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Heterotrophic flagellates from freshwater biotopes of Matveev and Dolgii Islands (the Pechora Sea)
Denis V. Tikhonenkov 1 and Yuri A. Mazei 2
1 Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Russia
2 Department of Zoology and Ecology, Penza V.G. Belinsky State Pedagogical University, Penza, Russia
Summary
The species composition and distribution of heterotrophic flagellates in freshwater biotopes of Matveev and Dolgii islands were investigated. Thirty-seven species and forms were identified. Paraphysomonas vestita and Spumella sp. were the most common species. Most flagellates belonged to cercomonads, diplomonads, choanoflagellates and kinetoplastids. Species richness in different habitats varied from 2 to 10 species. The curve "cumulative species number vs. sampling effort" does not flatten out, so the species list obtained should be considered as incomplete. Local species richness of moss biotopes is significantly higher than predicted by this curve, whereas local diversity of lake biotopes shows a significantly lower level. Our observations confirm previous studies maintaining that the majority of the heterotrophic flagellates have a worldwide distribution. The lower complexity of polar heterotrophic flagellate communities may be explained by poor sampling effort.
Key words: heterotrophic flagellates, species richness, community structure, polar regions
Introduction
Heterotrophic flagellates are broadly distributed in biotopes of different salinity (Fenchel, 1986, 1987). They are the most important consumers of bacteria in microbial communities. Heterotrophic flagellates make a considerable contribution to energy flow and biogeochemical cycling in aquatic ecosystems and play
a cardinal role in carbon transfer and nutrient regeneration (Sherr et al., 1982; Porter et al., 1985; Berninger et al., 1991; Arndt et al., 2000; Laybourn-Parry and Parry, 2000; Auer and Arndt, 2001; Domaizon et al., 2003).
Investigations of heterotrophic flagellates in polar regions were conducted predominantly in marine ecosystems (Throndsen, 1970; Thomsen, 1981;
© 2007 by Russia, Protistology
Marchant, 1985; Buck and Garrison, 1988; Garrison and Buck, 1989; Thomsen et al., 1990; Vors, 1993; Thomsen et al., 1995). Studies of species composition and structure of freshwater heterotrophic flagellate communities were sporadic (Tong et al., 1997; Arndt et al., 2000; Mylnikov, 2002). Moreover, planktonic and algal mat communities were predominantly analyzed (Cathey et al., 1981; Laybourn-Parry et al., 1995, 1996; Butler, 1999). Data on the polar benthic freshwater heterotrophic flagellates are few and mostly concern the Antarctic sites of different trophic status (Hawthorn and Ellis-Evans, 1984; Dietrich and Arndt, 2004). Investigations of community composition and distribution of benthic heterotrophic flagellates in the Arctic freshwater biotopes are scarce (Mylnikov and Zhgarev, 1984).
The aim of our study was to investigate the species composition of the heterotrophic flagellate community in freshwater locations in Matveev and Dolgii islands (Pechora Sea), North-West Russia.
Material and Methods
The samples were collected on September 15-16, 2003. Freshwater biotopes ofMatveev and Dolgii islands were investigated (Fig. 1).
The communities of heterotrophic flagellates in different biotopes (mosses, lakes, and streams) were analyzed. In every biotope, the samples were taken in various benthic habitats (organic detritus, silt, sand, moss). Fifteen samples were taken: 1 - Matveev island, lake no. 1 (200 m2 area), sandy habitat; 2 - Matveev island, lake no. 2 (300 m2 area), moss; 3 - Matveev island, lake no. 2, silt; 4 - Matveev island, stream, silt; 5 - Matveev island, lake no. 3 (800 m2 area), moss; 6 -Dolgii island, lake no. 1 (900 m2 area), organic detritus; 7 - Dolgii island, lake no. 1, moss; 8 - Dolgii island, lake no. 1, sand; 9 - Dolgii island, stream no. 1, silt; 10 - Dolgii island, wet terrestrial bryales mosses; 11 -Dolgii island, wet terrestrial sphagnum mosses; 12 -Dolgii island, lake no. 2 (500 m2 area), moss; 13 -Dolgii island, lake no. 3 (200 m2 area), moss; 14 -Dolgii island, lake no. 2, organic detritus; 15 - Dolgii island, stream no. 2, silt. Water temperature in all biotopes was in the range of 3-4°C. All samples from the lakes were taken near the shore at a depth of 30 cm. The lakes were located close to the sea coast. Samples were taken by handle piston corer (2 cm2 in diameter).
