Location, location, location: survival of Antarctic biota requires the best real estate

Abstract

The origin of terrestrial biota in Antarctica has been debated since the discovery of springtails on the first historic voyages to the southern continent more than 120 years ago. A plausible explanation for the long-term persistence of life requiring ice-free land on continental Antarctica has, however, remained elusive. The default glacial eradication scenario has dominated because hypotheses to date have failed to provide a mechanism for their widespread survival on the continent, particularly through the Last Glacial Maximum when geological evidence demonstrates that the ice sheet was more extensive than present. Here, we provide support for the alternative nunatak refuge hypothesis-that ice-free terrain with sufficient relief above the ice sheet provided refuges and was a source for terrestrial biota found today. This hypothesis is supported here by an increased understanding from the combination of biological and geological evidence, and we outline a mechanism for these refuges during successive glacial maxima that also provides a source for coastal species. Our cross-disciplinary approach provides future directions to further test this hypothesis that will lead to new insights into the evolution of Antarctic landscapes and how they have shaped the biota through a changing climate.

Full text

royalsocietypublishing.org/journal/rsbl
Opinion piece
Cite this article: Stevens MI, Mackintosh AN.
2023 Location, location, location: survival
of Antarctic biota requires the best real estate.
Biol. Lett. 19: 20220590.
https://doi.org/10.1098/rsbl.2022.0590
Received: 12 December 2022
Accepted: 2 March 2023
Subject Areas:
ecology, environmental science, evolution,
ecosystems
Keywords:
springtails, ice-free, glacial refuge, cosmogenic
dating, nunatak, ice sheet
Author for correspondence:
Mark I. Stevens
e-mail: mark.stevens@samuseum.sa.gov.au
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.6463332.
Global change biology
Location, location, location: survival
of Antarctic biota requires the best
real estate
Mark I. Stevens
1,2
and Andrew N. Mackintosh
3
1
Securing Antarctica’s Environmental Future, Earth and Biological Sciences, South Australian Museum,
SA 5000, Australia
2
School of Biological Sciences, University of Adelaide, SA 5005, Australia
3
Securing Antarctica’s Environmental Future, School of Earth, Atmosphere and Environment,
Monash University, Melbourne, VIC 3800, Australia
MIS, 0000-0003-1505-1639
The origin of terrestrial biota in Antarctica has been debated since the dis-
covery of springtails on the first historic voyages to the southern continent
more than 120 years ago. A plausible explanation for the long-term persist-
ence of life requiring ice-free land on continental Antarctica has, however,
remained elusive. The default glacial eradication scenario has dominated
because hypotheses to date have failed to provide a mechanism for their
widespread survival on the continent, particularly through the Last Glacial
Maximum when geological evidence demonstrates that the ice sheet was
more extensive than present. Here, we provide support for the alternative
nunatak refuge hypothesis—that ice-free terrain with sufficient relief above
the ice sheet provided refuges and was a source for terrestrial biota found
today. This hypothesis is supported here by an increased understanding
from the combination of biological and geological evidence, and we outline
a mechanism for these refuges during successive glacial maxima that also
provides a source for coastal species. Our cross-disciplinary approach
provides future directions to further test this hypothesis that will lead to
new insights into the evolution of Antarctic landscapes and how they
have shaped the biota through a changing climate.
1. Ancient relicts or recent colonizers?
The presence of biota, such as springtails (Arthropoda: Collembola) that inhabit
Antarctic ice-free areas year-round, has troubled biologists for more than 120
years since their discovery during the first historic voyages. The first springtails
collected were during the Belgian Antarctic Expedition (1897–1899) from Harry
Island (Antarctic Peninsula) [1,2], while Herluf Klövstad collected the first
springtails from continental Antarctica on the northern coast of Victoria Land
(Ross Sea Region) during the Southern Cross British Antarctic Expedition
(1898–1900) [3]. Springtails are now known to exist widely in ice-free areas
across Antarctica [4–7]. As more species were discovered, researchers began
to question whether they colonized since the Last Glacial Maximum (LGM;
26–19 kya [8]) when it was assumed that most of Antarctica was ice covered.
The alternative, and less favoured, scenario was that they were relict species
that survived in isolation for millions of years from pre-glacial times [9–13]
when they shared the continent with a suite of, now extinct, biota that included
Nothofagus-herb tundra, weevils, flies, freshwater fish, gastropods, bivalves and
ostracods [14–19]. Two issues have hampered our ability to adequately evaluate
© 2023 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original
author and source are credited.

