ISSN 1995-0829, Inland Water Biology, 2009, Vol. 2, No. 1, pp. 42–49. © Pleiades Publishing, Ltd., 2009. Original Russian Text © N.G. Kosolapova, D.B. Kosolapov, 2009, published in Biologiya Vnutrennikh Vod, No. 1, 2009, pp. 45–52.
ZOOPLANKTON, ZOOBENTHOS AND ZOOPERIPHYTON
The Diversity and Distribution of Heterotrophic Nannoflagellates in the Eutrophic Lake Nero N. G. Kosolapova and D. B. Kosolapov Institute for the Biology of Inland Waters, Russian Academy of Sciences, Borok, Nekouzskii raion, Yaroslavskaya oblast, 152742 Russia e-mail:
[email protected] Received October 1, 2007
Abstract—The fauna and abundance of heterotrophic nannoflagellates (HNF) and the quantitative distribution of their main food items (bacteria) have been studied in the highly eutrophic Lake Nero (Yaroslavskaya oblast). A total of 70 HNF species and forms were found, with representatives of the order Choanoflagellida dominant. Abundances of HNF and bacteria were high, reaching levels typical for productive waters. The pattern of HNF seasonal dynamics was characterized by two peaks in June and September and one low in August. The minimal levels of HNF coincided with the peak of bacterioplankton abundance. Key words: heterotrophic flagellates, bacterioplankton, species composition, abundance, biomass, eutrophic shallow lake. DOI: 10.1134/S1995082909010076
INTRODUCTION
average surface area of 51.7 km2. Twenty tributaries flow into the lake, the largest of which is the Sara River. The Veksa River flows out from the lake. The lake is shallow (mean depth is about 1 m), its water transparency is low: 30 to 50 cm during the vegetation period. The bottom of the lake is covered with a 5- to 20-cm-deep layer of sapropel containing 25–43% of organic matter. Lake Nero is subject to strong pollution from the town of Rostov and settlements situated ashore. This negatively influences the lake’s ecological state [11]. The planktic community of Lake Nero HNF was studied from May to October 2003–2004 at five sampling stations, one of which (St. 4) was located in the center at the deepest part of the lake (Fig. 1). The HNF species composition was identified using phase–contrast microscopy in non-preserved samples according to the standard methods [10, 25]. The abundances and sizes of HNF and bacterioplankton were determined by the epifluorescent microscopy technique using primulin fluorochromes and 4,6-diamidino-2phenil indole [15, 23].
The concept of the “microbial loop,” substantiating the importance of microbial food webs in the functioning of planktic communities and cycling of nutrients in aquatic ecosystems, was formulated in the 1980s [14, 28]. According to this concept, the heterotrophic nannoflagellates are a constant component of the “microbial loop”. These protists possess a high reproduction rate, reach large numbers, play an important role in the regeneration of nitrogen and phosphorus compounds, and serve as the main picoplankton consumers and as important food for ciliates and metazoic zooplankton in marine and freshwater ecosystems [2, 12]. The development of heterotrophic nannoflagellates (HNF) in most waterbodies is controlled by the food resources (control “from below”) or by microplankton pressure (control from “above”). Despite the important roles HNF play, their species diversity and ecology, as well as interrelations with other components of the “microbial loop” (especially with respect to seasonal fluctuations), are rarely studied. The goal of this paper is to study the abundance, species composition, trophic structure of the community, spatial distribution, and seasonal dynamics of heterotrophic nannoflagellates, as well as the quantitative development of their main food items (bacteria in the water column of Lake Nero).
RESULTS In the Lake Nero plankton, 70 species and forms of colorless flagellates were identified (Table 1). The largest number of HNF species (48) was found in the central open part of the lake (Station 4). At other stations, 27 to 34 species were registered. The highest species diversity (19 species) was exhibited by the order Choanoflagellida. The numbers of representatives of other orders were ≤9.
MATERIAL AND METHODS Lake Nero is the largest lake in Yaroslavl oblast. It is 12.5-km-long and has a maximum width of 8 km and an 42
THE DIVERSITY AND DISTRIBUTION OF HETEROTROPHIC NANNOFLAGELLATES
43
Veksa River
N
v
sto
Ro
5 7 8 4
3
Ugodichi
Sara Riv
er
Vorzha
Porechiye-Rybnoye Fig. 1. Scheme of sampling station locations in Lake Nero: 3–5, 7, and 8 are station numbers.
