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Inland aquatic biodiversity in Antarctica

Inland aquatic biodiversity in Antarctica

Information Summary

Version: 1.0

Published: 21/08/2019 GMT

Reviewed: 21/08/2019 GMT

Authors

Ian Hawes (1)*, Anne D. Jungblut (2), Josef Elster (3), Bart Van de Vijver (4), Jill Mikucki (5)

(1) University of Waikato, New Zealand
(2) Natural History Museum, UK
(3) University of South Bohemia in České Budějovice, Czech Republic
(4) Meise Botanic Garden, Belgium
(5) University of Tennessee, USA

* ian.hawes@waikato.ac.nz

Synopsis

Studies of Antarctic inland waters have been underway for more than a hundred years. Biodiversity is impoverished compared to other climatic zones and, for most groups of organisms, decreases from the Antarctic Peninsula, through the Coastal Oases to Continental deserts. Many groups of organisms have failed to colonise or survive in Antarctica allowing microbes to predominate in many food webs, especially at high latitudes. Modern molecular biology techniques offer promise towards elucidating patterns of biodiversity among poorly understood Antarctic microbial and viral communities. Subglacial aquatic environments may represent the vast majority of Antarctic inland waters, yet remain largely unexplored. The Antarctic aquatic biota includes organisms and species or strains that are unique to all, or parts, of Antarctica.  The greatest threat comes from non-native species, both from outside and from other parts of the continent. Existing protected areas contain inland waters representing most lake types, but geographic coverage is sparse and unrepresentative overall, in terms of current bioregion designations.


Summary

Inland aquatic biodiversity has been investigated since the earliest expeditions led by Scott and Shackleton [1,2], but knowledge remains patchy on both geographic and taxonomic bases.  The most complete data come from three regions; the Maritime Antarctic (MA, comprising the Antarctic Peninsula and associated islands), the coastal oases of East Antarctica (CO, which we consider as the series of ice-free uplift regions on the northern coast of East Antarctica from 0 to 120o E and at 65 to 70oS), and the more southerly McMurdo Dry Valleys region (MDV, centred on 162oE, 77.5oS). Recent reviews describe communities that are less species diverse than other parts of the globe, but contain assemblages providing all of the functions necessary to form robust food webs [3].  Most contain organisms that are found only in Antarctica [4], an evolution from a previous paradigm that few endemic species exist [5]. Understanding the age, origins, and continental distribution of Antarctic biota is important for developing a robust biodiversity management regime in the face of anticipated change.

Phototrophic primary producers

Cyanobacteria (blue-green algae) are an abundant phototrophic group in Antarctica, often forming mm-cm scale biofilms in fresh and saline inland waters [3,6] (Fig. 1). These thick biofilms contain a variety of other organisms, including protists and microinvertebrates [3,7,8]. Many of these mats dry out episodically with rise and fall of lake water, where the boundary between terrestrial and aquatic taxa is blurred in Antarctica. Water quality, salinity and hydrology are factors in determining taxonomic distribution, though most common taxa appear to have broad environmental growth ranges and wide geographic distributions [7-9]. The cyanobacterial group Oscillatoriales, particularly species of Phormidium/Microcoleus and Leptolyngbya [9], are responsible for most of the benthic biomass and primary production. Nitrogen-fixing cyanobacteria are also widely distributed in lakes and streams, particularly Nostoc, Calothrix and Nodularia. At least some of these dominant mat-forming cyanobacteria appear to be bipolar [10], though others are potentially endemic [9-13] and may have persisted through glaciations in ice-free refuges [5].

Aquatic Fig 1

Figure 1. Benthic microbial mats formed by cyanobacteria at 16 m depth in Lake Bonney (right – scale bar 20 mm) and a micrograph of Phormidium pseudopriestleyi (left – scale 10 μm). Microbial mats adopt a wide range of morphologies and are characteristic of Antarctic lakes, ponds, and streams. (Images Anne Jungblut and Ian Hawes)

Diatoms (Fig. 2) are abundant across Antarctic freshwater ecosystems. Characteristic genera include Luticola (12 taxa), Psammothidium (4 taxa) Pinnularia, Navicula and Muelleria (3 taxa) and Halamphora and Humidophila (2 taxa). Most taxa are endemic to the Antarctic Continent, and show a circumpolar distribution, consistent with persistence through glaciations rather than recent colonization, though due to taxonomic confusion their regional biogeography remains uncertain [14]. Consistent with this picture of persistence through glaciations, the CO and the MDV region show a relatively high diversity and endemicity, with typical taxa including Navicula shackletonii, Halamphora vyvermanii, Luticola gaussii and Muelleria peraustralis.

