 of the Ministry of Environment
of the Czech Republic. The authors have also been
authorized to handle free-living bats according to the
certificate of competency No 104/2002-V4 (§ 17 of
the law No. 246/ 1992).
Technical Equipment
The changes in bat activity with respect to the
boxes were monitored continually by passive IR Trail
Monitors, TM (TM550, TrailMaster, Goodson & Associates,
INC., USA — used by Thomas et al., 1995)
and active IR gate (Berková and Zukal, 2004). The IR
gate consisted of 2 infrared light emitters (diodes) and
two receivers (phototransistors). This technique allows
discrimination between those bats leaving and
those entering the bat box. With the event delay set to
0.1 minutes the TM record 10 events in a single
minute. Battery life of both types of recording systems
was usually two weeks or more. One bat box
was equipped by IR gate and two boxes by TM. The
TMs were situated in front of the entrance (see Fig. 1)
and the IR gate in the entrance of each bat box. Hobo
Data Loggers (Onset Computer Corporation, USA),
continuously recording the temperature (internal and
external) and the internal humidity, were situated under
the roof of each bat box. The sensors measuring
external temperature were situated about 50 cm apart
from each box. The relative humidity sensor had
an accuracy of ± 4% and the temperature sensor
± 0.4°C. The bats flying out and in were also monitored
using a digital video recorder HD-2166 and
AVC-720 connected with IR diode cameras B/WAVC
307R.
518 T. Bartonièka and Z. Øehák
Statistical Analysis
All variables showed a normal distribution after
log transformation. Statistica for Windows 7.0 was
used for data analyses (ANOVA, t-tests, correlations).
The level of activity (from TM) in morning hours
(1 to 5 a.m.) positively correlated with the number of
bats which rested in the box during the same day from
IR gate (Pearson’s correlation coefficient, r = 0.61,
P < 0.05). Therefore we chose medians of activity
from TM only from this period and pooled them with
data from IR gate to analyse impact of microclimatic
parameters and changes in bat numbers among bat
boxes. Generalised additive models (GAMs) were fitted
using the R-Gui 2.0.1 software package. Functions
for continuous variables were fitted using cubic
smoothing splines, initially with four degrees of freedom.
At the completion of the selection process the
function for each selected continuous variable was reduced
if this did not result in a significant (P < 0.05)
Influence of the microclimate of bat boxes on Pipistrellus pygmaeus 519
reduction in goodness-of-fit. These models assume
that the mean of the dependent variable depends on
an additive predictor through a nonlinear link function.
Generalized additive models permit the response
probability distribution to be any member of the exponential
family of distributions (Hastie and Tibshirani,
1990). Hourly values of microclimatic parameters
correlated positively (P < 0.05) with their means
during the light part of a day (sunrise to sunset)
(internal temperature, r = 0.53; external temperature,
r = 0.69; humidity, r = 0.85; in all cases the number
of ligh parts of day n1 = 330 and the number of hourly
values n2 = 1771). Therefore the model was fitted by
means of microclimatic parameters from the light
part of a day and the numbers of bats using a particular
bat box as their day roost. This step removed the
effect of shifts in temperature and other parameters
during the respective day from sunrise until sunset.
Materials
We monitored activity at the three bat boxes occupied
by P. pygmaeus for 111, 105 and 115 days, respectively.
Hourly values were available on internal
and external temperatures, and internal humidity. For
each day, the number of roosting bats was counted
resting in the box via passive TM and/or active IR
gate.
RESULTS
Insulating Properties of Bat Boxes
We found that the internal and external
temperature neared equilibrium within five
hours (median) after all bats left the particular
bat box (max. 8 hrs, min. 3 hrs). Although
each of the bat boxes under study
differed in exposure, no significant difference
among the boxes was found in the
time needed to balance the level of internal
and external temperatures (ANOVA,
F2, 19 = 0.69, P >> 0.05). When the bats
moved to another roost the next day, they
left the respective box soon after sunset
without returning to it during the night.
Therefore, the five-hour period, after
emerging, allowed us to exclude nightly
observations i.e., data obtained between
sunset and sunrise from further statistical
analyses.
FIG. 1. Wooden bat box. Monochrome (B/W) IR
diode camera monitored the entrance of the box and
was connected to a battery and digital recorder on the
ground. Two grey shapes mark out a space monitored
by passive IR Trail Master monitor (TM550) on
a bracket in front of the bat box. Internal temperature
was measured with help of Hobo Data Loggers
(Onset Computer Corporation) (inside box). Sensor
measuring external temperature was placed outside
roughly half a meter from the bat box
Impact of Internal Temperature and
Humidity
Factors with possible impact on changes
in internal temperature were only studied
during the periods of pregnancy and lactation.
The post-lactation period was omitted
because of great fluctuations in numbers of
roosting bats due to the weaning of young.
The following independent variables were
used in the GAM models: external temperature
(tex), internal humidity (hum), reproductive
stage [i.e., pregnancy versus lactation
(sez)], exposure of bat box (box), and
the number of bats roosting in the box during
next the day [ind]. Normal distribution
and link function identity was considered of
the dependent variable, which was internal
temperature (tin). The dependence of internal
temperature was defined as the function
of (tin) ≈ s(hum) + s(tex) + s(ind) + (sez) +
(box), where s is a specific smoothing
spline fit in a GAM. The interactions among
variables were found to be insignificant and
did not increase the proportion of variability
within the sample. The impact of each of
the first three independent variables on the
dependent variable was significant (humidity,
χ2
= 16.08, P < 0.01; external temperature,
χ2
= 26.11, P < 0.001; individuals,
χ2
= 8.45, P < 0.05; in all cases n = 27). Together
they described 87.1% of variability
of the internal temperature. The impact of
reproductive stage and exposure of bat box
was insignificant (t-test, t = 4.21 and t =
5.23, respectively; in both cases P > 0.05
and n = 27). There was an almost linear dependence
between the values of internal and
external temperature (Fig. 2). Internal temperature
also increased with internal humidity
(Fig. 2). The number of bats in the box
explained only 29% of the residual variability
of internal temperature (holding constant
external temperature and internal humidity).
Nevertheless, we found a negative correlation
between the internal temperature and
520 T. Bartonièka and Z. Øehák
FIG. 2. Graphic output of a generalised additive model for the internal temperature. Both graphs depict the
predicted probability of the external temperature (a) and internal humidity (b) holding other predictors constant.
95% confidence limits for the function are also shown as grey zone. Linear dependence between residuals of
internal temperature from GAM and external temperature was found. Internal temperature as factor in GAM
also increased with internal humidity. Degrees of freedom are in brackets in label of y-axes
Humidity (%)
Residuals[1]Residuals[3.08]
14 16 18 20 22 24
40 50 60 70 80 90 100
5
0
-5
5
0
-5
External temperature (°C)
the number of bats roosting in the box the
next day (Fig. 3). The highest median of the
number of roosting bats (75 individuals)
was found during pregnancy, i.e. at the time
when females form nursery colonies. The
size of roosting groups was very low during
the lactation and post-lactation periods.
Cross-correlations were also tested, but the
variability of internal temperature was better
described by correlations with individual
variables than with their combinations.
The dependence of internal humidity on
the number of roosting bats was again tested
by GAM [only pregnacy and lactation
periods, hum ≈ s(ind) + s(tex) + s(tin)
+ (box)]. It was found that changes in internal
humidity correlate with the number
of bats much better than do the changes in
internal temperature until 7th July (χ2
=
76.82, d.f. = 607, P < 0.001, Poisson distribution,
link function: log — Fig. 4). The
impact of bat box exposure was insignificant
again (t = 6.16, P > 0.05). The number
of bats described 52.6% of the variability of
internal humidity (holding constant external
Influence of the microclimate of bat boxes on Pipistrellus pygmaeus 521
FIG. 3. Graphic output of a generalised additive model
for the number of bats in bat boxes, holding all
other predictors (external temperature, humidity,
localization of bat boxes, seasonal aspect) constant
at their mean value. 95% confidence limits for the
function are also shown as grey zone. Degrees of
freedom are in brackets in label of y-axis
Number of individuals
and internal temperature). The correlation
found between the number of bats and humidity
in bat boxes was positive (Pearson’s
correlation coefficient, r = 0.40, n = 330,
P < 0.05). There was no correlation between
rainy days and presence or absence
of bats in bat boxes (r = 0.03, n = 330,
P >> 0.05).
Changes in Microclimatic Parameters
during The Season
Intraseasonal differences in microclimatic
parameters (internal, external temperature,
humidity) were evaluated with respect
to the reproductive periods. We chose
only days with the presence of bats.
ANOVA showed significant differences in
microclimatic parameters among the periods
(pregnancy, lactation, post-lactation —
F2, 81 = 2.08, P < 0.05). As shown by
a t-test, the differences arose entirely from
the fluctuation in internal temperature on
days when bats were present during the periods
of pregnancy and lactation (t = 2.20,
n1 = 11 and n2 = 13, P < 0.05). Concerning
the internal temperature, it was slightly
higher during pregnancy than during lactation
(Fig. 5). But the fact that external temperature
was significantly higher in lactation
than in pregnancy (t = -3.81, n1 = 11
and n2 = 13, P < 0.001) excludes its direct
dependence on internal temperature. This
indicates that different internal temperature
could reflect differences in thermoregulatory
strategies between pregnant and lactating
females rather than different external temperature.
To verify this result, we analysed
the same microclimatic parameters on the
days when bats were absent from the boxes.
In such cases, insignificant differences were
found among periods of the reproductive
season (pregnancy, lactation, post-lactation)
(ANOVA, F2, 249 = 0.49, P >> 0.05). Differences
in internal temperatures between boxes
occupied and not occupied by bats were
insignificant during both pregnancy (t-test,
5
0
-5
-10
Residuals[1.99]
0 50 100 150
t = 0.49, n1 = 15 and n2 = 13, P > 0.05) and
lactation (t = 0.34, n1 = 8 and n2 = 19, P >
0.05).
During the pregnancy period, the mean
humidity (71.7 ± 19.4%) was higher than
during lactation (55.1 ± 11.8%). During
the lactation period, humidity was significantly
higher in occupied than in not occupied
boxes (t-test, t = 3.49, n1 = 8 and
n2 = 19, P < 0.05), but insignificant differences
were found during pregnancy
(t = 0.58, n1 = 15 and n2 = 13, P >> 0.05).
Comparison of Microclimatic Parameters
and Bat Numbers among Bat Boxes
Analysis of variance showed significant
differences in microclimatic parameters and
numbers of bats among particular bat boxes
(ANOVA, F2, 330 = 159.63, P < 0.001). Students
t-tests were used to investigate the
impact of individual parameters. Significant
differences (in all cases n = 330) were
found concerning external temperature
(t = 2.10, P < 0.05), humidity (t = -6.25,
522 T. Bartonièka and Z. Øehák
FIG. 4. Changes in internal humidity and number of bats. Pointers show days with daily sum of the precipitations
higher than 2 mm. Numbers above pointers are precipitation values in mm. Progress in internal humidity along
with bats occurence is noticeable during the pregnancy and lactation periods (until 7th July)
FIG. 5. Differences in external and internal temperatures
found between pregnancy and lactation period.
Internal temperature, when bats are present, was
significantly higher during pregnancy than during
lactation. Mean — central tendency, SD — large box,
and min–max range as ‘whiskers’
Date
Humidity(%)
Individuals
P < 0.001) and number of bats (t = -8.60,
P < 0.001); no difference was revealed in
internal temperature (t = -0.45, P >> 0.05).
Throughout the season, the numbers of
bats roosting in the boxes differed significantly
(ANOVA, F2, 330 = 20.45, P < 0.001).
However, insignificant differences were revealed
by the paired test used to compare
Temperature(°C)
Lactation Pregnancy
the number of bats in a box the day before
the bats had left it, with the numbers of bats
in the remaining two boxes the following
day (Friedman ANOVA, χ2 = 5.57, n = 14,
P > 0.05). During the lactation period, the
largest number of bats was observed in the
box showing highest internal temperature
(20.5 versus 18.3 and 18.4°C; ANOVA,
F2, 27 = 8.76, P < 0.001).
DISCUSSION
Changes in Microclimatic Parameters over
The Season
Bats of temperate zones, when reproducing,
may have strict thermoregulatory requirements
on their shelters because low
roost temperatures induce torpor, which can
delay the development of embryos and offspring
(Racey and Swift, 1981; Kunz, 1982;
Wilde et al., 1995). For heterothermic bats
living under conditions of cool climate,
warm roosts are very important and allow
them to extend their natural range (Kunz,
1982). Lactating females may sometimes
choose warmer roosts to avoid torpor,
whereas pregnant females sometimes
choose cooler roosts to decrease their thermoregulatory
costs (Lewis, 1996; Kerth et
al., 2001). In contrast to the actual opinion,
we found that the internal temperature of
bat boxes with animals inside was higher
during pregnancy than during the lactation
period. In our study area, females were able
to become torpid also during lactation, not
only during pregnancy. Our observations
come from similar (even lower) altitude
(170 m a.s.l.) in central Europe as the
study areas of authors who offered similar
results (e.g., Kerth et al., 2001; Heise
2005), therefore they are fully comparable.
Heise (2005) found lactating females of
P. pygmaeus to be able to go into torpor,
frequently in periods with low temperatures.
The negative correlation between low
internal temperature and presence of a large
number of bats could also be the consequence
of their flying off when the bat box
was overheated. It seems that high internal
temperature is the factor restricting occupation
of roosts during pregnancy and lactation
periods (Weigold, 1973). We cannot assume
that box overheating is a possible risk,
because the test of internal temperature between
occupied and non-occupied boxes
was insignificant. We found empty boxes
when internal temperature reached above
40°C at all times (cf. Kerth et al., 2001;
Lourenço and Palmeirim, 2004). Box overheating
may not be so dangerous if a sufficient
supply of alternative roosts, mainly
tree cavities, are available in the vicinity.
Awareness of natural and/or artificial roosts
facilitates the maintenance of thermal comfort
due to roost switching which, at the
same time, strengthens the social relation-
ships.
Keeping other predictors constant, presence
of bats in bat boxes significantly influenced
internal temperature and humidity
even despite of high variability of microclimatic
conditions throughout pregnancy and
lactation periods. The comparison of internal
temperatures in the days when boxes
were and were not occupied shows differences
in bat thermopreferences during the
season. This fact complicates the use of
internal temperature as an indicator of bat
presence in the roost. Despite our expectation,
internal humidity indicated much better
the presence of bats, especially when
large numbers of bats were present in a box.
Internal humidity positively correlated with
the number of bats due to their respiration.
Changes in The Occurrence of Bats
Previous studies have shown that a colony
of bats can occupy a complex of tree
cavities in one area (e.g., O’Donnell and
Sedgeley, 1999; Cryan et al., 2001). Many
Influence of the microclimate of bat boxes on Pipistrellus pygmaeus 523
524 T. Bartonièka and Z. Øehák
of the arguments about roost switching in
tree dwelling bats are based on predator
avoidance, impact of parasites (Wolz, 1986)
or finding large numbers of short-lived
roosts (Barclay and Brigham, 2001), but
also on microclimatic conditions (Kerth et
al., 2001).
The data obtained from infrared activity
readers show the highest median numbers
of bats in boxes during pregnancy, while
they were usually lower during the lactation
and post-lactation periods. After weaning
the numbers of bats fluctuated considerably.
The boxes can be used by weaned young either
as temporary night roosts or as shelters
for several days, due to the increased competition
for warmer roosts (Entwistle et al.,
1997). At that time, bat boxes were occupied
by only few non-reproducing adults
during most of the days.
Concerning P. pygmaeus, this could be
confirmed by records of its high flight activity
in close vicinity of a big shelter
throughout the season, although the bats did
not use the shelter at every recording (Bartonièka
and Øehák, 2004). Among European
bats, the fission-fusion model was
shown by M. bechsteinii groups (Kerth and
König, 1999), but this may not apply to
other tree dwelling species (Willis et al.,
2003). We found small fluctuations in the
numbers of bats in particular bat boxes during
pregnancy. In the same period, Willis
and Brigham (2004) found a higher roostsharing
index for female Eptesicus fuscus.
High metabolic activity dependent on high
internal temperature positively influences
embryo development speed (Racey and
Swift, 1981). On the other hand, reproductive
stage and information exchange can enhance
the sharing of a low number of cooler
roosts by females facilitating their torpor
during early pregnancy (Kerth and König,
1999).
Numbers of females in colonies determine
an effectivity of thermoregulation and
affect the level of roost switching (Haddow,
1993; Barlow and Jones, 1999). In the
Czech Republic, lower mean numbers of female
P. pygmaeus in buildings were found
(65 individuals, authors’ personal observations)
than in Britain (200 individuals —
Barlow and Jones, 1999). The size of colonies
roosting in natural roosts is even lower
than in buildings. Therefore smaller colonies
roosting partly in hollows may switch
roosts more often due to difficult thermoregulation
than larger colonies roosting in
stone buildings e.g. in Scotland (Haddow,
1993).
Positive impacts of thermally different
roosts can have important implications for
the management of bat populations via their
shelters in forests. Not only must large numbers
of natural hollows be maintained, but
enough bat boxes also have to be recruited.
On the other hand, bat boxes alone can be
insufficient for successful reproduction of
bats in monoculture forests with little or no
natural cavities of adequate space. Our data
are consistent with the theory of Willis and
Brigham (2004). Bats roosting in caves or
big spaces in buildings are in a situation
different from tree-roosting bats because
the shelters fulfill their microclimatic requirements.
Tree-roosting bats are dependent
on shelters with different microclimate
and must often switch among several cavities
or boxes. Pipistrelles (both P. pipistrellus
and P. pygmaeus) are classified as hemisynanthropic
species, the nursery colonies
of which usually roost in buildings. But
concerning P. pygmaeus, it seems that the
roosts in buildings do not provide them with
microclimatic conditions suitable for the
whole reproduction season. They therefore
choose the strategy of roost-switching, typical
of forest-roosting bats.
ACKNOWLEDGEMENTS
We are very grateful to J. Gaisler, R. Obrtel
and anonymous reviewers for valuable comments on
the manuscript. V. Hanák and H. Jahelková are heartily
acknowledged for their unpublished data of
colonies and D. Motl for his effort in the development
of the IR gate. M. Koneèná provided excellent assistance
in the field. The study was supported by the
grants of Grant Agency of the Czech Republic No.
206/02/0961, 206/06/0954 and the grant of Ministry
of Education, Young and Sports of the Czech Republic
No. MSM0021622416.
REFERENCES
BARCLAY, R. M. R., and R. M. BRIGHAM. 2001.
Year-to-year reuse of tree-roosts by California
bats (Myotis californicus) in southern British
Columbia. American Midland Naturalist, 146:
80–85.
BARTONIÈKA, T., and Z. ØEHÁK. 2004. Flight activity
and habitat use of Pipistrellus pygmaeus in
a floodplain forest. Mammalia, 68: 365–375.
BARTONIÈKA, T., and J. ZUKAL. 2003. Flight activity
and habitat use of four bat species in a small town
revealed by bat detectors. Folia Zoologica, 52:
155–166.
BERKOVÁ, H., and J. ZUKAL. 2004. Seasonal changes
in flight activity of bats at the entrance of the
Kateøinská cave revealed by an automatic monitoring
system. Vespertilio, 8: 45–54. [In Czech
with English summary].
CRYAN, P. M., M. A. BOGAN, and G. M. YANEGA.
2001. Roosting habitats of four bat species in the
Black Hills of South Dakota. Acta Chiropterologica,
3: 43–52.
ENTWISTLE, A. C., P. A. RACEY, and J. R. SPEAKMAN.
1997. Roost selection by the brown long-eared
bat Plecotus auritus. Journal of Applied Ecology,
34: 754–763.
FEYERABEND, F., and M. SIMON. 2000. Use of roosts
and roost switching in a summer colony of 45
kHz phonic type pipistrelle bats (Pipistrellus pipistrellus
Schreber,1774). Myotis, 38: 51–59.
HADDOW, J. F. 1993. Pipistrelle roosts in Central Region.
Scottish Bats, 2: 18–23.
HASTIE, T. J., and R. J. TIBSHIRANI. 1990. Generalized
additive models. Monographs on Statistics and
Applied Probability, 43. Chapman and Hall, Lon-
don.
HEISE, G. 2005. Zur Tageslethargie gravider und laktierender
Fledermausweibchen. Nyctalus, 10:
37–40.
KERTH, G., and B. KÖNIG. 1999. Fission, fusion
and non random associations in female Bechstein’s
bats (Myotis bechsteinii). Behaviour, 136:
1187–1202.
KERTH, G., K. WEISSMANN, and B. KÖNIG. 2001. Day
roost selection in female Bechstein’s bats (Myotis
bechsteinii): a field experiment to determine the
influence of roost temperature. Oecologia, 126:
1–9.
KUNZ, T. H. (ed.). 1982. Ecology of bats. Plenum
Press, New York, 425 pp.
LAUSEN, C. L., and R. M. R. BARCLAY. 2002. Roosting
behaviour and roost selection of female big
brown bats (Eptesicus fuscus) roosting in rock
crevices in southeastern Alberta. Canadian Journal
of Zoology, 80: 1069–1076.
LEFEBVRE, D., N. MENARD, and J. S. PIERE. 2003.
Modelling the influence of demographic parameters
on group structure in social species with dispersal
asymmetry and group fission. Behavioral
Ecology and Sociobiology, 53: 402–410.
LEWIS, S. E. 1995. Roost fidelity of bats: a review.
Journal of Mammalogy, 76: 481–496.
LEWIS, S. E. 1996. Low roost-site fidelity in pallid
bats: associated factors and effect on group stability.
Behavioral Ecology and Sociobiology, 39:
335–344.
LOURENÇO, S. I., and J. M. PALMEIRIM. 2004: Influence
of temperature in roost selection by Pipistrellus
pygmaeus (Chiroptera): relevance for the
design of bat boxes. Biological Conservation,
119: 237–243.
MAZUREK, M. J. 2004. A maternity roost of Towsend’s
big-eared bats (Corynorhinus towsendii) in coast
redwood basal hollows in northwestern California.
Northwestern Naturalist, 85: 60–62.
O’DONNELL, C. F. J., and J. A. SEDGELEY. 1999. Use
of roosts in the long-tailed bat, Chalinobolus tuberculatus,
in temperate rainforest in New
Zealand. Journal of Mammalogy, 80: 913–923.
PARK, K. J., J. D. ALTRINGHAM, and G. JONES. 1996.
Assortative roosting in the two phonic of Pipistrellus
pipistrellus during the mating season.
Proceedings of the Royal Society of London,
263B: 1495–1499.
RACEY, P. A., and S. M. SWIFT. 1981. Variation
in gestation length in a colony of pipistrelle
bats (Pipistrellus pipistrellus) from year to
year. Journal of Reproduction and Fertility, 61:
123–129.
RANCOURT, S. J., M. I. RULE, and M. A. O’CONNELL.
2005. Maternity roost site selection of long-eared
Myotis, Myotis evotis. Journal of Mammalogy,
86: 77–84.
SWIFT, S. M. 1980. Activity patterns of pipistrelle bats
(Pipistrellus pipistrellus) in north-east Scotland.
Journal of Zoology (London), 190: 285–295.
THOMAS, D. W. 1995. Hibernating bats are sensitive
to nontactile human disturbance. Journal of Mammalogy,
76: 940–946.
Influence of the microclimate of bat boxes on Pipistrellus pygmaeus 525
THOMPSON, M. J. A. 1990. The pipistrelle bat
Pipistrellus pipistrellus Schreber on the Vale of
York. Naturalist, 115: 41–56.
THOMPSON, M. J. A. 1992. Roost philopatry in female
pipistrelle bats Pipistrellus pipistrellus Journal of
Zoology (London), 228: 673–679.
VONHOF, M. J., and R. M. R. BARCLAY. 1996. Roostsite
selection and roosting ecology of forest-dweling
bats in southern British Columbia. Canadian
Journal of Zoology, 74: 1797–1805.
WEBB, P. I., J. R. SPEAKMAN, and P. A. RACEY. 1996.
Population dynamics of a maternity colony of the
pipistrelle bats (Pipistrellus pipistrellus) in northeast
Scotland. Journal of Zoology (London), 240:
777–780.
WEIGOLD, H. 1973. Jugendentwicklung der Temperaturregulation
bei der Mausohrfledermaus, Myotis
myotis (Borkhausen, 1797). Journal of Comparative
Physiology, 85: 169–212.
WHITAKER, J. O., JR. 1998. Life history and roost
switching in six summer colonies of eastern
pipistrelles in buildings. Journal of Mammalogy,
79: 651–659.
WILDE, C. J., M. A. KERR, C. H. KNIGHT, and P. A.
RACEY. 1995. Lactation in vespertilionid bats.
Symposium of the Zoological Society of London,
67: 139–149.
WILLIS, C. K. R., and R. M. BRIGHAM. 2004. Roost
switching, roost sharing and social cohesion:
forest-dwelling big brown bats, Eptesicus fuscus,
conform to the fission-fusion model. Animal Behaviour,
68: 495–503.
WILLIS, C. K. R., K. A. KOLAR, A. L. KARST, M. C.
KALCOUNIS-RUEPELL, and R. M. BRIGHAM. 2003.
Medium- and long-term reuse of trembling aspen
cavities as roosts by big brown bats (Eptesicus
fuscus). Acta Chiropterologica, 5: 85–90.
WOLZ, I. 1986. Wochenstuben-Quartierewechsel bei
der Bechsteinfledermaus. Zeitschrift für Säugetierkunde,
51: 65–74.
526 T. Bartonièka and Z. Øehák
Received 25 September 2006, accepted 23 June 2007
BARTONIČKA T., BIELIK A. & ŘEHÁK Z., 2008
Roost switching and activity patterns in the soprano pipistrelle, Pipistrellus pygmaeus, during
lactation.
Annales Zoologici Fennici 45(6):503-512.
Ann. Zool. Fennici 45: 503–512 ISSN 0003-455X (print), ISSN 1797-2450 (online)
Helsinki 30 December 2008 © Finnish Zoological and Botanical Publishing Board 2008
Roost switching and activity patterns in the soprano
pipistrelle, Pipistrellus pygmaeus, during lactation
Department of Botany and Zoology, Masaryk University, 2, CZ-611 37 Brno, Czech
Republic (*corresponding author’s e-mail: bartonic@sci.muni.cz)
Received 2 Apr. 2007, revised version received 21 Feb. 2007, accepted 22 Feb. 2007
2008: Roost switching and activity patterns in the soprano
pipistrelle, Pipistrellus pygmaeus, during lactation. — Ann. Zool. Fennici 45: 503–512.
We studied roost switching and habitat selection of 16 P. pygmaeus females tagged
The highest foraging activity was observed over water bodies, at forest edges and
near street lamps. During each night, each female visited at least one night-roost, and
times per night. After parturition, the distances between night roosts and day roosts
increased. The number of night roosts used declined as pups neared weaning. Five
young in new roosts a conclusion was reached that some females transported their
offspring to new roosts at night. After lactation began, some females visited roosts
occupied by vocalizing males of P. pygmaeus and P. nathusii.
Introduction
Differences in peak frequency of echolocation
reproductive isolation and segment differences in
the cytochrome b gene (Barratt et al.
the main reasons for distinguishing between the
two species of common pipistrelle bats, Pipistrellus
pipistrellus and Pipistrellus pygmaeus.
