Turkish Journal of Fisheries and Aquatic Sciences 10: 305-313 (2010)
www.trjfas.org
ISSN 1303-2712
DOI: 10.4194/trjfas.2010.0302
© Published by Central Fisheries Research Institute (CFRI) Trabzon, Turkey
in cooperation with Japan International Cooperation Agency (JICA), Japan
Seasonal Dynamics and Biomass of Mixotrophic Flagellate Dinobryon
sertularia Ehrenberg (Chrysophyceae) in Derbent Reservoir (Samsun,
Turkey)
Introduction
Mixotrophy, known as a nutritional strategy, is a
feeding capacity of certain organisms in autotrophic
and heterotrophic environments. It is mostly used for
protists being phototrophic and phagotrophic. These
organisms can combine heterotrophy and
photototrophy (Stockner, 1988). Protists are
commonly found in coastal and open oceans,
including bays, euphotic zones, mesotrophic and
eutrophic waters from equator to polar areas.
The phenomenon of bacterial ingestion or uptake
unicellular algae by phytoflagellates has been
observed not only recently but also in the past
(Pascher, 1911; Aaronson and Baker, 1959;
Pringsheim, 1963). Mixotrophic species are known in
Beyhan Taş1,
*, Arif Gönülol2
, Erol Taş3
1
University of Ordu, Faculty of Arts and Science, Department of Biology, 52200, Ordu, Turkey.
2
Ondokuz Mayıs University, Faculty of Arts and Science, Department of Biology, 55139, Kurupelit, Samsun, Turkey.
3
Ondokuz Mayıs University, Faculty of Education, Department of Primary Science Education, 55139, Atakum, Samsun,
Turkey.
* Corresponding Author: Tel.: +90.452 2345010; Fax: +90. 452 5174368;
E-mail: beyhantass@gmail.com
Received 18 February 2009
Accepted 01 March 2010
Abstract
Mixotrophic protists, combining both heterotrophy and phototrophy, are found abundantly in eutrophic waters.
Dinobryon sertularia Ehr. from Chrysophyceae (golden algae) are mixotrophic organisms often make up blooms and colony
in pools, lakes and dam reservoirs. This study was carried out in Derbent Dam Lake in the Middle Black Sea Region.
Seasonal dynamics and biomass of D. sertularia were investigated at four stations between February 2001 and July 2002. D.
sertularia consisted of 47-60% in spring, 61-79% in summer, and 82-88% in autumn of all phytoplankton population. In
August 2001, D. sertularia was calculated in the highest amounts numbers (18,740-13,140 cells ml-1
). This species provided
important contributions to phytoplankton biomass. In the present study, it was found that there is an inverse correlation
between water depth and phytoplankton biomass production. According to Bray-Curtis Similarity Indice, 88% similarity was
determined among Station 3, Station 4 and 4-6 m of Station 1. D. sertularia was dominant and common organism in all
seasons. The reservoir water was defined as oligomesotrophic and alkaline characters (pH 7.98), and average temperature was
15.56○
C.
Keywords: Dinobryon sertularia, mixotrophy, phytoplankton, biomass, Derbent Reservoir.
Derbent Rezervuarı’nda (Samsun, Türkiye) Miksotrofik Flagellat Dinobryon sertularia Ehrenberg
(Chrysophyceae)’nın Biyoması ve Mevsimsel Dinamiği
Özet
Fototrofi ile heterotrofiyi birleştiren miksotrofik protistler ötrofik sularda bol bulunurlar. Tatlısu fitoplanktonik
flagellatlılarından olan Dinobryon sertularia Ehr. Chrysophyceae’den (altın sarısı algler), koloni oluşturan, planktonik, göl,
gölet ve baraj gölü fitoplanktonunda zaman zaman aşırı çoğalmalar yapan miksotrofik bir organizmadır. Bu çalışma Orta
Karadeniz Bölgesi’nde yer alan Derbent Baraj Gölü’nde yapılmıştır. D. sertularia’nın mevsimsel dinamiği ve biyoması dört
istasyonda Şubat 2001-Temmuz 2002 arasında incelenmiştir. D. sertularia, ilkbaharda fitoplanktonun %47-60’ını, yazın %61-
79’unu, sonbaharda ise %82-88’ini oluşturmuştur. Ağustos (2001) ayında en yüksek sayılarda kaydedilen D. sertularia
(18.740-13.140 cells ml-1
), bu ayda fitoplankton biyomasına önemli katkı sağlamıştır. Mevcut çalışmada biyomas üretimi ve
derinlik arasında zıt bir ilişkinin olduğu tespit edilmiştir. Bray-Curtis benzerlik indeksine göre 3. ve 4. istasyonlar ile 1.
