Quaternary Science Reviews · Invited Review Quaternary palaeoecology and nature conservation: a general review with examples from the neotropicsq T. Vegas-Vilarrúbiaa,*, V. Rullb,

lable at ScienceDirect

Quaternary Science Reviews 30 (2011) 2361e2388

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Quaternary Science Reviews

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Invited Review

Quaternary palaeoecology and nature conservation: a general reviewwith examples from the neotropicsq

T. Vegas-Vilarrúbia a,*, V. Rull b, E. Montoya b,c, E. Safont b

aDepartment of Ecology, University of Barcelona, Av. Diagonal 645, 08028 Barcelona, Spainb Palynology and Palaeoecology Lab, Botanical Institute of Barcelona (CSIC-ICUB), Pg. del Migdia s/n, 08038 Barcelona, SpaincDepartment of Animal Biology, Plant Biology and Ecology, Autonomous University of Barcelona, Faculty of Biosciences, Bld C1, Cerdanyola del Vallès, 08193 Barcelona, Spain

a r t i c l e i n f o

Article history:Received 12 March 2011Received in revised form5 May 2011Accepted 7 May 2011Available online 20 June 2011

Keywords:Long-term ecologyPalaeoclimatesBiotic responsesResilienceThreshold responsesPast analoguesGlobal changeHuman disturbanceAbrupt changesGradual changesTropical America

q This paper is dedicated to Margaret Bryan Davis fodevelopments.* Corresponding author. Tel.: þ34 934031376; fax:

E-mail addresses: [email protected] (T. Vegas-Vilarrú

0277-3791/$ e see front matter � 2011 Elsevier Ltd.doi:10.1016/j.quascirev.2011.05.006

a b s t r a c t

Palaeoecology, as an ecological discipline, is able to provide relevant inputs for conservation science andecosystem management, especially for issues involving long-term processes, such as ecological succes-sion, migration, adaptation, microevolution, and extinction. This use of palaeoecology has been noted forseveral decades, and it has become widely accepted, especially in the frame of ongoing and near-futureglobal warming and its potential biotic consequences. Selected palaeoecological insights of interest forconservation include the following: 1) species respond in an individualistic manner to environmentalchanges that lead to changes in community composition, suggesting that future ecosystems would haveno modern analogues; 2) in the short-term, acclimation is more likely a response of species that areexpected to persist in the face of global warming, but the possibility of evolutionary change linked to theexistence of pre-adapted genomes cannot be dismissed; 3) species unable to acclimate or adapt to newconditions should migrate or become extinct, which has been observed in past records; 4) currentextinction estimates for the near-future should be revised in light of palaeoecological information, whichshows that spatial reorganisations and persistence in suitable microrefugia have been more commonthan extinction during the Quaternary; 5) biotic responses to environmental changes do not necessarilyfollow the rules of equilibrium dynamics but depend on complex and non-linear processes that lead tounexpected “surprises”, which are favoured by the occurrence of thresholds and amplifying positivefeedbacks; 6) threshold responses can cause the movement of ecosystems among several potentiallystable states depending on their resilience, or the persistence of transient states; 7) species and theircommunities have responded to environmental changes in a heterogeneous fashion according to thelocal and regional features, which is crucial for present and future management policies; 8) the globalwarming that occurred at the end of the Younger Drays cold reversal (ca 13.0 to 11.5 cal kyr BP) tookplace at similar rates and magnitudes compared to the global warming projected for the 21st century,thus becoming a powerful past analogue for prediction modelling; 9) environmental changes have actedupon ecosystems in an indirect way by modifying human behaviour and activities that, in turn, have hadthe potential of changing the environment and enhancing the disturbance effects by synergisticprocesses involving positive feedbacks; 10) the collapse of past civilisations under climate stress has beenchiefly the result of inadequate management procedures and weaknesses in social organisation, whichwould be a warning for the present uncontrolled growth of human population, the consequent over-exploitation of natural resources, and the continuous increase of greenhouse gas emissions; 11) theimpact of fire as a decisive ecological agent has increased since the rise of humans, especially during thelast millennia, but anthropic fires were not dominant over natural fires until the 19th century; 12) firehas been an essential element in the development and ecological dynamics of many ecosystems, and ithas significantly affected the worldwide biome distribution; 13) climateefireehuman synergies thatamplify the effects of climate, or fire alone, have been important in the shaping of modern landscapes.

r her pioneering work in palaeoecology and its applications to nature conservation, which set the stage for all further

þ34 934111438.bia), [email protected] (V. Rull), [email protected] (E. Montoya), [email protected] (E. Safont).

All rights reserved.

T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e23882362

These general paleoecological observations and others that have emerged from case studies of particularproblems can improve the preservation of biodiversity and ecosystem functions. Nature conservationrequires the full consideration of palaeoecological knowledge in an ecological context, along with thesynergistic cooperation of palaeoecologists with neoecologists, anthropologists, and conservationscientists.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

This paper reviews the most significant literature available onthe usefulness of palaeoecology in the field of nature conservationto extract the more relevant lessons from the past to improvepresent and future ecosystem management. This paper alsoprovides several selected case studies from the Neotropical regionto show how palaeorecords can address real conservation prob-lems, with assessments and recommendations of immediateapplicability. This review also attempts to be a service to thepalaeoecological community to facilitate access to the more rele-vant knowledge and related literature on the subject. In addition,we hope that this contribution may enhance the interest ofpalaeoscientists on the importance of our disciplines for conser-vation, thereby promoting discussion and hopefully leading to thecontinuous improvement of our skills. Our approach is based on thebroad concept of ecology, which is seen as a discipline embracingpalaeoecology, neoecology and predictive ecology. Interactionbetween these disciplines is needed for a proper understanding ofthe biosphere and its functioning and to deal with its potentialreactions to future environmental change (Rull, 2010a). Asexpressed in the title, the emphasis is on global warming and fire asenvironmental stressors; other subjects, such as eutrophication,acidification, pollution, and soil erosion, have been reviewed anddiscussed elsewhere (e.g., Smol, 2008; Pelejero et al., 2010; Albrightet al., 2010). Emphasis will be placed on the Quaternary (i.e., the last2.58 million years (Ma), as defined by Gibbard et al. (2010);however, references to former periods will be included whennecessary.

The review begins with a discussion of the meaning of “long-term” in ecology to set a suitable temporal framework and toemphasise that neoecology and palaeoecology, despite methodo-logical differences, share common objectives. The second part isa summary of the biotic responses documented so far to pastclimate changes, and their significance to ongoing and future globalwarming. Following these sections, a summary is provided of keydevelopments in the applications of palaeoecology to conservation.This account is based mainly on review papers and aims to intro-duce the relevant concepts in a historical fashion and highlight theleading researchers and research groups in this field. The nextsection concerns potential past analogues for projected globalwarming, which could be used in forecast modelling. The anthropicfactor is then introduced in the section about indirect impacts ofclimatic change. This section is devoted to the possibility of dis-entangling natural from human causes for past ecological changesand records those situations in which synergies between these twodrivers have determined a priori unexpected ecological responses.Fire, which is among themore influential ecological disturbances ofanthropic origin, is then discussed based on its occurrence patternsand incidence throughout Earth’s history, with an emphasis on itsnatural or human-induced nature since the last glacial period,when present-day ecosystems developed. Concerning examples ofthe usefulness of past records for conservation, we use our ownwork in the Neotropical region of northern South America, mainlyin the Andean highlands, the Gran Sabana midlands, and thesummits of the Guayanan tabular mountains, or tepuis. We provide

past analogues for rapid and gradual climatic changes and fire,acting either separately or simultaneously, along with theirecological consequences. Finally, the main conclusions of thisreview are identified, and we highlight several conservationrecommendations derived from these conclusions.

2. Ecology and palaeoecology: what is long-term?

Presently, it is widely acknowledged that short-term ecologicalstudies are not enough for reliable predictions on the potentialconsequences of future environmental changes and humandisturbance, and long-term surveys are increasingly recognised asa necessary tool for this purpose (e.g., Huntley, 1996; Jackson,2001). However, there is no agreement on the meaning of short-term and long-term. For example, in a recent special issue ofTrends in Ecology and Evolution entitled “Long-term ecologicalstudies”, most papers deal with data extending to a couple ofdecades, and only one uses a palaeoecological approach (Williset al., 2010a). There is no standard definition for long-term inecology, but some explicit statements within papers on the subjectconsider a lower boundary between 20 and 50 years for long-termstudies (Willis et al., 2007a).

For obvious reasons, the connection between palaeoecology andconservation science has many coincidences with the relationshipbetween ecology and palaeoecology that, despite what their namesmay suggest, have progressed historically as separate disciplines.According to Rull (2010a), this unfortunate disjunction has beenfacilitated by the following: 1) the pastepresent dissociationcharacteristic of the human mind, 2) the diversity of fields ofprovenance for palaeoecologists, 3) the contrasting nature of theevidence and associated methodological differences, and 4)misunderstandings caused by the use of the prefix palaeo-.However, the principle of uniformitarianism emphasises that past,present and future are not discrete units, but rather a timecontinuum through which species and communities flow, changeand evolve, and that ecology and palaeoecology are simply differentapproaches with a common objective, which is the ecologicalunderstanding of the biosphere. Ecology, in a broad sense, includesinferences about the past (palaeoecology), present studies (neo-ecology or contemporary ecology) and future projections (predic-tive ecology). Therefore, palaeoecology is essentially communityecology stretched backward through the fourth dimension of time(Schoonmaker and Foster, 1991), or it can also mean ecologicalstudies that use the past as proxies (Rull, 2010a). In this context,long-term should have a single meaning.

The importance of temporal and spatial scales in ecology andpalaeoecology has been emphasised by Delcourt and Delcourt(1988). More recently, Jackson (2001) has distinguished threetime domains useful to deal with the ecologyepalaeoecologycontinuity. These domains are as follows: real-time, which is thetime frame usually considered in neoecology, which spans fromweeks to decades and includes processes such as populationdynamics, competition or predatoreprey interactions; Q-time(where Q is for Quaternary), which ranges from centuries tomillennia, encompasses processes such as succession, migration orextinction; and deep-time, which includes a wide range of

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timescales typically over 105 years and accounts for evolutionarytrends and large-scale biogeographic reorganisations. The timelength of the processes mentioned above depends on the organ-isms involved, mainly in relation to their generation times and theduration of their biological cycles. For example, ecological succes-sion in plankton communities may elapse over a year or merelya season, whereas in a forest, it may take centuries or millennia tooccur. Therefore, a multidecadal study would be able to captureactual long-term processes for the first case, but it is clearlyinsufficient in the second case. Therefore, it seems appropriate torefer to real-time phenomena as short-time ecological processes,and to use long-term for ecological processes occurring at Q-timescales (Rull and Vegas-Vilarrúbia, 2011). This will be theconvention used in this paper. Therefore, real long-term ecologicalstudies and, hence, conservation science need evidence from thepast, that is, palaeoecological input.

3. Biotic responses to environmental change: past and future

Forecasts about the nature of future responses to climate changeand other environmental disturbances require a deep knowledge ofthe past and present biotic responses to the same or similarecological forcings. Palaeoecology has provided decisive evidenceon the responses of organisms and their communities to pastenvironmental shifts, mainly in relation to climate changes. Multi-proxy studies are especially well suited for this purpose becausethey furnish independent physical and/or chemical evidence ofenvironmental change and avoid potential circular reasoning.Important aspects of the biotic responses to environmental shiftsare the nature (individualistic or collective), the type (migration,extinction), the magnitude and extent (local, regional, global), thetime lags with respect to the environmental shift, and the rates ofchange. Palaeorecords of these features can be used as pastanalogues to infer potential future responses of organisms andcommunities to the predicted future environmental changes. Therecords can also be used to disentangle natural from anthropiccauses of ecological change. Hewitt and Nichols (2005) have syn-thesised the three more important types of biotic responses in theexpression “adapt, move or die”, which equates to evolution, rangeshifts or extinction. However, there is a fourth possibility, which ispersistence, despite environmental change, because of phenotypicplasticity in the less sensitive species (Davis et al., 2005). Accordingto the palaeorecords, there are fivemainmodes inwhich organismsand communities respond to climatic variations: growth or death,species migration, changes in community composition, evolu-tionary changes, and extinction (Overpeck et al., 2003). The natureof the response depends on the scale, considered in both space andtime (see also Delcourt and Delcourt, 1988). The following sectionprovides an updated summary of the main elements required forthe evaluation of biotic responses to external factors based on theinformation provided by past records.

3.1. Individualistic responses and non-analogue communities

The issue of the individualistic (at the species level) vs. collective(at a community level) biotic responses has been a long ecologicaldebate between the Gleasonian and the Clementsian schools, whichare defenders of the first and second option, respectively (Clements,1916; Gleason, 1926). The classical works of Davis (1981) in NorthAmerica and Huntley and Birks (1983) in Europe have shown thatpostglacial recolonisationof thesecontinentsby trees fromtemperateforests proceeded in an individual fashion, and, as a consequence,current forests are composed of species that arrived at different timesfromvarious southernglacial refugia (SchoonmakerandFoster,1991).Furthermore, individual differences in response lags and migration

rates complicated thepicture. Another important consequence is thatcommunities have not been constant through time, suggesting thatthey are loose and relatively ephemeral assemblages of species pop-ulations, as formerly proposed by Whittaker (1951). Further palae-oecological evidence has reinforced this view (Bennett, 1997, andliterature therein). The projection of these results into the futureallowed researchers to prognosticate that, by the end of this century,the occurrence of novel climates and biotic communities with nomodern analogueswill be commonon the planet as a consequence ofongoing climate change (Williams and Jackson, 2007;Williams et al.,2007). Therefore,managementprocedures shouldadapt to thesenewcombinations, with unknown community organisation, functionalproperties and ecosystem dynamics (Hobbs et al., 2006; Willis et al.,2007b; Willis and Bhagwat, 2010). Current predictions of non-analogue or novel communities are based on ecological models par-ameterised from present-day observations that may fail to predictecological responses to novel climates. These models should be vali-dated against palaeoecological evidence to enhance their robustnessand predictive accuracy (Williams and Jackson, 2007).

Key elements to be considered in the individualistic behaviourof species in relation to environmental change include particulardifferences in their sensitivity to relevant environmental factors,response lags and migration ability, and the availability of specificniche requirements (suitable substrates, pollinators, etc.). Thesefactors would constitute a handicap for many organisms to trackthe projected climate change at similar rates. In principle, it couldbe assumed that organisms with short lifecycles (e.g., planktonicorganisms) would respond faster than thosewith longer generationtimes, such as trees, which could take decades to centuries torespond (Davis, 1985). However, several recent palaeoecologicalrecords have depicted short or absent time lags between rapidenvironmental shifts and a varied array of organisms, includingcladocera, chrinomids and vascular plants (Ammann et al., 2000;Birks and Birks, 2008). Historical records have also shown rela-tively rapid migrational responses (1 to several m per year,depending on the species) of vegetation to the global warmingexperienced during the last century, especially in the form of alti-tudinal and latitudinal migrations (Walther et al., 2002; Parmesanand Yohe, 2003; Parmesan, 2005, 2006; Kelly and Goulden, 2008;Lenoir et al., 2008; and literature therein). Therefore, according topalaeoecological and historical records, the capacity of organismsto track the ongoing climate change at similar rates seems to behigher than previously expected.

