Abstract
Antarctic arthropods (mites and springtails) have been the subject of numerous studies. However, by far, the most diverse and numerically dominant fauna in Antarctica are the limno-terrestrial microfauna (tardigrades, rotifers and nematodes). Although they have been the focus of several studies, there remains uncertainty of the actual number of species in Antarctica. Inadequate sampling and conserved morphology are the main cause of misclassification of species and underestimation of this diversity. Most species’ distributional records are dominated by proximity to research stations or limited opportunistic collections, and therefore, an absence of records for a species may also be a consequence of the limitations of sampling. Limitations in fundamental knowledge of how many species are present and how widespread they are prevents any meaningful analyses that have been applied more generally to the arthropods within Antarctica, such as exploring ancient origins (at least pre-last glacial maximum) and tracking colonisation routes from glacial refugia. In this review, we list published species names and where possible the distribution of microfaunal (tardigrade, rotifer and nematode) species reported for Antarctica. Our current state of knowledge of Antarctic records (south of 60°S) includes 28 bdelloid rotifers, 66 monogonont rotifers, 59 tardigrades and 68 nematodes. In the light of the difficulties in working with microfauna across such geographical scales, we emphasise the need for molecular markers to help understand the ‘true levels’ of diversity and suggest future directions for Antarctic biodiversity assessment and species discovery.
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Introduction
Antarctica has one of the most extreme and challenging environments on the planet, experiencing prolonged winters, freezing temperature and lack of liquid water. It spans nearly 30° of latitude (61°–90°S) and covers an area of 14 million km2 with only 0.3 % of its total area remaining ice- and snow-free year round (British Antarctic Survey 2004). It has been isolated from the other southern continents for around 28 million years by the Southern Ocean (Lawver et al. 1998), since the opening of the South Tasman Rise (32 My) and the Drake Passage (28 My) (Lawver and Gahagan 2003). It has also been covered in a permanent ice sheet for ~34 My (Tripati et al. 2005) and has experienced more than 10 major glacial cycles over the last million years (Hays et al. 1976). Despite this, life has managed to survive. Some of the Antarctic terrestrial arthropods consist of likely descendants of ancestors present in Gondwanan times that have diversified in ice-free isolated locations, such as nunataks, since the completion of glaciation in the late Miocene (~21–11 Mya) (Marshall and Pugh 1996; McInnes and Pugh 1998; Stevens and Hogg 2003; Stevens et al. 2006a). In the case of Antarctic lakes, few studies have dealt with their continuous presence since the break-up of Gondwana. De Smet and Gibson (2008) suggested survival of rotifers in freshwater environments since the last glacial maximum (LGM). Over the last decade, it has become well accepted that several Antarctic localities have remained ice-free throughout the LGM (e.g. Convey and Stevens 2007; Convey et al. 2008, 2009) and some likely to have been ice-free for much longer. Continental regions such as Dronning Maud Land (Marshall and Pugh 1996), Antarctic Peninsula (AP) (Pugh and Convey 2000), southern Victoria Land (Stevens and Hogg 2003, 2006b) and coastal areas (Burgess et al. 1994; Gore et al. 2001; Hodgson et al. 2001) have been suitable for the long-term survival of terrestrial life in ice-free refugia (Cromer et al. 2006; Convey and Stevens 2007) with many terrestrial habitats becoming available for colonisation from refuges within the current inter-glacial period (<17,000 years) (Stevens and Hogg 2003).
