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4 °C and beyond: what did this mean for biodiversity

in the past?
a c b d a c
Kathy J. Willis , Keith D. Bennett , Shonil A. Bhagwat & H. John B. Birks
a
Long-term Ecology Laboratory, Biodiversity Research Group, Oxford University Centre for
the Environment, Oxford, OX1 3QY, UK
b
School of Geography, Palaeoecology and Archaeology, Queen's University, Belfast, BT7
1NN, UK
c
Department of Biology, University of Bergen, PO Box N-5020, Bergen, Norway
d
Department of Earth Sciences, Uppsala, Villavägen 16, SE-752 36, Uppsala, Sweden
Version of record first published: 22 Mar 2010.

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 Systematics and Biodiversity (2010), 8(1): 3–9

Perspective
4 ◦ C and beyond: what did this mean for biodiversity in the past?

KATHY J. WILLIS1,3, KEITH D. BENNETT2,4, SHONIL A. BHAGWAT1 & H. JOHN B. BIRKS3

1
Long-term Ecology Laboratory, Biodiversity Research Group, Oxford University Centre for the Environment, Oxford OX1 3QY, UK
2
School of Geography, Palaeoecology and Archaeology, Queen’s University, Belfast BT7 1NN, UK
3
Department of Biology, University of Bergen, PO Box N-5020, Bergen, Norway
Downloaded by [UVA Universiteitsbibliotheek SZ] at 08:31 08 February 2013

4
Department of Earth Sciences, Uppsala, Villavägen 16, SE-752 36 Uppsala, Sweden
(Received 5 July 2009; revised 6 October 2009; accepted 17 November 2009)

How do the predicted climatic changes (IPCC, 2007) for the next century compare in magnitude and rate to those that Earth
has previously encountered? Are there comparable intervals of rapid rates of temperature change, sea-level rise and levels
of atmospheric CO2 that can be used as analogues to assess possible biotic responses to future change? Or are we stepping
into the great unknown? This perspective article focuses on intervals in time in the fossil record when atmospheric CO2
concentrations increased up to 1200 ppmv, temperatures in mid- to high-latitudes increased by greater than 4 ◦ C within
60 years, and sea levels rose by up to 3 m higher than present. For these intervals in time, case studies of past biotic
responses are presented to demonstrate the scale and impact of the magnitude and rate of such climate changes on
biodiversity. We argue that although the underlying mechanisms responsible for these past changes in climate were very
different (i.e. natural processes rather than anthropogenic), the rates and magnitude of climate change are similar to those
predicted for the future and therefore potentially relevant to understanding future biotic response. What emerges from these
past records is evidence for rapid community turnover, migrations, development of novel ecosystems and thresholds from
one stable ecosystem state to another, but there is very little evidence for broad-scale extinctions due to a warming world.
Based on this evidence from the fossil record, we make four recommendations for future climate-change integrated
conservation strategies.
Key words: biodiversity, climate warming, community turnover, conservation, fossil records, historical records, increasing
CO2 , migration, persistence, thresholds

Introduction scientific literature to highlight the potential perils of future

Of the many predictions for climate change in the next cen-
tury, a general consensus is emerging that global tempera-
tures will increase by 2–4 ◦ C and possibly beyond (Mein-
shausen et al., 2009), sea levels will rise (∼1 m ± 0.5 m),
and atmospheric CO2 will increase by up to 1000 ppmv
(Solomon et al., 2007). It is also widely suggested that the
magnitude and rate of these changes will result in many
plants and animals going extinct, for example within the
next century, over 35% of some biota will have gone ex-
tinct (Thomas et al., 2004; Solomon et al., 2007) and there
will be extensive die-back of the tropical rainforest due
to climate change (e.g. Huntingford et al., 2008). These
predictions, based predominantly on models constructed
using the present-day static distribution of species in rela-
tion to present-day climate, paint a depressing picture. And
it is these predictions that pervade the scientific and non-
Correspondence to: Kathy J. Willis. E-mail: kathy.willis@
ouce.ox.ac.uk
climate change and leading to the oft-cited sentiment that
future climate change poses an equal or greater extinction
threat to global biodiversity than land-use change (Parme-
san & Yohe, 2003; Thomas et al., 2004).
Some biologists and climatologists, however, have
heeded caution, pointing out that many of the predicted
increases in climate have happened before, in terms of both
magnitude and rate of change (e.g. Royer, 2008; Zachos
et al., 2008), and yet biotic communities have remained
remarkably resilient (Mayle & Power, 2008) and in some
cases thrived (Svenning & Condit, 2008). Rarely, however,
is this counter-argument presented in the climate-change
debate and, at worst, those who mention it are placed in the
‘climate-change denier’ category. But this discussion is not
about the denial of climate change – far from it – but rather
about presenting a sound scientific basis for understand-
ing biotic responses to the magnitudes and rates of climate
change predicted for the future through using the vast data
resource that we can exploit in fossil records.