Although the discovery of the systematic status
of the newly validated species Pipistrellus pygmaeus
was interesting, little is known about its
ecology, in particular its activity patterns and
habitat use. Pipistrellus pipistrellus can forage in
Warren et al. 2000, Gaisler et al. 2002, Davidof
prey of P. pygmaeus suggests that it is more
P. pygmaeus
spends a considerable percentage of its foraging
time over water. Furthermore, Russo and
important for P. pygmaeus in the Mediterranean
suggest that Pipistrellus pygmaeus selects seminatural
woodland and tree lines more often than
water habitats.
Females of P. pipistrellus sensu lato often
switch roosts during the season (Thompson 1990,
temporary and cooler roosts, moving to one main
parturition roost a few days before parturition
et al.
Scotland, large nursery colonies of P. pipistrellus
sensu lato
504 • ANN.ZOOL.FENNICI Vol.45
while individuals from less numerous nursery
more often, as found in P. pipistrellus sensu
stricto liminary
results suggest that the nursery colonies
of P. pygmaeus
of southeastern Moravia change roosts during
the summer.
Contrary to P. pipistrellus, which occupies
buildings in almost 95% of cases (Simon et al.
P. pygmaeus prefers forest and wetland
ery
colonies of the latter were usually found in
buildings (Park et al.
et al.
most records of P. pygmaeus come from low
The main range of this species is in the lowlands
of Moravia and central Bohemia and around
the alluvial plain of large rivers as well as pond
ing
the relatively high foraging activity of P.
pygmaeus
we expected that pipistrelles would use natural
roosts in hollows or similar types of roosts such
as bat boxes, hiding in them more often than in
buildings.
P.
pygmaeus switches its day roost as often as P.
pipistrellus
to describe the movement patterns and habitat
selection of females tagged in two nursery colonies
of P. pygmaeus
number of night/day roosts and frequency of
roost switching are an important factor for the
monitoring and conservation of pipistrelle bat
connected with possible energetic costs during
lactation.
Material and methods
Study area
Fieldwork was carried out in southeastern Moraroosted
under the roof of a pheasantry, a brick
building in the vicinity of the village of Vranovice,
in an oak wood forest along the Svratka
rounding
landscape is characterized by patches
Equipment,
tracking and spatial
analyses
Between June and July 2004, lactating females
were netted individually when emerging from
a colony roost. After capture and tagging, the
patches
around their nipples and the expression
captured and kept in captivity for a short time
Republic. The authors have been authorized to
handle free-living bats according to the cerStudies
have shown that low ambient temperatures
reduce bat activity by reducing the availability
of Diptera, the main prey of P. pygmaeus
temperatures were recorded on the nights of
tracking outside buildings where colonies were
roosting.
Fourteen females from colony A and two
minimum of eight days. The transmitters were
glued to the back of each bat between their scapulae,
after trimming the fur, using liquid cement
et
al.
representing 5% or less of their body mass were
reproductively active and did not suffer from
ANN.ZOOL.FENNICI Vol.45 • Roost switching in pipistrelles 505
major long-term effects. Davidson-Watts and
P. pyg-
maeus
The bats were released and then tracked conof
the tagged bats were recorded throughout
workers co-ordinated their movements using
were assigned into three distance classes, which
differed in open and forest habitats because of
differences in the diffusion of sound waves.
Therefore, we used different bufferings (circles
when we were in close proximity, e.g. close to
roosts or in small foraging areas when we could
in the accuracy of location were tested experimentally
for each transmitter prior to attaching
it to a bat in the two different habitats (forest and
into
the three distance classes mentioned above.
Differences between the estimated locations
t Z
p
between researchers differed by only 2.9% (n
Behaviour of the bats, their location time, the
position of the worker and the position’s accuracy
were immediately recorded on a handheld
tape recorder. The location of bats was estimated
entered into a geographic information system
activity was observed directly and vocalizations
recorded with bat detectors (D 240x, Pettersson
The foraging areas of the bats were determined
by the minimum convex polygon method
et al. -
with
the Animal Movement extension (Hooge
buffered by circles with classes of accuracy
and minimum polygons were separately calculated
around these locations for each night
etry
locations were used in space and habitat
analyses (Seaman et al.
divided into six categories, i.e. forests, tree-lines,
vegetation edges, water bodies, pastures and
estimated via the kernel estimation method using
95% of point locations with least-square crossto
exclude the effects of random outliers for genencloses
the foraging area in use (Schwartz et
al.
was negatively correlated with areas of other
classes, we used the single animals instead of the
locations as a sample unit in order to avoid the
constraints of compositional analyses (Aebischer
et al. tion,
resulting from short sampling intervals, was
not a problem with the data used in analyses (cf.
Statistical analyses and material
Females that were tracked for less than 60% of
the night were excluded from evaluation. The
(cf. McAney
The bats carried active transmitters for an
The two days with values below the 25th and
temperature, air temperature at 21 h, cloud cover,
506 • ANN.ZOOL.FENNICI Vol.45
mean daily humidity, wind speed and rainy nights
We recorded and analysed data for a total of
ally,
it is recommended to use data from individual
animals as sampling units when testing
habitat preference hypotheses (Bontadina et al.
in females from colony A (n
females showed relatively similar patterns of
the days of study and the females themselves
could be detected. Similar sample sizes were
used in studies dealing with the same research
abend
& Simon 2000 in pipistrelles; Bontadina
et al. 2002 in R. hipposideros
a hunting ground or in a roost was considered
a unit of the analysed set. The asymptote was
each of the females studied. Home range size
all, 15 roosts were used in the analysis to deterRoosting
and foraging activity data were not
normally distributed and were analysed using
formed
successfully to approximate normality
using arcsine transformation. logistic
regression were used to check changes in
roost switching and distances between night or
day roosts and foraging sites. The Bonferroni
correction was applied if multiple tests were
used for the same data set. Differences in habitat
use were tested using contingency tables ( 2
-
duct
the analyses.
Results
Roosting and flight activity
H = 11.62, n = 61, p >
(H n = 61, p >
(H n = 61, p
or among successive nights of one female. Therefore,
the data from different females and nights
were pooled for subsequent analyses.
Overnight changes in activity
H2
= 10.62, n = 61, p
foraging activity (H2
n = 61, p
were found among night thirds (early, middle and
cant
increase in roosting activity was recorded
during the 2nd third. Roosting activity was as
other hand, no differences in commuting activbats
left the roost and foraged continuously.
Foraging areas and habitat use
Habitat selection was investigated only in
females from colony A (n
range sizes depended on the number of telemetry
locations. Maximum size of foraging areas was
polygons
we calculated the absolute foraging
ing
area for the others (similar to Bontadina et
al.
H10
n = 111, p
comparison of habitat use in the core foraging
-
ferred
vegetation edges and water bodies more
ANN.ZOOL.FENNICI Vol.45 • Roost switching in pipistrelles 507
2
5, p -
-
tats
was not different between colony range and
the availability of foraging habitats ( 2
= 0.06,
df = 4, p
foraging habitats we used the area of a circle of
all females foraged at water bodies and vegetaHigh
foraging activity found in the vicinity of
street lamps was not representative for all tagged
females, as only six females foraged in this habitat
type.
Night roosts and roost switching
night and female. A quadratic polynomial regresvisits
at the beginning of lactation as well as the
decrease at the end of lactation (R2
= 0.45, F =
p
found in tree cavities and only two in buildings
colony A used six different day roosts, while
nursery colony B only three during the study
period. Tagged females from colony A used three
100 adult females, and three individual roosts.
321
Thirds of night
0
50
100
150
200
250
300
Minutes
foraging commuting roosting
*
*
**
*
Edge Water Open
Habitats
0
10
20
30
40
50
60
70
colony range
availability
activity
Percentage
Forest Street
lamps
Linear
0
Number of days after finding the first young
0
1
2
3
4
5
6
7
8
Numberofroostvisitspernight
5 10 15 20 25 30
Fig. 3. Number of roost visits per night during the
whole lactation period. A quadratic polynomial regression
describes, significantly, the increase of roost visits
at the beginning of lactation and the decrease at the
end of lactation.
Fig. 1. Foraging, commuting and roosting of Pipistrellus
pygmaeus (time in min) for the early, middle and late
thirds of the night. Mean (square, diamond, tringle);
box: 25% and 75% percentiles; whiskers: minimum–
maximum. * p < 0.01; ** p < 0.001.
Fig. 2. Habitat use by Pipistrellus pygmaeus. Comparisons
of habitat availability vs. habitat use are based on
the minimum convex polygon of all females vs. the level
of activity (mean percentage) per individual. Habitat
selection was investigated only for females from colony
A (n = 11).
508 • ANN.ZOOL.FENNICI Vol.45
Distances between roosts and foraging
sites
The median distance between night and day
F26
p tances
between foraging sites and roosts (F26
=
p
increase in the distance between night and day
spent by females in night roosts was constant
F p
distances between day roosts and foraging sites
used foraging sites more distant from their original
day roost in the building (mean ± SD = 446
between foraging areas and the new day roost
(paired t t = 2.50, n p
Other general observations
Three females probably transported their young
to night roosts, as evidenced by records of the
used at night. Four lactating females visited
P.
pygmaeus.
However, we located only one male roost. A
tagged female, accompanied by a male, zigzan
= 6, mean ±
ized
were more distant from the day roost than
night roosts used only by females (mean ± SD =
vs
lactating female was even found in a company of
one male P. pygmaeus and one P. nathusii in the
their day roosts in the vicinity of male territories.
All new female day-roosts within male territories
were over 1 km away from their main day roost
Discussion
Changes in activity
behaviour and roost switching between pipist-
Watts
et al. dal
nocturnal activity pattern in P. pipistrellus
0
Days of observation
0
200
400
600
800
1000
1200
1400
1600
Maximumdistanceofnightroost(m)
*
*
*
*
*
*
*
*
5 10 15 20 25 30
0 5 10 15 20 25 30
Days of observation
800
1400
200
Roost–foragingsitedistance(m)
Fig. 4. Linear regression (R2
= 0.18, F = 5.43, p
= 0.027) describing changes in maximum distance
between night and day roosts. * indicates nights when
females visited a male roost.
Fig. 5. Linear regression (R2
= 0.47, F = 20.83, p =
0.001) describing changes of distance between roosts
and foraging sites. An increase in distance between the
roosts and the foraging sites was found towards the
time of weaning.
ANN.ZOOL.FENNICI Vol.45 • Roost switching in pipistrelles 509
sensu lato during the lactation period. During the
observed 1.1 foraging bouts on average in P.
pygmaeus. However, in our study the number of
the other hand, several bouts were shorter, less
siderably
lower than those found by Davidsonby
Jenkins et al. P.
pipistrellus sensu lato. The relatively short time
spent foraging could be due to the availability of
as compared with those occurring in different
Foraging areas and habitat use
that
P. pipistrellus used more habitat types than P.
pygmaeus. Their results show that P. pygmaeus
seems to prefer a limited spectrum of habitat
types, while P. pipistrellus is more opportunist
and uses a wider range of habitats. The association
of P. pygmaeus with water is well known
(Vaughan et al.
Rydell et al. istrelles
above cluttered rather than open water
preference of water habitats in core foraging
areas as compared with a cluttered forest or
that P. pygmaeus also prefers vegetation edges
characterized by a high density of potential prey,
which can also be used more frequently due
to their proportionately greater presence in the
landscape under study compared to infrequent
istrelles
prefer vegetation edges.
Roost switching and distances
Pipistrellus pipistrellus/pygmaeus (e.g. Thompson
1992, Park et al. tion
period to study roost switching because of
moregulation
which affects the frequency of
P. pygmaeus
nursery colonies is about 200 females (Barlow
females in colonies in buildings (median = 65, n
may be due to more frequent roost switching
— induced by changes in preferred temperatures
during the reproductive season — as compared
with large pipistrelle colonies occupying stone
between eight different shelters in a colony consisting
of nearly 200 adult females. We found
three parallel shelters visited by females coming
The whole colony did not move between shelters
found in P. pipistrellus
the females moved between six shelters discovered
every other day.
There are no genetic data available to determine
kinship among bats within colonies of P.
pygmaeus, but the simultaneous use of more
shelters by females coming from one colony indiused
in Myotis bechsteinii
and Eptesicus fuscus
et
al.
that the foraging areas are close to the roosts.
tance
between day roosts to be several times
longer than the distance between the roost and
the foraging site. Although the sample was small
our results support the hypothesis that females
may change their roosts because they are closer
to attractive foraging sites (e.g. Feyerabend &
night foraging site and the previous day roost
was always longer than the distance between the
new day roost and the foraging site in the subsequent
night. However, females can also use different
roost types due to different microclimatic
510 • ANN.ZOOL.FENNICI Vol.45
conditions inside them (buildings versus natural
to
determine the actual size of a P. pygmaeus
simultaneously more than one roost. By contrast,
switch roosts for most of the reproductive season
vation
is very important especially in view of
long-term monitoring programmes in which the
size of maternal colonies is considered a basic
index of population dynamics.
Transport of young
Suckling female P. pygmaeus, similarly to P.
pipistrellus, were found to use several day roosts
all-night recordings, we found that one female
carried its naked suckling infant into the empty
box and returned for it some hours later. A similar
behavioural pattern was also observed (by
case of two tagged females from nursery colony
A. Juveniles were observed during the night in
all roosts. For lactating females, transporting
young and depositing them in a temporary roost
within the hunting ground can be less costly than
nursery.
Paying visits to males
Four lactating females visited sites where we
P. pygmaeus. We
concluded that they might have been uttered by
were registered later, after weaning the young.
during the lactation period at the end of June.
calls were also emitted during group foraging but
no feeding buzz was found during our recordings.
Calls were produced at regular intervals
indicating their attractive character (Lundberg &
showed signs of nursing but we cannot exclude
the possibility that their young died soon before,
or during our study. The day after males were
visited, three females chose their night roost in a
tree hole in the vicinity of the male territory they
had visited the previous night. Most observations
et al.
offspring other than their own, therefore we
suppose that the females had to carry their own
young. The possibility of the young remaining
inside a roost in the absence of its mother during
daylight needs to be tested in more controlled
females must be able to invest some of their
stored energy in visits to male territories even
during lactation, a period of highest energetic
cost.
of P. pygmaeus from a maternal colony use more
than one roost and the movements among these
roosts are often. This observation makes colonycounting
as a method commonly used to evaluate
changes in population dynamics unreliable
and should be consulted within the framework
of international conservation and management
measures. Roost switching and the transport of
young by females reduce energy costs related to
lactating females visit territorial males and share
their roost suggest that the lactation period is less
costly than is generally accepted.
Acknowledgements
-
tion
of the Czech Republic and a grant from the Ministry
MSM0021622416.
ANN.ZOOL.FENNICI Vol.45 • Roost switching in pipistrelles 511
References
Compositional analysis of habitat use from animal radiotracking
data. — Ecology
. — Swedish
-
servation.
Pipistrellus pipistrellus in Britain. — Journal of Zoology,
London
Animal
Behaviour
and wing morphology of two phonic types of Pipistrellus
pipistrellus. — Mammalian Biology
answers the call of pipistrelle bat species. — Nature
tat
use of Pipistrellus pygmaeus
— Mammalia
mate
of bat boxes on their occupation by the soprano
pipistrelle Pipistrellus pygmaeus
switching. — Acta Chiropterologica
otracking
reveals that lesser horseshoe bats Rhinolophus
hipposideros forage in woodland. — Journal of Zoology,
London
Pipistrellus
pipistrellus and Pipistrellus pygmaeus in lowland
Bat Research
News
ing
behaviour between Pipistrellus pipistrellus Schreber,
Pipistrellus pygmaeus Journal
of Zoology, London
habitat selection by Pipistrellus pipistrellus and Pipistrellus
pygmaeus
for cryptic species of echolocating bats. — Biological
Conservation
switching in a summer colony of 45 kHz phonic type
pipistrelle bats Pipistrellus pipistrellus
— Myotis
Chiroptera. — Folia Facultatis Scientiarum Naturalium
Universitatis Masarykianae Brunensis, Biologia
Folia
Zoologica
in historic landscape parks in relation to habitat composition
and park management. — Animal Conservation
— Scottish Bats
Harris, S., Cresswell, W. J., Forde, P. G., Trewhella, W. J.,
niques
particularly as applied to the study of mammals.
— Mammal Review
Animal movement
extension to ArcView version 1.1. — Alaska Science
Hughes, P. M., Speakman, J. R., Jones, G. & Racey, P. A.
Pipistrellus
pipistrellus. — Journal of Zoology, London
Pipistrellus
pipistrellus
northeast Scotland. — Animal Behaviour
Proceedings
of the Royal Society B
-
Holarctic
Ecology
the estimates of home range size, movements, and habiAnnales
Zoologici Fennici
associations in female Bechstein’s bats Myotis bechsteinii.
— Behaviour
and mate attraction in the bat Pipistrellus pipistrellus.
— Ethology
Pipistrellus
pipistrellus Journal of Zoology,
London
overnight and seasonal variation in the foraging activity
of lesser horseshoe bats. — Acta Theriologica
Eptesicus fuscus after radiotagging. — Journal of Mam-
malogy
size and spatial partitioning in cryptic and sympatric
pipistrelle bats. — Behavioral Ecology and Sociobiology
roost of the 55 kHz phonic type of pipistrelle bats Pipistrellus
pipistrellus. — Journal of Zoology, London
estimates in the analysis of radiotracking data. — Journal
of Wildlife Management
512 • ANN.ZOOL.FENNICI Vol.45
roosting in the two phonic of Pipistrellus pipistrellus
during the mating season. — Proceedings of the Royal
Society B
Pipistrellus
pipistrellus
Journal
of Animal Ecology
Pipistrellus and
Myotis
using a nonlinear model. — Myotis
conservation implications. — Ecography
Habitat use by bats along rivers in north east Scotland.
— Folia Zoologica
factors affecting the distribution of the sibling species
Pipistrellus pygmaeus and Pipistrellus pipistrellus.
— Mammian Biology
-
Ursus
sample size on kernel home range estimates. — Journal
of Wildlife Management
Ecology
and conservation of bats in villages and towns.
habit use when the individual animal is the sampling
units. — Mammalian Review
Pipistrellus
pipistrellus in northeast Scotland. — Journal of
Zoology, London
interval on estimates of homerange size. — Journal of
Wildlife Management
Pipistrellus
pipistrellus Naturalist
relle
bats Pipistrellus pipistrellus. — Journal of Zoology,
London
Chiroptera assessed by means of broadband acoustic
method. — Journal of Applied Ecology
Warren, R. D., Waters, D. A., Altringham, J. D. & Bullock,
Myotis
daubentonii and pipistrelle bats Pipistrellus pipistrellus
Vespertilionidae in relation to small-scale variation in
riverine habitat. — Biological Conservation
tion
dynamics of a maternity colony of the pipistrelle
bats Pipistrellus pipistrellus in northeast Scotland. —
Journal of Zoology, London
brown bats, Eptesicus fuscus
fusion model. — Animal Behaviour
lization
distribution in home-range studies. — Ecology
and error ellipses. — Canadian Journal of Zoology
This article is also available in pdf format at http://www.annzool.net/
8.2 Životní cyklus štěnic a přežívání v úkrytech netopýrů
BARTONIČKA T. & GAISLER J., 2007
Seasonal dynamics in the numbers of parasitic bugs (Heteroptera, Cimicidae): a possible
cause of roost switching in bats (Chiroptera, Vespertilionidae).
Parasitology Research, 100: 1323–1330.
ORIGINAL PAPER
Seasonal dynamics in the numbers of parasitic bugs
(Heteroptera, Cimicidae): a possible cause of roost switching
in bats (Chiroptera, Vespertilionidae)
Tomáš Bartonička & Jiří Gaisler
Received: 9 November 2006 /Accepted: 24 November 2006 / Published online: 10 January 2007
# Springer-Verlag 2007
Abstract The objective of the present paper is to extend
the knowledge of roosting strategies of bats and the
interaction of bats with their roost ectoparasites, the bat
bugs Cimex pipistrelli. The project was focussed on the
potential causality of bat movements and the variation in
bug numbers. For 2 years, three model bat boxes with
breeding female Pipistrellus pygmaeus were monitored
inside floodplain forest. After the arrival of bats in May,
adults and first instars of bugs were observed in the boxes.
During the lactation period in June, when the bats did not
occupy the roosts, the first instar bugs died out followed by
the adults. The decrease in bug numbers began only several
days after the bats had left the boxes. After a month of the
bats’ absence, the abundance of adult bugs decreased by
half of their number. Only the eggs survived the period
when the roosts were unoccupied in summer. In mid-July,
after the arrival of lactating females, an increase in the
number of bugs was observed. At the beginning of August,
however, no new eggs were found. Although adult C.
pipistrelli are able to survive the winter period in the boxes,
the bats, by shifting the roosts within the vegetation season,
prevent the massive reproduction of these parasites.
Introduction
Previous studies were mostly focussed on communities of
ectoparasites of different bat species with no regard to their
life strategies (e.g. Whitaker and Mumford 1978; Whitaker
et al. 2000; Ritzi et al. 2001; Ritzi and Whitaker 2003). Few
papers described the relationship between ectoparasite
density and the reproductive cycle of its bat host (Dietz
and Walter 1995; Christe et al. 2000). There are several
studies in which the impact of ectoparasites living permanently
on the host body (e.g. mites, Spinturnicidae) was
analysed (Lewis 1996; Giorgi et al. 2001). Bugs of the
family Cimicidae are the most important roost ectoparasites
of bats. The family includes 91 species, 61 of which
parasitize bats (Ryckman et al. 1981). Great mobility and
ability to survive without their hosts for a long time makes
the bugs important model ectoparasites, not only of bats
(Usinger 1966). Several authors dealt with the taxonomy of
bugs parasitizing bats, yet unsolved problems persist,
including the status of Cimex lectularius and Cimex
pipistrelli (Wendt 1941; Povolný 1957; Usinger 1966;
Péricart 1972; Aukema and Rieger 1995–1996; Péricart
1996). In this paper, both taxa mentioned above are
regarded as separate species.
Fast ontogeny enables the bugs to increase their numbers
rapidly soon after a roost was occupied by bats. Due to the
fact that it is also parasitizing man, the bed bug (C.
lectularius) is the best-known cimicid species. Female bed
bugs usually lay from two to four eggs per day. During its
life, a single female can lay as much as 500 eggs (Davis
1964). Bed bugs suck blood in periods of few days and are
able to starve for months (maximum 1.5 year). Due to their
long starvation capacity, bed bugs survive the winter period
or the absence of the host in its roosts (Johnson 1942;
Povolný 1957). Usinger (1966) found that the temperature
and humidity in the roost influences the survival of all
ontogenetic stages and the promptness of adults to copulate.
Bugs in general prefer lower roost temperature than other
bat parasites do because they stay on bats for a short time to
feed only (Usinger 1966). At present, scant information is
available on the possible impact of microclimate fluctuation
Parasitol Res (2007) 100:1323–1330
DOI 10.1007/s00436-006-0414-6
T. Bartonička (*) :J. Gaisler
Institute of Botany and Zoology, Masaryk University,
Kotlářská 2,
611 37 Brno, Czech Republic
e-mail: bartonic@sci.muni.cz
and the length of starvation on the survival of particular
ontogenetic stages and adults of the two sexes (Rivnay
1932; Johnson 1940; Omori 1941).
Nursery colonies of several bat species dwelling in
crevices of trees, hides or buildings switch roosts frequently
during the reproduction season (e.g. Thompson 1990 in
pipistrelles or Kerth and König 1999 in Myotis bechsteinii).
In the territory of the present Czech Republic, the bugs
(Cimicidae) were found in roosts occupied by Pipistrellus
pipistrellus s.l. (Gaisler 1966; Hůrka 1988). New observations
show that bat bugs C. pipistrelli occupy the roosts of
two pipistrelle species, P. pipistrellus and Pipistrellus
pygmaeus (Bartonička, unpublished). As in P. pipistrellus,
females of P. pygmaeus switch roosts very often. Typically,
groups of females leave their respective roosts in early June
and move to the main nursery roost few days before
parturition. They move back to their previous roosts with
flightworthy juveniles in mid-July (Swift 1980; Webb et al.
1996). The so-called fission–fusion model common in
primates, i.e. a temporary splitting of one nursery colony
into sub-groups, was described in M. bechsteinii (Kerth and
König 1999; Willis and Brigham 2004). Similar roost
switching strategy was observed in P. pipistrellus and P.
pygmaeus (Feyerabend and Simon 2000, own observation).
Sub-groups of genetically close females occupied a complex
of tree hollows and bat boxes within a small area and
switched roosts every 2 days (Willis and Brigham 2004).
Although the fact of roost switching was demonstrated, the
cause or causes of this phenomenon were not understood
completely till now (e.g. Lewis 1995; Vonhof and Barclay
1996; Brigham et al. 1997). There are several hypotheses
explaining why bats switch their roosts. The movements
may be caused by sudden changes in microclimatic
conditions, restricting the circulation of air inside a crevice
type shelter (Whitaker 1998; Lourenço and Palmeirim 2005)
or changes in thermoregulatory requirements of bats regarding
their reproduction cycle (pregnancy vs lactation) (e.g.
Thompson 1990; Hamilton and Barclay 1994; Kerth et al.
2001). In addition, the impact of humans, animal predators
or unknown factors can disturb bats (Lewis 1995).
In our study, we focussed on a hypothesis assuming that
by switching roosts the bats avoid the increasing invasion
by ectoparasites and keep their individual fitness (Wolz
1986; Lewis 1996). The large numbers of ectoparasites
observed on adult females and young after parturition show
synchronisation of the population cycles of ectoparasite and
host. Seasonal changes in the numbers of C. pipistrelli in
semi-natural roosts were evaluated regarding the presence
of bats. We attempted to answer the following two
questions: (1) Do temperature and humidity influence the
numbers of bat bugs in the roosts? (2) Is there any
correlation between the numbers of bats and bat bugs? We
think that the data on roost infestation by parasites together
with the knowledge of other parameters such as the
microclimate of occupied roosts (Lourenço and Palmeirim
2005; Bartonièka and Øehák 2007) can be utilised for the
purposes of conservation of bats and their shelters.
Materials and methods
Study area and technical equipment
Nursery and temporary colonies of P. pygmaeus with high
densities of bat bugs C. pipistrelli were monitored in three
wooden bat boxes inside the Křivé jezero floodplain forest
(S Moravia, Czech Republic) for 2 years. In the first
growing season (2004), all bat boxes were equipped with
passive IR Trail Monitors, TM (TM550, TrailMaster,
Goodson & Associates, USA) (after Thomas 1995) and
thermometers (Hobo, Onset Computer Corporation) to
record the presence of bats and the temperature in the
boxes over the season. TM monitors were situated in front
of the entrance to each box (Bartonička and Řehák 2007).
Hobo Data Loggers continuously recording internal temperature
and internal humidity were situated under the roof
of each bat box. The accuracy of the relative humidity
sensor was ±4% and that of the temperature sensor ±0.4°C.
Monitoring of bat bugs was carried out by manually
sampling from inside the box roof and recording the
activity of insects by a video system (B/W AVC 307R+12
IR diode). In each of the three boxes, the IR diode camera
monitored a particular inside area (3×10 cm) and recorded
the relative activity of bugs in 30 min periods. All
monitoring was carried out regularly in 10-day periods just
before most bats left a particular bat box to limit the effect
of human disturbance. Each sample of bat bugs was divided
into four groups: (1) adults, males and females together, (2)
first to third instars, (3) fourth and fifth instars and (4) eggs.
Females prevailed among the adult insects. In each group,
the number of bugs was recorded. Bug movements within
the experimental inside area scanned by the camera were
counted regardless of the groups.
