Exploring biological constraints on the glacial history of Antarctica

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Quaternary Science Reviews 28 (2009) 3035–3048

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Quaternary Science Reviews

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Exploring biological constraints on the glacial history of Antarctica

Peter Convey a,*,1, Mark I. Stevens b,c,1, Dominic A. Hodgson a,1, John L. Smellie a,Claus-Dieter Hillenbrand a, David K.A. Barnes a, Andrew Clarke a, Philip J.A. Pugh d,Katrin Linse a, S. Craig Cary e,f

a British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UKb South Australian Museum, Adelaide, SA 5000, Australiac Flinders University, School of Biological Sciences, Adelaide, SA 5001, Australiad Department of Life Sciences, Anglia Ruskin University, East Road, Cambridge CB1 1PT, UKe Department of Biological Sciences, University of Waikato, Private Bag 3105, Hamilton, New Zealandf University of Delaware, College of Marine and Earth Studies, Lewes, DE 19958, USA

a r t i c l e i n f o

Article history:Received 8 January 2009Received in revised form14 August 2009Accepted 17 August 2009

* Corresponding author. Tel.: þ44 1223 221588; faxE-mail address: [email protected] (P. Convey).

1 Equal lead contributors.

0277-3791/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.quascirev.2009.08.015

a b s t r a c t

The evolutionary and biogeographic history of the contemporary Antarctic terrestrial and marine biotasreveals many components of ancient origin. For large elements of the terrestrial biota, long-termisolation over timescales from hundreds of thousands to tens of millions of years, and thus persistencethrough multiple glacial cycles, now appears to be the norm rather than the exception. For the marinebiota there are some parallels with benthic communities also including ancient components, togetherwith an incidence of species-level endemism indicating long-term isolation on the Antarctic continentalshelf. Although it has long been known that a few ice-free terrestrial locations have existed in Antarcticafor up to 10–12 million years, particularly in the Dry Valleys of Victoria Land along with certain nunataksand higher regions of large mountain ranges, these do not provide potential refugia for the majority ofterrestrial biota, which occur mainly in coastal and/or low-lying locations and exhibit considerablebiogeographic regionalisation within the continent. Current glacial models and reconstructions do nothave the spatial resolution to detect unequivocally either the number or geographical distribution ofthese glacial refugia, or areas of the continental shelf that have remained periodically free from icescouring, but do provide limits for their maximum spatial extent. Recent work on the evolution of theterrestrial biota indicates that refugia were much more widespread than has been recognised and it isnow clear that terrestrial biology provides novel constraints for reconstructing the past glacial history ofAntarctica, and new marine biological investigations of the Antarctic shelf are starting to do likewise.

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1. Introduction

The current paradigm used to explain the evolutionary andbiogeographic history of the Antarctic terrestrial biota is under-pinned by the assumption that most ice-free low altitude surfaces(i.e. where most of the contemporary terrestrial biota occur) wouldhave been overrun by ice during previous glaciations. This criticalassumption derives from ice sheet reconstructions and glaciolog-ical modelling of, particularly, the last glacial period and Last GlacialMaximum (LGM; around 22–17 ka) but also previous Miocene(23–5 Ma), Pliocene (5–2.6 Ma) and Pleistocene (2.6 Ma–10 ka)glaciations. Although having coarse spatial resolution, ice sheet

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reconstructions based on glaciological models and geomorpho-logical field data, respectively, have been interpreted as implyingthat the thickened and extended ice sheets both in East and WestAntarctica would have covered most terrestrial areas during the lastglacial period and/or previous glacial maxima (Denton et al., 1984;Nakada et al., 2000; Huybrechts 1993, 2002; Denton & Hughes,2002; Denton & Sugden, 2005; Lewis et al., 2006; Pollard &DeConto, 2009). The marine continental shelf benthos (whichincludes the majority of described species for Antarctica) is simi-larly often considered to have been eradicated during glacialmaxima by the grounded ice-sheet advancing to the shelf break or,in shelf areas where grounded ice did not reach the shelf edge,starvation under permanent ice-shelf cover, or destruction byheavy iceberg scouring (Thatje et al., 2005).

In models of the LGM the ice sheet advances to the shelf breakaround almost all of the continent (Denton & Hughes, 2002; Huy-brechts, 2002; Pollard & DeConto, 2009). In the LGM model of

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Huybrechts (2002) most ice-sheet advances occur (1) over theWeddell Sea and Ross Sea embayments, (2) in the Amery Basin, and(3) around the Antarctic Peninsula (Fig. 2; see Fig. 1 for geographicposition of locations mentioned in the text). Marine geologicalreconstructions of grounding line positions of the Antarctic IceSheet during the last glacial period (Fig. 3) support this conclusion(Anderson et al., 2002). Multi-beam echo sounding mapping ofsubglacial bedforms (swath bathymetry) in combination withdating of sediment cores recovered from these bedforms hasenabled a precise identification of regional ice sheet limits duringthe last glacial period (e.g. Anderson et al., 2002; Heroy & Anderson,2005; O Cofaigh et al., 2005a; refs. in Sugden et al., 2006; Larteret al., 2009). These studies give direct evidence of grounded ice

Fig. 1. General map of Antarctica and the Southern Ocean, indicating locations mentioned thAntarctic continent.

advance to the shelf break around most of Antarctica (Fig. 4).Exceptions were outer shelf areas in the western Ross Sea (Lichtet al., 1996; Shipp et al., 1999) and Prydz Bay (Domack et al., 1998;O’Brien et al., 1999), which are both assumed to have been coveredby floating ice shelves (Domack et al., 1998; Shipp et al., 1999), andthe outermost shelf north of George V Land, which was heavilyiceberg scoured (Beaman & Harris, 2003). Similarly, cosmogenicdating of erratics, moraines and former ice trimlines on interiormountains and in coastal regions show that the ice was consider-ably thicker at glacial maxima than at present (e.g. Stone et al.,2003; Fogwill et al., 2004; Bentley et al., 2006; Fink et al., 2006;Johnson et al., 2008a,b). However, this is not the case at all locations(e.g. Oberholzer et al., 2008), and in some regions studies have

roughout the text; see also Fig. 5a for indication of the arbitrarily defined regions of the

Fig. 2. In ice sheet models (e.g. Huybrechts, 1993, 2002) the ice sheet reachesa maximum extent close to the shelf break around the continent by 15 ka. Most of theice-sheet advance is over the Weddell and Ross embayments, the Amery Basin, andaround the Antarctic Peninsula. Colours indicate surface elevation relative to presentsea level, contour interval is 250 m; the lowest contour is for 250 m which is generallyclose to the grounding line (s.l.e.¼ sea-level equivalent).