ISSN 1477-2000 print / 1478-0933 online

C 2010 The Natural History Museum
DOI: 10.1080/14772000903495833
 4 K. J. Willis et al.
This perspective focuses on intervals of time in the fossil
and long-term ecological record that display similar mag-
nitudes and rates of climate change to those predicted for
the next century. These include a consideration of the re-
sponse of: (i) the neotropical rainforest to higher tempera-
tures and atmospheric CO2 levels (up to 1200 ppmv); (ii)
terrestrial ecosystems in Europe to increases of ∼4 ◦ C in
<60 years; and (iii) the highly biodiverse coastal littoral
forests of Madagascar to sea levels 3 m higher than today.
These case studies have been chosen because they provide
good analogues for aspects of future climate change that
are seen as ‘worst-case scenarios’. In each example, we
present the evidence for the past climate conditions (mag-
nitude and/or rate of change), and ask: what are the biotic
responses to this change? In addition, we discuss the find-
Downloaded by [UVA Universiteitsbibliotheek SZ] at 08:31 08 February 2013
ings from a detailed study on biotic responses to recent
warming. Given the knowledge of these biotic responses,
we outline what information this knowledge can provide to
climate-change integrated conservation strategies in order
to enable long-term persistence of biodiversity.
Case studies
The response of neotropical rainforest to
atmospheric CO2 at 1200 ppmv
Within a time-frame of Earth’s history, current atmospheric
CO2 levels at 380 ppmv are relatively low compared with
the past; geological evidence and geochemical models sug-
gest intervals of time when levels have been up to 18 times
higher than present (Royer, 2008). The fossil record thus
provides plenty of opportunity to assess biotic responses to
intervals of higher global atmospheric CO2 and tempera-
tures. However, this only makes sense if it is also possible
to examine the responses of extant species, which have
modern-day distributions; and where the position of global
lithospheric plates is relatively similar to the present. There-
fore, an ideal time interval for consideration is the past
65 million years when many of the ancestors of modern
tropical and temperate trees had evolved (Willis & McEl-
wain, 2002; Murat et al., 2004; Morley, 2007). It is also fair
to assume that these species had broadly similar ecological
tolerances to present day; it has been demonstrated in a
number of studies that most species are remarkably conser-
vative in their ecological niches (Wiens & Graham, 2005),
and that these remain relatively unchanged through time de-
spite populations persisting through intervals of wide am-
plitude fluctuations in climate (Svenning & Condit, 2008).
The most recent climate models and fossil evidence
for the early Eocene Climatic Optimum (53–51 million
years ago) indicate that during this time interval atmo-
spheric CO2 would have exceeded 1200 ppmv and trop-
ical temperatures were between 5–10 ◦ C warmer than
modern values (Zachos et al., 2008). There is also ev-
idence for relatively rapid intervals of extreme global
warmth and massive carbon addition when global tem-
peratures increased by 5 ◦ C in less than 10 000 years
(Zachos et al., 2001). So what was the response of biota to
these ‘climate extremes’ and do we see the large-scale ex-
tinctions (especially in the Neotropics) predicted by some
of the most recent models associated with future climate
changes (Huntingford et al., 2008)? In fact the fossil record
for the early Eocene Climatic Optimum demonstrates the
very opposite. All the evidence from low-latitude records
indicates that, at least in the plant fossil record, this was one
of the most biodiverse intervals of time in the Neotropics
(Jaramillo et al., 2006). It was also a time when the tropi-
cal forest biome was the most extensive in Earth’s history,
extending to mid-latitudes in both the northern and south-
ern hemispheres – and there was also no ice at the Poles
and Antarctica was covered by needle-leaved forest (Mor-
ley, 2007). There were certainly novel ecosystems, and an
increase in community turnover with a mixture of tropi-
cal and temperate species in mid latitudes and plants per-
sisting in areas that are currently polar deserts. [It should
be noted; however, that at the earlier Palaeocene–Eocene
Thermal Maximum (PETM) at 55.8 million years ago in
the US Gulf Coast, there was a rapid vegetation response to
climate change. There was major compositional turnover,
palynological richness decreased, and regional extinctions
occurred (Harrington & Jaramillo, 2007). Reasons for these
changes are unclear, but they may have resulted from conti-
nental drying, negative feedbacks on vegetation to changing
CO2 (assuming that CO2 changed during the PETM), rapid
cooling immediately after the PETM, or subtle changes in
plant–animal interactions (Harrington & Jaramillo, 2007).]
Why is there such a discrepancy between model predic-
tions for future vegetational responses and the observed
responses in the past recorded in the fossil record? First, it
should be noted that modelled predictions are based upon
the present-day distribution of the plants under investiga-
tion, which almost certainly do not take into account their
full ecological tolerances (Svenning & Condit, 2008). It
is important also to note that ancestors of many of our
modern tropical and temperate plants evolved in the late
Cretaceous/early Palaeogene when global temperatures and
atmospheric CO2 were much higher than present (summa-
rized in Willis & McElwain, 2004) indicating that they have
much wider ecological tolerances than are predicted based
on present-day climates alone. In fact it is probable that
it is cold conditions and lower levels of atmospheric CO2
that pose a greater extinction threat to many tropical and
subtropical plants; a suggestion supported by the evidence
for widespread regional extinction of subtropical species in
Europe with the onset of the cold-stages of the Quaternary
(Svenning, 2003). Second, it is presumed that the rates of
climate change are going to be much higher than have been