Water samples were placed into 50-ml flasks, and maintained at approximately 3°C during transportation to the laboratory. The initial volume of the sample was 15 ml, which contained 12-13 ml of water and 2-3 mm3 of bottom substrate (or moss). From each sample, 10 ml were decanted into Petri dishes (5 ml in each of the two replicates) for development of the aerobic forms,
and 5 ml were decanted into the vials (small bottles) closed by resin plugs without air contact for development of anaerobic forms. In the beginning, no enrichment samples were observed in Petri dishes. Then a suspension ofbacteria Pseudomonas fluorescens was added to Petri dishes and 1g/l of pepton was added into the vials. The Petri dishes and vials were kept in darkness at 25°C. The Petri dishes were maintained for 9 days, species composition was studied on the 3rd, 6th, 9th days of exposition. The vials were maintained for 5 days, whereupon investigation of anaerobic forms was realized.
Heterotrophic flagellates were identified by means of observations on living cells with the exception of Paraphysomonas species. Suspensions of Paraphyso-monas cells were applied on cupreous grids sheeted by Formvar film and whole mounts were made as described by Moestrup and Thomsen (1980). Grids were shadow cast with tungsten oxide; as a result, the contrast of small cell structures was strengthened. Light microscopic observations were made under a Biolam-I microscope (Russia) equipped with phase contrast and water immersion objectives at a total magnification of+1000. The microscope was equipped with an analogous video camera AVT HORN MC - 1009/S, connected to a video recorder Panasonic NV-HS 850. Electron microscopy was carried out with a JEM - 100C microscope.
The classification of communities (R-analysis) by their species structure was conducted with the aid of cluster analysis (complete linkage) based on the Raup-Crick indices similarity matrix (Raup and Crick, 1979). Principal component analysis (PCA) was carried out in order to reveal general patterns of species distribution (Q-analysis). All computations were performed with the aid of the software packages STATISTICA 5.5 (StatSoft, Inc., 1999), PRIMER 5 (2001) and PAST (Hammer et al., 2001).
The systems of eukaryotes and protists used in this article are those presented by Lee et al. (2002) and Adl et al. (2005).
Results
Thirty-seven species and forms of heterotrophic flagellates from eleven super-generic taxa were found in the biotopes investigated (Table 1). The greatest number of the species was attributed to cercomonads (7 species), diplomonads (7 species), choanoflagellates (5 species), kinetoplastids (4 species).
Among the flagellates recorded, Paraphysomonas vestita and Spumella sp. were observed in more than 80% locations. Nine species (Bodo designis, Bodo saltans, Cercomonas radiatus, Diploeca angulosa, Heteromita globosa, Heteromita minima, Lagenoeca variabilis, Peta-
Fig. 1. Location of the study area (x).
lomonaspoosilla, Protaspis simplex) were found in more than 20% of samples. Twenty five species were detected in a single sample only.
The anaerobic forms Trigonomonas, Tetramitus, Trimastix, Trepomonas, Hexamita were found in 40% of biotopes. Interestingly, different species of anaerobic flagellates developed in different biotopes, i.e. none of the anaerobic organisms observed occurred in more than one sample.
Species number in different communities varied from 2 to 10. Reliable distinctions in species richness of communities, which formed in different biotopes and habitats, have not been found (Fig. 2). However, this parameter goes up in moss and stream communities in comparison with lake communities as well as communities in sand and silt substrates.
