A General Review with Examples from the Neotropicsq

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 review with examples from the neotropicsq

T. Vegas-Vilarrúbia a,*, V. Rull b, E. Montoya b,c, E. Safont b a Department of Ecology, University of Barcelona, Av. Diagonal 645, 08028 Barcelona, Spain b Palynology and Palaeoecology Lab, Botanical Institute of Barcelona (CSIC-ICUB), Pg. del Migdia s/n, 08038 Barcelona, Spain c Department of Animal Biology, Plant Biology and Ecology, Autonomous University of Barcelona, Faculty of Biosciences, Bld C1, Cerdanyola del Vallès, 08193 Barcelona, Spain article info abstract

Article history: Palaeoecology, as an ecological discipline, is able to provide relevant inputs for conservation science and Received 12 March 2011 ecosystem management, especially for issues involving long-term processes, such as ecological succes- Received in revised form 5 May 2011 sion, migration, adaptation, microevolution, and extinction. This use of palaeoecology has been noted for Accepted 7 May 2011 several decades, and it has become widely accepted, especially in the frame of ongoing and near-future Available online 20 June 2011 global warming and its potential biotic consequences. Selected palaeoecological insights of interest for conservation include the following: 1) species respond in an individualistic manner to environmental Keywords: changes that lead to changes in community composition, suggesting that future ecosystems would have Long-term ecology no modern analogues; 2) in the short-term, acclimation is more likely a response of species that are Palaeoclimates expected to persist in the face of global warming, but the possibility of evolutionary change linked to the Biotic responses existence of pre-adapted genomes cannot be dismissed; 3) species unable to acclimate or adapt to new Resilience conditions should migrate or become extinct, which has been observed in past records; 4) current Threshold responses extinction estimates for the near-future should be revised in light of palaeoecological information, which Past analogues shows that spatial reorganisations and persistence in suitable microrefugia have been more common Global change than extinction during the Quaternary; 5) biotic responses to environmental changes do not necessarily Human disturbance Abrupt changes follow the rules of equilibrium dynamics but depend on complex and non-linear processes that lead to Gradual changes unexpected “surprises”, which are favoured by the occurrence of thresholds and amplifying positive Tropical America feedbacks; 6) threshold responses can cause the movement of ecosystems among several potentially stable states depending on their resilience, or the persistence of transient states; 7) species and their communities have responded to environmental changes in a heterogeneous fashion according to the local and regional features, which is crucial for present and future management policies; 8) the global warming that occurred at the end of the Younger Drays cold reversal (ca 13.0 to 11.5 cal kyr BP) took place 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 acted upon ecosystems in an indirect way by modifying human behaviour and activities that, in turn, have had the potential of changing the environment and enhancing the disturbance effects by synergistic processes involving positive feedbacks; 10) the collapse of past civilisations under climate stress has been chiefly the result of inadequate management procedures and weaknesses in social organisation, which would be a warning for the present uncontrolled growth of human population, the consequent overexploitation of natural resources, and the continuous increase of greenhouse gas emissions; 11) the impact of fire as a decisive ecological agent has increased since the rise of humans, especially during the last millennia, but anthropic fires were not dominant over natural fires until the 19th century; 12) fire has been an essential element in the development and ecological dynamics of many ecosystems, and it has significantly affected the worldwide biome distribution; 13) climateefireehuman synergies that amplify the effects of climate, or fire alone, have been important in the shaping of modern landscapes.

q This paper is dedicated to Margaret Bryan Davis for her pioneering work in palaeoecology and its applications to nature conservation, which set the stage for all further developments. * Corresponding author. Tel.: þ34 934031376; fax: þ34 934111438. E-mail addresses: [email protected] (T. Vegas-Vilarrúbia), [email protected] (V. Rull), [email protected] (E. Montoya), [email protected] (E. Safont).

