Download The future of soil invertebrate communities in polar regions: different

Ecology Letters, (2013) 16: 409–419
doi: 10.1111/ele.12058
REVIEW AND
SYNTHESIS
Uffe N. Nielsen1,2 and Diana H.
Wall1
1
Natural Resource Ecology
Laboratory and Department of
Biology, Colorado State University,
Fort Collins, CO, 80523, USA
2
Hawkesbury Institute for the Envi-
ronment and School of Science and
Health, University of Western Sydney, Penrith, NSW, 2751, Australia
*Correspondence:
E-mail: [email protected]
The future of soil invertebrate communities in polar regions:
different climate change responses in the Arctic and Antarctic?
Abstract
The polar regions are experiencing rapid climate change with implications for terrestrial ecosystems. Here,
despite limited knowledge, we make some early predictions on soil invertebrate community responses to
predicted twenty-first century climate change. Geographic and environmental differences suggest that
climate change responses will differ between the Arctic and Antarctic. We predict significant, but different,
belowground community changes in both regions. This change will be driven mainly by vegetation type
changes in the Arctic, while communities in Antarctica will respond to climate amelioration directly and
indirectly through changes in microbial community composition and activity, and the development of, and/
or changes in, plant communities. Climate amelioration is likely to allow a greater influx of non-native species into both the Arctic and Antarctic promoting landscape scale biodiversity change. Non-native competitive species could, however, have negative effects on local biodiversity particularly in the Arctic where the
communities are already species rich. Species ranges will shift in both areas as the climate changes potentially posing a problem for endemic species in the Arctic where options for northward migration are limited. Greater soil biotic activity may move the Arctic towards a trajectory of being a substantial carbon
source, while Antarctica could become a carbon sink.
Keywords
Antarctic, Arctic, belowground, climate change, polar regions, precipitation, soil fauna, warming.
Ecology Letters (2013) 16: 409–419
INTRODUCTION
Arctic and Antarctic ecosystems are responding rapidly to recent
climate changes (e.g. Post et al. 2009; Turner et al. 2009a). For example, local warming in the Arctic has enhanced plant growth, caused a
shift in vegetation composition towards greater cover of shrubs, and
a northward migration of the tree line (Serreze et al. 2000; Callaghan
et al. 2011). Increased temperatures across maritime Antarctica have
similarly led to local population expansion of the two native vascular
plant species (Fowbert & Smith 1994), but also decreased survival
rates of Adelie penguins with confounding impacts on both terrestrial
and marine food webs (Ducklow et al. 2007). Global circulation models predict that twenty-first century climate changes will be greater,
both in terms of magnitude and speed of response, in the polar
regions (ACIA 2005; Turner et al. 2009a). As polar region ecosystems
appear to be highly sensitive to climate changes (Wall 2007) the
impacts may be particularly pronounced in the Arctic and Antarctic.
Terrestrial ecosystems in the polar regions are strongly influenced
by historical events, such as glaciations during ice ages, as well as
past and present environmental constraints. Ecosystem processes,
including primary productivity and nutrient cycling, and species
diversity are limited by low temperatures and/or limited water availability (Millennium Ecosystem Assessment 2005), and the biota have
adapted to the harsh conditions. For instance, most soil invertebrates
rely on life history traits that allow them to remain dormant throughout most of the year whilst taking advantage of short-term favorable
conditions (Convey 1996). Such survival strategies enhance the performance of the native biota under current climate conditions, but associated metabolic costs may impair growth rates and the organisms’
competitive ability under more favorable conditions. Many native species
are therefore at risk of being outcompeted by more competitive
species if the environment changes (Bergstrom & Chown 1999).
Understanding climate change response of belowground communities in the polar regions is of high importance. Soil organisms play
a vital role in ecosystem functioning (Nielsen et al. 2011a), and climate changes could cause a change in communities with potential
impacts on ecosystem processes (e.g. Wardle 2002). For instance,
while soil invertebrates may not play a large role in decomposition
of organic material under current environmental constraints (Wall
et al. 2008) their role may increase should the climate become more
suitable. One of the prominent concerns of climate change is the
potential loss of carbon (C) from permafrost. The northern circumpolar permafrost alone store about 1672 pg C or roughly twice the
amount of C found in the atmosphere (Tarnocai et al. 2009). An
increase in temperature could increase the efflux of C from Arctic
soils significantly, which would further accelerate climate change
locally and globally (Schuur et al. 2009). Arctic climate change
responses could thus have far reaching impacts. Furthermore, both
the Arctic and Antarctic host a range of unique ecosystem types
that support many endemic invertebrate species above and below
ground. Understanding climate change responses in the polar
regions may also help us predict future impacts in other ecosystem
types, such as those of increasing temperature and altered precipitation regimes around the globe, for example by allowing us to identify which mechanisms trigger climate change responses (Wall 2007;
Nielsen et al. 2012).
In this review we give an overview of the current knowledge of
climate change impacts on soil invertebrate communities in the
polar regions. Our goal is not to provide an exhaustive report of
previous findings but rather to highlight key information that may
© 2013 Blackwell Publishing Ltd/CNRS
410 U. N. Nielsen and D. H. Wall
help us predict future belowground climate change responses in the
Arctic and Antarctic. We aim not just to draw parallels in expected
belowground climate change responses between the two regions but
also emphasize why belowground communities may respond differently to climate changes based on geography and current environmental conditions. To accomplish this, we first provide a brief
description of the Arctic and the Antarctic as habitats including key
differences that may contribute to different responses of their
respective soil invertebrate communities to predicted climate
changes. We then outline observed and predicted climate changes
for the twenty-first century, and discuss how these changes may
directly and indirectly influence soil communities based on experimental and observational data as well as potential implications of
climate change impacts on C dynamics. We conclude the article
with some predictions on the future state of soil communities in
the polar regions and priorities for future research.
CHARACTERISTICS OF TERRESTRIAL ECOSYSTEMS IN THE POLAR
REGIONS
The Arctic is largely defined by a change in vegetation type from
forest to shrub and tundra, and we will follow the Millennium
Ecosystem Assessment (2005) definition of the Arctic: ‘all nonforested land north of 55° N′ for simplicity. The transition between
forest and tundra, the main ecosystem type of the Arctic, generally
coincides with average June temperatures of around 10 °C but varies widely in latitude between continents due to differences in geography and local weather patterns. The Arctic spans several
continents as well as a number of larger and smaller islands, and
covers approximately 12 million km2 of which roughly 2.5 million km2 is ice covered. The remaining area is defined as either barren (< 50% vegetation cover) or tundra (> 50% vegetation cover;
often referred to as the world’s largest wetland although not all is
strictly wetland), which cover about 3 and 5 million km2, respectively (Millennium Ecosystem Assessment 2005). The Arctic supports well developed and diverse vascular plant communities
(Callaghan et al. 2004), and is home to about 2000 species of soil
invertebrates (Chernov 1995). Moreover, the Arctic is home to a
range of migratory birds and large land mammals, including
humans, which have a substantial impact on local ecosystems and
contribute to the dispersal of flora and fauna (ACIA 2005).
By contrast, Antarctica is a mostly ice covered, isolated continent
and a few islands located south of 60° S. Of Antarctica’s 14 million km2 surface area only about 0.32% remains seasonally ice and
snow free (Ugolini & Bockheim 2008), and most of this is considered polar desert with no visible vegetation. Antarctica is colder and
drier than comparable latitudes in the Arctic (Convey 1996). The
terrestrial ecosystems within Antarctica are spatially isolated and
fragmented making it difficult for species to disperse between microhabitats (Huiskes et al. 2006), and the Southern Ocean functions
as a massive colonization barrier for terrestrial organisms (Convey
et al. 2008). With limited dispersal opportunities, the main vectors
for dispersal of flora and fauna, including potential invasive species,
to and within Antarctica are scientists and tourists (Chown et al.
2012). Antarctica’s plant communities are limited to two species of
vascular plants, approximately 111 mosses and 273 lichens (Ochyra
et al. 2008; Øvstedal & Smith 2009). Areas of maritime Antarctica
have well-developed plant communities in terms of ground cover
but in general primary productivity is very low.
© 2013 Blackwell Publishing Ltd/CNRS
Review and Synthesis
These differences indicate that the Antarctic biodiversity is more
constrained by present climatic conditions, dispersal limitations and
habitable land surface area than the Arctic (the key characteristics
of the Arctic and Antarctic are summarised in Table 1). An amelioration of any of these factors may therefore have disproportionally
large impacts on terrestrial ecosystems in Antarctica.