seen before, or at least for the past 60 million years – thus
exceeding the capacity of biota to respond – but again this
assumption should be questioned critically when looking
 4 ◦ C and beyond
at the fossil record. An ideal interval of time to address
this question is the late-glacial/post-glacial transition about
11 600 years ago.
The response of mid-latitude
environments to >4 ◦ C temperature
increases in less than 60 years
Evidence from many fossil records, but in particular from
ice-cores, indicate that two rapid increases in temperature
occurred in mid-latitude environments at approximately
14 700 years ago and 11 600 years ago at the end of the last
glacial with associated sharp increases in precipitation and
atmospheric CO2 and CH4 . The rapidity and magnitude of
this temperature increase have only become properly under-
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stood in the past few years. Estimates from the Greenland
ice-cores suggest an increase in air temperatures by as much
as 10 ◦ C in mid- to high-latitudes within 3–5 years for the
first abrupt shift at 14 700 cal. yr BP, and ∼60 years at
11 600 cal. BP (Steffensen et al., 2008).
Given that this temperature increase was greater in mag-
nitude and rate to anything predicted for the next century,
it is an extremely useful time interval to examine possible
biotic responses to 4 ◦ C and beyond. In order to assess bi-
otic responses, however, it is also important to have records
with a good temporal resolution, ideally annual resolution.
A review of the vegetational responses recorded in 11 sed-
imentary sequences with a suitably high temporal resolu-
tion from around the North Atlantic region (Williams et al.,
2002), indicates that in North America and Europe, in less
than 100 years, vegetation responded to the rapid climate
change 11 600 years ago. For tree populations, this change
often occurred in less than two or three generations. The
nature of the response depended upon the former vegeta-
tion; in central Europe (e.g. Willis et al., 1997; Feurdean
et al., 2007) and parts of eastern North America, for exam-
ple, there is evidence in many regions for a change from
needle-leaved dominated to broad-leaved dominated forest,
often in less than 100 years. In comparison, closer to the
ice-sheets, in western Norway, there was a rapid expansion
in the herbaceous and shrub flora and a later arrival of trees,
probably due to a time lag for migration from refugial areas
(Birks & Birks, 2008). The increase in tree populations,
however, even in these northerly regions was still rapid
(Birks & Ammann, 2000). A recent study from the East
Baltic region, for example, indicates that those trees that
survived in northerly refugial populations (Betula, Pinus,
Picea) established within a century, suggesting climate-
driven ecosystem changes rather than gradual plant succes-
sion on new deglaciated land (Heikkilä et al., 2009). Thus
some species expanded very fast in response to late-glacial
warming. There is also evidence, however, for species that
expanded slowly or largely failed to expand from their refu-
gia in response to this interval of rapid climate warming
(Svenning & Skov, 2007) suggesting that persistence and
5
expansion is also dependent on being in a location that was
continuously suitable during the glacial–interglacial ‘cycle’
(Bennett et al., 1991).
Biotic responses to this interval of rapid climate warming
throughout Europe and North America therefore include
evidence for (i) rapid expansion of in situ populations, (ii)
large-scale species range shifts (Birks & Willis, 2008), (iii)
community turnover (Birks & Birks, 2008) and (iv) the
formation of novel community assemblages (Williams &
Jackson, 2007). However, at no site yet studied, anywhere
in the world, is there evidence in the fossil record for large-
scale climate-driven extinction during this interval of rapid
climate change (Botkin et al., 2007). In some regions there
was local or regional extinction, as is apparent throughout
the cold-stages of the Quaternary when increasing numbers
of tropical species went locally or regionally extinct in Eu-
rope (Tallis, 1991; Svenning, 2003; Willis & Niklas, 2004).
There is evidence in the fossil record for the total extinc-
tion of only one species, the east North American spruce
Picea critchfieldii (Jackson & Weng, 1999), but evidence
for widespread global extinction of plants in this interval of
very rapid climate warming has yet to be demonstrated. It
had been argued previously that the large-scale megafaunal
extinction that occurred at the end of the Pleistocene was
climatically driven, but a large number of studies now sug-
gests that this was a predominantly human-driven extinction
event that spanned thousands of years (Koch & Barnosky,
2006; Johnson, 2009) rather than a rapid response to the
large temperature increase at the late-glacial/post-glacial
transition.
The response of Madagascar’s littoral
forest to sea levels 3 m higher than
present
The third case study to be examined is the biotic response
to sea-level change. With predicted sea-level rises in the
next century to be in the region of ∼1 m ± 0.5 m (IPCC,
2007), inundation of many coastal biodiversity hotspots
is inevitable, as is the disappearance of many atolls (Willis
et al., 2007). So what does this mean for biotic communities
that are growing close to or at sea level and closely aligned
to the coastal ecosystem in which they are established? Over
the Holocene there has been considerable variability in re-
gional sea levels (Gehrels, 2009) and probably one of the
most interesting past events for understanding the impact of
higher sea levels on vulnerable biodiverse ecosystems was
the estimated ∼3 m rise in sea level in the Indian Ocean
between 2500–3000 years ago. This higher sea-level stand
is well recorded in fossil corals and higher beaches, particu-
larly along the south-eastern Madagascar coastline (Camoin
et al., 2004). Along this Madagascar coastline is the highly
biodiverse littoral forest, classified as one of Conservation
International’s hottest biodiversity hotspots. A recent study
 6 K. J. Willis et al.