 

Aquatic Fig 2

Figure 2. Scanning electron micrograph of diatom (Luticola contii) from Maritime Antarctic lakes. Recent investigations suggest the occurrence of more than 50 distinct taxa and a higher degree of endemism than previously thought. (Image Bart Van de Vijver)

Phytoplankton under ice cover are dominated by flagellates, though in ice-free waters non-motile chlorophytes, cyanobacteria and occasionally diatoms are also present. Dinoflagellates are abundant in some saline CO waters and MA lakes [3].

Filamentous green algae are diverse and abundant in lakes and streams of the MA, less so in inland continental waters. Five morphospecies of Zygnemataceae in the MA decrease to one in the CO and none in the MDV.  Other large green algae are circumpolar, including species of Binuclearia, Ulothrix, Klebsormidium and Prasiola. One East Antarctic species of Prasiola (P. antarctica) and one western, P. glacialis, have been recognised, in addition to the widespread P. crispa, but are only distinguishable by molecular techniques [15].

Aquatic mosses are present in lakes and streams [16] and form important habitats for microorganisms (Fig. 3). Nine aquatic genera are known in Western Antarctica and four in Eastern; only Bryum pseudotriquetrum occurs in both. The latter is the only aquatic species to penetrate to the MDVs, where it is known from a single lake.  B. pseudotriquetum is an amphibious species, the case for most aquatic species. An exception is Drepanocladus longifolius, common in the northern MA, which otherwise has its centre of distribution in South America [16].

Aquatic Fig 3

Figure 3. Mosses (mostly Leptobryum sp.) form unique “pillars” in lakes of the Syowa Oasis, rising from prostrate microbial mats. They incorporate cyanobacteria and a diversity of protists and simple metazoans. (Image Dale Andersen, SETI Institute)

Fauna

All Antarctic inland waters lack vertebrates, and share depauperate macroinvertebrate communities [17].  Molluscs are absent and the only truly aquatic insect (Parochlus steinenii) is confined to the South Shetland Islands.  At least 19 species of crustaceans occupy Antarctic lakes, including planktonic and benthic grazers (Fig. 4) and a single predatory copepod (Parabroteus sarsi, MA only). Distributions suggest that some are long term residents of Antarctica, potentially since the Gondwanan break-up, while others are recent colonists from South America [17,18]. Crustacean diversity declines from nine taxa in the MA to seven in the CO (2 classes, including two saline species) to only 2 copepods in the MDV [18].  Antarctica has at least four endemic freshwater crustaceans, all with localised distributions in CO and MDV, where persistence through glaciations in ice-free refuges is again suggested [18].

Aquatic 4

Figure 4. The epibenthic fairy shrimp (Branchinecta gaini) is common in pools and lakes of the Antarctic Peninsula region (and South America). Its overwintering eggs tolerate temperatures below -20oC. Eggs hatch under spring ice cover to ensure that it can complete its life cycle during summer. (Image BAS)

Microinvertebrates are common in both the lake floor and water column communities, particularly protozoa (ciliates and amoeba), rotifers, nematodes, tardigrades (Fig. 5) and flatworms [3,7,8,19,20, 21].  

Aquatic Fig 5

Figure 5. Scanning Electron Micrograph of a tardigrade from a microbial mat in the MDV region. These animals are found even in extreme aquatic habitats and occupy a range of trophic levels. (Image Byron Adams)

In many systems, these occupy the top of food webs, and can accumulate to high numbers. Their taxonomy is difficult, with a high cryptic diversity, and distributions are likely incompletely understood [20]. Diversity in these groups appears to be similar across Antarctic regions, with little evidence of a north-south gradient in richness, though a high degree of distinctiveness between continental and maritime regions is evident [3]. Molecular approaches have confirmed the presence of endemic taxa, of which some are pan-Antarctic and others appear to be regionally distributed [19-21].