OBSERVED AND PREDICTED CLIMATE CHANGES IN THE POLAR
REGIONS
Here we give a brief overview of the climate changes observed in
the polar regions since modern records began and scenarios for the
twenty-first century because that is the scale at which most climate
models work. Fine-scale climate changes are inherently difficult to
model and beyond the scope of this paper; hence, we will focus on
larger scale patterns.
As noted earlier it is well documented that the climate in the polar
regions has changed since modern records began (e.g. ACIA 2005;
Millennium Ecosystem Assessment 2005; Turner et al. 2009a), and
that some of the largest increases in temperature measured on Earth
have been recorded in the Arctic and Antarctic. Two well known
examples illustrate this particularly well: temperatures at the Faraday/Vernadsky Station in maritime Antarctica increased by up to
0.56 °C per decade over the last half of the twentieth century
(Turner et al. 2005) and temperature increases of up to 1.19 °C per
decade between 1982 and 2005 were recorded in Greenland
(Comiso 2006). Climate changes are however somewhat less conspicuous at larger scales. For instance, rapid climate warming is
mostly limited to maritime Antarctica (e.g. along the Antarctic Peninsula and Scotia Arc; Turner et al. 2009a). There is little evidence
for any significant long term increases in temperature over continental Antarctica (Steig et al. 2009) although short-term (decadal) cooling trends were recorded in areas such as the McMurdo Dry Valleys
(MDVs) (Doran et al. 2002; Turner et al. 2005). However,
more recently there is evidence for the occurrence of extreme
warming events in the McMurdo Dry Valley Region of continental
Antarctica (e.g. Barrett et al. 2008a) as well as in the Arctic (Vincent
et al. 2009), which may pose particular problems for the soil invertebrates.
The Arctic has experienced a general increase in mean annual
temperature and precipitation, with trends being most pronounced
over the last few decades (Serreze et al. 2000; Comiso 2006). Satellite data indicate that the average temperature north of the Arctic
Circle increased by 0.72 0.1 °C per decade between 1982 and
2005 (Comiso 2006). However, while Greenland experienced an
increase of 1.19 0.2 °C dec 1, the increase over northern Eurasia
was 0.13 0.16 °C dec 1 in the same period (Comiso 2006). Some
regions even showed a cooling trend in the early part of last century, but it now appears that all of the Arctic is warming (Millennium Ecosystem Assessment 2005). Similarly, both local increases
and decreases in temperature and precipitation have been observed
in Antarctica (Turner et al. 2009a). Across the continent annual surface temperature increased by approximately 0.12 °C dec 1 between
1957 and 2006, but warming was more pronounced over West Antarctica (~0.17 °C dec 1) than East Antarctica (~0.10 °C dec 1;
Steig et al. 2009). Warming was particularly prominent on the Antarctic Peninsula (maritime Antarctica) over the last half of the twentieth century, in particular due to a great increase in winter
temperatures (Turner et al. 2005). Precipitation patterns in Antarc-
Review and Synthesis
Different polar region climate change impacts? 411
tica are not well documented and general patterns are thus not well
known (Turner et al. 2009a).
Climate models predict a more directional warming, and increased
precipitation, throughout the polar regions over the next century,
although the magnitude will show considerable regional variation. In
the Arctic, it is expected that the mean annual temperature will
increase by 4–7 °C and precipitation will increase 5–10% on average (but up to 35% in some high arctic regions; ACIA 2005). For
Antarctica, it is expected that precipitation rates will increase by
2.9 mm a 1 dec 1 and lead to an increase in snowfall of about
20% over the twenty-first century though most of this will fall during winter (Bracegirdle et al. 2008). Moreover, surface temperatures
will on average increase by about 0.34 °C dec 1 or about 3 °C in
total across the continent with the greatest temperature increases
occurring in the continental high altitude interior of East Antarctica
(Bracegirdle et al. 2008). The timescale of this increase is however
questionable in that the rate will depend on the amelioration of the
ozone hole that currently develops over Antarctica each spring. It
appears that this phenomenon has been causing local cooling over
interior continental Antarctica, and large increases in temperature
are unlikely here until the ozone hole phenomenon dissipates
(Turner et al. 2009b).
Finally, but perhaps more importantly, most models predict an
increase in the frequency of extreme events, i.e. heat waves, large
precipitation events, drought etc. in both the Arctic and Antarctic
(Tebaldi et al. 2006; Krinner et al. 2007; Steig et al. 2009). Despite
their short timeframe, extreme events can have disproportionally
large impacts by exposing biota, vegetation and ecosystems to
unusual climatic conditions. Such events may therefore be of greater
importance than long-term gradual changes in climate (Fig. 1; Jentsch & Beierkuhnlein 2008; Bokhorst et al. 2012; Nielsen et al.
2012). However, local changes in the frequency of such events are
inherently difficult to model and predict.
OBSERVED BELOWGROUND COMMUNITY RESPONSES TO
CLIMATE CHANGES
In this section we bring forward key findings that outline how climate change may impact on soil invertebrate communities of the
polar regions, information that is useful for understanding potential
future states. However, as will be apparent shortly, there is a dearth
of in-depth knowledge across taxa and many groups have received
little attention. We will focus on broad-scale responses but recognize that fine-scale responses may differ from those observed at larger scales. For instance, local soil moisture availability will depend
on topography and vegetation type in addition to the interaction
between changed precipitation and temperature (e.g. Peck et al.
2006).
Climate related impacts on soil invertebrates
Soil invertebrates of the polar regions are well adapted to variation
in climatic conditions at daily to annual time scales, and it has therefore been suggested that climate changes may not have a substantial
Extreme
ecological
response
Event size
Current
ecosystem
state
Ecological
resilience/
resistance
No change
in climate
Gradual change
in climate
Extreme
climatic event
Threshold
Duration
‘No’ biotic
changes
Adaptation by biota
Colonization by new species
Altered species interactions
Induced mortality
Altered soil properties
Changes in vegetation
Trophic cascades
No change in
ecosystem
state
Slow change in
ecosystem
state
Highly altered
ecosystem
state
Figure 1 Conceptual diagram showing potential ecosystem impacts related to climate change. Ecosystems experiencing no climate change are expected to show limited
short-term changes. Under gradual climate change biota will adapt to the new conditions while new species may colonize. This may cause changes in biotic interactions
and lead to a slow change in ecosystems over time. By contrast, an extreme event may cause highly altered ecosystem properties and significant mortality of organisms
above and below ground with potential trophic cascades and resulting in a highly altered ecosystem. The insert shows a hypothetical relationship between extreme
climatic events and ecological responses. The threshold indicates that extreme ecological responses occur when events deviate significantly from ‘normal’ conditions and/
or last for a long time.
© 2013 Blackwell Publishing Ltd/CNRS
412 U. N. Nielsen and D. H. Wall
Review and Synthesis
direct impact on these organisms (e.g. Peck et al. 2006). There is
however mounting evidence that climate change can impact soil
invertebrate communities in the polar regions. In this section we
discuss how warming and increased precipitation as well as other
climate change related factors, such as freeze-thaw cycles (FTCs),
depth of active layer and UV-B radiation, might influence soil invertebrate communities. Impacts more closely associated with microbial
and vegetation responses to climate change will be considered in
the next section.
A review of the current literature revealed a handful of studies
that report on long term trends of soil invertebrates associated with
observed climate changes and a limited number of studies that
report on the impacts of climate change manipulations. After
excluding articles that presented results covered elsewhere, we were
left with seven studies with 58 observations (Kennedy 1994; Sinclair
2002; Convey et al. 2002; Convey 2003; Bokhorst et al. 2008; Day
et al. 2009; Simmons et al. 2009) and five studies with 15 observations (Coulson et al. 1996; Reuss et al. 1999; Sjursen et al. 2005;
Dollery et al. 2006; Tsyganov et al. 2011) that report on soil invertebrate responses to experimental warming and/or water addition in
Antarctic and the Arctic, respectively. None of these studies report
on the response of soil invertebrates to water addition in the Arctic,
while three studies report on the impact of water addition in the
Antarctic with two of them further reporting on the interactive
effect of warming and water addition. The observed responses
(positive, neutral, negative) to experimental warming and/or water
additions of all soil invertebrate groups investigated are summarized
in Fig. 2 (mean effect sizes presented as ln response ratios of dominant groups are presented in Table S1). Care should be taken in
interpreting observed responses to climate change simulations as
such manipulations are often poor proxies for natural climate
change (Bokhorst et al. 2011), and high variability in soil invertebrate communities within ecosystems may obscure significant patterns under low replication. However, a general pattern emerges in
the climate change responses reported to date (Fig. 2). Across
groups of soil invertebrates and ecosystem types the response to climate warming is highly variable with negative, positive and no
responses observed, while water additions generally have no impact
(a)
or a positive influence on soil invertebrate communities. Closer
examination of the reported impacts indicate that most negative
warming responses are displayed by invertebrate groups sensitive to
low soil moistures (e.g. collembolans; Day et al. 2009) in ecosystems
where soil moisture availability may already be a limiting factor (e.g.