to examine the impact of past sea-level rise on this littoral change), while others (S. ornatus, S. monticolus) decreased
forest has revealed some interesting trends (Virah-Sawmy or remained unchanged (S. trowbridgii). What is also no-
et al., 2009). Initially the littoral forest appeared to be re- ticeable from this study is that nothing went locally extinct.
markably resilient to storm surges associated with sea-level
rise. However, a sudden threshold event then occurred when Discussion
the ecosystem switched from littoral forest to Ericaceous
So why is there this discrepancy between what the fos-
heathland in less than 50 years. This Ericaceous heathland
sil and historical records are telling us about extinctions
then persisted as an alternative ‘stable state’ for ∼3500
driven by climate change and those predicted through mod-
years before littoral forest once again became established.
els? Many biota, using evidence from fossil plant records,
The cause of this threshold event appears to have been a
likely have much wider ecological tolerances than are usu-
combination of storm surges with an interval of pronounced
ally assigned in models. Also, the present-day distribu-
aridity – thus it was a consequence of two climatic events,
tion of species, especially in mid to high latitudes, of-
presumably stressing the forest species both in terms of
ten has a strong historical/pre-historical cultural imprint
salinity and aridity, that triggered the crossing of a critical
(e.g. Bradshaw & Lindbladh, 2005) which again is often not
threshold.
Downloaded by [UVA Universiteitsbibliotheek SZ] at 08:31 08 February 2013