3.2. Migration and microrefugia

The more common biotic response to climate change during theQuaternary seems to have been migrational range shifts (Davis andShaw, 2001; Seppä and Bennett, 2003). The better known examplesof this are the postglacial recolonisations of northern temperatecontinents by tree forest species from southern refugia witha favourable climate, where they endured the last glaciation (Davis,1981;Huntley andBirks,1983). This led to estimatedmigration ratesbetween 100 and 1000 m/year, which are unrealistic consideringthe known dispersal mechanisms of the species involved (Clarket al., 2003; MacLachlan et al., 2005). Alternatively, migrationcouldhave also proceeded fromnumerous,more or lesswidespread,microrefugia, or “small areas with local favourable environmentalfeatures, in which small populations can survive outside their maindistribution area (the macrorefugium), protected from the unfav-ourable regional environmental conditions” (Rull, 2009c). Theexpansion of these widespread, small populations, favoured bypostglacial warming, is more consistent with the relatively rapidcontinental colonisation rates under the current dispersal mecha-nisms of these tree species (Pearson, 2006). These microrefugia are

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difficult to identifywith commonpalaeoecologicalmethodsbecauseof their assumed small size and unknown distribution (Rull, 2010b),but intra-specific genetic patterns of the involved species provideevidence of their existence and suggestions for their geographicaldistribution (Willis and van Andel, 2004; Bhagat and Willis, 2008;Petit et al., 2008; Provan and Bennett, 2008). The idea of micro-refugia is not only interesting for migration rates and species’genetic structure but also for biodiversity conservation purposesbecause hypothetical future microrefugia (natural or artificiallycreated) could help to mitigate the extent of the projected bioticextinction resulting from climate change by providing suitablemicrohabitat conditions for threatened species (Rull, 2009c).According to Davis and Shaw (2001), past records show that rangeshifts and genetic adaptation proceeded together during theQuaternary climatic changes and could not be considered alterna-tive biotic responses, but this topic will be analysed further in thenext section. The potential of palaeoecology records, especiallypollen, macrofossil and charcoal records, for the reconstruction ofplant migration and invasion patterns in both space and time hasbeen reviewed by Mitchell (2010), who emphasises the need forenhanced mapping of pollen and biomes on continental and globalscales and more collaborative efforts among palaeoecology,community ecology and genetic studies to improve the testing ofecological hypotheses.

3.3. Acclimation and adaptation

Sensitivity is another key parameter to understand the reactionsof organisms to environmental changes. In principle, the moresensitive species should be those with a narrow tolerance for therelevant environmental variables (stenotopic), or those living nearthe edge of their ranges. Eurytopic species, with a large phenotypicplasticity, should be less sensitive to changes, especially if they livefar from their range boundaries. In every case, to produce a bioticresponse, a given environmental change should cross a thresholddetermined by the range of tolerance of the involved species. Theprocess by which a species resists an environmental changebecause of its wide tolerance or phenotypic plasticity is calledacclimation, whereas adaptation involves genetic (i.e., evolu-tionary) changes. There is the general a priori perception that thehigh rates of climate change predicted for the near-future willprevent genetic adaptation, but some authors think that the role ofadaptation as a response to future climate change has been over-looked. According to these authors, populations may adapt to thenew climates through the occurrence of pre-adapted individualsthat can eventually increase their density (Davis and Shaw, 2001;Kelly et al., 2003). Indeed, species can adapt to new environmentsby either waiting for the appearance of novel, advantageousmutations or evolving immediately using alleles from the standing(pre-existing) genetic variation (Stapley et al., 2010). Therefore,the adaptation of populations to a different climate will depend onthe level of climate-related genetic variability already contained inthe population. Another source of adaptive genetic variation isadmixture and the resulting gene flow between two divergentpopulations (Barrett and Schlutter, 2008). In the case of relativelycontiguous populations, adaptation may be aided by migration(Jump and Peñuelas, 2005). These hypotheses, however, are diffi-cult to confirm or reject with the traditional Quaternary palae-oecological methods (Seppä and Bennett, 2003) because of lowertaxonomical resolution than required, and they have been evalu-ated in combination with molecular phylogenetic evidence (Williset al., 2003).

Recent molecular phylogenetic studies have shown thatQuaternary speciation has indeed occurred -for example, humansare only a 200,000-year-old Quaternary species (Tattersall and

Schwartz, 2009)- and has been important in many biomes (e.g.,Richardson et al., 2001; Lister, 2003; Rull, 2008; Valente et al.,2010); however, given the rapid rate at which the ongoingclimate change is predicted to occur during this century, it isdifficult to develop potential analogies. Hewitt and Nichols (2005)have reviewed this topic and concluded that there is no conclu-sive evidence supporting or denying genetic adaptation to changingclimates in the recent past. Palaeoecological records since the LastGlacial Maximum (LGM) show that changes in distribution fuelledby climate changes have had important consequences for intra-specific genetic diversity (see also Hewitt, 2000, 2003; Lascauxet al., 2003; Magri, 2008). The key question is if genetic changeshave persisted long enough to be fixed and, if so, if the standinggenetic diversity has influenced species’ fitness.

According to Davis et al. (2005) and Lavergne et al. (2010), bioticresponses to climate changes involve both ecological and evolu-tionary elements that cannot be disentangled. For example,responses, such as persistence, migration or extinction, are inti-mately linked to microevolutionary reorganisation that influencesspecies’ sensitivity and adaptation ability (Davis et al., 2005).Microevolution also affects ecosystem assembly and functioning(Cavender-Bares et al., 2009); therefore, emergent properties, suchas biodiversity or stability, affect not only the response to envi-ronmental changes but also future evolutionary trajectories.Therefore, the incorporation of eco-evolutionary feedbacks isneeded for biodiversity forecasting, and for a better understandingof ecological dynamics in relation to anthropic environmentalchanges (Lavergne et al., 2010). Currently, models to properlyforecast potential adaptation to environmental change are underdevelopment (Salamin et al., 2010). We should also note that thestructure and survival of source populations and their geneticlegacy may be endangered for many species, and the need foridentifying and conserving glacial refuge areas should beemphasised (Hewitt and Nichols, 2005).

3.4. Extinction

Extinction occurs when all the other potential responses fail.Under changing environments, extinction of a species may resultfrom an inability to migrate and to resist or adapt to changes, but itmay also occur if the species’ habitat is lost or fragmented/reducedto the extent that populations lack the genetic variability to survivenatural perturbations, such as extreme climatic events, epidemics,and fire (Overpeck et al., 2003). Additionally, because of theecological interplay within the ecosystem, the extinction of certainkey and/or dominant species may generate cascade effects affectingother related species (hosts, parasites, pollinators, etc.) in the formof the so-called secondary extinctions (e.g., Lafferty and Kuris,2009). Biodiversity loss by increased extinction because of direct(habitat fragmentation, pollution, fire) or indirect (global warming)consequences of human activities is a common output of predictivemodels for the end of this century (e.g., Thomas et al., 2004;Peterson et al., 2005). Some believe that the ongoing and futurehuman-induced global biodiversity reduction is comparable to oneof the five major extinctions that have occurred in the geologicalhistory of Earth (Courtillot, 1999), and they term it the sixthextinction (Wake and Vredenburg, 2008).

At a human time scale, the last significant extinction eventoccurred between 50,000 and 10,000 years ago, when most largemammals became extinct everywhere except Africa (Koch andBarnosky, 2006; Barnosky, 2009). Contrastingly, there is evidencefor the extinction of one single plant species (Picea critchfieldii,a spruce) in North America during the same period (Jackson andWeng, 1999). The competing causal mechanisms for mammalextinction were either climate change or human activities;

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however, it is now widely accepted that the extinction was causedby the synergy of both, especially the coincidence of the YoungerDryas cooling (ca 13.5 to 11.5 kyr BP) and increased human hunting(Barnosky and Lindsey, 2010). This has been considered a potentialanalogy for the present and the near-future because of the coinci-dence of rapid climate change and increased humanpopulation anddisturbance. In this sense, it is important to note that the failure toadjust to changing climates did not arise from themagnitude alone,but also from the rapid rates of change. Generally, a complicatingfactor to avoid extinction by biotic adjustment to environmentalchanges is that these have occurred at different rates and magni-tudes and over different temporal and spatial scales, thus causingdisequilibrium or dynamic equilibrium between the environmentand the biotic communities (Overpeck et al., 2003).

A contrasting view is provided by Willis et al. (2010b), who hasnoted that, in the fossil record, global extinctions due solely toglobal warming are very rare (mammal extinctions are associatedmainly to human action in this case), suggesting that extinctionrates because of future climate change would have been over-estimated (see also Pearson, 2006). This would be due in part to thecoarse scale of the models used to estimate habitat loss, which failto capture potential microclimatic features that could help speciesavoid extinction (Willis and Bhagwat, 2009; Sublette et al., 2011).Indeed, recent models using more detailed topographies haveresulted in less catastrophic extinction predictions (e.g., Randinet al., 2009; Hole et al., 2009). According to Willis and Bhagwat(2009), the more likely responses of future ecosystems to climaticchange will be, like in the past, rapid community turnovers, broad-scale migrations, threshold events and the formation of novelecosystems. This would be valid for widely distributed species, butlocal extinction, which has been well documented by palae-oecology (e.g., Postigo-Mijarra et al., 2010; González-Sampérizet al., 2010 and literature therein), can be fatal for endemic species.

3.5. Spatial heterogeneity

An important lesson from palaeoecological studies is that, likethe physical changes, the biotic responses have not been homoge-neous throughout the planet. Indeed, palaeoecological evidencehas shown that, in northern temperate latitudes, the most impor-tant responses of biota to past change have been migrations, orchanges in the spatial extent and location of species’ ranges, andextinctions by habitat loss. Adaptive responses have also beenrecorded, but mostly from persistent environmental shifts. Conse-quently, it was predicted that the main response to future climatechange will consist of extinctions and individual range adjust-ments, whereas evolutionary change will be limited (Huntley,2005). In the southern continents, human activities seem to havebeen decisive for current biotic patterns, and climate variability wasconsidered at least as important as climate absolutes in governingbiodiversity responses. Therefore, these two factors are consideredto be the most significant for future biotic patterns. Based on thepalaeoecological evidence, it was predicted that range adjustmentsto future climate changewill be difficult or impossible inmost casesbecause of the current, severe habitat fragmentation. Competitionwith introduced alien species will likely be another complicatingfactor for the survival of native species (Markgraf and McGlone,2005).

In the tropics, available palaeoecological evidence supports theobservation that species have been more resilient to climaticchange, and extinction has been rare. The main response to envi-ronmental shifts seems to have been changes in communitycomposition because of the individualistic behaviour of species.Therefore, it was prognosticated that, under future climatic change,species will expand or contract their ranges and determine the

replacement of current communities by novel species combina-tions. As a result, emphasis for biodiversity conservation was notplaced on the preservation of communities but on the maintenanceof species’ ecological niches (Bush and Hooghiemstra, 2005). Con-cerning marine ecosystems, the observed responses to past envi-ronmental shifts have been varied, ranging from largebiogeographical reorganisations to insignificant changes, even inthe face of significant climate changes, such as the gla-cialeinterglacial alternation, as in the case of corals (Roy andPandolfi, 2005). Similarly, some past climatic events seem to havedetermined widespread extinctions, whereas others of similarintensity have not. The cause of these heterogeneous patternsremains unknown. According to the same authors, a possiblesynergistic relationship between climate change and the conse-quences of human activities, primarily in the form of habitatdegradation and biodiversity loss, will be important for under-standing future marine responses to climate change.

3.6. Transient and non-linear responses

Potential future biotic responses to global change are oftenapproached by biome simulations, which implicitly assume bioticequilibrium responses. However, palaeoecological records haveshown that this equilibrium between organisms and climate israrely attained, and most of the time, the responding biota showsa transient response to environmental fluctuations characterised byextended time lags. This response, combined with the potentialoccurrence of unpredictable responses and the existence of positivebiosphere-climate feedbacks that can magnify both environmentalchanges and biotic responses, severely constrains the possibility ofanticipating future threats to biodiversity and ecosystem dynamics,even if future climatic changes are well known (Overpeck et al.,2003).

During the past decades, the concept of non-equilibriumecology has emerged, emphasising the complexity and non-linearity of ecosystem dynamics that explains such behaviour(Holling, 1973; May, 1977). According to the non-equilibriumconcept, rare events, management disturbances and resourceexploitation have the potential to move the systems betweenmultiple stable states. No large impacts are needed to promotedramatic shifts; even a tiny incremental change in conditions cantrigger a catastrophic shift if a critical threshold is passed (Hollinget al., 1995). Complex interactions, such as positive feedback,would account for this pathway (Suding and Hobes, 2009). In thiscontext, equilibrium would be a temporary artefact of observation,not an intrinsic system property (Wallington et al., 2005). There aresome recent examples that illustrate how such changes occursuddenly (Scheffer and Carpenter, 2003 and literature therein).

Sudden and unexpected responses in the behaviour of envi-ronmental and ecological systems have been called surprises(Broecker, 1987; Overpeck, 1996). Concerning conservation, themore important surprises seem to be those linked to abruptthreshold-crossing changes manifested as “jumps” in the palae-oecological records. Given the complexity and non-linearity ofnature, these jumps should be expected to occur in the future ina stochastic fashion, much as they have occurred in the past.Palaeoecology may be useful for predicting their occurrence,understanding their causes, and preventing their biotic conse-quences. The non-linear dynamics of the earth system and theexistence of thresholds, which, if crossed, may determine abruptand unexpected environmental and biotic changes, have also beenhighlighted by Bradley et al. (2003), who declared that the messagefrom the palaeorecords is that change is normal and the unex-pected can happen. According to these authors, abrupt responses togradual forcing are common in past records at all time and space

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scales. They also provide some selected examples. The upper andlower bounds within which atmospheric CO2 concentrations havevaried over the past four glacial cycles seem to be thresholds for theglobal carbon cycle, which influences photosynthetic efficiency.The glacial/interglacial cycles are thought to be threshold responsesto gradual insolation changes. Another threshold is the potentialmigration rate of organisms, which may determine their extinctionif environmental change proceeds faster. Willis and Bhagwat (2010)provide selected palaeoecological examples of ecological thresh-olds. If these thresholds are crossed, the ecosystem switches fromone stable state to another within a relatively short-time interval.Human impact is emphasised as a driver of these switches.

Another non-linear dynamic feature common to past climateand environmental processes is hysteresis, or the irreversibility ofchanges once a given threshold has been crossed. Examples of thisbehaviour are the thermohaline circulation shutdown thatoccurred at the onset of the Younger Dryas cold event and thepresent-day increase in atmospheric CO2 (Bradley et al., 2003).

