Download Biodiversity baselines, thresholds and resilience: testing predictions

Review
Special Issue: Long-term ecological research
Biodiversity baselines, thresholds and
resilience: testing predictions and
assumptions using palaeoecological
data
K.J. Willis1,3,4, R.M. Bailey2, S.A. Bhagwat1,2 and H.J.B. Birks1,2,3
1
Institute of Biodiversity at the James Martin 21st Century School, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
School of Geography and the Environment, University of Oxford, Oxford OX1 3QY, UK
3
Department of Biology, University of Bergen, Post Box 7803, N-5020 Bergen, Norway
4
Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK
2
Fossil records are replete with examples of long-term
biotic responses to past climate change. One particularly
useful set of records are those preserved in lake and
marine sediments, recording both climate changes and
corresponding biotic responses. Recently there has been
increasing focus on the need for conservation of ecological and evolutionary processes in the face of climate
change. We review key areas where palaeoecological
archives contribute to this conservation goal, namely:
(i) determination of rates and nature of biodiversity
response to climate change; (ii) climate processes responsible for ecological thresholds; (iii) identification of
ecological resilience to climate change; and (iv) management of novel ecosystems. We stress the importance of
long-term palaeoecological data in fully understanding
contemporary and future biotic responses.
Testing predictions and assumptions using
palaeoecological data
It has long been argued that to conserve biological diversity
it is essential to build an understanding of ecological
processes into conservation planning [1,2]. In particular,
an understanding of ecological and evolutionary processes
is vital for identifying those factors that might provide
resilience in the face of climate change [3].
While this need to incorporate dynamic processes of
species and their environmental interactions into conservation planning frameworks and tools is becoming increasingly accepted [3–7], the data-sets that can provide the
necessary detailed information are very often lacking. This
is because many ecological and evolutionary processes
occur over timescales that exceed even long-term observational ecological data-sets (100 years). One mechanism
for dealing with this data gap has been to rely on models
[8–10] with modelling output then being fed directly into
the planning tools. These models, however, mainly focus on
future spatial distribution of species and communities
under climate change (e.g. [10]) rather than the ecological
and evolutionary responses to climate change.
Another source of data, and the focus of this review, is
provided from fossil records contained in stratigraphic
sequences, such as marine and terrestrial sediments.
These records provide information on the dynamics of
species and their interactions with environmental change
spanning thousands of years [11–13]. The temporal resoGlossary
Alkenone Unsaturation Index: Some phytoplankton synthesise long-chain
ketone compounds (alkenones) containing carbon atoms with both two and
three double-bonds. The relative proportion of these bond types varies in
direct response to growth temperature. This ratio can be measured in material
preserved in marine sediment cores (e.g. Emiliania huxleyi coccoliths) and
interpreted in terms of past water temperature.
Bioturbation: The movement of sedimentary material, following deposition,
through biological activity such as burrowing and root growth.
Cenozoic: The geological era spanning the past ca. 65 million years, during
which time the trend in mean global temperature has been one of cooling.
Glacial: A period of relatively cold and dry conditions, typically lasting in the
region of 80 000 years, associated with expansion of high latitude continental
ice-sheets, sea level reduction of the order of 100 m and considerable changes
(compared to present) in terrestrial conditions across all latitudes.
Interglacial: A period of relatively warm conditions lasting approximately
10000–20000 years, associated with reduced ice-sheet extent and sea-levels
similar to those of today. Our current interglacial period is the Holocene, which
began approximately 11 500 years ago. In broad terms, interglacials have
occurred once every 100 000 years in the second half of the Quaternary period.
Ocean ventilation: The mixing of surface ocean water to depths where the
water body has remained isolated (on timescales of decades to millennia) from
gaseous exchange with the atmosphere. Ventilation has major impacts on, for
example, regional ocean productivity.
Orbital-forcing: The driving of major changes in the Earth system by periodic
variations in the geometry of Earth’s solar orbit, affecting the intensity and
distribution of incident solar radiation (‘insolation’). The effects of insolation
variations are observed at regional to global scales and on timescales of tens to
hundreds of thousands of years. Orbital forcing is the primary driver of the
Quaternary glacial–interglacial cycles.
Quaternary: The period of geological time spanning approximately the last two
million years. This period is characterised by major oscillations, over a range of
temporal and spatial scales, in conditions between glacial (relatively cold) and
interglacial (relatively warm) conditions.
Radiometric dating: Estimating geological time using the known decay rate of
radioisotopes present within the sample. Many different radioisotopes have
been used for this purpose. The sample age is defined as the time elapsed
since some past ‘re-setting event’, and the nature of this event is specific to
each material and radioisotopic method. For further details see Box 1.
Corresponding author: Willis, K.J. ([email protected]).
0169-5347/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2010.07.006 Trends in Ecology and Evolution 25 (2010) 583–591
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Box 1. Chronology
A sound chronological framework is essential in many aspects of
palaeoenvironmental research. All dating methods depend on a
measurable accumulation of physical changes, progressing at a
known rate, from a condition known at the time of the event to be
dated. Relevant time-dependent processes include the decay of
radioisotopes, the in-growth of decay (‘daughter’) products, and a
range of other physical changes. The lower age limit depends on the
minimal detection limits of these changes and the upper limit on the
time needed for the accumulation of changes to be complete.
Commonly used methods include: radiocarbon dating (e.g. dating
used for Figures 2–4), which gives the age at which incorporation of
radiocarbon into material ceased (typically the death of a living
organism, e.g. [83]); luminescence dating, which provides estimates
of the time elapsed since sedimentary material was deposited [84]
or pottery last fired [85]; and U-series methods, which date the point
at which a sample becomes a chemically closed system, such that
changes in the ratio of U to Th isotopes in the sample depend only
on radioactive decay (used extensively for dating coral and
speleothem records, e.g. [86,87]). In situations where discrete and
identifiable incremental changes occur over known time periods
(e.g. annual growth of tree rings, annual deposition of laminated
lake sediments, seasonal snow accumulation bands in ice-cores),
layer-counting methods have potential to provide highly precise
(annual and sub-annual) and reliable age estimates, e.g. [88,89]. The
accuracy and precision of the different radiometric methods vary
considerably, and depend in part on the context in which the
methods are applied. The use of multiple dating methods, each
reliant on different physical mechanisms and different underlying
assumptions, improves confidence in the overall chronology and is
an approach now commonly applied.
lution of these records can often be as fine as observational
ecological records, with annual layers in some sequences
providing records of yearly fluctuations [14]. Spatial resolution can also range widely from local to regional changes
in diversity [13]. An often perceived drawback of these
records is taxonomic resolution, which in most cases is to
genus-level rather than species-level, but with increasingly
sophisticated methods of identification, there are now
many records that are resolved to species-level [15,16].
