MARINE‐DERIVED DINOFLAGELLATES IN ANTARCTIC SALINE LAKES: COMMUNITY COMPOSITION AND ANNUAL DYNAMICS1*[link]

The saline lakes of the Vestfold Hills in Antarctica offer a remarkable natural laboratory where the adaptation of planktonic protists to a range of evolving physiochemical conditions can be investigated. This study illustrates how an ancestral marine community has undergone radical simplification leaving a small number of well‐adapted species. Our objective was to investigate the species composition and annual dynamics of dinoflagellate communities in three saline Antarctic lakes. We observed that dinoflagellates occur year‐round despite extremely low PAR during the southern winter, which suggests significant mixotrophic or heterotrophic activity. Only a small number of dominant dinoflagellate species were found in each lake, in contrast to the species‐rich Southern Ocean from which the lake communities are believed to be derived. We verified that the lake species were representatives of the marine polar dinoflagellate community, and not freshwater species. Polarella glacialis Montresor, Procaccini et Stoecker, a bipolar marine species, was for the first time described in a lake habitat and was an important phototrophic component in the higher salinity lakes. In the brackish lakes, we found a new sibling species to the brackish‐water species Scrippsiella hangoei (J. Schiller) J. Larsen, previously observed only in the Baltic Sea.     

The distribution and abundance of algae in saline lakes of Saskatchewan,Canada

Collections of algae, mainly planktonic, were made from 41 saline lakes in southern Saskatchewan ranging in salinity from 3.2 to 428 g l^-1. Algae in 7 phyla, 8 classes, 42 families, 91 genera and 212 species and varieties were identified. Fourteen species were restricted to hypersaline (50 g l^-1) waters and eleven of these were diatoms. In general, species diversity was inversely related to lake salinity. Algae that were important community constituents over a broad spectrum of salinities were the green algae Ctenocladus circinnatus, Dunaliella salina and Rhizoclonium hieroglyphicum, the blue-green Lyngbya Birgei, Microcystis aeruginosa, Oscillatoria tenuis, O. Utermoehli and Nodularia spumigena and the diatoms Melosira granulata, Stephanodiscus niagarae and Chaetoceros Elmorei. In general green algae were dominant when lake salinity exceeded 100 g l^-1 although diatoms played important roles in most of these highly saline lakes except for Patience Lake.     

The biology and evolution of Antarctic saline lakes in relation to salinity and trophy

. Five brackish to hypersaline lakes (Highway, Ace, Pendent, Williams and Rookery) in the Vestfold Hills, eastern Antarctica were investigated during the austral summer of 1999/2000. The aims were to characterise the functional dynamics of the plankton and gain an understanding of how the different environments in the lakes have led to the evolution of different communities. The plankton was dominated by microorganisms and differed across the salinity spectrum in relation to trophy, age and the presence of meromixis. However, some elements of the plankton were common to all of the lakes, e.g. the mixtrophic ciliate, Mesodinium rubrum, which reached abundances of 2.7᎒⁵ l^-1 and spanned a salinity gradient of 4-63‰. Marine dinoflagellate species also occurred in all of the lakes, often at high abundances in Highway Lake, Pendent Lake and Lake Williams. During December (mid-summer), primary production showed an increase along the salinity gradient from Highway Lake to Lake Williams; however, it was low in hyper-nutrified Rookery Lake because of the turbidity of the waters. Bacterial production followed the same trend and was extremely high in Rookery Lake (327 µg l^-1 h^-1 in January). The lakes possessed a marine microbial plankton that has become very simplified through time, and now contains a small number of highly successful species, which were pre-adapted to surviving in extreme Antarctic lakes.     