These general paleoecological observations and others that have emerged from case studies of particular problems can improve the preservation of biodiversity and ecosystem functions. Nature conservation requires the full consideration of palaeoecological knowledge in an ecological context, along with the synergistic cooperation of palaeoecologists with neoecologists, anthropologists, and conservation scientists. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction past analogues for rapid and gradual climatic changes and fire, acting either separately or simultaneously, along with their This paper reviews the most significant literature available on ecological consequences. Finally, the main conclusions of this the usefulness of palaeoecology in the field of nature conservation review are identified, and we highlight several conservation to extract the more relevant lessons from the past to improve recommendations derived from these conclusions. present and future ecosystem management. This paper also provides several selected case studies from the Neotropical region 2. Ecology and palaeoecology: what is long-term? to show how palaeorecords can address real conservation problems, with assessments and recommendations of immediate Presently, it is widely acknowledged that short-term ecological applicability. This review also attempts to be a service to the studies are not enough for reliable predictions on the potential palaeoecological community to facilitate access to the more rele- consequences of future environmental changes and human vant knowledge and related literature on the subject. In addition, disturbance, and long-term surveys are increasingly recognised as we hope that this contribution may enhance the interest of a necessary tool for this purpose (e.g., Huntley, 1996; Jackson, palaeoscientists on the importance of our disciplines for conser- 2001). However, there is no agreement on the meaning of short- vation, thereby promoting discussion and hopefully leading to the term and long-term. For example, in a recent special issue of continuous improvement of our skills. Our approach is based on the Trends in Ecology and Evolution entitled “Long-term ecological broad concept of ecology, which is seen as a discipline embracing studies”, most papers deal with data extending to a couple of palaeoecology, neoecology and predictive ecology. Interaction decades, and only one uses a palaeoecological approach (Willis between these disciplines is needed for a proper understanding of et al., 2010a). There is no standard definition for long-term in the biosphere and its functioning and to deal with its potential ecology, but some explicit statements within papers on the subject reactions to future environmental change (Rull, 2010a). As consider a lower boundary between 20 and 50 years for long-term expressed in the title, the emphasis is on global warming and fire as studies (Willis et al., 2007a). environmental stressors; other subjects, such as eutrophication, For obvious reasons, the connection between palaeoecology and acidification, pollution, and soil erosion, have been reviewed and conservation science has many coincidences with the relationship discussed elsewhere (e.g., Smol, 2008; Pelejero et al., 2010; Albright between ecology and palaeoecology that, despite what their names et al., 2010). Emphasis will be placed on the Quaternary (i.e., the last may suggest, have progressed historically as separate disciplines. 2.58 million years (Ma), as defined by Gibbard et al. (2010); According to Rull (2010a), this unfortunate disjunction has been however, references to former periods will be included when facilitated by the following: 1) the pastepresent dissociation necessary. characteristic of the human mind, 2) the diversity of fields of The review begins with a discussion of the meaning of “long- provenance for palaeoecologists, 3) the contrasting nature of the term” in ecology to set a suitable temporal framework and to evidence and associated methodological differences, and 4) emphasise that neoecology and palaeoecology, despite methodo- misunderstandings caused by the use of the prefix palaeo-. logical differences, share common objectives. The second part is However, the principle of uniformitarianism emphasises that past, a summary of the biotic responses documented so far to past present and future are not discrete units, but rather a time climate changes, and their significance to ongoing and future global continuum through which species and communities flow, change warming. Following these sections, a summary is provided of key and evolve, and that ecology and palaeoecology are simply different developments in the applications of palaeoecology to conservation. approaches with a common objective, which is the ecological This account is based mainly on review papers and aims to intro- understanding of the biosphere. Ecology, in a broad sense, includes duce the relevant concepts in a historical fashion and highlight the inferences about the past (palaeoecology), present studies (neo- leading researchers and research groups in this field. The next ecology or contemporary ecology) and future projections (predic- section concerns potential past analogues for projected global tive ecology). Therefore, palaeoecology is essentially community warming, which could be used in forecast modelling. The anthropic ecology stretched backward through the fourth dimension of time factor is then introduced in the section about indirect impacts of (Schoonmaker and Foster, 1991), or it can also mean ecological climatic change. This section is devoted to the possibility of dis- studies that use the past as proxies (Rull, 2010a). In this context, entangling natural from human causes for past ecological changes