3.7. Resilience

Resilience was formerly defined in ecological terms as themagnitude of disturbance that an ecosystem can experience beforeit shifts into a different stability domain (Holling, 1973), or, in otherwords, before crossing a threshold towards another stable state(Willis and Bhagwat, 2010). Ecological resilience was re-defined byFolke et al. (2004) as the capacity of an ecosystem to absorbdisturbance and reorganise to retain the same function, structure,identity, and feedbacks. It is believed that the resilience ofecosystems is being constantly eroded by the ongoing environ-mental deterioration because of human activities, resulting insystems that are progressively more vulnerable to changes thatcould have previously been absorbed (Folke et al., 2004). Therefore,in conservation ecology, it is essential to know how, when and whya given ecosystem is approaching a critical resilience threshold toadopt more adequate policies (Scheffer et al., 2009). According toRockström et al. (2009), humanity has already transgressed three ofthe nine known critical environmental thresholds, including therates of climate change and biodiversity loss and the interferencewith the nitrogen cycle.

Palaeoecology provides illustrative examples of ecosystemresilience to environmental change at several temporal domains,occasionally followed by threshold responses, which are often, butnot always, linked to climatic surprises and human impact (Carriónet al., 2001, 2010; Willis et al., 2007b; Willis and Bhagwat, 2010). Adetailed analysis of these past records can be useful to identify thenature, extent and magnitude of external forcings needed to affectrelevant ecosystem properties (i.e., biodiversity or composition)and improve conservation strategies. Of great interest is thepotential for palaeoecological records to provide information aboutthe combinations of biotic and abiotic processes that determineecosystem resilience and the multiplicity of potential equilibriumstates, which are two aspects considered critical for future biodi-versity conservation (Willis et al., 2007b).

4. Palaeoecology and conservation: historical background

Several reviews have been published recently by eminentscholars on the usefulness of a palaeoecological approach fornature conservation, with emphasis on biodiversity issues (e.g.,Lyman, 2006; MacDonald et al., 2008; Smol, 2008; Dietl and Flessa,2009; Davies and Bunting, 2010; Willis et al., 2007a, 2010a, amongothers). These papers already provide an excellent summary of thefindings on this subject. Here, we will only summarise them ina historical and conceptual fashion to provide a sound background

for our own approach. The following historical review should not beconsidered a comprehensive account of all the papers and authorsinvolved in the development of this field. Rather, it is an attempt toshow how the main concepts have progressively emerged throughtime to conform to the present state of the art. Despite the relativelyshort-time elapsed, barely two decades, the evolution of ideas andproposals on this topic has been intense, likely because of thesound ecological background of the leading scholars involved.

The importance of palaeoecological knowledge for natureconservation began after 1960, when it was realised that manyenvironments were seriously threatened by eutrophication, acidi-fication, pollution and accelerated soil erosion (Oldfield, 2004). Acouple of decades ago, the discussion about future global climaticand environmental changes, and their potential impact on Earth’slife, determined the full establishment of palaeoecology as animportant input for nature conservation (Delcourt and Delcourt,1991). The International GeosphereeBiosphere Programme (IGBP)was created in 1986 by the International Council of ScientificUnions (ICSU) to study the interactions between biological, chem-ical and physical processes and interactions with human systems todevelop and impart the understanding necessary to respond toglobal change (http://www.igbp.net). In 1991, PAGES (Past GlobalChanges) was launched as a core project of the IGBP to supportresearch aimed at understanding the Earth’s past environment tomake predictions for the future (http://www.igbp-pages.org).Therefore, PAGES is responsible for palaeoecological knowledge inthe context of global change. Despite this official appointment, therole of palaeoecology in conservation, and in ecological science ingeneral, has often been underrated by many scholars and institu-tions, and palaeoecological results have traditionally had littleimpact on ecological thinking (McGlone, 1996). This has favouredthe proliferation of reviews and opinion papers from palae-oecologists trying to convince the general ecological and conser-vation audience of the need for a palaeoecological approach (Rull,2010a).

Although not properly acknowledged in many recent reviewsand research papers on palaeoecology and conservation, theeminent palaeoecologist Margaret B. Davis pioneered this field andsummarised the contribution of palaeoecological knowledge tonature conservation into five lessons related to biotic responses toenvironmental change as follows (Davis, 1989, 1991): 1) speciesrespond individually to changing environments, which determineschanges in community composition through time (Davis, 1981); 2)biotic responses have a time lag with respect to environmentalshifts, where the magnitude depends on the duration of the life-cycle of the species involved; 3) disturbance regimes and climatechanges are not independent, as is shown by the higher firefrequency in drier climates, for example (Davis, 1985); 4) somehuman activities, notably agriculture, can have more impact thanclimate change on shaping the landscape; and 5) presently,a variety of impacts are occurring that have not been seen in thepalaeoecological records (warming, UV radiation increase, aciddeposition), which may result in new species’ assemblages. Thefirst comprehensive account trying to relate palaeoecology andconservation was a special issue of Trends in Ecology and Evolutionentitled “Biology and Palaeobiology of Global Climate Change”,coordinated byM.B. Davis. A general conclusion of this special issuewas that predictions of the effects of climate change on biologicalsystems required much more information on environmentalphysiology and its genetic control, at both organism and commu-nity levels (Davis, 1990). Shortly after, Hazel and Paul Delcourt, whogreatly contributed to the view of palaeoecology as an ecologicaldiscipline, proposed that the mid-Holocene Hypsithermal Intervalcould be a partial analogue for global warming-induced bioticchanges, which would be useful to anticipate the nature and

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geographic patterns of biotic response to the initial 2 �C warming(Delcourt and Delcourt, 1991). After the analysis of several palae-oecological case studies, these authors have proposed that moderncommunities may disassemble and lose biodiversity by local orglobal extinction. Community reassembling is considered, but notin the same geographical areas and only after a lag of severalmillennia, depending on differential migrational rates and thetrajectories of species. Additionally, palaeoecological records mayhelp to identify more vulnerable areas, which is useful informationneeded to select suitable sites for ecological preserves (Delcourtand Delcourt, 1991).

Coincidentally, another outstanding scientist who has led thefield from the beginning, Brian Huntley, has published interestingreviews of palaeoecological case studies oriented to demonstrateits potential usefulness for biodiversity conservation (Huntley,1990, 1991). According to this author, one of the main contribu-tions is to provide long-term records that are able to elucidate if thepresent-day nature of communities, sites and landscapes are theresult of either stability or change, including human disturbance.Like Davis (1989, 1991), Huntley (1990) emphasised the temporarynature of communities at a millennial time scale, mainly because ofthe individual character of the biotic response to environmentalchange and the consequent differential migration rates of species(Huntley and Birks, 1983; Huntley and Webb, 1989; Huntley et al.,1989). Concerning conservation strategies, this author emphas-ised that strategies that rely upon the conservation of isolated sitesin an otherwise inhospitable terrain will likely be unsuccessful.According to Huntley (1990), themain conservation concern shouldbe the human pollution of the atmosphere, primarily in the form ofglobal environmental change derived from increased amounts ofCO2 and other greenhouse gases.

The Intergovernmental Panel on Climate Change (IPCC) wascreated in 1989 as a joint effort of the World MeteorologicalOrganisation (WMO) and the United Nations EnvironmentalProgram (UNEP) to provide the governments of the world withbalanced information and a clear scientific view of climate change(http://www.ipcc.ch). The first IPCC assessment report, publishedone year later, used palaeodata to show the millennial-scale rela-tionship between atmospheric CO2 concentration and temperatureover the last 160,000 years and noted that the projected warmingfor the 21st century would be 15e40 times faster than naturalchanges (Houghton et al., 1990). Concerning the potential bioticresponse to warming, the first IPCC report mentioned that palae-oecological studies were able to provide insights on potential futureconsequences, emphasising poleward migration and extinction(Tegart et al., 1990). The striking progress of palaeoclimatic andpalaeoecological science experienced during the last two decadeshas produced high-quality historical records, with resolution andaccuracy that make them comparable to actual measurements and,therefore, useful to validate explanatory and predictive models(Huntley, 1996; Rull, 2010a). Consequently, palaeodata are nowrecognised as a necessary component of climate change studies andits potential impacts, as described in the latest IPCC report (Parryet al., 2007; Solomon et al., 2007). The following is an account ofthe progress towards this realisation.

PAGES began by orienting the palaeo-research efforts towardsthree main points: 1) methodological homogenisation to make therecords comparable; 2) focus on two temporal scales, namely thelast two millennia (Stream I) and the two glacial cycles (Stream II);and 3) the disentangling of natural and anthropic causes of envi-ronmental change (Eddy, 1992). From a geographical perspective,the PAGES research was organised into three main Pole-eEquatorePole (PEP) terrestrial transects (i.e., the PANASH focus):the American continent (PEP-I), Asia-Oceania (PEP-II), andEuropeeAfrica (PEP-III). Other PAGES foci were as follows : the

study of decade-to-century-scale climate variability (PAGES/CLI-VAR intersection), the mechanisms and consequences of pastclimatic changes using ocean sediments (IMAGES), palaeoclimateand environmental variability in polar regions, and interactionsbetween human activities, climate, and environmental processes(http://www.pages-igbp.org/science/formerfoci.html).

A few years after the creation of PAGES, Huntley (1996) noticedthat, 30 years before, the understanding of mechanisms by whichorganisms and communities respond to a changing environmentwould have been only of academic interest, whereas today thisknowledge is essential to nature conservation. During this time,palaeoecology (mainly pollen analysis and palaeolimnology)underwent significant developments in both methods andapproaches in several major areas: chronological accuracy, which isderived from the application of new radiometric techniques;quantification and modelling of underlying patterns and processes,such as pollen dispersal or sedimentation rates; research design,including more precise targets and testable hypotheses; taxonomicaccuracy, notably increasing the number of fossil taxa identified;spatial and temporal accuracy, by increasing the resolution orinterpretations to meter-scale and yearly records; higher precisionin the estimation of past environmental variables, such astemperature, precipitation, pH, and salinity, by using trainingdatasets and specific statistical methods; and the use of multi-proxy approaches that combine a variety of independent physico-chemical and biological indicators derived from more reliablereconstructions (Birks, 1996; Huntley, 1996). Despite theseimprovements and the potential contribution that palaeoecologywould have made to nature conservation, the lack of synergybetween conservation science and palaeoecology at that time wassurprising (Birks, 1996). To illustrate the potential usefulness ofpalaeoecology in this context, Birks (1996), who has been instru-mental in the development of modern palaeoecology, discussedusing illustrative examples of how this discipline would be helpfulfor conservation assessments on the naturalness, fragility, andstatus of endangered species, and for supporting ecosystem resto-ration decisions. However, the lack of detailed autoecologicalinformation for most species of interest was still a handicap(Huntley, 1996).

Swetnam et al. (1999) defined “historical ecology” as a disciplineembracing “data, techniques, and perspectives derived frompalaeoecology, land-use history from archival and documentaryresearch, and long-term ecological research from monitoring andexperiments extending over decades”, and “time series frominstrument-based observations of the environments”. According tothese workers, historical ecology can inform conservationmanagement by defining baseline conditions of vegetationcommunities, their range expansions and contractions throughtime, and by discriminating between natural and anthropic causesof environmental change. Historical ecology showed that theunpredictability of biotic responses to environmental change andthe climate-organism non-equilibrium paradigm were key factorsto consider. Therefore, the detection and explanation of historicaltrends and variability are essential for better nature management(Swetnam et al., 1999).

A review by Gorham et al. (2001) identified the following fivemajor questions linked to conservation that palaeoecology can helpto answer: What were the properties of communities, ecosystems,and landscapes prior to or following natural or human distur-bances? What has been the pattern of recovery from disturbance,and was the prior state re-established? What is the nature andmagnitude of natural variability and the frequency of unusuallyextreme conditions? Were communities and ecosystems relativelystable prior to disturbance, or were there significant trends orfluctuations in some of their properties? Do anthropic disturbances

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have effects that are different in degree or kind from those ofnatural disturbances? These authors stress thewide range of spatialand temporal scales at which palaeoecological analyses are usefuland the variety of environmental problems that it is able to address,emphasising freshwater acidification and biodiversity loss. Gorhamet al. (2001) also discuss what they call the “surprise factor” inpalaeoecology (see above). As a general conclusion, Gorham et al.(2001) stress the need for palaeoecological records to designmore adequate environmental monitoring programs, and recom-mend the use of multi-proxy methodologies.

A synthesis of the results obtained by PAGES until 2003 waspublished in a book entitled “Palaeoclimate, Global Change and theFuture” (Alverson et al., 2003). After analysing all the contributionsof the PAGES book, Bradley et al. (2003) recommended thefollowing policies: 1) reducing greenhouse gases to reduce globalwarming; 2) understanding, monitoring and possibly preventingchanges in regional climate linked to thermohaline circulation; 3)sequestering fossil fuel carbon in terrestrial or oceanic reservoirs;4) developing natural reserves to maintain biodiversity; 5)detecting and attributing global and regional change to natural oranthropic forcing; and 6) managing lake catchments, coastal zonesand landcover to protect them for future generations. In the samePAGES book, Overpeck et al. (2003) analysed the response of thebiosphere to the known past climate and environmental variabilityto extract information useful to predict potential future bioticreactions to ongoing global change. According to these authors,“assessments of future conditions without a strong palae-oenvironmental component will not be successful”, as “records ofpast climate and biosphere change are the only information wehave on the nature and consequences of large environmentalchanges”. The resulting recommendations for future palae-oecological researchwere as follows: 1) improve the understandingof climate variability and biosphere responses and feedbacks; 2)emphasise high-resolution records that reveal the nature of inter-annual climate and biosphere change; 3) increase the number ofinvestigations that examine the ecological consequences of futureclimatic change in light of past records; and 4) enhance the inter-action among disciplines, such as palaeoenvironmental, ecologicaland land-use management, climate and climate modelling, andsocial science communities (Overpeck et al., 2003). Oldfield (2004)has provided similar recommendations and added the need for pastanalogues of the ongoing global warming, a better understandingof the role of solar variability, more information on hydrologicalvariability, and a better understanding of Holocene eustatic sea-level changes.

As a result of this previous research and knowledge, the USNational Research Council officially recognised the importance ofpalaeoecology for nature conservation and published a mono-graphy entitled “The Geological Record of Ecological Dynamics:Understanding the Biotic Effects of Future Environmental Change”,which declared that “the understanding of the patterns, processes,and principles governing the participation of biological systems inenvironmental change e and understanding how those systemsrespond e is a scientific and societal priority of the highest rank”(NRC, 2005). In this sense, three initiatives were proposed: 1) to usethe geological record as a laboratory to frame and test ecologicaltheories at appropriate scales while encompassing a full range ofearth conditions; 2) to study ecological responses to past climaticchange to provide a more sound basis for forecasting the ecologicalconsequences of future climate change and variability; and 3) togain knowledge of the ecological legacies of societal activities toassess the ecological conditions and variability before humanimpacts and to gather the geohistorical records of how societalactivities have affected present-day ecosystem dynamics. Animportant consequence of this official pronunciation was the

commitment of the US National Ocean and Atmospheric Adminis-tration (NOAA), an organisation with a long tradition of involve-ment in research on palaeoclimate and management of marinefisheries, to take the lead not only in the management of globalmulti-proxy palaeoenvironmental databases and their forecastingpotential but also in the incorporation of biotic responses to pastclimate changes as a proxy for future predictions (NRC, 2005), a taskthat is still one of NOAA’s primary mandates (http://www.ncdc.noaa.gov/palaeo/palaeo.html).

