Nematode diversity and distribution in the southern maritime Antarctic—clues to history?

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Soil Biology & Biochemistry 38 (2006) 3141–3151 www.elsevier.com/locate/soilbio

Nematode diversity and distribution in the southern maritime Antarctic—clues to history? N.R. Maslen, P. Convey British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK Received 23 June 2005; received in revised form 9 December 2005; accepted 19 December 2005 Available online 21 February 2006

Abstract Nematode worms are one of the most important soil faunal groups in Antarctica. However, relatively little is known about their wider distribution, biogeography and history in the region, and taxonomic information remains confused or incomplete. Here, we hypothesise that the Alexander Island (southern maritime Antarctic) fauna includes elements that have survived (at least) the period of Pleistocene glaciation in situ, forming a regional centre of endemism and biodiversity hotspot. We describe nematological surveys carried out across a latitudinal gradient between 68 and 771S along the southern Antarctic Peninsula, comparing the data obtained with the maritime Antarctic fauna described in the few previous studies between northern Marguerite Bay and the South Orkney Islands (60–681S). In general, our survey supports previous findings of a lack of overlap at species level between the maritime and continental Antarctic biogeographical zones, with the large majority of specimens obtained from all survey sites being attributable to known maritime or new and currently endemic taxa. However, collections from Alexander Island, Alamode Island and the most westerly site sampled, Charcot Island, include specimens morphologically very close to two known continental Antarctic species, which may indicate a link between the two regions. The fauna obtained at the northern study sites (ca. 681S, Adelaide Island, Marguerite Bay) closely matches that described previously. However, in contrast with widely described patterns of decreasing diversity in other Antarctic biota, species richness increased markedly at locations on Alexander Island (ca. 721S), including a substantial element of undescribed species (50% of taxa across all locations, 40% of taxa found on Alexander Island). Finally, the most southerly samples obtained, from inland nunataks in Ellsworth Land (75–771S), indicate a fauna that does not include nematodes, which is exceptional not only in an Antarctic context but also for soils worldwide. r 2006 Elsevier Ltd. All rights reserved. Keywords: Nematode diversity; Endemism; Glacial refuge; Diversity trends; Antarctic biogeography

1. Introduction The terrestrial fauna of Antarctica is depauperate, both through lacking many of the higher groups typical of less extreme habitats worldwide, and in having low species richness even within the groups that are represented (Block, 1984; Convey, 2001). In the maritime Antarctic, higher insects are represented by only two species of Diptera (one endemic). Other than these, the terrestrial fauna is restricted to microarthropods, meiofaunal Nema-

Corresponding author. Tel.: +44 1223 221588; fax: +44 1223 221259.

E-mail address: [email protected] (P. Convey). 0038-0717/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.soilbio.2005.12.007

toda, Tardigrada and Rotifera, and various protozoan groups. Even with the limited current level of knowledge of the Antarctic nematode fauna, two features are particularly distinctive in a biogeographical context (Table 1). First, most members of the known Antarctic nematode fauna appear to be found nowhere else on Earth. Second, there is no overlap at species level between the maritime and continental Antarctic faunas (biogeographical zones following Smith (1984); taxonomy following the most recent and authoritative treatment of the Antarctic nematofauna (Andra´ssy, 1998)), a pattern which mirrors that found in two other major Antarctic terrestrial faunal groups, the Collembola (where a single species is shared, Greenslade,

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Table 1 Nematodes currently recognised from the maritime (M) and continental (C) Antarctic biogeographical zones Species and authority

M

Eumonhystera vulgaris (de Man, 1880) Andra´ssy, 1981 Geomonhystera antarcticola Andra´ssy, 1998 Geomonhystera villosa (Bu¨tschli, 1873) Andra´ssy, 1981 Plectus antarcticus de Man, 1904 P. belgicae de Man, 1904 P. frigophilus Kirjanova, 1958 P. insolens Andra´ssy, 1998 P. meridianus Andra´ssy, 1998 P. murrayi Yeates, 1970 P. tolerans Andra´ssy, 1998 Ceratoplectus armatus (Bu¨tschli, 1873) Andra´ssy, 1984 Chiloplectus masleni Bostro¨m, 1997 Chiloplacoides antarcticus Heyns, 1994 Teratocephalus pseudolirellus Maslen, 1979 T. rugosus Maslen, 1979 T. tilbrooki Maslen, 1979 Rhabditis krylovi Tsalolikhin, 1989 Cuticularia firmata Andra´ssy, 1998 Aphelenchoides haguei Maslen, 1979 A. helicosoma Maslen, 1979 A. vaughani Maslen, 1979 Antarctenchus hooperi Spaull, 1972 Scottnema lindsayae Timm, 1971 Panagrolaimus davidi Timm, 1971 Panagrolaimus magnivulvatus Bostro¨m 1995 Ditylenchus parcevivens Andra´ssy, 1998 Rotylenchus capensis van den Berg & Harris, 1996 Paramphidelus antarcticus Tsalolikhin, 1981 Coomansus gerlachei (de Man, 1904) Jairajpuri and Khan, 1977 Eutobrilus antarcticus Tsalolikhin, 1981 Mesodorylaimus imperator Loof, 1975 Calcaridorylaimus signatus (Loof, 1975) Andra´ssy, 1986 Eudorylaimus antarcticus (Steiner, 1916) Yeates, 1970 E. coniceps Loof, 1975 E. glacialis Andra´ssy, 1998 E. nudicaudatus Heyns, 1994 E. pseudocarteri Loof, 1975 E. shirasei Kito et al., 1996 E. spaulli Loof, 1975 E. verrucosus Loof, 1975 Amblydorylaimus isokaryon (Loof, 1975) Andra´ssy, 1998 Enchodelus signyensis Loof, 1975 Rhyssocolpus paradoxus (Loof, 1975) Andra´ssy, 1986