long-term should have a single meaning. and records those situations in which synergies between these two The importance of temporal and spatial scales in ecology and drivers have determined a priori unexpected ecological responses. palaeoecology has been emphasised by Delcourt and Delcourt Fire, which is among the more influential ecological disturbances of (1988). More recently, Jackson (2001) has distinguished three anthropic origin, is then discussed based on its occurrence patterns time domains useful to deal with the ecologyepalaeoecology and incidence throughout Earth’s history, with an emphasis on its continuity. These domains are as follows: real-time, which is the natural or human-induced nature since the last glacial period, time frame usually considered in neoecology, which spans from when present-day ecosystems developed. Concerning examples of weeks to decades and includes processes such as population the usefulness of past records for conservation, we use our own dynamics, competition or predatoreprey interactions; Q-time work in the Neotropical region of northern South America, mainly (where Q is for Quaternary), which ranges from centuries to in the Andean highlands, the Gran Sabana midlands, and the millennia, encompasses processes such as succession, migration or summits of the Guayanan tabular mountains, or tepuis. We provide extinction; and deep-time, which includes a wide range of T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2363 timescales typically over 105 years and accounts for evolutionary rates complicated the picture. Another important consequence is that trends and large-scale biogeographic reorganisations. The time communities have not been constant through time, suggesting that length of the processes mentioned above depends on the organ- they are loose and relatively ephemeral assemblages of species pop- isms involved, mainly in relation to their generation times and the ulations, as formerly proposed by Whittaker (1951). Further palae- duration of their biological cycles. For example, ecological succes- oecological evidence has reinforced this view (Bennett, 1997,and sion in plankton communities may elapse over a year or merely literature therein). The projection of these results into the future a season, whereas in a forest, it may take centuries or millennia to allowed researchers to prognosticate that, by the end of this century, occur. Therefore, a multidecadal study would be able to capture the occurrence of novel climates and biotic communities with no actual long-term processes for the first case, but it is clearly modern analogues will be common on the planet as a consequence of insufficient in the second case. Therefore, it seems appropriate to ongoing climate change (Williams and Jackson, 2007; Williams et al., refer to real-time phenomena as short-time ecological processes, 2007). Therefore, management procedures should adapt to these new and to use long-term for ecological processes occurring at Q- combinations, with unknown community organisation, functional timescales (Rull and Vegas-Vilarrúbia, 2011). This will be the properties and ecosystem dynamics (Hobbs et al., 2006; Willis et al., convention used in this paper. Therefore, real long-term ecological 2007b; Willis and Bhagwat, 2010). Current predictions of non- studies and, hence, conservation science need evidence from the analogue or novel communities are based on ecological models par- past, that is, palaeoecological input. ameterised from present-day observations that may fail to predict ecological responses to novel climates. These models should be vali- 3. Biotic responses to environmental change: past and future dated against palaeoecological evidence to enhance their robustness and predictive accuracy (Williams and Jackson, 2007). Forecasts about the nature of future responses to climate change Key elements to be considered in the individualistic behaviour and other environmental disturbances require a deep knowledge of of species in relation to environmental change include particular the past and present biotic responses to the same or similar differences in their sensitivity to relevant environmental factors, ecological forcings. Palaeoecology has provided decisive evidence response lags and migration ability, and the availability of specific on the responses of organisms and their communities to past niche requirements (suitable substrates, pollinators, etc.). These environmental shifts, mainly in relation to climate changes. Multi- factors would constitute a handicap for many organisms to track proxy studies are especially well suited for this purpose because the projected climate change at similar rates. In principle, it could they furnish independent physical and/or chemical evidence of be assumed that organisms with short lifecycles (e.g., planktonic environmental change and avoid potential circular reasoning. organisms) would respond faster than those with longer generation Important aspects of the biotic responses to environmental shifts times, such as trees, which could take decades to centuries to are the nature (individualistic or collective), the type (migration, respond (Davis, 1985). However, several recent palaeoecological extinction), the magnitude and extent (local, regional, global), the records have depicted short or absent time lags between rapid time lags with respect to the environmental shift, and the rates of environmental shifts and a varied array of organisms, including change. Palaeorecords of these features can be used as past cladocera, chrinomids and vascular plants (Ammann et al., 2000; analogues to infer potential future responses of organisms and Birks and Birks, 2008). Historical records have also shown rela- communities to the predicted future