P. Convey et al. / Quaternary Science Reviews 28 (2009) 3035–3048 3037

concluded that the ice was significantly thinner than predicted byice-sheet models (e.g. Mackintosh et al., 2007; Smellie et al., 2008,2009). It should be noted that most of these studies relate only tothe last glacial period, and that much less evidence is availablepertaining to earlier glacial advances.

Fig. 3. Marine geological reconstructions of grounding line positions of the Antarctic Ice Sheof the continental shelf. This figure shows the oldest constraining ages for initial ice sheet reet al., 2002).

The current generation of ice-sheet models are only designed togive a simplified overview of the maximum extent of the LGM icesheet at a relatively coarse spatial resolution (e.g. horizontal reso-lutions of 20 km in the model of Huybrechts, 2002, and 40 km inthe model of Pollard & DeConto, 2009) and are not appropriate forsimulating the behaviour of individual outlet glaciers or icestreams, while geological reconstructions cover only small areas ofthe Antarctic continent and the surrounding shelf (Anderson et al.,2002; Denton & Hughes, 2002; Sugden et al., 2006). Additionally,the geological observations are only occasionally used to validateLGM ice-sheet models. Nevertheless, collectively these recon-structions suggest that most of the ice-free habitats other than highmountain ranges (nunataks) might have been overrun at somepoint during the last and/or earlier glacial maxima, which leads tothe hypothesis that most pre-Neogene (older than 23 Ma) terres-trial life of Antarctica, with the possible exception of sub-surfacebacteria, would have been wiped out by successive glacialadvances. There are parallels in the marine environment wheremodels of ice sheet advance during the last glacial period wouldappear to imply extensive offshore grounding of ice and eradicationof continental shelf benthic habitats.

For the terrestrial biota, the paradigm of eradication duringglacial maxima has been reinforced by the presence of fossils inVictoria Land representing a now extinct Antarctic community thatappears to have included the last surviving relicts from pre-glacialAntarctica. These fossils describe a suite of assemblages, includingNothofagus-herb tundra vegetation, together with both terrestrial(e.g. weevils, flies) and freshwater (e.g. gastropods, bivalves, ostra-cods, fish) faunas all of which survived ice sheet formation around34 Ma until they became extinct sometime during the middleMiocene (w14–12 Ma) or possibly later, with debate continuing overthe precise dating of these deposits (Ashworth & Cantrill, 2004;

et at the LGM demonstrate that in many regions the ice extended out towards the edgetreat from the shelf. Deeper grey shades indicate the continental slope (after Anderson

Fig. 4. (a) Recent multi-beam echo sounding surveys (swath bathymetry) haveenabled precise mapping of past ice limits at the LGM. This image shows line-sourcedgullies directly offshore from the axis of Anvers Trough (coastal shelf west of theAntarctic Peninsula). These, and other similar features found around Antarctica, arebelieved to be formed by meltwater debouching beneath ice grounded at the shelfbreak (Heroy & Anderson, 2005). (b) Multi-beam image from the outer shelf in thesouthern Bellingshausen Sea showing mega-scale glacial lineations (MSGL) in theBelgica Trough. The trough was eroded into the shelf by a grounded ice stream, whichadvanced to the shelf break during the last glacial period and thereby carved the MSGLinto the till substratum at its base (for details see O Cofaigh et al., 2005b).


Ashworth et al., 2007; Lewis et al., 2008; Williams et al., 2008). Thishas led to the widely held but not critically assessed assumption thatmost, possibly all, contemporary terrestrial organisms colonised thecontinent from lower latitudes during subsequent Interglacialperiods when the ice retreat made terrestrial habitats availableagain (see also Wise,1967, 1971; Adams et al., 2007). Brundin (1970)in effect recognised the weakness of this assumption, but this did notlead to further work, and the paradigm of glacial eradication came todominate both biogeographic and evolutionary discussion of theAntarctic terrestrial biota.

2. The requirement for ice-free glacial refugia

Many extant Antarctic terrestrial organisms are known from andrestricted to low altitude habitats, generally in coastal regions(Block, 1984; Smith, 1984; Marshall & Convey, 2004; Adams et al.,2006; Convey, 2007). In the most biodiverse regions of Antarcticathis is where much of the ice-free ground occurs, although acrossAntarctica as a whole the majority of exposed ground area iscontributed by higher altitude inland and biologically depauperatemountain ranges, while ‘distance from the coast’ is skewed by thepresence of fringing ice shelves and glaciers even at lower altitudes(e.g. the Bunger Hills and Victoria Land Dry Valleys) (see Peat et al.,2007; Fig. 5; Table 1). Therefore in order for a hypothesis of long-term (pre-LGM or longer) biological persistence to be viable, ice-free refugia are required both at low altitude and in proximity to thecoast. Such an LGM refugium might have existed in the Bunger Hills(East Antarctica), where the ice sheet had already retreated from 30to 20 ka (Gore et al., 2001). In a small number of locations there isdirect evidence that refugia did exist throughout the last glacial–Interglacial cycle. For example, a late-Quaternary refuge for lakefauna, diatoms and cyanobacteria has been described in theLarsemann Hills (Hodgson et al., 2005; Cromer et al., 2006; Tatonet al., 2006), confirming survival over ca. 150 ka. However, one ofthe main problems in locating these refugia over longer timescalesis that successive post-Palaeogene ice sheet extension events haveobscured or destroyed evidence of previous boundaries and surfaceelevations (Florindo et al., 2003; Smellie et al., 2008).

For many areas of the continent there are no field estimates forprevious ice sheet thicknesses (cf. Bentley et al., 2006), whichconsiderably restricts our ability to identify potential refugia loca-tions or regions. Notable exceptions include the Dry Valleys andTransantarctic Mountains of southern Victoria Land, wheregeomorphology supports ice-free conditions throughout the last12–10 Ma (Sugden et al., 2006) and recent cosmogenic isotopesurface exposure dating studies support relatively constant icesheet thickness from the early Pliocene to the present (Oberholzeret al., 2008), and parts of the Prince Charles Mountains, which mayhave been ice-free for at least two million years (Fink et al., 2006).Unfortunately, few of these areas have received specialist biologicalresearch (cf. Peat et al., 2007; Fig. 5), and their true significance asterrestrial biotic refugia has yet to be confirmed.