The reproductive season under study was divided into
three parts: pregnancy (till 6 June), lactation (7 June till 6
July) and post-lactation (since 7 July). The time of
parturition was indicated by the presence of seven
newborns in one of the three boxes.
Statistical analysis
No significant differences were found between the two
seasons, 2004 and 2005, which allowed to pool the data.
All variables showed a normal distribution (Kolmogorov–
Smirnov test). Statistics for Windows 7.0 was used for data
analyses (PCA, ANOVA, t tests, correlations). The level of
1324 Parasitol Res (2007) 100:1323–1330
morning bat activity (returning from foraging flights at 1–
5 AM) (Trail Monitors) positively correlated with the
number of bats found in a box later during that day when
the boxes were checked manually (Pearson’s correlation
coefficient, r=0.73, p<0.05). The numbers of bugs,
revealed from records of their activity by a video system,
positively correlated with that obtained by manual sampling
from inside the box roof (r=0.84, p<0.05). No significant
differences were found in the numbers of bugs and presence
of bats between particular bat boxes (ANOVA, number of
bugs, F=0.57, ns; presence of bats, F=2.10, ns), therefore
the data were pooled. Analysis of variance (ANOVA) was
used to check the differences between the parts of season
and t test as post hoc. Principal component analysis (PCA)
was used to check the effect of partly correlated variables
(internal temperature, internal humidity, numbers of bugs
and bats). The model was fitted by means of microclimatic
parameters from the light part of the day and the number of
bats using a particular bat box as their day roost. Bonferroni
correction was applied if multiple tests were used for the
same data set.
Material
During the two growing seasons, the three bat boxes
occupied by soprano pipistrelles (P. pygmaeus) were
monitored for 151, 199 and 115 days, respectively. For
each day, hourly values were available for internal
temperature, internal humidity and the level of the bats’
activity. The samples of bat bugs (C. pipistrelli) were taken
on 19 occasions.
Results
Seasonal changes in the occupancy of bat boxes
The differences in the numbers of bugs and presence of bats
among 19 checks were statistically significant (ANOVA, F=
1.89, p<0.01). Two peaks in the occupancy of boxes by
bats were recorded in May and August. Pregnant females
used these roosts before parturition and some of them
returned with flightworthy young (Fig. 1). During the
pregnancy of bats until the parturitions in mid-June, a
significant increase in the number of bat bug eggs was
recorded (t test, t=−6.69, Bonferroni correction, p=0.001,
n1=3, n2=3). A significant decrease was found from early
June until the end of July. No bug eggs were found on
subsequent checks (Fig. 1). The number of adult female
bugs, surviving from previous winter, decreased until midJune
(t=−83.59, Bonferroni correction, p=0.001, n1=3, n2=
3) when they died out. Only nymphal stages were present in
the boxes during the first half of August. A rapid increase in
the number of adult bugs was registered after the bats,
mainly young ones, returned to the boxes in mid-August (t=
−3.34, Bonferroni correction, p=0.01, n1=3, n2=3). After
mid-September, when the metamorphosis of the last (fifth
instar) nymphae was completed, the number of adults
stagnated. Only adults survived the winter period. Two
peaks in the presence of bats were distinct throughout the
season. The first peak during pregnancy, however, was
insignificant (t test, t=2.03, Bonferroni correction, ns, n1=3,
n2=3). During the lactation period, the number of bats in the
boxes was very low. A significant increase was found from
the beginning of July until the second half of August (t=
−1.54, Bonferroni correction, p=0.001, n1 =3, n2 =3)
(Fig. 1). During the period in which the bats were absent
(lactation, June), a rapid dying of the early stages of bugs
(first to third instars) was recorded. After all the bats had left,
the abundance of this bug group decreased to a half in
9 days. A similar decrease in the number of fourth and fifth
instar bugs was observed in 16 days. Likewise, the number
of adults decreased to less than a half during the absence of
bats. In general, the population of bat bugs survived the
summer absence of bats in the egg and nymphal stages.
Relationship among particular variables
Internal temperature, relative humidity, number of bugs
(adults, first to third instar, fourth and fifth instar), number
of eggs and number of bats were included in the principal
component analysis. The first two factors accounted for
78.8% of variability. Table 1 shows the relations of
individual components and variables. The cluster of days
during bat pregnancy differed due to the positive correlation
of component 1 with the number of adults and first to
third instar bugs and due to the negative correlation with
the number of eggs, which increased rapidly in these days.
A large number of eggs were also observed during
lactation, but nymphal and adult bugs and bats were
found in very low numbers. The cluster of days in the
post-lactation period was characterized by positive correlation
of numbers of adult bugs and bats at the absence of
eggs (Fig. 2). Furthermore, significant differences using
discrimination analysis were found related to the reproduction
period (Wilks’ λ=0.34, F=2.91, p<0.002).
A positive correlation was found between the number of
adult and fourth and fifth instar bugs (Pearson’s correlation
coefficient, r=0.52, p=0.005) and between the number of
eggs and number of individuals of first to third instar (r=
0.33, p=0.001). The number of eggs and relative humidity
correlated negatively (r=−0.37, p=0.01). The presence of
bats positively correlated with the number of first to third
instar bugs (r=0.39, p=0.001). The possible impact of
temperature on the number of bugs was tested. A positive
correlation was found only between the internal temperaParasitol
Res (2007) 100:1323–1330 1325
Fig. 1 Changes in numbers of
bat bug adults, all instars and
eggs, and numbers of bats;
mean—central tendency,
SD—large box
Table 1 Correlations (Pearson’s correlation coefficient) between variables and components of PCA
A B C D Bats Tin Hum
Component 1 0.68* 0.47* 0.39* −0.69* 0.46* 0.04 0.34*
Component 2 0.23 −0.27 0.25 0.21 0.05 −0.62* 0.05
A: adult bed bugs, B: fourth and fifth instars, C: first to third instars, D: eggs, Tin: internal temperature, Hum: relative humidity.
*p<0.05, all values are significant.
1326 Parasitol Res (2007) 100:1323–1330
ture 10 days before the checks and the number of first to
third instar bugs (Pearson’s correlation coefficient, r=0.41,
n=38, p<0.005).
Discussion
Microclimatic conditions
From among various environmental factors, temperature
seems to be the most important because it influences the
development and activity of bugs. In most roosts, temperature
varies significantly during both the season and the
day, being rather constant only in large caves and similar
shelters (Usinger 1966). In this paper, however, nearly no
correlation between the temperature and the number of bat
bugs was revealed. The only exception was a positive
correlation between the temperature in the boxes and the
number of early developmental stages of bugs found
10 days later. This may have been due to the accelerated
embryonic and nymphal development at optimum temperature.
In contrast to C. lectularius, no information is
available concerning the response of C. pipistrelli to various
microclimatic conditions (e.g. Rivnay 1932; Johnson 1940;
Omori 1941) but the main aspects may be similar in the two
species. In C. lectularius, the embryonic development is
accelerated by temperature increasing up to 30°C, when it is
the shortest (3.7 days, Omori 1941). The upper temperature
limit, blocking the hatching, nymphal development and adult
activity, is 37°C in C. lectularius (Omori 1941). Mortality
sets in at 44–45°C (Hase 1917) but for a short time, in the
order of hours, bed bugs are able to survive even such high
temperatures. During our study, the temperature in the boxes
reached values of this kind on 13 days yet the daily mean
temperature never exceeded 30°C. Laboratory testing is
required to reveal the impact of temperature on the timing of
development in bat bugs.
Relative humidity of air is another factor that possibly
influences the seasonal dynamics of bat bugs. The experiments
with C. lectularius suggested that in some instars
their development was shortened at 32°C when the
humidity was low; in contrast, at 22°C the development
was shortened when the humidity was high (Rivnay 1932).
According to Kemper (1936), extremely low relative
humidity (0–20%) often causes the death of nymphae in
the course of ecdysis. The negative impact of low humidity
on the first instar may even be greater. At relative humidity
<60%, its survival is reduced to a fifth (Jones 1930).
Mortality is caused by dehydration (Mellanby 1932). In the
bed bug, both high and low temperatures when combined
with high humidity cause up to 90% mortality of eggs
(Johnson 1940). Correspondingly, the results of our study
on the bat bug show negative correlation of the number of
eggs with relative humidity. The combination of low
temperature and high humidity was typical for the postlactation
period when no new eggs were recorded. As
indicated by the results of laboratory experiments with C.
lectularius, the survival of eggs of C. pipistrelli during the
humid autumn season is reduced if not impossible. The
hibernation of adults and not of eggs, therefore, could be an
Fig. 2 Principal component
analysis (PCA): on the axes are
values of the two first factors
(describing 78.8% of inner variability).
Ellipses represent the
75% confidence interval for the
days of the reproduction
periods—pregnancy (dashed
line), lactation (dotted line)
and post-lactation (solid line).
A: Adult bat bugs, B: fourth and
fifth instars, C: first to third
instars, D: eggs, Tin: internal
temperature, Hum: relative
humidity
Parasitol Res (2007) 100:1323–1330 1327
adaptation to the cold and humid climate of the temperate
zone.
Availability of food
In the bed bug, the availability of food affects oviposition,
duration of individual instars and total length of life
(Usinger 1966). The frequency of bloodsucking is positively
correlated with temperature, e.g. every third day at
27°C in adults (Kemper 1936). The nymphae are able to
feed 24 h after ecdysis but they suck in shorter intervals
than the adults do. Concerning various developmental
stages, early instars are the most vulnerable if they do not
have enough food. Food deficiency has a negative impact
mainly when ambient temperatures are high. Such temperatures,
though not yet lethal, force the bugs to suck more
often because they prevent bug torpidity and increase the
danger of dehydration. The availability of food affects the
weight of a particular adult female, which is positively
correlated with the number of eggs laid. When feeding
regularly twice a week, the females produce 2.76–8.26
(average 5) eggs per week for about 18 weeks (Johnson
1942). The adult life span may encompass 12–18 months
and after harvesting, they usually die (Usinger 1966). The
results of this study correspond to these data in that the early
instar bugs will die soon after their hosts have left the boxes
and no eggs were found at the end of July. The presence of
pregnant female bats after the end of April is essential to
start the process of gradation of the bug numbers and assure
the production of sufficient number of eggs that will survive
the absence of bats during lactation.
Impact of bugs on bats
Abundant bat bugs may induce heavy stress to their hosts.
The trouble they cause may lead to disquiet of bats
resulting in their abnormally frequent scratching, cleaning
of fur and wing membranes and efforts to catch the
parasites on their body. Several authors argue that the
increased number of roost parasites forces the bats to leave
the roost and find another one (e.g. Wolz 1986; Lewis
1996; Walter 1996). Roost switching seems to be a good
anti-parasitizing strategy of bats with respect to C.
pipistrelli. This bug species was by far not recorded in all
maternity colonies of bat species known as its potential
hosts. According to Reinhardt and Siva-Jothy (2007), only
12% of Myotis myotis colonies were parasitized by C.
pipistrelli. In shelters of bat species preferring tree hollows
and various fissures in summer, such as P. pipistrellus and
Nyctalus noctula, the presence of bat bugs was recorded
more often (K. Hůrka, unpublished). However, it is more
difficult to check fissure-like roosts than spacious shelters
such as lofts of buildings for the presence of bugs. At
present it seems that in the territory of the Czech Republic,
C. pipistrelli is common in “fissure” bat species that often
change their roosts, while C. lectularius occurs rarely and
only in “space” bat species with a high degree of philopatry
to their summer shelters (O. Balvín, unpublished). Further
research is needed to specify the differences in seasonal
dynamics between the two species of bugs.
In Europe and North America, the highest abundance of
bat ectoparasites has usually been recorded in the second
half of May when maternity colonies of bats are wellestablished
(e.g. mites, Estrada-Peña et al. 1991; Lučan
2006). The simultaneous use of more shelters by females
coming from one colony was observed in certain bat
species during pregnancy (e.g. Kerth and König 1999;
Willis and Brigham 2004). Shortly before parturition,
heavily pregnant females return to their original large
maternity shelter. They give births there and suckle their
young. Among other initially tree bats, this is also the case
of pipistrelles (Swift 1980). During the lactation period,
most satellite roosts are empty (bat-free). The present study
shows that the absence of hosts, coupled with high
temperatures and natural mortality of parasites reduces the
number of bat bugs in bat boxes to less than a half of the
number recorded before the bats left. Immature bugs die
almost totally. However, why do female bats return to the
satellite roosts after lactation and perhaps show them to
their young in spite of the previous bad experience with bat
bugs? The answer may be that the roost selection of female
bats is governed by their thermopreferendum: they seek
thermally optimum shelters that differ within their reproduction
cycle (Thompson 1990).
The bugs are not the only ectoparasites of temperate bat
species. Very likely, bat anti-parasitizing strategies against
mites, fleas, nycteribids and bugs are mutually different. In
bat species parasitized mainly by spinturnicid mites, e.g.
Miniopterus schreibersii and M. daubentonii, the course of
clustering and shift of shelters of reproducing females
during the season is different from that in bats parasitized
mainly by bugs (Estrada-Peña and Serra-Cobo 1991; Dietz
and Walter 1995). To conclude, the study shows that
pipistrelle bats are able to prevent the massive reproduction
of bat bugs by temporarily abandoning particular roosts.
Nevertheless, they are unable to rid their roosts of the
ectoparasites completely, which is the obvious consequence
of the co-evolution of Pipistrellus bats and Cimex bugs
under the conditions of the temperate climate.
Acknowledgments The authors are indebted to R. Obrtel (Brno) for
both his revision of the English and his comments on the study from
an entomologist’s point of view. The study was supported by grant no.
MSM 0021622416 of the Ministry of Education, Youth and Sports of
the Czech Republic, grand no. 206/07/P098 of Science Foundation of
the Czech Republic and the Czech Bat Conservation Trust. The boxes
were checked under the licence no. 922/93-OOP/2884/93 of the
1328 Parasitol Res (2007) 100:1323–1330
Ministry of Environment of the Czech Republic. The authors were
also authorized to handle free-living bats according to the certificate of
competency no. 104/2002-V4 (Section 17, Law no. 246/1992).
References
Aukema B, Rieger C (1995–1996) Catalogue of the heteroptera of the
Palearctic region. Nederlandse Entomologische Vereiniging, Wageningen
Bartonička T, Řehák Z (2007) Influence of the microclimate of bat boxes
on their occupation by the soprano pipistrelle Pipistrellus pygmaeus:
possible cause of roost switching. Acta Chiropt (in press)
Brigham RM, Vonhof MJ, Barclay RMR, Gwilliam JC (1997)
Roosting behaviour and roost-site preferences of forest-dwelling
California bats (Myotis californicus). J Mammal 78:1231–1239
Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a
parasitic mite (Spinturnix myoti) in relation to the reproductive
cycle and immunocompetence of its bat host (Myotis myotis).
Ecol Lett 3:207–212
Davis MT (1964) Studies of the reproductive physiology of Cimicidae
(Hemiptera). I. Fecundation and egg maturation. J Insect Physiol
10:947–963
Dietz M, Walter G (1995) Zur Ektoparasitenfauna der Wasserfledermaus
(Myotis daubentonii Kuhl, 1819) in Deutschland unter der
besonderen Berücksichtigung der saisonalen Belastung mit der
Flughautmilbe Spinturnix andegavinus Deunff, 1977. Nyctalus
5:451–468
Estrada-Peña A, Serra-Cobo J (1991) The acarinia and nycteribidia
zones of Miniopterus schreibersii Kuhl (Mammalia: Chiroptera)
in the northeast of Spain. Folia Parasitol 38:345–354
Estrada-Peña A, Peribáñez MA, Serra J (1991) The life cycle of
Spinturnix psi (Mesostigmata: Spinturnicidae) on Miniopterus
schreibersii (Mammalia: Chiroptera). In: Dusbábek, Bukva V
(eds) Modern acarology, vol 2. Academia, Prague, pp 475–480
Feyerabend F, Simon M (2000) Use of roosts and roost switching in a
summer colony of 45 kHz phonic type pipistrelle bats (Pipistrellus
pipistrellus Schreber, 1774). Myotis 38:51–59
Gaisler J (1966) A tentative ecological classification of colonies of the
European bats. Lynx n.s. 6:35–39
Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic
grooming costs imposed by a parasitic mite (Spinturnix myoti)
upon its bat host (Myotis myotis). Proc Biol Sci 268:2071–2075
Hase A (1917) Die Bettwanze (Cimex lectularius L.) ihr Leben und
ihre Bekämpfung. Monographien zur angewandten Entomologie
IV, 1. Verlagsbuchhandlung Paul Parey, Berlin
Hamilton IM, Barclay RMR (1994) Patterns of daily torpor and day
roost selection by male and female big brown bats (Eptesicus
fuscus). Can J Zool 72:744–749
Hůrka L (1988) Die Zwergfledermaus (Pipistrellus pipistrellus)
(Mammalia: Chiroptera) in Westböhmen. Folia Mus Rerum Nat
Bohem Occident Plzeň 27:1–31
Johnson CG (1940) Development, hatching and mortality of the eggs
of Cimex lectularius L (Hemiptera) in relation to climate, with
observations on the effects of preconditioning to temperature.
Parasitology 32:127–173
Johnson CG (1942) The ecology of the bed-bug, Cimex lectularius L.,
in Britain. J Hyg 41:345–361
Jones RM (1930) Some effects of temperature and humidity as factors
in the biology of the bedbug (Cimex lectularius Linn.). Ann
Entomol Soc Am 23:105–119
Kemper H (1936) Die Bettwanze und ihre Bekämpfung. Z Kleintierk
Pelztierk 12:1–107
Kerth G, König B (1999) Fission, fusion and nonrandom associations
in female Bechstein’s bats (Myotis bechsteinii). Behaviour
136:1187–1202
Kerth G, Weissmann K, König B (2001) Day roost selection in
female Bechstein’s bats (Myotis bechsteinii): a field experiment
to determine the influence of roost temperature. Oecologia
126:1–9
Lewis SE (1995) Roost fidelity of bat: a review. J Mammal 76:481–
496
Lewis SE (1996) Low roost-site fidelity in pallid bats: associated
factors and effect on group stability. Behav Ecol Sociobiol
39:335–344
Lourenço SI, Palmeirim JM (2005) Influence of temperature in roost
selection by Pipistrellus pygmaeus (Chiroptera): relevance for the
design of bat boxes. Biol Conserv 119:237–243
Lučan R (2006) Relationship between the parasitic mite Spinturnix
andegavinus (Acari: Spinturnicidae) and its bat host, Myotis
daubentonii (Chiroptera: Vespertilionidae): seasonal, sex- and
age-related variation in infestation and possible impact of the
parasite on the host condition and roosting behaviour. Folia
Parasitol 53:147–152
Mellanby K (1932) Effects of temperature and humidity on the
metabolism of the fasting bed-bug (Cimex lectularius). Parasitology
24:419–428
Omori N (1941) Comparative studies on the ecology and physiology
of common and tropical bed bugs, with special references to the
reactions to temperature and moisture. Journal of the Medical
Association of Taiwan 60:555–729
Péricart J (1972) 7. Hémiptères anthocoridae, cimicidae et microphysidae
de l’Ouest-Paléartique. Faune de l’Europe et du Bassin
Méditerranéen. Mason et Cue Édit., Paris
Péricart J (1996) Family cimicidae. In: Aukema B, Rieger Ch (eds)
Catalogue of the heteroptera of the Palearctic region. Nederlandse
Entomologische Vereiniging, Wageningen, pp 141–144
Povolný D (1957) Kritická studie o štěnicovitých (Het. Cimicidae) v
Československu. (A critical study on bugs (Heteroptera, Cimicidae)
in Czechoslovakia). Zool Listy 6:59–80 (in Czech with a
summary in Russian)
Reinhardt K, Siva-Jothy MT (2007) Biology of the bed bugs
(Cimicidae). Annu Rev Entomol 52:351–374
Ritzi CM, Whitaker JO Jr (2003) Ectoparasites of small mammals
from the Newport chemical depot, Vermillion county, Indiana.
Northeastern Naturalist 10:149–158
Ritzi CM, Ammerman LK, Dixon MT, Richerson JV (2001) Bat
ectoparasites from the Trans-Pecos region of Texas, including
notes from Big Bend National Park. J Med Entomol 38:400–404
Rivnay E (1932) The influence of relative humidity upon the rate of
development of the bed bug C. lectularius L. Bull Soc Roy
Entomol d’Egypte 16:13–16
Ryckman RE, Bentley DG, Archbold EF (1981) The Cimicidae of the
American and oceanic islands. A checklist and bibliography. Bull
Soc Vector Ecol 6:93–142
Swift SM (1980) Activity patterns of pipistrelle bats (Pipistrellus
pipistrellus) in north–east Scotland. J Zool Lond 190:285–295
Thomas DW (1995) Hibernating bats are sensitive to nontactile human
disturbance. J Mammal 76:940–946
Thompson MJA (1990) The pipistrelle bat Pipistrellus pipistrellus
Schreber on the Vale of York. Naturalist 115:41–56
Usinger RL (1966) Monograph of Cimicidae (Hemiptera–Heteroptera).
Thomas Say Foundation, vol 7. Entomological Society of
America, New York
Vonhof MJ, Barclay RMR (1996) Roost-site selection and roosting
ecology of forest-dwelling bats in southern British Columbia.
Can J Zool 74:1797–1805
Walter G (1996) Zum Ektoparasitenbefall der Fledermäuse und den
potentiellen Auswirkungen. Myotis 34:85–92
Webb PI, Speakman JR, Racey PA (1996) Population dynamics of a
maternity colony of the pipistrelle bats (Pipistrellus pipistrellus)
in north–east Scotland. J Zool Lond 240:777–780
Parasitol Res (2007) 100:1323–1330 1329
Wendt A (1941) Familie Cimicidae Latreille, 1804. In: Gulde J (ed) Die
Wanzen Mitteleuropas. P. O. H. Werde, Frankfurt a. M, pp 119–131
Whitaker JO (1998) Life history and roost switching in six summer
colonies of eastern pipistrelles in buildings. J Mammal 79:651–659
Whitaker JO, Mumford RE (1978) Food and ectoparasites of bats
from Kenya, East Africa. J Mammal 59:632–634
Whitaker JO Jr, Deunff J, Belwood JJ (2000) Ectoparasites of neonate
Indiana bats, Myotis sodalis (Chiroptera: Vespertilionidae), with
description of male of Paraspinturnix globosa (Acari: Spinturnicidae).
J Med Entomol 37:445–453
Willis CKR, Brigham RM (2004) Roost switching, roost sharing and
social cohesion: forest-dwelling big brown bats (Eptesicus
fuscus) conform to the fission–fusion model. Anim Behaviour
68:495–503
Wolz I (1986) Wochenstuben-Quartierewechsel bei der Bechsteinfledermaus.
Z Säugetierk 51:65–74
1330 Parasitol Res (2007) 100:1323–1330
BARTONIČKA T., 2010
Survival rate of bat bugs (Cimex pipistrelli, Heteroptera) under different microclimatic
conditions.
Parasitology Research, 107:827–833.
ORIGINAL PAPER
Survival rate of bat bugs (Cimex pipistrelli, Heteroptera)
under different microclimatic conditions
Tomas Bartonicka
Received: 12 March 2010 /Accepted: 26 May 2010 /Published online: 11 June 2010
# Springer-Verlag 2010
Abstract Survival of facultative ectoparasites, e.g. bed
bugs (Cimex spp.), is more intensely affected by climatic
factors, namely temperature, than that of permanent
ectoparasites. The ontogenetic time of the bat bug (Cimex
pipistrelli) in bat roosts is limited by different survival rates
under different temperatures in particular nymphal stages.
This limitation could affect bug densities and cause
asynchrony between the ectoparasite and bat reproductive
cycle. Therefore, bug survival under different temperatures
was tested in the laboratory. Survival success was evaluated
by three types of survival analyses: Kaplan–Meier estimation,
the Cox proportional hazards model and Weibull
parametric regression. The bugs survived for only a few
hours at 45°C; however, such a high temperature was never
found in natural roosts. Different survival probability
among different ontogenetic stages was found at the
temperatures of 5–35°C, and it was the highest in adult
females and nymphs of fourth and fifth instar. Early instars
first to third were found to be the most sensitive with the
highest mortality of all stages studied and having their best
survival at 5°C. The hazard rate ratio of Weibull regression
shows the low daily failure rate of 2.23–4.34% within the
span of 5–35°C. C. pipistrelli had the shorter life cycle and
the better survival at higher temperature (35°C) than C.
lectularius. The ability of the former to survive high
temperatures could be the consequence of its long-term
coexistence with bats preferring crevice-like roosts or attics
which become overheated during the summer months.
Introduction
Fast ontogenesis, high reproductive potential, mobility and,
at the same time, a hidden way of life make bugs
(Cimicidae) important ectoparasites. All species of this
family inhabit the shelters of warm-blooded animals, but
mostly without physical contact with their hosts. They fully
engorge in 10 to 20 min, after which they return to their
refugium (Usinger 1966). Up to the present, studies
concerning the life history of bugs have dealt mainly with
species which are usually human parasites and vectors of
more than 40 human diseases (Cimex lectularius and Cimex
hemipterus, Hwang et al. 2005; Goddard and deShazo
2009). Neglected, though more abundant in central Europe,
are bugs from the species group Cimex pipistrelli, obligatory
ectoparasites, wholly associated with bats or birds
(Reinhardt and Siva-Jothy 2007). A high bat bug population
density in a roost soon after its settlement by bats is
caused by synchronisation of the ectoparasite density with
the reproductive cycle of bats (Bartonička 2008). Roost
switching in bats during one season is well-known and
seems to be an anti-parasite strategy with respect to bat
bugs (Bartonička and Gaisler 2007). The authors showed
that the absence of bats in satellite roosts during the
lactation period, coupled with high temperatures and
natural mortality of parasites, reduced the number of bat
bugs and their ontogenetic stages in bat boxes to less than
half the initial number. According to the present state of
knowledge, two climatic factors, temperature and humidity
seem to have the largest impact on bugs survival (Usinger
1966). The effect of humidity, however, is quite incalculable
and could only have been discovered by investigations
in the laboratory (Rivnay 1932). Usinger (1966) demonstrated
that temperature and humidity significantly affect
survival of all ontogenetic stages and also the relative
T. Bartonicka (*)
Department of Botany and Zoology, Masaryk University,
Kotlářská 2,
611 37 Brno, Czech Republic
e-mail: bartonic@sci.muni.cz
Parasitol Res (2010) 107:827–833
DOI 10.1007/s00436-010-1935-6
promptness to copulation in bed bugs (C. lectularius).
However, it is generally stated that bed bugs are very little
affected by different degrees of humidity (Kemper 1936).
Rivnay (1932) tested the effect of humidity (10–70%) on
the ontogeny of C. lectularius nymphs. He found only
small insignificant differences in life cycles and assumed
the humidity effect was negligible. Nevertheless, direct
correlation between temperature and relative humidity is
well-known. However, up to the present, only few surveys
have dealt with ecological relations between temperature
and survival of particular instars after starvation periods of
various lengths (cf. Funakoshi 1977; Overal 1980). Previous
studies showed high tolerance towards dehydration (up
to 40% loss in body water) and a desiccation hardiness
against high temperatures (35–40°C; Dubinin 1947; Southwood
1954). Early instars with higher body water content
could have worse survival under high temperatures in
climatically extreme conditions of natural bat roosts (Jones
1930; Johnson 1960; Usinger 1966). In general, bugs prefer
lower temperatures than do other bat ectoparasites which
live on their hosts' bodies permanently (Usinger 1966).