istasyonun 4-6 m derinlikleri arasında %88 oranında benzerlik kaydedilmiştir. Oligo-mezotrofik karakterli, bazik özellik
gösteren (7,98) ve ortalama sıcaklığı 15,56 °C olan Derbent Rezervuarı’nda D. sertularia her mevsim dominant ve çok yaygın
organizmalar içinde yer almıştır.
Anahtar Kelimeler: Dinobryon sertularia, Miksotrofi, Fitoplankton, Biyomas, Derbent Baraj Gölü.
306 B. Taş et al. / Turk. J. Fish. Aquat. Sci. 10: 305-313 (2010)
many groups such as Chrysophyceae,
Prymnesiophyceae, Xanthophyceae, Dinophyceae and
Cryptophyceae (Porter, 1988). They may reach
similar ingestion rates as purely heterotrophic
flagellates in oceans (Estep et al., 1986; Arenovski et
al., 1995) and lakes (Bird and Kalff, 1986; Sanders et
al., 1989). Besides, they also contribute to the nutrient
supply via ingestion of bacteria, as a carbon source
(Doddema and Van Der Veer, 1983; Nygaard and
Tobiesen, 1993; Li et al., 2000 ).
Mixotrophy is quite prevalent in most of
phytoplanktonic organisms including ciliates,
sarcodines and flagellates as Chrysophyta,
Cryptophyta and Dinophyta. Some genus included in
the phytoplankton communities as Chrysochromulina,
Ochromonas, Dinobryon, Gymnodinium, Peridinium,
Cryptomonas and Rhodomonas were defined as
mixotrophic algae in literature (Sanders and Porter,
1988; Tranvik et al., 1989; Boraas et al., 1992; Jones,
1994). Microalgae are mostly thought as facultative
photosynthetic organisms. However, an important part
of microalgae species have heterotrophic or
mixotrophic growth ability. These organisms can also
display heterotrophic development in most of the
taxonomic classes (Droop, 1974; Hellebust and
Lewin, 1977; Neilsen and Lewin, 1974; Kaplan et al.,
1986). In general, photosynthetic cells can obtain
nutrients from an organic carbon source in insufficient
light conditions. In other words, they have growth
ability in lightness environments. Algae that have
growth ability as heterotrophic and mesotrophic can
increase their biomass at high level by taking
advantage of this feeding strategies.
Chrysophyta members found in fresh waters and
pools are mostly present in winter. They reach
maximum amount in spring and autumn months.
Dinobryon is generally known as a bacteria nourished
as microtrophic.
Dinobryon can growth in the phytoplankton of
both acidic and basic waters. Some species can be
found in the mucilage colonies of Cyanobacteria or on
the frustule of diatom Tabellaria (Prescott, 1951).
Dinobryon can prevalently find in the phytoplankton
of boreal and temperate areas where the water has
poor nutrient and alkalinity. Also, it is very
widespread in the lakes of the areas where the soils
are mountainous and acidic (Canter-Lund and Lund,
1995). The potassium concentration of environment
can be toxic to the most of the freshwater Dinobryon
species. D. sertularia develops in water at 20ºC or
less (Lehman, 1980). Dinobryon including
oligotrophic lake phytoplankton has a high tolerance
to all conditions except low phosphate (Tanyolaç,
1993). Among the Dinobryon genus, there are many
species having a phagocytic strategy in addition to
photosynthesis. D. sertularia feed on bacteria and use
the carbon. These species die in lightness and can not
use the organic carbon. Phagotrophy does not seem to
be dependent on metabolic energy supply in the
species, it is rather dependent on the physiological
state of the cell (Jones and Rees, 1994).