Combined with good chronological control (Box 1), such
records are a valuable data-source for understanding ecological and evolutionary processes in response to climate
change [17].
Given current threats posed by the combined cocktail of
climate change and habitat destruction [18], key questions
for biodiversity conservation that require an understanding of evolutionary and ecological processes include the
following. (i) What will be the rates and nature of changes
in ecological processes in response to climate change? (ii)
Which combinations of abiotic and biotic processes will
result in a given ecological threshold being exceeded? (iii)
What processes bolster resilience to climate change? (iv)
How can we manage the novel ecosystems that result from
biotic responses to climate change? This paper reviews
palaeoecological archives of biotic responses to past climate changes that are available to help address these
questions. The message that emerges is that such
palaeo-records have much to offer not only in terms of
understanding the ecological and evolutionary processes
responsible for biodiversity, but also in guiding the
management strategies necessary to ensure biodiversity
conservation.
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Rates and nature of changes in ecological processes in
response to climate change
Predicted climate changes over the next 50–70 years
suggest that global temperatures may increase by up to
48C and atmospheric CO2 concentrations may rise from
today’s 380 ppmv to >1000 ppmv [19,20]. Furthermore, the
rate of these changes will be rapid with some models
predicting a rise of 0.418C/decade (IPCC A2 scenario) in
tropical regions [21]. A key question for conservationists,
therefore, is what will be the nature and rates of ecological
responses to these changes? Whilst studies on present-day
species distributions in relation to current climate can
provide information on possible future distributions
through modelling [8–10], it is much more difficult to model
the response of ecological processes (which affect whole
communities) to these broad-scale predicted changes in
Box 2. Terrestrial and marine archives
Marine sedimentary sequences include material that accumulates
both from within the ocean (e.g. primary productivity) and from
outside it (e.g. windblown dust from deserts and iceberg-borne
sediments from higher latitudes) and as such they provide a richly
diverse and effectively continuous archive spanning tens of millions
of years [24] (e.g. see Figure 1).
One of the most important palaeoenvironmental records obtained
from marine sediments is the ratio of stable isotopes of oxygen
(18O/16O) found in the calcareous tests of benthic foraminifera (e.g.
see Figure 1) which is interpreted as a proxy for global ice-volume
and temperatures [90]. The compiled d18O record provides an icevolume/temperature framework for the Cenozoic [24], and a detailed
record of Quaternary glacial–interglacial transitions [91]. Estimates
of atmospheric CO2 from ocean sediments have also been obtained
using the dependence of isotopic fractionation (d13C) on dissolved
CO2 in phytoplankton photosynthesis [92,93].
Terrestrial sedimentary sequences (primarily lake and peat
deposits) include material produced within the water body (for
example due to primary and secondary productivity) plus that
derived externally (material transported by water or wind). Consequently, these sediments also provide rich environmental archives,
and organic remains provide a large proportion of the available
proxies. Pollen and spores are produced in great abundance by
many plants and, due to their chemically resistant outer wall, are
typically found in high concentrations in terrestrial sedimentary
sequences. Changes in pollen assemblages through time are used
extensively in palaeoecology (e.g. Figures 2–4) to infer changes in
regional and local vegetation composition and structure [11–13,17].
Other biological indicators used include plant macro-fossils, the
remains of aquatic organisms (e.g. diatoms and ostracods), insects
(e.g. chironomids and beetle remains), dung spores (a record of
mega-faunal presence), as well as charcoal and geochemical
signatures of biological activity (e.g. stable isotopes of carbon and
nitrogen). Changes in the occurrence of these indicators can be
interpreted in terms of climatic shifts, changes in lake conditions
and/or landscape (catchment) alteration and of ecosystem functioning through time [17] (e.g. see Figure 4).
Another important archive of past environmental change is
preserved in ice-sheets. Records that span 100 000 years have
been obtained in Greenland [94] (e.g. see Figure 2) and 800 000
years in Antarctica (EPICA members [95]). Shorter records have also
been derived from lower latitude locations, such as mountain
glaciers, e.g. [96]. Two key features of these records, that are of
particular relevance to this paper, are their ability to provide detailed
evidence on the concentration of past atmospheric greenhouse
gases (including CO2 and CH4), measured in atmospheric samples
trapped as bubbles in the ice, and the apparent magnitude and
rapidity of past climatic changes [34] (measured through ratios of
various isotopes within the glacial ice which are determined
predominantly by air temperature [98,99]).
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climate. In particular, the interactions of abiotic and biotic
processes might lead to very different outcomes to those
predicted by models. Arguably one of the most worrying
model predictions is that within the next 50 years the
combination of increasing temperatures and CO2 concentrations could result in up to 80% of the tropical rainforest
biome becoming savannah (e.g. [22]), a prediction that is
now leading to changes in funding strategies for conservation organisations. It is therefore important to know how
reliable this prediction is and to forecast accurately what
will happen to tropical rainforests under predictions of
greatly elevated global temperatures and atmospheric
CO2 levels.
Ocean sedimentary sequences provide an excellent archive for reconstructing intervals in Earth’s history when
CO2 and global temperatures exceeded current predictions
for 2070 (Box 2). Measurements of stable isotopes in these
long continuous records provide a record of temperature
and CO2 variations over the past 65 million years [23,24].
What these measurements demonstrate is that during the
Eocene thermal maximum (55–53 Ma), atmospheric CO2
levels increased to 1200 ppmv and tropical temperatures
were up to 5–108C higher than they are at present [23].
These climate conditions exceed those currently predicted
and so we might ask what was the biodiversity response?
Here, records of past biotic responses obtained from tropical lake sedimentary sequences containing pollen and
plant macrofossils (Box 2) provide critical insights [25].