The total species richness of a region obviously correlates with the number of samples taken there. To take into account the effect of unequal sampling, we considered the relation between the number of species found, SN, and number of samples (N). To do this, the mean species numbers were calculated for repeated draws of N samples chosen randomly from the total dataset of 15 samples using the rarefaction procedure. The cumulative species number as a function of sampling effort (Fig. 3) follows well the linear relation SN = 6.15 + 2.16N (r = 0.99). In other words, the expected richness increases approximately twice with a two-fold increase in sample number. The curve does not flatten out, so the species list obtained for these sites
is far from being complete, and each new sample should yield new species.
The local species richness data on the stream biotope and silt, sandy and organic detritus habitats (shown as triangles in Fig. 3) fit well the rarefaction curve, and individual deviations do not exceed the confidence limits. Thus, the between-site differences in local species richness are mainly determined by unequal sampling efforts. However, local species richness of moss biotope and habitat is characterized by a significantly higher level than predicted by the rarefaction curve, whereas the local diversity of the lake biotope has, on the contrary, a significantly lower level (these localities are shown as stars in Fig. 3).
Hierarchical cluster-analysis (Fig. 4) and principal component analysis (Fig. 5) were performed to classify the samples by species composition and to reveal species that tend to be associated with concrete biotopes. Classification of samples indicates three groups of communities (Fig. 4). Ordination of samples (Fig. 5) shows separation of community group "C" from others along 1 PC (which explains 26.6% of the total community variance). This separation is caused by four species: Bodo designis and Petalomonaspoosilla are the characteristic species of the group "C", whereas Bodo saltans and Heteromita globosa do not occur in this community group. Separation between group "A" and "B" is along 2 PC (which explains 21.0% of the total community variance). Diploeca angulosa and Para-physomonas vestita tend tobe associated with com-
Table 1. Relative occurrence (%) of heterotrophic flagellates in different localities.
Biotopes Habitats
Species lakes streams mosses moss sand organic detritus silt
OPISTHOKONTA Cavalier-Smith, 1987, emend. Cavalier-Smith and Chao, 1995, emend. Adl et al., 2005 *Choanomonada Kent, 1880 **Monosigidae Zhukov and Karpov, 1985
Monosiga ovata Kent, 1880 **Salpingoecidae Kent, 1880 0.0 33.3 0.0 0.0 0.0 0.0 0.0
Diploeca angulosa de Saedeleer, 1927 20.0 66.7 66.7 28.6 0.0 50.0 20.0
Lagenoeca variabilis Skuja, 1956 20.0 0.0 33.3 28.6 0.0 0.0 20.0
Salpingoeca balatonis Lemmermann, 1910 0.0 33.3 0.0 0.0 0.0 0.0 0.0
S. megachelia Ellis, 1929 RHIZARIA Cavalier-Smith, 2002 *Cercozoa Cavalier-Smith, 1998, emend. Adl et al., 2005 **Cercomonadida (Poche, 1913), emend. Vickerman, 1983, emend. Mylnikov, 1986 ***Cercomonadidae Kent, 1880, emend. Mylnikov and Karpov, 2004 Cercomonas agilis (Moroff, 1904) Mylnikov and 0.0 33.3 0.0 0.0 0.0 0.0 0.0
Karpov, 2004 C. granulifera (Hollande, 1942) Mylnikov and 10.0 0.0 0.0 14.3 0.0 0.0 10.0