The base of HNF diversity at different parts of the lake was composed of representatives of orders Choanoflagellida, Chrysomonadida, and Kinetoplastida (Fig. 2). Choanoflagellates were dominant at Stations 3, 4, and 7, where their shares ranged from 21 to 26% of the total HNF species number. At the place of sapropel excavation (Station 5) and in the coastal zone of the lake (Station 8), the representatives of orders Chrysomonadida and Kinetoplastida were dominant (23 and 21% of the total number of species, respectively). The following species were constantly (frequency of occurrence ≥50%) found in the water column: Codonosiga botrytis, Bodo designis, B. saltans, Monosiga ovata, Paraphysomonas imperforate, and Spumella sp. 1. However, the highest contribution to the HNF species diversity in Lake Nero was made by rare species with occurrence frequencies less than 25 or 62% of the total number of species found in the lake [4, 6]. INLAND WATER BIOLOGY
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Ten flagellate species (14% of the total number of species) were found at all stations: Codonosiga botrytis, Bodo designis, Phyllomitus apiculatus, Rhynchomonas nasuta, Goniomonas truncata, Spumella sp. 2, Paraphysomonas imperforata, Bicosoeca lacustris, Heteromita reniformis, and Kathablepharis sp. Some species were found only at a few stations. The highest number of such species (15) was found in the central part of the lake (Station 4); the lowest (8 species at each location) was found in the lake parts situated 50 m from Rozhdestvenskii Island (Station 3) and in the near-shore zone off the west coast (Station 8). Six and five species were registered at the place of sapropel excavation at the northern part (Station 5) and in the littoral zone off the west coast (Station 7), respectively. Among HNF, bacteriodetritivores–filtrators are considered the main consumers of solitary free–living bacteria. The bacteriodetritivores–gatherers feed on the epi-
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Species composition of heterotrophic flagellates in Lake Nero Species
Number of sampling stations 3 4 5 7 8
Choanoflagellida Kent, 1880 Codonosiga botrytis Kent, 1880 C. sp. Monosiga ovata Kent, 1880 Desmarella moniliformis Kent, 1880 Diploeca angulosa de Saedeleer, 1927
+ – + + –
Diplosiga francei Lemmermann, 1914 D. socialis Frenzel, 1892
– –
Lagenoeca globulosa France, 1897 L. ruttneri Bourrelly, 1952 Salpingoeca amphora Kent, 1880 S. amphoridium Clark, 1868 S. balatonis Lemmermann, 1910 S. globulosa Zhukov, 1978 S. minuta Kent, 1880 S. minor Dangeard, 1910 S. pixidium Lemmermann, 1910
– – + + – – + + –
S. schilleri (Schiller) Starmach, 1968
–
S. vaginicola Stein, 1878 S. sp. Kinetoplastida Honigberg, 1963 Bodo curvifilus Griessmann, 1913 B. designis Skuja, 1948 B. globosus Stein, 1878 B. minimus Klebs, 1893
– +
B. saltans Ehrenberg, 1832
–
B. rostratus (Kent) Klebs, 1893
–
Parabodo nitrophilus Skuja, 1948 Phyllomitus apiculatus Skuja, 1948 Rhynchomonas nasuta (Stokes, 1888) Klebs, 1892 Euglenida Bütschli, 1884, emend. Simpson, 1997 Scytomonas pusilla Stein, 1878 Petalomonas angusta Klebs, 1893 P. minuta Hollande, 1942 P. pusilla Skuja, 1948 Peranema fusiforme (Larsen, 1987) Larsen et Patterson, 1990 Cryptomonadida Senn, 1900 Goniomonas truncata (Fresenius) Stein, 1887 Chrysomonadida Engler, 1898 Anthophysa vegetans (O.F. M.) Stein, 1878 Spumella sp. 1
– + +
S. sp. 2 S. sp. 3 Paraphysomonas imperforata Lucas, 1967
+ + – –
Species
P. vestita (Stokes) De Saedeleer, 1929 + + + + P. sp. + – – – Ciliophryida Febvre-Chevalier, 1985 + – + + Actinomonas mirabilis Kent, 1880 + – – – Pteridomonas pulex Penard, 1890 – + – – Spongomonadida Hibberd, 1983, emend. Karpov, 1990 + – – – Spongomonas uvella Stein, 1878 + – – – Bicosoecida Grasse, 1926, emend. Karpov, 1998 + – – – Bicosoeca exilis Penard, 1921 + – + – B. crystallina (Lackey) Skuja, 1956 + – + + B. lacustris Skuja, 1948 – – + – B. ovata Lemmermann, 1914 – – + – B. petiolata (Stein) Bourrelly, 1951 – – – + B. socialis Skuja, 1956 + + – + B. sp. + – + + Thaumatomonadida Shirkina, 1987 – + – – Thaumatomonas lauterborni De Saedeleer, 1931 + – + – Cercomonadida Poche, 1913, emend. Vickerman, 1983, emend. Mylnikov, 1986 – – + – Allantion tachyploon Sandon, 1924 + – – – Cercomonas crassicauda Dujardin, 1841 C. longicauda Dujardin, 1841 + + – + C. minimus Mylnikov, 1992 + + + + C. metabolicus Mylnikov, 1992 – – – + C. sp. + – – + Heteromita minima (Hollande, 1942) Mylnikov et Karpov, 2004 + + + + H. reniformis (Zhukov, 1978) Mylnikov et Karpov, 2004 + – – – Protaspis gemmifera Larsen and Patterson, 1990 + – – – Diplomonadida (Wenyon) Brugerolle + + + + Trepomonas rotans Klebs, 1893 + + + + Colpodellida Cavalier-Smith, 1993
Colpodella angusta (Dujardin, 1841) Simpson et Patterson, 1996 + – – + + Colponemida Cavalier-Smith, 1993 – + – – – Colponema loxodes Stein, 1878 – – + – – Pelobiontida Page, 1976 – – + + + Mastigella polymastix Frenzel, 1897 + – – – – Mastigamoeba sp.