The Eocene appears to have been one of the most biodiverse intervals in Earth’s history with the highest level of
diversity recorded in tropical pollen records over the past
45 Ma [26] and the most extensive distribution of the
tropical rainforest biome, with tropical forest extending
from the equator up to latitudes of 40o north and south
[25,27] (Figure 1).
Why is there such a discrepancy between the indications
from palaeoecological records and the model predictions?
One suggestion is that with higher levels of atmospheric
CO2, the effects of CO2 fertilisation [28] over-ride the
negative impacts of higher temperatures [29,30]. Recent
models that include CO2 fertilisation effects indicate that
if fertilisation is included, the tropical biome remains
largely unaffected [30]. An outstanding question for
palaeoecological biodiversity archives covering this time
interval is whether it is possible to find proxy evidence for
a CO2 fertilisation effect and then determine its spatial
and temporal consequences in relation to increasing CO2
concentrations.
Another critical question relating to future climate
change is whether rates of predicted change will be too
rapid for ecological processes to react and so prevent
species and communities persisting. There is also the
question of whether species will be able to migrate quickly
enough to new locations with a suitable climate. Studies
based on data from extant populations and modelling
suggest that rapid rates of change could pose a serious
threat for many species and communities unable to track
climate space quickly enough, resulting in extensive
extinctions [9,31]. But it is also known from fossil records
that there have been numerous previous intervals of
abrupt climate change [32,33]. What were the responses
[(Figure_1)TD$IG]
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Figure 1. Global climate, atmospheric carbon dioxide, plant diversity and extent of
tropical forests during the period 20–65 Ma. Greatest levels of plant diversity and the
most extensive global distribution of tropical rainforest are apparent during intervals
of elevated CO2 (>1000 ppmv) and high mean global temperatures (>10 8C warmer
than present) (the Eocene thermal maximum). The top panel shows (18O isotope
data (after data from Refs [23,24] available at: www.ncdc.noaa.gov/paleo/metadata/
noaa-ocean-8674.html). Changes in d18O are interpreted as reflecting changes in
mean global temperature and total global ice volume. During the time of the Eocene
thermal maximum (marked in the figure) global mean temperatures are estimated to
have been 12 8C warmer than present [24]. The middle panel shows number of
morphospecies (open circles), a measure of floral species richness estimated from
fossil pollen from sites in central Colombia and western Venezuela [26]. Adapted
from Jaramillo, C. et al. (2006) Cenozoic Plant Diversity in the Neotropics. Science,
311, 1893-1896. Reprinted with permission from AAAS. Filled squares show
estimates of atmospheric CO2 concentration. Here, plotted values are estimates
derived from palaeosols, phytoplankton and stomatal density indices. For clarity,
all values with statistical uncertainty >30% have been omitted, reducing the size
of the dataset (ftp://ftp.ncdc.noaa.gov/pub/data/paleo/climate_forcing/trace_gases/
royer2006co2.txt) by 17%. The lower panel shows the estimated extent of tropical
forests during the period 50–60 Ma, based on macro-fossil and pollen data [27].
of past biodiversity to these previous intervals of rapid
climate change? The existence of highly detailed evidence
from ice-core records (Box 2) spanning the last full glacial
cycle provides an ideal opportunity to examine biodiversity
responses to rapid climate change. For example, ice-cores
indicate that temperatures in mid to high latitudes oscillated repeatedly by more than 4oC on timescales of decades
or less [34] (Box 2). Numerous records of biodiversity
response from North America and Europe across this
time-interval reflect ecological changes with a decadal
resolution [35–37]. While they demonstrate clear evidence
for rapid turnover of communities (e.g. Figure 2), novel
assemblages, migrations and local extinctions, there is no
evidence for the broad-scale extinctions predicted by models; rather there is strong evidence for persistence [25].
However, there is also evidence that some species expanded their range slowly or largely failed to expand from their
refugia in response to this interval of rapid climate warming [38]. The challenge now is to determine which specific
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(Figure_2)TD$IG][ Review
Figure 2. Increased biodiversity (estimated pollen and spore richness) and
elevated community turnover are apparent during the interval of rapid warming
at the late-glacial to early Holocene transition, 11 550 years ago (vertical dashed
line) at Kråkenes, western Norway [43]. The pollen richness (open circles with
fitted, solid line) is estimated by rarefaction analysis, an interpolation procedure
that estimates how many pollen and spore types would have been found if all the
sample counts were the same count size. A locally weighted smoother (span = 0.5)
has been fitted to highlight the major trends in the richness estimates. The
temperature curve shown (lower solid line) is from the Greenland NGRIP ice-core
([97,98] and Box 2). The lower plot in the small box shows the relationship between
pollen compositional turnover in standard deviation (SD) units [43] and magnitude
of summer temperature change as inferred from changes in the sub-fossil
chironomid assemblages [99] in 250–300-year time intervals within 11 625–9750
years ago. High turnover (>0.5 SD units) occurs when chironomid-inferred
temperature changes are highest (0.90 SD, 1.84 8C change at the onset of the
Holocene 11 550–11 300 years ago; 0.68 SD, 0.95 8C change at 11 300–11 000 years
ago). The fitted line is a simple linear regression (r2 = 0.68). This plot shows the
increase in compositional turnover with rapid climate change.
factors enable persistence during intervals of rapid climate
change, since such information is crucial to conservation
strategies for the future. Palaeoecological archives suggest
that rapid rates of spread [39], realised niches broader
than those seen today [40], landscape heterogeneity in
space and time [41,42], and the occurrence of many small
populations in locally favourable habitats [29,37,43–44]
might all have contributed to persistence during the rapid
climate changes during the transition to interglacial conditions approximately 11 500 years ago.
Determination of ecological thresholds driven by
climate change
Ecological thresholds, where a community or ecosystem
switches from one stable state to another, usually within a
relatively short time-interval, are well documented in both
marine and terrestrial ecosystems, and have long been
recognised in sedimentary records [45–49]. Past and present human impact is well known to be a driver of such
switches (e.g. [50]), with evidence to suggest that the
likelihood of ecological thresholds may increase when
humans reduce resilience [51] (see www.resalliance.org).
However, there are many thresholds that occur in the
absence of humans and a key question is what combination
of climatic variables result in a regime shift, and what
impact it has on biodiversity.