these competing theories of introduction versus long-term
survival; first, that the morphological characters used to
define species have erroneously provided an illusion that
some are cosmopolitan (e.g. [4,5]), and second, that early
ice sheet reconstructions suggested that Antarctica was cov-
ered by a significant ice sheet at the LGM (e.g. [20]), which
presumably subsumed most currently ice-free terrain. These
issues led to the assumption that biota colonized the conti-
nent during interglacial periods when ice retreat provided
sufficient ice-free habitats; the assumption of glacial eradication
came to dominate (e.g. [21]).
More recently, the alternative nunatak refuge hypothesis—
that the survival of the vast majority of biota during glacial
maxima occurred on terrain that protruded through the ice
sheet (nunataks) with sufficient relief to have remained ice-
free—has gained support based only on the unique assem-
blage of biota present [9,10,22]. Despite this support, it has
remained perplexing because it fails to account for the vast
majority of biota that today resides in low-elevation coastal
margins of Antarctica [22]. In an attempt to reconcile the
presence of Antarctic species along or near the Antarctic
coastal margins, geothermal activity was proposed as a sol-
ution [23]. Here, we detail limitations of this hypothesis to
account for the most biodiverse regions in Antarctica and
provide support for the alternative nunatak refuge hypothesis.
Importantly, we have compiled support by using an
increased understanding from the combination of biological
and geological evidence, and we detail a mechanism that
provides an essential source for coastal species.
2. A framework for the survival of Antarctic biota
during glacial maxima
(a) Geothermal glacial refugia hypothesis
The most extensive reviews exploring the survival of Antarc-
tic biota during glacial maxima, although acknowledging the
unique endemic species that exist on the continent, struggle
to explain the majority of biota that is currently found near
the coastal regions of Antarctica [11–13,22]. In an attempt to
reconcile the persistence of Antarctic coastal biota, one
hypothesis suggested by Convey & Lewis Smith [23] and
later tested by Fraser et al. [24] postulated that geothermal
activity provides a mechanism to maintain ice-free land near
coastal margins during glacial maxima. For geothermal activity
to provide a plausible mechanism maintaining ice-free coastal
refuges, it would require there to be sufficient sites through-
out Antarctica where regionally isolated endemic species
would have persisted across the LGM and into the present.
Fraser et al. [24], using a 100 km radius, showed that the sur-
vival of springtails (and other biota) occurs today in the
vicinity of some geothermal sites on the South Shetland
Islands and northern Antarctic Peninsula (figure 1; electronic
supplementary material, figure S1), which were also recently
suggested as playing a role in the persistence of springtails
across the LGM and prior [29]. However, these species have
much wider distributions, including the Antarctic Peninsula
and offshore islands [6]. Likewise, the proximity to geother-
mal sites of three (of eight) species in Victoria Land is at
least within 100 km (figure 1; electronic supplementary
material, figures S4 and S5). However, for springtails that
are not found outside Antarctica [6] and predominantly are
distributed along coastal margins, the vast majority do not
overlap with any geothermal site (figure 1; electronic sup-
plementary material, figures S1–S7). Geothermal activity
and other potential refugia (see [22]), while perhaps locally
important in a few specific cases, do not provide an expla-
nation for broader species survival in coastal regions at the
LGM or through previous glacial maxima.
(b) Nunatak refuge hypothesis
(i) Geological evidence
For the nunatak refuge hypothesis to be robust, we need to
explore if variations in ice sheet thickness across Antarctica
during glacial maxima allowed for widespread ice-free habi-
tats to be maintained. Modern ice sheet reconstructions based
on both onshore and offshore geological evidence, as well as
dating of these features shows that the ice sheet at the LGM
expanded onto the continental shelf and in coastal regions
it thickened by hundreds of metres [30,31], with the greatest
increases (greater than 1 km) observed in West Antarctica
[32,33]. Cosmogenic isotope dating is uniquely suited to Ant-
arctic environments [34] where geological dating of glacial
deposits on the flanks of Antarctic nunataks indicates in
many cases mountain slopes and some moraines remained
uncovered during the LGM [35–45]. Furthermore, cosmo-
genic isotope data from regions with extensive datasets
and/or consistent findings from multiple nuclides (see elec-
tronic supplementary material) indicate that persistent ice-
free conditions have likely existed since at least the LGM
and in many cases much longer [35,37,38,40,43,46–51]
(figure 2a; electronic supplementary material, figures S1–
S7). Most of these regions harbour short-range endemic
biota, including springtails (figure 2a). In some locations,
such as Victoria Land, Transantarctic Mountains and Dron-
ning Maud Land, there is evidence of ice-free conditions
persisting for millions of years [40,43,46]. In Victoria Land,
low-altitude moraines provide an additional habitat [4],
and such features may persist for thousands of years, particu-
larly when they are associated with long-standing nunataks
[53]. By contrast, despite evidence for ice-free nunataks
[33,38,40,49–51], springtails appear to be entirely absent
from marine-based sectors of the ice sheet (West Antarctica,
the Weddell Sea sector, and Wilkes and Aurora subglacial
basins) where the ice is grounded below sea level [54]
(figure 2a; electronic supplementary material, figures S3, S6
and S7). Such marine-based glaciers are known to be highly
dynamic, substantially expanding and contracting during
glacial-interglacial cycles (for example, in East Antarctica,
Marie Byrd Land and Ellsworth Land [33,55–57]) providing
limited long-term refuge for biota.