Two new lines of evidence are now refining our picture ofAntarctic biogeographic history. First, new geological (glacio-volcanism, cosmogenic isotope dating) and geomorphologicalevidence is providing fresh insights for constraining past Antarcticice sheet thickness. Second, biology is contributing clear evidenceof the long-term evolutionary persistence of terrestrial biota on thecontinent through multiple glacial cycles, in some cases even sincethe break-up of Gondwana. The purpose of this inter-disciplinaryreview is to provide an overview of recent advances in these fieldsas applied to Antarctica. In particular, we integrate evidence forspecific marine and terrestrial regions maintaining ice-freeelements over different timescales, and the implications that thishas for reconstructions of local ice sheet history. This approachdevelops previous work that has focused only on terrestrialevidence (Convey et al., 2008).

3. Geological and geomorphological evidence

Geomorphological evidence and cosmogenic isotope surfaceexposure dating are providing new constraints on past ice sheetconfiguration both on land and on the Antarctic continental shelf.Bentley et al. (2006), for example, have reconstructed the LGMconfiguration of the Antarctic Peninsula Ice Sheet (APIS) showingthat it experienced several hundred metres of thickening leaving

Fig. 5. (a) Map of Antarctica illustrating the current extent of botanical research on the continent. Degree latitude-longitude boxes which contain >1000 m2 ground free frompermanent ice/snow are coloured green if at least a single plant record has been recorded from them and brown if there are no records (after Peat et al., 2007). Plants are recordedfrom 30% of these boxes. The total area of ice-free ground in boxes with plant records is 2.2727� 1010 m2, and in those without plant records is 2.2828� 1010 m2. (b) Map of allbenthic sampling sites in Antarctica illustrating the extremely variable historical sampling distribution and intensity around the continent.


striations on most sampled mountain summits in the southern andcentral parts of the Antarctic Peninsula. This is consistent with (1)other geological evidence of the APIS configuration during the LGM(e.g. Bentley & Anderson,1998; Ingolfsson et al., 2003; Sugden et al.,2006); (2) ice sheet modelling (e.g. Denton et al., 1991; Nakadaet al., 2000; Anderson et al., 2002; Huybrechts, 2002) which hassuggested that a large ice sheet straddled the Antarctic Peninsula,and (3) marine geophysical studies which have also demonstratedthat the APIS extended repeatedly out towards the shelf edgeduring the Neogene and Quaternary (e.g. Larter et al., 1997; Bart &Anderson, 2000; Heroy & Anderson, 2005; Sugden et al., 2006; Bartet al., 2007, and references therein).

None of these studies provides direct geological evidence for thepersistence of low altitude refugia through the last glacial period inthis region. In contrast, recent biological evidence, in the form ofdiversity hotspots with high levels of endemism and estimates ofthe timescale of evolutionary divergence from molecular clockstudies, points clearly to the existence of these refugia (Section 4,

Table 1The distribution of ice-free ground across the Antarctic continent (see Fig. 5a for sector locare derived from the Antarctic Digital Database version 5 (www.add.scar.org, 2008), withis a function of survey data available, and varies substantially between sectors (see also

Sector Total areaof sector(includingice shelves;km2; 3 s.f.)

Area (km2)(% of totalsector area)of ice freeground withinsector

Area (km2)(% of totalsector area)of ice freeground wit10 km ofcurrent coa

Byrd 1.59� 106 2353 (0.148) 59.6 (0.00Enderby 3.12� 106 7363 (0.236) 1460 (0.04Graham 1.29� 105 3092 (2.39) 2374 (1.84Maud 2.25� 106 3555 (0.158) 0 (0)Palmer 2.65� 105 3630 (1.37) 161 (0.06Ronne 1.35� 106 3564 (0.264) 4.9 (0.00S. Orkney 6.25� 102 98.1 (15.7) 98.1 (15.7S. Shetland 3.85� 103 423.5 (11.0) 423.5 (11.0Scott 1.42� 106 21584 (1.52) 1761 (0.12Wilkes 3.51� 106 667 (0.019) 146 (0.00Total area (km2) 13.6� 106 4.62� 104 (0.34) 6488 (0.04

below). However, in the northern Antarctic Peninsula, glacio-volcanic evidence, now supported by results of climate modelling,shows that ice thickness, although not directly identifying ice-freeground (see below; Smellie et al., 2006, 2008, 2009), was typicallybetween 200 and 400 m with rarer episodes of thicker ice, up toc. 750 m in the north and increasing to >c. 850 m in the south. Inparticular, there is no evidence for the much thicker ice cover(up to> 2 km thick) postulated by some models for the LGM(Denton et al., 1991; Nakada et al., 2000), at least during the pastc. 5 m.y. (Smellie et al., 2008, 2009).

This evidence comes from several large and long-lived basalticvolcanic centres and numerous monogenetic volcanic fields thaterupted during the past 7 Ma (Fig. 6). Geological studies havedemonstrated that these outcrops were mainly formed in associa-tion with an ice sheet (the former APIS), which was surprisinglythin throughout the late Neogene period (< 7.7 Ma), although therecord is not continuous (Fig. 7) (Smellie et al., 2006, 2008, 2009).In addition, the largely pristine appearance of the highest surfaces

ations), and the South Shetland and South Orkney archipelagos of the Scotia arc. Data‘coast’ considered as the current edge of ice shelves; data accuracy and completenessFox & Cooper, 1994).

hin

st

% of ice freeground in sectorbetween 0 and200 m altitude

% of ice freeground insector between200 and 500 maltitude

% of ice freeground insector >500 maltitude

375) 2.41 7.82 89.868) 28.6 11.7 59.7) 31.9 27.1 41.0

0.756 0.824 98.409) 2.28 14.9 82.80365) 0.735 1.50 97.8) No data No data No data) 72.0 7.74 20.34) 3.81 8.09 88.1416) 87.3 5.94 6.768)

http://www.add.scar.org

Fig. 6. Cartoon view of a small volcano erupting under an ice sheet. Such eruptions leave a clear geological record of the former ice sheet and its characteristics, e.g. thickness,surface elevation (after Smellie 2006; Smellie et al., 2006, 2008).


currently exposed on James Ross Island, now ca. 620 m a.s.l. butprobably lower at the time of formation, were thought to havepossibly been ice-free since they formed during eruptions at4.69 Ma (Smellie et al., 2008). However, new cosmogenic isotopeexposure dating of those surfaces suggests an alternative scenario,namely that they could have been continually covered by snowand/or cold-based ice since they were first formed, and may onlyhave become exposed during the last c. 15 ka, thus considerablyreducing their potential as long-lived biological refugia (Johnsonet al., in press).