Karpov, 2004 C. radiatus (Klebs, 1892), Mylnikov and Karpov, 10.0 0.0 33.3 14.3 0.0 0.0 10.0
2004 30.0 0.0 33.3 28.6 0.0 0.0 30.0
Cercomonas sp. ***Heteromitidae Kent, 1880, emend. Mylnikov, 1990, emend. Mylnikov and Karpov, 2004 0.0 0.0 33.3 14.3 0.0 0.0 0.0
Allantion tachyploon Sandon, 1924 10.0 0.0 0.0 14.3 0.0 0.0 10.0
Heteromita globosa Stein, 1878 H. minima (Hollande, 1942) Mylnikov et Karpov, 10.0 33.3 66.7 28.6 0.0 0.0 10.0
2004 H. reniformis (Zhukov, 1978) Mylnikov et Karpov, 20.0 0.0 33.3 14.3 50.0 0.0 20.0
2004 0.0 33.3 0.0 0.0 0.0 0.0 0.0
Protaspis simplex V?s, 1992 CHROMALVEOLATA Adl et al., 2005 *Cryptophyceae Pascher, 1913, emend. Schoenichen, 1925 **Goniomonadales Novarino and Lucas, 1993 Goniomonas amphinema Larsen and Patterson, 20.0 33.3 0.0 0.0 50.0 0.0 20.0
1990 *Stramenopiles Patterson, 1989, emend. Adl et al., 2005 ** Bicosoecida Grasse, 1926, emend. Karpov, 1998 10.0 0.0 0.0 14.3 0.0 0.0 10.0
Bicosoeca conica Lemmermann, 1914 10.0 0.0 33.3 14.3 0.0 0.0 10.0
B. paropsis Skuja, 1956 **Chrysophyceae Pascher, 1914 Paraphysomonas vestita (Stokes, 1885) De 0.0 0.0 33.3 14.3 0.0 0.0 0.0
Saedeleer, 1929 80.0 100.0 100.0 100.0 100.0 50.0 80.0
Spumella sp. **Dictyochophyceae Silva, 1980 ***Pedinellales Zimmermann, Moestrup and Hallfors, 1984 90.0 33.3 100.0 100.0 50.0 100.0 90.0
Table 1. Continuation.
Pteridomonas pulex Skuja, 1956 EXCAVATA Cavalier-Smith, 2002, emend. Simpson, 2003 *Fornicata Simpson, 2003 **Eupharyngia Cavalier-Smith, 1993 ***Diplomonadida Wenyon, emend. Brugerolle et al., 1975 10.0 33.3 33.3 14.3 0.0 0.0 10.0
Hexamita inflata Dujardin, 1838 10.0 0.0 0.0 0.0 0.0 50.0 10.0
H. rostrata Stein, 1878 0.0 33.3 0.0 0.0 0.0 0.0 0.0
Tetramitus pyriformis Klebs, 1892 10.0 0.0 0.0 0.0 50.0 0.0 10.0
Trepomonas rotans Klebs, 1892 0.0 33.3 0.0 0.0 0.0 0.0 0.0
T. steini Klebs, 1892 0.0 33.3 0.0 0.0 0.0 0.0 0.0
Trigonomonas tortuosa Skuja,1956 10.0 0.0 0.0 0.0 0.0 50.0 10.0
Trigonomonas sp. *Preaxostyla Simpson, 2003 **Trimastix Kent, 1980 10.0 0.0 0.0 0.0 50.0 0.0 10.0
Trimastixmarina Kent, 1880 *Euglenozoa Cavalier-Smith, 1981, emend. Simpson, 1997 **Euglenida B?schli 1884, emend. Simpson, 1997 Notosolenus scutulum Larsen and Patterson, 10.0 0.0 0.0 14.3 0.0 0.0 10.0
1990 Petalomonas marginalis Larsen and Patterson, 10.0 0.0 0.0 0.0 0.0 50.0 10.0
1990 0.0 33.3 0.0 0.0 0.0 0.0 0.0
P. poosilla Larsen and Patterson, 1990 **Kinetoplastea Honigberg, 1963 ***Metakinetoplastina Vickerman in Moreira, Lopez-Garicia and Vickerman, 2004 ****Neobodonida Vickerman in Moreira, Lopez-Garicia and Vickerman, 2004 40.0 33.3 0.0 14.3 100.0 50.0 40.0
Cryptaulaxelegans Larsen and Patterson, 1990 10.0 0.0 0.0 0.0 50.0 0.0 10.0
Rhynchobodo thiophila Skuja, 1956 ****Eubodonida Vickerman in Moreira, Lopez-Garicia and Vickerman 2004 0.0 33.3 0.0 0.0 0.0 0.0 0.0
Bodo curvifilus Griessmann, 1913 0.0 0.0 33.3 14.3 0.0 0.0 0.0
B. designis Skuja, 1948 20.0 33.3 0.0 0.0 100.0 0.0 20.0
B. saltans Ehrenberg, 1832 Incertae sedis EUKARYOTA 20.0 33.3 33.3 28.6 0.0 50.0 20.0
Phyllomitus apiculatus Skuja, 1948 0.0 33.3 0.0 0.0 0.0 0.0 0.0
Number of samples taken 10 3 2 7 2 2 4
munity group "A", whereas Spumella sp., Heteromita minima, Protaspis simplex, Lagenoeca variabilis, Cerco-monas radiatus are characteristic of group "B".