Coulsen et al. 1996; Simmons et al. 2009). Similarly, in both of the
studies that reported on the interaction between warming and water
addition, negative impacts of warming on nematodes (Simmons
et al. 2009) and collembolans (Day et al. 2009) were alleviated by
water addition.
Combining experimental data and long term records of soil invertebrate community responses to observed climate change allows us
to draw some conclusions on potential belowground impacts.
Experimental warming has been shown to increase nematode densities in the Arctic and maritime Antarctic (Convey 2003), while a
local cooling trend observed between 1986 and 2000 (Doran et al.
2002) had a negative impact on densities of the dominant nematode
Scottnema lindsayae in the MDVs (Barrett et al. 2008b). These results
suggest that warming will have a largely positive impact on local
nematode densities but may change community composition (e.g.
Nielsen et al. 2011b) although local responses may vary depending
on local soil characteristics (e.g. Simmons et al. 2009). Warming has
also been shown to increase mite densities in Polar ecosystems
(Kennedy 1994; Sjursen et al. 2005; Dollery et al. 2006), although
other studies found no response (Coulson et al. 1996; Webb et al.
1998) suggesting that the response is both habitat and group specific. For instance, Sjursen et al. (2005) found an increase in oribatid
mites and a decrease in mesostigmatid mites under increased temperatures, respectively, although the pattern was only significant in a
glade and a fellfield and not in a heath. By contrast, collembolans
often respond negatively to experimental warming in the Arctic
(Sjursen et al. 2005; Dollery et al. 2006) while both positive
(Kennedy 1994; Day et al. 2009) and negative responses have been
observed in maritime Antarctica (Bokhorst et al. 2008). The idiosyncratic responses of mites and collembolans to warming are supported by laboratory studies, which show that the mites are
generally more tolerant to high temperatures than collembolans
(Block et al. 1994; Hodkinson et al. 1996). Moreover, it should be
(b)
Figure 2 Summary of observed soil fauna group responses to warming and/or water addition in (a) the Antarctic and (b) the Arctic. Only studies that experimentally
increased mean temperature (i.e. not extreme events) and/or added water to plots are included. An observation is defined as the response of a distinct soil fauna group
(including Protista, Rotifera, Tardigrada, Nematoda, Collembola, Acari, Diptera) to climate change within a single site or habitat type, i.e. one study can have multiple
observations if it reports on responses of several soil fauna groups, ecosystems and/or sites (soil fauna responses were considered significant if P < 0.05). When multiple
studies were found to report results from the same experiment, only the most recent, longer-term, data were included.
© 2013 Blackwell Publishing Ltd/CNRS
Review and Synthesis
mentioned that there is often a change in community composition
under changed climate even if there were no overall response in
density of the group (e.g. Webb et al. 1998; Sjursen et al. 2005;
Dollery et al. 2006). There is very little information on the response
of other taxa for either the Arctic or the Antarctic. It is however
established that water stress is likely to impact groups that live in
moist to wet soils or on water films on soil aggregates (Convey et al.
2003), such as nematodes, rotifers, tardigrades, enchytraeids and
Diptera larvae (Hodkinson et al. 1999), and soft bodied animals
such as collembolans and prostigmatid mites as well as nymphs of
other mites (e.g. Day et al. 2009; Bokhorst et al. 2012). In short,
increased temperatures are likely to increase the abundance of soil
invertebrates in both the Arctic and the Antarctic as long as it is
not associated with a significant decrease in soil moisture availability, and it is furthermore likely to lead to a shift in the composition
of the belowground communities as soil organisms differ in their
ability to cope with climatic changes.
As mentioned earlier a ‘novelty’ of predicted climate change scenarios is the potential increase in the frequency and magnitude of
extreme events (ACIA 2005; Tebaldi et al. 2006; Krinner et al. 2007),
and there is evidence that such events may have a disproportionally
large impact on soil communities in the polar regions. For example, a
particularly warm summer increased soil moisture availability
throughout Taylor Valley (MDVs, Antarctica), which was evident for
several years, and caused a change in nematode community structure
and an increase in the abundance of a nematode species associated
with more moist soils (Barrett et al. 2008a). However, life in the polar
deserts of the MDVs is generally limited by water due to low temperatures, and increased temperatures may have opposite impacts elsewhere (Nielsen et al. 2012). Accordingly, an unusually hot and dry
Arctic summer caused high mortality of collembolans in an area with
relatively low precipitation (Coulson et al. 1996), indicating that
drought during hot summers may have negative impacts on belowground community composition in the Arctic. Similarly, the Ward
Hunt Island region in the Canadian high arctic experienced a hot
summer in 2008 (air temperatures up to 20.5 °C), and high temperatures had a significant influence on the landscape scale distribution of
key soil microhabitats with potential large-scale impacts on soil communities (Vincent et al. 2009). Such extreme events may therefore
lead to alternate ecosystem states with long lasting effects. However,
very few studies have experimentally assessed the impacts of extreme
events in the polar regions and we could learn a lot from such manipulations. For instance, recent work has shown that extreme winter
warming has a strong negative impact on microarthropod communities (e.g. Bokhorst et al. 2012). This work highlights potential negative
implications of increased winter temperatures or through decreased
snow cover which buffers temperature variability in the soil.
Other climate change related factors that may influence on
belowground communities include the frequency of FTCs, the
development and duration of ice layers, and increased UV radiation. It is likely that increased physiological stress associated with
FTCs could have a negative impact on soil invertebrates (Turner
et al. 2009a) but the impact will depend on the severity of the
FTCs. A study conducted in the sub-arctic found that the frequency of FTCs had a positive influence on the abundance of
collembolans and oribatid mites at the site where the increase in
FTCs were most pronounced (Konestabo et al. 2007). As the
authors hypothesize it is likely that an increase in time where the
soil is thawed in the plots with increased FTCs compared with
Different polar region climate change impacts? 413
continuously frozen may outweigh the negative effects of the
FTCs themselves. In particular, it needs to be considered that
most polar region biota are well equipped to survive and even
metabolize at temperatures well below the point of freezing, and
only severe frost may have any significant impact on their survival.
Moreover, the impact of increased variation in air temperature on
soil temperature depends strongly on local characteristics, and it
has for instance been shown that the temperature of Antarctic dry
soils are much more responsive to changes in air temperature than
moist or wet soils due to the buffering capacity of water (Lewis
Smith 1999). By contrast, the aforementioned study by Bokhorst
et al. (2012) indicated that an increase in FTCs negatively impacted
mite and collembolan densities. The authors ascribe the contrasting
results to a higher frequency of FTCs than that imposed by
Konestabo et al. (2007). Hence, the impact of FTCs on belowground communities will depend on frequency and how low the
realized soil temperatures are. Moreover, the susceptibility to FTCs
is group specific with laboratory studies suggesting that collembolans are less tolerant to FTCs than oribatid mites (Coulson et al.
2000). Changes in the frequency of FTCs may thus cause a shift
in soil communities.
Also altered depth and extent of snow cover, permafrost melt and
recession of glaciers may impact belowground communities. Snow
packs provide insulation against climate extremes, and soils underneath packs are typically warmer and show lesser variation in temperature (Walker et al. 1999). Snow packs also influence soil moisture
availability and soil chemistry, and through this have a large impact on
the distribution of soil biota (Gooseff et al. 2003) but impacts may be
both positive and negative depending on local conditions and more
knowledge is needed to make good predictions of future impacts.
Warming is expected to increase the depth of the active layer by 30–
40% as permafrost melts in the Northern Hemisphere by the end of
the twenty-first century (Stendel & Christensen 2002). This may
increase the area of high biological activity in the soils and enhance
soil biodiversity. However, the melt of permafrost may also have
severe impacts on soil communities through the formation of thermokarsts, a problem very evident in the Arctic (e.g. Osterkamp et al.
2000; Vogel et al. 2009). Also the large-scale retreat and melt of glaciers (Cook et al. 2005) will influence belowground communities. For
example, the water released from glaciers in arid regions, such as the
polar deserts of Antarctica, may enhance water availability and thereby
promote soil organisms, and glacial recessions may provide new areas
to colonize (Kennedy 1995; Kaufmann 2002).