These studies illustrate the considerable difficulty in identifyingand verifying sites of likely long-lived biological refugia inAntarctica. Taking into account marine geological evidenceobtained through high-resolution swath bathymetric surveys forlocal APIS thicknesses in excess of 1600–1700 m in deep basinsformerly occupied by outlet glaciers on parts of the inner shelf(O Cofaigh et al., 2005a; Domack et al., 2006), these findings indi-cate that the APIS thickness and extent during the last glacial periodmust have varied significantly. However, the tenet that the APISwas generally thin (hundreds of metres, not thousands, over mostof its geographical extent) seems valid (Smellie et al., 2008, 2009).

Fig. 7. Schematic reconstruction of how part of the APIS might have looked duringmuch of the previous 6 Ma. The view is looking to the northwest across James RossIsland toward the eastern flank of the Antarctic Peninsula. Although periods of thickerice cover are known, none would have been capable of completely swamping thetopography. The dark brown colouration denotes snow- and ice-free areas.

This in turn raises the realistic possibility that, locally, rock outcropswould have remained uncovered as nunataks, although does notdirectly prove this contention.

Considerable regional variations in snow accumulation, icethickness and ice flow dynamics during the last glacial period arealso known from the East Antarctic Ice Sheet (EAIS) and thus mayapply more generally across the Antarctic continent. For example,landscape development, glaciovolcanic and cosmogenic datingstudies in Victoria Land also show that, while the ice cover wasgenerally thin (few hundred metres) along 200 km of the EAISmargin in late Miocene times (c. 10–4 Ma), there were also a fewperiods of overriding, when ice thicknesses were much greater,although precise estimates of maximum thickness and geograph-ical extent are currently not available (cf. Denton & Sugden, 2005;Johnson et al., 2008b; Oberholzer et al., 2008; Welten et al., 2008;J. Smellie & S. Rocchi, unpublished data). Similarly, for the WestAntarctic Ice Sheet (WAIS), new geological results from theANDRILL AND-1B drill core in the Ross Sea (Naish et al., 2009) anda new ice-sheet model (Pollard & DeConto, 2009) suggest that boththe thickness and the extent of the WAIS may have undergone hugevariations throughout the Pliocene and the Pleistocene.

4. Biological evidence for the long-term evolutionarypersistence of terrestrial and freshwater biota

4.1. Biogeographic inferences

Entomological research carried out in both East and WestAntarctica as early as the 1960s, following on from the InternationalGeophysical Year (1957–1958), recognised that at least a proportionof the limited terrestrial biota then known could not easily beexplained by recent colonisation (e.g. Gressitt, 1967; Brundin,1970). However these results did not feed into subsequent biolog-ical or cross-disciplinary work, and only recently have sufficientdistributional data become available to permit detailed scrutiny ofterrestrial biogeographic patterns in Antarctica. Recent biogeo-graphic analyses have confirmed long-term persistent elements inthe Antarctic biota (Fig. 8). Importantly, these studies also clearlydemonstrate that regionalisation of the Antarctic terrestrial biota isgreater than was previously realised (Adams et al., 2006; Barrettet al., 2006; Maslen & Convey, 2006; Chown & Convey, 2007;Convey & Stevens, 2007; Yergeau et al., 2007a,b; Convey et al. 2008;Pugh & Convey, 2008; Wood et al., 2008), precluding the treatmentof Antarctica as a single biological entity, with different regions atlarge scale within the continent able to act as mutual refugia for

Fig. 8. Schematic illustration of inferred evidence for continuous presence of major biological groups (excepting most micro-organisms) in the terrestrial, freshwater and marineenvironments of Antarctica since the break-up of Gondwana based on molecular, phylogenetic, classical biogeographic and fossil evidence. Note that the geological timescale is non-linear.


each other over time. For example, a biological boundary separatesterrestrial fauna between the Antarctic Peninsula and the rest ofAntarctica (the ‘Gressitt Line’) (Chown & Convey, 2007), whileconsiderable levels of within-sector species endemism characterisethe invertebrate faunas of all of the standard ‘sectors’ of theAntarctic continent (Pugh & Convey, 2008), even though these arearbitrarily defined. Of the terrestrial fauna that dominates today’scommunities, only a single apparently ‘pan-Antarctic’ species ofCollembola (springtail; but this is not supported by new molecularphylogenetic analyses, see Pugh & Convey, 2008; Torricelli et al., inpress) and no Acari (mites) or Nematoda (nematode worms orthreadworms) are shared across the Gressitt Line (Andrassy, 1998;Maslen & Convey, 2006; Pugh & Convey, 2008), indicating anancient, yet mostly independent signature of high regional ende-mism (Table 2).

Table 2Levels of species endemism in Antarctic invertebrates within the recognised geographic

Maud Enderby Wilkes

Invertebrates endemic to sector 16 7 1Invertebrates endemic to Antarctica 28 23 10Total invertebrates in sector 38 51 26

Around 50% of Antarctic lichen, tardigrade and dipteran speciesare endemic to (i.e. are only known from) the continent as a whole,along with most mites and springtails, and possibly all nematodes(Andrassy, 1998; Øvstedal & Smith, 2001; Convey & McInnes, 2005;Maslen & Convey, 2006; Pugh & Convey, 2008), again consistentwith an ancient regional origin for these taxa. For bacteria andother microbial groups, it has been hypothesised that their highpotential for aerial transport would lead to large numbers ofcosmopolitan species (Finlay, 2002). Unfortunately, because manymicrobial species are difficult to identify using morphologicalexamination it has been impossible to explore adequately whether‘uniqueness’ equates to ‘endemicity’ (Vincent, 2000; Finlay, 2002;Sjoling & Cowan, 2003; Tindall, 2004; Boenigk et al., 2006; Tatonet al., 2006), and work in this area is now largely reliant onmolecular data (see Section 4.2; De Wever et al., 2009). Low

al sectors of the Antarctic continent (derived from Pugh & Convey, 2008).