taken into account in the models. However, the discrepancy

The biotic response to sea-level rise in Madagascar
is also in part due to the coarse scale of the models used to
was therefore rapid and dramatic – with a switch from
estimate climate change-induced habitat loss. For example,
one ecosystem (littoral forest) to another (heathland).
a recent study to assess whether climate change-induced
What is also important to note, is that nothing went
habitat losses predicted at the European scale (16 km ×
regionally extinct; the forest that recovered was of a
16 km grid cells) are also predicted from local-scale data
different combination, but it would appear that populations
and modelling (25 m × 25 m grid cells) in two regions of
of littoral forest species existed in the mosaic landscape
the Swiss Alps indicated that whereas the European-scale
around the coastal region during the higher sea level, and
model predict loss of all suitable habitats, local-scale mod-
repopulated the coastal zone once the sea level fell again
els predict persistence of suitable habitats in up to 100%
(Virah-Sawmy et al., 2009). It also became apparent from
of species (Randin et al., 2009). A similar conclusion was
this study that the littoral forest was more resilient to
also reached in a study to assess the predictive accuracy
sea-level change than another coastal forest type in this
of bioclimatic envelope models for the future distribu-
region, open Uapaca woodland. The latter demonstrated
tion of European butterflies (Luoto & Heikkinen, 2008).
a similar threshold event in response to sea-level rise, but
Here, of the 100 species studied, a model that included
this region has remained open heathland ever since.
topography predicted only half of the species losses for
Historical responses to recent warming the period 2051–2080 compared with those predicted by a
climate-only model. In contrast, the number of species pre-
The examples presented above are typical of the vast
dicted to disappear from flatlands doubled. It would appear
majority of fossil records extending through both deep
from both these studies that habitat heterogeneity resulting
and Quaternary timescales; all suggest that broad-scale
from topographic diversity may be an essential factor for
extinctions related solely to climate change at the rate
persistence of biota in a future changing climate (Willis &
and magnitude predicted for the next century, are highly
Bhagwat, 2009).
unlikely. This somewhat controversial conclusion is also
Based on these studies, and many others using fossil and
borne out in a detailed recent case study of a 100-year
historical records, we argue that evidence for the widely
record from Yosemite National Park (Moritz et al., 2008).
cited view that future climate change poses an equal or
In this study, the biota was systematically re-surveyed in
greater threat to global biodiversity than anthropogenic
the same region that had been surveyed ∼100 years ago.
land-use change and habitat loss (Thomas et al., 2004)
The advantage of this study was not only the availability of
is equivocal: extinctions driven by the latter processes of
excellent historical baseline data against which to compare
habitat loss pose a far greater threat to global biodiversity.
present-day distributions, but also that there have been
It is also questionable, however, whether it is even possible
restricted human activities in the Yosemite National Park
to now separate the two processes, given that over 80% of
over this time. This study therefore provides a record of
the Earth’s terrestrial biomes now have evidence of an an-
responses of small-mammal communities to the past 100
thropogenic impact upon them (Ellis & Ramankutty, 2008).
years of climate change that can be separated from the
What we probably need to be considering is the synergistic
impacts of human land-use change. Results from this work
effect of these two factors on biodiversity (Travis, 2003).
demonstrated that responses of small mammals to ∼3 ◦ C
increase in minimum temperatures was far from straight-
forward, and that even within a single genus (e.g. common How can we preserve biodiversity?
shrew, Sorex), some species such as S. palustris increased How can we preserve biodiversity, given potential migra-
their altitudinal range (probably in response to climate tions, compositional changes and turnover, in many cases
 4 ◦ C and beyond
occurring in a highly fragmented landscape? Fossil and
historical records provide some important pointers for cli-
mate change-integrated conservation strategies to help the
long-term persistence of biodiversity. These include:
(i) Managing for novel ecosystems. What clearly emerges
from fossil records during intervals of rapid climate change
is evidence for the formation of novel ecosystems (Williams
& Jackson, 2007). When combining the impacts of hu-
man activities and rapid climate change, these can be
predicted for the future with some confidence. Manage-
ment of novel ecosystems, however, is going to require
a very different set of conservation practices to those fo-
cused on preventing declines and local extinctions of cer-
tain species (Seastedt et al., 2008). Management should be
focused on conserving ecosystem function and evolution-