Alkaline soda Lake Velika Rusanda (Serbia): the first insight into diatom diversity of this extreme saline lake

Alkaline soda lakes are unique habitats found in specific geographic regions, usually with dry climate. The Carpathian Basin is one of those regions very important for habitat and biodiversity conservation in Europe, with natural soda lakes found in Austria, Hungary and Serbia. In comparison to other two countries from Central Europe, algal biodiversity studies of saline soda lakes in Serbia are scarce. Lake Velika Rusanda has the highest measured salinity of all saline lakes in the Carpathian Basin and there were no reports of its diatom species richness and diversity till now. We conducted 2-year investigation programme to study biodiversity and seasonal dynamics of diatoms in this lake. A total of 27 diatom taxa were found, almost all of them attached to reed and much less in benthos and plankton. Five new diatom species for Serbia were recorded, Craticula halopannonica, Navicymbula pusilla, Hantzschia weyprechtii, Nitzschia thermaloides and Navicula staffordiae. The last mentioned is new for Europe as well. Lake Velika Rusanda is inhabited mostly by alkaliphilous and halophilic diatoms. Since diatoms are used as bioindicators in soda lakes, our results will improve their further application in ecological status assessment of these fragile habitats in the Carpathian Basin.

     

Gladioferens Henry (Copepoda: Calanoida) discovered in Antarctica: G. antarcticus sp. nov. described from a lake in the Bunger Hills

A new species of Gladioferens is described from a freshwater lake in the Bunger Hills, Greater Antarctica. A key to the six species of Gladioferens is provided for both sexes. Most species of the subgenus containing G. antarcticus sp. nov. are remarkable in possessing asymmetries in the second legs (male) and fourth legs (female). This suggests that the mating behaviour of these species may be radically different from that in most heterarthrandrian calanoids and calls for further study. However, G. antarcticus is more primitive than its consubgeners in having, in the male, symmetrical second legs and 3-segmented endopods in the fifth legs. The genus shows a highly disjunct distribution (Australia, New Zealand and Bunger Hills) and its biogeography is now of outstanding interest.     

Nematodes from saline and freshwater lakes of the Vestfold Hills,East Antarctica,including the description of <Emphasis Type="Italic">Hypodontolaimus antarcticus</Emphasis> sp. n.

The invertebrate fauna of many Antarctic ice-free areas, even those close to permanent research stations, can be poorly known. Here we describe some nematodes from freshwater and saline, marine-derived lakes of the Vestfold Hills, East Antarctica. The freshwater lakes contained the widespread East Antarctic endemic species, Plectus frigophilus Kirjanova, 1958. The saline lakes were inhabited by two recently described species, Halomonhystera halophila Andrássy, 2006 and Halomonhystera continentalis Andrássy, 2006, and by a new species described in this report, Hypodontolaimus antarcticus sp. n. Originally marine but now brackish Highway Lake contained a nematode fauna with both freshwater and marine-derived components. The nematode fauna of Antarctica now consists of 54 named species, 22 of which are found in East Antarctica.     

<Emphasis Type="Italic">Rhinoglena kutikovae</Emphasis> n.sp. (Rotifera: Monogononta: Epiphanidae) from the Bunger Hills,East Antarctica: a probable relict species that survived Quaternary glaciations on the continent

A new species of rotifer, Rhinoglena kutikovae n.sp. (Monogononta: Epiphanidae), is described from a freshwater lake in the Bunger Hills, East Antarctica. The new taxon is characterized by the following combination of characters: body conical to vase-shaped; a single toe; distal foot pseudosegment bulged; tail prominent, semi-circular; two small spherical pedal glands with common duct, forming a complex with caudal ganglion; trophi with seven major teeth with offset head and two smaller teeth without offset head. The new species is compared with R. fertoeensis, R. frontalis and R. tokioensis, of which scanning electron microscopic information is presented of the trophi. R. kutikovae n.sp. is probably a relict species that survived Quaternary glaciations in glacial lacustrine refugia on the Antarctic continent.     