There is much information available from palaeoecological records relevant to biodiversity conservation in this
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respect, in particular information on alternative stable
states, rates of change, possible triggering mechanisms
and systems that demonstrate resilience to thresholds.
In a study from central Spain, for example, it has been
demonstrated that over the past 9000 years, several
threshold changes occurred, shifting from one stable forest
type to another (pine to deciduous oak and then evergreen
oak to pine) [52]. The trigger appears to have been a
combination of at least two abiotic variables; in the first
shift, an interval of higher precipitation combined with less
evaporation and in the second, increased aridity combined
with increased fire frequency. A similar ‘double-trigger’
was also found to be important in regime shifts along
the south-east coastline of Madagascar [53] where a
threshold shift from closed littoral forest to open Ericadominated heathland occurred in response to the combined
effects of aridity and sea-level rise. Neither of the variables
occurring alone resulted in a shift but the combination of
the two did.
What relevance is this information to biodiversity conservation? First, this information is important in determining the true climatic baseline of an ecosystem (i.e. what
might be expected for a given climate state). Natural
variability in ecosystems through time is well-documented
[54] but it is increasingly apparent from palaeoecological
records that in many cases it is not variability around a
steady state but rather variability around alternative
stable states that is important. As an example, a study
of the Sierra de Manatalan IUCN biosphere reserve in
Mexico demonstrated that, during more arid intervals,
there is a Pinus-dominated forest (as there is now), but
during intervals of increased humidity, this pine forest
type has been replaced by cloud forest [55], which is a
different stable configuration. The transition between
these two forest types (stable states) is rapid [<50 years:
one forest generation]. Predicting the point at which interstate transitions occur is notoriously difficult and data
provided by palaeoecological studies have potential to
provide valuable insights.
Second, it is apparent from palaeoenvironmental
records that it is not only ecosystems that should be viewed
as possessing alternative stable states: climatic systems
have them as well [54]. Recent work on past mega-droughts
in North America, recorded through tree-ring records [Box
1] indicate numerous intervals of past drought, with each
being interspersed by more humid conditions [56,57]. An
interesting aspect of these records is that the droughts
during the Mediaeval period around 1000 years ago were
remarkably more severe in duration and extent than those
experienced since then. The fact that these droughts were
as severe in both magnitude and length as those predicted
by IPCC model projections for the future has many important implications for conservation planning. Using these
past records should not only provide an indication of what
might become locally extinct but also which regions provide
refugia for biodiversity during mega-drought intervals.
Such information (see Ref. [57] for Asia) should be routinely incorporated into conservation planning and reserve
design because it is these regions that will allow persistence of biodiversity during future droughts and conserve
future evolutionary and ecological processes [3,58].
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Figure 3. The vegetation response at two Madagascan sites (Fossa and Bassin) to an environmental perturbation (sea-level rise and climatic aridity, approximately 1000
years ago). At both sites, the early part (>1200 years ago) of the record shows stable forested conditions, followed by a transition to heathland (1000 years) in response to
the perturbation. Subsequently, vegetation at Fossa recovers towards the previous stable state (higher ecological resilience) while at Bassin the vegetation state continues
to diverge (lower ecological resilience). Each main panel shows a time-series of relative pollen abundance (P, continuous line) and a smoothed version (dashed line; a
robust locally-weighted polynomial model, with a span of 0.25). ‘Heathland’ refers to Erica, Asteraceae and grass species; ‘Forest’ refers to sum of littoral forest tree species
at the Fossa site and sum of open Uapaca forest tree species at the Bassin site, ‘Recovery’ refers to return to forest conditions (full details of these data are found in [53,59]).
The inset panel in each case shows a phase plot for the smoothed pollen data, where the relative pollen abundance (P) (vertical axis) is plotted against the local gradient (DP/
Dt). The smoothed data were interpolated and re-sampled (for the same total number of points as contained in the original data set) at uniform intervals in time. These
points are shown on the phase plots and their proximity along each trajectory indicates the rate of change in system state (arrows indicate the direction of time). The dashed
ovals enclose the stable (forest) state prior to the perturbation. Noticeable is the difference in trajectories between the two sites: the systems appear to be heading for full
recovery at Fossa, whilst no sign of recovery is apparent in the trajectories associated with Bassin.
Identification of ecological resilience to climate change
Two other key questions that can be addressed through
examination of palaeoecological records are which
combinations of biotic and abiotic processes will result
in ecological resilience to climate change and where these
combinations might occur. The detailed study of long-term
dynamics of the highly diverse coastal forests of south-east
Madagascar [59] discussed above in relation to ecological
thresholds, also provides unique insights into ecological
resilience to climate change. Biotic changes were reconstructed for the last 6000 years at four sites from pollen
assemblages preserved in small sites along the coast.
Abiotic changes such as aridity phases and storm surges
were also reconstructed. From such multi-proxy evidence,
threshold events could be identified, as discussed above, in
response to the combined influence of storm surges (resulting from sea-level rise) and aridity intervals causing
switches from forest to heathland. What is relevant here
in considering resilience is that by studying four sites
supporting different vegetation types today, it was possi-
ble to show that diverse, closed-canopy littoral forest was
resilient to storm surges and aridity, whereas open
Uapaca woodland was much less resilient. The latter
underwent a threshold shift in response to storm surges
and aridity from which it has never recovered, remaining
heathland ever since (Figure 3). Thus the initial composition structure and density of the coastal forests appear to
have been important determinants of resilience to storm
surges and aridity. Why some ecosystems are more resilient to climate change than other systems is unclear, but
the Madagascar study illustrates the value of palaeoecological archives in identifying different degrees of resilience in different systems. This is a good example of where
present conditions are partly dependent on previous
states, namely a hysteretic response, operating on temporal scales only accessible through palaeoenvironmental
data. It has clear implications for assessing the multiplicity of equilibrium states and the notion of a unique ecological baseline. Such information is of critical importance
in future conservation strategies.
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Another important factor for the maintenance of resilience is the conservation of genetic diversity. It has long
been argued that this will provide a basis for adaptation
and resilience to environmental stress and climate change
(e.g. [60]) and enable organisms to continue to adapt and
evolve to new circumstances [2]. It is therefore important to
conserve regions that contain high genetic diversity and
species or areas that are phylogenetically distinct [61].