The Antarctic limno-terrestrial microfauna is fragmented, patchily distributed and taxonomically restricted, and mostly comprises rotifers, tardigrades and nematodes (e.g. Wharton 2003; Sohlenius et al. 2004; Sohlenius and Boström 2005, 2008; Huiskes et al. 2006). Microfaunal communities have commonly been associated with habitats rich in organic material (algae, moss or lichen), in the vicinity of bird colonies (e.g. Sohlenius et al. 2004; Sohlenius and Boström 2005; Wall 2007), or in lakes or melt pools (e.g. Kirjanova 1958; Suren 1990; Dartnall 2000; Andrássy and Gibson 2007; De Smet and Gibson 2008). The limno-terrestrial microfauna form a vital component of the food web, playing an essential function in soil ecosystem processes, mainly in recycling nutrients and processes of decomposition (Sands et al. 2008). Today fewer than 550 non-marine invertebrate species have been identified from Antarctica (Adams et al. 2006; Convey et al. 2008, 2009). Most of these are endemic (58 %) and can be defined as continental (>25 %) or maritime (>29 %), with only 3 % of species having a pan-Antarctic distribution (Pugh and Convey 2008). Diversity is greatest for the microfauna (rotifers, tardigrades and nematodes) (e.g. Dastych 1984; Andrássy 1998; Convey and McInnes 2005; Adams et al. 2006; Sohlenius and Boström 2008), followed by arthropods, particularly springtails (Collembola) and mites (Acari) (e.g. Hogg and Stevens 2002; Sinclair and Stevens 2006; Stevens and Hogg 2006b). Given these basic statistics, it is surprising that the arthropods have received a disproportionate amount of attention and that there is no single study that provides a complete list of diversity and distribution for the Antarctic microfaunal species of the Phyla Rotifera, Tardigrada and Nematoda. Such an important synopsis of the microfauna may have been seen as a difficult task when it is widely regarded that identification to morpho-species of these minute microfauna are often difficult given the lack of distinctive morphological features (e.g. Andrássy 1998; Floyd et al. 2002; Robeson et al. 2009) resulting in misclassification and underestimation of diversity (Adams et al. 2006; Fontaneto et al. 2009; Stevens et al. 2011).
In order to assess microfaunal diversity in Antarctica (south of 60°S), we have used, for continental Antarctica, the sectors: Maud, Enderby, Wilkes, Scott, Byrd and Ronne (see Pugh 1993). We have also included the AP, and the maritime Antarctica (west of AP, and the sub-Antarctic islands of South Orkney and South Shetland; Fig. 1). The selection of these largely empirical sectors has also been adopted by other studies (e.g. McInnes and Pugh 1998; Convey and McInnes 2005; Pugh and Convey 2008) but do not represent the bioregions as defined by Terauds et al. (2012). The aim here is to compile the current state of knowledge of Antarctic limno-terrestrial microfaunal diversity and distribution based on morphology of rotifers, tardigrades and nematodes (collectively referred to in this review as microfauna) from continental and maritime Antarctica. We then discuss potential dispersal mechanisms and the need to establish diversity by combining molecular methods. We conclude with suggestions for future directions for Antarctic biodiversity assessment and species discovery.
Current state of knowledge
Microfauna community
Tardigrada
The Phylum Tardigrada is divided into three Classes (Heterotardigrada, Mesotardigrada and Eutardigrada), which comprise a total of ~800 species of freshwater, terrestrial and marine tardigrades worldwide (McInnes and Pugh 1998). Most of the limno-terrestrial forms belong to the Class Eutardigrada, and to some extent the Heterotardigrada (which also include marine forms) (Kinchin 1994). To date, 64 published species of tardigrades have been reported for Antarctica and sub-Antarctic islands (including records north of 60°S; McInnes and Pugh 2007), although no species list was included in their work. In the present review, we list 59 records of Antarctic tardigrades (south of 60°S) from 34 references and compiled a species distribution list for all named Antarctic tardigrades (Table 1). Records for continental Antarctica include 42 species, while for maritime Antarctica, 36 species are reported (19 shared species). We found no records for Byrd sector and only three records for Ronne sector, because of a probable lack of studies in these areas. The most widespread tardigrades in Antarctica are the pan-Antarctic species Acutuncus antarcticus Binda and Pilato 2000 and Milnesium tardigradum Doyère, 1840 (Table 1). Misidentifications and species synonyms have been included in the online Supplementary Material (Online Resource 1).