So far, some studies have been made in Derbent
Reservoir (Taş, 2006; Taş and Gönülol, 2007). D.
sertularia, represented with only species in
Chrysophyta division, was quite abundant found in all
months and seem to be a very effective organism in
the phytoplankton biomass. In this study, the
seasonal dynamics and biomass of D. sertularia was
investigated.
Material and Methods
Study Site
Derbent Reservoir (DR) is located on Samsun
province in the Middle Black Sea Region in Turkey
(41°25'06″N-35°49'52″E). The reservoir was made of
rock filling style and constructed on the Kızılırmak
River which is the longest river (1,355 km) in Turkey
(Figure 1). The reservoir was built with aim to control
1
2
3
4
N
1/25000
1
2
3
4
N
1/25000
Figure 1. The map of Derbent Reservoir and the sampling stations for the present study.
B. Taş et al. / Turk. J. Fish. Aquat. Sci. 10: 305-313 (2010) 307
flood
ny
and product energy and irrigation of the Delta
where Ramsar Site (wetland of international
importance). The surrounding of the reservoir is used
as recreational activities. In DR, Rainbow trout
(Oncorhynchus mykiss) aquaculture and natural
fishing have been operated for 20 years. Some of fish
species in the lake are: Cyprinus carpio, Capoeta sp.,
Leuciscus cephalus, and Perca fluviatilis living in the
lake. The hydrological characteristics of DR were
given in Table 1.
The area is characterized by the coastal Black
Sea climate regime. The weather is hot in summer and
mild and rainy in winter. The study area exhibits West
Mediterranean type of rain regime. The amount of
rainfall increases in February (102.4 mm) and
December (68.0 mm) (Anonymous, 2002).
Sampling and Measurements
Samples were collected monthly from four
different stations in DR between February 2001 and
June 2002 (Figure 1). With aim to determine physical
and chemical characteristics, the station 1 (st 1) was
selected from the deepest and the largest zone.
Temperature and oxygen values were measured in all
stations by Oksiguard Handy Mk III digital apparatus.
Other analyses were made by using standard
techniques in water analyses laboratory at Samsun
DSI (APHA, 1992).
Phytoplankton samples were taken from the
surface (0-20 cm) in all stations. Just for st 1, samples
were collected from 2, 4, 6, 8, and 10 m depth, with
2.0 liter capacity standard water sampler acc. to
Ruttner (Hydro-Bios). Organisms in the water were
collected by applying the sedimentation method of
Utermohl (Utermohl, 1958). Counting was made with
Olympus inverted plankton microscope (Lund et al.,
1958). Biomass measure was made by taking into
account of the volume and the weight of the
organisms that its numbers is known. D. sertularia
was identified according to Graham and Wilcox
(2000) and John et al. (2003). BioDiversity Pro 2.0
and SPSS 13.0 software were used in the analyses of
datas.
Results
Frequency coefficient of D. sertularia was
calculated by presence-absence table for quantitative
samples. According to this, the most prevalent species
were recorded as 61-100% at all stations and all
depths of st 1 (Figure 2). D. sertularia was found
significantly dense in the phytoplankton (Figure 3).
Once the seasonal dynamics of D. sertularia had
been investigated, algal blooms were observed in
spring months and the end of summer months (Figure
4). D. sertularia caused little blooms in winter months
but blooms increased in spring months. In all stations,
this amount was changed between 2-88% in the
phytoplankton density. D. sertularia was dominant by
constituting 47-60% of total organisms in spring
months. But, this species was not observed in a
Table 1. The hydrological characteristics of the Derbent
Reservoir
Altitude (m) 60
Height (m) 29
Min. operating code (m) 54.50
Max. operating code (m) 57.50
Max. water level (m) 60.0
Lake area according to min.
operating code (ha)
525
Lake area according to min.
operating code (ha)
1650
Lake volume according to min.
operating code (m3
)
167x106
Lake volume according to max.
operating code (m3
)
213x106
Annual average stream (m3
) 5.4x109
Figure 2. The abundance distribution of Dinobryon sertularia in the depths of the st. 1 and st. 2, 3, 4.
f=(Na/N)X100 (Na: sampling number containing a species, N: All sampling number)
rare present species 1-15%, frequent present species 16-40%, prevalent present species 41-60%, very prevalent species 61-100%.