environmental changes. The tively rapid migrational responses (1 to several m per year, records can also be used to disentangle natural from anthropic depending on the species) of vegetation to the global warming causes of ecological change. Hewitt and Nichols (2005) have syn- experienced during the last century, especially in the form of alti- thesised the three more important types of biotic responses in the tudinal and latitudinal migrations (Walther et al., 2002; Parmesan expression “adapt, move or die”, which equates to evolution, range and Yohe, 2003; Parmesan, 2005, 2006; Kelly and Goulden, 2008; shifts or extinction. However, there is a fourth possibility, which is Lenoir et al., 2008; and literature therein). Therefore, according to persistence, despite environmental change, because of phenotypic palaeoecological and historical records, the capacity of organisms plasticity in the less sensitive species (Davis et al., 2005). According to track the ongoing climate change at similar rates seems to be to the palaeorecords, there are five main modes in which organisms higher than previously expected. and communities respond to climatic variations: growth or death, species migration, changes in community composition, evolu- 3.2. Migration and microrefugia tionary changes, and extinction (Overpeck et al., 2003). The nature of the response depends on the scale, considered in both space and The more common biotic response to climate change during the time (see also Delcourt and Delcourt, 1988). The following section Quaternary seems to have been migrational range shifts (Davis and provides an updated summary of the main elements required for Shaw, 2001; Seppä and Bennett, 2003). The better known examples the evaluation of biotic responses to external factors based on the of this are the postglacial recolonisations of northern temperate information provided by past records. continents by tree forest species from southern refugia with a favourable climate, where they endured the last glaciation (Davis, 3.1. Individualistic responses and non-analogue communities 1981; Huntley and Birks,1983). This led to estimated migration rates between 100 and 1000 m/year, which are unrealistic considering The issue of the individualistic (at the species level) vs. collective the known dispersal mechanisms of the species involved (Clark (at a community level) biotic responses has been a long ecological et al., 2003; MacLachlan et al., 2005). Alternatively, migration debate between the Gleasonian and the Clementsian schools, which could have also proceeded from numerous, more or less widespread, are defenders of the first and second option, respectively (Clements, microrefugia, or “small areas with local favourable environmental 1916; Gleason, 1926). The classical works of Davis (1981) in North features, in which small populations can survive outside their main America and Huntley and Birks (1983) in Europe have shown that distribution area (the macrorefugium), protected from the unfav- postglacial recolonisation of these continents by trees from temperate ourable regional environmental conditions” (Rull, 2009c). The forests proceeded in an individual fashion, and, as a consequence, expansion of these widespread, small populations, favoured by current forests are composed of species that arrived at different times postglacial warming, is more consistent with the relatively rapid from various southern glacial refugia (Schoonmaker and Foster,1991). continental colonisation rates under the current dispersal mecha- Furthermore, individual differences in response lags and migration nisms of these tree species (Pearson, 2006). These microrefugia are 2364 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 difficult to identify with common palaeoecological methods because Schwartz, 2009)- and has been important in many biomes (e.g., of their assumed small size and unknown distribution (Rull, 2010b), Richardson et al., 2001; Lister, 2003; Rull, 2008; Valente et al., but intra-specific genetic patterns of the involved species provide 2010); however, given the rapid rate at which the ongoing evidence of their existence and suggestions for their geographical climate change is predicted to occur during this century, it is distribution (Willis and van Andel, 2004; Bhagat and Willis, 2008; difficult to develop potential analogies. Hewitt and Nichols (2005) Petit et al., 2008; Provan and Bennett, 2008). The idea of micro- have reviewed this topic and concluded that there is no conclu- refugia is not only interesting for migration rates and species’ sive evidence supporting or denying genetic adaptation to changing genetic structure but also for biodiversity conservation purposes climates in the recent past. Palaeoecological records since the Last because hypothetical future microrefugia (natural or artificially Glacial Maximum (LGM) show that changes in distribution fuelled created) could help to mitigate the extent of the projected biotic by climate changes have had important consequences for intra- extinction resulting from climate change by providing suitable specific genetic diversity (see also Hewitt, 2000, 2003; Lascaux microhabitat conditions for threatened species (Rull, 2009c). et al., 2003; Magri, 2008). The key question is if genetic changes According to Davis and Shaw (2001), past records show that range have persisted long enough to be fixed and, if so, if the standing shifts and genetic adaptation proceeded together during the genetic diversity has influenced species’ fitness. Quaternary climatic changes and could not be considered alterna- According to Davis et al. (2005) and Lavergne et al. (2010), biotic tive biotic responses, but this topic will be analysed further in the responses to climate changes involve both ecological