Viruses in the plankton of freshwater and saline Antarctic lakes

1. Virus‐like particle (VLP) abundances in nine freshwater to saline lakes in the Vestfold Hills, Eastern Antarctica (68° S) were determined in December 1999. In the ultra‐oligotrophic to oligotrophic freshwater lakes, VLP abundances ranged from 1.01 to 3.28 × 10⁶ mL^–1 in the top 6 m of the water column. In the saline lakes the range was between 6.76 and 36.5 × 10⁶ mL^–1. The lowest value was found in meromictic Ace Lake and the highest value in hypersaline Lake Williams. Virus to bacteria ratios (VBR) were lowest in the freshwater lakes and highest in the saline lakes, with a maximum of 23.4 in the former and 50.3 in the latter. 2. A range of morphologies among VLP was observed, including phages with short (Podoviridae) and long tails, icosahedric viruses of up to 300 nm and star‐like particles of about 80 nm diameter. 3. In these microbially dominated ecosystems there was no correlation between VLP and either bacterial numbers or chlorophyll a. There was a significant correlation between VLP abundances and dissolved organic carbon concentration (r=0.845, P < 0.01). 4. The data suggested that viruses probably attack a spectrum of bacteria and protozoan species. Virus‐like particle numbers in the freshwater lakes were lower than values reported for lower latitude systems. Those in the saline lakes were comparable with abundances reported from other Antarctic lakes, and were higher than most values published for lower latitude lakes and many marine systems. Across the salinity spectrum from freshwater through brackish to hypersaline, VLP concentrations increased roughly in relation to increasing trophy. 5. Given that Antarctic lakes have a plankton almost entirely made up of bacteria and protists, and that VLP abundances are high, it is likely that viruses play a pivotal role in carbon cycling in these extreme ecosystems.     

The plankton community of a young, eutrophic, Antarctic saline lake

A shallow, saline lake (Rookery Lake) close to the sea and surrounded by a penguin rookery was investigated during the austral spring and summer of 1996/1997. The proximity to the sea means that the lake is likely to have been formed recently during isostatic uplift. Inputs of carbon and nutrients from the penguin rookery have rendered Rookery Lake eutrophic compared with other brackish and saline lakes in the Vestfold Hills. Chlorophyll a concentration, bacterioplankton, heterotrophic nanoflagellate and phototrophic nanoflagellate abundances were all significantly higher than in other non-enriched lakes. The high productivity created seasonal anoxia during winter and spring below ice cover. The ciliate community resembled the marine community, and was dissimilar to that seen in older saline lakes within the Vestfold Hills. Thus Rookery Lake provides valuable evidence of the impact of natural eutrophication on an Antarctic lake, as well as of the evolution of the typical microbial community which dominates the older lakes of the Vestfold Hills. Accepted: 2 May 1999     

The biodiversity and ecology of Antarctic lakes: models for evolution

Antarctic lakes are characterised by simplified, truncated food webs. The lakes range from freshwater to hypersaline with a continuum of physical and chemical conditions that offer a natural laboratory in which to study evolution. Molecular studies on Antarctic lake communities are still in their infancy, but there is clear evidence from some taxonomic groups, for example the Cyanobacteria, that there is endemicity. Moreover, many of the bacteria have considerable potential as sources of novel biochemicals such as low temperature enzymes and anti-freeze proteins. Among the eukaryotic organisms survival strategies have evolved, among which dependence on mixotrophy in phytoflagellates and some ciliates is common. There is also some evidence of evolution of new species of flagellate in the marine derived saline lakes of the Vestfold Hills. Recent work on viruses in polar lakes demonstrates high abundance and high rates of infection, implying that they may play an important role in genetic exchange in these extreme environments.     

Salinity, depth and the structure and composition of microbial mats in continental Antarctic lakes