x

Total species recognised

C

x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x x X x x x x x 29

14

1995) and free-living Acari (Pugh, 1993). These features have fundamental implications, and are directly relevant to ideas proposed in this paper linking present-day biogeography and evolutionary history of Antarctic terrestrial faunas and ecosystems. Until the study described here, no detailed zoological survey work focussing on microinvertebrate groups had been completed at maritime Antarctic locations south of Marguerite Bay (Fig. 1) and, hence, nothing was known of the fauna inhabiting the large boundary region linking the maritime and continental Antarctic (i.e. the entire region south of Marguerite Bay,

westwards to the Ross Sea (ca. 1501W) and eastwards to Dronning Maud Land (ca. 0151W). Nematodes are an important, if often ignored, element of the soil fauna across the world. However, in the simple, low diversity, terrestrial ecosystems of the Antarctic, they assume an importance and dominance rarely seen elsewhere. Thus, even in the Antarctic, as environmental conditions become more extreme, groups such as the microarthropods reach their environmental tolerance limits, leading to communities containing only nematodes, tardigrades, rotifers and protozoans. Those from the Ross Sea Dry Valley region of the Antarctic continent have been described as the simplest faunal communities on Earth (Freckman and Virginia, 1997). More recently, even simpler communities lacking nematodes have been described from an entire inland continental Antarctic region (Convey and McInnes, 2005) and from specific inland nunataks (Sohlenius and Bostro¨m, 2005). Both nematodes and tardigrades possess a range of ecophysiological abilities giving them exceptional tolerance of cold and desiccation stresses, in some cases allowing full development of anhydrobiosis (Wharton, 1995, 2002). These abilities are likely to underlie their exceptional success in extreme Antarctic environments, while also being implicated as providing potentially very effective dispersal mechanisms, relative to other terrestrial invertebrate groups (Convey, 1996). The first Antarctic nematodes (Plectus antarcticus, P. belgicae and Mononchus gerlachei) were collected by the 1897–1899 ‘Belgica’ Expedition and subsequently described by de Man (1904). These were all from the western Antarctic Peninsula and associated islands, in the area now described as the maritime Antarctic biogeographical zone. The first nematode from the continental zone (Eudorylaimus antarcticus) was described by Steiner (1916), and it was then some 42 years before another new nematode, P. frigophilus, was described (Kirjanova, 1958). From the 1970s there was an intensification of research activities in Antarctica, with a corresponding increase in the number of new species formally described from both zones, including Yeates (1970) [1 new species], Timm (1971) [2], Spaull (1972, 1981) [2], Loof (1975) [9], Maslen (1979a) [6], Tsalolikhin (1981, 1989) [3], Heyns (1994) [2], Bostro¨m (1995, 1997) [2], Kito et al. (1996) [1], van den Berg and Heyns (1974) [1], and Andra´ssy (1998) [7]. Finally, as part of a South African study, van den Berg and Harris (1996) listed a new continental Antarctic record of a South African species (Rotylenchus capensis van den Berg and Heyns, 1974), of which single specimens were reported from separate nunataks in Dronning Maud Land (see below). As well as describing several new species, Andra´ssy’s (1998) thorough review of the known Antarctic fauna also reversed the synonymy proposed by Timm (1971) between P. antarcticus de Man, 1904 and P. murrayi Yeates, 1970. While this does lead to some difficulty in reconciling published records of the different species, we have elected to follow the taxonomy of Andra´ssy, being

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Fig. 1. Map and inset enlargements of the Antarctic Peninsula, indicating the sampling locations described in the text.

both most up-to-date and minimising the likelihood of perpetuating errors created through initial conflicting or poor description. Resolution of these taxonomic issues is outwith the scope of this paper, requiring both fresh material obtained across the regions under consideration and, ideally, the application of a complementary molecular phylogenetic approach. Although, clearly, much basic survey and taxonomic description remains to be done, 29 formally described terrestrial and limno-terrestrial nematode species have so far been recorded from the maritime Antarctic and 14 species from the continental Antarctic (Andra´ssy, 1998; Table 1). The literature (e.g. Spaull, 1973; Maslen, 1979b) also contains further reference to separable taxa identified to genus, but without further opportunity for formal description. While this is not an ideal situation, it remains a pragmatic necessity within ecological studies, and is a practice we have followed in this study. Three cosmopolitan taxa have been reported from the Antarctic (Eumonhystera vulgaris, Geomonhystera villosa,

Ceratoplectus armatus), but these reports are not accompanied by a description of the material on which the identification was based, and are best considered as ‘not proven’. Coomansus gerlachei and Rotylenchus capensis have been reported on the basis of formally described material. C. gerlachei was considered to be endemic to the maritime Antarctic until reported from the Arctic by Mulvey (1978), although Andra´ssy (1998) subsequently reviewed this taxon and concluded that C. gerlachei is solely an Antarctic species. Rotylenchus capensis, as mentioned above, is a South African species more recently described from Antarctica by South African workers. Andra´ssy (1998, pp. 164–165) highlights difficulties in interpreting the presence of a tylenchid at an inland continental Antarctic site largely devoid of macroscopic vegetation, concluding that the specimens found may not represent ‘‘true’’ R. capensis. Such debates will, as above, only be resolved through the application of molecular phylogenetic techniques, and require collection of fresh material. However, with several authors recording

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representatives of nematode genera at continental Antarctic locations that are generally thought to be plant feeding elsewhere (Yeates, 1979; Sohlenius et al., 2004; Sohlenius and Bostro¨m, 2005), important questions clearly remain to be addressed in understanding the biology of such species in this region. More generally, it is also the case that very few detailed autecological data are available relating to the field biology, life cycle and trophic interactions of any Antarctic nematodes and, hence, any discussions relating to these aspects of their biology are largely speculative. This paper reports the results of nematological surveys of several locations in the region of the southern Antarctic Peninsula, much of which has not been studied previously. This region includes the boundary between the maritime and continental Antarctic biogeographical zones. The primary aims of this study were, therefore, to document nematode diversity in this region, to use the data obtained to specify more accurately the boundary between the two biogeographical zones, and to refine currently accepted patterns of nematode diversity in the Antarctic. 2. Methods 2.1. Study sites The study examined material from a range of sites from northern Marguerite Bay southwards to Alexander Island and thence Ellsworth Land, and westwards to Charcot