308 B. Taş et al. / Turk. J. Fish. Aquat. Sci. 10: 305-313 (2010)
Figure 3. The cell density of D. sertularia in the surface waters of the all stations (a) and in the depths of the st.1 (b) within
the total phytoplankton.
Figure 4. The monthly variation at cell density of D. sertularia in all stations and the depths.
stations in May 2001. However, it was recorded as
dominant organism in May 2002. The ratio of D.
sertularia was between 3-18% of the phytoplankton at
the beginning of summer and green algae were
dominant organism in this period (Chlorella vulgaris,
C. ellipsoidea, Tetraedron minimum, T. muticum). At
the end of summer, D. sertularia was found as
dominant organism by making blooms at 79%, 78%,
67% and 61% ratio the stations of 1, 2, 3, and 4,
respectively. Also, blooms occurred in autumn
months. This species was recorded at 82%, 83%, 88%
and 86% ratio in DR phytoplankton in the stations
from 1 to 4, respectively (Figure 5). In August 2001,
it was recorded at the highest amount as 8,740-13,140
cells ml-1
in the surface, 2 m, 4 m, and 6 m depth of st
1. And also, it was recorded as 16,100 cells ml-1
,
18,075 cells ml-1
and 18,525 cells ml-1
in st 2, 3, 4 in
October 2001, respectively. In March 2002, this
species was determined as 7,050 cells ml-1
at 8 m
depth and 9450 cells ml-1
at 10 m depth in st 1 (Figure
4-5).
D. sertularia have provided very important
contributions to the phytoplankton biomass of DR
apart from the st 1. The highest phytoplankton
biomass in the surface stations was enrolled in spring
months and the end of summer months (Figure 6). In
August, the highest biomass recorded as 6.56 µg ml-1
in st 1 and 5.48 µg ml-1
in st 2. The biomass was 2.72
µg ml-1
in st 3, and 1.95 µg ml-1
in st 4. In the middle
of autumn, the highest biomass was found as 6.13 µg
ml-1
in st 4.
The seasonal variation of the biomass in the
surface waters was determined to be similar to st 1,
according to vertical analysis (Figure 6). But, it was
B. Taş et al. / Turk. J. Fish. Aquat. Sci. 10: 305-313 (2010) 309
observed to be decrease in biomass amount towards
depths. The highest biomass was determined as 6.11
µg ml-1
(st 2), 4.97 µg ml-1
(st 3) and 4.60 µg ml-1
(st
4) in August. In October, the biomass was not high at
the surface water of the stations. This amount was
found as 2.36 µg ml-1
and 1.79 µg ml-1
in October.
The highest biomass in March was found as 3.60 µg
ml-1
in 2 m and 3.30 µg ml-1
in 10 m at spring bloom
in 2002. It was calculated as 2.84 µg ml-1
in 10 m in
April.
A Bray-Curtis similarity index was undertaken
by using cluster analysis for the density of D.
sertularia at the surface and from the depths of the
stations. In the end of analysis, the highest similarity
was seen (88.8%) at the surface of the st 3-st 4 and
also 4 m-6 m (88.8%) in the depths of st 1 (Figure 7).
Physical and chemical analysis results of st 1
were given in Table 2. Cation arrangement of the
reservoir water with base character were found as Na+
> Ca++
> Mg++
> K+
> Fe++
> NH4
+
-N and also, anion
arrangement was found as SO4
=
> Cl>
NO3
-N
>
NO2
-N.
Having the highest biomass, water
temperature was at 25.5°C water temperature, the
highest biomass was recorded in August month. In
autumn bloom, the water temperature was measured
as 17.2°C. In spring bloom, it was measured as 9.4°C
in March and 11.5°C in April (Taş, 2006).