The importance of palaeoecology for conservation scienceexperienced a promising increase, with regard to publications since2007, coinciding with the publication of the fourth IPCC assess-ment, in which palaeoecology played a significant role (Parry et al.,2007; Solomon et al., 2007). The formerly limited use of historicalevidence in biodiversity conservation has been attributed to theperception of insufficient resolution in both space and time, thelack of accessibility of palaeoecological records to non-specialists,and the lack of a positive attitude of many Quaternary scientiststowards conservation issues (Willis et al., 2007a; Froyd and Willis,2008). Since then, a number of palaeoecologists have devotedimportant efforts to make evident the direct usefulness of palae-oecology in conservation, not only from a theoretical perspective,as occurred previously, but also by providing examples and casestudies and enumerating the areas in which the study of the pastwould be especially helpful. An interesting contribution, publishedalmost at the same time as the fourth IPCC report, was made byEdwards et al. (2007), who explored the usefulness of palae-oecology to provide more robust estimates of temperature increasefor this century. They concluded thatmodelling should benefit fromthe large amount of available palaeodata syntheses and palae-oclimatic reconstructions and that model simulations should focuson local rather than regional averages. The Oxford Long-TermEcology Laboratory, headed by Katherine J. Willis, has madesignificant contributions to the utility of palaeoecology in conser-vation. This research team and several associated co-workers haveshown that palaeoecology can significantly help conservationscience, especially biodiversity conservation, in the following areas:1) the identification of species at risk from extinction, 2) the settingof realistic goals and targets for conservation, 3) the identificationof management tools for the maintenance or restoration of a givenbiological state, 4) the determination of baselines and naturalecosystem variability, 5) the understanding of ecological thresholdsand resilience, 6) the assessment of climate change and conserva-tion strategies, 7) the documentation of biological invasions, 8) thedetermination of rates and the nature of biotic response to climatechange, 9) the management of novel ecosystems, and 10) theimprovement of red lists and similar conservation tools (Williset al., 2007a,b; 2010a; Froyd and Willis, 2008; Guillson et al.,2008; Willis and Bhagwat, 2010). The usefulness of palae-oecological knowledge for ecosystem restoration was emphasizedby Jackson and Hobbs (2009). Additionally, Davies and Bunting(2010) identified 24 conservation questions, from the 100 posedby Sutherland et al. (2006), inwhich palaeoecology canmakemajorcontributions (Table 1). Concerning conservation strategies forprotecting biodiversity, historical records can provide significantadvice on the following: 1) managing novel ecosystems, as theemergence of unprecedented species’ combinations will likely befavoured by future climate change; 2) retaining ecological memoryin the form of microrefugia; 3) conserving regions of high geneticdiversity, as they may hold high evolutionary potential; and 4)developing resilience to threshold events (Willis et al., 2010b).

Smol (2008) offered an excellent review and discussion, withmany illustrative and convincing examples, on the contribution ofpalaeolimnological records to conservation aspects, such as acidi-fication, eutrophication, metal and organic pollution, soil erosion,

Table 1The main conservation questions to which palaeoecology can significantly contribute, according to the 100 questions about conservation policy identified by Sutherland et al.(2006). Extracted from Davies and Bunting (2010).

Area Subject

Ecosystem services What are the benefits of protected habitats relative to non-protected land?What is the role of biodiversity in maintaining specific ecosystem functions?

Farming How will CAP reform affect biodiversity at the landscape scale?What are the environmental consequences of farming patterns?How do farming systems compare in terms of their effects on environmental impacts?What are the ecological consequences of changes in upland grazing regimes for biodiversity and soil ecology?

Forestry What are the relative benefits for biodiversity of the re-introduction of management to semi-naturalwoodlands vs. absence of active management?

Fisheries, aquaculture andmarine conservation

How long does it take the seabed to recover from disturbance?

Pollution What are the critical thresholds for nitrogen and phosphorus inputs into water?How will acidification of surface water from rising CO2 concentrations affect marine organisms?

Climate change Which species are likely to be the best indicators of the effects of climate change on natural communities?What time lags can be expected between climate change and ecological change?What is the likely relationship between the extent of climate change and the pattern of species extinction?How does climate change interact with other ecological pressures?How can we increase the resilience of habitats and species to cope with climate change?How will changes in oceanographic conditions affect marine ecosystems?

Conservation strategies With what precision can we predict the ecological impact of different policy options and theecological effects of management action?

Habitat Management and restoration What are the ecological consequences of ’wilding’ as a long-term conservation strategy?What are the consequences of different moorland management techniques for the uplands?How do recreated habitats differ from their semi-natural analogues?

Connectivity and landscape structure What are the lag times between habitat fragmentation and the loss of species?Making space for water What have been the consequences of past and present riparian engineering works?

What would be the ecological implications of large-scale rive and floodplain restoration schemesand would they be cost-effective..?What methods most accurately measure ecological status in the EU Water Framework Directive?

Fig. 1. PAGES scientific structure: four thematic foci (coloured circles) are com-plemented by four circling Cross-Cutting Themes that are of relevance to all foci.Reproduced from http://www.pages-igbp.org/science/index.html.

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species invasion, and ozone depletion, among others. Potentialfuture ocean acidification has also been discussed recently, in thecontext of palaeoecological evidence, by Pelejero et al. (2010).

Conservation palaeobiology, a term coined by Flessa (2002), hasbeen recently revived byDietl and Flessa (2009). It has been definedas “a synthetic field of research that applies the theories andanalytical tools of palaeontology to the solution of problems con-cerning the conservation of biodiversity” (Dietl and Flessa, 2010).This concept involves two different time scales: the “near-time”,which considers the last few million years, and the “deep-time”,which takes advantage of the entire history of life as a naturalecological and evolutionary laboratory. According to the sameauthors, the second approach sets the field apart from historicalecology, which is considered a sister discipline; such an approach isneeded todealwith aspects like speciation, extinctionor adaptation,which require a longer temporal perspective. The main palae-obiological contributions to conservation highlighted by Dietl andFlessa (2009, 2010) are the potential for defining baselines andnatural variability, the identification of more vulnerable species tobe protected, and the nature of biotic responses to climate change.

Much of the recent progress on the application of palaeoecologyto conservation can be attributed to ongoing developments, such ashigher chronological resolution, better models on atmospher-eebiosphere system functioning, the incorporation of new chem-ical and biological proxies to reconstruct past species distributionsand past climates, the availability of large geo-referenced databaseswith biogeographical and climatic data, and new approaches con-cerning fossil morphology and molecular DNA techniques(MacDonald et al., 2008). All of the previously mentioned authorsrecognise structural barriers to developing multidisciplinary teamsand networks with ecologists and decision makers, but theyemphasise the need for such collaboration for suitable natureconservation.

PAGES has progressively adapted its structure, objectives,programs and priorities according to new findings and the

evolution of palaeo climatology and palaeoecology outcomes.Currently, the PAGES research structure is organised around fourfoci and four Cross-Cutting Themes (CCT). Each focus covers a set ofquestions of prime importance to the global community. The CCTare more general in their scope and are of fundamental relevance toall foci and to palaeoscience in general (Fig. 1). Concerning

Fig. 2. Comparison of the IPCC warming predictions for the 21st century and theGreenland warming inferred from ice core records for the end of the Younger Dryasreversal. Estimated global temperature trends based on actual instrumental measuresare represented by a black solid line. Minimum (B1) and maximum (A2) IPCC averageestimates of 21st century global warming (Solomon et al., 2007) are represented byblue and red lines, respectively. These trends are attached to the left scale, which is thetemperature change with respect to the 1980e1999 average. Joint confidence intervalsfor all the IPCC estimates are represented by the gray area. The green line is theestimated Greenland temperature increase as deduced from ice core records (Alley,2000), which follows the right temperature scale. The estimated rate of change forthe YD warming is 4.1 �C/century, which falls within the range of the A1B, A2 and A1FIscenarios (1.7e6.4 �C/century) and coincides with the best estimate for the A1FIscenario (4.0 �C/century). Data for the YD warming have been downloaded from theNOAA World Data Center for Paleoclimatology at http://www.ncdc.noaa.gov/paleo/data.html (Alley, R.B. 2004. GISP2 Ice Core Temperature and Accumulation Data.IGBP PAGES/World Data Center for Paleoclimatology Data Contribution Series #2004-013).

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databases, the NOAA has become the worldwide repository ofpalaeoenvironmental and palaeoecological data, in the form ofmulti-proxy records on all subjects related to climate change(http://www.ncdc.noaa.gov/palaeo/palaeo.html). Additionally, theuse of both continental and marine core data as the original sourcefor palaeoecological records can be found on the websites of theInternational Continental Scientific Drilling Programme (ICDP), athttp://www.icdp-online.org, and the Ocean Drilling Program, athttp://www.icdp-online.org. Researchers can use these sites todownload the palaeodata required for model calibrations andsimulations at local, regional and global levels.

5. Past analogues for future global change

Often, it is argued that the global change predicted for thiscentury is unprecedented, mainly because of the high prognosti-cated rates at which it will occur. However, palaeoecologistscontinue to look for past analogues, for which high-resolutionrecords are essential. The latter estimates predict, for this century,a likely increase in average temperatures between 2 and 4 �C (witha maximum of up to 6.5 �C), a sea level rise of around 1 m and anincrease in atmospheric CO2 concentration of about 1000 pmmv,which is w2.5 times the present concentration (Solomon et al.,2007; Meinshausen et al., 2009). The better candidates for pastanalogues of such fast trends are changes associated with “abrupt”or “rapid” climate shifts, typically occurring at a centennial scale orbelow (Broecker, 2000). Willis et al. (2010a) provide severalexamples of palaeoecological records showing similar rates ofchange for temperature, sea level and atmospheric CO2.

The more recent of these events was the rapid warming thatoccurred during the transition between the Younger Dryas (YD) coldevent and the Holocene, just before 11.5 kyr BP, when Greenland airtemperatures increasedmore than10 �C inabout 60years (Steffensenet al., 2008). According to Jackson and Overpeck (2000), an averageincrease of 5 �C in 50 years occurred at the end of the YD. Taken asa whole, the warming at the end of the YD proceeded at a rate ofaround 4 �C/century, which matches with the higher IPCC warmingscenarios for the 21st century (Fig. 2). Vegetation responses to thisrapidwarminghavebeen recordedpalynologically inmany regionsofEurope and North America and include the following (Willis et al.,2010a): rapid expansion of local populations, large-scale speciesrange shifts, community turnover, and formationofnovel communityassemblages (Williamsand Jackson,2007;BirksandBirks,2008;Birksand Willis, 2008). There is no evidence of large-scale extinction inplants; only local or regional extinctions have been documented(Postigo-Mijarra et al., 2010), which contrasts with the conspicuousand well-documented mammal extinctions (see above). Especiallynoteworthy are the high-resolution studies around theYDperformedinNorthEurope,whichalloweddetailed studiesof thebiotic responseto warming. This made the long temporal scales of palaeoecologicalresults compatible with the fine temporal scales of modern obser-vations (Birks andBirks, 2008; Bakke et al., 2009). The responseof thedifferent organisms studied, including both plants (pollen, macro-fossils, mosses, diatoms) and animals (Chironomidae, Cladocera,Coleoptera, Trichoptera, Oribatidae), to warming showed cleardifferences in lags, rates and magnitudes (Birks and Ammann, 2000;Birks et al., 2000) that were likely due to different spatial scales, life-history temporal scales, sensitivities and ecological behaviours (Birksand Birks, 2008). The YDeHolocene transition seems to be an excel-lent past analogue for the predicted 21st century warming (Cole,2009) because it occurred at very similar magnitudes and rates andacted on the same species that exist today.

Other potential past analogues are linked to the 1500-year Bondcycles, which occurred during both glacial and interglacial periods(Bond et al., 1997). These cycles were manifested as either abrupt

warmings or coolings within glacial or interglacial conditions,respectively, and have been proposed as models to evaluate thepossible consequences of the ongoing greenhouse gas buildup(Broecker, 2000). These cycles have been broadly identified,correlated and named, and the vegetation response to these cycleshas been studied using pollen analysis (e.g., Tzedakis et al., 2004;Fletcher et al., 2010); however, suitable candidates for globalwarming analogues have not been proposed.

Some have also proposed the warming recorded at the Palae-oceneeEocene transition as another past analogue (McInerney andWing, 2011). This warming trend initiated around 59 Ma andculminated with the Early Eocene Climatic Optimum, between 53and 51Ma (Zachos et al., 2008).Within this relatively gradual trend,a sudden acceleration occurred around 55 Ma, known as thePalaeoceneeEocene Thermal Maximum (PETM), during which thetemperature increased more than 5 �C in less than 10,000 years(Zachos et al., 2001). During that time, the Earth was a “greenhouseEarth” (i.e., free from ice caps, even in the poles); average temper-atures were between 8 �C and 12 �C higher than today, and theatmospheric CO2 concentration was around 1000 ppmv or higher(Zachos et al., 2008). Apparently, such a scenario could be similar to

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the scenario predicted under near-future global warming. However,the PETM occurred at rates 100 times lower than the 21st centurypredictions, and they took place during a gradual warming overapproximately 10 million years. This is a very different situationfrom today’s “icehouse Earth”, which is characterised by the gla-cialeinterglacial alternation. Additionally, very few, if any, of theextant species, and probably few genera, existed by that time (Rull,2008, and literature therein), which prevents the possibility ofapplying the niche stability assumption. Therefore, the PETM seemsless powerful than the YD as a past analogue for the global warmingprognosticated for this century.

A past analogue for the predicted sea level increase has beenproposed by Virah-Sawmy et al. (2009), using a w3 m rise thatoccurred in the Indian Ocean 2500e3000 years ago, based on fossilcorals and higher beaches along the coasts of Madagascar (Camoinet al., 2004). At that time, these coasts were dominated by a highlybiodiverse littoral forest, which was suddenly replaced by a heath-land in less than 50 years. This heathland remained for thousandsof years until the sea level fell again, and the littoral forest was re-established with a different composition than the former forest(Virah-Sawmy et al., 2009). This dramatic replacement of thelittoral forest by the heathland has been interpreted in terms ofa threshold response of the forest, determined by changes insalinity and aridity linked to the higher sea level (Willis et al.,2010b).

6. Indirect impacts of climate changes: human disturbancesand humaneclimate synergies

We still know little about the probable impact of climatechanges on the trajectory of human history, and we are even moreuncertain of the environmental impact that human responses tothose climate changes have had. In response to climate changes,human societies make adjustments to maintain their modes of life,or they try to lessen the magnitude of the derived impacts, therebyfavouring the emergence of new environmental changes andproblems with which future generations will have to cope.

Even when satisfactory records of climate change and high-resolution archaeological data exist for a given region, appro-priate and sufficient palaeoenvironmental and/or palaeoecologicalinformation is missing, such as ecosystem recovery after depopu-lation or stresses on food resources after sedimentary settlement.This information is needed to allow for credible assertions on thecausal links between human responses to climate and the derivedenvironmental affectation. To establish such causal links, it isnecessary first to show that climate impacts on human activitieshave indeed occurred and subsequently to show that these changesin human activities have prompted environmental and ecologicalmodifications on a causeeeffect basis.