Scott Byrd Ronne Palmer Graham

34 1 1 21 850 1 1 44 4067 1 1 65 84


diversity in isolation is perhaps not unexpected (e.g. Yergeau et al.,2007a), and at very large spatial scales, as with larger organisms,there is a striking decrease in levels of microbial diversity withprogression into the continental interior (Lawley et al., 2004).

Some studies have identified intra-regional endemism at evensmaller scales than described above. For example, south-easternAlexander Island shows both high species diversity and endemism(40% in Nematoda), implying the existence of local refugia (Maslen& Convey, 2006) during multiple glacial cycles. The limited overlapbetween the Alexander Island arthropod and nematode faunasand those of neighbouring Marguerite Bay and the AntarcticPeninsula (Convey & Smith, 1997) implies that additional refugiaare also required in those areas. In a characterized eukaryotic‘hotspot’ on southern Alexander Island, Mars Oasis (Convey &Smith, 1997; Lawley et al., 2004), the microbial diversity is alsounique and elevated well above that expected for that latitude(Yergeau et al., 2007b).

Forty percent of the lichen flora of the remote and young(formed 3.1–0.03 Ma) maritime Antarctic South Sandwich archi-pelago are species endemic to Antarctica, indicating that thecontinent itself has been a source of colonizing propagules to lowermaritime Antarctic latitudes throughout the Late Pliocene andPleistocene (Convey et al., 2000). Similarly, morphological studiesimply that Antarctica harbours ancestral species within Gond-wanan/Southern Hemisphere groups, including the endemicfreshwater copepod Gladioferens antarcticus from the Bunger Hills(Bayly et al., 2003). Taken together these examples cover diversebiological groups and parts of the continent, but serve to illustratethe level of biogeographical detail becoming available from recentstudies, and highlight the need for multiple glacial refugia onregional and local scales within Antarctica (Fig. 8).

The levels of endemism in terrestrial microarthropods identifiedthroughout the Transantarctic Mountains also reveal an ancient,isolated, biota (Gressitt, 1967; Brundin, 1970; Adams et al., 2006).Furthermore, nunatak biota in other regions of East Antarcticademonstrate the persistence of a few ancient specialists having littleor no overlap with coastal biotas. The endemic mite family Maud-heimiidae (Oribatida) provides a striking example (Marshall & Pugh,1996; Marshall & Coetzee 2000), because it may have continuouslyinhabited montane regions of East Antarctica at least since the finaldisintegration of Gondwana, and shows patterns of intra-familialdifferentiation consistent with 40–100 ka orbital (Milankovitch)glacial–Interglacial cycles leading to speciation on Pliocene–Pleis-tocene timescales (Marshall & Coetzee, 2000). Michaux & Leschen(2005) propose a similarly relictual element of Gondwanan originwithin the terrestrial biotas of islands of the Campbell Plateau (NewZealand sub-Antarctic islands, Macquarie Island).

On Pleistocene timescales, there is direct palaeolimnologicalevidence that the cladoceran Daphniopsis studeri has been contin-uously present in Lake Reid, Larsemann Hills, for over 120 ka(Cromer et al., 2006; Gibson & Bayly, 2007). It has also been inferredthat the copepod Boeckella poppei has been present in a series oflakes in the Amery Oasis near the Prince Charles Mountains overa similar period (Gibson & Bayly, 2007). Although direct evidence ofits presence here in the form of preserved DNA and exoskeletonfragments is limited to 10–12 ka, this age still predates the earliestrecorded post-glacial recolonisation by this species of lakes else-where in its contemporary distribution on the Antarctic Peninsulaand Scotia arc (Bissett et al., 2005; Gibson & Bayly, 2007). Further-more, the rapid post-glacial recolonisation of the latter lakes by thispoorly-dispersing crustacean is also suggestive of a local rather thanan extra-continental refugium (Gibson & Bayly, 2007). Whileevidence such as described is currently limited to the most recentglacial cycle, it does provide a proof of principle for the persistence ofAntarctic lacustrine refugia through successive cycles.

4.2. Molecular biological approaches

The biogeographical inferences described above provide strongbut ultimately circumstantial support for an ancient origin for manyelements of the Antarctic terrestrial and freshwater biota. Molec-ular dating is a valuable tool in this respect, but there are certaincaveats (e.g. Graur & Martin, 2004; Heads, 2005; Upchurch, 2008).The accumulation of random mutations ultimately relies onknowing the mutation, or substitution, rate per generation (Welch& Bromham, 2005; Sanders & Lee, 2007) and this is likely to differamong species with different life-histories (e.g. Stevens & Hogg,2006b). Often ‘per generation’ has been replaced by ‘per year’ asuniversal clocks were calculated from a correlation betweenmolecular divergence and particular geological events (e.g. Brower,1994; Gaunt & Miles, 2002; Quek et al., 2004). These calculationshave become increasingly complex as they attempt to simulate ormodel evolutionary processes (e.g. Drummond et al., 2006; Sanders& Lee, 2007), but one thing is certain – increasing ability to incor-porate individual substitution rates and constraints on minimumdates allows far greater confidence in dating estimates.

With molecular biological analyses an increased understandingof evolutionary relationships and timescales is possible, generatingthe potential to constrain the dating of significant evolutionaryevents (e.g. Sunnucks, 2000; Stevens & Hogg, 2006a). For example,on sub-Antarctic Marion Island the phylogeography of the miteEupodes minutus corroborates evolutionary steps corresponding toboth major local volcanic events and Pleistocene glacial cycles(Mortimer & Jansen van Vuuren, 2007). Similar timescales of lessthan one million years have been proposed to correspond todivergences among springtail populations (Collembola) fromVictoria Land, East Antarctica (Stevens & Hogg, 2003; Stevens et al.,2007; McGaughran et al., 2008). However, in the same region,considerably greater divergences in mites than in springtails havebeen identified (Stevens & Hogg, 2006b), which are as yet unex-plained but either may indicate very different evolutionary rates indifferent endemic taxa, or that the key lineage splits happened atdifferent points in time. One potential implication is that thetimescale may be even older for the more slowly evolving spring-tails. In a study examining inter-population divergence of twospringtail species occurring, respectively, in the Antarctic Penin-sula/Scotia arc and southern Victoria Land, McGaughran et al.(in press) concluded that both showed clear evidence of multipledivergence events within these regions corresponding to thePleistocene glaciations, even with demographic differences takeninto account.