Island (Fig. 1, Table 2). The general biology and geology of the sites in northern Marguerite Bay are described in detail by Convey and Smith (1997) and Dewar (1970), respectively. Terrestrial communities are dominated by closed or open cryptogamic (bryophyte, lichen) vegetation typical of the maritime Antarctic, with faunas consisting of generally detritivorous microarthropods and meiofaunal groups (Block, 1984; Smith, 1984; Convey, 2001). Microbial groups are also well represented, with extensive development of foliose algae and cyanobacterial mats. Heywood (1977), Smith (1988) and Convey and Smith (1997) describe the biology of ice-free ablation areas of south-eastern Alexander Island, with geological, geomorphological and glaciological information given by Moncrieff and Kelly (1993), Sugden and Clapperton (1981), Clapperton and Sugden (1982, 1983), Meiklejohn (1994), Crame and Howlett (1988) and Taylor et al. (1979). These habitats are regarded as intermediate between those typical of the continental and maritime zones (Smith, 1984), particularly in terms of the degree of water stress experienced. Macroscopic vegetation and arthropod groups are much more restricted in their distributions, with microbial producers and meiofaunal groups being dominant in their representation. Convey et al. (2000) detail the unusual plant, lichen and arthropod communities found on the very limited ice-free coastal nunataks of Charcot Island. The unusual composition of these communities, for instance lacking the major arthropod group of Collembola, is most

Table 2 Study site location data (see also Fig. 1) and samples examined Site

Date sampled

Samples examined

Habitats sampled

Altitude range (m)

Northern Marguerite Bay, Adelaide Island Rothera Point

1997–1998

2

0–20

Reptile Ridge Stork Ridge Killingbeck Island Anchorage Island

1997–1998 1997–1998 1997–1998 1997–1998

2 4 1 9

Le´onie Island

1997–1998

3

Moss, lichen, soil, microbial mat Moss, lichen, soil Moss, lichen Moss, lichen, soil Moss, grass, lichen, soil, microbial mat, freshwater Moss, grass, lichen, soil, microbial mat, freshwater

Central Marguerite Bay Alamode Island

2000–2001

9

Moss

0–20

North of Alexander Island Rhyolite Island Charcot Island

2000–2001 1997–1999

1 3, 17

Moss, grass Moss, lichen, soil

0–10 50–100

South-eastern Alexander Island Ablation Valley

2000–2001

52

20–750

Mars Oasis

1998–2001

48, 29

Coal Nunatak

1998–1999

11

Moss, lichen, soil, microbial mat Moss, lichen, soil, microbial mat, freshwater Moss (limited), lichen, soil

Ellsworth Land Hauberg, Behrendt, Merrick, Sweeney Mountains, Sky Hi, Quilty, Haag Nunatak

2000–2001

93

Moss (very limited), lichen, microbial mat, soil

300 500–600 0–15 0–30 0–50

20–600 600–700 500–1500

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likely attributable to a stochastic consequence of the extreme isolation and recent exposure of the nunataks. The remaining sites have received little or no previous biological study. Rhyolite Island, in the mouth of George VI Sound, is the most southerly known location in Antarctica where the grass Deschampsia antarctica occurs. The inland nunatak groups sampled in Ellsworth Land are described by Convey and McInnes (2005). Here, terrestrial habitats are extremely limited in extent and often barren to the naked eye. With the exception of very occasional occurrence of tiny areas of moss, vegetation is limited to crustose and very limited patches of foliose lichens. The limited soils present in rock crevices and frost boils are sometimes colonised by visible fungal hyphal and algal mats. 2.2. Sample collection and extraction Due to varying levels of accessibility and logistical constraints applying to each site, the intensity of sampling differed at each. The most detailed work was possible at Mars and Ares Oases (south-eastern Alexander Island) and in the vicinity of Rothera Research Station (Adelaide Island), which are long-term terrestrial study sites operated by the British Antarctic Survey (BAS) (Convey and Smith, 1997; Convey and Wynn–Williams, 2002; Convey, 2003a). Material from sites in Ellsworth Land (Convey and McInnes, 2005) and from Ablation Valley (Alexander Island) was obtained during single field campaigns of 2–4 weeks, with individual sampling locations being visited once within this period. Finally, some sites could only be visited for short periods of up to several hours, from opportunistic boat (Alamode, Rhyolite Islands) or aeroplane landings (Charcot Island, three separate brief visits; Convey et al., 2000). The range of habitats available at each location varied widely, particularly in the extent and type of soil or vegetation (Table 2), factors that obviously constrained the amount of substrata that could be collected for extraction. Samples (typically 10–100 g fresh mass) were obtained from as wide a range of habitats as practicable, where they were encountered, including mosses, lichens, microbial (fungal, cyanobacterial, algal) mats, soils, waterlogged and freshwater habitats. These were stored separately in sealed plastic bags at local field ambient temperatures until it was possible to return them to refrigerated facilities at the BAS Rothera Research Station. This period varied between minutes to hours (sites in the vicinity of the research station), hours to days (Mars and Ares Oases, Charcot Island), up to 1–3 weeks (Ellsworth Land), as a function of the field operational support available. On return to Rothera Research Station, each sample was subjected to a modified Baermann extraction (Convey and McInnes, 2005), being wrapped in tissue paper and submerged in a water-filled funnel for 24–36 h at room temperature before extracted fauna were run off in ca. 5 ml of water. Nematodes and other meiofauna were killed and preserved