Finally, it has been suggested that the increased UV radiation
associated with the formation of the ozone hole over Antarctica
could limit soil communities (Kennedy 1995). We find it questionable that this should have a large direct impact on growth and
survival rates of soil biota although there is some evidence that
UV exposure can influence belowground invertebrate communities
(e.g. Rinnan et al. 2005; Tosi et al. 2005). However, there may be
significant indirect effects through impacts on soil microbes and
plant communities. When plants are subjected to high UV irradiation they produce UV-B absorbing compounds which increase
their metabolic cost and contribute to a potential limitation of
aboveground biomass and plant height (Newsham & Robinson
2009). Moreover, incubation studies suggest that UV-B can inhibit
the growth of several Antarctic fungi in the surface layers of the
soil (Hughes et al. 2003). This could indirectly influence belowground communities by altering resource quality (i.e. plant palat© 2013 Blackwell Publishing Ltd/CNRS
414 U. N. Nielsen and D. H. Wall
ability) and quantity, and through this nutrient cycling (Convey
et al. 2002).
Vegetation and microbial driven climate change effects
There is a strong link between the plant community composition
aboveground and belowground communities (Wardle 2002), and climate change is likely to have strong effects on soil invertebrate
communities through changes in vegetation type. While the strength
of the link between above and below ground communities has not
been explicitly investigated in the polar regions there is some evidence that support such a link. For instance, as discussed in Nielsen
et al. (2011b) Antarctic soils with vegetation harbor substantially
greater abundances of soil fauna and support different communities
than does bare ground. It is also apparent that soil fauna communities differ between vegetation types in the Arctic (e.g. Coulson et al.
2003).
Vegetation composition responses to recent climate changes are
widespread in the Arctic (Callaghan et al. 2011) and the Antarctic
(e.g. Fowbert & Smith 1994; Parnikoza et al. 2009). For example, in
the Arctic, soil temperature directs changes in the functional composition of the vegetation (Brooker & van der Wal 2003) and
increasing temperatures generally enhance net and gross primary
production (Marchand et al. 2004). In maritime Antarctica, the
observed local range expansion of vascular plants as well as bryophytes (Fowbert & Smith 1994) appears to be tightly linked to local
temperature trends (Parnikoza et al. 2009). Climate warming is also
expected to have a positive influence on net carbon assimilation in
Antarctica, as the temperature is generally lower than the temperature required for optimum carbon assimilation shown by native
plants (Kennedy 1995). Moreover, a warmer and wetter climate is
likely to enhance successful colonization events as well as germination of plants residing in the local soil seed bank (Lewis Smith &
Ochyra 2006). Hence, considering the current low biomass, productivity and diversity of plants in Antarctica, warming and increased
precipitation is very likely to lead to the development of more
favorable habitats for soil organisms thus enhancing the complexity
of the soil food webs in Antarctica.
Similarly, climate change responses of the microbial communities
could have cascading impacts on the soil invertebrate communities,
particularly in the polar deserts dominated by vast expanses of bare
ground where the soil invertebrates rely almost solely on the microbial communities for resources (e.g. Nielsen et al. 2011b). There is
some evidence that microbial communities respond to imposed
long-term climate changes (Rinnan et al. 2007; Timling & Taylor
2012), but whether directional responses exist is still unknown.
However, several studies have found that warming tends to increase
nutrient availability and enhance decomposition rates (e.g. Schmidt
et al. 2002; Hill & Henry 2011), which is likely to positively impact
invertebrate communities. For example, Rinnan et al. (2007) speculates that limited microbial biomass responses to climate change
manipulations could be due to increased grazing by soil invertebrates. This is supported by the large increase in nematode populations observed in the plots (Reuss et al. 1999). Hence, greater
microbial activity may contribute to trophic cascades. By contrast, it
seems that a warmer and wetter climate will have a more consistent
impact on microbial communities in Antarctic ecosystems. A recent
study used open top chambers to investigate the impacts of warming on microbial communities across a latitudinal gradient in Ant© 2013 Blackwell Publishing Ltd/CNRS
Review and Synthesis
arctica (Yergeau et al. 2012). The authors found that the soil
microbial communities show consistent responses to short-term climate warming with an increase in both bacterial (under vegetation
only) and fungal abundances, and changes in the bacterial community composition likely reflecting greater nutrient availability (Yergeau et al. 2012). Increased microbial biomass would likely be able
to support more soil invertebrates, while changes in the microbial
community composition may impact on the species composition of
soil invertebrates.
Implications of belowground community responses to climate
change for C dynamics
The climate change impacts on soil biota in the polar regions may
have implications for global C dynamics through enhanced rates of
decomposition and faster turnover of nutrients. While this is mainly
driven by enhanced microbial activity, it appears likely that the role of
soil invertebrates in decomposition processes, which is currently limited mainly due to climatic constrains of biological activity (e.g. Wall
et al. 2008), will increase as the climate becomes more favorable. This
is a concern considering the potential positive feedback on future climate changes (Chapin et al. 2005). Already it appears that permafrost
melt and greater biological activity associated with climate warming
during the late 20th century have caused the Arctic as a whole to
switch from being a C sink to a C source (e.g. Schuur et al. 2009; Jahn
et al. 2010). However, there is still large uncertainty about the scale of
C efflux as warming has been found to both increase (Biasi et al.
2008), decrease (Sj€
ogersten et al. 2008) or have no impact on soil C
efflux locally (Lamb et al. 2011). These idiosyncratic responses appear
to be related to differences in soil moisture. For example, a study
explored soil respiration rates to warming in the Arctic, and found
that dry tundra is more responsive to climate warming than moist
and wet tundra (Oberbauer et al. 2007). The authors hypothesize that
the response of respiration rates in wet and moist tundra to climate
warming are dampened due to higher water tables and soil moisture
contents (Oberbauer et al. 2007). Similarly, a recent study suggests
that Arctic wetland ecosystems generally act as C sinks rather than C
sources (Lund et al. 2010). Hence, it is likely that warming will have
the most pronounced impact on C stocks in drier habitats initially
and may only later, if at all, impact C stocks in moist to wet habitats.
Moreover, a study of old C release from Arctic soils showed that the
release of old C increased with time since permafrost thaw because
initially the increase in C efflux is offset by increased uptake of C by
plants (Schuur et al. 2009). This suggests that short-term measurements of soil respiration are unlikely to capture the true extent of C
release, and we might therefore have underestimated the potential
impacts of Arctic climate warming. By contrast, the minimal organic
content of Antarctic soils suggests that these soils are likely to
become a C sink under a warmer and wetter climate. Indeed, a recent
study found that warming had a positive effect on aboveground biomass as well as C stocks of soils dominated by vascular plants in maritime Antarctica (Day et al. 2008).
THE FUTURE STATE OF BELOWGROUND COMMUNITIES IN THE
POLAR REGIONS
Based on current knowledge described above we have outlined
some broad predictions of future climate change responses of
belowground communities, but there are two important aspects of
Review and Synthesis
Different polar region climate change impacts? 415
Table 1 Key geographic and environmental characteristics of the Antarctic and Arctic
The Antarctic
Landscape
Vegetation
Soil invertebrates
Other characteristics
The Arctic
~14 million km of which only
ca. 0.32% is seasonally ice and snow free*
Continental Antarctica is a polar desert
with no to sparse vegetation. Some areas
in maritime Antarctica more vegetated†
Two native vascular plant species, both
restricted to maritime Antarctica.
Approximately 111 species of moss
and 273 lichens‡,§
Some 520 terrestrial invertebrates of
which about 170 are endemic**,††, but
likely underestimated
Geographically isolated and the Southern
ocean function as a large-scale dispersal barrier
Habitable areas very fragmented within the continent
Ozone-hole currently limits warming in interior
continental Antarctica¶¶ and high UV radiation
may be damaging to flora and fauna***
2
~12 million km2 of which 2.5 million
km2 is ice covered†
~3 million km2 is polar desert or sparsely
vegetated (< 50% vegetation cover) while the
remaining ~5.1 million km2 is tundra (> 50% vegetation cover)†
Some 5900 species including 1800 vascular plant species¶
Over 2000 species of soil invertebrates incl. some 700
mites, 400 springtails, 500 nematodes and 70 oligochaetes‡‡,§§
Less isolated but some dispersal limitation between
continents and islands
Habitable areas larger, widespread and more connected
Climate gentler than comparable latitudes in the Antarctic†††
*Ugolini & Bockheim (2008).
†Millennium Ecosystem Assessment (2005).
‡Ochyra et al. (2008).
§Øvstedal and Smith.
¶Callaghan et al. (2004).
**Adams et al. (2006).
††Convey (2008).
‡‡Danks (1990).