Reinhardt et al. (2008) compared the temperature in a roost
of the fruit bat (Rousettus aegyptiacus) and in the refugia of
its ectoparasite, the cimicid bug Afrocimex constrictus.
They found that bugs preferred moving several metres to
staying together with fruit bats and risked suboptimal
conditions in which they were unlikely to reproduce. Even
relatively small temperature differences can be translated
into ectoparasite fecundity.
Surviving water and temperature stress considerably
prolonged periods of inactivity, hence the readiness for
sucking could be different within particular ontogenetic
stages. We examined all stages of C. pipistrelli to illustrate
their survival shift under a wide range of temperature
conditions, to pinpoint the stage which is most or least
vulnerable.
Material and methods
Bat roosts and sampling of bat bugs
Bat bugs (C. pipistrelli) were sampled from two nursery
colonies of mouse-eared bats (Myotis myotis) roosted under
roofs of the castles in Jevišovice and Luhačovice (south
Moravia, Czech Republic). Both populations of bat bugs
belong to the haplotype B group that is very homogenous
throughout central Europe (Balvín 2008). Bugs were
collected with soft forceps and exhaustors into small plastic
boxes (10×10×5 cm) lined with soft paper. A Hobo Data
Logger (Onset Computer Corporation, USA), continuously
recording the temperature and relative humidity, was
situated at the site of the highest density of bat bugs under
the roof of the Jevišovice castle during the growing season
2007 (April–October). Microclimatic data were used to
design experiments in the laboratory.
Equipment and experimental settings
The sampled bat bugs were manually divided by instars and
sex and placed in laboratory containers using a binocular
following the method by Stutt and Siva-Jothy (2001). To
sort the samples according to developmental stages and sex
safely and reliably using tweezers and to transfer the
insects into experimental tubes, individual bat bugs were
immobilised by sudden “freezing” at 0°C for 10 min.
Particular instars would be very difficult to breed separately
because of their metamorphosis over several days.
Therefore, they were divided into four groups as follows:
mixed age, viz, first–third instar, fourth–fifth instar, adult
males and adult females. They were kept in glass tubes, ten
bugs in each. The tubes were plugged with mineral cottonwool
swabs to enable air circulation between the tube and
thermostat atmosphere. All bugs were fed at the beginning
of experiments with blood of a specific host (M. myotis).
All groups of bat bugs were exposed to typical temperatures
that occur during the growing season in their natural
shelters (5, 20, 25, 30, 35, 40 and 45±0.5°C). Kemper
(1936) showed that dry conditions (relative humidity 0–
20%) during ecdysis often leads to high mortality of
nymphs. A somewhat high and stable relative humidity of
65–75%, typical for natural bat roosts, was therefore fixed
for all experimental bug groups (see Fig. 1). Numbers of
dead bugs were monitored each day. To test the promptness
to suck blood after a period of starvation, when mortality
exceeded 50% in each bug group, the box with one adult
non-reproducing female M. myotis and a sample of the
remaining bugs were placed together in a thermostat (30°C)
for 20 min (cf. Giorgi et al. 2004). After the feeding period,
all bugs were removed from the box and collected from the
bat. Their numbers and feeding status were determined.
Collecting five bugs took about 30 s as they were clearly
visible on the wings and tail membrane of the bat. In total,
five non-reproducing females were used to test the
promptness to suck and bats were changed after feeding
each two bug groups. Bats were fed ad libitum with a
mixed diet consisting of crickets (Acheta sp.) and mealworms
(Tenebrio molitor) and after experiments returned
back to the colony. The bats were captured, handled and
temporarily kept in captivity under the licence no. 922/93OOP/2884/93
and 137/06/38/MK/E/07 of the Ministry of
Environment of the Czech Republic. The author has been
authorised to manipulate with free-living bats according to
the certificate of competency no. 104/2002-V4 (§ 17 of the
law no. 246/1992). Experiments were carried out between
April and August in 2007 and 2008.
828 Parasitol Res (2010) 107:827–833
Statistical analysis
All variables showed a normal distribution after log transformation.
Statistica for Windows 8.0 was used for data analyses.
Survival analyses and GLM were used to compare the
changes in survival among particular age classes and
temperature. Survival was evaluated during 1 month as this
corresponds to the period of bat absence from the crevice-like
roosts (cf. Bartonička and Gaisler 2007) and/or using other
ectoparasite free sites within large attics (own unpubl. data).
A mortality of 50% in a sample was considered significant to
finish the experiment, and such a session was marked as
complete in the database. Other groups were evaluated as
censored. The differences among temperatures and age
groups were tested using the Kaplan–Meier survival functions.
For the Cox proportional hazards model and Weibull
regression, the Chi-square value was estimated as a function
of the log-likelihood for the model with all covariates. It was
suspected that the effect of the treatment (exposure to
different temperatures) on the underlying hazard was not
constant, that is, that the proportionality assumption may be
violated. To test whether this assumption was tenable, a
model was fitted to the data that included the fixed covariate
“temperature”. We tested only data concerning the first–third
instar because of their high influence by temperature (see
Fig. 2, Kaplan–Meier tests).
Material
During two growing seasons, a total of 840 bat bugs were
collected in bat roosts. Each experiment (at one temperature)
was repeated three times (3×10 bat bugs). For
experiments with seven different temperatures, 210 individual
bat bugs in each age group were used, viz, first–third
instar, fourth–fifth instar, adult males and adult females, as
mentioned above.
0
5
10
15
20
25
30
35
40
45
13-Mar 2-Apr 22-Apr 12-May 1-Jun 21-Jun 11-Jul 31-Jul 20-Aug 9-Sep 29-Sep 19-Oct
temperature(°C)
0
10
20
30
40
50
60
70
80
90
100
13-Mar 2-Apr 22-Apr 12-May 1-Jun 21-Jun 11-Jul 31-Jul 20-Aug 9-Sep 29-Sep 19-Oct
relativehumidity(%)
Fig. 1 Temperature (°C) and
relative humidity (%) measured
at sites with high bat bug density
under the roof of Castle
Jevišovice
Parasitol Res (2010) 107:827–833 829
Fig. 2 Cumulative survival functions for age groups of bat bugs,
showing the fraction surviving in relation to the different temperature.
Kaplan–Meier survival functions for T 5°C, χ2
=10.15, n.s. (a); T 20°C,
χ2
=39.19, p<0.001 (b); T 25°C, χ2
=66.99, p<0.001 (c); T 30°C, χ2
=
124.77, p<0.001, however, M adults and fourth to fifth instar had same
dynamic (d); T 35°C, χ2
=58.14, p<0.001 (e); T 40°C, χ2
=1.56, n.s.
(f); and T 45°C, χ2
=0.77, n.s. (g). “Complete” means at least 50%
mortality in the particular bug group
830 Parasitol Res (2010) 107:827–833
Results
Changes in the microclimate of bat roosts
In bat roosts, the internal temperature was usually <30°C
and, only in two cases, the maximum internal temperature
reached 41–42°C. Very low temperatures (5°C) were found
during April and September. The relative humidity varied
between 25% and 75%. High humidities correlated with
rainy days during the second half of May and in July and
September (Fig. 1).
Survival at different temperatures
Survival among particular age groups at different temperatures
was tested using GLM. Different changes were found
only in temperatures between 20°C and 35°C, i.e. T 20°C
(GLM, F=10.68, p<0.002), T 25°C (F=166.83, p<0.001),
T 30°C (F=352.92, p<0.001) and T 35°C (F=126.42, p<
0.001). Apparent Kaplan–Meier estimates are presented for
each temperature and age group. Survival probabilities
among different ages were highest in adult females and
groups of fourth and fifth instar (Fig. 2). At T 5°C and
20°C, the survival probability of fourth and fifth instar was
even higher than in adult bugs. However, survival under
high temperatures, i.e. 40°C and 45°C, was the lowest in all
age groups (5±1 days at 40°C and 3.7±0.2 days at 45°C for
50% of mortality). The most vulnerable stage was the age
group first–third instar, which displayed the highest
mortality in general. Their best survival was found at T
5°C (50% mortality within 21 days). The difference between
the temperature survival of early instars (first–third) is due to
the assumption in the Cox model that the ratio of the hazard
rates is not constant over time and temperature (χ2
=256.66,
df=6, p<0.001).
The daily mortality rate estimated hazard rate functions
as predicted by the Weibull regression model for all tested
temperatures. The Weibull model showed a similar hazard
rate ratio for the first–third instars in temperature ranges of
5–35°C while higher temperatures caused the hazard rate to
increase (Fig. 3). The hazard rate ratio in relation to date
(treated as a linear variable for temperatures of 5°C to 35°C),
increased the daily failure rate by 2.23–4.34% (95% CI, p<
0.001) per day, but at T 40°C and 45°C, an increase was
found with mean daily failure of 12.10% and 22.06%
(treated as a logarithmic) per day.
Concerning the relative promptness to suck blood in bat
bugs of different age and sex after starvation periods,
significant differences were found in first–third instars
(ANOVA, F=5.77, df=24, p=0.003), in fourth–fifth instars
(F=8.95, df=24, p=0.001) and adult males (F=5.13, df=
24, p=0.006). In these age groups, temperature negatively
correlated with relative promptness to suck blood (Pearson
correlation coefficient; first–third instars, r=−0.81, p<0.05;
fourth–fifth instars, r=−0.78, p<0.05; adult males, r=−0.56,
p<0.05). Adult females had high promptness to suck even at
high temperatures.
Developmental changes
Changes in nymphal development at various constant
temperatures were tested. On temperature gradient plate of
5–40°C, it was found that C. pipistrelli had the shortest
development at 35°C (mean 21.1 days). In general, the third
and fourth instars needed the shortest time period between
ecdyses at all constant temperatures (Table 1). Low
temperatures (5°C, 20°C) prolonged the time between two
ecdyses and increased the survival probability.
Discussion
Ambient temperature is well-known to be by far the most
important environmental factor affecting all aspects of the
activities of these insects, e.g. nymphal development,
timing of ecdysis or feeding. There are only few bat roosts,
e.g. warm caves in the tropics, where the fluctuation of
temperature during day or year is so uniform that it does not
affect the rate of vital activities of bugs (Usinger 1966).
Results of experiments showed that bug survival, especially
of adults, is highest at low temperatures (5°C, 20°C). This
is an important point contributing to survival over the
0,0
0,1
0,2
0,3
0,4
0,5
0,6
0,7
0,8
0 10 20 30 40
days
Dailymortalityrate
T 5
T 20
T 25
T 30
T 35
T 40
T 45
Fig. 3 Daily mortality rate of early instars predicted by the Weibull
regression model for all tested temperatures, treated as a linear
variable for temperatures between 5°C and 35°C and as a logarithmic
model for temperatures 40°C and 45°C
Parasitol Res (2010) 107:827–833 831
winter; it is also found in other insect groups (e.g. Lee
1991). Hase (1930) noted the threshold for cessation of all
bug metabolic activities to be between 13°C and 15°C,
though they can tolerate even lower temperatures for brief
periods. In general, adult females had the best survival, and
early instars were the most vulnerable to temperature.
Although bugs are well-known to have high tolerance of
drying, they died of water deficiency associated with lower
relative humidities (0–60%). In particular, survival of early
instars rapidly decreases with decreasing humidity (Mellanby
1935). The low survival rate of adult males is similar to
that of early instars, in contrast to the best survival of
adult females. This might correlate with an unknown sexbiased
factor (e.g. immunodepression after mating, female
guarding, etc.).
The mere ability to survive extreme life conditions such
as high temperature or long periods without feeding does
not evidence completely the viability of a starving bug
population. To safely approach the host and maintain
readiness to suck blood are no less important. Success in
blood sucking may not be trivial because of the high
mobility of bats in roosts, their antiparasitic behaviour or
host unavailability during its day torpor (Bartonička 2008).
Experiments showed that early nymphs and probably adult
males, which survive longer without a host, are often
unable to find it and suck. Adult females were more
efficient, and a high percentage of the survivors sucked.
This ability of adult females explains their position as the
most often recorded bug stage on netted bats. For the same
reason, adult females are the optimum vector and founder
of a bug colony in a new still uninfested bat roost
(Reinhardt and Siva-Jothy 2007).
In bat boxes, bugs survive the temporal host absence as
eggs (Bartonička and Gaisler 2007), and this period is, at
the same time, usually the hottest. If the first instars
hatched, e.g. 1 week before the return of bats to the roost
and under high temperatures (40°C), their mortality would
be 50% during the next 5 days. Development timing, i.e.
keeping synchronisation of the bug density with the
reproductive cycle of bats, is a very important ectoparasite
life strategy. This strategy, therefore, could represent a
mechanism facilitating early development from eggs, as
described in flies (Reckardt and Kerth 2007).
The thermal death point was found between 44°C and
45°C (Omori 1941), but our present results showed that
development of all stages of C. pipistrelli ceased at 40°C.
Such a high temperature (40°C) was observed in bat roosts
only rarely, but no simultaneous decrease in bug numbers
was found (cf. Bartonička and Gaisler 2007). Therefore, bat
bugs are probably able to roost in thermally more
favourable sites, usually cooler, with temperatures different
among ontogenetic stages. Different survival rates with
respect to the temperature gradient could lead to an agerelated
microhabitat segregation (O. Balvín unpubl. data).
Temperature-sensitive sensors present on the bug antenae,
and mobility of bugs very likely enable them to determine
thermally favourable sites and move there (Sioli 1937).
The less specific requirements for roost conditions found
in bed bugs C. lectularius led us to anticipate a similar
dependency of survival on temperature gradient in C.
pipistrelli (Usinger 1966). Both species are frequent roost
ectoparasites of bats. C. pipistrelli parasites mainly on
crevice-dwelling bats Pipistrellus pipistrellus and Nyctalus
noctula switching their roosts several times per growing
season. In contrast, C. lectularius parasites usually on M.
myotis, which is more faithful to one roost (Audet 1990).
Sun-exposed roosts in buildings are well-known for
extreme temperature fluctuations (Kunz and Fenton 2003).
Therefore, bat bugs could be more tolerant to the high
temperatures. The results of this study showed that C.
pipistrelli has the shortest development at higher constant
temperature (ca. 35°C), while C. lectularius matures
quicker at 30°C (Usinger 1966). At temperatures >30°C,
its development slowed and ceased completely at 36°C
(Omori 1941). The efficiency of C. pipistrelli to tolerate
high temperatures could be the consequence of its longterm
coexistence with bats preferring crevice-like roosts in
both trees and buildings but also to more spacious attics
becoming overheated during the summer months. Direct
observations of bat bugs in reproduction colonies of M.
myotis show that, as long as the temperature does not
exceed the thermal death point, the cause of the decrease in
population density is not only temperature, but the absence
of bat hosts at the same time. Usually, the bats left their
roosting places and moved either to cooler sites or those
with less or no bug infestation, often in the same building.
T (°C)/stage 1st 2nd 3rd 4th 5th Total days
5 33.2 29.3 26.7 24.8 41.9 155.9
20 21.0 19.0 16.0 20.4 28.9 105.3
25 8.5 7.6 6.1 5.6 9.4 37.2
30 6.1 4.2 3.1 4.7 6.3 24.4
35 5.1 3.2 3.1 4.5 5.3 21.2
40 5.0 6.2 unfinished [5] unfinished [4] 5.2 24.4
Table 1 Total period of mean
development of C. pipistrelli at
various constant temperatures
T 45°C was excluded because of
the high mortality of all instars.
At T 40°C, the number of days
in brackets are estimates, as
most nymphs died before
metamorphosis
832 Parasitol Res (2010) 107:827–833
Acknowledgements I am very grateful to K. Zednikova for her
excellent assistance in the laboratory and to J. Gaisler and W. G. Filby
for valuable comments on the manuscript. The study was supported by
grant no. 206/07/P098 of the Science Foundation of the Czech
Republic and the Czech Bat Conservation Trust, and by grants from
the Ministry of Environment and the Ministry of Education, Youth and
Sports of the Czech Republic No. MSM0021622416.
References
Audet D (1990) Foraging behaviour and habitat use by a gleaning bat,
Myotis myotis (Chiroptera: Vespertilionidae). J Mammal 71:
420–427
Balvín O (2008) Revision of the West Palaearctic Cimex species.
Preliminary report. Bull Insec 61:129–130
Bartonička T (2008) Cimex pipistrelli (Heteroptera, Cimicidae) and
the dispersal propensity of bats: an experimental study. Parasitol
Res 104:163–168
Bartonička T, Gaisler J (2007) Seasonal dynamics in the numbers of
parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost
switching in bats (Chiroptera, Vespertilionidae). Parasitol Res
100:1323–1330
Dubinin VB (1947) Ekologicheskie nabludeniya nad krovososushchimi
klopami sem. Cimicidae Daurskoi stepi. Entomol Oboz
29:232–246
Funakoshi K (1977) Ecological studies on the bats fly, Penicillida
jenynsii (Diptera. Nycteribiidae), infesting the Japanese longfingered
bat, with special reference to their adaptation to the life
cycle of their hosts (in Japanese). Jap J Ecol 27:125–140
Giorgi MS, Arlettaz R, Guillaume F, Nusslé S, Ossola C, Vogel P,
Christe P (2004) Causal mechanisms underlying host specificity
in bat ectoparasites. Oecologia 138:648–654
Goddard J, deShazo R (2009) Bed bugs (Cimex lectularius) and
clinical consequences of their bites. JAMA 30:1358–1366
Hase A (1930) Weitere Versuche zur Kenntnis der Bettwanzen Cimex
lectularius L. und Cimex rotundatus Sign. (Hem.-Rhynch.). Z
Parazitenk 2:368–418
Hwang SW, Svoboda TJ, De Jong IJ, Kabasele KJ, Gogosis E (2005)
Bed bug infestations in an urban environment. Emerg Infect Dis
11:533–538
Johnson CG (1960) The relation of weight of food ingested to increase
in body-weight during growth in the bed-bug, Cimex lectularius
L. (Hemiptera). Ent Exp Appl 3:238–240
Jones RM (1930) Some effects of temperature and humidity as factors
in the biology of the bedbug (Cimex lectularius Linn.). Ann
Entomol Soc Am 23:105–119
Kemper H (1936) Die Bettwanze und ihre Bekämpfung. Z Kleintierk
Pelztierk 12:1–107
Kunz TH, Fenton MB (2003) Bat Ecology. The University of Chicago
Press, Chicago, IL
Lee RE Jr (1991) Principles of insect low temperature tolerance. In:
Lee RE Jr, Denlinger DL (eds) Insects at low temperature.
Chapman & Hall, New York, pp 17–46
Mellanby K (1935) A comparison of the physiology of the two species
of bed-bug which attack man. Parasitology 31:111–122
Omori N (1941) Comparative studies on the ecology and physiology
of common and tropical bed bugs, with special references to the
reactions to temperature and moisture. J Med Ass Formosa
60:555–729
Overal WL (1980) Host-relations of the bat fly Megistopoda aranea
(Diptera: Streblidae) in Panama. Univ Kans Sci Bull 52:1–20
Reckardt K, Kerth G (2007) Roost selection and roost switching of
female Bechstein's bats (Myotis bechsteinii) as a strategy of
parasite avoidance. Oecologia 154:581–588
Reinhardt K, Siva-Jothy MT (2007) Biology of the bed bugs
(Cimicidae). Annu Rev Entomol 52:351–374
Reinhardt K, Naylor RA, Siva-Jothy MT (2008) Temperature and
humidity differences between roosts of the fruit bat, Rousettus
aegyptiacus (Geoffroy, 1810), and the refugia of its ectoparasite,
Afrocimex constrictus. Acta Chiropterol 10:173–176
Rivnay E (1932) The influence of relative humidity upon the rate of
development of the bed bug C. lectularius L. Bull Soc Roy
Entomol Egypte 16:13–16
Sioli H (1937) Thermotaxis und Perzeption von Wärmestrahlen bei
der Bettwanze (Cimex lectularius L.). Zool Jahrb Physiol
Morphol Tiere 58:284–296
Southwood TRE (1954) The production of fertile eggs by Cimex
pipistrelli Jenyns 1839 (Hem. Cimicidae) when fed on human
blood. Entomol Mon Mag 90:35
Stutt AD, Siva-Jothy MT (2001) Traumatic insemination and sexual
conflict in the bed bug Cimex lectularius. PNAS 98:5683–5687
Usinger RL (1966) Monograph of Cimicidae (Hemiptera–Heteroptera).
Entomological Society of America, New York
Parasitol Res (2010) 107:827–833 833
BARTONIČKA T. & RŮŽIČKOVÁ L., 2013
Recolonization of bat roost by bat bugs (Cimex pipistrelli): could parasite load be a cause of
bat roost switching?
Parasitology Research, 112: 1615–1622.
ORIGINAL PAPER
Recolonization of bat roost by bat bugs (Cimex pipistrelli):
could parasite load be a cause of bat roost switching?
Tomáš Bartonička & Lucie Růžičková
Received: 18 October 2012 /Accepted: 21 January 2013 /Published online: 6 February 2013
# Springer-Verlag Berlin Heidelberg 2013
Abstract Roost ectoparasites are believed to have a negative
impact on fitness of their hosts as birds or mammals.
Previous studies were mostly focussed on the synchronization
between reproduction cycles of ectoparasites and hosts
living in infested roosts. However, to date, it has not been
examined how fast ectoparasites colonize new, non-infested
roosts and thus increasing the impact on the local populations
of hosts. The parasite–host model was studied, including
bat bugs Cimex pipistrelli and soprano pipistrelles
Pipistrellus pygmaeus, where bat behaviour was observed
which tended to reduce the parasite load in bat roosts. We
investigated (1) whether bats change their roosting behaviour
when we discontinued synchronization of their reproduction
and the life cycle of the bat bugs and (2) how fast
and which stages of bat bugs reoccupy cleaned roosts. In a
3-year field experiment, we removed all bat bugs from six
bat boxes in each spring. Pipistrelles bred young in all noninfested
boxes during these 3 years. In addition, 8 years of
regular observations before this experiment indicate that
bats avoided breeding in the same bat boxes at all. Bat bugs
were found again in clean boxes in mid-May. However, their
densities did not maximise before the beginning of June,
before parturition. A re-appearance of bugs was observed
after 21–56 days after the first bat visit. Adult bugs, mainly
females, colonised cleaned boxes first though at the same
time there were a lot of younger and smaller instars in nonmanipulated
roosts in the vicinity.
Introduction
Roosts and their availability play a crucial role in bat ecology
(e.g. Russo et al. 2004). Females have evolved to spend
at least part of their lives roosting together in nursery colonies.
Regarding the different requirements during reproduction,
there is growing interest in identifying roosting
strategies (Kunz and Lumsden 2003). A number of studies
have provided critical insights into roost switching and have
suggested several reasons for why bats change roosts, i.e. to
minimize the costs of thermoregulation (e.g. Kerth et al.
2001, Willis and Brigham 2005), to reduce the risk of
predation (Vonhof and Barclay 1996) and to allow for an
optimal group size and increased survival (e.g. Barclay and
Kurta 2007). Roost switching in bats is often phenomenon,
is known as fission-fusion (Kummer 1971), where a social
unit of roosting bats may split into several subunits when the
bats select their diurnal roosts (e.g. O’Donnell 2000). Under
this scenario, roost sharing and switching between roosts
within a local area could serve to increase the knowledge of
potential trees for roosting and/or maintain cohesiveness of
the colony (e.g. Willis and Brigham 2004).
However, pipistrelles do not switch roosts as many times
as typical forest species, e.g. Myotis bechsteinii or Eptesicus
fuscus, where the causes of roost switching most probably
relate to the fission-fusion social organization (Kerth and
König 1999; Willis and Brigham 2004), although some
roost selection to avoid ectoparasites was observed in treedwelling
species like M. bechsteinii (Reckardt and Kerth
2007). Pipistrelles usually only switch roosts two to three
times in one season, according to the reproduction phase.
Typically, groups of females leave their respective roosts in
early June and move to the main nursery roost a few days
before parturition. They move back to their previous roosts
with flightworthy juveniles in mid-July (Webb et al. 1996).
Therefore, we think that there may be a cause other than
T. Bartonička (*) :L. Růžičková
Department of Botany and Zoology, Masaryk University,
Kotlářská 2,
61137 Brno, Czech Republic
e-mail: bartonic@sci.muni.cz
L. Růžičková
e-mail: lruzickova@mail.muni.cz
Parasitol Res (2013) 112:1615–1622
DOI 10.1007/s00436-013-3316-4
social demands for this behaviour, which is probably related
to a reduction in the parasite load. When leaving the shelter
should lead to a reduction of parasite load, it is advisable to
find out how long it will take for bugs to occupy new or
abandoned roosts, and when they reach there the maximum
population.
Avoiding infested habitats is known to be the most effective
behavioural parasite defence strategy in order to reduce
costs associated with infestation (e.g. Christe et al. 1994;
Moore 2002). Most studies on bat ectoparasites have dealt
with different species and their ontogenetic stages that permanently
live on their hosts’ bodies (e.g. Gannon and Willig
1995; Giorgi et al. 2001; Dick et al. 2009). These studies are
not sufficient to elucidate the correlation between parasite
load and roosting strategies related to movements within
and outside the shelters. Probably only such strategies could
be effective when avoiding pressure from ectoparasites that
spend on the body of their host a short time only and have
low ability to colonize new host roosts. Therefore, as an
improved model, we chose bat bugs (Cimex pipistrelli)
which, except for the time they spend engorging, mostly
co-habit without physical contact with their hosts and are
rarely found on bats netted out of roosts (Reinhart and SivaJothy
2007).
Currently, it is unknown whether roost switching is an
adaptation for reducing parasite load or whether the observed
decrease in the number of parasites (e.g. Bartonička
and Gaisler 2007) is only a side effect of switching. Prior to
this field experiment, there were no bat boxes and no nonfledged
young bats. Pipistrelles leave the roosts just before
parturition because of a growing parasite load or different
microclimatic demands during pregnancy and lactation
(Bartonička and Řehák 2007). Bats can monitor the level
of roost infestation during their repeated visits during pregnancy
and choose a roost with a relatively low parasite load
or even with none at all (Reckardt and Kerth 2007). The
odour produced by bat bugs is very intense and is probably
easily distinguishable by bats even outside the roost (Usinger
1966). Females become torpid more often during pregnancy
than during lactation, and therefore are less available for bat
bugs (Montes et al. 2002). Populations of bat bugs usually
reach the first gradation at the end of May (Bartonička and
Gaisler 2007). Laboratory experiments showed higher
levels of infestation in young bats than in adults. The
movement of females to non-infested roosts just before
parturition could have an important role in the postnatal
growth of the young and could be seen as a kind
of maternal effect (Kunz and Stern 1995).
We present a field study in which a roost manipulation
experiment was combined with a long-term study on the
roosting strategies of pipistrelles (Pipistrellus pygmaeus).
The aim of our study was to determine whether or not the
removal of bat bugs from infested roosts would lead to a
change in the roost selection pattern and whether or not the
females would bear and wean young in roosts with no bat
bugs. The goal of this paper was to reveal, by a simple field
experiment, what is the speed of (re)colonization of new
roosts and whether or not the parasite load is a possible
cause of roost switching in this particular bat species.
Methods
Study area and technical equipment
Nursery and temporary colonies of P. pygmaeus with high
densities of C. pipistrelli bat bugs were monitored in eight
wooden bat boxes inside the Křivé jezero floodplain forest
and the Bulhary game-hunting ground. Both of these localities
belong to one woodland complex near Milovice village
(Milovice Wood), in southern Moravia, Czech Republic.