3145

following Hooper (1986a, b), by heating briefly to 50–60 1C and then addition of an equal volume of 10% formalin. On return of preserved material to the United Kingdom, samples were examined initially on sorting trays under a binocular microscope, with reference to keys and taxonomic details given by Andra´ssy (1998) and Maslen (1979a, b), under the expectation that the species obtained would be attributable to the known fauna of the maritime Antarctic. As it quickly became clear that this assumption was simplistic, samples were subjected to more detailed examination using a Zeiss Axiovert inverted microscope, and more difficult specimens were examined on temporary slide mounts using Wild M11 or Nikon Optiphot microscopes, with wider reference to the full taxonomic literature given above. However, it remains the case that the scope of this study has not permitted full critical taxonomic evaluation and description of the apparently undescribed taxa found and hence the conclusions drawn must remain preliminary. 3. Results Nematodes were present in extractions from all sites examined with the clear exception of those from Ellsworth Land. As almost 140 extractions have been completed across all available habitats from the latter region (with detailed analysis presented by Convey and McInnes, 2005), demonstrating the presence of a range of tardigrades and a small number of rotifers, our data strongly imply that nematodes are not a component of the fauna here. Distributional data obtained in the current survey are presented in Table 3. Across all study sites, a total of 42 distinct taxa were obtained, of which 21 (50%) cannot be assigned to described species (Table 4). The nematode fauna obtained from the more northerly sites (northern Marguerite Bay, Adelaide Island) conforms largely (16/17 taxa) to that already known from the wider maritime Antarctic (Table 3), providing some degree of confidence that this fauna is reasonably well documented. This material contained no undescribed taxa, but did include a single specimen morphologically similar to the continental species P. murrayi (note taxonomic comments above). All these sites are located within 10 km of Rothera Point. Four of the six sites examined are islands and/or coastal low altitude, and these shared elements of a broadly similar fauna with differences in species richness most likely explained by sampling intensity. The final two sites were montane and either lacked faunal elements common to the coastal sites (Reptile Ridge, ca. 300 m asl, also adjacent to the coast) or included a largely distinctive set of maritime Antarctic species (Stork Ridge, ca. 600 m asl). The different species richness at the latter two sites may be better linked with habitat availability, but no further comment can be made here in the absence of more detailed site-specific studies. Specimens morphologically very close to two continental Antarctic species (described here as P. cfr. murrayi and

Mesodorylaimus imperator M. (C.) signatus Mesodorylaimus sp. 1

+ + + + + +

Monhystera sp. A Monhystera sp. B Rhabdolaimus sp. A Plectus antarcticus P. tolerans P. belgicae P. cfr. murrayi P. cfr. frigophilus Plectus sp. 1 Plectus sp. 2 Plectus sp. 3 Plectus sp. (uncertain) Teratocephalus tilbrooki T. pseudolirellus T. rugosus Panagrolaimus sp. A Aphelenchoides haguei A. helicosoma A. vaughani Ditylenchus sp. A Tylenchus sp. A Paramphidelus sp. A Coomansus gerlachei

+ +

+

+ + + + + + + + +

M

Taxon

+? +?

C

Stork Ridge

+

+

+

+

+

+

+ +

+

+ +

+ + + +

Anchorage I.

North of Alexander Island

+ +

+

+ +

+

+ + +

+ +

+

+

+ + +

+ +

+ + + + +

+ + +

+ +

+

+

+

+ + +

+ +

+ +

+ +

+

+

+

+ +

+ +

+

+

Ablation Coal Valley Nunatak

South-east Alexander Island

Leonie I. Alamode Rhyolite Charcot Mars I. I. I. Oasis

Northern Marguerite Bay

Rothera KillingPoint beck I.

+

Reptile Ridge

Adelaide Island

Maslen, 1979a Maslen, 1979a Maslen, 1979a de Man, 1904 Andra´ssy, 1998 de Man, 1904 Yeates, 1970 Kirjanova, 1958 This study This study This study This study Maslen, 1979b + Maslen, 1979b Maslen, 1979b Maslen, 1979a Maslen, 1979b + + Maslen, 1979b Maslen, 1979b Maslen, 1979a Maslen, 1979a + This study de Man, 1904; Jairajpuri & Khan, 1977 Loof, 1975 Loof, 1975; Andra´ssy, 1986a This study

Main previous records

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Table 3 Nematode taxa recorded from locations along the west coast of the Antarctic Peninsula (see Section 2 and Fig. 1 for further location details)

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+

3

+

2

+

+

2

+ + +

+

0 0

No. of new/unrecorded taxa

% of new/unrecorded taxa

0

0 0

0 0

0 0

0

11

0

0

11

25

2

8

0

0

17

2

12

+

36

9

25

+

36

5

14

+

+

+

75

3

4

+

+

The wider distribution of each taxon (other than those erected by this study) is summarised as M (maritime Antarctic) or C (continental Antarctic), and the primary literature source given for described and previously recognised but currently undescribed taxa.

6

5

+

+

+ + +

+

This study This study This study This study This study This study This study Loof, 1975

+

+

+

+ + +

This study

Loof, 1975; Andra´ssy, 1986b

+

+

+

1975 1975 1975 1975 1975

Loof, Loof, Loof, Loof, Loof,

+ +

+

+

Maslen in Heywood, 1977

This study Maslen in Heywood, 1977

Taxa per location

Mesodorylaimus sp. 2 Mesodorylaimus sp. 3 + ( ¼ Mesodorylaimus sp. A of Maslen, 1979a, b) Mesodorylaimus sp. 4 (close + to Mesodorylaimus sp. B of Maslen, 1979a, b) Eudorylaimus coniceps + E. spaulli + E. pseudocarteri + E. verrucosus + E. (Amblydorylaimus) + isokaryon E. (Rhyssocolpus) + paradoxus Eudorylaimus sp. H (close to E. coniceps) Eudorylaimus sp. J Eudorylaimus sp. K Eudorylaimus sp. L Eudorylaimus sp. M Eudorylaimus sp. N Eudorylaimus sp. P Eudorylaimus spp. indet. Enchodelus signyensis +

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Table 4 Summary of nematode species richness within broad subsections of the transect studied, also indicating the proportion of taxa found referable to species currently undescribed Location

Total number of taxa present

% undescribed

Adelaide Island and northern Marguerite Bay islands (Ryder Bay) Alamode Island (central Marguerite Bay) Islands north of Alexander Island in southern Marguerite Bay (Charcot, Rhyolite Islands) South-east Alexander Island