(ii) Biological evidence
For Antarctic biota, there is a growing body of molecular
evidence revealing long-term isolation and persistence of
short-range endemic species on the Antarctic continent
[7,58–64]. For springtails that are a dominant driver for biodi-
versity patterns across the Antarctic realm [25] (figure 1), data
show that these endemic species were likely present in
ice-free refuges for at least 15–12 Ma [17,46,58]. Endemism
is present in most sectors of the continent [6,7], and this
is supported by geological dating indicating long-term ice-
free conditions at sites (figure 2a; see also electronic
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supplementary material, file). So how does this explain species
presence today in coastal habitats? Clues to this remarkable sur-
vival come from well-known alpine and polar studies (e.g.
[65–68]). In alpine and polar regions, the greatest biodiversity
is found living in or near glacial forelands [65–71] and studies
have shown that biota occupy this glacial foreland ecosystem as it
‘shifts’adjacent to glacial margins as they expand or contract
[49,65,66,68,71,72]. This association adjacent to modern ice
has also been identified as one of the most biodiverse ecologi-
cal zones in Antarctica, despite the proximity of biota to a
much-expanded ice front during glacial maxima [69–71].
This scenario is illustrated in figure 2b, where, during glacial
maxima, species contract to small pockets of favourable habi-
tat (such as a glacial foreland ecosystem or analogous
moraine ecosystems) in terrain that protruded above or on
the modern ice sheet ( figure 2b). During an interglacial,
species disperse down slopes and valleys with the glacial
foreland that shifts with glacial margins as the ice retreats
(figure 2c), with dispersal also potentially being assisted by
meltwater (that is well known as a dispersal vector, e.g.
[73]) spreading biota towards coastal areas as they become
ice-free. Today, the presence of every known endemic spring-
tail species on the continent and central Antarctic Peninsula is
within 100 km of known LGM ice-free refuges indicated by
cosmogenic dating (figure 2a; electronic supplementary
material, figures S1–S7). The converse is also true; springtails
are absent from extensive ice-free regions (see figures 1 and
2a), likely because these regions do not contain terrain with
appropriate environments to serve as refuges when lowland
ice expanded during glacial maxima.
3. New directions
Our suggested framework provides the necessary way
forward to test predictions using an evidence-based approach.
We posit that Antarctica’s nunataks provide the most
likely refuge for the long-term survival of species, and
this explains the patterns of isolated short-range endemic
species we find today, where there is an increasing body
of evidence that none are shared between regions and
some regions are entirely lacking in species. The nunatak
refuge hypothesis also explains how species can be present
during interglacials in coastal areas adjacent to their
refugia—they do so by shifting up and down slopes
within glacial foreland ecosystems.
Going forward, cross-disciplinary collaborations can provide
a more complete picture of the evolution of Antarctic land-
scapes and the biota they harbour, but this requires
cosmogenic isotope dating specifically targeted towards iden-
tifying ice-free terrain at the LGM or older (e.g. [40,43,45]),
integrated with biological investigations that unequivocally
define connectivity versus isolation (e.g. [7,59,61,62,64,74,75])
to identify broader refugial sites. While we have well-synchro-
nized geochronology with springtail presence in ice-free
conditions in Victoria Land, the Transantarctic Mountains
and Dronning Maud Land (figure 2a), there are three specific
tests that can be carried out to further evaluate the nunatak
refuge hypothesis: (1) the Antarctic Peninsula has well-docu-
mented springtail records, but their provenance is uncertain
[6,29] and age control on LGM and earlier landscapes is
sparse [38]—further biological (using robust molecular
Figure 1. All terrain ice-free today shown as colour-shaded regions that represent the 16 currently recognized Antarctic Conservation Biodiversity Regions (ACBRs),
where those labelled in bold text contain springtail species that accounts for 82% of the total ACBR area [25]. Springtail species occur in two of the four volcanic
regions (within 100 km) highlighted by ellipses, where small (orange) and large (red) geothermal-specific sites are indicated (adapted from [24]). Blue shade around
Antarctica matches the current below sea level shown in figure 2a. Map created using Quantarctica [26] in QGIS ver. 3.22.7 [27] with our compiled data files [28].