and evolu- next section. The potential of palaeoecology records, especially tionary elements that cannot be disentangled. For example, pollen, macrofossil and charcoal records, for the reconstruction of responses, such as persistence, migration or extinction, are inti- plant migration and invasion patterns in both space and time has mately linked to microevolutionary reorganisation that influences been reviewed by Mitchell (2010), who emphasises the need for species’ sensitivity and adaptation ability (Davis et al., 2005). enhanced mapping of pollen and biomes on continental and global Microevolution also affects ecosystem assembly and functioning scales and more collaborative efforts among palaeoecology, (Cavender-Bares et al., 2009); therefore, emergent properties, such community ecology and genetic studies to improve the testing of as biodiversity or stability, affect not only the response to envi- ecological hypotheses. ronmental changes but also future evolutionary trajectories. Therefore, the incorporation of eco-evolutionary feedbacks is 3.3. Acclimation and adaptation needed for biodiversity forecasting, and for a better understanding of ecological dynamics in relation to anthropic environmental Sensitivity is another key parameter to understand the reactions changes (Lavergne et al., 2010). Currently, models to properly of organisms to environmental changes. In principle, the more forecast potential adaptation to environmental change are under sensitive species should be those with a narrow tolerance for the development (Salamin et al., 2010). We should also note that the relevant environmental variables (stenotopic), or those living near structure and survival of source populations and their genetic the edge of their ranges. Eurytopic species, with a large phenotypic legacy may be endangered for many species, and the need for plasticity, should be less sensitive to changes, especially if they live identifying and conserving glacial refuge areas should be far from their range boundaries. In every case, to produce a biotic emphasised (Hewitt and Nichols, 2005). response, a given environmental change should cross a threshold determined by the range of tolerance of the involved species. The 3.4. Extinction process by which a species resists an environmental change because of its wide tolerance or phenotypic plasticity is called Extinction occurs when all the other potential responses fail. acclimation, whereas adaptation involves genetic (i.e., evolu- Under changing environments, extinction of a species may result tionary) changes. There is the general a priori perception that the from an inability to migrate and to resist or adapt to changes, but it high rates of climate change predicted for the near-future will may also occur if the species’ habitat is lost or fragmented/reduced prevent genetic adaptation, but some authors think that the role of to the extent that populations lack the genetic variability to survive adaptation as a response to future climate change has been over- natural perturbations, such as extreme climatic events, epidemics, looked. According to these authors, populations may adapt to the and fire (Overpeck et al., 2003). Additionally, because of the new climates through the occurrence of pre-adapted individuals ecological interplay within the ecosystem, the extinction of certain that can eventually increase their density (Davis and Shaw, 2001; key and/or dominant species may generate cascade effects affecting Kelly et al., 2003). Indeed, species can adapt to new environments other related species (hosts, parasites, pollinators, etc.) in the form by either waiting for the appearance of novel, advantageous of the so-called secondary extinctions (e.g., Lafferty and Kuris, mutations or evolving immediately using alleles from the standing 2009). Biodiversity loss by increased extinction because of direct (pre-existing) genetic variation (Stapley et al., 2010). Therefore, (habitat fragmentation, pollution, fire) or indirect (global warming) the adaptation of populations to a different climate will depend on consequences of human activities is a common output of predictive the level of climate-related genetic variability already contained in models for the end of this century (e.g., Thomas et al., 2004; the population. Another source of adaptive genetic variation is Peterson et al., 2005). Some believe that the ongoing and future admixture and the resulting gene flow between two divergent human-induced global biodiversity reduction is comparable to one populations (Barrett and Schlutter, 2008). In the case of relatively of the five major extinctions that have occurred in the geological contiguous populations, adaptation may be aided by migration history of Earth (Courtillot, 1999), and they term it the sixth (Jump and Peñuelas, 2005). These hypotheses, however, are diffi- extinction (Wake and Vredenburg, 2008). cult to confirm or reject with the traditional Quaternary palae- At a human time scale, the last significant extinction event oecological methods (Seppä and Bennett, 2003) because of lower occurred between 50,000 and 10,000 years ago, when most large taxonomical resolution than required, and they have been evalu- mammals became extinct everywhere except Africa (Koch and ated in combination with molecular phylogenetic evidence (Willis Barnosky, 2006; Barnosky, 2009). Contrastingly, there is evidence et al., 2003). for the extinction of one single plant species (Picea critchfieldii, Recent molecular phylogenetic studies have shown that a spruce) in North America during the same period (Jackson and Quaternary speciation has indeed occurred -for example, humans Weng, 1999). The competing causal mechanisms for mammal are only a 200,000-year-old Quaternary species (Tattersall