§§Chernov (1995).
¶¶Turner et al. (2009b).
***Kennedy (1995).
†††Convey (1996).
the observed and predicted climate changes that need consideration
before we proceed. First, the rates of change, both that observed
and those predicted for the twenty-first century, are high compared
to most known climate changes in Earth’s geological history. It has
however been suggested that very rapid increases in temperature
occurred at the end of the last glacial period (up to 10 °C at midto high-latitudes over as little as 3–5 years around 14 700 years BP
and similar changes over roughly 60 years around 11 600 years BP;
Steffensen et al. 2008). These abrupt temperature increases led to a
complete turnover of plant species locally within Europe and North
America. Despite the shift in plant community composition the
event appeared to have no significant impact on overall biodiversity,
i.e. species ranges shifted but the climate change did not cause
large-scale species extinctions (Willis et al. 2010). One major difference between these past climate change events and those predicted
for the twenty-first century in the polar regions suggests that current climate changes could have a different outcome. While the
retreat of the ice sheet after the last glaciation would allow northward migration and range expansion of ecosystems and associated
species, and therefore not cause large-scale extinctions, this is not
possible today at least for some Arctic ecosystems. In particular, a
northward shift in range of the Arctic tundra may be geographically
restricted (i.e. there is no new land to colonize; Fig. 2). Thus, temperature increases are likely to decrease the total area of tundra and
likely the number of species found therein. In contrast, this is much
less likely in Antarctica where large landmasses are currently snow
or ice covered and new land may become available as glaciers and
snow packs retract, retreat southward or to higher elevation (Fig. 3).
Secondly, the predicted climate changes include an increase in frequency of extreme events (Tebaldi et al. 2006; Krinner et al. 2007;
Turner et al. 2009a). Such events may have disproportionally large
impacts on ecosystems by subjecting them to conditions beyond
their climatic thresholds and result in alternate ecosystem states (e.g.
Jentsch & Beierkuhnlein 2008; Nielsen et al. 2012). In short, the
predicted climate changes may have greater biotic impacts than
those observed in the past.
Community composition
We predict a general change in the composition of soil invertebrate
communities throughout both the Arctic and Antarctic. However,
we expect that belowground invertebrate communities will respond
most strongly to changes in the microbial community composition
and to vegetation type changes caused by climate changes in the
Arctic. In Antarctica, the belowground invertebrate communities
will respond positively to increased temperatures and water availability through stress release, which will allow greater growth rates
and lower induced mortality. Furthermore, we expect to see an
overall increase in the abundance and biomass of soil invertebrates
as microbial communities become more active and plant communities expand, become more complex and show greater primary productivity. This is also likely to promote the diversity and complexity
of Antarctic soil food webs and create opportunities for stronger
biotic interactions. By contrast, climate changes may not have a significant impact on overall biomass in the Arctic where the communities are more complex, although we do predict a shift in the soil
© 2013 Blackwell Publishing Ltd/CNRS
416 U. N. Nielsen and D. H. Wall
Review and Synthesis
The Arctic
Carbon pools and fluxes
North
Forest
Expansion north
Tundra
Shift north
Expansion/Contraction?
Polar desert
Atmosphere (↑)
Shift north
Contraction
Increased release
of CO2 through
decomposition
Glaciers
Contraction
Ocean
The Antarctic
Soil (↓)
Increased
uptake of CO2
by plants
Increased carbon input
from plants
Vegetation (↑)
South
Plant dominated
Expansion south
Polar desert
Shift south
Expansion
Atmosphere (↓)
Glaciers
Contraction south/to higher elevations
Limited release
of CO2 due to
low organic
content of soils
Increased
uptake of CO2
by plants
Vegetation (↑)
Soil (↑)
Increased carbon input
from plants
Figure 3 Conceptual diagram of polar region landscape scale responses to a warmer and wetter climate (not to scale; see text for details). Arctic tundra, barrens and polar
desert will shift northward and may decrease in area due to encroachment of woodlands. Antarctic vegetation will expand southward as glaciers and snowpacks retreat. In
the Arctic, higher temperatures will likely increase decomposition rates, potentially causing increased efflux of C. However, the net release of C will depend on the
balance between increased decomposition and increased uptake by vegetation particularly as the cover of shrubs and trees increase. More C is likely to be incorporated
into the vegetation and soil organic matter pools in Antarctica, but this will be limited by climatic constraints.
food web structure as organisms such as mites and collembolans
differ in their capacity to tolerate increased temperature and associated greater or lower soil moisture availability.
Finally, while it is difficult to foresee the impact of a potential
increase in the frequency of extreme events, such events are likely
to have disproportionally large impacts on the distribution of species and local communities and the effects may be positive or negative depending on local conditions. For example, in the Antarctic
MDVs, heat waves tend to increase soil moisture availability and
through this could promote the development of (by local standards)
diverse soil communities and provide dispersal opportunities for soil
organisms through the development of streams (e.g. Nielsen et al.
2012). Hence, the positive impacts may outweigh the negative
impacts here. Still, extreme events are likely to have a negative
impact on soil invertebrates on more broad scales. For instance, the
development of thermokarsts and increased wild fires as observed
recently in the Arctic (Mack et al. 2011) could have substantial
impacts on soil communities beyond the initial disturbance impacts
through loss of habitat and nutrients.
Diversity
While the species diversity of soil organisms is unlikely to increase
significantly in the Arctic ecosystems that already display rather high
diversity (e.g. Wu et al. 2011), a warmer and wetter Antarctica would
be favorable for range expansion of the existing species and promote successful colonization events by new species (e.g. Turner
© 2013 Blackwell Publishing Ltd/CNRS
et al. 2009a; Convey 2011; Nielsen et al. 2011b). Furthermore, glacial
recession and increased soil formation processes are likely to provide new habitable areas (Fig. 3). Hence, the diversity of soil invertebrates is likely to increase in Antarctica under the predicted
climate changes. However, increasing temperatures may also promote the colonization of invasive species, both in the Arctic and
the Antarctic. Considering the low diversity of Antarctic ecosystems
this may have substantial impacts on the communities (i.e. the
native species may be eliminated from the communities through
competition but they will be substituted by other new species), but
the effect at large scales is a net increase in species diversity. By
contrast, the connectivity and greater diversity currently observed in
Arctic ecosystems suggests that competitive invasive species could
have a negative impact on species diversity locally, and potentially
even at larger scales. Moreover, limited northward range shift of
ecosystems may have substantial impacts on overall species diversity
of Arctic communities, which is not of great concern for Antarctic
biota. Hence, we predict an overall increase in species diversity in
Antarctic ecosystems both at fine and broad scales although some
native species such as the nematode S. lindsayae may experience a
reduction in their distribution. It seems likely that climate change
will have little impact on species diversity in the Arctic in the short
term, but that displacement of native ecosystems through encroachment by other ecosystem types (i.e. woodland and forests etc.;
Fig. 2) could lead to species extinctions in the longer term. Ultimately, the impact will depend on the balance between species
introduction and extinction.
Review and Synthesis
Soil processes
Turnover rates and primary productivity are likely to go up in
both the Arctic and the Antarctic as climate conditions become
more favorable. A warmer and wetter climate would promote
greater activity of soil invertebrates and the microbial community.
The role of soil invertebrates in nutrient cycling would increase
through their participation in decomposition processes and
increased microbial grazing (e.g. Wall et al. 2008) with potential
ecosystem effects. In particular, the accelerated rate of decomposition is likely to lead to a net efflux of C in the Arctic, which
could become a substantial source of C with potential implications
for future climate changes through positive feedbacks (Fig. 3).
However, we stress that more data are needed to resolve this
question. In contrast, we expect that the development of more
extensive microbial, soil invertebrate and plant biomass will lead to
an accumulation of organic matter in soils throughout most of
Antarctica (Fig. 3). Antarctic ecosystems may thus become a C
sink during the expansion and following succession of the aboveand belowground communities, although this is unlikely to offset
the increase in C release from the Arctic.
RESEARCH PRIORITIES
It is evident that climate change is likely to impact significantly on
belowground communities and ecosystem functioning in the Arctic
and Antarctic, although responses will depend on the current state
of the ecosystems. However, our literature review reveals a scarcity
of information on the impact of climate change on soil invertebrates in the polar regions. Furthermore, as highlighted by Convey
(2011), predicting climate change responses is limited by our lack of
baseline knowledge of polar region biota. An increased use of
molecular approaches in conjunction with more ‘old-fashioned’
methods would enable us to make considerable progress in cataloguing the diversity and distribution of soil organisms, and their
role in ecosystem functioning.