Human responses to change may alter feedbacks betweenclimate, ecological, and social systems, producing a complex web ofmultidirectional connections in time and space (Constanza et al.,2007). Ensuring sustainable future responses to the current globalwarming may partly depend on our understanding of this past weband how to adapt to future surprises. However, several questionsbecome apparent: What is the time span needed by humans tobecome aware of an ongoing climate change and respond with ananticipatory behaviour?What kind of information dowe need fromthe past to link the effect of past human responses to predictablehuman responses to current climate change? Are there really usefulpast analogues? In this section, we combine and discuss somepublished palaeoecological, palaeoclimatic and anthropologicalstudies to show how, and to what temporal and spatial extent,human responses to gradual and abrupt climate changes haveaffected the environment and ecosystems, and we contribute this

information to the ecological debate and conservationmanagement.

6.1. Gradual changes

The climate has changed over millennia, and these changes arelikely to affect ecosystems and the physical environment, whichoften respond at the centennial to millennial scale and encompasslong-term processes like succession, migration, extinction andlandscape changes. However, gradual climate changes can triggerprompt shifts in ecosystems to an alternative state because of a lossof resilience (Scheffer et al., 2001). Drastic shifts in climate can alsooccur within a century or less (Dansgaard et al., 2003), triggeringresponses from the terrestrial biosphere and the physical envi-ronment in less than 200 years (Allen et al., 2000).

The ability of humans to recognise and respond to climatechange is related to the limitation of the human scale and dependsupon the culturally conditioned canons of perception andcomprehension of the populations involved. Human societies areable to respond to climatic signals if they are within the scope oftheir perceptual time span. Within weeks to decades, rapid climatechanges can be inferred from perceived or measurable modifica-tions in direct climatic proxies (Hassan, 2009). Short-term envi-ronmental responses (such as resource shortages or habitat loss)are visible within the time frame of one to three human generationsand prompt adjustments to maintain survival or social stability;however, long-term responses escape human awareness andcannot be taken into account. In fact, the long-term consequencesof any decision to cope with climatic crises are commonly notwithin the lifetime of a person or a couple of generations (Hassan,2009). The indirect effects of climate changes deal with the wayspeople respond to those changes and have received little attention,both in policy deliberations and scientific research with regard tocurrent and past climate changes.

The climate varies gradually onmillennial and centennial scales.Such changes are less likely to raise people’s awareness, and distantmemories of how climate was before tend to fade gradually.However, practices that ensure survival in the face of gradualclimate changes are slowly adopted, and cultural changes appearthat can profoundly affect the environment (Hassan, 2009). Anexamplemight be the climate-driven origin of agriculture proposedby many authors (e.g., Reed, 1977; Richerson et al., 2001; Hassan,2009; Turner et al., 2010a). This activity probably occurred asecosystems responded to the drastic climate shift during thePleistoceneeHolocene transition, together with processes oper-ating from within human social systems (Piperno et al., 2007).Richerson et al. (2001) hypothesised that, besides the decisive factthat the humans of the Last Interglacial were neither cognitivelynor culturally able to develop agricultural subsistence, agriculturecould not have easily evolved in the Pleistocene because of theharsh climatic conditions that prevailed. Instead, the beginning ofplant-intensive, resource-use strategies would have started onlyafter the gradual amelioration of climate took place during thePleistoceneeHolocene boundary. In fact, the oldest traces of agri-culture date between 11,000 and 9000 cal. BP (Willcox, 2005;Piperno and Dillehay, 2008; Crawford, 2009). The associatedchanges from an ecological and environmental context would havecreated new selective pressures on hunter-gatherer human pop-ulations and their subsistence, leading to innovative and ultimatelysuccessful strategies that included exploitation of plant resources.For example, Piperno et al. (2007) illustrate this process for theNeotropic, showing that, during the late-glacial period(14,000e10,000 BP), three lake beds of the Central Balsas (Mexico)were dry and covered by open, cool adapted vegetation, with Zeamays as a constituent element. Strong shifts in climate and

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vegetation associated with the last phases of tropical deglaciationtook place as the Pleistocene was ending. Temperature andprecipitation rose and the lakes filled up, becoming active humanfoci near water sources and allowing Z. mays to be cultivated at thelake edges, starting between 10,000 and 5000 BP.

During the Holocene climate conditions allowed the evolution ofagriculture more or less simultaneously in vast areas with relativelywarm, wet climates in the Near East, along with access to irrigation(Willcox, 2005). The transition from the barest beginnings of wildplant cultivation during the Neolithic to almost full dependence ondomesticated foodstuffs occurred at a millennial scale (Liu et al.,2007; Piperno et al., 2007; Jones and Liu, 2009). The gradualclimate change taking place was probably imperceptible to people,and the acquisition of a new innovation or technology happenedonly after several generations. At each point in time, lifestylechanges most likely seemed a result of traditions unrelated to thegradual warming trend. In contrast to these parts of the planet,intermittent and unpredictable droughts occurred in SoutheastAmazonia. Droughts, together with environmental constraints onagriculture intensification and reliance on wild sources of protein,led to the perpetuation of nomadism and hindered cultural devel-opment (Meggers, 2007).

Human occupation and utilisation of plant and animal resourceshave led towidespread landscape changes all over theworld duringthe last 10,000 years. Land use and landcover changed because ofwater withdrawal; agriculture was most likely the primary way inwhich humans affected water regimes; irrigation and deforestationfor agriculture have redistributed global evapotranspiration andaltered the regional climate; the use of fertiliser led to nutrientrunoff and promoted eutrophication in aquatic ecosystems aroundthe world. These changes have driven a decline in ecosystemservices other than agriculture, such as fisheries and flood regula-tion (Gordon et al., 2008). Environmental impacts derived from thepost-Neolithic expansion of agriculture have been extremelyimportant. Over the long-term, these impacts are probably asimportant as those generated by the industrial revolution. In fact,Ruddiman (2003) pushed back the start of the Anthropocene era bythousands of years based on awide array of archaeological, culturaland geological evidence. The term “Anthropocene” was originallycoined to denote the fact that current human activity was indeedchanging the Earth on a scale comparable with some of the majorevents of the ancient past (Crutzen and Steffen, 2003). Thedefenders of the early Anthropocene hypothesis (Ruddiman, 2003;2007; Ruddiman and Ellis, 2009) proposed that the start of forestclearance by humans reversed a naturally decreasing CO2 trend7000 years ago and promoted a new increase in CO2 values,whereas early rice irrigation and livestock tending had a similareffect on the methane trend beginning 5000 years ago. In pre-industrial times, the annual rates of carbon release may havebeen more than 10 times lower, as populations were much smallerand technology was much more primitive than today, but thecumulative emissions could still have been extremely large becauseof the extended time interval over which they operated. Theassociated atmospheric warming was estimated to be 0.8e2 �C, onaverage. According to the authors, this would have been largeenough to have stopped the glaciation of north-eastern Canadaforecasted by two different climatic models.

If the hypotheses of climate-driven agriculture and earlyhuman-induced warming can be demonstrated, it could beassumed that the early human-induced global warming was anindirect effect of the onset of agriculture activities, giving rise toa positive feedback mechanism with important environmentalconsequences. The effects of these climate changes on the envi-ronment could have never been properly anticipated by humansbecause of the slow and gradual pace of both phenomena.

Additionally, many of the effects are cumulative, which implies thatthey only achieved global significance by the widespread nature oftheir effects or because of their cumulative magnitude (Turneret al., 1990). In terms of conservation purposes, this means thatthe large-scale effects of slow environmental changes and theassociated human responses are difficult to foresee and impossibleto manage unless appropriate long-term records are available andconsidered when testing hind- and fore-cast model projections.The application of Quaternary palaeoecology to conservation poli-cies and actions could provide the necessary time perspective toanticipate impacts, such as succession, migration, extinction, andlandscape changes, in a more realistic way. Time scales in conser-vation studies are typically limited to relatively short-time intervalsand commonly ignore the magnitude of human responses and thedynamics of long-term processes with high environmental impact.

6.2. Abrupt changes

The palaeoclimatic record details how some climate changeswere vast and in many cases occurred abruptly (Broecker, 2000;Alley et al., 2003). Rapid climate changes have often hadprofound effects on biological populations by imposing strongerselection and distance from environments to which they areadapted (Davis and Shaw, 2001).

The US National Research Council (NRC) study ‘Abrupt climatechange (ACC): inevitable surprises’ defines ACC from two differentpoints of view:

“technically, an abrupt climate change occurs when the climatesystem is forced to cross some threshold, triggering a transitionto a new state at a rate determined by the climate system itselfand faster than the cause. The cause may be chaotic and thusundetectably small (NRC, 2002, p. 14)”;“from the point of view of societal and ecological impacts andadaptations, abrupt climate change can be viewed as a signifi-cant change in climate relative to the accustomed or backgroundclimate experienced by the economic or ecological system beingsubject to the change, having sufficient impacts to make adap-tation difficult (NRC, 2002, p. 121)”.

Note that “abrupt” does not necessarily mean “severe”. The firstdefinition highlights a fast transition to a new state and theapparent irrelevance of the cause, rather than the magnitude ofthe change. The second definition contrasts the abruptness of thechange and its effects with the capacity of human and ecologicalsystems to adapt and overcome the negative impacts over time orundergo remedial actions. This capacity depends more on ecolog-ical and social features, such as stability, resilience, vulnerability,flexibility and scale, than on the severity of the climatic disturbance(Hassan, 2009). The level of global climate variability and climatechange that is tolerable varies enormously depending upon thegeographic region and the society or ecosystem. The effect of ACCmay be temporary, and the systems may recover if the environ-mental perturbation has not been too large (Alley et al., 2003).

ACC has had profound impacts on ecosystems (Davis and Shaw,2001) and civilisations worldwide and is still the subject of muchresearch by Quaternarists. Contrary to non-abrupt climate changes,ACC can be perceived and measured by humans because they takeplace in the frame of years or decades. Therefore, people are likelyto recall and compare extreme events and deviations from “normalconditions” that they have experienced in their lifetimes, or thosereported by previous generations (usually no more than three).Such awareness allows for adaptation or mitigation responses tothe new conditions (Hassan, 2009; Turner et al., 2010b). AlthoughACC has been blamed on the collapse of complex civilisations (deMenocal, 2001; Weiss and Bradley, 2001), it has been proposed

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that mismanagement of natural resources and the vulnerability ofsocial organisations have played a key role in these outcomes(Hassan, 2009). One example is the Classic Maya Collapse (AD750e830), which coincided with the most severe and prolongeddrought of the last millennium. It happened at or near the timewhen other South and Mesoamerican cultures experienceddeclines, apparently also as a result of severe droughts. Forexample, the irrigation-dependent Moche civilisation in Perúsuffered destruction and famines during the 6th century; the city ofTeotihuacán (México) was abandoned between AD 750 and 800;and the Tiwanaku civilization, in the central Andes, collapsedaround AD 1000 (Hodell et al., 2004, 2001; Weiss and Bradley,2001). Droughts associated with the Maya Collapse occurred ina context of unsustainable use of resources, shifts in organisationaland economic strategies and population movements, which likelyhastened the civilization’s demise (Hassan, 2009).

Worldwide comparisons of the impact of different climatechange events on past civilizations indicate that climate has beena driving force in some instances, and has played a significant rolein others. In societies where environmental impacts of climatechanges are not visible, climate shifts may be perceived simply asbackground noise (Catto and Catto, 2004). It is only recently thatQuaternarists have looked at historical data to search for analogieswith the present-day situation, where human emissions of green-house gases, combined with profound impacts on landscape andecosystems, are leading to unprecedented transformations in theearth’s climate and creating new forms of vulnerability to rapidonset disasters and long-term environmental change (Anthes et al.,2006; Parry et al., 2007; WBGU, 2008). An increasing number ofobservational evidence indicates that climate change is alreadyhaving effects on biological populations (Walther et al., 2002), suchas changes in the extension of vegetative periods (Peñuelas andFilella, 2001) and the upward migrations of plants and animals(Peñuelas et al., 2002; Parmesan and Yohe, 2003), and on theenvironment, such as more frequent and severe hurricanes (Antheset al., 2006) and greater fire risk (Flannigan et al., 2000).

Awareness of climate change triggers two types of humanresponse, namely adaptation (involving actions aimed atpreserving those systems of interest) and mitigation (actions tolessen the rate and magnitude of the change) (Turner et al., 2010b).Most mitigation efforts address the environmental change itself toprevent or mitigate climatic disturbances (Smithers and Smith,1997). These efforts include seeking a reduction in CO2 emissions,encouraging the use of non-carbon or carbon-neutral energysources, and the promotion of carbon sinks through land-use andhabitat management. In poor and vulnerable populations of theworld, climate-induced displacement may be the most likelymitigation response because of aridity, sea level rise, meltingglaciers, coastal subsidence and erosion, which threaten roughly600 million people (Johnson and Krishnamurthy, 2010). TheGerman Advisory Council (WBGU, 2008) identified the followingfive regional “hotspots”, where significant climate-induceddisplacement and conflict are expected to occur, most of thembeing the result of flooding, windstorms and rising sea levels: theCaribbean and the Gulf of Mexico; North Africa, especially the NileDelta; South Asia, especially the GangeseBrahmaputra Basin;Eastern China; and the Sahel zone. In this regard, paleoecologicalrecords have already shown how coasts dominated by a biodiverselittoral forest can be quickly replaced by a heathland in less than 50years (Camoin et al., 2004).

Depending on the way mitigation actions are performed, theycan generate unintended environmental and ecological conse-quences (Paterson et al., 2008). Adaptation can result in purposefulresponses or spontaneous adaptations to shifts in environmentalconditions, which can differ from policy. Smithers and Smith (1997)

identified three dimensions to accommodate human adaptation toclimate changes: the force of change, the properties of the systemthat may influence its sensitivity, and the type of adaptation that isundertaken. More concretely, per capita income, inequality in thedistribution of income, universal health care coverage and highaccess to information have been regarded as important determi-nants of adaptive capacity (Alberini et al., 2006).

Current approaches to ecosystem conservation still rely on theclassic view of predictable and stable point equilibria of ecosystems(Wallington et al., 2005), and habitat management in most systemstraditionally assumes linear succession-like trajectories (Scoones,1999). Over the past several years, conservation and restorationbiologists and managers have become aware that the potential forsudden shifts in ecosystem states is alarming, indicating thata system can be less resilient than expected (Suding and Hobbs,2009). Non-equilibrium ecology may explain such behaviour. Ifdisturbances can cause systems to shift between multiple stablestates, it is reasonable to assume that indirect human impacts ofclimate change that are derived from adaptation or mitigation canwiden the range of already vulnerable habitats, where thresholddynamics can occur and shift communities into new states that aredifficult to reverse.Humanactivities tocopewith climate changecanincorporate new threshold triggers by converting transient eventsinto persistent disturbances, by introducing chronic stress andstarting new disturbances, or eliminating important disturbancepatterns. The abrupt character of current climate change mayaccelerate these processes. The timely recognition of such situationsis crucial to ecosystem management and conservation policies(Wallington et al., 2005). In this regard, threshold models in resto-ration and conservation that are being developed as a response tothis shift in ecological thinking are central to cope with humanresponse to climate change Suding andHobbs, 2009). These authorsconsider that current utilisation of threshold models in habitatmanagement still lacks rigorous testing and underlying assump-tions, and they suggest a framework for incorporating thresholdmodels that effectively helps decision making and management onrelatively short-time scales in human impacted systems.