In order to determine its relationship with
environmental conditions of Dinobryon sertularia,
correlation analysis and anova test were performed by
using SPSS 13.0 package program. According to the
results obtained from two-way-analysis of variance
(ANOVA) test, it was determined to be a positive
relation among dissolved oxygen (P<0.001), pH
(P<0.001) and total alkalinity (P<0.009) with the
numbers of the D. sertularia.
In respect of correlation analysis, there was a
relatively negative relationship between the numbers
of the organism and total alkalinity in the lake water
(r= -0.497, P<0.05). It was seen to be a quite positive
relations among Electrical Conductivity (EC)-SO4
=
(r=0.900), Cl-EC
(r=0.808), SO4
=
- Cl(r=0.643)
Na+
EC
(r=0.757), Na+
-Cl(r=0.678),
K+
-Cl-
(r=0.632),
SO4
=
-Na+
(r=0.820), Ca++
-Na+
(r=0.700), Ca++
-SO4
=
(r=0.669), SO4
=
-Fe++
(r=0.616) (P<0.01) in the
physico-chemical parameters of the reservoir water,
respectively. Despite this, it was found to be relatively
negative relations among TAL- NO2
(r=-0.528),
ECTAL
(r=-0.528), SO4
=
-TAL (r=-0.491), K+
-TAL (r=-
0.509) (P<0.05) in the lake water, respectively.
Discussion
Confusion on feeding terminology of algae
results from the similarity of nourishment way or
transition phase in nourishment mode. Therefore,
algae usually can be classified according to
nourishing style. But, they can not classify as
certainly by this way. Because, they have changing
capacity of nourishment way in terms of
Figure 5. Monthly variations in relative biomass of D. sertularia in the surface waters of the all stations (a) and in the depths
of the st. 1 (b).
310 B. Taş et al. / Turk. J. Fish. Aquat. Sci. 10: 305-313 (2010)
Figure 6. The biomass variation of D. sertularia in the surface waters of the all stations (a) and in the depths of the st.1 (b).
Figure 7. The hierarchical clustering among the surface stations (a) and the depths of the st.1 (b) according to the Bray-Curtis
similarity index.
B. Taş et al. / Turk. J. Fish. Aquat. Sci. 10: 305-313 (2010) 311
o
Table 2. Variation of the most important environmental characteristics in the Derbent Reservoir
Mean Variable Minimum Maximum
Temperature (°C) 15.56 4.0 26.1
Dissolved O2 (mg L-1
) 10.39 8.1 12.0
pH 7.98 7.1 8.6
Conductivity (µS cm-1
) 1525 1040 1992
Total alkalinity (mg L-1
CaCO3) 163.7 130.0 190.0
Total hardness (mg L-1
CaCO3) 439.2 355.0 587.5
Na+
(mg L-1
) 171.3 92.0 200.1
K+
(mg L-1
) 4.47 2.53 5.46
Ca2+
(mg L-1
) 102.73 71.0 115.06
Mg2+
(mg L-1
) 42.39 3.25 72.96
Fe2+
(mg L-1
) 0.21 nd 1.51
Cl(mg
L-1
) 246.54 159.75 280.45
o-PO4
3(mg
L-1
) 0.053 nd 0.16
SO4
2(mg
L-1
) 295.16 164.16 448.32
NH4
+
-N (mg L-1
) 0.18 nd 0.5
NO2
-N
(mg L-1
) 0.05 nd 0.009
NO3
-N
(mg L-1
) 0.96 0.33 2.33
nd: not determined
environmental conditions.
Mixotrophic organisms play an important role
in the flow of energy and substance through food web
in aquatic ecosystems. A current concept concerning
organic matter dynamics within pelagic food webs
consists of two processes: the traditional food web
(nutrients–phytoplankton–zooplankton–fish), which
considers that the phytoplankton is the dominant
‘producer’, and the microbial loop (Azam et al.,
1983), which implies that a portion of matter and
energy flows through unicellular organisms, such as
bacteria, to mixotrophic and heterotrophic protists,
bearing in mind that several phytoplanktonic
organisms can also be consumers. Based on these two
concepts, the small-sized fractions of phytoplankton
communities play fundamental roles in the pelagic
trophic interactions. In particular, in oligotrophic
waters the autotrophic picoplankton can dominate the
phytoplankton biomass and production (Stockner and
Antia, 1986; Stoecker, 1998), and besides, together
with bacteria, constitute the prey for the protistan
assemblage. The nanoplanktonic size fraction, to
which most of the mixotrophic protists belong, also
represents the food for herbivorous zooplanktonic
organisms.