and extinction were either climate change or human activities; T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2365 however, it is now widely accepted that the extinction was caused replacement of current communities by novel species combina- by the synergy of both, especially the coincidence of the Younger tions. As a result, emphasis for biodiversity conservation was not Dryas cooling (ca 13.5 to 11.5 kyr BP) and increased human hunting placed on the preservation of communities but on the maintenance (Barnosky and Lindsey, 2010). This has been considered a potential of species’ ecological niches (Bush and Hooghiemstra, 2005). Con- analogy for the present and the near-future because of the coinci- cerning marine ecosystems, the observed responses to past envi- dence of rapid climate change and increased human population and ronmental shifts have been varied, ranging from large disturbance. In this sense, it is important to note that the failure to biogeographical reorganisations to insignificant changes, even in adjust to changing climates did not arise from the magnitude alone, the face of significant climate changes, such as the gla- but also from the rapid rates of change. Generally, a complicating cialeinterglacial alternation, as in the case of corals (Roy and factor to avoid extinction by biotic adjustment to environmental Pandolfi,2005). Similarly, some past climatic events seem to have changes is that these have occurred at different rates and magni- determined widespread extinctions, whereas others of similar tudes and over different temporal and spatial scales, thus causing intensity have not. The cause of these heterogeneous patterns disequilibrium or dynamic equilibrium between the environment remains unknown. According to the same authors, a possible and the biotic communities (Overpeck et al., 2003). synergistic relationship between climate change and the conse- A contrasting view is provided by Willis et al. (2010b), who has quences of human activities, primarily in the form of habitat noted that, in the fossil record, global extinctions due solely to degradation and biodiversity loss, will be important for under- global warming are very rare (mammal extinctions are associated standing future marine responses to climate change. mainly to human action in this case), suggesting that extinction rates because of future climate change would have been over- 3.6. Transient and non-linear responses estimated (see also Pearson, 2006). This would be due in part to the coarse scale of the models used to estimate habitat loss, which fail Potential future biotic responses to global change are often to capture potential microclimatic features that could help species approached by biome simulations, which implicitly assume biotic avoid extinction (Willis and Bhagwat, 2009; Sublette et al., 2011). equilibrium responses. However, palaeoecological records have Indeed, recent models using more detailed topographies have shown that this equilibrium between organisms and climate is resulted in less catastrophic extinction predictions (e.g., Randin rarely attained, and most of the time, the responding biota shows et al., 2009; Hole et al., 2009). According to Willis and Bhagwat a transient response to environmental fluctuations characterised by (2009), the more likely responses of future ecosystems to climatic extended time lags. This response, combined with the potential change will be, like in the past, rapid community turnovers, broad- occurrence of unpredictable responses and the existence of positive scale migrations, threshold events and the formation of novel biosphere-climate feedbacks that can magnify both environmental ecosystems. This would be valid for widely distributed species, but changes and biotic responses, severely constrains the possibility of local extinction, which has been well documented by palae- anticipating future threats to biodiversity and ecosystem dynamics, oecology (e.g., Postigo-Mijarra et al., 2010; González-Sampériz even if future climatic changes are well known (Overpeck et al., et al., 2010 and literature therein), can be fatal for endemic species. 2003). During the past decades, the concept of non-equilibrium 3.5. Spatial heterogeneity ecology has emerged, emphasising the complexity and non- linearity of ecosystem dynamics that explains such behaviour An important lesson from palaeoecological studies is that, like (Holling, 1973; May, 1977). According to the non-equilibrium the physical changes, the biotic responses have not been homoge- concept, rare events, management disturbances and resource neous throughout the planet. Indeed, palaeoecological evidence exploitation have the potential to move the systems between has shown that, in northern temperate latitudes, the most impor- multiple stable states. No large impacts are needed to promote tant responses of biota to past change have been migrations, or dramatic shifts; even a tiny incremental change in conditions can changes in the spatial extent and location of species’ ranges, and trigger a catastrophic shift if a critical threshold is passed (Holling extinctions by habitat loss. Adaptive responses have also been et al., 1995). Complex interactions, such as positive feedback, recorded, but mostly from persistent environmental shifts. Conse- would account for this pathway (Suding and Hobes, 2009). In this quently, it was predicted that the main response to future climate context, equilibrium would be a temporary artefact of observation, change will consist of extinctions and individual range adjust- not an intrinsic system property (Wallington et al., 2005). There are ments, whereas evolutionary change will be limited (Huntley, some recent examples that illustrate how such changes occur 2005). In the southern