Discussion
Species richness of heterotrophic flagellates in freshwater ecosystems of Matveev and Dolgii islands is one of the highest found so far in polar regions. Among the species identified from these lakes, 24% (Bodo
curvifilus, B. designis, B. saltans, Heteromita reniformis, Hexamita inflata, Lagenoeca variabilis, Monosiga ovata, Pteridomonaspulex, Trepomonas sterni) were previously observed in other Arctic freshwater biotopes (Mylnikov and Zhgarev, 1984); 40% (Allantion tachyploon, Bicosoeca conica, Bodo curvifilus, B. designis, B. saltans, Cercomonas sp., Heteromita globosa, H. reniformis, Hexamita inflata, Lagenoeca variabilis, Monosiga ovata, Paraphysomonas vestita, Pteridomonas pulex, Spumella sp., Trepomonas sterni), in polar (both Arctic and
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streams
type of the biotope
o
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Fig. 2. Species richness (average number of species per sample) of communities in different localities. Whiskers - standard error of the arithmetic mean. In all cases p > 0.05.
Antarctic) freshwater biotopes (Cathey et al., 1981; Hawthorn and Ellis-Evans, 1984; Mylnikov and Zhgarev, 1984; Butler, 1999; Tong et al., 1997); 54% (Allantion tachyploon, Bicosoeca conica, Bodo curvifilus, B. designis, B. saltans, Cercomonas agilis, Cryptaulax elegans, Diploeca angulosa, Goniomonas amphynema, Heteromita globosa, H. minima, Lagenoeca variabilis, Monosiga ovata, Petalomonas poosilla, Phyllomitus apiculatus, Protaspis simplex, Pteridomonas pulex, Salpingoeca balatonis, Spumella sp., Trepomonas sterni), in marine ecosystems of high latitudes (Mylnikov and Zhgarev, 1984; Larsen, 1987; Patterson et al., 1993; Vhrs, 1993; Railkin, 1995; Ikavalko and Gradinger, 1997; Tong et al., 1997; Mazei and Tikhonenkov, 2006) and over 90%, in temporary freshwater ecosystems (Kent, 1880; Skuja, 1956; Vhrs, 1992; Zhukov, 1993; Zhukov et al., 1998; Bernard et al., 2000; Auer and Arndt, 2001; Kosolapova, 2002; Mazei et al., 2005a; Mazei et al., 2005b; Tikhonenkov, 2006). Three species (Cryptaulaxelegans, Notosolenusscutulum, Petalomonas marginalis) were described from tropical marine sediments (Larsen and Patterson, 1990). Therefore, our
observations confirm previous studies maintaining that the majority of the heterotrophic flagellates have a worldwide distribution (Patterson and Simpson, 1996; Tong et al., 1997).