1. Lakes and ponds in the Larsemann Hills and Bølingen Islands (East‐Antarctica) were characterised by cyanobacteria‐dominated, benthic microbial mats. A 56‐lake dataset representing the limnological diversity among the more than 150 lakes and ponds in the region was developed to identify and quantify the abiotic conditions associated with cyanobacterial and diatom communities. 2. Limnological diversity in the lakes of the Larsemann Hills and Bølingen Islands was associated primarily with conductivity and conductivity‐related variables (concentrations of major ions and alkalinity), and variation in lake morphometry (depth, catchment and lake area). Low concentrations of pigments, phosphate, nitrogen, DOC and TOC in the water column of most lakes suggest extremely low water column productivity and hence high water clarity, and may thus contribute to the ecological success of benthic microbial mats in this region. 3. Benthic communities consisted of prostrate and sometimes finely laminated mats, flake mats, epilithic and interstitial microbial mats. Mat physiognomy and carotenoid/chlorophyll ratios were strongly related to lake depth, but not to conductivity. 4. Morphological‐taxonomic analyses revealed the presence of 26 diatom morphospecies and 33 cyanobacterial morphotypes. Mats of shallow lakes (interstitial and flake mats) and those of deeper lakes (prostrate mats) were characterised by different dominant cyanobacterial morphotypes. No relationship was found between the distribution of these morphotypes and conductivity. In contrast, variation in diatom species composition was strongly related to both lake depth and conductivity. Shallow ponds were mainly characterised by aerial diatoms (e.g. Diadesmis cf. perpusilla and Hantzschia spp.). In deep lakes, communities were dominated by Psammothidium abundans and Stauroforma inermis. Lakes with conductivities higher than ±1.5 mS cm^?1 became susceptible to freezing out of salts and hence pronounced conductivity fluctuations. In these lakes P. abundans and S. inermis were replaced by Amphora veneta. Stomatocysts were important only in shallow freshwater lakes. 5. Ice cover influenced microbial mat structure and composition both directly by physical disturbance in shallow lakes and by influencing light availability in deeper lakes, as well as indirectly by generating conductivity increases and promoting the development of seasonal anoxia. 6. The relationships between diatom species composition and conductivity, and diatom species composition and depth, were statistically significant. Transfer functions based on these data can therefore be used in paleolimnological reconstruction to infer changes in the precipitation–evaporation balance in continental Antarctic lakes.     

The microbial composition of three limnologically disparate hypersaline Antarctic lakes

16S rRNA clone library analysis was used to examine the biodiversity and community structure within the sediments of three hypersaline Antarctic lakes. Compared to sediment of low to moderate salinity Antarctic lakes the species richness of the hypersaline lake sediments was 2-20 times lower. The community of Deep Lake (32% salinity, average sediment temperature -15 degrees C) was made up almost entirely of halophilic Archaea. The sediment communities of two meromictic hypersaline lakes, Organic Lake (20% salinity, -7 degrees C) and Ekho Lake (15% salinity, 15 degrees C) were more complex, containing phylotypes clustering within the Proteobacteria and Cytophagales divisions and with algal chloroplasts. Many phylotypes of these lakes were related to taxa more adapted to marine-like salinity and perhaps derive from bacteria exported into the sediment from the lower salinity surface waters. The Ekho Lake clone library contained several major phylotypes related to the Haloanaerobiales, the growth of which appears to be promoted by the comparatively high in situ temperature of this lake.     

Depth distribution of euryhaline halophilic bacteria in Suribati Ike, a meromictic lake in East Antarctica

Euryhaline halophiles grow over a wide range of salinity, from <3% NaCl (seawater equivalent) to >15% NaCl and even saturation level (about 30% NaCl). Several species of euryhaline halophiles occur worldwide, especially in marine environments and also in aquatic and terrestrial habitats of the Antarctic ice-free areas. A biogeographic view of Antarctic halophiles is that their migration among lakes on land is more difficult than in marine setting. Ponds and lakes on land may thus serve as “islands” which facilitate the selection and separation of unique species. We isolated euryhaline halophiles from the saline lake, Suribati Ike, near Syowa Station and placed them into seven groups, each demonstrating a clear depth-related distribution. Six of the seven groups probably represent new species of the genera Halomonas and Marinobacter. This result suggests that Antarctic saline lakes exhibit high selectivity of unique euryhaline halophiles and possibly of other microbial groups.     

Diatom community response along a productivity gradient of shallow Antarctic lakes

Summary Antarctic lakes are simple ecosystems ranging in productivity from extremely low productive melt-water lakes to highly productive guano lakes. With the aim to assess the importance of environmental variables for species composition and abundance of periphytic diatoms, we quantified light availability and nutrient concentration in the water and in the sediment of 21 Antarctic lakes. Of a total of 66 diatom taxa identified, the distribution of 16 species were investigated in detail. Four of these (25%) showed highest abundance in highly productive lakes (low light/high nutrient availability), whereas three species (19%) increased in abundance as productivity decreased (high light/low nutrient availability). Some ecological theories predict that species richness shows a maximum in medium productive systems and a decreasing trend as productivity increases further due to competition. Other theories suggest that physical factors, including climate, is the major factor determining species richness. The results from our study suggest that none of the theories are completely wrong or right, but that they have to be combined to explain as much as possible of the variation in species richness.     