Longer timescales received little attention until the origins ofcontinental Antarctic endemic springtails were examined in thecontext of related circum-Antarctic taxa (Stevens et al., 2006). Thiswork suggested dispersal/colonization events in the genusCryptopygus on some sub-Antarctic volcanic islands within the last2 Ma, noting a close association between divergence times(estimated by molecular clocks) and ages of island formation. Fourcontinental Antarctic species, by contrast, showed old (21–11 Ma)divergences which, given the levels of isolation identified forcongeners in ice-free refugia throughout the TransantarcticMountains, was most likely caused by the mid to late Mioceneglaciation step (cf. Ashworth et al., 2007; Lewis et al., 2008).A similar pattern has been observed amongst ameronothroid miteswhere several closely related genera and species from selected sub-Antarctic islands, the Scotia arc and the Antarctic Peninsula, reveala group radiating within the last 10 million years (Jansen vanVuuren et al., 2007).

Further work has examined the three chironomid midgesindigenous to the Antarctic Peninsula and Scotia arc (Allegrucciet al., 2006). The data obtained indicate that two closely related


‘sister’ species are central to unravelling the evolutionary history ofthe region. Belgica antarctica is endemic to the Antarctic Peninsulaand South Shetland Islands, and Eretmoptera murphyi to sub-Antarctic South Georgia. Thus, each is restricted to an entirelyseparate regional tectonic element, isolated during the final sepa-ration from southern South America (cf. Livermore et al., 2007). Thedivergence between these two species’ evolutionary lineages wasestimated at around 49 Ma, and from more distantly related generawithin the same subfamily at around 68 Ma. The timing ofseparation events between South Shetland and South Georgianpopulations of the third species from this region, the wingedchironomid Parochlus steinenii, was estimated at around 7 millionyears. This species had previously been assumed, although not onthe basis of specific study, to be most likely a recent colonist as it isthe only Antarctic species capable of flight (Convey & Block, 1996).While, as describd above, there are potential inaccuracies inherentwithin these molecular methods (e.g. Welch & Bromham, 2005;Sanders & Lee, 2007), the divergence of the species clearly occurredover tens of millions of years, on timescales consistent with thedisintegration of Gondwana and major glaciation steps inAntarctica (cf. Zachos et al., 2001; DeConto et al., 2008).

Even though biogeographic and phylogenetic studies of micro-bial groups in Antarctica are in their infancy, results from recentstudies are starting to demonstrate comparable levels of regionalendemism as discussed above. In doing so, data from the Antarcticnow appear to be challenging the hypothesis of global ubiquity(Finlay, 2002). Instead, these studies support higher levels ofregional microbial endemicity and uniqueness at the molecular levelthan was suggested by previous morphological studies (Vincent,2000; Sjoling & Cowan, 2003; Lawley et al., 2004; Tindall, 2004;Barrett et al., 2006; Boenigk et al., 2006; Smith et al., 2006; Tatonet al., 2006; Yergeau et al., 2007a,b; Wood et al., 2008; De Weveret al., 2009), again consistent with an ancient regional origin forthese taxa. That Antarctic microbial taxa are distinct at the molecularlevel indicates that, even for these apparently highly dispersiblegroups, rates of dispersal are insufficient to overcome the signal ofevolutionary processes of divergence since original colonisation.

5. Biological evidence for the long-term evolutionarypersistence of marine benthic biota

These recent changes in our view of the evolutionary history ofthe Antarctic terrestrial and freshwater fauna have a strong parallelin the marine realm (Fig. 8). As with Antarctic terrestrial habitats,there are still many marine benthic areas unvisited (Clarke et al.,2007), and our current understanding is influenced strongly bywork on a relatively limited range of taxa (Eastman & Grande, 1989;Hain, 1990; Brandt, 1991; Strugnell et al., 2008; Griffiths et al.,2009). Although it has long been recognised that the Antarcticmarine fauna illustrates considerable endemism and a long historyof evolutionary radiation (Arntz et al., 1994, 1997; Clarke & John-ston, 2003), the most recent Southern Ocean biogeographic studiesare revealing that in many groups levels of species endemism,while still significant, may have been greatly overestimated (e.g.see Griffiths et al., 2009, and references therein). It is also clear thatthe Antarctic marine environment is not as isolated from lowerlatitudes as its terrestrial counterpart, and there are a number ofpotential pathways for marine organisms to cross the AntarcticPolar Front (APF) in either direction (e.g. Bargelloni et al., 2000a,b;Page & Linse, 2002), with the distributions of many Southern Oceanmarine species extending into the Atlantic, Indian and Pacificoceans (Clarke et al., 2005; Barnes et al., 2006; Pawlowski et al.,2007a,b; Raupach et al., 2007; Griffiths et al., 2009). Nevertheless,the Antarctic shelf fauna is probably the most distinct marine faunaon the planet (e.g. Gili et al., 2006).

Dispersal across the APF is indicated by studies applyingmolecular clock estimates to taxon splits in molecular phylogeniesof nothothenioid fish, euphausiid crustaceans and limid bivalves.The split between the notothenioid fish genera Patagonotothen andLepidonotothen that now occur respectively north and south of theAPF is dated at 6.6–9 Ma (9 Ma in Bargelloni et al., 2000a,6.6–7.1 Ma in Stankovic et al., 2002), that between the krill speciesEuphausia vallentini and E. frigida at w7 Ma (Bargelloni et al.,2000b) and likewise between the bivalve species Limatula ovalisand L. pygmaea (Fig. 8) based on the mitochondrial 16S gene (Page& Linse, 2002). Molecular studies have shown that Antarcticbenthic species ranges extend into the oceans further north, forexample in the munnopsidid deep-sea isopod Betamorphafusiformis (Raupach et al., 2007) and in benthic foraminiferans(Pawlowski et al., 2007a,b). Pawlowski et al. (2007a) also showeda high genetic similarity in populations of the common deep-seaforaminiferan species Epistominella exigua, Cibicides wuellerstorfiand Ordidorsalis umbonatus from Arctic and Antarctic localities.Individuals of the species Epistominella vitrea, identified from theNorth Atlantic, Gulf of Mexico, North Pacific and pelagic SouthernOcean, are also genetically almost identical to those from theAntarctic shelf and continental margin (Pawlowski et al., 2007b).These authors suggested a shelf origin for the ancestors of themodern Southern Ocean population of E. vitrea that then latercolonized the deep-sea. The Southern Ocean has recently receivedprominence as being the source region for subsequent cephalopod(e.g. octopus) radiations in the other oceans (Strugnell et al., 2008),with the Antarctic endemic shelf octopus genus Adelieledone beingbasal to the clade that comprises the Antarctic and global deep-seaoctopuses. Within deep-sea benthic genera, the basal species arethose with a shallower depth range on the Antarctic continentalslope. This research indicates progressive submergence of Antarcticshelf species followed by northwards dispersal via the deep-sea,and subsequent species radiation in the deep-sea. Strugnell et al.(2008) estimated that the deep-sea lineage diverged w33 Ma andradiated at 15 Ma (Fig. 8).