There is increasing awareness of the need to assess the indirecteffects of climate change derived from adaptation and mitigationactions: as people adapt to climate change across multiple scales,ranging from local to national and international, a wide range ofnew risks to ecosystems and biodiversity will emerge. Nonetheless,the effects of current climate change have not been pronouncedenough to have prompted significant mitigation or adaptationefforts (Turner et al., 2010b).

Long-term ecological knowledge needs long-term biodiversitybaselines and palaeoecological data, which are crucial for testingpredictions about ecosystem thresholds and resilience (Dietl andFlessa, 2010; Willis et al., 2010a; Rull and Vegas-Vilarrúbia, 2011).Some messages have been derived from these initiatives(Wallington et al., 2005; Suding and Hobbs, 2009) that are impor-tant for palaeoecology because the temporal dynamics of ecosys-tems have a number of implications for conservation managementbefore considering the indirect human impacts to climate change:

� Ecosystems are complex and dynamic, and gradual or suddenchanges in composition and structure can be expected overtime. By understanding the history of a place to be preserved,we may improve our understanding, conservation actions andprediction of future responses, as it forms part of the essentialcontext within which to evaluate current trends and probablefuture outcomes of any conflict, adaptation or mitigationactions.

� Rates of change can be highly variable and are essential infor-mation that managers need to maintain over the system they

Fig. 3. Estimated atmospheric oxygen levels over the last 600 Ma; adapted fromBerner and Canfield (1989), and Scott (2000).

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are watching. The kind of managerial response to slow or fastchanges as part of mitigation action may be very different andmay determine the success of a given conservation strategy.

� Natural disturbance is an integral part of ecosystems withhuman assets and livelihoods and are important to consider.Natural disturbances plus anthropic initiatives may precipitatethreshold dynamics of the ecosystem to be preserved. Adap-tation strategies should take this synergy into account whentrying to accommodate the new climate or climate derivedsituation.

� History of landscape use and human disturbance legacies maybe important elements in shaping the current composition andstructure of a particular ecosystem in such a way that the linksbetween biotic assemblages and abiotic settings are notstraightforward, thereby complicating the development ofconservation actions.

7. Past fire records

Fire is a natural and/or anthropic element present in all vege-tated lands. The main drivers of fire are the following: 1) theenvironment, mainly temperature, precipitation and the balance ofatmospheric gas concentrations; 2) the flammability of fuels,mainly vegetation; 3) the existence of ignition sources; and 4)human activities (Flannigan et al., 2009; Whitlock et al., 2010).Understanding the complex mechanisms involved in fire ecology isnot an easy task because internal and external variables act ina complex and non-linear fashion, resulting in synergies andpositive feedbacks that lead to unexpected results (Bowman et al.,2009; Krawchuk et al., 2009). For example, vegetation flammabilityincreases in dry climates because of a decrease in internal watercontent and the common occurrence and increased concentrationof flammable metabolites, which may lead to fire events of unex-pected virulence. This is the case of the so-called pyrophilousvegetation types, common in Mediterranean ecosystems, wherefire is considered an important part of their ecological dynamics(Carrión et al., 2010). Bond et al. (2005) proposed that fire has beenand is currently a major factor in theworldwide biome distribution.For example, it has been suggested that, in the absence of fires,cloud forests would double their global cover, mostly at theexpense of ecosystems dominated by C4 grasses, as is the case inmost tropical savannas (Bond et al., 2005). Non-linear responsesand spatially heterogeneous fire patterns should be considered topredict future ecological scenarios (Cochrane and Barber, 2009;Flannigan et al., 2009; Krawchuk et al., 2009). In this sense, posi-tive feedback between climate and vegetation, non-homogeneouseffects of global warming on the different climatic regions, andlocal peculiarities in the hydrological balance have been consideredthe most relevant factors for more accurate predictions (Hoffmannet al., 2002; Cardoso et al., 2003).

Fire has been a significant driver of ecological changes in thebiosphere through its history, especially during the last millennia,when the human impact on ecosystems increased dramatically. Ithas also been predicted that fire will be a crucial factor in the near-future because of the ongoing global warming, especially in thoseregions where the hydrological balance (precipitation/evapotrans-piration or P/E) will be depleted (Parry et al., 2007; Solomon et al.,2007). A critical question concerns the causes of the recorded fires,which is clear for times before human appearance but becomesmore puzzling over the last w20,000 years, when human societieshave become outstanding factors in burning. In this sense, impor-tant challenges include the identification of the potential causes forpast fires (i.e., natural or anthropic) and the potential influence ofenvironmental conditions on fire occurrence, both directly andindirectly, by modifying human behaviour. Past fire records mostly

rely on the findings of macroscopic and/or microscopic charcoal inrecent sediments and in older sedimentary rocks (Scott, 2000;Whitlock and Larsen, 2001). Fires appear in the geological recordin the Devonian (onset at 416 million years ago or Ma). The absenceof both humans and fire-prone plant species provides an excellentopportunity to address the relationship between fire and envi-ronmental parameters. In these conditions, atmospheric O2concentration (O2 hereafter) has been proposed as the main forcingfactor promoting fire, even on a priori non-flammable biologicalmaterial. Combustion occurs when O2 is over 13%, and variations inO2 levels correlate with fire activity throughout Earth’s history(Scott, 2000). For instance, the Carboniferous (359.2e303.4 Ma)was modelled as the period of highest O2 (Berner and Canfield,1989), and many studies have shown extensive Carboniferouscharcoal deposits throughout the Earth, interpreted as the productofmajor and extensivewildfires (Scott, 2000) (Fig. 3). Subsequently,an interval of lower fire incidence followed until the early Creta-ceous (onset at 145.5Ma), when an increase in fire events coincidedwith a new increase in O2. In the CretaceouseTertiary boundary (K/T, at 65.5 Ma), consistent evidence for a global fire event, as wouldbe expected by the meteorite impact hypothesis (Alvarez et al.,1980), is lacking, and fire records at that time have been inter-preted as the result of normal fire regimes or fires of regionalcharacter (Scott, 2000). For the purposes of the present review, thefocus will be on the Quaternary, especially the last glacial cycle,when modern ecosystems were shaped with the help of anthropicfires.

The YD reversal has already been discussed as an example ofrapid climatic change between 13 and 11.5 cal ky BP and asa potential historical model for present and future climatic shifts.The YD reversal also provides examples of increased fire incidenceand their natural or anthropic nature. For example, Marlon et al.(2009) have reviewed the patterns of fire incidence and biomassburning during the YD in North America and have shown anincreasing trend at both the onset and the end of this interval, withthe last one being themore intense. The authors favoured a climaticorigin for both, although they did not neglect other direct (delib-erate or accidental burning) and indirect causes linked to the arrivaland dispersion of human populations after crossing the Beringpassage, such as the increase in flammable vegetation coverbecause of the decrease of herbivores, attributable to the well-documented megafaunal extinction prior to the YD. According toMarlon et al. (2009), the main climatic drivers of YD fires wouldhave been the increase in average temperatures recorded since theonset of the Bølling-Allerød interstadial, which began approxi-mately 14.7 cal kyr BP, just before the YD, and the abrupt warming

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at the YD/Holocene transition, which has been considered a pastanalogue for ongoing global warming. This climatic hypothesis hasalso been supported by other studies worldwide (e.g., Haberle andLedru, 2001; van der Hammen and Van Geel, 2008). Moreover,Daniau et al. (2010) observed that, during the last glaciation, fireregimes varied synchronously with millennial-scale climatechanges associated with DansgaardeOeschger (D/O) events, whichare part of the above-discussed 1500-year Bond cyclicity. Accordingto the same authors, fire incidence increased during D/O warmingsand decreased during rapid coolings, thus supporting the climatichypothesis. The defenders of this hypothesis argue that, globally,climate has been the major control on fire regimes, even during thelast two millennia, despite the dramatic increase in human pop-ulation and the associated disturbances resulting from land use.They also argue that anthropic fires became more important afterAD 1870 (Marlon et al., 2008). This contrasts with the proposal that,in the tropics, historical fire incidence has been regulatedmainly byhuman activities and climateehuman synergisms (Power et al.,2008). For example, ENSO variability coupled with human migra-tions and settlement shifts have been proposed as the main driversfor neotropical fire regimes since the mid-Holocene (Meggers,1994; Uhl, 1998); However, now, and likely in the near-future,anthropic fires dominate the scene (Cochrane and Barber, 2009).Fires of human origin have also been proposed as important in theNeotropics during the Lateglacial, including the YD interval, and theHolocene (Bush et al., 2007; Rull, 2009b). As noted above, ata global scale, human fires would have been responsible for theearlier increase in atmospheric CO2 concentration and the onset ofthe Anthropocene in the early Holocene (Ruddimann, 2003, 2007).

The importance of Quaternary charcoal records as proxies forpast fires and the associated changes in vegetation composition,diversity or local extinctions has beenwidely recognised (Whitlockand Larsen, 2001). These palaeorecords can be used not only toobserve how past fires have disturbed the vegetation but alsoas modelling inputs to derive realistic scenarios of futurefireeclimateevegetationehuman relationships for managementpurposes. Whitlock et al. (2010) show the complexity of under-standing fire behaviour at different levels and the need to incor-porate long-term studies to obtain a more accurate view of fireevents as a part of Earth-system dynamics. According to theseauthors, the following important points should be considered inthe study of past fires: 1) fire regimes operate at different spatialand temporal scales, with distinct drivers at each scale; 2) clima-teefire, fuelefire, and humanefire relationships also act at differentscales; 3) there is a huge impact from human practices whereclimate and fuel are not limiting factors, such as occurs in extremeconditions like desserts (no fuel) or rainforests (no favourableclimate for ignition); and 4) the “fire regime” concept should berevised. The current definition of fire regime only considers short-term studies that are unable to capture the full range of fire vari-ability in many ecosystems. Whitlock et al. (2010) have introducedthe “super-fire regime” concept to better address the characteristicnature of fire within a biome by taking into account all the forcingfactors involved, including humans at the appropriate temporalscales. This concept, with an important palaeoecological compo-nent, is more powerful to anticipate future variability withina given biome because it considers long-term ecosystem behaviourand humans as part of ecosystems and “climate changers”(Whitlock et al., 2010).

As an effort to manage the available information on firepalaeorecords, the Global Palaeofire Working Group (GPWG)was established to follow the rules of the IGBP Fast TrackInitiative on Fire (http://www.gpwg.org). The open-access GlobalCharcoal Database (http://www.ncdc.noaa.gov/palaeo/impd/gcd.html), created in 2003, gathers the available fire palaeorecords

since the LGM. Using this database, Power et al. (2008) haveobserved thatfire activity has varied globally and continuously sincethe LGM in response to long-term changes in global climate andshort-term regional changes in climate, vegetation, and human landuse. Fire frequency has been continuously increasing since the LGMuntil the present, with a significant increase in spatial heterogeneitybeginning around 12 cal kyr BP. The hope is that this database willcontribute to a better understanding of fire patterns at global,regional and local scales to optimise conservation practices.

8. Neotropical examples

The Neotropics is a key region from a conservation perspectivebecause of its amazing biodiversity and endemism patterns and theoccurrence of extensive rainforests, some of which are in nearlypristine states; the Neotropics contain several conservation hot-spots (Myers, 2001; Huber and Foster, 2003). This region is less wellknown than the northern temperate areas from a palaeoecologicalpoint of view, but several studies are available showing its suit-ability to provide case studies with conservation significance andhighlighting the need for further studies (e.g., Bush, 1996, 2002;Bush and Silman, 2007; Mayle et al., 2007; Figueroa-Rangel et al.,2010; McKey et al., 2010). The examples provided here have beenselected from our own research in northern South America.

8.1. The YD coolingewarming shift in the northern Andes: bioticresponses

As stated above, the rapidwarming initiated at the end of the YDis a potential analogy for the predicted future global warming, andits study may help forecast near-future biotic responses and facil-itate the adoption of conservation policies. The occurrence of theYD cooling in the Neotropical region has been debated for decades.Several palaeoecological records favoured its existence, whereasothers did not (Hansen, 1995; van der Hammen and Hooghiemstra,1995; Rull et al., 2010a). Some records reported a cooling aroundthe YD dates, but the dating was not good enough to provide thenecessary bracketing for accurate correlations (van’t Veer et al.,2000; Mahaney et al., 2008). The first clear record was obtainedin the Cariaco Basin (Fig. 4), where both palaeoclimatic recon-struction and dating supported a cool and dry event coincidingwith the YD (Haug et al., 2001; Lea et al., 2003). On the continent,the first undisputed YD equivalent has been found recently in thesediments of a high-altitude Andean lagoon (Los Anteojos) aftera multi-proxy study. Sedimentological and geochemical indicatorsdocumented a sudden cooling and a glacier advance initiated at12.85 cal ky BP, with a maximum of around 3 �C below presentaverage temperatures at 12.65 cal ky BP, followed by a rapidwarming initiated at 12.3 cal ky BP, which ended near theYDeHolocene boundary. As in Cariaco, the Anteojos cooling wasalso characterised by dry climates (Stansell et al., 2010).

The response of vegetation to the cooling was heterogeneous,where the more sensitive taxa were Podocarpus (a genus of treesliving at the upper altitudinal forest levels), Polylepis sericea (a treethat forms almost monospecific stands above the upper forest line,or UFL, within the “páramo” open vegetation), Huperzia (a genus offerns typical of humid “páramos”), and Isoëtes (an aquatic pteri-dophyte growing submerged in shallow waters, including lakeshores) (Fig. 5). Other taxa that responded to the cooling were thefamilies Asteraceae and Poaceae, but the homogeneous pollenmorphology of their genera and species prevented the necessarytaxonomic resolution to analyse their detailed responses to climateshifts. However, these families characterise the open “páramo”vegetation in the northern Andes and increased during the cooling,which indicates an increase in this vegetation type. All the sensitive

Fig. 4. Map of northern South America showing the study sites mentioned in the text (Section 8). The yellow box corresponds to the Gran Sabana region (containing also the tabularmountains or tepuis represented as green patches), which is enlarged below. The sampling localities are represented as red dots. Tepuian sites: ACO e Acopán, AMU e Amurí, CHU e

Churí, ERU e Eruoda, TOR e Toronó; Gran Sabana sites: CHO e Lake Chonita, ENC e Lake Encantada, MAP e Mapaurí, URU e Urué. Radar image courtesy of NASA/JPL-Caltech.

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genera and species mentioned reacted to the Anteojos cooling bydecreasing their percentages, but the most sensitive taxa werePolylepis and Isoëtes, with pollen and spores that disappeared fromthe sediments during the maximum cooling and did not re-appearuntil the onset of the warming that initiated at 12.3 cal BP. This wasinterpreted as a downslope migration of the sensitive taxa anda decrease in lake levels because of cool and dry climates (Rull et al.,2010b).