Rotifera
The Phylum Rotifera includes the Classes Bdelloidea, Monogononta and Seisonidea, with the former two being most common in Antarctica. Segers (2007) listed 92 rotifer species and assigned them to ‘Antarctica’ (including sub-Antarctic islands north of 55°S) but without specifying geographical regions. We confirmed, from other references, the presence of 63 of those species (44 monogononts and 19 bdelloids) listed by Segers (2007) to occur in continental and/or maritime Antarctica (south of 60°S) (see Tables 2 and 3). Most records in the literature correspond to the widely known Antarctic endemic Philodina gregaria Murray 1910, which has been reported from across Antarctica. Frequently found with P. gregaria is another endemic Antarctic rotifer Adineta grandis Murray 1910 and two cosmopolitan species Epiphanes senta Müller, 1773 and Cephalodella catellina Müller, 1786. All four species are usually found in bodies of water that remain frozen in the winter and have a circumpolar distribution similar to other cosmopolitan species from terrestrial habitats (Adineta gracilis Janson, 1893) and lake habitats (Collotheca ornata cornuta Dobie, 1849 and Lepadella patella Müller, 1773) (Dartnall 1983). We have compiled a distribution list (based on published species) of Antarctic limno-terrestrial rotifers that includes 66 monogonont and 28 bdelloid species from 24 different reference sources (Tables 2 and 3). Species records reported by Segers (2007) for Antarctica that were not confirmed by other references can be found in the Supplementary Material (Online Resource 2). For a list of species synonyms, refer to the Online Resource 3.
Nematoda
Nematodes are usually associated with rotifers and tardigrades and generally found in areas where moss, lichens or algae are present (e.g. Timm 1971; Sohlenius et al. 2004; Velasco-Castrillón et al. 2014). Some species (Plectus frigophilus Kirjanova 1958; Halomonhystera spp) have also been recorded from Antarctic lakes (Kirjanova 1958; Andrássy and Gibson 2007) or in highly organic soils adjacent to bird colonies, for example Panagrolaimus (Sohlenius 1989; Sinclair 2001). According to Wharton (2003), nematodes are the most diverse and abundant invertebrates in both the maritime and continental Antarctic regions. The Phylum includes the Classes Dorylaimia, Enoplia and Chromadoria (Meldal et al. 2007), which according to Andrássy (2008a) are represented by 54 species from Antarctica, 32 in the maritime region and 22 from continental Antarctica. In the present review, we list 68 published species for Antarctica (Table 4). We identified 34 species occurring in continental Antarctica and 37 species in maritime Antarctica (see Velasco-Castrillón and Stevens 2014). Of particular interest is the geographical overlap of three species (Plectus murrayi Yeates 1970; P. frigophilus and Teratocephalus tilbrooki Maslen, 1979). P. murrayi and P. frigophilus (commonly known for continental Antarctica) were represented by unconfirmed records for maritime Antarctica. While T. tilbrooki known from maritime Antarctica, (Andrássy 1998) was reported for continental Antarctica (Table 4). Unfortunately, no morphological or molecular data were provided in these studies. The overlap of P. murrayi with other species could be a result of the difficulties encountered in the identification of Plectus species and especially of those lacking males (see Boström 2005). Species synonyms have been included in Supplementary Material (Online Resource 4).
Microfaunal dispersal and occurrence
Information on dispersal of Antarctic invertebrates results from casual observations from arthropod collections, which have received comparatively more work in Antarctica (see Convey et al. 2008, 2009). It is believed that air currents are one potential mode of passive dispersal (Miller and Heatwole 1995; Greenslade et al. 1999; Muñoz et al. 2004; Nkem et al. 2006; Hawes et al. 2007). This method of transport may not be as successful for arthropods (springtails, mites, dipterans) due to potential desiccation (see Marshall and Pugh 1996). Other possible dispersal mechanisms are birds (Stevens and Hogg 2002), bubbles carried in water currents (Rounsevell and Horne 1986) or on floating materials in melt-water streams (Moore 2002; Sinclair and Stevens 2006). For nematodes, tardigrades and rotifers, with a specialised dispersal life stage, a far greater potential for dispersal via wind and water has been suggested (Stevens and Hogg 2006a). However, long-range dispersal (inter-oceanic), even during the anhydrobiotic phase, has been questioned by McInnes and Pugh (1998). Dispersal by human activities has also been reported in the literature, particularly for the sub-Antarctic islands and maritime Antarctica (e.g. Burn 1984; Greenslade and Wise 1984; Rounsevell and Horne 1986).