Number of sampling stations 3 4 5 7 8 – + + + – – + + – – + + – – – – – – + – + – + – – – – + – + – –
+ + + – – – –
– – + + – – –
+ – + – – + +
– – + – – – +
– + – – –
+ – – – – – +
– – + + + + +
+ + – – – – –
+ – – – – + +
+ – – – – + +
+ + + + + + + – + + – + – – – + – + – + – + – + + – – – + + – + – – –
Ancyromonadida Cavalier-Smith, 1997 + + + + + Ancyromonas sigmoides Kent, 1880 + + + – + Jakobida Cavalier-Smith, 1993 – + – + – Histiona aroides Pascher, 1942 – + + + – + Collodictyonida Brugerolle, Bricheux, Philippe et Coffe, 2002 + + + + + Aulacomonas submarina Skuja, 1939 – – – – + – Kathablepharida Cavalier-Smith, 1993 + + + + + Kathablepharis sp. + Total 29 INLAND WATER BIOLOGY
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Fig. 2. Taxonomic structure of the HNF community at different parts of Lake Nero: (a)–(e) stations 3–5, 7, and 8, respectively; 1. Choanoflagellida, 2. Bicosoecida, 3. Chrisomonadida, 4 Kinetoplastida, 5 Euglenida, 6 Cercomonadida, 7 Protista incertae sedis, 8 others; the numbers in figure designate number of species, % of total.
phytic bacteria attached to surfaces of various substrata. This group of protists also includes predators feeding on smaller flagellates and omnivorous organisms. Different groups of HNF possess specific features of feeding and respective morphological differences [2, 16, 24]. The majority of Lake Nero flagellates are classified as bacteriodetritivores (60 species), 34 of which are filtrators and 26 are gatherers. Additionally, four species of euryphages were found (Goniomonas truncata, Paraphysomonas imperforate, P. vestita, and Paraphysomonas sp.) along with six species of obligate predators (Allantion tachyploon, Aulacomonas submarina, Colpodella angusta, Colponema loxodes, Katablepharis sp., and Phyllomitus apiculatus). The trophic structure of HNF communities at examined parts of the lake varied insignificantly. Bacteriodetritivores–gatherers and filtrators, which regulate the abundance and structure of bacterioplankton, prevailed (Fig. 3). During the vegetation period in Lake Nero, the number of HNF species in a water sample varied from 2 to 16 (10.6 ± 0.9 on average). The number and biomass of flagellates ranged from 960 to 13200 ex./ml (4921 ± 648 in average) and 19.8 to 1414 mg/m3 (451 ± 91 mg/m3 on average), respectively. The peaks in the seasonal abundance and biomass dynamics were observed in June and September; the lows were in August (Fig. 4). The HNF species number was highest from the end of summer to INLAND WATER BIOLOGY
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fall. The mean for the vegetation period’s quantitative parameters of the HNF development differed inconsiderably between lake parts (Fig. 5). However, the number of species and abundance and biomass of HNF in the open part of the lake (Station 4) were lower than in coastal shallows. % 80
40
3 1
4
5 2
7 8 Number of stations 3
4
Fig. 3. Trophic structure of planktic HNF community (% of the total number of species) at different parts of the lake: 1. Bacteriodetritivores–filtrators; 2. Predators; 3. Bacteriodetritivores–gatherers; 4. Euryphages.
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Fig. 4. Seasonal changes in the HNF number of species (a), abundance (b), biomass (c), and abundance (d) and biomass (e) of bacterioplankton.
Fig. 5. Average for the vegetation period number of species (a), abundance (b), biomass (c) of HNF, and abundance (d) and biomass (e) of bacterioplankton at different parts of the lake.