Palaeoecological records in combination with molecular
phylogenies have an important role to play in the identification of both of these factors [58]. There are now a number
of combined analyses based on terrestrial fossil sequences
and molecular phylogeographic data indicating that
regions of greatest genetic diversity (containing genetically
distinctive populations) are those where, over the long
term, plants and animals have persisted in cold-stage
refugia during intervals of adverse climatic perturbations
[62–64]. Often these populations are at the trailing edge of
the current species distribution [65]. It is only through
knowledge of species’ past distributions in refugia during
the Pleistocene ice-ages, as determined through fossil
pollen and macrofossil records (e.g. [44,66–69]; Box 2), that
a detailed understanding of the spatial extent (and often
patchy distribution) of genetic diversity can be appreciated
[64]. A detailed study combining palaeoecological records
and molecular data [69] for the European beech (Fagus
sylvatica), for example, shows great genetic diversity in
Mediterranean populations, especially in the Balkans and
Iberia, but little post-glacial spread. The major spread of
beech started from scattered cold-stage refugia in central
Europe, an area with low genetic diversity today.
It is also interesting to note that a number of studies
indicate that there is often no positive correlation between
extant species density and genetic diversity; the former
tending to be associated with extant suitable habitats (e.g.
soil type and moisture availability) and the latter with
location of former glacial-stage refugia and routes of postglacial (Holocene) colonisation (e.g. [70]).
Whilst knowledge of cold-stage refugia has been the focus
of many such studies, an important and as yet understudied
research area is the location of warm-stage refugia. Given
future climatic conditions, location of warm-stage refugia
may be more relevant in ensuring the future persistence and
genetic diversity of cool temperate species including many
endemic alpine and arctic taxa [58]. A good point in time to
examine refugia for these species is the mid-Holocene climatic optimum within 8–6 ka when, for example, summers
in northern and central Europe were 2–2.58C and winters
1–1.58C warmer than today. Clear spatial differences are
apparent in the distribution of many arctic and alpine
species during this time period and have led to the identification of pockets of so-called ‘cryptic’ refugia [44].
How can such information on cold- and warm-stage
refugia be incorporated into conservation management
and planning? In fact, the idea of refugia, particularly
those associated with previous intervals of aridity, is already being incorporated into strategic conservation planning. In a recent attempt to identify important areas for
conservation of ecological processes in Australia, for example, locations of refugia during previous intervals of aridity
(spanning a five-year period from July 2000 to June 2005)
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were incorporated into the spatial planning framework for
determining regions for conservation [3]. It was argued
that these areas provide the most probable regions of
persistence during future intervals of aridity and therefore
represent important regions for conservation. Although
this approach is predominantly focused on preserving
areas important for persistence and the ecological processes responsible for this, it will also contribute to the longevity of species and communities and thus conserve
evolutionary processes [59].
Management of novel ecosystems
Projected climate trends suggest that by 2200, up to 48% of
Earth’s land surface might experience novel climates,
leading to unexpected biotic associations [71]. There is
increasing recognition amongst conservationists that these
novel ecosystems will be markedly different from what we
know today and therefore a pragmatic management approach is needed [72–74]. At the same time, management
of these transient ecosystems calls for a greater understanding of their functioning. For instance, it is crucial to
understand whether new species combinations will lead to
new forms of community organisation, functional properties, and ecosystem dynamics [73].
Palaeoecological archives (Box 2) offer insights into
ecosystem dynamics over a range of timescales, including
those occurring over millennial scales. These archives
often span the past 20 000 years, during which the global
transition from glacial to interglacial conditions took place,
and suggest that few major terrestrial ecosystems have
remained unchanged for more than the past 12 000 years
[74]. These archives also often demonstrate that over
millennial timescales, assembly and disassembly of ecological communities are common, leading to ecosystems
with a variety of structures and functions [75,76]. For
example, Williams et al. [77] found that late-glacial eastern
North American fossil pollen assemblages deposited between 17 000–12 000 BP, indicated widespread ‘mixed
parkland’, a biome that is currently non-existent in North
America. Pollen assemblages associated with this biome
are characterised by high abundances of boreal conifers,
herbaceous pollen and broad-leaved deciduous trees, but
low abundances of pine (Pinus), alder (Alnus), and birch
(Betula). Dissimilarity analyses of fossil and modern pollen
spectra indicate that the late-glacial assemblages were
very different from modern samples. One possible explanation is that these no-analogue vegetation types might
have been linked to now-extinct Pleistocene megafaunal
communities [77]. Recently, a multi-proxy record based on
a sedimentary archive from eastern North America has
examined the relationships between the formation of nonanalogue vegetation types, changes in fire regimes, and
megafaunal declines [78]. This record suggests that the
megafaunal decline closely preceded enhanced fire regimes
and the development of non-analogue vegetation types
(Figure 4). Therefore, release from herbivory in addition
to novel climates (highly seasonal insolation and temperatures) may have led to the formation of novel vegetation
types 13 700 years ago.
Late-Pleistocene sedimentary archives from the Brazilian Amazon similarly suggest that climate cooling by up to
(Figure_4)TD$IG][ Review
Trends in Ecology and Evolution
Vol.25 No.10
services, then palaeoecological archives can provide information on what might be feasible solutions (i.e. stable
ecosystem states) and how far existing systems have
drifted from historical states. In addition, information
provided by long-term archives gives restoration ecologists
‘‘permission to accept environmental and ecological change
and to intervene in ways that foster biodiversity and vital
ecosystem functions’’ [82]. These archives also point to
conditions under which ecosystem recovery does and does
not occur and therefore inform managers about the level of
intervention needed in ecosystem restoration.
Conclusions
Palaeoecological archives of past biodiversity changes provide much relevant data for assessing biodiversity
responses to climate change. These archives indicate the
complexity of responses to climate change over time, ranging from inherent variability through to rapid compositional turnover, broad-scale migrations, regime shifts, and
the creation of novel ecosystems. They also indicate the
dynamic interactions of biotic and abiotic processes that
sometimes lead to thresholds and in other situations enable resilience and persistence. The record of these biotic
responses obtained from palaeoecological records provides
an important resource for conservation strategies to conserve and manage ecological and evolutionary processes.