Heterotrophic and chemosynthetic prokaryotes

Bacteria and Archaea are, of course, key components of all Antarctic aquatic ecosystems and, together with viruses [22], contribute significantly to biomass on the continent. Indeed, viruses are highly dynamic in Antarctic lakes and may play a more important role in food webs than in other regions [22]. Based on a growing number of molecular surveys using next-generation sequencing techniques, diverse microbial communities are distributed throughout Antarctic surface waters. Bacteria responsible for all major nutrient cycles appear to occur in all aquatic ecosystems where conditions are suitable [23]. For example, Antarctic prokaryotes in fresh and saline lakes and ponds mediate nitrogen, sulphur, iron and methane cycling. While functional commonalities exist in inland waters, even geographically close water bodies, such as the lakes of the MDV, have distinct bacterial diversity [24].

Diverse and abundant microbial taxa have been detected in the most isolated and poorly studied inland aquatic waters on the continent: subglacial ecosystems [25,26] (Fig. 6).   

Aquatic Fig 6

Figure 6. An electron micrograph of a bacterium from Subglacial Lake Willans. (Image Alicia Purcell)

The limited data available suggest that subglacial biota is exclusively Bacteria and Archaea, and diverse metabolic groups have been detected. In the absence of sunlight, these systems derive primary production via chemosynthetic pathways [25-27]. Isolation of subglacial environments may have resulted in locally distinct microbiomes, however testing this is dependent on access to more of the hundreds of inland subglacial Antarctic waters.

Conservation and management

Protection of the biodiversity of inland water bodies is enshrined in the Protocol on Environmental Protection to the Antarctic Treaty, particularly Annex II that requires minimal interference with native taxa, protection from invasive species and avoidance of adverse effects on aquatic environments. A ‘code of conduct’ on Antarctic subglacial lakes exploration was presented at the 2011 Antarctic Treaty Consultative Meeting (ATCM),  with an updated version endorsed by Resolution by Parties at the 2017 ATCM. Specific protection in the form of ASMA and ASPA status is given to some areas containing inland waters; ASMAs 2 and 6 (McMurdo Dry Valleys and the Larsemann Hills), and ASPAs 119 (Pensacola Mountains) 126 (Byers Peninsula), 135 (North East Bailey Peninsula), 136 (Clarke Peninsula), 141 (Yudikori Valley), 147 (Alexander Island) 165 (Edmonson Point) (Fig. 7).  Together these protected areas contain examples of many of the different lake types found in Maritime and Continental Antarctica; though freshwater systems are potentially under-represented in Antarctic protected areas across all Antarctic bioregions.

Aquatic Fig 7

Figure 7. Locations of ASMAs and ASPAs containing significant aquatic habitats in Antarctica. Other known major concentrations of lakes are: SI – Signy Island; ScO – Schirmacher Oasis; SyO Syowa Oasis; VH – Vestfold Hills; BH Bunger Hills. 


Key Events

1903: Scott's "Discovery" expedition: First collections of samples from lakes and ponds.

1908-09: Shackleton’s "Nimrod" expedition: James Murray undertakes detailed study of life in ponds on Ross Island.

1957-58: International Geophysical Year. Limnological research begins in earnest with establishment of facilities in the McMurdo Dry Valleys, Vestfold Hills, Sôya Coast, Schirmacher Oasis and Bunger Hills.

1963: Limnology begins on Signy Island, South Orkney Islands and continues for many decades.

1964: Lake Vostok suggested to exist.  Its presence is confirmed in 1993, leading to initiation of research on subglacial lakes and development of protocols to minimize contamination.

1966: Byers Peninsula protected as a Specially Protected Area (SPA No. 10).  Re-designated as a Site of Special Scientific Interest in 1975 (SSSI No. 6).  Re-designated as an Antarctic Specially Protected Area (ASPA 126) in 2002.

1990: Initiation by the US of the Dry Valleys Long Term Ecological Research program.

1991: Davis Valley and Forlidas Pond identified as a Specially Protected Area (SPA 23) noting that the Area contains some of the most southerly (82.5oS) freshwater ponds known in Antarctica containing plant life.  Re-designated as an Antarctic Specially Protected Area (ASPA 119) in 2002.

2004: Dry Valleys ASMA established through Measure 1 (2004).

2007: Byers Peninsula, Livingstone Island, established as an international limnological reference point by Spain.

2007: Larsemann Hills established as ASMA 6.

2016-18: The United States’ ‘WISSARD program’ demonstrates subglacial hydro-connectivity and collects examples of subglacial organisms.