Our poor understanding of climate change impacts on belowground communities in the polar region could with relative ease be
addressed by upgrading existing climate manipulation facilities to
incorporate both warming and precipitation manipulations and then
supplement these with sites so as to cover an environmental gradient. As noted previously by Wall et al. (2011) it is essential that such
experimental facilities take a more holistic approach to responses
induced by climate change as well as other human induced changes
and document both changes in processes and communities of key
organisms above- and belowground across ecosystem types to fully
understand the mechanisms that underpin observed responses.
These climate change facilities should be complemented by long
term monitoring stations that record natural variation in communities over time and facilitate greater data sharing (e.g. Wall et al.
2011). This would not only increase our knowledge on polar region
ecosystems considerably but also help substantiate fundamental ecological principles.
ACKNOWLEDGEMENTS
The US National Science Foundation (OPP 0423595 and 1115245)
supported this work which is a contribution to the McMurdo
Different polar region climate change impacts? 417
LTER. We thank the editor and the three anonymous reviewers for
their helpful comments.
STATEMENT OF AUTHORSHIP
UN and DW contributed with conceptual ideas. UN undertook the
literature review and wrote the paper with significant contribution
from DW.
REFERENCES
ACIA. (2005). Arctic Climate Impact Assessment. Cambridge University Press,
Cambridge.
Adams, B.J., Bardgett, R.D., Ayres, E., Wall, D.H., Aislabie, J., Bamforth, S.,
et al. (2006). Diversity and distribution of Victoria Land biota. Soil Biol.
Biochem., 38, 3003–3018.
Barrett, J.E., Virginia, R.A., Wall, D.H., Doran, P.T., Fountain, A.G., Welch,
K.A., et al. (2008a). Persistent effects of a discrete climate event on a polar
desert ecosystem. Glob. Change Biol., 14, 2249–2261.
Barrett, J.E., Virginia, R.A., Wall, D.H. & Adams, B.J. (2008b). Decline in a
dominant invertebrate species contributes to altered carbon cycling in a lowdiversity ecosystem. Glob. Change Biol., 14, 1734–1744.
Bergstrom, D.M. & Chown, S.L. (1999). Life at the front: history, ecology and
change on southern ocean islands. Trends Ecol. Evol., 14, 472–477.
Biasi, C., Meyer, H., Rusalimova, O., H€ammerle, R., Kaiser, C., Baranyi, C., et al.
(2008). Initial effects of experimental warming on carbon exchange rates, plant
growth and microbial dynamics of a lichen-rich dwarf tundra in Siberia. Plant
Soil, 307, 191–205.
Block, W., Webb, N.R., Coulson, S.J. & Hodkinson, I.D. (1994). Thermal
adaptation in a high arctic collembolan Onychiurus arcticus. J. Insect Physiol., 40,
715–722.
Bokhorst, S., Huiskes, A., Convey, P., van Bodegom, P.M. & Aerts, R. (2008).
Climate change effects on soil arthropod communities from the Falkland
Islands and the Maritime Antarctic. Soil Biol. Biochem., 40, 1547–1556.
Bokhorst, S., Huiskes, A., Convey, P., Sinclair, B.J., Lebouvier, M., Van der
Vijver, B., et al. (2011). Microclimate impacts of passive warming methods
in Antarctica: implication for climate change studies. Polar Biol., 34, 1421–
1435.
Bokhorst, S., Phoenix, G.K., Bjerke, J.W., Callaghan, T.V., Huyer-Brugman, F. &
Berg, M.P. (2012). Extreme winter warming events more negatively impact
small rather than large soil fauna: shift in community composition explained
by traits not taxa. Glob. Change Biol., 18, 1152–1162.
Bracegirdle, T.J., Connolley, W.M. & Turner, J. (2008). Antarctic climate change
over the twenty-first century. J. Geophys. Res., 133, D03103. DOI: 10.1029/
2007JD008933.
Brooker, R. & van der Wal, R. (2003). Can soil temperature direct the
composition of high arctic plant communities? J. Veg. Sci., 14, 535–542.
Callaghan, T.V., Bj€orn, L.O., Chernov, Y., Chapin, T., Christensen, T.R.,
Huntley, B., et al. (2004). Biodiversity, distribution and adaptations of Arctic
species in the context of environmental change. Ambio, 33, 404–417.
Callaghan, T.V., Tweedie, C.E., Akerman, J., Andrews, C., Bergstedt, J., Butler,
M.G., et al. (2011). Multidecadal changes in tundra environments and
ecosystems: synthesis of the International Polar Year-Back to the Future
Project (IPY-BTF). Ambio, 40, 705–716.
Chapin, F.S. III, Sturm, M., Serreze, M.C., McFadden, J.P., Key, J.R., Lloyd,
A.H., et al. (2005). Role of land-surface changes in Arctic summer warming.
Science, 310, 657–660.
Chernov, Y.I. (1995). Diversity of the Arctic terrestrial fauna. In: Arctic and
Alpine Biodiversity: Patterns, Causes and Ecosystems Consequences (eds Chapin, S.F.
III & K€orner, C.). Springer-Verlag, Berlin, pp. 81–95.
Chown, S.L., Huiskes, A.H.L., Gremmen, N.J.M., Lee, J.E., Terauds, A., Crosbie,
K., et al. (2012). Continent-wide risk assessment for the establishment of
nonindigenous species in Antarctica. Proc. Natl. Acad. Sci. USA, 109, 4938–4943.
Comiso, J.C. (2006). Arctic warming signals from satellite observations. Weather,
61, 70–76.
© 2013 Blackwell Publishing Ltd/CNRS
418 U. N. Nielsen and D. H. Wall
Convey, P. (1996). Overwintering strategies of terrestrial invertebrates from
Antarctica – the significance of flexibility in extremely seasonal environments.
Eur. J. Entomol., 93, 489–505.
Convey, P. (2003). Soil faunal community response to environmental
manipulation on Alexander Island, southern maritime Antarctic. In: Antarctic
Biology in a Global Context (eds Huiskes, A.H.L., Gieskes, W.W.C., Rozema, J.,
Schorno, R.M.L., van der Vies, S.M. & Wolff, W.J.). Backhuys Publishers,
Leiden, the Netherlands, pp. 74–78.
Convey, P. (2008). Antarctic ecosystems. In: Encyclopedia of biodiversity (ed Levin,
S.A.). Vol. 1, 2nd edn. Academic Press, San Diego.
Convey, P. (2011). Antarctic terrestrial biodiversity in a changing world. Polar
Biol., 34, 1629–1641.
Convey, P., Pugh, P.J.A., Jackson, C., Murray, A.W., Ruthland, C.T., Xiong, F.S.,
et al. (2002). Responses of Antarctic terrestrial microarthropods to long-term
climate manipulations. Ecology, 83, 3130–3140.
Convey, P., Block, W. & Peat, H.J. (2003). Soil arthropods as indicators of
water stress in Antarctic terrestrial habitats? Glob. Change Biol., 9, 1718–
1730.
Convey, P., Gibson, J.E.A., Hillenbrand, C.-D., Hodgson, D.A., Pugh, P.J.A.,
Smellie, J.L., et al. (2008). Antarctic terrestrial life – challenging the history of
the frozen continent? Biol. Rev., 83, 103–117.
Cook, A.J., Fox, A.J., Vaughan, D.G. & Ferrigno, J.G. (2005). Retreating
glacier fronts on the Antarctic Peninsula over the past half-century. Science,
308, 541–544.
Coulson, S.J., Hodkinson, I.D., Webb, N.R., Block, W., Bale, J.S., Strathdee,
A.T., et al. (1996). Effects of experimental temperature elevation on higharctic soil microarthropod populations. Polar Biol., 16, 147–153.
Coulson, S.J., Leinaas, H.P., Ims, R.A. & Sovik, G. (2000). Experimental
manipulation of the winter surface ice layer: the effects on a high Arctic soil
microarthropod community. Ecography, 23, 299–306.
Coulson, S.J., Hodkinson, I.D. & Webb, N.R. (2003). Microscale distribution
patterns in high Arctic soil microarthropod communities: the influence of
plant species within the vegetation mosaic. Ecography, 26, 801–809.
Danks, H.V. (1990). Arctic insects: instructive diversity. In: Canada’s missing
dimension: science and history in the Canadian arctic islands (ed Harrington, C.R.).
Canadian Museum of Nature, Ottawa, pp. 444–470.
Day, T.A., Ruhland, C.T. & Xiong, F.S. (2008). Warming increases aboveground
plant biomass and C stocks in vascular-plant-dominated Antarctic tundra.
Glob. Change Biol., 14, 1827–1843.