Milovice Wood is one of the largest remaining oakwoods
in this part of the north-western fringe of the Pannonian
Basin. All of the bat boxes were regularly observed from the
year 2000: at least once at month. At the beginning of the
season in 2003, all of the bat boxes were equipped with
active infrared gates (IRG, Litschmann and Suchý, AMET,
Czech Republic) or passive IR Trail Monitors, TM (TM550,
TrailMaster, Goodson and Associates, INC., Kansas, USA)
and thermometers (Hobo, Onset Computer Corporation,
Southern MA, USA) to record the presence and/or numbers
of bats and the internal and external temperatures inside/outside
the boxes throughout the seasons. Monitoring of the bat
bugs was carried out by manually sampling from inside the
box roof. In each spring of 2008, 2009 and 2010, we
removed all bat bugs from six bat boxes (three boxes in
the Křivé jezero and three in the Bulhary game-hunting
ground). Only IRGs were used to monitor the bats during
these three seasons. One box in each locality was left alone;
therefore, the normal life cycle of the bugs could proceed. In
January, the manipulated bat boxes were inserted into plastic
bags, to which several drops of benzene were added. The
next day, we returned the bat boxes to their original places in
the field. Hobo Data Loggers, which continuously recorded
the temperature (internal and external) and the internal relative
humidity, were situated under the roof of each bat box.
The sensors that measured the external temperature were
situated about 50 cm apart on each box. The relative humidity
sensor had an accuracy of ±4 %, and the temperature
sensor had an accuracy of ±0.4 °C. All bat boxes were
regularly monitored over 10-day periods just before the
end of July to limit the effect of human disturbance. Each
sample of bat bugs was divided into four groups: (1) adults,
males and females, (2) first to third instars, (3) fourth and
fifth instars, and (4) eggs (cf. Bartonička and Gaisler 2007).
The number of bugs in each group was recorded. The
1616 Parasitol Res (2013) 112:1615–1622
number of young present was evaluated. The reproductive
season studied was divided into three parts: pregnancy (up
until June), lactation (7 June to 6 July) and post-lactation
(from 7 July). In each season, the time of parturition (8 June
2008, 3 June 2009 and 15 June 2010) was indicated by the
presence of the first newborns.
Statistical analysis
All variables showed a normal distribution after log transformation
(Kolmogorov–Smirnov test). Statistics for Windows
9.0 was used for the data analyses (GLM, ANOVA,
logistic regression). The level of returning and emerging bat
activity (returning from foraging flights at 1:00–5:00 a.m.;
Trail Monitors) positively correlated with the number of bats
(IRG) found in the boxes (Pearson’s correlation coefficient,
r=0.81, P<0.05); therefore, the number of bats roosted in
boxes during the day could be estimated. Analysis of variance
(repeated measures ANOVA) was used to check for differences
between the levels of bat activity, and logistic regression
was used to test for changes in occupancy in the manipulated
and non-manipulated bat boxes. Logistic regression was also
used to check for differences between the internal temperature
and bat numbers in different bat boxes.
Material
During the three seasons of 2008–2010, the six manipulated
bat boxes occupied by soprano pipistrelles (P. pygmaeus) were
monitored for 660 (2008, 110 days/box), 732 (2009,
122 days/box) and 780 (2010, 130 days/box) days, and two
non-manipulated bat boxes for 216 (2008, 108 days/box), 194
(2009, 97 days/box) and 238 (2010, 119 days/box) days,
respectively. On each day, hourly values of internal and external
temperature, internal humidity and the level of the bat
activity (presence/absence of bats, number of bats throughout
the day, night exploring activity) were recorded. Samples of
bat bugs (C. pipistrelli) were taken on 11 (2008), 9 (2009) and
13 (2010) occasions in each bat box. In addition, monthly
observations of the numbers of bats and bat bugs were available
for the 8 years preceding the present experimental study.
Results
Seasonal changes in occupancy of the bat boxes
No significant differences in number of bats were found
between two localities (Křivé jezero and Bulhary), the seasons
when the bat bugs were removed (GLM, F=0.871, NS,
df=2,154; effect of bat box, Tukey test, F=0.827, NS; effect
of season, F=0.329, NS) and among years when boxes were
not manipulated (GLM, F=0.331, NS, df=642; effect of bat
box, Tukey test, F=0.016, NS; effect of season, F=0.771,
NS), thus allowing us to pool the data to the two groups, i.e.
manipulated and non-manipulated. Logistic regression
showed significant differences in the patterns of bat box
occupancy between the manipulated and non-manipulated
boxes (F(1, 2,171)=30.48, p<0.001; Fig. 1).
Exploration activity of the bats and bug transport
The use of infrared gates allowed us to evaluate the numbers of
bats that roosted in the bat boxes during the daytime, when the
bugs could suck onto the bats, but also the level of bat exploration
activity overnight, when the bat bugs could be transported
to clean boxes. Although the bats were not observed in
manipulated bat boxes during the lactation period, a high
exploration activity was noted during most of the nights. When
we tested the exploration activity between the manipulated and
non-manipulated bat boxes, significant differences were found
(logistic regression; F(1, 2,171)=4.62, p=0.032; Fig. 2).
In the non-manipulated boxes, from which bat bugs were
not removed, two peaks in bat numbers were observed—at the
end of May and at the end of July (Fig. 1). Although there
were many overnight visits by the bats (Fig. 2b), no young
were found in these boxes in any of the three experimental
years. The manipulated bat boxes were re-occupied by adult
bugs, mainly females, whereas many first to third instars were
observed in the non-manipulated boxes. The first bat bugs
were usually found in manipulated boxes from mid-May to
mid-June (21 May in 2008, 13 May in 2009 and 16 June in
2010) 21–56 days after the first bats had flown. Other than
adult bugs, we found several first instar individuals, but always
later on in each year. Although bat bugs were observed early in
the growing season in 2008, and even in mid-May, no first
stages of gradation were found, and only the second gradation
stage appeared at the end of July (only in 2008) (Fig. 3).
Microclimatic conditions
Regarding the positions of the non-manipulated bat boxes and
the manipulated boxes in the two forest locations, we determined
how they differed in internal temperature throughout the
daylight hours. Although each of the bat boxes studied differed
in the degree of exposure, no significant difference was found
among the boxes in the daily mean internal, external temperatures
and humidity (ANOVA, F(7, 2,819)=0.69, NS).
Discussion
Different factors lead to roost switching
Day roosts in trees or artificial bat boxes are essential for
tree-dwelling microbats, providing shelter, protection from
Parasitol Res (2013) 112:1615–1622 1617
predators and an appropriate microclimate for energy balancing
and reproduction. Bats often make use of multiple
roosting sites, frequently shifting between roosts. Previous
experimental studies of bat behavioural responses to ectoparasites
indicated that the costs to bats differed, with the
costs caused by ectoparasites found in the roost eliciting a
stronger response than those remaining permanently attached
to the hosts (Côte and Poulin 1995). Therefore,
long-term monitoring data, along with field-based experiments,
were used to examine the influence of roost ectoparasites
on roost selection patterns and roost fidelity. There are
at least three commonly cited causes of roost switching in
vespertilionid bats, i.e. (1) different microclimatic demands
during reproduction, (2) high ectoparasite loads and (3)
social organization, for example the fission-fusion model
(Lewis 1996). However, the pipistrelles left their respective
roosts in early June, a few days before parturition, and
moved back to their previous roosts with flightworthy juveniles
(e.g. Swift 1980; Webb et al. 1996). This behaviour is
different from that found in E. fuscus bats, which were
found to switch roosts every 1.7±0.7 days (Willis and
Brigham 2004). Therefore, the behaviour of the pipistrelles
could not be explained by the fission-fusion model based on
social interactions alone. More probable are movements
related to different microclimatic demands between pregnancy
and the lactation period or parasite load. Willis and
Brigham (2007) calculated that individuals would save 53 %
of their daily energy budget by roosting in a group (45 bats).
20-Apr
25-Apr
30-Apr
5-May
10-May
15-May
20-May
25-May
30-May
4-Jun
9-Jun
14-Jun
19-Jun
24-Jun
29-Jun
4-Jul
9-Jul
14-Jul
19-Jul
24-Jul
29-Jul
date
0
20
40
60
80
numbersofbatsandbatbugs
20-Apr
25-Apr
30-Apr
5-May
10-May
15-May
20-May
25-May
30-May
4-Jun
9-Jun
14-Jun
19-Jun
24-Jun
29-Jun
4-Jul
9-Jul
14-Jul
19-Jul
24-Jul
29-Jul
date
0
20
40
60
80
numbersofbatsandbatbugs
a
b
bats
bugs
Fig. 1 Changes in the numbers
of bats and patterns in the
numbers of all bat bug stages a
in boxes from which the bat
bugs were removed and b in
control boxes from which the
bugs were not removed during
the same seasons; mean—
central tendency, standard
deviation—large box
1618 Parasitol Res (2013) 112:1615–1622
Bartonička and Řehák (2007) tested the microclimatic theory
of pipistrelle movement because the demands between
the pregnancy and lactation periods are completely different.
They assumed that the role of the bat boxes studied was as
“satellite” roosts, separate from a larger communal roost,
that were only occupied during pregnancy and the postlactation
period. They also assumed that the bat boxes were
microclimatically suboptimal roosts because for a few days
in each season the internal temperature exceeded 40 °C, and
the bats left the overheated boxes. Unfortunately, they did
not consider ectoparasite load. We cannot confirm that the
bats could survive in overheated boxes because internal
temperature in the present study (at least during three manipulated
years) did not exceed 40 °C. Humidity and evaporative
water loss may also be important and could influence
the bats to select roosts close to sources of water (Jenkins et
al. 1998). However, all of the bat boxes studied were equidistant
from the nearest calm water source. In this study, we
did not evaluated prey availability, but Bartonička et al.
20-Apr
25-Apr
30-Apr
5-May
10-May
15-May
20-May
25-May
30-May
4-Jun
9-Jun
14-Jun
19-Jun
24-Jun
29-Jun
4-Jul
9-Jul
14-Jul
19-Jul
24-Jul
29-Jul
date
0.0
0.5
1.0
1.5
2.0
2.5
3.0
meanofexploringactivity
lactation period
20-Apr
25-Apr
30-Apr
5-May
10-May
15-May
20-May
25-May
30-May
4-Jun
9-Jun
14-Jun
19-Jun
24-Jun
29-Jun
4-Jul
9-Jul
14-Jul
19-Jul
24-Jul
29-Jul
date
0.0
0.5
1.0
1.5
2.0
2.5
3.0
meanofexploringactivity
a
b
Fig. 2 Changes in exploration
activity (1–4, where 1 is the
lowest activity) in a boxes from
which the bugs were removed
and b control boxes where the
bat bugs were present; the
arrow shows when the first bat
young was observed. The
arrow shows when the first
instance of bat suckling was
observed, and the line shows
the duration of the lactation
period
Fig. 3 Bat bugs (C. pipistrelli), adults and early instars have successfully
colonized the new roost (photo by O. Balvín)
Parasitol Res (2013) 112:1615–1622 1619
(2008) showed similar distances of foraging sites of bats
coming from non-manipulated or in future manipulated bat
boxes.
Switching the roost may be related to the decrease of
food supply in foraging area and moving to other foraging
sites (e.g. Feyerabend and Simon 2000). Bat boxes in the
Křivé jezero have been monitored since 2000 and within the
8 years, pipistrelles occupied boxes only during pregnancy
and then in the postlactating period. Between June and July
2004 during radiotracking research on pipistrelles, lactating
females roosted in a guest house in the village of Nové
Mlýny, situated 1.5 km far from Křivé jezero (Bartonička
et al. 2008). However, all tagged females foraged in the oldgrowth
floodplain forest Křivé jezero. Therefore, it is unlikely
that change in the roost occupation after reducing
parasite load could be explained by change of the foraging
sites due to e.g. decreased prey availability there.
Pre-natal maternal effect
Unfortunately, we could not determine the primary mechanisms
that enabled the bats to distinguish between infested
and non-infested roosts. Bartonička (2008) assumed that the
bats left their roosts after bug bites. It is improbable that all
bats visiting the bat boxes during the night were attacked by
bat bugs; however, if only one bat was bitten, the other bats
would have realized that bat bugs were present from the
behaviour of the bitten bat (Bartonička 2008). In addition,
bats might be able to recognize an infested roost by other
signs, i.e. the smell of fresh bug faeces, which is very
intense (Usinger 1966). The fact that females leave an
infested roost just before parturition could be an interesting
example of pre-natal maternal behaviour similar to the maternal
effect of androgens or milk composition, which might
also influence offspring competitiveness (Pontier et al.
1993; East et al. 2009). However, there are also bat species
that roost in one infested shelter throughout the entire reproduction
season, but no switching strategies are currently
known in such nursery colonies (e.g. Myotis myotis). Only a
few life history analyses of bats have included representatives
of such behaviour (e.g. Read and Harvey 1989), and
further examinations of the main factors that influence postnatal
growth are desired.
Colonization of new roosts by bat bugs
Reckardt and Kerth (2007) found that M. bechsteinii reoccupied
bat boxes just 1 month after their first occupation,
when they were infested by the bat fly (Basilia nana).
During this period, the bats were safe in terms of bat fly
infestation because fly puparia only become contagious later
on. Such an adaptation in bats occupying bug-infested
roosts is inconvenient because adult bugs are always
prepared to suck. Whenever infested bats roosted in a bat
box in spring during the daytime, a bug outbreak was
always observed at the end of May. We found that nonmanipulated
bat boxes were repeatedly visited during the
lactation period even though bats did not roost here during
the daytime. However, commuting bats transported bat bugs
to different roosts. The probability of bug transport is very
low, as shown by the low number of bat bugs found on
commuting or foraging bats (e.g. Heise 1988). Since only a
few early instars, better transported because of their size,
were found in the manipulated bat boxes, we believe that
they are not able to stay in the fur of a flying bat or they
cannot survive the microclimate changes in the new roost. A
re-appearance of bugs in the manipulated boxes was observed
during the period when a high number of early stages
were observed in non-manipulated boxes (May and June),
when adult females were rapidly dying off (Bartonička and
Gaisler 2007). It seems that the transport of bat bugs by their
hosts to new roosts is not entirely random (cf. Balvín et al.
2012). Heise (1988) supposed that the bugs may travel on
the body of their hosts on the purpose of dispersal, not only
because they did not manage to escape when the bats
emerged from roost to forage. Pfiester et al. (2009) found
that the females actively disperse earlier than males when
bedbug abundance is increasing. Unfortunately, it was not
shown if the dispersing females were mated or virgin. However,
in almost all manipulated boxes we found a few new
eggs and early instars after the appearance of first adult bug.
This fact showed that at least some females were mated
before the transport.
The period of high fluctuation in the numbers of roosted
bats during pregnancy is very convenient for the colonization
of new roosts. But the time for transport to the other
roosts is limited. At about 27 °C, recently emerged adult bed
bugs (Cimex lectularius), when fed and mated, will start
ovipositing about 3 days later. When bugs are fed weekly
but not mated again, which is most probable when they are
moved to different roosts separately, three eggs per day are
produced over a period of 5 weeks. Oviposition ceases after
11 days if the bugs are not fed again (Davis 1966). The
limited time available for the successful transport and settling
of a new population could be optimized by asynchronization
in the timing of oviposition between different bug
females. However, this theory needs to be tested further.
A second gradation stage in the bug populations was only
observed in 2008, probably because of the early transport of
bat bugs to the manipulated bat boxes, when bugs were
found in boxes 21 days after the first appearance of bats.
No other gradation stages were observed in 2009 or 2010,
when the re-appearance of bugs occurred later in the vegetation
season. In 2008, fed and mated females were transported.
Therefore, the bug population grew and reached the
original numbers at the end of July. Bat bugs transported in
1620 Parasitol Res (2013) 112:1615–1622
2009 and 2010 were probably not fed or mated (cf. Davis
1966). The fact that bat bugs are able to move to a different
roost and reach a high population density all in one season
correlates well with the very fast ontogenesis that is reportedly
even faster than in the bed bug (C. lectularius; Bartonička
2010). A fast ontogenesis could be a consequence of the
coevolution between bugs and roost-switching bats.
Acknowledgments We are very grateful to J. Gaisler for his valuable
comments on the manuscript and Josef Chytil for help with fieldwork.
This study was supported by grant no. 206/07/P098 of the Science
Foundation of the Czech Republic and the Czech Bat Conservation
Trust, and by grants from the Ministry of the Environment and the
Ministry of Education, Youth and Sports of the Czech Republic no.
MSM0021622416. The boxes were checked under the licence no. 922/
93-OOP/2884/93 and 137/06/38/MK/E/07 of the Ministry of Environment
of the Czech Republic. The authors have also been authorized to
handle free-living bats according to the certificate of competency no.
104/2002-V4 (§17, law no. 246/1992).
References
Balvín O, Munclinger P, Kratochvíl L, Vilímová J (2012) Mitochondrial
DNA and morphology show independent evolutionary histories
of bedbug Cimex lectularius (Heteroptera: Cimicidae) on
bats and humans. Parasitol Res 111:457–469
Barclay RMR, Kurta A (2007) Ecology and behaviour of bats roosting
in tree cavities and under bark. In: Lacki MJ, Hayes JP, Kurta A
(eds) Bats in forests, conservation and management. Johns Hopkins
University Press, Baltimore, pp 17–60
Bartonička T (2008) Cimex pipistrelli (Heteroptera, Cimicidae) and the
dispersal propensity of bats: an experimental study. Parasitol Res
104:163–168
Bartonička T (2010) Survival rate of bat bugs (Cimex pipistrelli,
Heteroptera) under different microclimatic conditions. Parasitol
Res 107:827–833
Bartonička T, Gaisler J (2007) Seasonal dynamics in the numbers of
parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost
switching in bats (Chiroptera, Vespertilionidae). Parasitol Res
100:1323–1330
Bartonička T, Řehák Z (2007) Influence of the microclimate of bat
boxes on their occupation by the soprano pipistrelle Pipistrellus
pygmaeus: possible cause of roost switching. Acta Chiropterol
9:517–526
Bartonička T, Bielik A, Řehák Z (2008) Roost switching and activity
patterns n the soprano pipistrelle, Pipistrellus pygmaeus, during
lactation. Ann Zool Fenn 45:503–512
Christe P, Oppliger A, Richner H (1994) Ectoparasite affects choice
and use of roost sites in the great tit, Parus major. Anim Behav
47:895–898
Côte IM, Poulin R (1995) Parasitism and group size in social animals:
a meta-analysis. Behav Ecol 6:159–165
Davis NT (1966) Reproductive physiology. In: Usinger RL (ed) Monograph
of cimicidae (Hemiptera–Heteroptera), entomological society
of America. Thomas Say Foundation, New York, pp 167–178
Dick CW, Esberard CEL, Graciolli G, Bergallo HG, Gettinger D
(2009) Assessing host specificity of obligate ectoparasites in the
absence of dispersal barriers. Parasitol Res 105(5):1345–1349
East ML, Höner OP, Wachter B, Wilhelm K, Burke T, Hofer H (2009)
Maternal effects on offspring social status in spotted hyenas.
Behav Ecol 20:478–483
Feyerabend F, Simon M (2000) Use of roosts and roost switching in a
summer colony of 45 kHz phonic type pipistrelle bats Pipistrellus
pipistrellus Schreber, 1774. Myotis 38:51–59
Gannon MR, Willig MR (1995) Ecology of ectoparasites from tropical
bats. Environ Entomol 24:1495–1503
Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic
grooming costs imposed by a parasitic mite (Spinturnix
myoti) upon its bat host (Myotis myotis). Pro Royal Soc
London B 268:2071–2075
Heise G (1988) Zum Transport von Fledermauswanzen (Cimicidae)
durch ihre Wirte. Nyctalus 2:469–473
Jenkins EV, Laine T, Morgan SE, Speakman JR (1998) Roost
selection in the pipistrelle bat, Pipistrellus pipistrellus (Chiroptera,
Vespertilionidae), in the northeast Scotland. Anim
Behav 56:909–917
Kerth G, König B (1999) Fission, fusion and non random associations
in female Bechstein’s bats (Myotis bechsteinii). Behaviour
136:1187–1202
Kerth G, Weismann K, König B (2001) Day roost selec tion in
female Bechstein’s bats (Myotis bechsteinii): a field experiment
to determine the influence of roost temperature. Oecologia
126:1–9
Kummer H (1971) Primate societies: Group techniques of ecological
adaptations. Aldine-Atherton Publisher, Chicago
Kunz TH, Lumsden LF (2003) Ecology of cavity and foliage roosting
bats. In: Kunz TH, Fenton MB (eds) Bat ecology. The University
of Chicago Press, Chicago, pp 3–39
Kunz TH, Stern AA (1995) Maternal investment and post-natal growth
in bats. Symp Zool Soc Lond 67:123–138
Lewis SE (1996) Low roost-site fidelity in Pallid bats: associated
factors and effect on group stability. Behav Ecol Sociobiol
39:335–344
Montes C, Cuadrillero C, Villela D (2002) Maintenance of a
laboratory colony of Cimex lectularius (Hemiptera: Cimicidae)
using an artificial feeding technique. J Med Entomol
39:675–679
Moore J (2002) Parasites and the behavior of animals. Oxford series in
ecology and evolution. Oxford University Press, New York
O’Donnell CFJ (2000) Cryptic local populations in a temperate rainforest
bat Chalinobolus tuberculatus in New Zealand. Anim Conserv
3:287–297
Pfiester M, Koehler PG, Pereira RM (2009) Effect of population
structure and size on aggregation behavior of Cimex lectularius
(Hemiptera: Cimicidae). J Med Entomol 46:1015–1050
Pontier D, Gaillard JM, Allainé D (1993) Maternal investment per
offspring and demographic tactics in placental mammals. Oikos
66:424–430
Read AF, Harvey PH (1989) Life history differences among the eutherian
radiations. J Zool Lond 219:329–353
Reinhart K, Siva-Jothy MT (2007) Biology of the bed bugs
(Cimicidae). Ann Rev Entomol 52:351–374
Reckardt K, Kerth G (2007) Roost selection and roost switching of
female Bechstein’s bats (Myotis bechsteinii) as a strategy of
parasite avoidance. Oecologia 154:581–588
Russo D, Cistrone L, Jones G, Mazzoleni S (2004) Roost selection by
barbastelle bats (Barbastella barbastellus, Chiroptera: Vespertiliniodae)
in beech woodlands of central Italy: consequences for
conservation. Biol Conserv 117:73–81
Swift SM (1980) Activity patterns of pipistrelle bats (Pipistrellus
pipistrellus) in north-east Scotland. J Zool Lond 190:285–295
Usinger RL (1966) Monograph of Cimicidae (Hemiptera–Heteroptera).
Entomological Society of America. Thomas Say Foundation,
New York
Vonhof MJ, Barclay RMR (1996) Roost-site selection and roosting
ecology of forest-dwelling bats in southern British Columbia. Can
J Zool 74:1797–1805
Parasitol Res (2013) 112:1615–1622 1621
Webb PI, Speakman JR, Racey PA (1996) Population dynamics of a
maternity colony of the pipistrelle bats (Pipistrellus pipistrellus)
in north-east Scotland. J Zool Lond 240:777–780
Willis CKR, Brigham RM (2004) Roost switching, roost sharing and
social cohesion: forest-dwelling big brown bats, Eptesicus fuscus,
conform to the fission-fusion model. Anim Behav 68:495–505
Willis CKG, Brigham RM (2005) Physiological and ecological aspects
of roost selection by reproductive female Hoary bats (Lasiurus
cinereus). J Mammal 86:85–94
Willis CKG, Brigham RM (2007) Social thermoregulation, not cavity
microclimate, explain forest roost preferences in a cavity-dwelling
bat. Behav Ecol Sociobiol 62:97–108
1622 Parasitol Res (2013) 112:1615–1622
8.3 Vliv štěnic na chování netopýrů
BARTONIČKA T., 2008
Cimex pipistrelli (Heteroptera, Cimicidae) and the dispersal propensity of bats: an
experimental study.
Parasitology Research, 104:163–168.
ORIGINAL PAPER
Cimex pipistrelli (Heteroptera, Cimicidae) and the dispersal
propensity of bats: an experimental study
Tomáš Bartonička
Received: 8 July 2008 /Accepted: 18 August 2008 /Published online: 13 September 2008
# Springer-Verlag 2008
Abstract Previous results have shown frequent movements
of crevice-dwelling bats between different shelters. Low
roost fidelity of some dwelling bat species reduces the
reproductive success of ectoparasites. The question of
whether high densities of bat bugs (Cimex pipistrelli)
represent a cost for crevice-dwelling bats (Pipistrellus
pygmaeus), resulting in roost switching, has been examined.
Sessions in a volary equipped with two bat boxes
were carried out. One of the boxes was loaded with
ectoparasites (low and high densities), the other served as
a control and new roost for bats, which left the loaded box.
Differences in the level of bat self-grooming, movements
inside experimental boxes, and leaving the boxes between
experiments with bat bugs and controls were significant.
Allogrooming was observed only in few cases; therefore,
the hypothesis of cooperation among individual bats in
defense against bat bugs was rejected. Experiments with
artificial parasitation, when bugs were added to a bat roost,
showed that leaving a confined roost infested by bat bugs,
i.e., roost switching, is a natural reaction of crevicedwelling
bat species, which reduces parasite load.
Introduction
Behavioral responses of hosts during their exposure to
parasites usually reduce the effects of costly parasitism
(Moore 2002). Field and experimental research has demonstrated
that nest ectoparasites can reduce reproductive
success of their hosts (Loye and Carroll 1991; de Lope and
Moller 1993; Richner et al. 1993; Christe et al. 1996).
Some birds have shown sensitivity to costs associated with
parasites and the ability to discriminate levels of possible
infestation and to choose less soiled nests (Barclay 1988;
Opplinger et al. 1994; Rendell and Verbeek 1996). Low
roost fidelity observed in many dwelling bat species
significantly reduces the reproductive success of ectoparasites
such as bat flies (Reckardt and Kerth 2006) or bat
bugs (Bartonička and Gaisler 2007). However, up to the
present, studies on the life history of bat ectoparasites have
mainly dealt with species and their ontogenetic stages,
which live on their hosts’ bodies permanently (mites, e.g.,
Giorgi et al. 2001; nycteribiids, e.g., Reckardt and Kerth
2006, 2007; streblids, Gannon and Willig 1995).
As a result, the relations between bat species roosting in
crevices and their ectoparasites living in the same shelters
but mostly without physical contact with their hosts are
unclear and often based only on speculation. Reckardt and
Kerth (2007) showed that roost switching of Myotis
bechsteinii between seasons can be explained as bat
adaptive behavior to the life cycle of bat flies, i.e., their
emergence from puparia. Roost switching during one
season is well-known in pipistrelles, and seems to be an
anti-parasite strategy with respect to roost parasites such as
bat bugs (Bartonička 2007). Bartonička and Gaisler (2007)
showed that the absence of bats in satellite roosts during the
lactation period, coupled with high temperatures and
natural mortality of parasites, reduced the number of bat
bugs in bat boxes to less than half the initial number.
Whereas bat bugs are common not only in fissure-like
roosts but also in spacious shelters such as attics of
building, we observed that some bat species (e.g., Myotis
myotis) can reduce the load of parasitation by movements
within such large roosts (Bartonička and Gaisler, unpublished
observation).