Geophysical data indicate that in many regions, during the lastglacial (and possibly at previous glacial maxima) the continentalshelf was over-ridden by grounded ice or covered with thick iceshelves (e.g. Bart & Anderson, 2000; Anderson et al., 2002). Thiscould be taken as indicating that this was representative of theentire Antarctic continental shelf and that all shelf fauna wastherefore eradicated. In this scenario, the current shelf fauna musthave recolonised either from the Antarctic continental slope(Brandt, 1991; Brey et al., 1996), the deep sea (Raupach et al., 2004;Thatje et al., 2005) or the sub-Antarctic regions. However, thisunderstanding of the glacial history of the Antarctic continentalshelf comes from marine geology and in particular from detailedmulti-beam swath bathymetric mapping of the seafloor, which hasprimarily focused on large cross-shelf troughs that were eroded bymajor outlet glaciers and covers only a small area of the totalAntarctic shelf. This allows for the alternative scenario that theremay have been (as yet undiscovered) permanently ice-free areas onthe Antarctic shelf (permanent refugia) (Dayton & Oliver, 1977;Clarke & Crame, 1989), or that the shelf was not ice-covered in allplaces at the same time, allowing benthos to migrate from onetemporary refugium to another (Thatje et al., 2005). Either or bothof these scenarios would have allowed shelf fauna to survive atleast at a regional scale and some molluscan lineages (snails etc.)have a fossil history implying persistence on the Antarctic conti-nental shelf throughout the Neogene (Clarke & Crame, 1989).Molecular studies of the population structures of the sea lilly(feather star or crinoid) Promachocrinus kerguelensis (Wilson et al.,2007) and the sea spider Nymphon australe (Mahon et al., 2008)suggest that populations have survived on the Antarctic continental


shelf during the LGM. The concept of a time-transgressive ice-sheetcoverage of the Antarctic shelf during the last glacial period assuggested by Thatje et al. (2005) is supported by a glaciologicalmodel that indicates a diachronous ice-sheet advance across theshelf (Huybrechts, 2002), and by the diachronous onset of marinesedimentation on the shelf subsequent to ice-sheet retreat(Anderson et al., 2002; Heroy & Anderson, 2007). A time-trans-gressive waxing and waning of the Antarctic ice sheets during thelast glacial period, which is also consistent with terrestrial findings(Wagner et al., 2004), would have significant consequences for theestimated contribution of Antarctic ice-sheet volume to the globaleustatic sea level fall at the LGM (e.g. Bentley, 1999).

A complete eradication of the Antarctic continental shelf faunawith subsequent colonisation since the LGM would also appear tobe inconsistent with the considerable diversity that is characteristicof the current continental shelf fauna (Arntz et al., 1994; Clarke &Johnston, 2003; Barnes et al., 2009). Richness takes time to estab-lish, which is why (other factors being equal) old islands havea richer fauna than younger ones (MacArthur & Wilson, 1967).Insights into the rate at which diversity builds after eradication alsocome from studies of recovery from recent iceberg scouring (Smaleet al., 2008). At larger spatial scales (and hence longer temporalscales), destruction of shelf habitats by volcanic activity, such as hasbeen seen at Deception Island (South Shetland Islands) or SouthernThule (South Sandwich Islands), can assist estimation ofrecolonisation rates. Although no mega- or macro-benthic faunawere found in samples collected immediately following volcaniceruptions (1969–1970), a recent investigation of both the caldera ofDeception Island and a literature survey of reported fauna foundthat 163 species are now present (Barnes et al., 2009). The shelffauna at Southern Thule is also relatively species-poor, as might beexpected given its age and isolation, but some brooding infauna aresurprisingly well represented, suggesting that their ability torecolonise might have been underestimated (Kaiser et al., 2008).The recent collapse of extensive ice shelves, such as the Larsen B IceShelf in 2002, may provide an opportunity to determine thetimescale of colonisation of newly available marine benthichabitats.

Recent studies of the biogeographical affinities of the Antarcticshelf benthic fauna have also provided evidence in support of a longperiod of evolution in situ, implying the existence of fairlysubstantial refugia rather than recent recolonisation since the LGM.Early studies recognised that the Antarctic shelf fauna can bedivided into biogeographical regions, and the broad regionalisationestablished by the early workers (notably Hedgpeth, 1969) haslargely been substantiated by recent work (Linse et al., 2006; Clarkeet al., 2007). Although this regionalisation was based largely onmolluscs and polychaetes, more recent work on bryozoans andpycnogonids has confirmed the pattern of a decreasing SouthAmerican influence on species composition clockwise aroundAntarctica, concomitant with the direction of the AntarcticCircumpolar Current (Griffiths et al., 2009). These two lines ofevidence (regionalisation and spatial differences in South Americanaffinities) both point strongly to a long persistence on the conti-nental shelf. Furthermore the presence of many regional endemics(Linse et al., 2006; Griffiths et al., 2009) also argues for a long periodof evolution in situ. Especially in the Southern Ocean wheregeneration times are slow, it seems highly unlikely that suchpatterns could have evolved since the last glacial period (i.e. withinthe last ca. 10–20 ka), which would be required by the hypothesis ofcomplete eradication and subsequent recolonisation.