The study of the vertical distribution of flagellates in the central part of the lake (Station 4) during the summer calm-weather period has shown that the maximal abundance and biomass were noted near the water surface; the lowest were near the bottom (Fig. 6b). However, the maximal number of HNF species were found near the bottom and the minimal were found at the surface (Fig. 6a). It is noteworthy that choanoflagellates (planktic forms) and cercomonads belonging predominantly to benthic organisms were dominant throughout the whole water column.
increase in bacterioplankton abundance and biomass was observed in the near-surface and near-bottom water layers (Fig. 5c).
The number and biomass of the lake bacterioplankton were high, ranging from 4.2 to 13.6 × 106 cells/ml (mean (8.1 ± 3.2) × 106 cells/ml) and from 444 to 1472 mg/m3 (mean 858 ± 327 mg/m3), respectively. The maximal values of these parameters were registered in August, when the quantitative development of HNF was lowest (Fig. 4). The averages of vegetation seasonal values of bacteria abundance and biomass, like that of flagellates, fluctuated inconsiderably over the lake area (Fig. 5). During calm weather in the central part of the lakes, an
Small solitary cells dominated Lake Nero bacterioplankton, with abundance ranging from 70 to 90% of the total (mean 82%); biomass ranged from 48 to 82% (mean 69%) of the total. The second, in terms of the abundance of the ecomorphological group, were the cells associated with detritus and phytoplankton (12.6% of the total number). The bacteria in micrcolonies, large solitary bacteria, and filaments were scarce: 3.8, 1.4, and 1.0% of the total number, respectively. However, filamentous bacteria and cells associated with detritus and phytoplankton notably contributed to the formation of bacterioplankton biomass, averaging 12.3 and 9.6% of the total biomass, respectively. The development of these groups exhibited seasonal fluctuations: there was an increase in the filamentous bacteria biomass in May and October (up to 36% of the total bacterial biomass) and an increase of detritus- and phytoplankton-associated bacteria in July and September INLAND WATER BIOLOGY
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30 0
(b) 4000 cells/ml 0
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Fig. 6. Vertical distribution of number of species (a), abundance and biomass (b) of HNF, and abundance and biomass (c) of bacterioplankton in the central part of the lake (Station 4): 1. Abundance (top abscissa); 2. Biomass (bottom abscissa); Depth, ordinate axis.
(up to 20% of the sum biomass). The share of large bacilla averaged 4.9% of the bacterioplankton biomass; that of microcolony-forming bacteria averaged 3.6%. DISCUSSION The species composition of the Lake Nero flagellates was found to be similar to other lakes, rivers, and reservoirs in the Volga River basin [1, 4, 5, 9, 12]. Only a few species of order Choanoflagellida (Desmarella moniliformis, Diplosiga francei, D. socialis, and Salpingoeca schilleri) are rarely noted in the faunistic lists of waterbodies. The choanoflagellates of order Choanoflagellida are an important component of the community, accounting for 28% of the total HNF species number. In the rivers, ponds, and bogs of Yaroslavskaya oblast, HNF species made up ≤16% of the total number of species [6]. The Lake Nero trophic structure is also similar in many aspects to that of other waterbodies [6, 12]. The share of bacteriodetritivores was about 70% the total number of lake planktic flagellates. Comparing the data on HNF abundance and biomass in small and large waterbodies of the Volga basin (lakes, rivers, man-made lakes, ponds, and bogs) revealed that the average values of these parameters in Lake Nero reach maximal levels [1, 3, 6]. This presumably relates to the high trophic state of the lake [8]. As a rule, in highly productive waters, HNF reach a high level of quantitative development and play an important role in the consumption of picoplankton and the transfer of carbon to the highest trophic levels in the planktic food web [17]. For instance, in the eutrophic backwater in the Danube River (Austria), the number of flagellates fluctuated during the year from 0.57 to 2.2 (mean 1.1 ± 0.39) × 103 cells/ml, the mean cell volume fluctuated from 17.3 to 120.7 INLAND WATER BIOLOGY
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(mean 43.4 ± 19.0) µm3, and the biomass fluctuated from 4.4 to 41.7 (mean 10.7 ± 6.5) mg C/m3 [27]. The abundance of flagellates was minimal in winter, increased in spring, and reached its maximum in May (during that time, small cells dominated the community). In summer the abundance of HNF decreased and stayed at the level of 500–1000 cells/ml until August and September, when some rise was observed, followed by drop down to the minimal winter level. In general, small organisms with sizes of 2.5–5.0 µm were dominant in the HNF community, averaging 54.5 ± 15.0% of the total number. The studies on a series of lenthic waterbodies differing in trophic states, oxygen content, pH, color, and other parameters also revealed that the highest abundances and biomasses of flagellates were found in waterbodies with a high content of organic matter [6]. On the contrary, in a large shallow eutrophic lake (Vortsjarvi, Estonia) with the same low water transparency (