Among the trees from the upper forest levels recorded throughpalynological analysis (including other well known indicators ofthis vegetation type, such as Alnus, Hedyosmum and Weinmannia),only Podocarpus has reacted to the YD climate shifts. This indicatesthat the taxonomic composition of these forests changed because of

the different individual requirements of each taxon. It is alsonotable that sensitive taxa showed immediate responses to boththe cooling and the subsequent warming, without any time lag atthe resolution of the study, which is decadal to centennial (Fig. 6).This indicates that these taxa not only are the more sensitive butalso react quickly to climate shifts, even the rapid ones. Conse-quently, they would be useful to monitor the biotic responses toongoing warming to prognosticate the expected biotic changes inthe near-future. It is known that high-altitude biomes are highlysensitive to climate changes and are therefore preferred environ-ments for global change studies (Ives, 1999). Also, the Andeanforests are known to be among the more biodiverse ecosystems onthe planet, holding outstanding hotspots for conservation (Myers,

Fig. 5. Summary percentage pollen diagram for the Lateglacial, as recorded in the Lake Anteojos sediments (northern Andes). The Anteojos cold reversal (grey band), equivalent tothe YD, was defined according to independent sedimentary and geochemical proxies. The left column is the summary of all pollen taxa subdivided into three categories representingforest trees and páramo shrubs and herbs. The more sensitive pollen taxa are depicted individually. Algae remains include Pediastrum, Botryococcus, Debarya, Spirogyra and Zygnema(Rull et al., 2010b); Redrawn from Stansell et al. (2010).

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2001). Therefore, the information obtained in the Anteojos casestudy on the biotic responses of high-altitude ecosystems to rapidwarming should be considered for management purposes.

8.2. Fire, climate change, and savanna expansion in the GranSabana (Guayana region)

The Gran Sabana (GS) is a vast region of approximately18,000 km2 located in SE Venezuela, between the Orinoco and theAmazon Basins. The GS is a huge island of savannas within the

Fig. 6. Correlations of the Pollen Index (PI) and the Polylepis curves with selected physico-chreconstructions containing the YD event (Cariaco and GISP). The PI was calculated as the ratiGray bands represent the stadials based on the GISP isotopic curve. The glacier advance definTi curves. Note the parallelism among the curves of physico-chemical proxies for climate chaRedrawn from Rull et al. (2010b).

normally forested Guayana landscape. These savannas form largeextensions of treeless grasslands and are intermingled in someplaces with forests and shrublands, developing typical forest-savanna mosaics (Huber, 1994a). The GS is the homeland of thePemón indigenous group, from the Carib-speaking family. It hasbeen postulated that this culture reached the GS relatively recently,or approximately 300 years ago (Thomas, 1982; Colson, 1985), butsome archaeological evidence may suggest an earlier humanoccupation beginning in the early Holocene (Gassón, 2002). Adefinitive assessment on the age of human settlements in the GS is

emical palaeoclimatic proxies measured in the same core and referential palaeoclimatico between sensitive taxa: ( Podocarpus þ Polylepis þ Huperzia)/(Asteraceae þ Poaceae).ed by Stansell et al. (2010) in the Anteojos core is indicated by a box around the MS andnge, and the PI, and especially, the rapid response of Polylepis to environmental shifts;

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not yet possible. Fire is an important component of the Pemónculture. They use it every day to burn great expanses of savannasand occasionally forests (Fig. 7). However, the high fire incidence ofbetween 5000 and 10,000 observed fires per year (Huber, 1995;Leal, 2010) contrasts with the nearly inexistent agriculture orcattle e raising practices typical of other cultures strongly linked tofire. In the Pemón culture, fire practices are initiated for variousreasons, such as for hunting, shifting agriculture, fire prevention,communication, savanna cleaning, firewood drying, aesthetics, andmagic (Kingsbury, 2001; Rodríguez, 2004, 2007).

The GS is also important from an economic point of viewbecause it lies on the headwaters of the Caroní River, which is themain provider of hydroelectrical power for the country (Castro andGorzula,1986). The organisation in charge of the exploitation of thisenergy (EDELCA) has developed a conservation program for theCaroní River Basin that includes the control of fire in the headwa-ters to protect its ecosystems (Castro and Gorzula, 1986). In addi-tion, the GS is part of several national and international officialprotection areas, such as national parks, biosphere reserves andworld heritage sites (Huber, 1995, http://whc.unesco.org/en/list/701). Despite this, only about 13% of fires lighted by the Pemónare controlled and extinguished (Sletto, 2008; Bilbao et al., 2010).This low success is due to the large extension of the GS, the highnumber of daily fires compared to the available prevention andextinction resources, and the unpredictability of fire locations(Rodríguez, 2007; Bilbao et al., 2010). There is a vivid debatebetween EDELCA and several local ecologists, on one hand, and thePemón and their defenders, on the other, about fire dynamics in theGS. The first defend the current protection rules and the ecologicalknowledge, whereas the second argue in favour of the indigenoustraditional practices, in which fire is an essential element (Rull,2009a). A subjacent question in this debate concerns the origin ofthe GS savannas, given their isolated nature among the extensiveGuayana and Amazon rainforests, in a climate more favourable forforest formations. It has been postulated that the open vegetationtype of the GS may be due either to the action of anthropic fires orto palaeoclimatic and edaphic factors (Fölster, 1986; Fölster andDezzeo, 1994; Huber, 2006).

Palaeoecological records can help to address these problems byproviding additional tools for conservation purposes. The proposalof the climatic hypothesis predated the palaeoecological study ofthe region and was based on palaeoclimatic and biogeographicassumptions. According to this hypothesis, the GS is a relic of theformer extension of savannas that dominated the Neotropicsduring the LGM because of the prevalence of drier climates (Eden,1974). Recent palaeoecological studies have documented the

Fig. 7. Savanna fires in the Gran Sabana near Stanta Elena de Uairén (Photo: V. Rull).

replacement of either forests or shrublands by savannas during theLateglacial and the early Holocene, thus bringing into question theclimatic proposal. In the Mapaurí locality, a mountain cloud forestdominated the landscape until approximately 10.2 cal ky BP, whenit was replaced by a treeless savanna (Rull, 2007a) (Fig. 8). In theLake Chonita catchment, the Lateglacial was characterised bya shrubland with no modern analogues, which persisted during theentire YD and was substituted with a treeless savanna in theYDeHolocene transition (Montoya et al., 2011) (Fig. 9). In bothcases, the treeless savannas persist until today. These biotic shiftscoincided with the late YDeearly Holocene global warming(Kaufman et al., 2004; Kaplan and Wolfe, 2006) and were locallycharacterised by a decrease in the hydrological balance. In the caseof Lake Chonita, the disappearance of the shrubland coincided witha charcoal peak, indicating a sudden increase of fire incidence(Montoya et al., 2011). In Mapaurí, local forests appeared slightlyafter the vegetation replacement, when the savannas were alreadyestablished, but regional forests were already increasing during thevegetation replacement (Rull, 2009b). Therefore, a synergisticeffect between climate and fire seems to have been the driver of theestablishment of present-day savannas in these areas. The origin ofthese fires (natural or anthropic) is still unknown, but theirtemporal patterns and intensity are very similar to recent records ofanthropic fires. In addition, it has been proposed that the consistentoccurrence of high charcoal concentrations is a strong indicator ofhuman presence, even in the absence of other obvious evidence ofland use (as is the case of the GS) (Bush et al., 2007). Therefore,a Lateglacial to early Holocene establishment of human populationsusing fire cannot be dismissed, though more clear evidence is stillneeded (Montoya et al., 2011).

Fig. 8. Summary percentage pollen diagram and charcoal concentration for theHolocene recorded from the Mapaurí peat bog sediments (Gran Sabana). The forestassemblage at the base of the diagram is dominated by Catostemma pollen, whereasmost of the pollen of herbaceous plants corresponds to Poaceae. Charcoal particleswere classified into two categories: small (<100 mm), as a proxy for regional fires, andlarge (>100 mm), as a proxy for local fires (Rull, 1999). Note the good temporal matchbetween forest reduction and savanna establishment and charcoal increase; Modifiedfrom Rull (2009b).

Fig. 9. Summary percentage pollen diagram and charcoal concentration for the Lateglacial recorded from the Lake Chonita sediments (Gran Sabana). Charcoal I corresponds to smallcharcoal particles (<100 mm) and charcoal II to the larger fraction. The lower part of the sequence was barren for palynomorphs, probably because of meteorisation. Note thecoincidence between the establishment of treeless savannas at the expense of the YD shrublands and the dramatic fire increase; Modified from Montoya et al. (2011).

Fig. 10. Morichal (Mauritia flexuosa) stands around Lake Encantada (Photo: V. Rull).

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The GS forests and shrublands did not recover, resulting ina clearance that remains today. This is true even in the absence offurther increases in fire intensity, as is shown in the palae-oecological record of Laguna Encantada covering the last 7500years (Montoya et al., 2009). According to present-day ecologicalstudies, the burning of GS forests triggered an irreversible degra-dational sequence leading to the establishment of savannas, andforest recovery was prevented by edaphic impoverishment, both innutrients and water retention capacity (Fölster, 1986, 1992; Fölsterand Dezzeo, 1994). This low forest resilience is supported by theUrué record, through the palaeoecological reconstruction ofa secondary succession after a fire event that eradicated the forestfrom the site. The detailed record of the last millennium showeda degradational sequence from the original forests to opensecondary forests of different composition, followed by shrub-lands, fern communities and, finally, treeless savanna, in theabsence of further local fires (Rull, 1999). There were also increasesin the moisture balance in the last centuries that were not fol-lowed by forest recovery, except for the establishment of “mor-ichales” or palm stands dominated by Mauritia flexuosa (Fig. 10),which is a typical element of the present-day GS gallery forests(Rull, 1998). The same sequence has been observed in other GSlakes during the last two millennia (Rull, 1992). In all cases, theMauritia arrival and expansion coincided with a remarkablecharcoal increase, which likely represents the establishment of

modern GS inhabitants with common burning practices (Montoya,2011) (Figs. 11 and 12).

In summary, fire and its synergies with climate are largelyresponsible for the present-day GS landscape. Palaeoecologicalreconstructions reveal a progressive forest clearance and savannaexpansion since the YD, mainly because of the low resilience of GS

Fig. 11. Summary percentage pollen diagram and charcoal concentration for the lastmillennia recorded from Lake Chonita sediments (Gran Sabana). Note the coincidencebetween the sudden appearance and increase of Mauritia pollen and the onset of fireincidence, interpreted as the establishment of the present-day indigenous culture.Modified from Montoya (2011).

Fig. 13. View of the Tirepón-tepui and its densely forested slopes, close to the Eruoda-tepui, in the Chimantá massif (Photo: V. Rull).

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forests, which were unable to recover after fire, even underfavourable climatic conditions. Forest clearance has acceleratedduring the last two millennia because of an intensification ofhuman-driven fire incidence. Therefore, it could be predicted thatsavanna expansion at the expense of forest and shrub formationswill continue in the GS if the current fire management continues.Fire extinction practices are not a solution because of their above-mentioned low efficiency. Forest conservation should focus onpreventive rather than corrective policies; however, the deeprooting of fire practices in the Pemón culture is a handicap. At

Fig. 12. Fires affecting a morichal community near Santa Elena de Uairén. Note thatMauritia flexuosa palms are not burnt because of the rapidity in which fire propagatesthrough herbs (Photo: V. Rull).

present, there is a multidisciplinary initiative to improve commu-nication among the different actors involved in the GS conservation(Bilbao et al., 2010). However, it largely relies on the Pemónknowledge of fire and the a priori correctness of their practices forlandscape management. Palaeoecological knowledge presentedhere should be considered for a more objective approach.

8.3. Biotic responses to environmental change in the GuayanaHighlands’ undisturbed ecosystems

The Guayana Highlands (GH) are an assemblage of more or lessflat summits of the quartzite/sandstone table mountains, locallycalled “tepuis”, located in the neotropical Guayana region ofnorthern South America (Figs. 13 and 14). From a biogeographicpoint of view, the GH summits above 1500 m (which are thehighest) constitute a biogeographic province called Pantepui(Huber, 1987, 1994b). The tepui summits can reach extensions up toabout 1000 km2 and altitudes up to 3000 m, and they containamazing levels of diversity and endemism, as manifested in theapproximately 2500 known species of vascular plants, of whichalmost 30% are Pantepui endemics and around 25% are localendemics or restricted to one single mountain (Berry et al., 1995;Berry and Riina, 2005). The Pantepui biomes have lasted in analmost-pristine state of conservation because of their remotenessand inaccessibility and, probably more importantly, the lack ofnatural resources to exploit (Huber, 1995). This makes them uniqueenvironments to record natural climatic variability and the corre-sponding ecosystem responses (Rull, 2007b, 2010c). The GH have

Fig. 14. General view of the Ilú-Tramen tepuian massif (Photo: V. Rull).

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been free from direct human disturbances, such as mining for goldand diamonds, logging and burning, shifting cultivation, populationpressure, and tourism, which are common in the surroundinglowlands and midlands (Huber, 1995). However, one of the mainconcerns for Pantepui biota is the potential effect of the ongoingglobal warming if the IPCC predictions for this century are accurate(Rull and Vegas-Vilarrúbia, 2006). Recent studies suggest that,under this scenario, a drastic reduction in the available habitat forsummit taxa because of warming-driven upward migration wouldresult in the extinction by habitat loss of around 80% of the Pan-tepui species (Rull et al., 2009, Nogué et al., 2009a).

Palaeoecological records may help to evaluate the reliability andthe eventual impact of such estimates by comparing themwith thenatural upward migration rates since the LGM. Based on twosequences from the lowlands and midlands around the GuayanaHighlands, it has been estimated that natural rates of temperatureincrease since the LGM have been approximately 0.025 �C/century,which corresponds to upward shifts of around 5 m/century (Bushet al., 2004; Rull, 2007a). The estimated rates for the projectedglobal warming of the 21st century in northern South America are3 �C/century (Solomon et al., 2007), which is equivalent to anupward migration of approximately 500 m/century (Rull andVegas-Vilarrúbia, 2006; Nogué et al., 2009a). Therefore, globalwarming rates would be 100 times the natural rates for Pantepuispecies. Unfortunately, the lack of autoecological studies for the

Fig. 15. Percentage pollen diagram from the summit of the Eruoda-tepui, in the Chimantáduring the Holocene; Modified from Nogué et al. (2009b).

Pantepui taxa prevent an inference of their potential response tothis warming acceleration, but similar rates have been measuredfor recent upward migrations forced by the ongoing global warm-ing in other mountain regions (e.g., Kelly and Goulden, 2008; Lenoiret al., 2008). To test the ability of Pantepui species to migrate atsimilar rates in response to global warming, a comparison of thepresent-day situation with historical botanical records is needed(Rull et al., 2009).