18

0%

All sites

8

25.0%

12

14.3%

32

39.5%

42

50

P. cfr. frigophilus) were also present in the faunas of Alamode Island (central Marguerite Bay) and Charcot Island (eastern Bellingshausen Sea), with both also being widespread at two or all three of the sites examined on south-eastern Alexander Island (Table 3). Although keying to these two species on the basis of morphological features, full confirmation requires further material and systematic work (in progress), preferably backed by molecular analyses. Note also that these two continental taxa have previously been suggested as an example of speciation through polyploidy (Yeates, 1986; with P. murrayi then described as the synonymised P. antarcticus, after Timm, 1971). If these identifications can be confirmed, they would form the first records of species previously known only from the continental Antarctic at sites within the maritime Antarctic. In addition to Alexander Island, Alamode and Charcot Islands also included new undescribed taxa in their nematode fauna. However, the Alexander Island fauna was most distinctive in two respects. First, almost 40% of the 32 taxa recorded there were not referable to described species. Second, including these undescribed taxa, the species richness of the nematode community on southeastern Alexander Island is considerably greater than that known from the relatively well studied northern Marguerite Bay, and exceeds the described diversity of the entire maritime Antarctic zone (cf. Table 1). Even allowing for the possibility that critical taxonomic analysis might not support all of the separate taxa recognised here, the high proportion of undescribed taxa remains striking. 4. Discussion Terrestrial habitats of the maritime Antarctic are, typically, low altitude and coastal in nature, and are currently generally thought to be of very recent origin, exposed as glaciers retreated after the Pleistocene. Radiocarbon dating of the deepest peat banks found in the maritime Antarctic, in the South Orkney Islands and South Shetland Islands, suggests maximum ages of 5–6000 years

(Fenton, 1982; Bjo¨rk et al., 1991). Regional glacial and ice sheet reconstructions indicate a similar age (Sugden and Clapperton, 1977; Clapperton and Sugden, 1982, 1988; Lorius et al., 1985; Smith, 1990; Pudsey and Evans, 2001). Taken together, these studies are generally accepted as indicating the absence of exposed coastal ground at glacial maxima as, even allowing for lower sea level, coastal ice sheets often extended across the continental shelf to the point of shelf drop-off (Larter and Vanneste, 1995; O´ Cofaigh et al., 2002; COHIMAR/SEDANO Scientific Party, 2003). The situation is more complex in continental Antarctica. It is likely that the majority of coastal locations, which currently have analogous morphology and biology to those of the maritime zone, have a similar history of Pleistocene glaciation. However, recently, it has become clear that at least one coastal location remained partly clear of permanent ice cover throughout the most recent glacial maximum, and perhaps for as long as 50,000 years (Hodgson et al., 2001). It is also clear that parts of the unique ablation areas of the Victoria Land Dry Valleys and Pensacola Mountains have remained ice free for at least three to four million years. Finally, the continental Antarctic includes a range of climatically extreme and geographically isolated inland nunataks, some of which are likely to have remained exposed throughout the progressive glaciation of Antarctica over the last 25–30 million years. In apparent contrast with the implications of geomorphological and glacialogical reconstructions, recent studies of terrestrial invertebrate faunas of both maritime and continental Antarctica have concluded that these include remnants of an ancient regional fauna (Greenslade, 1995; Marshall and Pugh, 1996; McInnes and Pugh, 1998; Pugh and Convey, 2000; Stevens and Hogg, 2003; Convey and McInnes, 2005). In the continental Antarctic some of the species concerned are currently montane, and hence could have occupied the limited nunatak refugia even at glacial maxima. However, this hypothesis does not satisfactorily explain the maritime fauna, as most species are restricted to low altitude coastal localities, while the zone does not appear to have an obligate montane arthropod fauna. The distinctive, isolated, nature of the Antarctic nematode fauna, both in terms of overall endemicity to the region and the lack of species-level overlap between maritime and continental zones, has been recognised (Andra´ssy, 1998). However, the wider phylogeographic implications have not been fully grasped in the context of understanding the evolutionary processes leading to the contemporary Antarctic fauna and, particularly, the implications carried for reconstructing glacial history within the continent. When considering the implications of contemporary biodiversity patterns within the Antarctic, particularly in relation to species with coastal as distinct from inland nunatak distributions, it is clear that a new hypothesis is required, viz. that a coastal fauna has been able to survive in situ at currently unknown refuge sites in

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the maritime Antarctic at least throughout the Quaternary glacial episodes (Convey, 2003b), and that this factor requires taking into account when preparing glacial reconstructions. Species richness patterns obtained across the latitudinal gradient covered by this study provide significant new support to this hypothesis. The northern locations sampled here (northern Marguerite Bay) hosted a fauna almost entirely consistent with that known already from the maritime Antarctic, giving encouragement that nematode diversity in this zone is reasonably well described. Species richness appears to decrease at locations in central and southern Marguerite Bay and the eastern Bellingshausen Sea although this conclusion may be confounded by limited sampling intensity. However, even allowing for the different sampling intensities practicable at some of the study locations, it is clear that the widely assumed pattern of decreasing diversity with increasing latitude (and, hence, environmental severity) found in other macroscopic faunal and floral groups (Convey and Smith,1997; Convey, 2001; Clarke, 2003) is not supported when the nematode fauna of Alexander Island is considered. Rather, the reverse is found, with species richness being almost 80% greater than that found in northern Marguerite Bay, and 10% greater than currently known from the entire maritime Antarctic. This difference in species richness is accounted for by the high (almost 40%) proportion of distinct undescribed taxa present on Alexander Island. The only other element of the fauna of Alexander Island to have received detailed study is the arthropods (Convey and Smith, 1997). These again include largely known maritime Antarctic species, but also a single endemic springtail (of two Collembola present). However, the overall very low diversity of arthropods found with increasing latitude renders this group less suitable than the nematodes for the elucidation of biogeographical patterns in this region. It is also known that currently undescribed new species of tardigrade are present (S. McInnes, unpubl. data). We infer that the level of endemicity and overall species richness present in the Alexander Island nematode fauna are such that they cannot be explained simply through recent colonisation from the north (maritime Antarctic). The complete lack of nematodes in the fauna of Ellsworth Land (Convey and McInnes, 2005) argues against colonisation from the south (from the continental Antarctic), and also that this region does not include nematode species that are endemic to inland nunatak habitats (such as those reported from Dronning Maud Land by Sohlenius et al., 2004). The presence of two possibly continental species, if confirmed, would support colonisation from the continental coastline, associated with the general westerly airflow in the region. Indeed, Alexander Island itself could also be considered as a candidate source for many of the species now found at locations around Marguerite Bay. The colonisation routes available to permit movement of biota into or between the sites considered in this study, either on a local scale by already indigenous biota, or on a