Acknowledgements
We are indebted to members of the Oxford Long-term Ecology
Laboratory, Hilary Birks and Cathy Jenks for invaluable discussions
and help, and to Keith Bennett, Donatella Magri and Stephen Jackson for
perceptive comments on an earlier draft.
References
Figure 4. Summary pollen diagram from Appleman Lake, Indiana, USA for the
period 8000–17 000 years ago [78]. Only the major tree pollen types are shown.
Pollen assemblages with non-analogue modern pollen assemblages [77] occur
within 13 700–11 900 years ago (grey-shaded area). The percentage of spores of the
dung fungus Sporormiella, a record of mega-faunal presence, and number of
charcoal particles, a record of fire frequency and extent, are also shown. This multiproxy record suggests that the non-analogue pollen assemblages closely followed
in time the mega-faunal decline, whereas enhanced fire regimes began soon after
the non-analogue assemblages. Loss of mega-herbivores may have altered
ecosystem processes by the release of palatable hardwood trees from herbivore
pressure and the accumulation of combustible fuel. The non-analogue pollen
assemblages may thus have resulted from novel climates [76] and release from
mega-faunal herbivory. Adapted from Gill, J.L. et al. (2009) Pleistocene
megafaunal collapse, novel plant communities, and enhanced fire regimes in
North America. Science 326, 1100-1103. Reprinted with permission from AAAS.
5oC during the late Pleistocene [79] might have been
responsible for the formation of novel vegetation types.
Bush et al. [80] found that during late Pleistocene cooling,
Amazonian forest changed in composition due to the expansion or invasion of Andean floral elements (e.g. Podocarpus, Alnus and Drimys) creating communities of the
mesic forest biome without modern analogues.
These archival records therefore suggest that environmental and ecological changes are perhaps the most common feature of a world in continual climatic flux [81].
Jackson and Hobbs [82] argue that it is through this
long-term lens that the management of novel ecosystems
should be approached. If the goal of management is to
design novel ecosystems to provide ecological goods and
1 Pressey, R.L. et al. (2007) Conservation planning in a changing world.
Trends Ecol. Evol. 22, 583–592
2 Mace, G.M. and Purvis, A. (2008) Evolutionary biology and practical
conservation: bridging a widening gap. Mol. Ecol. 17, 9–19
3 Klein, C. et al. (2009) Incorporating ecological and evolutionary
processes into continental-scale conservation planning. Ecol. Appl.
19, 206–217
4 Boitani, L. et al. (2008) Change the IUCN protected area categories to
reflect biodiversity outcomes. PLoS Biol. 6, 436–438
5 Williams, S.E. et al. (2008) Towards an integrated framework for
assessing the vulnerability of species to climate change. PLoS Biol.
6, 2621–2626
6 Edwards, H.J. et al. (2010) Incorporating ontogenetic dispersal,
ecological processes and conservation zoning into reserve design.
Biol. Cons. 143, 457–470
7 Cadotte, M.W. and Davies, T.J. (2010) Rarest of the rare: advances in
combining evolutionary distinctiveness and scarcity to inform
conservation at biogeographical scales. Divers. Distrib. 16, 376–385
8 Elith, J. and Leathwick, J.R. (2009) Species distribution models:
ecological explanation and prediction across space and time. Annu.
Rev. Ecol. Evol. Syst. 40, 677–697
9 Ackerly, D.D. et al. (2010) The geography of climate change:
implications for conservation biogeography. Divers. Distrib. 16,
476–487
10 Kearney, M. et al., (2010) Correlative and mechanistic models of
species distribution provide congruent forecasts under climate change.
Conserv. Lett. 3, 203–213. DOI: 10.1111/j.1755-263X.2010.00097.x
11 MacDonald, G.M. et al. (2008) Impacts of climate change on species,
populations and communities: palaeobiogeographical insights and
frontiers. Prog. Phys. Geog. 32, 139–172
12 Jackson, S.T. et al. (2009) Paleoecology and resource management in
dynamic landscapes: Case studies from the Rocky Mountain
headwaters. In Conservation Paleobiology: Using the Past to Manage
589
Review
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
590
for the Future, Paleontological Society Short Course, October 17th,
2009 (Dietl, G.P. and Flessa, K.W., eds), The Paleontological Society
Papers Volume 15
Ritchie, J.C. (1995) Current trends in studies of long-term plant
community dynamics. New Phytol. 130, 469–494
Peglar, S.M. (1993) The mid-Holocene Ulmus decline at Diss Mere,
Norfolk, UK: a year-by-year pollen stratigraphy from annual
laminations. The Holocene 3, 1–13
Peglar, S.M. (1993) The development of the cultural landscape around
Diss Mere, Norfolk, UK, during the past 7000 years. Rev. Palaeobot.
Palynol. 76, 1–47
van Leeuwen, J.F.N. et al. (2008) Fossil pollen as a guide to
conservation in the Galápagos. Science 322, 1206
National Research Council (2005) The Geological Record of Ecological
Dynamics, National Academic Press
Travis, J.M.J. (2003) Climate change and habitat destruction: a deadly
anthropogenic cocktail. Proc. R. Soc. Series B-Biol. Sci. 270, 467–473
Meinshausen, M. et al. (2009) Greenhouse-gas emission targets for
limiting global warming to 2 degrees C. Nature 458, 1158-1162
Solomon, S. et al. (2007) Climate Change 2007: The Physical Science
Basis. Contribution of Working Group I to the Fourth Assessment
Report of the Intergovernmental Panel on Climate Change,
Cambridge University Press
Parry, M. et al. (2007) Climate Change 2007: Impacts, Adaptation and
Vulnerability. Contribution of Working Group II to the Fourth
Assessment Report of the Intergovernmental Panel of Climate
Change, Cambridge University Press
Huntingford, C. et al. (2008) Towards quantifying uncertainty in
predictions of Amazon ‘dieback’. Phil. Trans. R. Soc. B-Biol. Sci.
363, 1857–1864
Zachos, J. et al. (2001) Trends, rhythms, and aberrations in global
climate 65 Ma to present. Science 292, 686–693
Zachos, J.C. et al. (2008) An early Cenozoic perspective on greenhouse
warming and carbon-cycle dynamics. Nature 451, 279–283
Willis, K.J. et al. (2010) 4 degrees C and beyond: what did this mean for
biodiversity in the past? Syst. Biodiv. 8, 3–9
Jaramillo, C. et al. (2006) Cenozoic plant diversity in the Neotropics.