Records of species in some areas could be relicts from a warmer pre-Pleistocene period in Antarctica (McInnes and Pugh 1998), descendants of more recent arrivals from outside the continent (Sohlenius et al. 2004), or simply the result of misidentification (McInnes 1995; Czechowski et al. 2012). Successful colonisation requires suitable conditions for the propagules to survive, establish and reproduce (Miller et al. 1994). Given the isolation of ice-free habitats, we would expect a very low probability of colonisation and the presence of habitat patches lacking microfauna (Sohlenius et al. 2004). For slow, more gradual changes (climate and environmental change) dispersal to new areas of suitable habitat may be possible provided that the rate of change does not exceed their dispersal ability to find a new alternative habitat. At a larger scale (hundreds of kilometres), the rate of change may occur in conjunction with other changes (soil formation, vegetation growth), although long-distance dispersal between habitats may be limited (Wise 1967; Hogg and Stevens 2002; Stevens and Hogg 2002). Furthermore, several studies have suggested that the time since the last glaciation has been insufficient for successful colonisation of favourable habitats by soil taxa (Convey and Block 1996; Convey and Stevens 2007; Convey et al. 2008), and this is supported by recent data for arthropods (Stevens et al. 2006a; Stevens and Hogg 2006a). Accordingly, the natural dispersal of animals, other than local, seems unlikely to provide an adequate response to any environmental change. Long-term patterns can be useful in determining whether taxa are capable of migrating over large distances, whether they have persisted over long-term environmental change, or if they are the result of exotic introductions either by natural (passive) or by anthropogenic means. Such analyses for the microfauna is, however, currently limited until accurate widespread data for species identifications can lead to informed diversity and distributions.
Establishing diversity and distribution
Rotifera, Tardigrada and Nematoda are the most abundant and diverse microfaunal groups in the Antarctic region, but even greater levels of cryptic diversity are expected. Studies on the arthropods (Collembola and Acari) (e.g. Stevens et al. 2006b) have revealed that several new genetic entities (species) are present in the Antarctic and on sub-Antarctic islands, and this has also been found for the microfauna (Fontaneto et al. 2008; Sands et al. 2008; Czechowski et al. 2012). The species diversity of these ecologically important animals is still unresolved because taxonomic work has been dominated by arthropods (Greenslade and Wise 1984; Greenslade 1995; Stevens et al. 2006b). However, it is apparent that species diagnosis is difficult in many cases due to the conservative morphology of the microfauna (e.g. Andrássy 1998; Floyd et al. 2002; Robeson et al. 2009).
Molecular studies are needed to delineate species boundaries and dispersal patterns (e.g. Stevens et al. 2006b; Sands et al. 2008; Torricelli et al. 2010). It will then be possible to make accurate assessments of the patterns and processes of biodiversity of the microfauna, which will further our knowledge of the evolutionary history throughout the Southern Hemisphere (Convey and Stevens 2007; Convey et al. 2008). These studies are now beginning to explain the significance of glacial events in determining patterns of species’ distribution and genetic diversity for terrestrial communities in Antarctica (Courtright et al. 2000; Frati et al. 2001; Stevens and Hogg 2006a). They have revealed that some taxa of little dispersal capability have large-scale biogeographic distributions across Antarctica and the sub-Antarctic islands (e.g. Convey and McInnes 2005; Stevens and Hogg 2006a; Czechowski et al. 2012). Collectively, these studies have revealed a significant effect of glacial and sea–ice barriers to examine the mobility and gene flow of Antarctic taxa across fragmented landscapes over evolutionary time scales.