The existence of shelf taxa with a long evolutionary history,coupled with the relatively high diversity, must somehow becompatible with the geophysical evidence for extension of the icesheet to the edge of the continental shelf over wide areas at the

LGM. Taken together, these various lines of evidence point toa history of range fragmentation and contraction to refugia, both onspatial (shelf and down the continental slope) and temporal scales(diachrony permitting temporal overlap of refugia) at glacialmaxima, coupled with subsequent coalescence of expandingpopulations at glacial minima. Clarke & Crame (1989, 1992)identified this as a key mechanism for both causing extinction insome lineages and generating diversity, and drew an analogybetween the periodic fragmentation and expansion of geographicranges on Milankovitch (orbital) frequencies with the diversitypump of Valentine (1968). Subsequently the same process has beenidentified in the dynamics of northern hemisphere terrestrial biota,and termed orbitally forced range dynamics (Dynesius and Jansson,2000; Jansson & Dynesius, 2002). The key factor in these dynamicsis the existence of refugia, although permanent refugia have not, asyet, been identified on the Antarctic continental shelf. In theterrestrial environment, Stevens et al. (2006) reported molecularbiological evidence for an analogous contraction – coalescencecycle (i.e. signals of both divergence after isolation and subsequentrejoining of populations) over a million-year timescale in terrestrialecosystems throughout the Transantarctic Mountains.

6. Concluding discussion

In re-examining the existing literature in the light of recentadvances, it is already clear that there is tangible, and robust,support for an ancient origin for much of the Antarctic terrestrialbiota. There are a number of lines of evidence that indicate survivalin situ at multiple localities. Strengthening evidence for the long-term persistence of Antarctic terrestrial biota at multiple sitescannot be easily reconciled with the previous widely assumed viewof (almost) complete obliteration of the biota over the last 23million years by successive Neogene and Quaternary glacialmaxima. The environmental changes resulting from glacial cyclesand ice sheet advance have inevitably rendered most of thecontemporary Antarctic terrestrial biota both disharmonic andimpoverished. But it is now clear that explanation of contemporarybiogeographic patterns does not necessarily require extinctionfollowed by post-glacial recolonisation of the continent (Convey &Stevens, 2007; Convey et al., 2008).

The presence of relict biota restricted to known areas of expo-sure through glacial cycles, such as nunataks and parts of the DryValleys, is relatively straightforward to understand, at least giventhe continuous presence of habitats within these with appropriateenvironmental conditions. Such examples cannot, however, explainbiotic persistence elsewhere, as their respective biotas are sodifferent. A much greater conceptual challenge is presented by lowaltitude and coastal ecosystems, where the existence of a relictbiota carries the very clear and fundamentally important corollaryof requiring suitable terrestrial habitats to have existed continu-ously within the region. Other than in the Transantarctic Moun-tains, explicit geological/glaciological evidence supporting suchrefugia is extremely limited and then only on a pre-LGM (i.e. latePleistocene) timescale. Biological evidence points to the require-ment for much more widespread and regionally independentrefugia than currently recognised, although identification of thelocations of potential refugia remains elusive other than at a broadscale (Pugh & Convey, 2008).

We are now recognising a very similar pattern in the sea.Recent studies have confirmed two key features of the continentalshelf fauna, namely its relatively high diversity and the existenceof taxa with a long evolutionary history in situ. Coupled with morerecent analyses confirming a high incidence of species-levelendemism, marked regionalisation of fauna and decreasing SouthAmerican affinity in a circumpolar manner away from the


Antarctic Peninsula, together these all point to a long andcontinuous existence of a marine fauna in at least some locationson the shelf. In a direct analogy to the terrestrial realm, it is clearthat while much geophysical evidence demonstrates that largeareas of the continental shelf were over-ridden by grounded ice orrendered inhospitable by permanent ice-shelf coverage orfrequent iceberg scouring during the last glacial period (and byinference at previous glacial maxima), clear biological evidencepoints to the persistence of the fauna in refugia. Unlike theterrestrial biota, given the caveat above of lack of precise location,we have yet to identify where these refugia might have been evenat a ‘regional’ scale. Of particular interest may be those continentalshelf areas which were only covered by ice shelves at the LGM,because lateral advection of food from nearby sea-ice free zones(polynyas) may have enabled the in situ survival of benthic fauna(Thatje et al., 2008). However, if the hypothesis of diachrony canbe applied to the shelf environment, a clear corollary is thatindividual long-term refugia may neither have existed nor beidentifiable. Rather, biota may have moved between temporallyoverlapping refugia (a principle that may also be partly applicableto the terrestrial environment where some organisms have a lifehistory stage capable of dispersal), as has recently been proposedto explain biogeographic distributions of plants with signalsextending to Cretaceous timescales within New Caledonia, south-west Pacific (Heads, 2008).

For Quaternary scientists, the constraints which new biologicaland geological data impose on ice sheet thickness and/or extent arepotentially highly important, and require a degree of refinement orfine-scale spatial resolution that is not currently included in mostreconstructions or models. For example, the current generation ofglaciological models simulating the configuration of the Antarcticice sheets at the LGM does not have the spatial resolution tosimulate outlet glaciers or ice streams that are smaller than20–40 km and are therefore unsuitable to prove or exclude theexistence of locally restricted refugia. Resolving these issues forboth terrestrial and marine realms requires a more detailedmultidisciplinary understanding of the persistence of habitats thanthe current generation of ice sheet models permits. In particular, itpoints logically to a need for biological evidence to be includedamongst the constraints applied in glaciological reconstruction andmodelling, particularly where biological data require thepersistence of ice free biological refugia within specific (sub-)regions. Such application of an integrated approach comes asa timely step forward for Antarctic research, particularly as wemark the 50th anniversary of the International Geophysical Yearwith the largest-ever international research assault on Antarcticaduring the International Polar Year (2007–2008).

Acknowledgements

We are very grateful for the many discussions with colleaguesthat have led to the development of the ideas presented, and inparticular to Lloyd Peck, John Gibson, Ian Hogg, Wim Vyverman,Elie Verleyen, Koen Sabbe, Aaike De Wever, Annick Wilmotte,Arnaud Taton, Raphael Fernandez-Carazo and Alan Rodger; and toJamie Oliver, Helen Peat, Huw Griffiths, Kevin Newsham, PeterFretwell and A. Paul R. Cooper for either providing or assisting withthe figures and images. This paper forms an integrated output ofthe BAS BIOFLAME, CACHE, GRADES, and GEACEP, Antarctica NewZealand (KO24 and IPY Terrestrial Biocomplexity, University ofWaikato), Australian Antarctic Division (ASAC 2355), and SCAREBA research programmes, and the BelSPO-HOLANT and AMBIOprojects (DAH).

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Exploring biological constraints on the glacial history of Antarctica

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