Parasitol Res (2008) 104:163–168
DOI 10.1007/s00436-008-1175-1
T. Bartonička (*)
Department of Botany and Zoology, Masaryk University,
Kotlářská 2,
611 37 Brno, Czech Republic
e-mail: bartonic@sci.muni.cz
Little is known about parasite-induced behavior of bats
within the roost, e.g., grooming. In this paper, I tested
whether self-grooming or allogrooming can serve to reduce
the parasite load. An experimental test of the hypothesis that
high parasite load increases the probability of roost switching
in crevice-dwelling bats is presented. In particular, the
level and type of grooming and movement behavior with
respect to different levels of parasitation, survival rate, and
sucking success of bat bugs during laboratory infestation of
bats are reported. Based on this new data, I discuss possible
co-evolutionary responses between bat bugs and parasiteinduced
bat behavior, sucking success of bugs, and energy
loss caused by roost switching.
Materials and methods
Volary sessions and equipment
Only adult female bugs of the Cimex pipistrelli Jenyns 1839
group were selected for the experiments. Until the
beginning of experimental sessions, bat bugs were kept in
darkness at low temperature (15°C, humidity 70%) when
their survival without food was longest (Jones 1930;
Johnson 1941 observed in Cimex lectularius Linnaeus
1758). Sessions were held in a volary (3×3×2.5 m)
equipped with two bat boxes and under standard microclimatic
conditions (temperature 25°C, humidity 70%). The
soprano pipistrelles (Pipistrellus pygmaeus Leach 1825)
used in the experiment were netted in the roof of a brick
building housing a pheasantry at the village of Vranovice
(48°57′50″ N; 16°37′51″ E), Czech Republic where a large
colony of this species was situated. Only 20 females were
kept in captivity simultaneously. The bats were fed each
day after a session and had access to water enriched with
vitamins. All bats were returned to their original colony
after the sessions. During captivity, the light regime was
natural and the air condition is stable. The boxes were
equipped with thermometers and hygrometers (HOBO,
Onset Computer Corporation, software BoxCar 3.7); they
provided the only roosting space to bats in the volary. Both
bat boxes were equipped with a camera (SONY DCR SR
52E) to monitor the bat behavior; another camera was
installed on a tripod in the middle of the volary. Bat bugs
were last fed 1 week prior to the beginning of the
experiments (first release of the bugs into the appropriate
box) (Hase 1917; Adkins and Arant 1959).
Other ectoparasites were removed from all bats before
the first session. Bats inhabited the volary 1 week before
the first session. Each session started 2 h before sunset,
when bats were still in torpor, thus avoiding mutual
disturbance. Only infrared light was applied during the
observations. C. pipistrelli sample was divided into two
experimental groups with different numbers (20, 50) of bat
bugs. Only one bat box was infested by bat bugs, the other
was bug-free unless the bats themselves carried the parasites
into it.
At the beginning of each session, bugs were applied
directly into the box via a small hole using a glass tube.
Video sequences were recorded during 1 h after application
of the bugs. One day after a session with addition of bugs to
the roost, a control was carried out with an identical bat
group and started 2 h before sunset. In control sessions,
video recordings were made 120–60 min before sunset.
After each session, all bugs were removed from the boxes,
and their numbers, feeding status, and visible injuries were
reported.
The bats were captured, handled, and temporarily kept in
captivity under license numbers 922/93-OOP/2884/93 and
137/06/38/MK/E/07 of the Ministry of Environment of the
Czech Republic. The author has been authorized to
manipulate with free-living bats according to the certificate
of competency number 104/2002-V4 (section 17 of the law
number 246/1992).
Experimental groups and observed behavior
Video sequences lasting 1 h recorded the level of
allogrooming and self-grooming, the number of bat movements
within the box, and the number of bats leaving the
box. The experiments were carried out with early pregnant,
post-lactating, lactating females, and newly fledged young.
Video sequences were recorded of two different bat
assemblages: (1) early pregnant or post-lactating females
(ten individuals in each session, 20 session pairs—
experiment and control) and (2) age-mixed groups (five
lactating females and their five young, ten session pairs).
Statistical analysis
All variables showed a normal distribution (Kolmogorov–
Smirnov test). Statistica for Windows 7.0 (StatSoft, Tulsa,
OK, USA) was used for data analyses. Paired t tests were
used to check the differences between the level of grooming
and movements of bats under experimental and control
conditions. T tests were used to test differences in the
numbers of sucked (clearly visible blood in the abdomen)/
unsucked (no blood mark in the abdomen) bat bugs found on
bats, which stayed inside/left. The Bonferroni correction was
applied if multiple tests were used for the same data set.
Materials
In all, I carried out 20 experiments (half with 20 and half
with 50 bugs) and 20 controls without bugs. In the volary, I
also tested ten age-mixed (five adult and five newly fledged
164 Parasitol Res (2008) 104:163–168
young) bat groups and ten controls without bugs. To
quantify the level of grooming, the number of movements
and the condition of bat bugs (unsucked/sucked, lost, dead,
on/off the bat body), 3,600 min of video records were
examined.
Results
Level of grooming
All variables showed a normal distribution (Kolmogorov–
Smirnov test); therefore, mean values were used. Paired t
tests were used to check the differences between the level
of self-grooming and allogrooming and the movements of
bats in the experiments (with bugs) and in the controls (no
bugs). The differences in the level of self-grooming
(t=7.65, p<0.001, n=20), movements inside experimental
boxes (t=5.40, p<0.001, n=20), and bats leaving between
experiments (t=5.98, p<0.001, n=20) and controls were
statistically significant (Fig. 1). Allogrooming was observed
only in a few cases and differences were not
significant (t=2.02, ns, n=20).
When comparing the session with 20 and 50 bugs, the
differences were found in the level of self-grooming (t test,
t=−7.66, p<0.001, n1=10, n2=10), movements (t=−5.74,
p<0.001, n1=10, n2=10), and the number of bats leaving
the boxes (t=−4.04, p<0.001, n1=10, n2=10), and no
differences were found in the levels of allogrooming
(t=−0.16, ns, n1=10, n2=10) (Fig. 1).
Bat movements and bugs
Bats with bugs stuck on their bodies were significantly
more frequent among those that left a box than among those
that stayed inside (t=3.96, p<0.001, n1 =10, n2 =10)
(Fig. 2). Because bats started to move shortly after being
bitten by a bug, the number of sucked bugs on bats that left
the box did not differ even when different numbers of bugs
were used in the session (t=−1.80, ns, n1=10, n2=10),
whereas a higher number of bats left the more infested roost
at the same time. The time of the last bat emerging from the
box was longer at the higher level of parasitation (t=−3.81,
p<0.001, n1=10, n2=10). On average, 1.3 (range 0–3)
sucked bugs were found per bat leaving the box. Furthermore,
a higher level of parasitation of juveniles than adult
females was observed (t=−4.70, p<0.001, n1=5, n2=5) in
both levels of parasitation (Fig. 3). The majority (89.9%) of
bugs stuck on bats that left a box was recorded on
juveniles, with a mean of 1.6 (1–3) bugs per bat. In all
sessions (mixed and non-mixed-age bat groups together),
only 0.43 (0–1) bugs per bat were recorded on adult
females that left a box, resulting in 51% of the total number
of bugs. Female bats were not stressed by the presence of
bugs but were stressed by the bite of bat bugs after which
they usually left the roost. Bat bugs were not able to suck
on bats during their daily torpor because of the low body
temperature, when bat body temperatures were around
24.1°C (±4.3°C).
Discussion
Fast ontogenesis of the roost ectoparasites allows them to
increase their numbers rapidly soon after the roost
occupation by bats (e.g., Usinger 1966). Brown and Brown
(1986) described the impact of ectoparasites on hosts’
fitness and the negative influence on the coloniality of
hosts. Bugs of the family Cimicidae are important roost
ectoparasites of bats. An increase in parasite density is
usually caused by high starting parasite abundance in the
Fig. 1 Level of self-grooming, allogrooming, number of bat movements,
and bats leaving bat box under different number of bat bugs.
One asterisk (*) shows significant paired t tests (p<0.001) between
the control (self, allo, mov., and bats control) and experiment and
double asterisks (**) significant t tests between level of grooming and
number of bat movements under different number of bat bugs. Box–
whisker plots (mean—central tendency, the standard deviation—large
box and min–max range as whiskers). Bonferroni correction was
applied (p<0.012)
Parasitol Res (2008) 104:163–168 165
host’s roost, low antiparasitic behavior and/or immunity
reaction, optimal microclimate—microhabitats that are
favorable for the parasite, decreased natal dispersal, and
occupancy of the same roost for a long time (uninterrupted
occupying of roosts by bats) (Brown and Brown 1986;
Zahn and Rupp 2004). Resistance of bats against parasites
can be influenced by sufficient nourishment; therefore,
there are different numbers of parasites during the same
time periods and in the same roosts (Christe et al. 2000).
Frequent roost switching reduces the numbers of roost
ectoparasites, namely, bugs in the abandoned roosts, which
can be re-occupied later during the same or in the next
season (Bartonička and Gaisler 2007). Although roost
switching has been demonstrated as antiparasitic behavior,
the phenomenon was not completely understood until now
(cf. Lewis 1995; Vonhof and Barclay 1996; Brigham et al.
1997). It seems that parasitation is sufficiently important to
be a cause of roost switching.
Ability to suck blood
It is well-known that the bugs spend only the time
necessary for feeding on their host’s body (Usinger 1966).
At the beginning of each session, bat bugs orientated
themselves in the experimental boxes quickly and they
moved to the cluster of bats in daily torpor immediately.
Marx (1955) suggests that the bed bug C. lectularius
detects human hosts from as far as 1.5 m away through the use
of heat cues, host kairomone(s), and/or CO2. Temperature
sensors on the antennae are capable of resolving differences
of 1–2°C (Sioli 1937). Rivnay (1932) carried out an
experimental study on host’s preference of C. lectularius
and found that a hungry bug can feed on all vertebrates
whose body temperature exceeds ambient temperature by at
least 3°C. The optimal blood temperature with respect to
sucking in C. lectularius was found to be 37°C (Montes
et al. 2002).
In this study, although bugs were unable to suck on bats
during the daily torpor because of low blood temperature,
they were able to localize them and reach their bodies. This
statement is illustrated by the observation of high locomotor
activity of bat bugs on the bats’ bodies without host reaction
during the first 20 min of most experimental sessions.
However, bug activity can cause the activation of the bats,
which consequently leads to an increase of their body
temperature and allows the bugs to suck. Differences in the
availability of feeding are very important with respect to the
timing of parasite pressure during the day. If bugs can feed
on bats only when they are active, the parasite load of bat
bugs will be highest during the short activity period before
leaving and after returning to the roost when bats are not
torpid. Also when bugs bite bats, the latter can leave the roost
and transport bat bugs to a non-infested roost at a distance.
Antiparasitic behavior
Bats, when in torpor, were not stressed by the presence of
the bugs themselves, but when woken up and stressed by
the bug bites, they normally left the roost. The host’s
reactions to bug bites are probably caused by substances in
the saliva (Valenzuela et al. 1995). Also, allergic response
can often be present (Hecht 1930). Adaptive parasiteinduced
behavior (an effort to kill or eat ectoparasite, or to
groom, fidget, and scratch) can decrease the level of
successful sucking (Moore 2002). However, results from
Fig. 3 Different levels of parasitation of juveniles and adult females.
Bonferroni correction was applied (p<0.012)
Fig. 2 Numbers of sucked/unsucked bat bugs found on bats that left
or remained in the box during the sessions. One asterisk (*) shows
significant t tests (p<0.001) among different bug groups. Box–
whisker plots (mean—central tendency, the standard deviation—large
box and min–max range as whiskers). Bonferroni correction was
applied (p<0.006)
166 Parasitol Res (2008) 104:163–168
the current volary experiments did not show any
behavior, which might reduce the pressure of roost
ectoparasites before the blood loss. Usinger (1966) notes
that bats avoid eating bat bugs because of their intensive
smell (an alarm pheromone); therefore, it can be expected
that bats would not bite bugs during experimental sessions
(cf. Overal and Wingate 1976). However, bat bugs were
served periodically together with the common food
(mealworm larvae, Tenebrio molitor; and crickets, Gryllus
assimilis) to bats kept in the volary. Bats ate bugs without
restraint and even during several days. Analyses of prey of
P. pygmaeus also showed the presence of Cimex spp. body
fragments in pellets (Bartonička et al. 2008). Despite the
bats’ ability to feed or to bite bat bugs, they refrain from
doing so during experiments although it could prevent
their blood loss.
Cooperation in grooming
Allogrooming (grooming of conspecifics) is one form of
social behavior that can be observed in many social
mammals (O’Brien 1993; Hart 1994; Mooring and Hart
1995; Gompper et al. 1997). It is suggested that allogrooming
has both social and hygienic function. Bats groomed
their colony mates mainly on the body parts that are
difficult to reach. The hypothesis of cooperation among
individual bats in defense against bat bugs has not been
confirmed so far, though allogrooming was observed in
other bat species, mainly between parents and offspring
(Wilkinson 1986; Kerth et al. 2003; Willis and Brigham
2004). The same authors (i.e., Wilkinson 1986; Kerth et al.
2003) did not find significant positive correlation between
the time a bat was groomed and the time it groomed itself,
and allogrooming was very rare compared to self-grooming
in their study. Also in my sessions, only a few allogrooming
events were observed. Adult bats did not cooperate in
defending each other against bat bugs; neither did the
females defend their offspring, despite the higher level of
parasitation of juveniles. A higher number of sucked bugs
found on the young were also reported by Christe et al.
(2000). On the other hand, there is no direct correlation
between the number of bugs in the roost during lactation
(non-fledging period of young) and first-year survival
probability. Therefore, the breeding lifespan, which is
usually used as the major indicator of fitness (in birds,
e.g., Brown and Brown 1998), should be determined
between infested and non-infested roosts. Finally, it can
be assumed that the two observed behavior modes,
allogrooming and self-grooming, do not serve exactly the
same purpose. I suggest that in pipistrelles, self-grooming is
used to remove ectoparasites (bat bugs), whereas allogrooming
serves mainly for social functions.
Movement of bats and number of bugs
The emergence time of the last bat from the experimental
box was shorter when a lower number of bat bugs were
applied. A comparison of the number of bugs adhering to
bats that left the bat box under low and high parasite load
shows that bats react to one of the first bug bites and, when
changing position and self-grooming is unsuccessful, they
leave the box. Thus, the emergence time can correlate with
changing (increasing) the success of bugs to find bats with
body temperatures suitable for sucking and, at the same
time, with a higher level of self-grooming. Consequently,
the bats disturb each other and indirectly induce an increase
in the body temperature of adjacent bats. As a result, these
bats can also be attacked by bat bugs because of their
higher body temperature. Experiments with artificial parasitation,
when bugs were added to the roost manually, show
that leaving confined roost occupied by a high number of
ectoparasites is a natural reaction of crevice-dwelling bat
species. However, vacation of the roost is not always
needed; bats prefer changing location within the roost in
case this strategy helps to reduce the parasite load.
Therefore, further studies are needed in species occupying
more spacious roosts, which allow effective changes of
position.
Acknowledgments I am very grateful to J. Gaisler, D. Zounková, G.
Filby, and M. Nicolls for valuable comments on the manuscript, and
the whole staff of the Department of Population Biology, Institute of
Vertebrate Biology, ASCR at Studenec for providing a safe place to
situate an experimental volary. I would also like to acknowledge the
Administration of the Moravian Karst Landscape Protected Area and
the Ministry of Environment of the Czech Republic for providing the
facilities and handling permits. The study was supported by grant no.
206/07/P098 of the Science Foundation of the Czech Republic and the
Czech Bat Conservation Trust, the grant from the Ministry of
Environment and the grant from the Ministry of Education, Youth
and Sports of the Czech Republic, grant no. MSM0021622416.
References
Adkins TR, Arant FS (1959) A technique for the maintenance of a
laboratory colony of Cimex lectularius L. on rabbits. J Econ
Entomol 52:685–686
Barclay RMR (1988) Variation in the costs, benefits, and frequency of
nest reuse by barn swallows (Hirundo rustica). Auk 105:53–60
Bartonička T (2007) Bat bugs (Cimex pipistrelli, Heteroptera) and roost
switching in bats. Ber Naturforsch Ges Oberlausitz 15:29–36
Bartonička T, Řehák Z, Andreas M (2008) Diet composition and
foraging activity of Pipistrellus pygmaeus in a floodplain forest.
Biologia 63:1–7
Bartonička T, Gaisler J (2007) Seasonal dynamics in the numbers of
parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost
switching in bats (Chiroptera, Vespertilionidae). Parasitol Res
100:1323–1330
Parasitol Res (2008) 104:163–168 167
Brigham RM, Vonhof MJ, Barclay RMR, Gwilliam JC (1997)
Roosting behaviour and roost-site preferences of forest-dwelling
California bats (Myotis californicus). J Mammal 78:1231–1239
Brown RC, Brown WB (1986) Ectoparasitsm as a cost of coloniality
in cliff swallows (Hirundo pyrrhonata). Ecology 67:1206–1218
Brown CR, Brown MB (1998) Fitness components associated with
alternative reproduction tactics in cliff swallows. Behav Ecol
9:158–171
Christe P, Opplinger A, Richner H (1996) Begging, food provisioning,
and nestling competition in Great Tit broods infested with
ectoparasites. Behav Ecol 7:127–131
Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a
parasitic mite (Spinturnix myoti) in relation to the reproductive
cycle and immunocompetence of its bat host (Myotis myotis).
Ecol Lett 3:207–212
de Lope F, Moller AP (1993) Female reproductive effort depends on the
degree of ornamentation of their mates. Evolution 47:1152–1160
Gannon MR, Willig MR (1995) Ecology of ectoparasites from tropical
bats. Environ Entomol 24:1495–1503
Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming
costs imposed by a parasitic mite (Spinturnix myoti) upon its bat
host (Myotis myotis). Proc R Soc Lond B 268:2071–2075
Gompper ME, Gittleman JL, Wayne RK (1997) Genetic relatedness,
coalitions and social behaviour of white-nosed coatis, Nasua
narica. Anim Behav 53:781–797
Hart BL (1994) Behavioural defense against parasites: interaction with
parasite invasiveness. Parasitology 109:139–151
Hase A (1917) Die Bettwanze Cimex lectularius L.: ihr Leben und
ihre Bekämpfung. Monogr Angew Entomol Z Angew Entomol
Beiheft 4:1–144
Hecht O (1930) Hautreaktionen auf die Stiche blutsaugender Insekten
und Milben als allergische Erscheinungen. Zentralbl Haut Geschl
Krankh 44:241–255
Johnson CG (1941) The ecology of the bed-bug, Cimex lectularius L.,
in Britain. J Hyg 41:345–361
Jones RM (1930) Some effects of temperature and humidity as factors
in the biology of the bedbug (Cimex lectularius Linn.). Ann
Entomol Soc Am 23:105–119
Kerth G, Almasi B, Ribi N, Thiel D, Lüpold S (2003) Social
interactions among wild female Bechstein‘s bats (Myotis bechsteinii)
living in a maternity colony. Acta Ethologica 5:107–114
Lewis SE (1995) Roost fidelity of bats: a review. J Mammal 76:481–496
Loye JE, Carroll SP (1991) Nest ectoparasite abundance and cliff
swallow colony site selection, nestling development, and departure
time. In: Loye JE, Zuk M (eds) Bird–parasite interactions.
Oxford University Press, Oxford, UK, pp 222–241
Marx R (1955) Über die Wirtsfindung und die Bedeutung des
artspezifischen Duftstoffes bei Cimex lectularius Linné. Zeitschr
Parasitenk 17:41–73
Montes C, Cuadrillero C, Villela D (2002) Maintenance of a
laboratory colony of Cimex lectularius (Hemiptera: Cimicidae)
using an artificial feeding technique. J Med Entomol 39:675–679
Moore J (2002) Parasites and the behavior of animals. Oxford
series in ecology and evolution. Oxford University Press,
New York
Mooring MS, Hart BL (1995) Differential grooming rate and tick load
of terrestrial male and female impala. Behav Ecol 6:94–101
O’Brien TG (1993) Allogrooming behaviour among adult female
wedge-caped capuchin monkeys. Anim Behav 46:499–510
Opplinger H, Richner H, Christe P (1994) Effect of an ectoparasite on
lay date, nest-site choice, desertion, and hatching success of the
great tit (Parus major). Behav Ecol 5:130–134
Overal WL, Wingate LR (1976) The biology of the bat bug
Stricticimex antennatus (Hemiptera: Cimicidae) in South Africa.
Ann Natal Mus Pietermaritzb 22:821–828
Reckardt K, Kerth G (2006) The reproductive ecology of the bat fly
Basilia nana (Diptera: Nycteribiidae) is affected by low roost
fidelity of its host, the Bechstein’s bat (Myotis bechsteinii).
Parasitol Res 98:237–243
Reckardt K, Kerth G (2007) Roost selection and roost switching of
female Bechstein’s bats (Myotis bechsteinii) as a strategy of
parasite avoidance. Oecologia 154:581–588
Rendell WB, Verbeek NAM (1996) Old nest material in nestboxes of
tree swallows: effects on reproductive success. Auk 98:142–152
Richner H, Opplinger A, Christe P (1993) Effect of an ectoparasite on
reproduction in great tits. J Anim Ecol 62:703–710
Rivnay E (1932) Studies in tropisms of the bedbug Cimex lectularius
L. Parasitology 24:121–136
Sioli H (1937) Thermotaxis und perzeption von Wärmestrahlen bei
der Bettwanze (Cimex lectularius L.). Zool Jahrb Physiol
Morphol Tiere 58:284–296
Usinger RL (1966) Monograph of cimicidae (Hemiptera–Heteroptera).
Entomological Society of America. Thomas Say Foundation,
New York
Valenzuela JG, Walker FA, Ribeiro JMC (1995) A salivary nitrophorin
(nitric-oxide-carrying hemoprotein) in the bedbug Cimex lectularius.
J Exp Biol 198:1519–1526
Vonhof MJ, Barclay RMR (1996) Roost-site selection and roosting
ecology of forest-dwelling bats in southern British Columbia.
Can J Zool 74:1797–1805
Wilkinson GS (1986) Social grooming in the common vampire bat,
Desmodus rotundus. Anim Behav 34:1880–1889
Willis CKR, Brigham RM (2004) Roost switching, roost sharing
and social cohesion: forest-dwelling big brown bats, Eptesicus
fuscus, conform to the fission–fusion model. Anim Behav
68:495–505
Zahn A, Rupp D (2004) Ectoparasite load in European vespertilionid
bats. J Zool Lond 262:383–391
168 Parasitol Res (2008) 104:163–168
BARTONIČKA T. & RŮŽIČKOVÁ L., 2012
Bat bugs (Cimex pipistrelli) and their impact on non-dwelling bats
Parasitology Research, 111: 1233–1238.
ORIGINAL PAPER
Bat bugs (Cimex pipistrelli) and their impact
on non-dwelling bats
Tomáš Bartonička & Lucie Růžičková
Received: 26 January 2012 /Accepted: 3 May 2012 /Published online: 24 May 2012
# Springer-Verlag 2012
Abstract Bat bugs are often roost ectoparasites of bats.
Previous studies have shown that bats shifting roosts
within the growing season prevent the massive reproduction
of these parasites. We postulated that there
could be other antiparasitic strategies of philopatric bats
roosting in non-dwelling spacious roosts. Unfortunately,
there are no studies devoted to such a topic. For 3 years,
two attics highly and less infested by bat bugs (Cimex
pipistrelli) with breeding females of Myotis myotis were
monitored. From April, after the arrival of the bats, to
November, abundance of all instars and adult bugs was
sampled in the attics by adhesive traps. We found
different patterns in the bug abundances and dynamics
in the two attics. In highly infested attic, bat bugs
induced pregnant females to move from the infested site
of the attic to the non-infested one. Internal temperature
and relative humidity were similar in both infested and
non-infested sites. Females roosted in the infested site
till time before parturition and then moved to the noninfested
site within attic. When bats were absent in their
old site, the abundance of nymphal instars of bugs
decreased by half. Although adult bats can survive
under high parasite loads of bat bugs, reproducing
females prevent parasite reproduction and simultaneously
reduce parasite load in the young by shifting inside
spacious roosts.
Introduction
Bat bugs (Cimex pipistrelli, Cimicidae, Heteroptera) are
often roost ectoparasites of bats, which, except for the time
spent engorging (Walter 1996), mostly co-habit without
physical contact with their hosts (Reinhardt and Siva-Jothy
2007). Fast ontogeny enables the bugs to increase their
numbers rapidly soon after a roost has been occupied by
the hosts. Bugs, in general, prefer lower roost temperatures
than permanent bat parasites, because they associate with
bats for a short time only to feed (Usinger 1966). Therefore,
they inhabit crevices, restricting the circulation of air inside
(Lourenço and Palmeirim 2004; Whitaker 1998), but in
close vicinity of bats. Although previous studies have
shown high tolerance towards dehydration and a desiccation
hardiness against high temperatures in adult bugs (Dubinin
1947; Southwood 1954), early instars with higher body
water content have worse survival rates under high temperatures
of the climatically extreme conditions in natural bat
roosts (Johnson 1960; Jones 1930). In such cases, even short
absences of hosts in infested roosts can induce a sharp
decrease in bug numbers (Bartonička and Gaisler 2007).
High densities of haematophagous ectoparasites composed
of Cimex entail a health risk associated with blood
loss, unease, stress and changes in grooming behaviour after
the bug bites (Giorgi et al. 2001; Walter 1996). Experiments
with artificial parasitation, with bugs added to the roost
manually, show that leaving a confined roost occupied by
a high number of ectoparasites is a natural reaction of
crevice-dwelling bat species (Bartonička 2008). Bats left
highly infested roosts even when other conditions such as
temperature, humidity or air circulation were optimal (Evans
2009). Roost switching during one season is well known in
pipistrelles and seems to be partly an anti-parasite strategy
with respect to roost parasites such as bat bugs (Bartonička
T. Bartonička (*) :L. Růžičková
Department of Botany and Zoology, Masaryk University,
Kotlářská 2,
611 37 Brno, Czech Republic
e-mail: bartonic@sci.muni.cz
L. Růžičková
e-mail: lruzickova@mail.muni.cz
Parasitol Res (2012) 111:1233–1238
DOI 10.1007/s00436-012-2957-z
and Gaisler 2007). Pipistrelles do not switch roosts as many
times as typical forest-dwelling species, e.g. Myotis bechsteinii
or Eptesicus fuscus, where the causes of roost switching
most probably relate to the fission–fusion social
organisation or changing requirements connected with reproduction
(Kerth et al. 2001; Lourenço and Palmeirim
2004; Willis and Brigham 2004). However, some forms of
roost selection to avoid ectoparasites have been observed in
tree-dwelling species (Reckardt and Kerth 2007).
The supply of artificial roosts is more limited in bat
species that have roosted for a long time (several decades)
in summer shelters (associated with roosts in buildings) than
that for species that use roosts of short lifespan like pieces of
detached bark (Willis et al. 2003). In the case of Myotis
myotis, females of this species, despite knowing other roosts
of nursery colonies in the vicinity, switch rarely, usually as a
post-disruption movement (Schneider and Hammer 2006).
We postulate that philopatric species roosting in spacious
shelters have other anti-parasitic strategies. Therefore, we
present a field study in which the roosting strategy of greater
mouse-eared bats (M. myotis) was carried out. We think that
vacation of the roost is not always needed. Bats might prefer
changing location within the spacious roost in case this
movement strategy helps to reduce the parasite load. The
aim of our study was to determine (1) if bats moved inside
the large spacious roosts, and (2) if yes, whether the cause of
movements was high parasite densities in the previous sites so
that the females wanted to bear and wean their young within
sites where there were no or low numbers of bat bugs.