Science 311, 1893–1896
Willis, K.J. and McElwain, J.C. (2002) The Evolution of Plants, Oxford
University Press
Lloyd, J. and Farquhar, G.D. (2008) Effects of rising temperatures and
CO2 on the physiology of tropical forest trees. Phil. Trans. R. Soc. BBiol. Sci. 363, 1811–1817
Willis, K.J. and Bhagwat, S.A. (2009) Biodiversity and climate change.
Science 326, 806–807
Lapola, D.M. et al. (2009) Exploring the range of climate biome
projections for tropical South America: The role of CO2 fertilization
and seasonality. Global Biogeochem. Cy. 23, GB3003, DOI:10.1029/
2008GB003357
Thomas, C.D. (2010) Climate, climate change and range boundaries.
Divers. Distrib. 16, 488–495
Pitman, A.J. and Stouffer, R.J. (2006) Abrupt change in climate and
climate models. Hydro. Earth Sys. Sci. 10, 903–912
Skinner, L. (2008) Facing future climate change: is the past relevant?
Phil. Trans. R. Soc. A-Math. Phys. Eng. Sci. 366, 4627–4645
Steffensen, J.P. et al. (2008) High-resolution Greenland ice core data
show abrupt climate change happens in few years. Science 321, 680–
684
Williams, J.W. et al. (2002) Rapid and widespread vegetation responses
to past climate change in the North Atlantic region. Geology 30,
971–974
Birks, H.H. and Ammann, B. (2000) Two terrestrial records of rapid
climatic change during the glacial-Holocene transition (14,000-9,000
calendar years BP) from Europe. Proc. Nat. Acad. Sci. U. S. A. 97, 1390–
1394
Heikkila, M. et al. (2009) Rapid Lateglacial tree population dynamics
and ecosystem changes in the eastern Baltic region. J. Quat. Sci. 24,
802–815
Svenning, J.C. and Skov, F. (2007) Ice age legacies in the geographical
distribution of tree species richness in Europe. Global Ecol. Biogeog.
16, 234–245
Birks, H.H. (2008) The Late-Quaternary history of arctic and alpine
plants. Plant Ecol. Divers. 1, 135–146
Trends in Ecology and Evolution Vol.25 No.10
40 Gonzales, L.M. et al. (2009) Expanded response-surfaces: a new method
to reconstruct paleoclimates from fossil pollen assemblages that lack
modern analogues. Quat. Sci. Rev. 28, 3315–3332
41 Scherrer, D. and Körner, C. (2010) Infra-red thermometry of alpine
landscapes challenges climatic warming projections. Global Change
Biol. 16, 2602–2613
42 Scherrer, D. and Körner, C. (2010) Topography-controlled thermalhabitat differentiation buffers alpine plant diversity against climate
warming. J. Biogeog. (in press)
43 Birks, H.J.B. and Birks, H.H. (2008) Biological responses to rapid
climate change at the Younger Dryas-Holocene transition at
Krakenes, western Norway. The Holocene 18, 19–30
44 Birks, H.J.B. and Willis, K.J. (2008) Alpines, trees, and refugia in
Europe. Plant Ecol. Divers. 1, 147–160
45 Scheffer, M. et al. (2001) Catastrophic shifts in ecosystems. Nature 413,
591–596
46 Andersen, T. et al. (2009) Ecological thresholds and regime shifts:
approaches to identification. Trends Ecol. Evol. 24, 49–57
47 Smith, A.G. (1965) Problems of threshold and inertia related to
post-Glacial habitat changes. Proc. R. Soc. B-Biol. Sci. 161, 331–
342
48 Cole, K. (1985) Past rates of change, species richness, and a model
of vegetational inertia in the Grand Canyon, Arizona. Am. Nat. 125,
289–303
49 Walker, D. (1982) Vegetation fourth’s dimension. New Phytol. 90, 419–
429
50 Dearing, J.A. (2008) Landscape change and resilience theory: a
palaeoenvironmental assessment from Yunnan, SW China. The
Holocene 18, 117–127
51 Folke, C. et al. (2004) Regime shifts, resilience, and biodiversity in
ecosystem management. Annu. Rev. Ecol. Evol. Syst. 35, 557–581
52 Carrion, J.S. et al. (2001) Crossing forest thresholds: inertia and
collapse in a Holocene sequence from south-central Spain. The
Holocene 11, 635–653
53 Virah-Sawmy, M. et al. (2009) Threshold response of Madagascar’s
littoral forest to sea-level rise. Global Ecol. Biogeog. 18, 98–110
54 Jackson, S.T. et al. (2009) Ecology and the ratchet of events: Climate
variability, niche dimensions, and species distributions. Proc. Nat.
Acad. Sci. U. S. A. 106, 19685–19692
55 Figueroa-Rangel, B.L. et al. (2008) 4200 years of pine-dominated
upland forest dynamics in west-central Mexico: Human or natural
legacy? Ecology 89, 1893–1907
56 Cook, E.R. et al. (2004) Extra-tropical Northern Hemisphere land
temperature variability over the past 1000 years. Quat. Sci. Rev. 23,
2063–2074
57 Cook, E.R. et al. (2010) Asian monsoon failure and megadrought during
the last millennium. Science 328, 486–489
58 Willis, K.J. and Bhagwat, S.A. (2010) Questions of importance to the
conservation of global biological diversity: Answers from the past.