Future directions in biodiversity assessment and species discovery in Antarctica
With increased access to molecular techniques (Hebert et al. 2003), the diversity of Antarctic invertebrates and the association between organisms and environments can now be estimated to levels previously unimaginable (Peck 2005; Ji et al. 2013). Molecular techniques can be used to test hypotheses related to connectivity (i.e. gene flow) and reveal phylogeographic processes that have moulded the pattern of genetic diversity among populations, as well as their evolutionary history and relationships to other taxa (Stevens and Hogg 2006a). The usefulness of the mitochondrial cytochrome c oxidase I (COI) gene as a DNA barcode to determine sequence divergence among invertebrates and discern among morphologically similar (cryptic) species is now well established (e.g. Hebert et al. 2003; Stevens and Hogg 2003; Stevens et al. 2006a). COI records can now be found for Antarctic arthropods (e.g. Stevens and Hogg 2003, 2006a; Stevens et al. 2006a; Stevens and D’Haese 2014) and collectively have revealed patterns of recolonisation from glacial refugia that show far greater diversity than known previously. Most of the success of these data have been due to capturing most of the geographical range for species. Comparatively, molecular data for the microfauna from Antarctica are limited to tardigrades (Sands et al. 2008; Czechowski et al. 2012) and more recently nematodes (Velasco-Castrillón and Stevens 2014) and bdelloid rotifers (Velasco-Castrillón et al. 2014). These studies have tended to have restricted sample sizes and/or geographical coverage limiting their use for biogeographic comparisons beyond diversity and systematics. Despite this, they have revealed greater diversity in Antarctica than has been previously recognised. With an increasing attention of microfauna outside continental Antarctica on bdelloid rotifers (Fontaneto et al. 2008) and nematodes (e.g. Blouin 2000; Derycke et al. 2010; Prosser et al. 2013), the potential for examining the distribution of microfauna throughout Antarctica and its neighbouring landmasses will provide one of the most comprehensive datasets for any group of organisms across the continent.
Rotifera, Nematoda and Tardigrada are critical microfaunal groups given their role in nutrient recycling and their importance in Antarctic limno-terrestrial ecosystems. Unfortunately, we are in our infancy in our understanding of these ecosystems in Antarctica and we highlight below three areas that are fundamental in providing information on diversity, distributional range and type of habitats in which microfauna are found; information that is critical for future conservation and land management, and in detecting new species and species introductions.
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(1)
Molecular techniques need to be applied to the identification of species. Most of the Antarctic microfauna to date are limited to morphological assessments, and past molecular studies have shown that this has not accurately reflected the biodiversity present, particularly where wide species ranges have been reported. This is fundamental information necessary for understanding and managing sustainable biodiversity as well as detecting exotic introductions.
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(2)
Sampling in Antarctica has tended to ignore information linked to abiotic data (e.g. soil chemistry, mineral analyses, and other environmental) which are important in establishing comparisons among biotic communities (i.e. do the same communities occur in similar habitats) and can also be used in predictive modelling of Antarctic biodiversity and habitat requirements (e.g. Convey et al. 2014; Fraser et al. 2014).
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(3)
Recently, biotic data have been assessed for Antarctica in an attempt to determine biogeographic regions (Terauds et al. 2012). The use of GIS systems to define Antarctic Conservation Biogeographic Regions (ACBR) (see Terauds et al. 2012) is an important step forward, but only with the inclusion of phylogenetically informed biodiversity will we be able to have accurate ACBRs. The implementation of the current knowledge on microfaunal diversity (as shown in this review) with genetic lineages identified by phylogenetic studies combined with abiotic data will help to better delineate ACBRs.
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Acknowledgments
We thank Dieter Piepenburg for editorial comments and two anonymous reviewers. In particular, we thank Dr. Sven Boström for providing a thorough review of the nematodes and Dr. Sandra McInnes for assisting with the tardigrades. We are grateful to the University of Adelaide (http://www.sciences.adelaide.edu.au/) for a PhD scholarship to AVC and the South Australian Museum Mawson Trust for providing funding for the Sir Douglas Mawson Doctoral Scholarship (http://www.samuseum.sa.gov.au/). This study was partially supported and funded by the Australian Antarctic Division (http://www.antarctica.gov.au/) Project (ASAC 2355 to MIS).
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Velasco-Castrillón, A., Gibson, J.A.E. & Stevens, M.I. A review of current Antarctic limno-terrestrial microfauna. Polar Biol 37, 1517–1531 (2014). https://doi.org/10.1007/s00300-014-1544-4
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DOI: https://doi.org/10.1007/s00300-014-1544-4