Widespread occurrence of populations of the unique autotrophic ciliate Metodinium rubrum (Ciliophora: Haptorida) in brackish and saline lakes of the Vestfold Hills (eastern Antarctica)

The occurrence of the unique autotrophic ciliate Mesodinium rubrum was investigated in a suite of lakes of various salinities situated in the Vestfold Hills oasis, Princess Elizabeth Land (eastern Antarctica). M. rubrum was found to occur in all but the most hypersaline lakes in the survey but was most numerous in the more brackish lakes. Salinity and water column temperature appeared to be the most important factors controlling the occurrence and abundance of this species. Nutrient levels (phosphate and nitrate) did not appear to be important controlling factors, although their influence may have been distorted by the fact that nutrient concentrations were generally higher in the more saline lakes. The widespread occurrence of this species in brackish and saline lakes of the Vestfold Hills provides opportunities to study the ecology and possible physiological and ultrastructural adaptations to living in a high-latitude environment of this ubiquitous and important species in marine microbial food webs.     

Diversity, ecology and biogeography of the freshwater diatom communities from Ulu Peninsula (James Ross Island, NE Antarctic Peninsula)

The diversity, ecology and biogeography of diatoms in lakes, seepage areas and streams on the Ulu Peninsula, a large ice-free area in the northern part of James Ross Island (Weddell Sea), were studied. A diverse diatom flora of 123 taxa was observed, dominated by several Nitzschia taxa, Psammothidium papilio, Eolimna jamesrossensis, Fragilaria capucina and Fistulifera saprophila. The results from the similarity and diversity analysis suggest James Ross Island to be biogeographically positioned within the Maritime Antarctic region, yet with some affinities with the flora of Continental Antarctica, as shown by the presence of Luticola gaussii and Achnanthes taylorensis. Based on our data, James Ross Island can thus be located close to the boundary of the two main Antarctic biogeographical regions. Diatom communities present in streams and seepage areas could be clearly distinguished from those in lakes, the latter being much more species rich. Based on the multivariate analysis, conductivity and nutrients were selected as the two main environmental factors determining the diatom composition in the Ulu Peninsula lakes. The revised taxonomy of the Antarctic diatom flora induced the construction of a transfer function for water conductivity in the studied lakes that can be applied in further palaeoecological studies.     

Epilithic diatoms of mountain lakes of the Tatra Mountains (Slovakia)

In the framework of the international project EMERGE, species composition of epilithic diatoms of 34 selected high mountain lakes of Slovak part of the Tatra Mountains were investigated. In all, 127 taxa of diatoms belonging to 26 genera were recorded. Comparison of the epilithic assemblages of the investigated lakes showed differences both in relative abundance and taxa present in the individual lakes. On the basis of species composition and relative abundance of epilithic diatoms using hierarchical cluster analysis, two main groups of lakes were created. The first group includes 4 lakes which can be classified as strongly acidified and 9 lakes which are acidified or threatened by acidification. In this group, acidophilous species such as Achnanthes helvetica, A. marginulata, Aulacoseira distans and Tabellaria flocculosa prevailed. The second group includes 19 non-acidified lakes. The most common diatoms in these lakes were Achnanthes minutissima, A. helvetica, Cymbella minuta and Denticula tenuis which occur practically in all these lakes but with different abundances. The division of lakes due to their diatom species composition mostly confirmed the status of these lakes as judged from their water chemistry.     