The available palaeoecological information for the tepuisummits refers mainly to the Holocene. Most records proceed fromthe Chimantá tepuian massif, except for two from the Guaiquinimamassif. In the Chimantá massif, three tepuis (Acopán, Amurí andToronó) showed an outstanding vegetation constancy over the last6000 years, with only minor local reorganisations between Steg-olepis meadows and Bonnetia gallery forests, which is likely due tolateral migration of water currents along the extensive alluvialplains (Rull, 2005a). In the Eruoda-tepui, of the same massif,vegetation constancy was also the norm during the Holocene(Nogué et al., 2009b) (Fig. 15). However, a gentle vegetation shift atapproximately 100e200 m elevation has been linked to an upwarddisplacement of the altitudinal ecotone between the Stegolepismeadows and the Chimantaea shrublands in the Churí-tepui,approximately 2.5 cal ky BP (Rull, 2004a,b,c) (Fig. 16). The Guai-quinima records showed successive replacements of three vege-tation types e Stegolepis meadows, Archytaea gallery forests and

massif. Note the constancy of the pollen assemblages throughout the whole diagram

Fig. 16. Summary percentage pollen diagram from the summit of the Churí-tepui(Chimantá massif). Assemblage A is dominated by Stegolepis (S) and corresponds to theherbaceous meadows typical of this massif. Assemblage B is dominated by Chimantaea(Ch), an endemic genus of the Chimantá and a few adjacent tepuis, and represents theunique shrublands of the Chimantá. The upper altitudinal limit of Stegolepis is around2300 m, whereas the Chimantaea shrublands grow above this elevation. The vegetationshift before 1450 cal yr BP was interpreted as an upslope biotic migration, likelybecause of a gentle warming; Redrawn from Rull (2004a).

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upland forests-during the last 8 cal ky BP, which were attributed tomoisture changes, probably of regional extent (Rull, 2005b). Basedon these tepuian records, palaeoecological and palaeoclimaticcorrelations have been elusive, and the norm seems to be anextended biotic constancy spiked with local ecological rearrange-ments or a spatial heterogeneity in the responses to minortemperature and moisture changes experienced during the Holo-cene (Rull, 2010c). Another factor to be considered is the sensitivityof the studied sites to climatic changes and variations. For example,the Churí site, the only one in which an altitudinal ecological shifthas been recorded, is in a key ecotone. Other Chimantá localites,notably Acopán, Amurí amd Toronó, are near the middle of themeadows’ altitudinal range, where a small climatic oscillation is notenough to determine a significant vegetation change.

The observed spatial heterogeneity of vegetation responses toHolocene climatic changes in the tepuian summits prevents anygeneralisation and complicates forecasts relating to global warm-ing. On the one hand, local moisture changes seem to have been thedecisive factor for biotic change, except for Churí, where a slighttemperature shift seems to have played a role in vegetationreplacement. This complicates the predictions of future responsesof Pantepui biota to global warming and suggests that forecastingbased only on temperature changes may overestimate the magni-tude of projected extinctions by habitat loss. In addition, thepotential existence of microsites with suitable environmentalconditions for the persistence of the potentially threatened specieswould relax environmental stresses and favour the survival ofa number of theoretically endangered species. Indeed, the potentialoccurrence of glacial and late-glacial microrefugia was firstproposed for the tepuian summits (Rull et al., 1988; Rull, 2009c).

In summary, modelling based on present-day biogeographicalpatterns, physiography and an average IPCC scenario for the 21stcentury suggest catastrophic extinctions by habitat loss in thePantepui vascular flora, which involves the extinction of a signifi-cant number of endemic species; however, palaeoecologicalrecords provide a more optimistic view, suggesting the possibilityof survival for a number of species because of their ecologicaltolerance and/or ability to thrive in microrefugia. In the first case,only ex situ conservation strategies (botanical gardens, seed andgermoplasm banks, etc.) would be able to guarantee species’conservation, whereas in the second, in situ practices would

contribute to biodiversity preservation (Rull et al., 2009). The hopeis that modelling and palaeoecological results will progressivelyhave better agreement, when models will be properly para-meterised and calibrated based on palaeoecological knowledge anduse lower grid sizes to account for local topographical and micro-climatic features (Willis and Bhagwat, 2009; Sublette et al., 2011).

9. Conclusions

Palaeoecological knowledge provides valuable clues to under-stand biotic responses to natural and human disturbances, as wellas the synergies between them, and is a necessary input for natureconservation because it furnishes essential tools to anticipatepotential biological consequences of ongoing global change,thereby contributing to better conservation policies. From theabove literature review on the subject, the following lessons havebeen highlighted:

� The significance of palaeocological studies for nature conser-vation issues could be considered a manifestation of theimportance of past records for the elucidation of long-termecological processes, which are difficult to resolve with onlyneoecological surveys that only cover several decades. Indeed,processes such as ecological succession, secular migration,extinction, adaptation, and microevolution may take centuriesor even millennia to occur, depending on the duration of thelifecycle of the involved species. Therefore, predictions aboutpotential biological consequences of near-future environ-mental changes rely on an appropriate knowledge of bioticresponses to past, secular to millennial, environmentalchanges, which are only available from palaeoecologicalrecords.

� The available palaeoecological knowledge shows that potentialbiotic responses to environmental changes transcend theframework of neoecological studies. For example, the oldecological debate about individual or collective responses toenvironmental disturbances has been recently resolved infavour of the first option in the context of palaeoecologicalrecords. An interesting consequence is the possibility of newunknown species combinations with no modern analoguesresulting from future environmental shifts. Past records havealready shown similar situations and provided usefulanalogues for hypothesis testing about potential futurescenarios.

� Acclimation and/or adaptation, with the first relying onphenotypic plasticity and the second involving genetic changesof potential evolutionary significance, have been proposed astwo possible reactions to future global warming and as alter-natives to extinction by habitat loss. Genetic adaptation seemsto be an unlikely option given the short temporal frameinvolved. However, palaeoecological and molecular phyloge-netic studies would support the possibility of rapid evolu-tionary changes resulting from the existence of pre-adaptedgenomes that would eventually be successful under the newpredicted climatic conditions.

� In the context of the palaeoecological data available so far, theresponse of organisms and communities to future globalwarming is not expected to be homogeneous but rather highlydependent on local and regional environmental conditions.This highlights the importance of conductingmicro- andmeso-scale surveys that consider local particularities for conservationplanning.

� Current predictions of species extinction by habitat loss wouldoverestimate these risks and should be revised because theyrarely consider the possibility of survival within small local

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microsites with favourable conditions (microrefugia) for theinvolved species. Past records suggest that microrefugia wouldhave been decisive for the preservation of particular geneticcombinations during significant environmental changes, suchas the Pleistocene glaciations, and contribute to an under-standing of the present-day genetic structure of species andtheir populations. To properly revise the existing extinctionforecasts, models using spatial grids as small as possible arerecommended to capture local topographical and microcli-matic conditions as potential future microrefugia. From thisperspective, and accounting for the palaeoecological back-ground, some authors propose that spatial reorganisationswithout extinction will be the dominant biotic response to thenear-future global changes.

� Predictions about future biotic responses to future changescommonly rely on an implicitly assumed equilibrium betweenorganisms, their communities, and the environment. However,palaeoecological records show that biotic reactions would bemuch more complex because of the non-linearity of theecological processes involved, which would lead to unexpectedbiotic responses through enhanced feedback. The morecommon mechanism for the occurrence of these “surprises” isthe existence of inherent biotic thresholds that, once sur-passed, may lead to different potential stable states of theaffected ecosystems. Environmental changes need not benecessarily abrupt to produce threshold responses; even subtleand gradual shifts may determine ecological surprises. It is alsopossible that ecosystems never attain equilibrium, and tran-sient states perpetuate because of the recurrent action ofenvironmental change.

� The resilience of an ecosystem, or its capacity to absorbdisturbances with no significant changes, is a critical feature inthe biotic response to environmental reorganisations. Pastrecords provide examples of the type and magnitude ofexternal drivers needed to modify significant ecosystemproperties and determine threshold responses. One of themainlessons from this is that ecosystems may express their resil-ience when confronted with environmental shifts by attainingseveral possible equilibrium states, as manifested in changes inbiodiversity and/or composition, without losing their ecolog-ical functions. Palaeoecological reconstructions also show thatsuch ecological changes are often irreversible (hysteresis).

� Palaeoecology is able to provide past analogues for projectedglobal warming and the corresponding biotic responses, whichis of high relevance for delineating successful conservationpolicies. The global warming recorded at the end of theYounger Dryas (ca 13.0 to 11.5 kyr BP) emerges as one of themore powerful of these analogues because bothmagnitude andrates of change parallel those predicted for the present century.We should also note that the main biotic response to thispalaeoclimatical event seems to have consisted of ecologicalreorganisations and changes in community compositionbecause of differential species migration patterns and rates. Sofar, it has not been possible to associate large-scale extinctionsto the YD climatic reversal. High-resolution studies of the YDwould be decisive, not only to improve our knowledge on bioticresponses of present-day species to climate shifts but alsobecause it would provide the necessary link between paleo-ecology and modern observations.

� Throughout history, humans have not always been aware ofongoing climate changes. Gradual shifts have occurred imper-ceptibly but have promoted profound and irreversible culturalchanges, whereas abrupt changes have prompted adaptation ormitigation responses. In both cases, new environmentalchanges and problems have emerged. A suitable collaboration

between palaeoecology and anthropology may furnish thenecessary information to establish causal links, not only on theinfluence of climate changes in human activities but also onhow the resulting changes in human practices may in turnaffect the environment and ecological function. This, togetherwith a sound knowledge of where and how sensitive ecosys-tems develop, would greatly improve forecasting and antici-pation skills when confronted with current climate change.

� Mismanagement of natural resources combined with vulner-able social organisation seem to have played a key role inprecipitating the collapse of complex past civilisations underclimatic stress. Present drawbacks, such as the exponentialgrowth of human population under a globalised economybased on market rules and consumerism, promote socialinjustice and cause the overexploitation of natural resources,the uncontrolled increase of greenhouse gas emissions, andother environmental damages. Using historical examples asanalogues would illustrate the structural weaknesses ofmodern societies, leading to the inability to appropriately copewith current and future climate change. The non-linearity ofecological processes would be an additional handicap tosuccessfully adapt to or mitigate these unprecedented trans-formations of Earth’s climate. Indeed, negative synergismswould cause the appearance of new threshold triggers,promoting chronic stresses, which may result in the appear-ance of new disturbances and the elimination of others. Thetimely recognition of such situations is crucial for ecosystemmanagement and conservation policies.

� The correct assumptions of threshold conservation models willstrongly rely on knowledge about key indicator parameters andtheir spatial and temporal patterns of change. Ecologicalmonitoring and surveys spanning weeks to decades are able toprovide relevant indicator variables and threshold patterns.However, as noted above, many ecological processes occur overtimescales that exceed the so-called long-term observationalecological datasets. Real long-term ecological knowledge needslong-term biodiversity baselines and paleoecological data,which are crucial for testing predictions about ecosystemsthresholds and resilience. Paleoecological records may helpanswer key questions about the threshold dynamics ofecosystems, such as the following: What is the capacity forrebuilding an ecosystem? Have there been several stable statesover time? What is the biotic capacity of a given ecosystem tocope with disturbance triggers? Are there particularly resilientspecies? Which situations have increased the vulnerability ofa system in the past, favouring a change of state? Can transientstates be recognised? Where and when are thresholds morefrequent?

� One of the main drivers of ecological change introduced byhumans has been fire incidence, through increases in bothfrequency and intensity. The occurrence of wildfires has beenextensively documented through the history of the biospherebefore humans and has been related to the flammability ofvegetation, which is dependent on the O2 atmosphericconcentration, climate, internal water content and the accu-mulation of flammable compounds. Fire has been consideredan important factor for the distribution of vegetation because,in the absence of burning, forests would double their presentglobal cover at the expense of open vegetation dominated bygrasses.

� Fire incidence has increased and coincided with the rise ofhuman populations and their geographical dispersal, especiallyfrom approximately 20,000 years ago. Fire events recordedduring the last glaciation seem to have been synchronous withmillennial-scale warmings associated with D/O events, thus

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suggesting that climate shifts have favoured their occurrence.The same is true for the YD, when an increase in fire incidencehas been documented, especially during the YDeHoloceneglobal warming. Since that time, the causes of fires docu-mented in the palaeoecological records e either natural oranthropic e are difficult to ascertain, but there is a generalconsensus that human activities have been the main drivers offire during the last millennia, especially since the 19th century.Another important element to consider is the occurrence andsuitability of the available fuel (mostly vegetation). Synergisticeffects among climate, human activities and fuel characteristicshave also been considered decisive factors because of theoccurrence of positive feedbacks.

� The neotropical case studies presented here emphasise theimportance of concentrating efforts on the YD shift and theassociated biotic responses as an analogue for ongoing globalwarming, the potential role of fire in the development ofpresent-day neotropical landscapes, the spatial heterogeneityof biotic responses to climate changes, and the need forrevising current habitat loss estimates as a consequence ofglobal warming predicted for the 21st century. Another inter-esting consequence for conservation is that palaeoecology mayprovide decisive clues for choosing more appropriate sites andmore sensitive organisms and communities to study bioticresponses to both natural and anthropic disturbances. Forexample, high-altitude Andean environments would bea preferred target because of the occurrence of conspicuousvertical migrations in response to climatic shifts, which areeasily recognisable in palaeoecological records. Also, thedetection of sensitive taxa, such as Podocarpus, Polylepis,Huperzia or Isoëtes, which are widely distributed in thenorthern Andes, provide suitable indicators for monitoring andmodelling the biotic consequences of climate shifts, possibly ata regional level.

� The Gran Sabana and the Guayana highlands provide examplesof contrasting situations. Indeed, despite a low populationdensity, anthropic fires are the major driver of present-daylandscapes in the Gran Sabana, whereas the tepui summitsare a unique example of pristine ecosystems in which naturalenvironmental changes have been the main force for ecologicalchange. Concerning indicator taxa, in the context of thepalaeoecological results, M. flexuosa would be considereda good proxy for the establishment of present-day indigenousculture in the Gran Sabana, and taxa, such as Chimantaea andStegolepis, emerge as keystone species in the understanding ofthe responses of tepuian vegetation to climatic shifts. Thesetwo examples also reveal the suitability of ecotones aspreferred palaeoecological targets to provide key informationon biotic responses to environmental change of natural and/oranthropic origin.

The historical review carried out in this paper providesevidence that, despite its relatively recent inception in theconservation arena, palaeoecology is becoming an important andnecessary discipline needed to properly understand subjacentecological processes useful for management purposes. However,the lack of synergy between palaeoecologists, neoecologists,anthropologists and conservation scientists is still a handicap.We hope that this paper may contribute and improve the situa-tion by showing the variety of aspects in which palaecology canbe of utility for conservation and by showing that palae-oecological input, beyond a theoretical proposal, should bebased on sound knowledge, including real case studies andspecific propositions and recommendations with straightforwardapplicability.

Acknowledgements

The authors would like to thank the QSR Editorial Office for theinvitation to write this review. Funding has been provided by theBanco de Bilbao Vizcaya Argentaria Foundation (FBBVA, projectBIOCON-08-031), the Spanish Ministry of Science and Innovation(MICINN, project CGL2009-07069/BOS), and the Higher Council forScientific Research (CSIC, project 200830I258). We acknowledgeSimonConnor forhishelp regarding thehuman impactbibliography.

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