Day, T.A., Ruhland, C.T., Strauss, S.L., Park, J.-H., Krieg, M.L., Krna, M.A.,
et al. (2009). Response of plants and the dominant microarthropod, Cryptopygus
antarcticus, to warming and contrasting precipitation regimes in Antarctic
tundra. Glob. Change Biol., 15, 1640–1651.
Dollery, R., Hodkinson, I.D. & J
onsdottir, I.S. (2006). Impact of warming and
timing of snow melt on soil microarthropod assemblages associated with
Dryas-dominated plant communities on Svalbard. Ecography, 29, 111–119.
Doran, P.T., Priscu, J.C., Lyons, W.B., Walsh, J.E., Fountain, A.G., McKnight,
D.M., et al. (2002). Antarctic climate cooling and terrestrial ecosystem
response. Nature, 415, 517–520.
Ducklow, H.W., Baker, K., Martinson, D.G., Quetin, L.B., Ross, R.M., Smith,
R.C., et al. (2007). Marine pelagic ecosystems: the West Antarctic Peninsula.
Philos. Trans. R. Soc. Lond. B Biol. Sci., 362, 67–94.
Fowbert, J.A. & Smith, R.I.L. (1994). Rapid population increases in native
vascular plants in the Argentine islands, Antarctic Peninsula. Arct. Alp. Res.,
26, 290–296.
Gooseff, M.N., Barrett, J.E., Doran, P.T., Fountain, A.G., Lyons, W.B., Parsons,
A.N., et al. (2003). Snowpack influence on soil biogeochemical processes and
invertebrate distribution in the McMurdo Dry Valleys, Antarctica. Arct.
Antarct. Alp. Res., 35, 91–99.
Hill, G.B. & Henry, G.H.R. (2011). Responses of High Arctic wet sedge tundra
to climate warming since 1980. Glob. Change Biol., 17, 276–287.
Hodkinson, I.D., Coulson, S.J., Webb, N.R. & Block, W. (1996). Can Arctic
soil microarthropods survive elevated summer temperatures? Funct. Ecol., 10,
314–321.
Hodkinson, I.D., Webb, N.R., Bale, J.S. & Block, W. (1999). Hydrology, water
availability and tundra ecosystem function in a changing climate: the need for
a closer integration of ideas? Glob. Change Biol., 5, 359–369.
© 2013 Blackwell Publishing Ltd/CNRS
Review and Synthesis
Hughes, K.A., Lawley, B. & Newsham, K.K. (2003). Solar UV-B radiation
inhibits the growth of Antarctic terrestrial fungi. Appl. Environ. Microbiol., 69,
1488. DOI: 10.1128/AEM.69.3.1488-1491.2003.
Huiskes, A., Convey, P. & Bergstrom, D.M. (2006). Trends in Antarctic
terrestrial and limnetic ecosystems. In: Trends in Antarctic Terrestrial and Limnetic
Ecosystems: Antarctica as a Global Indicator (eds Bergstrom, D.M., Convey, P. &
Huiskes, A.H.L.). Springer, Dordrecht, Germany, pp. 1–13.
Jahn, M., Sachs, T., Mansfeldt, T. & Overesch, M. (2010). Global climate change
and its impact on the terrestrial Arctic carbon cycle with special regards to
ecosystem components and the greenhouse-gas balance. J. Plant Nutr. Soil Sci.,
173, 627–643.
Jentsch, A. & Beierkuhnlein, C. (2008). Research frontiers in climate change:
effects of extreme meteorological events on ecosystems. C. R. Geosci., 340,
621–628.
Kaufmann, R. (2002). Glacier foreland colonisation: distinguishing between
short-term and long-term effects of climate change. Oecologia, 130, 470–
475.
Kennedy, A.D. (1994). Simulated climate change: a field manipulation study of
polar microarthropod community response to global warming. Ecography, 17,
131–140.
Kennedy, A.D. (1995). Antarctic terrestrial ecosystem response to global
environmental change. Annu. Rev. Ecol. Syst., 26, 683–704.
Konestabo, H.S., Michelsen, A. & Holmstrup, M. (2007). Responses of springtail
and mite populations to prolonged periods of soil freeze-thaw cycles in a subarctic ecosystem. Appl. Soil Ecol., 36, 136–146.
Krinner, G., Magand, O., Simmonds, I., Genthon, C. & Dufresne, J.-L. (2007).
Simulated precipitation and surface mass balance at the end of the twentieth
and twenty-first centuries. Clim. Dyn., 28, 215–230.
Lamb, E.G., Han, S., Lanoil, B.D., Henry, G.H.R., Brummell, M.E., Banerjee, S.,
et al. (2011). A high Arctic soil ecosystem resists long-term environmental
manipulations. Glob. Change Biol., 17, 3187–3194.
Lewis Smith, R.I. (1999). Biological and environmental characteristics of three
cosmopolitan mosses dominant in continental Antarctica. J. Veg. Sci., 10,
231–242.
Lewis Smith, R.I. & Ochyra, R. (2006). High altitude Antarctic soil propagule
bank yields an exotic moss and potential colonist. J. Hattori Bot. Lab., 100,
325–331.
Lund, M., Lafleur, P.M., Roulet, N.T., Lindroth, A., Christensen, T.R., Aurela,
M., et al. (2010). Variability in exchange of CO2 across 12 northern peatland
and tundra sites. Glob. Change Biol., 16, 2436–2448.
Mack, M.C., Bret-Harte, M.S., Hollingsworth, T.N., Jandt, R.R., Schuur, E.A.G.,
Shaver, G.R., et al. (2011). Carbon loss from an unprecedented Arctic tundra
wildfire. Nature, 475, 489–492.
Marchand, F.L., Nijs, I., de Boeck, H.J., Kockelbergh, F., Mertens, S. & Beyens,
L. (2004). Increased turnover but little change in the carbon balance of higharctic tundra exposed to whole growing season warming. Arct. Antarct. Alp.
Res., 36, 298–307.
Millennium Ecosystem Assessment. (2005). Ecosystems and Human Well-being:
current State and Trends. Findings of the Condition and Trends Working Group. Vol. 1.
Island Press, Washington DC, USA.
Newsham, K.K. & Robinson, S.A. (2009). Responses of plants in polar regions
to UVB exposure: a meta-analysis. Glob. Change Biol., 15, 2574–2589.
Nielsen, U.N., Ayres, E., Wall, D.H. & Bardgett, R.D. (2011a). Soil biodiversity
and carbon cycling: a review and synthesis of studies examining diversityfunction relationships. Eur. J. Soil Sci., 62, 105–116.
Nielsen, U.N., Wall, D.H., Adams, B.J. & Virginia, R.A. (2011b). Antarctic
nematode communities: observed and predicted responses to climate change.
Polar Biol., 34, 1701–1711.
Nielsen, U.N., Wall, D.H., Adams, B.J., Virginia, R.A., Ball, B.A., Gooseff, M.N.,
et al. (2012). The ecology of pulse events: insights from an extreme climatic
event in a polar desert ecosystem. Ecosphere, 3(2), 17.
Oberbauer, S.F., Tweedie, C.E., Welker, J.M., Fahnestock, J.T., Henry,
G.H.R., Webber, P.T., et al. (2007). Tundra CO2 fluxes in response to
experimental warming across latitudinal and moisture gradient. Ecol. Monogr.,
77, 221–238.
Ochyra, R., Bednarek-Ochyra, H. & Smith, R.I.L. (2008). New and rare moss
species from the Antarctic. Nova Hedwigia, 87, 457–477.
Review and Synthesis
Osterkamp, T.E., Viereck, L., Shur, Y., Jorgenson, M.T., Racine, C., Doyle, A.,
et al. (2000). Observations of thermokarst and its impact on boreal forests in
Alaska. Arct. Antarct. Alp. Res., 32, 303–315.
Øvstedal, D.O. & Smith, R.I.L. (2009). Further additions to the lichen flora of
Antarctica and South Georgia. Nova Hedwigia, 88, 157–168.
Parnikoza, I., Convey, P., Dykyy, I., Trokhymets, V., Milinevsky, G., Tyschenko,
O., et al. (2009). Current status of the Antarctic herb tundra formation in the
Central Argentine Islands. Glob. Change Biol., 15, 1685–1693.
Peck, L.S., Convey, P. & Barnes, D.K.A. (2006). Environmental constraints on
life histories in Antarctic ecosystems: tempos, timings and predictability. Biol.
Rev., 81, 75–109.
Post, E., Forchhammer, M.C., Bret-Harte, M.S., Callaghan, T.V., Christensen,
T.R., Elberling, B., et al. (2009). Ecological dynamics across the Arctic
associated with recent climate change. Science, 325, 1355–1358.