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much larger intercontinental scale for currently nonresident taxa, appear to be particularly limited. Essentially, two routes are available, through the transport of life stages possessing suitable resistance adaptations through the air column, or through accidental transport associated with other animals. In recent years, a third route has become available to biota, through inadvertent transport associated with human activity (Frenot et al., 2005). However, it is important to note that no nematodes have yet been recorded or implicated as arriving in an Antarctic location via any of these routes, although relatively few detailed studies have been attempted. It is also the case that the more southern locations (Ellsworth Land, Mars and Ares Oases) examined in the current study have no resident bird population and record only occasional and transient individuals. That these routes are viable for at least some biota is demonstrated by aerobiological studies in the northern maritime Antarctic and at a site on the continental Antarctic coastline, which have demonstrated aerial transfer of a range of microbiota and moss and lichen propagules (Signy Island—Marshall, 1996; Davis Station—Downs, 2003), and earlier studies indicating that microbiota (algae) can be transferred around the Antarctic on birds’ feet (Schlichting et al., 1978). Thus, we propose that Alexander Island is a good candidate to include the locations of long-term biological refuge sites that have survived throughout Antarctic glacial cycles and, in the context of wider patterns of Antarctic biogeography, it may also be described as a biodiversity hotspot or a centre of endemism. Further support for this proposal will require the use of complementary approaches, such as ‘molecular clock’ techniques (although these are limited by the need for independent dating of species separation events) and phylogeographical reconstruction through molecular divergence (cf. Allegrucci et al., 2005), as well as being linked with geological and geomorphological dating of potential refuge areas, including any that lie below current sea level. Acknowledgements This study would not have been possible without support from the British Antarctic Survey (BAS) biological field assistants Paul Geissler and Mairi Nicolson, logistical support from the BAS Operations section at Rothera (particularly Rod Arnold, field general assistants Rachel Duncan, Maggie Annat and Tim Blakemore, and the skills of the BAS Air Unit). Additional substrata collections were provided from Ablation Valley (Colin Harris), Ellsworth Land (Morag Hunter) and islands in southern Marguerite Bay (Jerome Poncet/National Geographic). We thank BAS for analytical support to NRM. Fig. 1 was prepared by Peter Fretwell. This paper forms part of the BAS project ‘Biological Responses to Environmental Stress in Antarctica’, contributes to the SCAR programme ‘Regional Sensitivity to Climate Change in Antarctica’, and is part of a special issue resulting from NSF OPP-0406141 support

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to D.H. Wall for the Victoria Land Synthesis workshop. Dr P. Pugh and two anonymous referees are thanked for constructive comments on earlier versions. References Allegrucci, G., Carchini, G., Todisco, V., Convey, P., Sbordoni, V., 2005. A molecular phylogeny of Antarctic Chironomidae and its implications for biogeographical history. Polar Biology. Andra´ssy, I., 1986a. The genus Mesodorylaimus Andra´ssy, 1959 and its relatives (Nematoda, Dorylaimidae). Acta Zoologica Hungarica 32, 207–261. Andra´ssy, I., 1986b. The genus Eudorylaimus Andra´ssy, 1959 and the present status of its species (Nematoda: Qudsianematidae). Opuscula Zoologica, Budapest XXII XXII, 3–42. Andra´ssy, I., 1998. Nematodes in the sixth continent. Journal of Nematode Systematics and Morphology 1, 107–186. van den Berg, E., Harris, J.M., 1996. Rotylenchus capensis Van den Berg and Heyns (Tylenchida: Hoplolaimidae) in soils of isolated nunataks in western Dronning Maud Land, Antarctica. African Plant Protection 2, 19–24. van den Berg, E., Heyns, J., 1974. South African Hoplolaiminae 3. The genus Rotylenchus Filipjev, 1936. Phytophylactica 6, 165–184. Bjo¨rk, S., Malmer, N., Hjort, C., Sandgren, P., Ingo´lfsson, O., Walle´n, B., Smith, R.I.L., Jo´nsson, B.L., 1991. Stratigraphic and palaeoclimatic studies of a 5500-year-old moss bank on Elephant Island, Antarctica. Arctic and Alpine Research 23, 361–374. Block, W., 1984. Terrestrial microbiology, invertebrates and ecosystems. In: Laws, R.M. (Ed.), Antarctic Ecology. Academic Press, London, pp. 163–236. Bostro¨m, S., 1995. Populations of Plectus acuminatus Bastian, 1865 and Panagrolaimus magnivulvatus n. sp. (Nematoda) from nunataks in Dronning Maud Land, East Antarctica. Fundamental and Applied Nematology 18, 25–34. Bostro¨m, S., 1997. Chiloplectus masleni sp. nov. and variability in populations of Plectus acuminatus Bastian, 1865 (Nematoda:Plectidae) from the nunatak Basen, Vestfjella, Dronning Maud Land, East Antarctica. Polar Biology 17, 74–80. Clapperton, C.M., Sugden, D.E., 1982. Late quaternary glacial history of George VI Sound area, West Antarctica. Quaternary Research 18, 243–267. Clapperton, C.M., Sugden, D.E., 1983. Geomorphology of the Ablation Point massif, Alexander Island, Antarctica. Boreas 12, 125–135. Clapperton, C.M., Sugden, D.E., 1988. Holocene glacier fluctuations in South America and Antarctica. Quaternary Science Reviews 7, 185–198. Clarke, A., 2003. Evolution, adaptation and diversity: global ecology in an Antarctic context. In: Huiskes, A.H.L., Gieskes, W.W.C., Rozema, J., Schorno, R.H.L., van der Vries, S.M., Wolff, W.J. (Eds.), Antarctic Biology in a Global Context. Backhuys, Leiden, pp. 3–17. COHIMAR/SEDANO Scientific Party, 2003. Uncovering the footprint of former ice streams off Antarctica. Eos, Transactions, American Geophysical Union 84 (11) 97, 102–103. Convey, P., 1996. The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biological Reviews 71, 191–225. Convey, P., 2001. Antarctic ecosystems. In: Levin, S.A. (Ed.), Encyclopedia of Biodiversity, Vol. 1. Academic Press, San Diego, pp. 171–184. Convey, P., 2003a. Soil faunal community response to environmental manipulation on Alexander Island, southern maritime Antarctic. In: Huiskes, A.H.L., Gieskes, W.W.C., Rozema, J., Schorno, R.H.L., van der Vries, S.M., Wolff, W.J. (Eds.), Antarctic Biology in a Global Context. Backhuys, Leiden, pp. 74–78. Convey, P., 2003b. Maritime Antarctic climate change: signals from terrestrial biology. In: Domack, E., Burnett, A., Leventer, A., Convey, P., Kirby, M., Bindschadler, R. (Eds.), Antarctic Peninsula Climate Variability: Historical and Palaeoenvironmental Perspectives. Antarc-