Shifts in the dominance between diatoms and cryptophytes during three late summers in the Bransfield Strait (Antarctic Peninsula)

Recent global warming reduces surface water salinity around the Antarctic Peninsula as a result of the glacial meltwater runoff, which increases the occurrence and abundance of certain phytoplankton groups, such as cryptophytes. The dominance of this particular group over diatoms affects grazers, such as Antarctic krill, which preferentially feed on diatoms. Using three late summer data sets from the Bransfield Strait (2008–2010), we observed variations in the dominant phytoplankton groups determined by HPLC/CHEMTAX pigment analysis and confirmed by microscopy. Results indicate that the dominance of diatoms, particularly in 2008 and 2009, was associated with a deeper upper mixed layer (UML), higher salinity and warmer sea surface temperature. In contrast, cryptophytes, which were dominant in 2010, were associated with a shallower UML, lower salinity and colder sea surface temperatures. The low diatom biomass observed in the summer of 2010 was associated with high nutrient concentration, particularly silicate, and low chlorophyll a (summer monthly average calculated from satellite images). The interannual variability here observed suggests a delayed seasonal succession cycle of phytoplankton in the summer of 2010 associated with a cold summer and a late ice retreat process in the region. This successional delay resulted in a notable decrease of primary producers’ biomass, which is likely to have impacted regional food web interactions. This study demonstrates the susceptibility of the Antarctic phytoplankton community structure to air temperature, which directly influences the timing of ice melting and consequently the magnitude of primary production and succession pattern of phytoplankton groups.     

Biogeographical distribution and ecological ranges of benthic cyanobacteria in East Antarctic lakes

For the first time, the cyanobacterial diversity from microbial mats in lakes of Eastern Antarctica was investigated using microscopic and molecular approaches. The present study assessed the biogeographical distribution of cyanobacteria in Antarctica. Five samples were taken from four lakes spanning a range of different ecological environments in Larsemann Hills, Vestfold Hills and Rauer Islands to evaluate the influence of lake characteristics on the cyanobacterial diversity. Seventeen morphospecies and 28 16S rRNA gene-based operational taxonomic units belonging to the Oscillatoriales, Nostocales and Chroococcales were identified. The internal transcribed spacer was evaluated to complement the 16S rRNA gene data and showed similar but more clear-cut tendencies. The molecular approach suggested that potential Antarctic endemic species, including a previously undiscovered diversity, are more abundant than has been estimated by morphological methods. Moreover, operational taxonomic units, also found outside Antarctica, were more widespread over the continent than potential endemics. The cyanobacterial diversity of the most saline lakes was found to differ from the others, and correlations between the sampling depth and the cyanobacterial communities can also be drawn. Comparison with database sequences illustrated the ubiquity of several cyanobacterial operational taxonomic units and their remarkable range of tolerance to harsh environmental conditions.     

On the use of high‐throughput sequencing for the study of cyanobacterial diversity in Antarctic aquatic mats

The study of Antarctic cyanobacterial diversity has been mostly limited to morphological identification and traditional molecular techniques. High‐throughput sequencing (HTS) allows a much better understanding of microbial distribution in the environment, but its application is hampered by several methodological and analytical challenges. In this work, we explored the use of HTS as a tool for the study of cyanobacterial diversity in Antarctic aquatic mats. Our results highlight the importance of using artificial communities to validate the parameters of the bioinformatics procedure used to analyze natural communities, since pipeline‐dependent biases had a strong effect on the observed community structures. Analysis of microbial mats from five Antarctic lakes and an aquatic biofilm from the Sub‐Antarctic showed that HTS is a valuable tool for the assessment of cyanobacterial diversity. The majority of the operational taxonomic units retrieved were related to filamentous taxa such as Leptolyngbya and Phormidium, which are common genera in Antarctic lacustrine microbial mats. However, other phylotypes related to different taxa such as Geitlerinema, Pseudanabaena, Synechococcus, Chamaesiphon, Calothrix, and Coleodesmium were also found. Results revealed a much higher diversity than what had been reported using traditional methods and also highlighted remarkable differences between the cyanobacterial communities of the studied lakes. The aquatic biofilm from the Sub‐Antarctic had a distinct cyanobacterial community from the Antarctic lakes, which in turn displayed a salinity‐dependent community structure at the phylotype level.