Dinobryon benefits from organic elements as
vitamins and minerals. When mineral elements are
insufficient, it demonstrates mixotrophic or
heterotrophic activity. It is known that D. sertularia
displays facultative bacterial nourishing from
literature and has mixotrophic strategy (Porter, 1988;
Jones, 1994; Isaksson, 1998). This characteristic of
Dinobryon is significantly effective adaptation for
this type of aquatic environment (Isaksson, 1998).
Mixotrophic property of Dinobryon provides
important advantages when nutrients are limited
(Gaedke, 1998; Kümmerlin, 1998). Similar findings
are reported some investigations (Pugnetti and
Bettinetti, 1999).
According to the results obtained from the study,
total 180 taxa belonging to 8 divisions were identified
in the phytoplankton of the DR. Dinobryon sertularia
from Chrysophyta was found as only species. This
species has often made blooms in the phytoplankton
(Taş and Gönülol, 2007).
D. sertularia was fairly abundant in the DR
phytoplankton having oligo-mesotroph characteristics
(Taş and Gönülol, 2007). This species was determined
in some locations of Suat Uğurlu Dam Lake (Yazıcı
and Gönülol, 1994) and Akgöl Lake (Ersanlı et al.,
2006). The crysophyte Dinobryon spp. are the most
dominant mixotroph in Lake Constance (Gaedke,
1998). In a study made in the North Patagonian
Lakes, it is reported that D. divergens and D.
sertularia are mostly dominant in microphytoplankton
(Queimalinos, 2002). This genus is commonly found
in water where is insufficient phosphorus (Lee, 1980;
Sandgren, 1988), and it is an important grazer of
bacteria (Bird and Kalff, 1986). Orthophosphate in the
surface water changed in the range 0-0.16 mg L-1
.
Average value was determined as 0.053 mg L-1
(Taş
2006). Having the highest biomass, orthophosphate
was found as 0.001 mg L-1
in the end of summer. In
autumn bloom, orthophosphate was not determined in
October month. But, it was found as 0.09 mg L-1
in
March and 0.05 mg L-1
in April in spring months.
Water temperature is very important regarding
the seasonal variation of phytoplankton (Richardson
et al., 2000). When Dinobryon spp. compared with
other species, it has quite high tolerance to low
temperatures. These tolerance levels provide the
dominancy of various species in different seasons
(Fogg, 1975). By means of this potential, D.
sertularia made blooms in different seasons and
temperatures in DR. Blooms provided significant
contributions on phytoplankton biomass. The biomass
of D. sertularia was found at changing ratios as 0-
6.56 µg ml-1
in the surface water of all stations and 0-
6.11 µg ml-1
in the depths of st 1. Chrysophytes found
in cold freshwater lakes and ponds are reported t
312 B. Taş et al. / Turk. J. Fish. Aquat. Sci. 10: 305-313 (2010)
make frequently water blooms in spring months
(Graham and Wilcox, 2000). While only D. sertularia
from Chrysophytes was found in DR phytoplankton,
it was determined to be a very common species by
making blooms in autumn, spring months and the end
of summer. According to physical and chemical
analyses of the water, DR has the characteristics of
oligo-mesotrophic lakes.
When physical and chemical parameters of the
lake water were examined, there are some relations
between both these parameters and organism number.
According to the results obtained from ANOVA
analysis, it was determined to be a positive relation
among dissolved oxygen, pH and total alkalinity
(TAL) with the numbers of the D. sertularia. Also, In
respect of correlation analysis, there was a relatively
negative relationship between the numbers of the
organism and total alkalinity in the lake water. Once
these results compare with previous studies, important
similarities are seen among physical and chemical
features of the lake water (Jeong, 2001; Kim et al.,
2007; Tay and Kortatsi, 2008; Shakeri et al., 2009)
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