The communities analyzed have many common features with Antarctic benthic communities, which occur in sites with very limited trophic complexity and mainly consist of species from the same orders (Dietrich and Arndt, 2004). It is especially interesting, since the existence of discriminate limnetic ciliate communities in both polar regions was earlier suggested (Petz, 2003). Probably, patterns of macroscale distribution of the tiniest protists (heterotrophic flagellates) and the generally larger ones (ciliates) are different. Besides, the number of species recorded in each of the previous polar studies does not exceed 40. In this respect, polar island communities are characterized by a lower species diversity than those from similar small freshwater sites of temperate latitudes (Auer and Arndt, 2001; Kosolapova, 2001, 2002; Mazei et al., 2005a; Mazei et al., 2005b). However, in each paper dealing with polar heterotrophic flagellates, more than 50% of the species
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Fig. 3. Mean number of species found in samples. Circles: random draws from all 15 samples. Triangles: total richness of those localities, whose species richness level does not exceed confidence limits of rarefaction curve. Stars: total richness of those localities, whose species richness level exceeds confidence limits of rarefaction curve. Whiskers - standard error of the arithmetic mean.
0
5
list is considered as a new record for higher latitudes. As stated above, species diversity is a function of the number ofsamples taken. Probably, the lower complexity of polar communities of heterotrophic flagellates is an effect of poor sampling effort in such extreme biotopes. Several investigations did not cover all types ofbiotopes and were conducted during a short period. Thus, the total species diversity in polar biotopes may be much higher than currently thought. One of the theoretical reasons is the following: recently it has been proposed that small organisms (such as nematodes, ciliates, diatoms) show weak or no correlations between species richness and latitude and are less influenced by large-scale processes (Finlay et al., 1996, 1997; Fenchel et al., 1997; Azovsky, 2000, 2002; Hillebrand and Azovsky, 2001). This may confirm the point of view that small organisms exhibit generally a high local (a-) but low regional (2- and y-) or global species richness. Our study shows that 37 species in 15 samples is not the limit for arctic ecosystems. More intensive investigations of heterotrophic flagella-tes in higher latitudes are likely to prolong the species list of these organisms in polar ecosystems.
The kinetoplastids are the richest group in terms of species diversity in the different polar ecosystems (Mylnikov and Zhgarev, 1984; Vhrs, 1993; Railkin, 1995). These flagellates have a very widespread occurrence and were found both in freshwater and saline biotopes (Fenchel, 1986, 1987; Zhukov, 1993; Patterson and Simpson, 1996; Arndt et al., 2000). Many kinetoplastids are halotolerant (Gorjacheva et al., 1978; Mylnikov, 1983; Patterson and Simpson, 1996; Arndt
et al., 2000). For example, Bodo saltans is able to survive at a salinity of0 to 42%o (Mylnikov, 1983). The same species is observed in the marine Little Lagoon (Western Australia) with a salinity of 150%o (Patterson and Simpson, 1996). Cercomonads and diplomonads are other dominating groups in our samples. Cercomonads are a typical benthic group, which is generally discovered in samples rich in organic matter and detritus and in sewage waters (Hanel, 1979; Zhukov and Mylnikov, 1983; Mylnikov and Karpov, 2004). Anoxic conditions are often formed in benthic habitats: in most sediments of lakes, fjords and larger water bodies (Fenchel and Finlay, 1995). Such biotopes are inhabited by anaerobic bacteria and protists (Bernard et al., 2000). The free-living anaerobic flagellates mostly belong to groups lacking mitochondria, e.g. the diplomonads (Mylnikov, 1991).
Acknowledgments
We would like to thank Dr. A. Mylnikov for critical comments on the earlier draft of the manuscript. This study was supported by the Russian Foundation for Basic Research (grant numbers 04-04-48338 and 05-0448180).
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Address for correspondence: Denis V. Tikhonenkov. LInstitute for Biology of Inland Waters, Russian Academy of Sciences. Borok, Yaroslavskaya obl. 152742. Russia. E-mail: [email protected] or tikho-denis @yandex.ru
Editorial responsibility: Sergey Karpov