Material and methods
Study area and technical equipment
Nursery colonies of M. myotis were monitored in two
church attics: in Blansko (49 ° 21′ 36″ N, 16 ° 38′ 19″ E)
where 200 females roosted and Klentnice (48 ° 50′ 37″ N,
16 ° 38′ 40″ E) with 150 females, in southern Moravia
(Czech Republic). Both roosts were regularly (once every
10 days) observed in 2007, 2008 and 2009. Roost checks
occurred more often during lactation. Attics were equipped
with thermometers (Hobo; Onset Computer Corporation,
Southern MA, USA) to record temperatures and relative humidities
inside the roosts throughout the seasons. Thermometers
were placed in the sites occupied by bats and in new sites
where the bats moved to. Monitoring of the bat bugs was
carried out by manual sampling from inside the roosts.
Adhesive belts (width 5 cm) for immobilisation of crawling
insects (Bio Plantella) were placed on binding joists,
poles and rafters. Bat bugs were caught when they tried to cross
the belts towards the bats. Ground traps made from plastic
bowls turned against each other with longitudinal crevices at
the bottom to trap bugs on an adhesive plate (Bio Plantella
adhesive paper, 10×10 cm). Traps were taken on the ground
next to the piles of bat guano. In each locality, we placed three
ground traps and six 50-cm-long belts. Adhesive belts were
covered by a steel grill to prevent bats from sticking to it, but
allowing bat bugs to crawl through. The positions of the belts
were switched at each check. The same number of belts and
traps were placed in areas where bats moved during the study.
The sampled bat bugs were manually divided by instars
and sex and placed in laboratory containers using a binocular
(Olympus SZX 9), following the method of Stutt and
Siva-Jothy (2001) to reliably sort the samples according to
their developmental stages and sex using tweezers. Bugs
were divided into four groups as follows: first to second
instar, third to fifth instar, adult males and adult females.
Statistical analysis
All variables showed a normal distribution after log transformation.
Statistica for Windows 9.1 was used for data
analyses. Analysis of variance (ANOVA) and (paired) t test
were used to check for differences between the temperature
and humidity in two colony roosts. ANOVA was used also
to check the differences between parts of the season and t
test as post hoc. Logistic regression was used to test for
changes in the numbers of bat bugs, maximum daytime
temperatures and minimum relative humidity in new and
old colony sites and between the two different attics.
Material
During the three growing seasons of 2007 to 2009, the two
attics were monitored from the beginning of April to midOctober.
Samples of bat bugs (C. pipistrelli) and number of
bats throughout the day were taken on 19 (2007), 20 (2008)
and 20 (2009) occasions in each attic. On each day, hourly
values of internal temperature and humidity were recorded.
Results
Seasonal dynamic in bug numbers
No significant differences were found among the seasons in
Blansko (ANOVA, F(2, 59)00.961, NS) when the bat bugs
were sampled. However, in Klentnice, we found different
numbers of bat bugs (F(2, 59)01.196, p00.01). Differences
in the numbers of bugs among the checks in 1 year were
statistically significant (ANOVA, Klentnice, adults F(19, 59)0
14.19, p<0.001, third to fifth instars F(19, 59)06.44, p<0.001,
first to second instars F(19, 59)09.80, p<0.001; Blansko, adults
F(19, 59)03.10, p00.004, third to fifth instars F(19, 59)00.94,
NS, first to second instars F(19, 59)01.93, NS). In 2007, we
1234 Parasitol Res (2012) 111:1233–1238
found only few bugs in Klentnice; therefore, we pooled only
years with high bug density into the two datasets (Klentnice,
2008 and 2009; Blansko, all 3 years). However, there were
differences in seasonal dynamics of bat bugs between the two
roosts Klentnice and Blansko (paired t test, t0−4.62, p<0.001,
n1040, n2040, only 2008 and 2009). Two peaks in the densities
of bugs were recorded in Klentnice at the end of May
(adults) and mid-July (early instars) (Fig. 1). Comparing high
density of bat bugs in Klentnice, only low numbers of bugs
were recorded throughout the year in Blansko (Fig. 2).
In Klentnice, from the beginning of the season (midMay),
when the bats were pregnant, until the parturitions
in mid-June, a significant decrease in the number of adult
bugs were recorded (t test, t02.86, Bonferroni correction,
p00.035, n103, n204). A rapid increase in the number of
first to second instars (t0−6.88, p00.01, n104, n204) and
third to fifth instars (t0−3.10, p00.03, n104, n204) was
recorded during late pregnancy at the end of June. A significant
decrease in all instars was found from mid-July until
the end of August (t04.70, p00.003, n106, n206).
Although we found changes in the numbers of nymphal
instars in the highly infested roost in Klentnice, there was a
significant change only in the numbers of adult bugs in the
low infested roost in Blansko. The number of adult bugs
surviving from the previous winter decreased until the end
of May, when they practically died out (t04.36, p00.02,
n103, n202). At the beginning of July, a new generation of
adult bugs were observed.
Site switching
A group of females left their respective roosts in early June
(2008 and 2009, Klentnice) and moved to the southern part
of the attic, 20 m from the old site, in the days when the first
young were observed. During the period in which the bats
were absent from their old site (17 days in 2008 and 21 days
in 2009), a rapid dying of nymphal stages (first to fifth
instars) of bugs was recorded (linear regression model, F0
14.66, p00.005, both years). An obvious, but not significant
increase in the number of bat bugs at the new site was also
observed (F02.40, NS). After all bats had moved, the abundance
of bugs decreased at the old site to less than half
during 17 to 21 days.
Microclimatic conditions
Although the studied roosts were 56 km apart and, most
probably, differed in the degree of exposure, no significant
difference was found in the internal temperatures and humidity
(ANOVA, internal temperature F(1, 1,036)02.11, NS;
humidity F(1, 1,036)01.43, NS). Moreover, there were no
significant differences in the maximum internal temperature
(ANOVA, F(2, 538)00.83, NS) and minimum relative humidity
(F(2, 538)01.02, NS) among the years. In the bat roosts,
the internal temperature was usually below 30°C, and in
only two cases (Klentnice), the maximum internal temperature
reached 37°C. Very low relative humidity, 25 to
40 %, was found in Blansko, while the relative humidity
in Klentnice varied usually between 25 and 60 %.
The maximum temperature (paired t test, 2008, t00.13;
NS, n1017, n2017; 2009, t01.89; NS, n1021, n2021)
and relative humidity (2008, t00.73; NS, n1014, n2014;
2009, t01.13; NS, n1021, n2021) did not differ between
the old site, occupied by bats in pregnancy and
postlactation, and the new site in Klentnice, occupied
during the lactation period (Fig. 3).
Fig. 1 Changes in the numbers
of adult bat bugs and nymphal
stages in Klentnice. Black line
on top of the graph shows the
period of bat presence in the
roost, while the white one
shows the lactation period.
Mean, central tendency;
standard deviation, whiskers
Parasitol Res (2012) 111:1233–1238 1235
Discussion
From among various environmental factors, temperature
seems to be the most important, since it influences the
development and activity of ectothermic animals like roost
ectoparasites and, subsequently, their endothermic hosts, the
bats. Many roost activities, including metabolism, are affected
by the thermal environment of the roost (Kunz and
Fenton 2003). Many studies suggest that females at summer
colonies agglomerate in cold days and conversely disperse
during hot days (e.g. Kolb 1950; Mislin 1942). Average or
extreme temperatures have been reported as the most important
factor for bat movements in roosts. On very hot
days, bats usually abandon positions near the ridge of the
roof and seek refuge in cooler parts of the loft (e.g. Licht and
Leitner 1967). Moreover, bats begin to move when the ambient
temperature approaches 40°C (Lourenço and Palmeirim 2008).
Movements of Tadarida sp. in laboratory thermal gradients
suggest that these bats do not voluntarily expose themselves to
an ambient temperature above 36°C, and movements within or
between roosts are used to avoid high temperatures (Henshaw
1960). Therefore, we postulate that if the temperature is the
only determinant of bat roosting behaviour, we expect bats to
roost at different sites with varying temperatures in the attic to
avoid areas that overheat during the day. However, in our
study, bats moved to a different part of the attic and occupied
the ridge as in the case of the old site where maximum day
temperatures did not differ from those of the old site. We
suppose the cause of bat movements within the attics must
have been due to a different reason other than very high
temperatures.
Bat bugs formed stable populations (eggs and early instars
observed) in both the studied roosts; however, their densities
at the sites occupied by the bats and between years differed
significantly. In Blansko, we found only 25 % of total bug
numbers in Klentnice during the seasonal graduation in 2008
and 2009. The low relative humidity (<30 %) there could
often be linked to low bug densities (Rivnay 1932). Bat
movements were observed only in Klentnice and only in years
with high bug densities. Therefore, we assume that bats always
occupied the same site in the large space roof every year,
switching their positions in the attics only in the years when
bug densities were very high. Roost manipulation experiments,
such as removing bat bugs completely from spacious
roosts, might be few successful, regarding many crevices and
cracks in wood constructions where bugs hide. However, such
removal experiments in bat boxes, where are not too much
bug shelters, by Bartonička and Růžičková (under review),
have already confirmed that roost switching in bats could be
the outcome of a high roost parasite load.
Fig. 2 Changes in the numbers
of adult bat bugs and nymphal
stages in Blansko. Mean,
central tendency; standard
deviation, large box. Bats
occupied the roost during the
whole study period. Mean,
central tendency; standard
deviation, whiskers
Fig. 3 Changes in the numbers of nymphal stages at the site usually
occupied by bats (old) and at the site (new) occupied during lactation in
Klentnice. Mean, central tendency; standard deviation, whiskers
1236 Parasitol Res (2012) 111:1233–1238
At the old site, when the bats were absent (during lactation
in July), there was a rapid decline in most of the
nymphal stages of the bugs. Although bugs are known to
have high tolerance of drying, they died of water deficiency
associated with lower relative humidities (0 to 60 %).
According to Kemper (1936), extremely low relative humidity
(0 to 20 %) often causes the death of nymphs in the
course of ecdysis. We did not find differences in the minimum
relative humidity between the old and new sites in the
attic of Klentnice, relative humidity during lactation being
very low (37.3±10.5 %) at both sites. The negative impact
of low humidity on early instars may even be greater when
combined with food inaccessibility (Bartonička and Gaisler
2007). Therefore, bats left the old site in the attic because of
the increase in the number of parasites, mainly early instars.
They could do it just before parturition because reproducing
females and their hairless offsprings usually have the highest
level of parasitation (Zahn and Rupp 2004; Lučan 2006).
Therefore, the fact that females leave an infested roost just
before parturition could be an interesting example of prenatal
maternal behaviour similar to other kinds of maternal
effects already published (e.g. East et al. 2009). Very important
seems to be absence of bugs in sites where females
leave young while forage.
Only few individuals of nymphal stages and adults of bat
bugs were sampled by adhesive belts at the new site. It
seems that bat bugs cannot move to host that are far away
or to the new host site. The means of finding a host is the
most controversial subject in the studies of bat/bed bug
behaviour. Rivnay (1932) claimed that the bugs searched
entirely randomly until they were 3 or 4 cm from the host,
when they recognised a temperature differential of 2°C.
However, Marx (1955) found that bugs could perceive a
human body from a distance of 1.5 m. Nymphal stages of
Cimex lectularius can travel at a speed of 13 to 28 cm/min,
and adults, 126 cm/min (Hase 1917). Therefore, they should
be able to reach a distance of 20 m very quickly. In addition,
Kemper (1936) found that bugs successfully travelling to
very distant hosts followed paths that involved considerable
turning from a direct line. They most probably follow faecal
spots, food prints or pheromone trails by dragging the
engorged abdomen (Hase 1930; Aldana et al. 2008). Unfortunately,
there is no detailed study explaining how long the
smell of trails lasts. The fact that bats occupy different sites
within an attic was observed for the first time in this study,
even though a revision nursery colony in Klentnice, evaluated
several times a year since 2000, has not confirmed that
bat bugs have to regularly find moving hosts. Moreover,
only a few faecal spots and exuviae were found at the new
site because of short bat stays and very few bugs found. In
general, no such high bug densities occur in all infested bat
roosts every year (see Klentnice 2007 and Blansko all the
time) because the between-year levels of parasitation
depend highly on the number of successfully overwintering
adults (Bartonička and Gaisler 2007). Therefore, we expect
that bats move only occasionally between infested and noninfested
sites within the attic, and trapped bugs could be
transported to the new site by commuting bats.
Our results show that roost/site switching could be a
suitable strategy to prevent the massive reproduction of bat
bugs. Bartonička and Gaisler (2007) presented evidence to
support the theory that some crevice-dwelling bats switch
roosts of nursery colonies due to bat bug infestation. This
study documents for the first time that not only did bats
prefer fissure-like roosts, but also occupied non-dwelling
spacious roosts, with the strategy of temporarily abandoning
particular roosts/sites to decrease parasite load.
Mark-recapture and molecular genetic studies have recently
documented that female bats exhibit natal philopatry
and roost fidelity in temperate regions (e.g. Petri et al.
1997). In many species, such as M. myotis, maternity colonies
are persistently used for decades, suggesting that natal
philopatry leads to long-term association among individuals
in a colony (Entwistle et al. 2000). Long-term use of one
roost provides optimal conditions for parasites to synchronise
their life cycle as closely as possible to that of its host.
On the other hand, the possibility of finding adequate microclimates
within a roost during pregnancy and lactation is
probably thought to favour roost philopatry (Harbusch and
Racey 2006). Site-switching behaviour within one large roof
appears to be a convenient trade-off, enabling high survival
rates of the young and avoiding high parasite loads.
Acknowledgments We are very grateful to J. Gaisler for valuable
comments on the manuscript and G. Filby for correction of English.
The study was supported by grant no. 206/07/P098 of the Science
Foundation of the Czech Republic and the Czech Bat Conservation
Trust, and by grants from the Ministry of Environment and the Ministry
of Education, Youth and Sports of the Czech Republic no.
MSM0021622416.
References
Aldana E, Abramson CI, Lizano E, Vegas R, Sulbaran-Romero E (2008)
Learning and orientation to odour in the bug Rhodnius prolixus Stal
1859 under laboratory conditions. Parasitol Res 103:587–594
Bartonička T (2008) Cimex pipistrelli (Heteroptera, Cimicidae) and the
dispersal propensity of bats: an experimental study. Parasitol Res
104:163–168
Bartonička T, Gaisler J (2007) Seasonal dynamics in the numbers of
parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost
switching in bats (Chiroptera, Vespertilionidae). Parasitol Res
100:1323–1330
Dubinin VB (1947) Ekologicheskie nabludeniya nad krovososushchimi
klopami sem. Cimicidae Daurskoi stepi. Entomol Oboz
29:232–246, In Russian
East ML, Höner OP, Wachter B, Wilhelm K, Burke T, Hofer H (2009)
Maternal effects on offspring social status in spotted hyenas.
Behav Ecol 20:478–483
Parasitol Res (2012) 111:1233–1238 1237
Entwistle AC, Racey PA, Speakman JR (2000) Social and population
structure of a gleaning bat, Plecotus auritus. J Zool London 225:11–17
Evans LN (2009) Roosting behaviour of urban microbats: the influence
of ectoparasites, roost microclimate and sociality. PhD thesis,
Faculty of Veterinary Science, University of Melbourne
Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming
costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host
(Myotis myotis). Proc R Soc Lond B Biol Sci 268:2071–2075
Harbusch C, Racey PA (2006) The sessile serotine: the influence of
roost temperature on philopatry and reproductive phenology of
Eptesicus serotinus (Schreber, 1774) (Mammalia: Chiroptera).
Acta Chiropterol 8:213–229
Hase A (1917) Die bettwanze (Cimex lectularius L.) ihr leben und ihre
bekämpfung. Monogr Angew Entomol 1 (Z Angew Entomol 4,
Beiheft I)
Hase A (1930) Weitere versuche zur kenntnis der bettwanzen Cimex
lectularius L. und Cimex rotundatus Sign. (Hem. Rhinch.). Parasitol
Res 2:368–418
Henshaw RE (1960) Responses of free-tailed bats to increase in cave
temperature. J Mammal 41:396–398
Johnson CG (1960) The relation of weight of food ingested to increase
in body-weight during growth in the bed-bug, Cimex lectularius
L. (Hemiptera). Ent Exp Appl 3:238–240
Jones RM (1930) Some effects of temperature and humidity as factors
in the biology of the bedbug (Cimex lectularius Linn.). Ann
Entomol Soc Am 23:105–119
Kemper H (1936) Die bettwanze und ihre bekämpfung. Zeitt Kleintierk
Pelztierk 12:1–107
Kerth G, Weissmann K, König B (2001) Day roost selection in female
Bechstein's bats (Myotis bechsteinii): a field experiment to determine
the influence of roost temperature. Oecologia 126:1–9
Kolb A (1950) Beiträge zur Biologie einheimischer Fledermäuse. Zool
Jb (Syst) 78:547–572
Kunz TH, Fenton MB (2003) Bat ecology. University of Chicago, Chicago
Licht P, Leitner P (1967) Behavioral responses to high temperatures in
three species of california bats. J Mammal 48:52–61
Lourenço SI, Palmeirim JM (2004) Influence of temperature in roost
selection by Pipistrellus pygmaeus (Chiroptera): relevance for the
design of bat boxes. Biol Conserv 119:137–285
Lourenço SI, Palmeirim JM (2008) Which factors regulate the reproduction
of ectoparasites of temperate-zone cave-dwelling bats?
Parasitol Res 104:127–134
Lučan RK (2006) Relationships between the parasitic mite Spinturnix
andegavinus (Acari: Spinturnicidae) and its bat host, Myotis
daubentonii (Chiroptera: Vespertilionidae): seasonal, sex- and
age-related variation in infestation and possible impact of the
parasite on the host condition and roosting behaviour. Folia Parasitol
53:147–152
Marx R (1955) Ueber die Wirtsfindung und die Bedeutung des artsspezifischen
duftstoffes bei Cimex lectularius Linné. Parasitol Res
17:41–72
Mislin H (1942) Zur biologie der Chiroptera. I. Beobachtungen im
sommerquartier der Myotis myotis Borkh. Rev Suisse Zool
49:200–206
Petri B, Pääbo S, von Haeseler A, Tautz D (1997) Paternity assessment
and population subdivision in a natural population of the larger
mouse-eared bat Myotis myotis. Mol Ecol 6:235–242
Reckardt K, Kerth G (2007) Roost selection and roost switching of
female Bechstein’s bats (Myotis bechsteinii) as a strategy of
parasite avoidance. Oecologia 154:581–588
Reinhardt K, Siva-Jothy MT (2007) Biology of the bed bugs (Cimicidae).
Annu Rev Entomol 52:351–374
Rivnay E (1932) Studies in tropisms of the bed bug Cimex lectularius
L. Parasitology 24:121–136
Schneider M, Hammer M (2006) Monitoring the greater mouse-eared
bat Myotis myotis on a landscape scale. In: Hurford C, Schneider
M (eds) Monitoring nature conservation in cultural habitats.
Springer, the Netherlands, pp 231–146
Southwood TRE (1954) The production of fertile eggs by Cimex
pipistrelli Jenyns (Hem., Cimicidae) when fed on human blood.
Entomol Monthly Mag 40:35
Stutt A, Siva-Jothy M (2001) Traumatic insemination and sexual
conflict in the bed bug Cimex lectularius. Proc Natl Acad Sci
USA 98:5683–5687
Usinger RL (1966) Monograph of Cimicidae (Hemiptera—Heteroptera).
Entomological Society of America, College Park
Walter G (1996) Zum ektoparasitenbefall der fledermäuse und den
potentiellen auswirkungen. Myotis 34:85–92
Whitaker JO Jr (1998) Life history and roost switching in six summer
colonies of eastern Pipistrelles in buildings. J Mammal 79:651–659
Willis CKR, Brigham MM (2004) Roost switching, roost sharing and
social cohesion: forest-dwelling big brown bats, Eptesicus fuscus,
conform to the fission–fusion model. Anim Behav 68:495–505
Willis CKR, Kolar KA, Karst AL, Kalcounis-Rueppell MC, Brigham
RM (2003) Medium- and long-term reuse of trembling aspen cavities
by big brown bats (Eptesicus fuscus). Acta Chiropterol 5:85–90
Zahn A, Rupp D (2004) Ectoparasite load in European vespertilionid
bats. J Zool 262:383–391
1238 Parasitol Res (2012) 111:1233–1238
8.4 Hostitelská specifita štěnic
WAWROCKA K. & BARTONIČKA T., 2013
Two different lineages of bedbug (Cimex lectularius) reflected in host specificity.
Parasitology Research, 112: 3897-904
ORIGINAL PAPER
Two different lineages of bedbug (Cimex lectularius) reflected
in host specificity
Kamila Wawrocka & Tomáš Bartonička
Received: 7 June 2013 /Accepted: 12 August 2013 /Published online: 28 August 2013
# Springer-Verlag Berlin Heidelberg 2013
Abstract Co-speciation between host–parasite species is
generally thought to result in mirror-image congruent phylogenies.
For the last several centuries, many bat species have
been turning synanthropic, especially those that are hosted by
bedbugs in Europe. There is evidence of only limited gene
flow from the population of people to the population of bats.
This study was focused on comparison of survival, development,
and the reproduction rate based on cross-feeding experiments.
In our research, we used two bedbugs groups of Cimex
lectularius—bat- and human-associated and respectively as
specific/non-specific host bat and commercial human blood.
Both lineages show different behavior according to their host
preferences. During the bat blood experiment, we found significant
differences between both human- and bat-associated
bedbugs (Log rank test fourth χ2
=9.93, p >0.05; fifth χ2
=
11.33, p <0.05), while no differences occurred with the human
blood experiment between the survival levels. In molting,
differences between both groups were significant particularly
in the case of the bat blood experiment (fourth χ2
=5.91, p <
0.05). In the case of the bat blood experiment, we found a
higher probability of molting in bat-associated groups than in
human-associated groups. In the case of the human blood
experiment, molting probability was stable in both specific
and non-specific, showing similar pattern in both cases for all
stages. Our results indicate an occurrence of two ecotypes
within the one species C. lectularius. These findings support
earlier data about morphological and mitochondrial DNA
differences. The differentiation of both lineages fits the concept
of specific host choice.
Introduction
Host specificity and anatomical and morphological adaptations
are essential for understanding the variability of life
strategies and the evolution of parasitic species. There is a
wide list of parasites that are connected with a host via their
life cycle and that fact, next to dispersal limitations, decrease
potential host switching and limit host’s range. Most parasites
occur on a restricted number of hosts and show some evidence
of specificity. Specialization for particular hosts may result by
fidelity to different hosts and sympatric occurrence at the same
time, host-associated genetic differentiation, and/or restricted
but appreciable mutual gene flow (Dres and Mallet 2002).
Under such conditions, closely related parasites may be specialized
in a particular host. Poulin (2007) described two host
choices by parasite: (1) encounter filter, when parasite excludes
the host which he can not colonize and feed on because
of behavioral or ecological reasons and (2) compatibility filter,
excluding all host individuals on which parasite can not feed
because of morphological, physiological, and immunological
reasons. Host specificity was defined by Dick and Patterson
(2007) as a degree to which a parasite species occurs in
association with host species. Host-specific parasites generally
have a major-primary host (5 % or more host individuals are
infested) and a few less frequently used hosts (Tripet et al.
2002). Even generalists show a preference for some species
above others (Tripet and Richner 1997; Johnson et al. 2002).
The bedbug, Cimex lectularius Linnaeus, 1758, is likely
the most widely known cimicid species. Fast ontogenesis,
high reproductive potential, mobility, and at the same time, a
hidden way of life make bugs (Cimicidae) important ectoparasites.
Despite the fact that bedbugs were found on 8 species
of birds, 10 rodents and mustellids, 10 bat species, and
humans, we recognized only two primary hosts—human and
the greater mouse-eared bat (Myotis myotis) (Povolný 1957).
Since other hosts have different in ecology and behavior, their
infestation is probably relatively recent (Povolný and Usinger
K. Wawrocka (*) :T. Bartonička
Department of Botany and Zoology, Masaryk University,
Kotlářská 2, 611 37 Brno, Czech Republic
e-mail: kamila.freeme@gmail.com
T. Bartonička
e-mail: bartonic@sci.muni.cz
Parasitol Res (2013) 112:3897–3904
DOI 10.1007/s00436-013-3579-9
1966; Usinger 1966); the bedbug represents an optimal model
for a study on initial stages of host specialization. Since the
last decade, many studies of re-emerging bedbugs in USA and
Europe were published (Romero et al. 2007; Reinhardt et al.
2008).
In some cases, individuals from the Cimicidae family,
during the absence of the natural host, are able to switch on
non-specific host (Cimex pipistrelli, Whyte et al. 2001; Cimex
dissimilis, Smaha 1976). But to make the substitute host
proper for parasites, it has to fulfill certain conditions, especially
morphological, physiological and behavioral. As
Reinhardt and Siva-Jothy (2007) proven, such limitation
could be in some cases the size of the red cells. Erythrocytes
diameter can influence sucking ability (e.g., chicken erythrocytes
are almost twice as large as those in humans, 11 to
6 μm). Moreover, as was shown before, also sex, age, and
reproductive status has an influence on the reproduction of
parasites (Lourenço and Palmeirim 2008).
Recent studies suggest that Central European populations of
some bat species have shifted their roosting strategy in the last
decade, with prefab houses becoming places of their most
frequent occurrence. Large-scale renovations of those objects,
currently performed in Central Europe, pose a serious threat to
populations of several bat species. In cases when the bats
switch their roosts, or they are to dislodge from shelters by
renovations of houses, people complain repeatedly about the
presence of cimicids in their flats. These bugs intensively feed
on people (T. Bartonička, P. Schnitzerová personal observation).
These records not only come from C. pipistrelli, which is
more often found on bat hosts, but also from C. lectularius.
The ability of C. pipistrelli in attacking people and sucking on
them was confirmed, but they are not able to develop and
undergo a full cycle. Adults bugs that were fed on human blood
and laid eggs were successful but hatched larvas did not want to
suck human blood (Southwood 1953). According to previous
papers, it seems that blood meal temperature, not its specificity,
play a crucial role in blood feeding experiments (Moloo 1971).
Balvín et al. (2012) suggests that switches between the
human- and bat-associated groups of C. lectularius are only
occasional since their split and that the bedbugs mostly switched
from humans to bats. Beside the host choice or less fitness of
hybrids, this could be also a reason for the degree and shape of
the mutual gene flow; nevertheless, the limited evidence of the
contact of the two populations (bat- and human-associated
bugs), shows that bats could serve as reservoirs, covers the
temporary absence of the primary host, and can contribute to
the current dramatic spread of the bedbug among humans.
Moreover, some previous studies (e.g., Usinger 1966;
Balvín et al. 2012) show that bedbugs are also adapted to their
host morphologically. Balvín et al. (2012) shows differences
in relative leg lengths, i.e., longer legs in human-associated
bedbugs and shorter, stronger legs and more hair in batassociated
bedbugs. It also shows differences within widths
and lengths of rostral segments and dimension of antennal
segments or eyes. If these differences occur, we can expect
differences as well on an ecological and developmental level
(Usinger 1966).
