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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) 583–591 583 Review 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. 584 Trends in Ecology and Evolution Vol.25 No.10 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]). Review 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] Trends in Ecology and Evolution Vol.25 No.10 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 585 (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 586 Trends in Ecology and Evolution Vol.25 No.10 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]. (Figure_3)TD$IG][ Review Trends in Ecology and Evolution Vol.25 No.10 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. 587 Review 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) 588 Trends in Ecology and Evolution Vol.25 No.10 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. 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