tic Research Series, Vol. 79. American Geophysical Union, pp. 145–158. Convey, P., McInnes, S.J., 2005. Exceptional, tardigrade dominated, ecosystems from Ellsworth Land, Antarctica. Ecology 86, 519–527. Convey, P., Smith, R.I.L., 1997. The terrestrial arthropod fauna and its habitats in northern Marguerite Bay and Alexander Island, maritime Antarctic. Antarctic Science 9, 12–26. Convey, P., Wynn-Williams, D.D., 2002. Antarctic soil nematode response to artificial environmental manipulation. European Journal of Soil Biology 38, 255–259. Convey, P., Smith, R.I.L., Peat, H.J., Pugh, P.J.A., 2000. The terrestrial biota of Charcot Island, eastern Bellingshausen Sea, Antarctica an example of extreme isolation. Antarctic Science 12, 406–413. Crame, J.A., Howlett, P.J., 1988. Late Jurassic and early Cretaceous biostratigraphy of the Fossil Bluff Formation, Alexander Island. British Antarctic Survey Bulletin 78, 1–35. Dewar, G.J., 1970. The geology of Adelaide Island. British Antarctic Survey Scientific Reports, No. 57, 66pp. Downs, J., 2003. Factors affecting the introduction and distribution of fungi in the Vestfold Hills, Antarctica. Ph.D. Thesis, University of Nottingham. Fenton, J.H.C., 1982. The rate of peat accumulation in Antarctic moss banks. Journal of Ecology 68, 211–228. Freckman, D.W., Virginia, R.A., 1997. Low-diversity Antarctic soil nematode communities: Distribution and response to disturbance. Ecology 78, 363–369. Frenot, Y., Chown, S.L., Whinam, J., Selkirk, P., Convey, P., Skotnicki, M., Bergstrom, D., 2005. Biological invasions in the Antarctic: extent, impacts and implications. Biological Reviews 80, 45–72. Greenslade, P., 1995. Collembola from the Scotia Arc and Antarctic Peninsula including descriptions of two new species and notes on biogeography. Polskie Pismo Entomologiczne 64, 305–319. Heyns, J., 1994. Chiloplacoides antarcticus n. gen., n. sp. from western Dronning Maud Land, Antarctica (Nematoda: Cephalobidae). Fundamental and Applied Nematology 17, 333–338. Heywood, R.B., 1977. A limnological survey of the Ablation Point area, Alexander Island, Antarctica. Philosophical Transactions of the Royal Society of London B 279, 39–54. Hodgson, D.A., Noon, P.E., Vyverman, W., Bryant, C.L., Gore, D.B., Appleby, P., Gilmour, M., Verleyen, E., Sabbe, K., Jones, V.J., EllisEvans, J.C., Wood, P.B., 2001. Were the Larsemann Hills ice-free through the last glacial maximum? Antarctic Science 13, 440–454. Hooper, D.J., 1986a. Extraction of free-living stages from soil. In: Southey, J.F. (Ed.), Laboratory Methods for Work with Plant and Soil Nematodes. HMSO, London, pp. 5–30. Hooper, D.J., 1986b. Handling, fixing, staining and mounting nematodes. In: Southey, J.F. (Ed.), Laboratory Methods for Work with Plant and Soil Nematodes. HMSO, London, pp. 59–80. Jairajpuri, M.S., Khan, W.U., 1977. Studies on Mononchida of India IX. Further division of the genus Clarkus Jairajpuri, 1970 with the proposal of Coomansus n. gen. (Family Mononchidae Chitwood, 1937) and descriptions of two new species. Nematologica 23, 89–96. Kirjanova, E.S., 1958. Antarctic representatives of freshwater nematodes of the genus Plectus Bastian (Nematoda, Plectidae). Informatsionnyj Bulleten Sovetskoj Antarticheskoj Ekspeditsii, Leningrad 3, 101–103 (in Russian). Kito, K., Shishida, Y., Ohyama, Y., 1996. A new species of the genus Eudorylaimus Andrassy, 1959 (Nematoda: Qudsianematidae) from East Antarctica. Polar Biology 16, 163–169. Larter, R.D., Vanneste, L.E., 1995. Relict subglacial deltas on the Antarctic Peninsula outer shelf. Geology 23, 33–36. Loof, P.A.A., 1975. Dorylaimoidea from some sub-Antarctic islands. Nematologica 21, 219–255. Lorius, C., Jouzel, J., Ritz, C., Merlivat, L., Barkov, N.I., 1985. A 150,000-year climate record from Antarctic ice. Nature 316, 591–596. de Man, J.G., 1904. Ne´matodes libres. Expe´dition Antarctique Belge. Re´sultats du voyage du S.Y. Belgica, 1897–1899. Rapports Scientifiques. Zoologie 8, 1–51.