To find out the existence of host specificity within bedbug
C. lectularius, we carried out an experiment which is supposed
to show not only the ability to suck on different hosts
but also to illustrate different survival between two lineages of
bedbugs (bat and human associated) under specific and nonspecific
host feeding. The aim of the study was to check what
and if there are some reasons for host choice as specific ones
and how the host choice influence on bugs life expectancy,
speed of molting, or mortality.
Material and methods
Sampling of bedbugs
Bedbugs (C. lectularius) associated with bats were sampled
from a nursery colony of greater mouse-eared bats (M.
myotis) roosted under roofs of the church in Hanušovice
(north Moravia, Czech Republic). Other samples of bedbugs
associated with human host were sampled from hostels in the
cities of Ostrava and Bohumín (north Moravia, Czech
Republic). Bugs were collected with soft forceps and exhausters
into small plastic boxes (10×10×5 cm) lined with
soft paper. Together, we had 27 samples (one female and a few
males) for each host lineage i.e., human- and bat-associated
bedbugs in each experiment. In each tube appeared different
stages (from egg–adult).
Equipment and experimental settings
During segregation and forming groups, we avoided infestation
of samples with eggs or instars from delivered tubes and
chose only adult individuals. To sort the samples, individual
bedbugs were immobilized by sudden “freezing” at 0 °C for
10 min. Experimental groups (one female and one or more
males) were stored in separate plastic pellucid tubes (6×1 cm).
Each tube was equipped with a piece of paper 4×1 cm to let
the bedbugs move, defecate, and lay eggs on it. All tubes were
numbered and tightly closed with a piece of cotton.
Afterwards, they were positioned in a thermostatically controlled
apparatus (ST2, POL-EKO Aparatura, Poland) under
stable temperature (27±0.1 °C) and humidity (75±10 %)
which according to Omori (1941) and Usinger (1966) was
best for the development of C. lectularius. Humidity was
controlled using water in a Petri dish on the bottom of the
glass jar with samples and damp cotton. Bugs were fed every
4 days. To facilitate observations during everyday checks and
feeding, up-to-date dead individuals and rest from after
molting were taken out and stored separately according to
3898 Parasitol Res (2013) 112:3897–3904
particular instars. All experiments were carried out between
April and October 2012.
Bat blood feeding
Special cylinder tube with one bat and a sample of the bedbugs
were placed together in a dark thermostatically controlled unit
(30 °C) for 15 min (cf. Usinger 1966 or Giorgi et al. 2004). To
reduce stress for animal and to avoid antiparasitic behavior
including eating bugs, the bat was covered with dressing gauze
and situated in a feeding tube. Before putting bugs into the
feeding tube, they were counted to be sure that afterwards, all of
them were collected back. After feeding period, the bat was
then taken out from the tube, carefully revised, especially wing
membrane, ears, and uropatagium, and bugs that still were
attached into the bat’s body were delicately removed with
entomological soft tweezers to counteract crushing, especially
very soft instars. The number of bugs and their feeding status
(fed, unfed) were determined. In total, two non-reproducing
females of Vespertilio murinus and two males of M. myotis
were used and the bats were changed after feeding each two
bug groups. Bats were fed ad libitum with a mixed diet
consisting of crickets (Acheta sp.) and mealworms (Tenebrio
molitor) and after experiments, returned back to the colony.
The bats were captured, handled, and temporarily kept in
captivity under the license no. 922/93-OOP/2884/93 and 137/
06/38/MK/E/07 of the Ministry of Environment of the Czech
Republic. The author has been authorized to operate with freeliving
bats according to the certificate of competency no. 104/
2002-V4 (§ 17 of the law No. 246/1992).
Human blood feeding
Human blood for feeding (laboratory commercial blood,
Japan Medical Supply, B+) was stored in a fridge. Durex
condoms were tightly fitted on the plastic tube, which perfectly
fit over bug-breeding tubes. During artificial feeding, blood
was warmed up to 45 °C in the cylinder and 5 ml of blood was
added to each roller. It was crucial to give bugs access to the
blood meal, thus, the situate roller was low enough and
covered all surface of the condom membrane with blood (cf.
Montes et al. 2002). Feeding tubes were closed and thermostatically
controlled under stable temperature 27 °C. The most
suitable blood temperature was experimentally established on
37–38 °C. Too high or too low (<35 and >38 °C) didn’t attract
bugs (K. Wawrocka, personal observation). Feeding was continued
till the moment when ca 80 % of individuals had taken
the blood.
Statistical analysis
All variables showed a normal distribution after log transformation.
SPSS for Windows 7.0 (IBM Statistics 19) was used
for all statistic analysis. A mortality (molting) of 50 % in a
sample was considered significant to finish the experiment and
such a session was marked as complete in the database. Other
groups were evaluated as censored. The differences in survival
rate and molting speed among age groups were tested using the
Kaplan–Meier survival functions. For the Cox proportional
hazards model, the chi-square value was estimated as a function
of the log-likelihood for the model with all covariates. It was
suspected that the effect of the treatment (exposure to different
host) on the underlying hazard was not constant; that is, that the
proportionality assumption may be violated. To check the
differences in molting and survival rate among age groups
models, we used the Log rank test. We also used the
Wilcoxon test to compare survival distribution among groups.
Weibull regression was used to estimate molting probability for
certain instars in both human and bat-associated bedbugs.
Differences between specific and non-specific hosts in amount
of the days after which they are able to undergo molting were
tested using Mann–Whitney U test.
Results
Survival at different host-associated bedbugs
During analysis, we excluded individuals who undergo
molting or were alive. No different changes were found in
the survival rate within instars in the case of bat blood in batassociated
bedbugs, specific host (Kaplan–Meier survival test,
χ2
=7.56, df =4, n.s.) neither in the case of human-associated,
non-specific host (χ2
=4.61, df =4, n.s.) (Fig. 1). While we
compared both lineages fed on bat blood, we found statistically
significant differences in the fourth and fifth instars at
survival rate (Log rank test, fourth instars χ2
=9.93, p <0.05
and fifth instars χ2
=11.33, p <0.05). Cox proportional hazards
model for bat blood experiment showed that the differences
between bat and human-associated bugs are significant
(χ2
=22.51, df =9, p =0.007).
Same tests were made also for human blood experiment,
where no statistical differences were found among instars in
human-associated bedbugs and specific host (Kaplan–Meier
survival test, χ2
=7.56, df =4, n.s.), neither in bat-associated
bedbugs and non-specific host (χ2
=2.08, df =4 n.s.). While
comparing both associated groups fed on human blood, no
statistically significant differences between instars were
found. Cox model for human blood experiment compared
bat- and human-associated bugs and did not show statistically
significant differences (χ2
=15.28, df =9, n.s.).
Different molting in host lineages
Evaluating the different molting rate among instars and host
lineages we conducted by Kaplan–Meier survival test where
Parasitol Res (2013) 112:3897–3904 3899
we tested the level of molting. We excluded dead individuals
and those who didn’t undergo molting, but survived.
In the case of bat blood experiment, we found no statistically
significant differences among all instars of bat and
human-associated bugs (Kaplan–Meier survival test, χ2
=
5.023, df =4, n.s.; χ2
=5.242, df =4, n.s.). When we compared
both host lineages between each other, we found that a
statistically significant difference exists in the molting of
fourth instars (Log rank test, fourth instars χ2
=5.91, p <
0.05). Nevertheless, the Cox model did not show any statistically
significant differences (χ2
=14.61, df =9, n.s.).
We tested in the same way human blood experiments and
found no significant differences among instars of humanassociated
bedbugs (χ2
=1.16, df =4, n.s.) but we found
days
Cumulativenumberofsurvivors
Fig. 1 Cumulative survival function for first–fifth instars, showing the
fraction surviving according to different blood meal (specific—a, c/nonspecific—b,
d). Kaplan–Meier survival functions of instars in case of bat
blood in bat-associated bedbugs (a); in human-associated (b); survival
functions of instars in case of human blood in human-associated (c) and
bat-associated bedbugs (d). “Complete” means at least 50 % mortality in
particular instars
3900 Parasitol Res (2013) 112:3897–3904
differences in the case of bat-associated bugs (χ2
=11.66, df =
4, p =0.02). Comparisons of both human- and bat-associated
bug lineages showed that there is no significant difference
between them. Cox model did not show significant differences
between molting in both lineages (χ2
=10.59, df =9, n.s.).
Probability of molting
Different probabilities of undergoing molting in time (days)
for certain instars is described by Weibull regression. We
found significant differences between bat- and humanassociated
bedbugs in the case of bat blood experiment
(χ2
=75.18, df =9, p <0.001) as well in the case of human
blood experiment (χ2
=54.04, df =4, p <0.001). Batassociated
bug shows low molting in earlier instars (first–
third) and higher in later instars (fourth, fifth) and in same
case, human-associated bugs had the highest molting probability
of early instars (second) and the lowest in later instars
(fourth). In the case of human blood experiment, molting
probability was stable in both specific and non-specific showing
similar pattern in both cases for all instars (Fig. 2).
Time period between ecdyses
We found the differences between specific and non-specific
hosts in the amount of days after which they are able to undergo
molting. Analyzed data starts from the first instar till becoming
adults. Mann–Whitney U test showed in both cases that ecdyses
time differs significantly only in bat blood experiment (U =5.0,
n.s.) as in human blood experiment (U =11.5, n.s.) (Table 1).
Discussion
Although in the course of research in the last decades there
have been found numerous occasional hosts of bedbugs
(Cimex lectularius), the primary hosts are only bats and
humans (Usinger 1966). Previous studies have suggested that
Probabilityofmetamorphosis
days
Fig. 2 Probability of molting. Weibull regression for first–fifth instar
showing probability of metamorphosis according to different blood meal
(specific a, c/non-specific b, d). Molting probability of instars in case of
bat blood in bat-associated bedbugs (a), human-associated bedbugs (b),
regression model for human blood experiment in human-associated bedbugs
(c), and bat-associated bedbugs (d)
Parasitol Res (2013) 112:3897–3904 3901
bedbugs’ primary host were bats (Povolný and Usinger 1966)
and from them, they were transferred on humans. Recent
studies (Balvín et al. 2012a) showed an interesting hostassociated
differentiation of the population of the bedbug on
both morphological and molecular data.
We are seeing probably a gradual ecological niche diversification
and perhaps the origin of reproductive isolating barriers.
From this perspective, the study of the host in C.
lectularius specificity seems to be a good model for the study
of microevolutionary mechanisms connected with speciation
and adaptive radiation within the group (Fig. 3).
In our study, we used two host lineages of C. lectularius—
bat- and human-associated bedbugs. In cross-feeding experiment
type of the host, specific/non-specific, seems to have an
impact on survival, molting, and development rate in both
cross-feedings conducted in vitro. The most common bat host
of the bedbug, M. myotis, is originally the cave-roosting bat. It
is perhaps a coincidence that this species began to inhabit
buildings all over Europe only several centuries ago.
Moreover C. lectularius is not found in their cave roosts in
Europe (Simov et al. 2006), likely because of the climatic
conditions in caves. The only exception in central Europe is
the Hranická abyss, which roost a large nursery colony of M.
myotis, but the bedbugs were never found on emerging bats
despite repeated nettings (Z. Řehák in litt.). So, while M.
myotis and human very often inhabit buildings, populations
of bat and human-associated bedbugs show a minimum exchange
of individuals between them (Balvín et al. 2012).
Balvín et al. (2012) found that nursery colonies of greater
mouse-eared bat are more often parasite by C. pipistrelli than
C. lectularius and moreover, both bug species have never
been found together in one bat roost. However, on human
host, C. pipistrelli is found very rare always in anecdotic
observations, especially if an infested apartment is near to
temporary abandoned bat roost and hungry bugs are looking
for food. It has long been known, that C. pipistrelli can feed
on human host, but it has a significantly lower survival rate
than on a specific host bat (Usinger 1966), and at the same
time, there is a notable reproductive barrier between C.
lectularius and C. pipistrelli. This isolation of particular bug
populations shows a very limited capacity to transport and
dispersion to another or even new host (cf. Giorgi et al. 2004).
Host switching is usually complicated, especially when the
primary host has a very different life strategy than the potential
new host. Bat-associated bugs usually inhabit only these parts of
buildings attics which are suitable for bats, but from there, they
have only a limited ability to move (Bartonička and Růžičková
2012). The frequency of movements between bugs and man is
hard to monitor and on this issue, we have only limited information
(Balvín et al. 2012). Adult bedbugs can travel at a speed
of 126 cm per minute (Hase 1917) and therefore, they should be
able to reach large distances very quickly. When bugs can follow
fecal spots, food prints, or pheromone trails by dragging the
engorged bugs, (Hase 1917; Aldana et al. 2008) they can
successfully travel to very distant hosts (Kemper 1936). In cases
when the host is available, bat-associated bugs have no reason to
find a new one. The probability of sucking on humans is
therefore not reduced by the distance of infested attics from the
people occupied parts of buildings, but also by human effort to
eliminate new bug population in the case of successful transmission.
Moreover, no cases of movement of C. lectularius
from bat host to people in the same building have yet been
published. Bugs are adapted to long starving periods. It might
confirm Romero et al.’s (2007) experiment, where individuals
starved for a shorter time showed much higher activity and
movement level than those who were starving for a few weeks.
This might help them to limit energy loss connected with
movements and decrease metabolism. It appears, therefore, that
the bugs are adapted to wait rather than to actively search the
Table 1 Ecdyses between undergoing molting in certain stages (first— adult) for specific and non-specific host in bat and human blood experiment
(days ± SD)
Experiment/age
stages
1st (Specific/
non-specific)
2nd (Specific/
non-specific)
3rd (Specific/
non-specific)
4th (Specific/
non-specific)
5th (Specific/
non-specific)
Adults (both sexes)
(specific/non-specific)
Bat blood 5±0.81/6±0.74 4±0.89/5±0.74 3±0.64/6±1.12 4±0.67/5±0.48 4±0.90/6±0.95 7±0.32/9±0.46
Human blood 4±0.96/6±0.87 3±0.68/5±0.79 7±0.87/10±1.09 8±0.46/15±1.47 4±0.64/2±0.44 9±0.93/7±1.10
Fig. 3 Bed bug (Cimex lectularius) bat-associated. Visible main characteristic
differing them from human-associated bugs: stronger and shorter
legs, more hair, difference in antennal segments dimension and eye which
is connected with adaptations to certain host (by O. Balvin)
3902 Parasitol Res (2013) 112:3897–3904
host. Such strategy could lead between the two host-associated
bug groups to higher degree of mutual isolation.
Blood sucking parasites may favor and choose higher
quality hosts who can give them a better blood meal. On the
other hand, such host might be hard to feed on (Møller 2000;
Khokhlova et al. 2007). Our experiments clearly show the
importance of the specific host. However, it can not be assumed
that the quality of the blood of a bat and human should
be fundamentally different, because other studies showing the
gradual isolation of both bedbug populations associated with
different host lineages (Povolný and Usinger 1966). As suggested
before (Hase 1926; Tawfik 1968), we did not find any
significant differences between bat and human red cells diameter
(Wawrocka in prep.). The cause of low survival rate on
non-specific host might be in immunocompetence (T cell
response) and the condition of the host, as evidenced by the
numerous proofs has been "well-fed host strategy" (Christe
et al. 2000). Previous research showed already differences at
morphological level in case of bedbug according to the host
type—human or bat (Balvín et al. 2012). Host specificity has
impact not only on the parasite himself but also on his host,
including the human. Preferences to some hosts can, on one
hand, decrease feeding efficiency but on the other hand, make
it easier for parasite to feed on host, whose immune system
and ecology is already well known to him. As Dick et al.
(2009) suggested that lack of some barriers that occur in
nature can break down host specificity.
Bats, as partly synanthropic species, adapted to new conditions
and also treat connections with human population
expansion that impact their natural landscape, food decrease
by habitat adaptations, and degradation, forcing bats to use
alternative roosts and foraging sites and move to cities. They
start to share shelters with humans (attics, churches, basements,
vacant buildings, etc.), what provided them cozy,
warm, and safe places that they would not find in the wild.
Bat–human conflict is a well-known phenomenon. Bat noises,
droppings, and presence itself is a big problem for bat conservation.
What more is that together with bats appear also their
parasites as cimicids. It was suspected that bats are the one of
the main reservoirs of global recuperation of bedbug populations
(Szalanski et al. 2008) thus they do not possess other
than roosts switching (Bartonička and Gaisler 2007) the ability
to reduce infestation. That fact could unfortunately deepen
antipathy to bats. Nevertheless, there is no evidence at the
genetical level that bats could be responsible for their expansion
(Balvín et al. 2012) which is much more wider in the case
of, for example, poultry (Szalanski et al. 2008). Spreading this
information and knowledge among society is crucial in bat
conservation.
This study showed the significant limitations in the ability
of survival and molting in confusion of the two primary bug
hosts and it is likely to fit the concept of host races according
to Dres and Mallet (2002). The next step to elucidate the
taxonomical status of both bedbug lineages could be to verify
whether between the two ecotypes, are there any reproductive
mechanisms limiting the free hybridization of bedbugs.
Acknowledgments We are very grateful to J. Gaisler for his valuable
comments on the manuscript and Martin Toman for help with fieldwork
and sampling bedbugs associated with human host. This study was
supported by grants from the Ministry of the Environment and the
Ministry of Education, Youth and Sports of the Czech Republic No.
MSM0021622416,grant No. MUNI/A/0976/2009.
References
Aldana E, Abramson CI, Lizano E, Vegas R, Sulbaran-Romero E (2008)
Learning and orientation to odor in the bug Rhodnius prolixus Stal
1859 under laboratory conditions. Parasitol Res 103:587–594.
doi:10.1007/s00436-008-1014-4
Balvín O, Munclinger P, Kratochvíl L, Vilímová J (2012) Mitochondrial
DNA and morphology show independent evolutionary histories of
bedbug Cimex lectularius (Heteroptera: Cimicidae) on bats and
humans. Parasitol Res 111:457–469
Bartonička T, Gaisler J (2007) Seasonal dynamics in the numbers of
parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost
switching in bats (Chiroptera, Vespertilionidae). Parasitol Res
100:1323–1330
Bartonička T, Růžičková LL (2012) Bat bugs (Cimex pipistrelli) and their
impact on non-dwelling bats. Parasitol Res 111:1233–1238
Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a parasitic
mite (Spinturnix myotis) in relation to the reproductive cycle and
immunocompetence of its bat host (Myotis myotis). Ecol Lett
3:207–212
Dick CW, Patterson BD (2007) Against all odds: explaining high host
specificity in dispersal-prone parasites. Int J Parasitol 37:871–876
Dick CW, Esberard CEL, Graciolli G, Bergallo HG, Gettinger D (2009)
Assessing host specificity of obligate ectoparasites in the absence of
dispersal barriers. Parasitol Res 105:1345–1349
Dres M, Mallet J (2002) Host races in plant-feeding insects and their
importance in sympatric speciation. Philos Trans R Soc B-Biol Sci
357:471–492
Giorgi MS, Arlettaz R, Guillaume F, Nusslé S, Ossola C, Vogel P, Christe
P (2004) Casual mechanisms underlying host specificity in bat
ectoparasites. Oecologia 138:648–654
Hase A (1917) Die Bettwanze (Cimex lectularius L.), ihr Leben und ihre
Bekampfung. Z Angew Entomol 4, 144 pp
Hase A (1926) Über verfahlen zur Untersuchung von Quaddeln und
anderen Hauterscheinungen nach Insektenstichen. Z Angew
Entomol 1926:243–249
Johnson KP, Williams BL, Drown DM, Adams RJ, Clayton DH (2002)
The population genetics of host specificity: genetic differentiation in
dove lice (Insecta: Phthiraptera). Mol Ecol 11:25–38
Kemper H (1936) Die Bettwanze und ihre Bekämpfung. Z Kleintierk
Pelztierk 12:1–107
Khokhlova IS, Fielden LJ, Degen AA, Krasnov BR (2007) Feeding
performance of fleas on different host species : is phylogenetic
distance between hosts important? Parasitology 139:60–68
Lourenço S, Palmeirim JM (2008) Which factors regulate the reproduction
of ectoparasites of temperate-zone cave-dwelling bats? Parasitol
Res 104:127–134
Montes C, Cuadrillero C, Villela D (2002) Maintenance of a laboratory
colony of Cimex lectularius (Hemiptera: Cimicidae) using an artificial
feeding technique. J Med Entomol 39:675–679
Parasitol Res (2013) 112:3897–3904 3903
Møller AP (2000) Survival and reproductive rate of mites in relation to
resistance of their barn swallow hosts. Oecologia 124:351–357
Moloo SK (1971) An artificial feeding technique for Glossina.
Parasitology 63:507–512
Omori N (1941) Comparative studies on the ecology and physiology of
common and tropical bed bugs, with special references to the
reactions to temperature and moisture. J Med Assoc Formosa
60:555–729
Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton
University Press, Princeton
Povolný D (1957) Kritická studie o štěnicovitých (Het. Cimicidae) v
Československu. [Review study on cimicids (Het. Cimicidae) in
Czechoslovakia] (in Czech). Folia Zool 6:59–80
Povolný D, Usinger RL (1966) The discovery of a possibly aboriginal
population of the bed bug (Cimex lectularius Linnaeus, 1958). Acta
Mus Moraviae, Sci biol 51:237–242
Reinhardt K, Siva-Jothy MT (2007) Biology of the bed bugs (Cimicidae).
Ann Rev Entomol 52:351–374
Reinhardt K, Harder A, Holland S, Hooper J, Leake-Lyall C (2008) Who
knows the bed bug? Knowledge of adult bed bug appearance
increases with people age in three counties of Great Britain. J Med
Entomol 45:956–958
Romero A, Potter MF, Haynes KF (2007) Insecticide resistance in the
bedbugs: a factor in the pest sudden resurgence? J Med Entomol
44:175–178
Simov N, Ivanova T, Schunger I (2006) Bat-parasitic Cimex species
(Hemiptera: Cimicidae) on the Balkan Peninsula, with zoogeographical
remarks on Cimex lectularius, Linnaeus. Zootaxa 1190:59–68
Smaha J (1976) Die Fledermauswanze, Cimex dissimilis (Horvath)
(Heteroptera: Cimicidae), als Lastling in Paneeltafelhausern. Anz
Schädlingsk, Pflanzen, Umweltschutz 49:139–141
Southwood TRE (1953) The production of fertile eggs by Cimex
pipistrelli Jenyns (Hem., Cimicidae) when fed on human blood.
Entomol mon mag XC:35
Szalanski AL, Austin JW, McKern JA, Steelman CD, Gold RE (2008)
Mitochondrial and ribosomal internal transcribed spacer 1 diversity
of Cimex lectularius (Hemiptera: Cimicidae). J Med Entomol
45:229–236
Tawfik MS (1968) Feeding mechanisms and the forces involved in some
blood-sucking insects. Quaest Entomol 4:92–111
Tripet F, Richner H (1997) The coevolutionary potential of a‘generalist’
parasite, the hen flea Ceratophyllus gallinae. Parasitology 115:419–427
Tripet F, Jacot A, Richner H (2002) Larval competition affects the life
histories and dispersal behavior of an avian ectoparasite. Ecology
83:935–945
Usinger RL (1966) Monograph of Cimicidae (Hemiptera – Heteroptera).
Entomological Society of America. Thomas Say Foundation, New
York
Whyte AS, Garnett PA, Whittington AE (2001) Bats in the belfry, bugs in
bed? Lancet 357:604
3904 Parasitol Res (2013) 112:3897–3904
9. Seznam dalších publikací k tématu
Články v recenzovaných časopisech a sbornících
1. Bartonička T., 2007: Bat bugs (Cimex pipistrelli, Heteroptera) and roost switching in
bats. Berichte der Naturforschenden Gesellschaft der Oberlausitz, 15(1): 29-36.
2. Balvín O., Ševčík M., Jahelková H., Bartonička T., Orlova M., Vilímová J., 2013:
Transport of bugs of the genus Cimex (Heteroptera: Cimicidae) by bats in western
Palaearctic. Vespertilio, 16: 43-54.
3. Balvín O., Bartonička T., Simov N., Paunovic M., Vilímová J., 2015: Distribution
and host relations of species of the genus Cimex on bats in Europe. Folia Zoologica,
accepted.
4. Balvín O., Bartonička T., 2014: Cimicids and bat hosts in Czech and Slovak
Republics: ecology and distribution. Vespertilio, 17, accepted.
Konferenčních abstrakta
1. Bartonička T., Řehák Z., 2005: Are changes in internal roost temperature a good
reason for bat movement? Abstracts of Xth European Bat Research Symposium, 21-26
August 2005, Galway, 2005. p. 16.
2. Bartonička T., Řehák Z., 2005: Changes in activity and habitat use of the soprano
pipistrelle Pipistrellus pygmaeus revealed by radio-tracking. Abstracts of 10th
European Bat Research Symposium, Galway, Ireland, 21-26 August. 2005, p. 16.
3. Bartonička T., Řehák Z., 2005: Changes in activity and habitat use of the soprano
pipistrelle Pipistrellus pygmaeus revealed by radio-tracking. Abstracts of 19th
Ogolnopolska Konferencja Chiropterologiczna, Pokrzywna, 4-6 November, 2005, p.
10.
4. Bartonička T., 2006: Bedbugs (Cimicidae): a possible cause of roost switching by
vespertilionid bats. Abstracts of conference – 3rd Bats of Sudety Mts., St. Marienthal,
2006, p. 3.
5. Bartonička T., 2007: Microclimate and bugs (Cimicidae): a possible cause of roost
switching by vespertilionid bats. Abstracts of XIV International Bat Research
Conference in Merida, Mexico, 2007, p. 170.
6. Bartonička T., 2008: Bat bugs (Cimicidae, Heteroptera): a possible cause of roost
switching by bats. Abstracts of XIth European Bat Research Symposium, Rumunia,
Cluj-Napoca, p. 19.
7. Bartonička T., 2008: Vliv úkrytových parazitů, štěnic druhu Cimex pipistrelli
(Heteroptera) na netopýry. Abstrakty z konference Zoologické dny České Budějovice,
2008, s. 24.
8. Růžičková L., Bartonička T., 2009: Jsou štěnice Cimex pipistrelli významným
stresorem i pro filopatriské druhy netopýrů? Abstrakty z konference Zoologické dny
Brno 2009, s. 161.
9. Bartonička T., 2010: Vliv úkrytového parazita na netopýry a rychlost rekolonizace
úkrytu. Abstrakty z konference Zoologické dny Praha 2010, s. 29-30.
10. Růžičková L., Bartonička T., 2011: Ovlivňuje druh hostitele ontogenezi a přežívání
štěnice Cimex pipistrelli? Abstrakty z konference Zoologické dny Brno, 2011, s. 191-
192.
11. Wawrocka K. J., Bartonička T., 2013: Host specifity of bedbugs (Cimex lectularius).
Abstrakty z konference Zoologické dny Brno, 2013, s. 250-251.
12. Wawrocka K., Bartonička T., 2014: Host specificity in bed bugs and its implication
for bat conservation. Abstracts of VIIIth European Bat Research Symposium, Croatia,
2014, p. 165.
13. Wawrocka K. J., Bartonička T., 2014: Multiplex panels of polymorphic microsatellite
loci for bat bug (Cimex pipistrelli) in Central Europe. Abstracts of Xth European
Congress of Entomology, University of York, UK, 2014, p. 145.
14. Wawrocka K. J., Bartonička T., 2014: Erythrocyte size in bats - factor determining
host choice in cimicids (Heteroptera: Cimicidae). Abstracts of VIIIth European Bat
Research Symposium, Croatia, 2014, p. 165.