Reuss, L., Michelsen, A., Schmidt, I.K. & Jonasson, S. (1999). Simulated climate
change affecting microorganisms, nematode density and biodiversity in
subarctic soils. Plant Soil, 212, 63–73.
Rinnan, R., Keinanen, M.M., Kasurinen, A., Asikainen, J., Kekki, T.K.,
Holopainen, T., et al. (2005). Ambient ultraviolet radiation in the Arctic
reduces root biomass and alters microbial community composition but has no
effects on microbial biomass. Glob. Change Biol., 11, 564–574.
Rinnan, R., Michelsen, A., B
a
ath, E. & Jonasson, S. (2007). Fifteen years of
climate change manipulations alter soil microbial communities in a subarctic
heath ecosystem. Glob. Change Biol., 13, 28–39.
Schmidt, I.K., Jonasson, S., Shaver, G.H., Michelsen, A. & Nordin, A. (2002).
Mineralization and distribution of nutrients in plants and microbes in four
arctic ecosystems: responses to warming. Plant Soil, 242, 93–106.
Schuur, E.A.G., Vogel, J.G., Crummer, K.G., Lee, H., Sickman, J.O. &
Osterkamp, T.E. (2009). The effect of permafrost thaw on old carbon release
and net carbon exchange from tundra. Nature, 459, 556–559.
Serreze, M.C., Walsh, J.E., Chapin, F.S. III, Osterkamp, T., Dyurgerov, M.,
Romanovsky, V., et al. (2000). Observational evidence of recent changes in the
northern high-latitude environment. Clim. Change, 46, 159–207.
Simmons, B.L., Wall, D.H., Adams, B.J., Ayres, E., Barrett, J.E. & Virginia, R.A.
(2009). Long-term experimental warming reduces soil nematode populations in
the McMurdo Dry Valleys, Antarctica. Soil Biol. Biochem., 41, 2052–2060.
Sinclair, B.J. (2002). Effects of increased temperatures simulating climate change
on terrestrial invertebrates on Ross Island. Pedobiologia, 46, 150–160.
Sj€
ogersten, S., van der Wal, R. & Woodin, S.J. (2008). Habitat type determines
herbivory controls over CO2 fluxes in a warmer Arctic. Ecology, 89, 2103–
2116.
Sjursen, H., Michelsen, A. & Jonasson, S. (2005). Effects of long-term soil
warming and fertilization on microarthropod abundances in three sub-arctic
ecosystems. Appl. Soil Ecol., 30, 148–161.
Steffensen, J.P., Andersen, K.K., Bigler, M., Clausen, H.B., Dahl-Jensen, D.,
Fischer, H., et al. (2008). High-resolution Greenland ice core data show abrupt
climate change happens in few years. Science, 321, 680–684.
Steig, E.J., Schneider, D.P., Rutherford, S.D., Mann, M.E., Comiso, J.C. &
Shindell, D.T. (2009). Warming of the Antarctic ice-sheet surface since the
1957 International Geophysical Year. Nature, 457, 459–463.
Stendel, M. & Christensen, J.H. (2002). Impact of global warming on permafrost
conditions in a coupled GCM. Geophys. Res. Lett., 29, DOI: 10.1029/
2001GL014345.
Tarnocai, C., Canadell, J.G., Schuur, E.A.G., Kuhry, P., Mazhitova, G. & Zimov,
S. (2009). Soil organic carbon pools in the northern circumpolar region. Global
Biogeochem. Cycles, 23, GB2023. DOI: 10.1029/2008GB03327.
Tebaldi, C., Smith, R.L., Nychka, D. & Mearns, L.O. (2006). Quantifying
uncertainty in projections of regional climate change: a Bayesian approach to
the analysis of multimodel ensembles. J. Clim., 18, 1524–1540.
Timling, I. & Taylor, D.L. (2012). Peeking through a frosty window: molecular
insights into the ecology of Arctic soil fungi. Fungal Ecol., 5, 419–429.
Tosi, S., Onofri, S., Brusoni, M., Zucconi, L. & Vishniac, H. (2005). Response of
Antarctic soil fungal assemblages to experimental warming and reduction of
UV radiation. Polar Biol., 28, 470–482.
Different polar region climate change impacts? 419
Tsyganov, A.N., Nijs, I. & Beyens, L. (2011). Does climate warming stimulate or
inhibit soil protest communities? A test on testate amoebae in high-Arctic
tundra with free-air temperature increase. Protist, 162, 237–248.
Turner, J., Colwell, S.R., Marshall, G.J., Lachlan-Cope, T.A., Carleton, A.M.,
Jones, P.D., et al. (2005). Antarctic climate change during the last 50 years. Int.
J. Climatol., 25, 279–294.
Turner, J., Bindschadler, R., Convey, P., Di Prisco, G., Fahrbach, E. & Gutt, J.
et al. (2009a). Antarctic Climate Change and the Environment. Scientific Committee
for Antarctic Research, Cambridge, pp. 554.
Turner, J., Comiso, J.C., Marshall, G.J., Lachlan-Cope, T.A., Bracegirdle, T. &
Maksym, T. et al. (2009b). Non-annular atmospheric circulation change
induced by stratospheric ozone depletion and its role in the recent increase of
Antarctic sea ice extent. Geophys. Res. Lett., 36, L08502. DOI: 10.1029/
2009GL037524.
Ugolini, F.C. & Bockheim, J.G. (2008). Antarctic soils and soil formation in a
changing environment: a review. Geoderma, 144, 1–8.
Vincent, W.F., Whyte, L.G., Lovejoy, C., Greer, C.W., Laurion, I., Suttle, C.A.,
et al. (2009). Arctic microbial ecosystems and impacts of extreme warming
during the International Polar Year. Polar Sci., 3, 171–180.
Vogel, J., Schuur, E.A.G., Trucco, C. & Lee, H. (2009). Response of CO2
exchange in a tussock tundra ecosystem to permafrost thaw and thermokarst
development. J. Geophys. Res., 114, G04018. DOI: 10.1029/2008JG000901.
Walker, M.D., Walker, D.A., Welker, J.M., Arft, A.M., Bardsley, T., Brooks, P.D.,
et al. (1999). Long-term experimental manipulation of winter snow regime and
summer temperature in arctic and alpine tundra. Hydrol. Process., 13, 2315–2330.
Wall, D.H. (2007). Global change tipping points: above- and below-ground
interactions in a low diversity ecosystem. Philos. Trans. R. Soc. Lond. B Biol. Sci.,
362, 2291–2306.
Wall, D.H., Bradford, M.A., St. John, M.G., Trofymow, J.A., Behan-Pelletier, V.,
Bignell, D.E., et al. (2008). Global decomposition experiment shows soil
animal impacts on decomposition are climate-dependent. Glob. Change Biol., 14,
2661–2677.
Wall, D.H., Lyons, W.B., Chown, S.L., Convey, P., Howard-Williams, C.,
Quesada, A., et al. (2011). Long-term ecosystem networks to record climate
change: an international imperative. Antarct. Sci., 23, 209.
Wardle, D.A. (2002). Communities and ecosystems: linking the aboveground and
belowground components (Monographs in Population Biology 34). Princeton
University Press, NJ.
Webb, N.R., Coulson, S.J., Hodkinson, I.D., Block, W., Bale, J.S. & Strathdee,
A.T. (1998). The effects of experimental temperature elevation on populations
of cryptostigmatid mites in high Arctic soils. Pedobiologia, 42, 298–308.
Willis, K.J., Bennett, K.D., Bhagwat, S.A. & Birks, H.J.B. (2010). 4 °C and
beyond: what did this mean for biodiversity in the past? Syst. Biodivers., 8, 3–9.
Wu, T., Ayres, E., Bardgett, R.D., Wall, D.H. & Garey, J.R. (2011). Molecular
study of worldwide distribution and diversity of soil animals. Proc. Natl. Acad.
Sci. USA, 108, 17720–17725.
Yergeau, E., Bokhorst, S., Kang, S., Zhou, J., Greer, C.W., Aerts, R., et al.
(2012). Shifts in soil microorganisms in response to warming are consistent
across a range of Antarctic environments. ISME J., 6, 692–702.
SUPPORTING INFORMATION
Additional Supporting Information may be downloaded via the online
version of this article at Wiley Online Library (www.ecologyletters.com).
Editor, Richard Bardgett
Manuscript received 13 August 2012
First decision made 13 September 2012
Second decision made 21 November 2012
Manuscript accepted 26 November 2012
© 2013 Blackwell Publishing Ltd/CNRS