ARTICLE IN PRESS N.R. Maslen, P. Convey / Soil Biology & Biochemistry 38 (2006) 3141–3151 Marshall, D.J., Pugh, P.J.A., 1996. Origin of the inland Acari of continental Antarctica, with particular reference to Dronning Maud Land. Zoological Journal of the Linnean Society 118, 101–118. Marshall, W.A., 1996. Biological particles over Antarctica. Nature 383, 680. Maslen, N.R., 1979a. Six new nematode species from the maritime Antarctic. Nematologica 25, 288–308. Maslen, N.R., 1979b. Additions to the nematode fauna of the Antarctic region with keys to taxa. British Antarctic Survey Bulletin 49, 207–230. McInnes, S.J., Pugh, P.J.A., 1998. Biogeography of limno-terrestrial Tardigrada, with particular reference to the Antarctic fauna. Journal of Biogeography 25, 31–36. Meiklejohn, K.I., 1994. Valley asymmetry on south-eastern Alexander Island, Antarctica, and valley forms in the High Drakensburg, southern Africa. South African Geographical Journal 76, 68–72. Moncrieff, A.C.M., Kelly, S.R.A., 1993. Lithostratigraphy of the uppermost Fossil Bluff Group (early Cretaceous) of Alexander Island, Antarctica: history of an Albian regression. Cretaceous Research 14, 1–15. Mulvey, R.H., 1978. Predaceous nematodes of the family Mononchidae from the Mackenzie and Porcupine river systems and Somerset Island, N.W.T. Canada. Canadian Journal of Zoology 56, 1847–1868. O´ Cofaigh, C., Pudsey, C.J., Dowdeswell, J.A., Morris, P., 2002. Evolution of subglacial bedforms along a paleo-ice stream, Antarctic Peninsula continental shelf. Geophysical Research Letters 29, 1199. Pudsey, C.J., Evans, J., 2001. First survey of Antarctic sub-ice shelf sediments reveals mid-Holocene ice shelf retreat. Geology 29, 787–790. Pugh, P.J.A., 1993. A synonymic catalogue of the Acari from Antarctica, the sub-Antarctic Islands and the Southern Ocean. Journal of Natural History 27, 232–421. Pugh, P.J.A., Convey, P., 2000. Scotia Arc Acari: antiquity and origin. Zoological Journal of the Linnean Society 130, 309–328. Schlichting, H.E., Speziale, B.J., Zink, R.M., 1978. Dispersal of algae and protozoa by Antarctic flying birds. Antarctic Journal of the United States of America 13, 147–149. Smith, R.I.L., 1984. Terrestrial plant biology of the sub-antarctic and antarctic. In: Laws, R.M. (Ed.), Antarctic Ecology. Academic Press, London, pp. 61–162. Smith, R.I.L., 1988. Bryophyte oases in ablation valleys on Alexander Island, Antarctica. Bryologist 91, 45–50. Smith, R.I.L., 1990. Signy Island as a paradigm of biological and environmental change in Antarctic terrestrial ecosystems. In: Kerry, K.R., Hempel, G. (Eds.), Antarctic Ecosystems, Ecological Change and Conservation. Springer, Berlin, pp. 32–50. Sohlenius, B., Bostro¨m, S., 2005. The geographic distribution of metazoan microfauna on East Antarctic nunataks. Polar Biology 28, 439–448.

3151

Sohlenius, B., Bostro¨m, S., Jo¨nsson, K.I., 2004. Occurrence of nematodes, tardigrades and rotifers on ice-free areas in East Antarctica. Pedobiologia 48, 395–408. Spaull, V.W., 1972. Antarctenchus hooperi n. g., n. sp. (Nematoda: Dolichodoridae) from Signy Island, South Orkney Islands, with the erection of a new subfamily. Nematologica 18, 353–359. Spaull, V.W., 1973. Distribution of soil nematodes in the maritime Antarctic. British Antarctic Survey Bulletin 37, 1–6. Spaull, V.W., 1981. Observations on Coomansus gerlachei (de Man) (Nematoda: Mononchidae), a predaceous nematode from the Antarctic. British Antarctic Survey Bulletin 53, 195–200. Steiner, G., 1916. Beitrage zur geographischen Verbreitung freilebender Nematoden. Zoologischer Anzeiger 46, 311–335. Stevens, M.I., Hogg, I.D., 2003. Long-term isolation and recent range expansion from glacial refugia revealed for the endemic springtail Gomphiocephalus hodgsoni from Victoria Land, Antarctica. Molecular Ecology 12, 2357–2369. Sugden, D.E., Clapperton, C.M., 1977. The maximum ice extent on island groups in the Scotia Sea, Antarctica. Quaternary Research 7, 268–282. Sugden, D.E., Clapperton, C.M., 1981. An ice-shelf moraine, George VI Sound, Antarctica. Annals of Glaciology 2, 135–141. Taylor, B.J., Thomson, M.R.A., Willey, L.E., 1979. The geology of the Ablation Point—Keystone Cliffs area, Alexander Island. British Antarctic Survey Scientific Reports No. 79, 65pp. Timm, R.W., 1971. Antarctic soil and freshwater nematodes from the McMurdo Sound Region. Proceedings of the Helminthological Society of Washington 38, 42–52. Tsalolikhin, S.J., 1981. A revision of the genus Tobrilus (Nematoda:Tobrilidae). Zoologicheskij Zhurnal 9, 1302–1313 (in Russian). Tsalolikhin, S.J., 1989. Rare and new nematode species from Antarctica. Trudy Zoologischeskogo Instituta Akademii Hauk, Leningrad 194, 96–101 (in Russian). Wharton, D.A., 1995. Cold tolerance strategies in nematodes. Biological Reviews 70, 161–185. Wharton, D.A., 2002. Life at the Limits: Organisms in Extreme Environments. Cambridge University Press, Cambridge 307pp. Yeates, G.W., 1970. Two terrestrial nematodes from the McMurdo Sound Region, Antarctica, with a note on Anaplectus arenicola Killick, 1964. Journal of Helminthology 44, 27–34. Yeates, G.W., 1979. Terrestrial nematodes from Bunger Hills and Gaussberg, Antarctica. New Zealand Journal of Zoology 6, 641–643. Yeates, G.W., 1986. Stylet and body lengths as niche dimensions in plant parasitic nematodes. Zoologischer Anzeiger 216, 327–337.