3
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dating, e.g. [76]) and geochronology are required to evaluate
whether nunataks remained ice-free; (2) regions where geo-
chronology indicates that nunataks likely remained ice-free at
the LGM (for example in the Prince Charles Mountains;
[40,77]), but where, to date, evidence for springtail presence
remains equivocal albeit for recent environmental DNA signa-
tures from soils [78]—such biological signals warrant further
exploration and (3) greater focus on regions where the
geochronology is suggestive of ice-free nunataks at the LGM
[35,36,47–51] and biological investigations are limited or
yet to be done, for example, in Enderby Land, Ellsworth
Mountains and Transantarctic Mountains (figure 2a).
4. Conclusion
We have described a mechanism that allowed for springtails
to survive in isolation in refugia across the LGM in ice-free
habitats. Support for long-term continuity across Antarctic
ice-free terrain is provided by geological dating of glacial
deposits since the ice sheet first formed (approx. 34 Ma;
[79–81]). More recently, molecular data have revealed that
species found on the continent are a suite of unique locally
endemic survivors from at least the last 15–12 Ma [7,56,58]
when ice sheet thickening appears to have reached its maxi-
mum [17,46,82]. Together, these data highlight striking
(a) land elevation topography
(b)(c)glacial maxima
high-altitude refugia—extreme isolation low-altitude habitat—regional isolation
glacial minima
1000
m.a.s.l.
500
0
–500
Figure 2. (a) Distribution of springtail species shown as coloured dots with ellipses indicating short-range endemic species, overlaid on the land elevational topo-
graphy of Antarctica (blue = below sea level, green/yellow/brown = above sea level, see key in (b)). The presence of every known endemic springtail species on the
continent and central Antarctic Peninsula is within 100 km of LGM ice-free refuges indicated by cosmogenic dating (red diamonds) and these occur in six ACBRs,
while potential ice-free refugia without springtails occur in three ACBRs (orange diamonds) (compiled from https://www.ice-d.org/). (b) Survival of springtails
(colours represent isolated species) in ice-free terrain shift with glacial margins (foreland) as ice expands during glacial maxima. (c) Dispersal of springtails
during glacial minima (interglacial) shift with the glacial foreland as lower altitude ice-free land becomes available; biota disperse into low-elevation habitats
into coastal regions. Map and distance measurements performed using Quantarctica and land elevational topography created using BedMachine [52], in QGIS
with our compiled data files [28].
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levels of endemism on the continent revealing biodiversity
patterns in ice-free Antarctica that contributes significant
insights to the now widely accepted ‘Antarctic Continental
Biodiversity Regions’(ACBRs) [25] (figure 1).
Recent modelling of snow and ice melt indicates that cur-
rent ice-free regions in Antarctica may expand up to 25%
within the twenty-first century [83]. If these projections are cor-
rect, Antarctica will be changed forever with anthropogenic
climate change, and endemic springtails once regionally iso-
lated may no longer need refugia that have served them well
for millions of years. How these once isolated communities
cope with a vastly changing landscape with biotic interactions
not experienced for millions of years remains largely unknown.
Data accessibility. Supplementary files, including all data files we used in
QGIS for springtail records, geothermal and geochronological sites
shown in figures 1 and 2 are available from the Dryad Digital
Repository: https://doi.org/10.5061/dryad.zw3r228bx [28].
The data are provided in the electronic supplementary material
[84].
Authors’contributions. M.I.S.: conceptualization, data curation, formal
analysis, funding acquisition, investigation, methodology, project
administration, software, validation, visualization, writing—original
draft and writing—review and editing; A.N.M.: conceptualization,
data curation, funding acquisition, investigation, methodology, vali-
dation, writing—original draft and writing—review and editing.
All authors gave final approval for publication and agreed to be
held accountable for the work performed therein.
Conflict of interest declaration. We declare we have no competing interests.
Funding. This manuscript was supported in part from the Australian
Research Council (ARC) funding under the SRIEAS (grant agreement
no. SR200100005) (Securing Antarctica’s Environmental Future).
Acknowledgements. We thank Lawrence Bird for technical assistance
with QGIS and BedMachine, Fern Meppem for the figures, and
Greg Balco, Duanne White, Richard Jones, Byron Adams, Matthew
Ferris, Steven Cooper and four anonymous reviewers for valuable
discussions and comments.
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