Clim. Past Discuss. 6, 1139-1162
59 Virah-Sawmy, M. et al. (2009) How does spatial heterogeneity
influence resilience to climatic changes? Ecological dynamics in
southeast Madagascar. Ecol. Monogr. 79, 557–574
60 Schaberg, P.G. et al. (2008) Anthropogenic alterations of genetic
diversity within tree populations: Implications for forest ecosystem
resilience. For. Ecol. Management 256, 855–862
61 Isaac, N.J.B. et al. (2007) Mammals on the EDGE: Conservation
priorities based on threat and phylogeny. PLoS One 2, e296 DOI:
10.1371/journal.pone.0000296
62 Hewitt, G. (2000) The genetic legacy of the Quaternary ice ages. Nature
405, 907–913
63 Douglas, M.E. et al. (2006) Evolution of rattlesnakes (Viperidae;
Crotalus) in the warm deserts of western North America shaped by
Neogene vicariance and Quaternary climate change. Mol. Ecol. 15,
3353–3374
64 Petit, R.J. et al. (2008) Forests of the past: A window to future changes.
Science 320, 1450–1452
65 Hampe, A. and Petit, R.J. (2005) Conserving biodiversity under climate
change: the rear edge matters. Ecol. Lett. 8, 461–467
66 Willis, K.J. et al. (2004) The evolutionary legacy of the Ice Ages Papers of a discussion meeting held at the Royal Society on 21 and 22
May 2003 - Introduction. Phil. Trans. R. Soc. Series B-Biol. Sci. 359,
157–158
Review
67 Bhagwat, S.A. and Willis, K.J. (2008) Species persistence in northerly
glacial refugia of Europe: a matter of chance or biogeographical traits?
J. Biogeog. 35, 464–482
68 Binney, H.A. et al. (2009) The distribution of late-Quaternary woody
taxa in northern Eurasia: evidence from a new macrofossil database.
Quat. Sci. Rev. 28, 2445–2464
69 Magri, D. et al. (2006) A new scenario for the Quaternary history of
European beech populations: palaeobotanical evidence and genetic
consequences. New Phytol. 171, 199–221
70 Puscas, M. et al. (2008) No positive correlation between species and
genetic diversity in European alpine grasslands dominated by Carex
curvula. Divers. Distrib. 14, 852–861
71 Williams, J.W. et al. (2007) Projected distributions of novel and
disappearing climates by 2100 AD. Proc. Nat. Acad. Sci. U. S. A.
104, 5738–5742
72 Wilkinson, D.M. (2004) The parable of Green Mountain: Ascension
Island, ecosystem construction and ecological fitting. J. Biogeog. 31,
1–4
73 Hobbs, R.J. et al. (2006) Novel ecosystems: theoretical and
management aspects of the new ecological world order. Global Ecol.
Biogeog. 15, 1–7
74 Jackson, S.T. (2006) Vegetation, environment, and time: The
origination and termination of ecosystems. J. Veg. Sci. 17, 549–557
75 Jackson, S.T. and Williams, J.W. (2004) Modern analogs in Quaternary
paleoecology: Here today, gone yesterday, gone tomorrow? Annu. Rev.
Earth Planet. Sci. 32, 495–537
76 Williams, J.W. and Jackson, S.T. (2007) Novel climates, no-analog
communities, and ecological surprises. Front. Ecol. Environ. 5, 475–482
77 Williams, J.W. et al. (2001) Dissimilarity analyses of late-Quaternary
vegetation and climate in eastern North America. Ecology 82, 3346–3362
78 Gill, J.L. et al. (2009) Pleistocene megafaunal collapse, novel plant
communities, and enhanced fire regimes in North America. Science
326, 1100–1103
79 Stute, M. et al. (1995) Cooling of tropical Brazil (5-Degrees-C) during
the Last Glacial Maximum. Science 269, 379–383
80 Bush, M.B. et al. (2004) Amazonian paleoecological histories: one hill,
three watersheds. Palaeogeog. Palaeoclim. Palaeoecol. 214, 359–393
81 Jackson, S.T. and Overpeck, J.T. (2000) Responses of plant populations
and communities to environmental changes of the late Quaternary.
Paleobiology 26 (Suppl.), 194–220
Trends in Ecology and Evolution
Vol.25 No.10
82 Jackson, S.T. and Hobbs, R.J. (2009) Ecological restoration in the light
of ecological history. Science 325, 567–569
83 Bronk Ramsey, C. (2008) Radiocarbon dating: revolutions in
understanding. Archaeometry 50, 249–275
84 Duller, G.A.T. (2004) Luminescence dating of Quaternary sediments:
recent advances. J. Quat. Sci. 19, 183–192
85 Aitken, M.J. (1985) Thermoluminescence Dating, Academic Press
86 Thomas, A.L. et al. (2009) Penultimate deglacial sea-level timing from
uranium/thorium dating of Tahitian corals. Science 324, 1186
87 Wand, Y. et al. (2008) Millennial- and orbital-scale changes in the East
Asian monsoon over the past 224,000 years. Nature 451, 1090–1093
88 Hughes, M.K. (2002) Dendrochronology in climatology—The state of
the art. Dendrochronologia 20, 95–116
89 Svensson, A. et al. (2008) A 60 000 year Greenland stratigraphic ice
core chronology. Clim. Past 4, 47–57
90 Ruddiman, W.F. (2003) Orbital insolation, ice volume, and greenhouse
gases. Quat. Sci. Rev. 22, 1597–1629
91 Lisiecki, L.E. and Raymo, M.E. (2005) A Plio–Pleistocene stack of 57
globally distributed benthic delta18O records. Paleoceanography 20,
1003
92 Royer, D.L. et al. (2001) Phanerozoic atmospheric CO2 change:
evaluating geochemical and paleobiological approaches. Earth-Sci.
Rev. 54, 349–392
93 Royer, D.L. (2006) CO2-forced climate thresholds during the
Phanerozoic. Geochim. Cosmochim. Acta 70, 5665–5675
94 NGRIP members (2004) High-resolution record of Northern Hemisphere
climate extending into the last interglacial period. Nature 431, 147–151
95 EPICA community members (2004) Eight glacial cycles from an
Antarctic ice core. Nature 429, 623–628
96 Thompson, L.G. (2005) Tropical ice core records: evidence for
asynchronous glaciation on Milankovitch timescales. J. Quat. Sci.
20, 723–733
97 Masson-Delmotte, V. et al. (2005) GRIP deuterium excess reveals rapid
and orbital-scale changes in Greenland moisture origin. Science 309,
118–121
98 Jouzel, J. et al. (2007) The GRIP deuterium-excess record. Quat. Sci.
Rev. 26, 1–17
99 Brooks, S.J. and Birks, H.J.B. (2000) Chironomid-inferred late-glacial
and early-Holocene mean July air temperatures for Kråkenes Lake,
western Norway. J. Paleolimnol. 23, 77–89
591