Downloaded by [UVA Universiteitsbibliotheek SZ] at 08:31 08 February 2013
ary process (Mace & Purvis, 2008), thereby maintaining
the conditions necessary to conserve overall biodiversity,
yet also accepting that community composition in a re-
gion will probably look very different to what was there
before.
(ii) Retaining ecological memory. Another point to
emerge from the fossil record is the importance of small,
isolated populations in a landscape for maintaining the eco-
logical memory (sensu Bengtsson et al., 2003) of a region. It
is apparent from studies of both cold-stage and warm-stage
refugia (Birks & Willis, 2008), that these small populations,
although often barely detectable in long-term ecological
records due to their low numbers, provide a continuum in
diversity through times of climatic/human impact includ-
ing threshold events. The evidence suggests that many of
these plants (and animals) were not in small, intact frag-
mented patches, but rather were present as a few individ-
uals within a ‘foreign’ landscape (e.g. a few trees within
an open grassland/heathland/agricultural landscape). Inter-
estingly, a recent large-scale study on the effect of habitat
area and isolation on present-day fragmented animal popu-
lations has indicated that patch area and isolation are poor
predictors of occupancy (Prugh et al., 2008). Instead they
found that it was the intervening matrix that was more im-
portant and in many cases, animals venturing outside of
patches found sufficiently benign conditions to live and
reproduce. What these studies therefore imply is that main-
taining ecological memory in refugia is important but also
that the environments for many will be those that are often
viewed as unsuitable (due to size, isolation or amount of
human modification) by conservationists (Bhagwat et al.,
2008; Chazdon et al., 2009).
(iii) Conserving regions of high genetic diversity. In or-
der to conserve long-term biodiversity it is often argued that
we must conserve evolutionary potential in the form of ge-
netic diversity (Mace & Purvis, 2008). It is also suggested
that this is particularly true in intervals of rapid climate
change when genetic diversity will, in theory, enable plas-
ticity in response to environmental change (Hellmann &
Pineda-Kirch, 2007). A combination of fossil records and
7
molecular phylogenies is essential in this respect (Hu et al.,
2009), because determination of areas with high genetic
diversity often requires an understanding of the history of
the former distribution of plants and animals. For example,
many regions of greatest genetic diversity in Europe are
where plants and animals were isolated in refugia during
the cold-stages of the Quaternary (Petit et al., 2008; Hu
et al., 2009). Ironically, in Europe these regions are also
some of the most heavily impacted through farming and
other human activities and often fall outside of protected
area designation.
(iv) Developing resilience to threshold events. Fossil and
historical records have been at the forefront in demonstrat-
ing the occurrence of threshold events and the transition
(often rapid) from one stable ecosystem state to another
and probable triggering mechanisms (Scheffer et al., 2001;
Dearing, 2008). However, they also have another important
role to play in future planning and that is in the determina-
tion of what makes some areas more resilient to threshold
events than others. For example, in the Madagascar example
discussed above, one forest type appears to have been more
resistant to storm surges associated with sea-level change
than another (Virah-Sawmy et al., 2009). This study demon-
strates the utility of fossil records both in the determination
of resilient and less-resilient communities, and also their
potential to provide testable hypotheses as to why this is the
case. Only with such information available will it be possi-
ble to try and build the concept of thresholds and resilience
into climate change-integrated conservation strategies.
In summary, fossil records contain large amounts of rel-
evant data for understanding current and future responses
to climate changes of 4 ◦ C and beyond. Based on such ev-
idence we urge some caution in assuming broad-scale ex-
tinctions of species will occur due solely to climate changes
of the magnitude and rate predicted for the next century.
The fossil record indicates remarkable biotic resilience to
wide amplitude fluctuations in climate and although there
may have been local or regional extinctions, global extinc-
tions due solely to climate change appear to have been ex-
tremely rare. However, evidence suggests that there will be
rapid community turnover, broad-scale migrations, thresh-
old events and the formation of novel ecosystems. These
biotic changes will require a different kind of climate
change-integrated conservation strategy, one that focuses
less on preventing species declines and more on preserving
ecological memory, ecosystem function and evolutionary
potential.
Acknowledgements
We are grateful to Elliot Shubert and an anonymous re-
viewer for constructive comments, to Hilary Birks and
members of the Oxford Long-term Ecology Laboratory for
valuable discussions, and to Cathy Jenks for editorial assis-
tance.
 8 K. J. Willis et al.

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