continents, human activities seem to have suddenly (Scheffer and Carpenter, 2003 and literature therein). been decisive for current biotic patterns, and climate variability was Sudden and unexpected responses in the behaviour of envi- considered at least as important as climate absolutes in governing ronmental and ecological systems have been called surprises biodiversity responses. Therefore, these two factors are considered (Broecker, 1987; Overpeck, 1996). Concerning conservation, the to be the most significant for future biotic patterns. Based on the more important surprises seem to be those linked to abrupt palaeoecological evidence, it was predicted that range adjustments threshold-crossing changes manifested as “jumps” in the palae- to future climate change will be difficult or impossible in most cases oecological records. Given the complexity and non-linearity of because of the current, severe habitat fragmentation. Competition nature, these jumps should be expected to occur in the future in with introduced alien species will likely be another complicating a stochastic fashion, much as they have occurred in the past. factor for the survival of native species (Markgraf and McGlone, Palaeoecology may be useful for predicting their occurrence, 2005). understanding their causes, and preventing their biotic conse- In the tropics, available palaeoecological evidence supports the quences. The non-linear dynamics of the earth system and the observation that species have been more resilient to climatic existence of thresholds, which, if crossed, may determine abrupt change, and extinction has been rare. The main response to envi- and unexpected environmental and biotic changes, have also been ronmental shifts seems to have been changes in community highlighted by Bradley et al. (2003), who declared that the message composition because of the individualistic behaviour of species. from the palaeorecords is that change is normal and the unex- Therefore, it was prognosticated that, under future climatic change, pected can happen. According to these authors, abrupt responses to species will expand or contract their ranges and determine the gradual forcing are common in past records at all time and space 2366 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 scales. They also provide some selected examples. The upper and for our own approach. The following historical review should not be lower bounds within which atmospheric CO2 concentrations have considered a comprehensive account of all the papers and authors varied over the past four glacial cycles seem to be thresholds for the involved in the development of this field. Rather, it is an attempt to global carbon cycle, which influences photosynthetic efficiency. show how the main concepts have progressively emerged through The glacial/interglacial cycles are thought to be threshold responses time to conform to the present state of the art. Despite the relatively to gradual insolation changes. Another threshold is the potential short-time elapsed, barely two decades, the evolution of ideas and migration rate of organisms, which may determine their extinction proposals on this topic has been intense, likely because of the if environmental change proceeds faster. Willis and Bhagwat (2010) sound ecological background of the leading scholars involved. provide selected palaeoecological examples of ecological thresh- The importance of palaeoecological knowledge for nature olds. If these thresholds are crossed, the ecosystem switches from conservation began after 1960, when it was realised that many one stable state to another within a relatively short-time interval. environments were seriously threatened by eutrophication, acidi- Human impact is emphasised as a driver of these switches. fication, pollution and accelerated soil erosion (Oldfield, 2004). A Another non-linear dynamic feature common to past climate couple of decades ago, the discussion about future global climatic and environmental processes is hysteresis, or the irreversibility of and environmental changes, and their potential impact on Earth’s changes once a given threshold has been crossed. Examples of this life, determined the full establishment of palaeoecology as an behaviour are the thermohaline circulation shutdown that important input for nature conservation (Delcourt and Delcourt, occurred at the onset of the Younger Dryas cold event and the 1991). The International GeosphereeBiosphere Programme (IGBP) present-day increase in atmospheric CO2 (Bradley et al., 2003). was created in 1986 by the International Council of Scientific Unions (ICSU) to study the interactions between biological, chem- 3.7. Resilience ical and physical processes and interactions with human systems to develop and impart the understanding necessary to respond to Resilience was formerly defined in ecological terms as the global change (http://www.igbp.net). In 1991, PAGES (Past Global magnitude of disturbance that an ecosystem can experience before Changes) was launched as a core project of the IGBP to support it shifts into a different stability domain (Holling, 1973), or, in other research aimed at understanding the Earth’s past environment to words, before crossing a threshold towards another stable state make predictions for the future (http://www.igbp-pages.org). (Willis and Bhagwat, 2010). Ecological resilience was re-defined by Therefore, PAGES is responsible for palaeoecological knowledge in Folke et al. (2004) as the capacity of an ecosystem to absorb the context of global change. Despite this official appointment, the disturbance and reorganise to retain the same function, structure, role of palaeoecology in conservation, and in ecological science in identity, and feedbacks. It is believed that the resilience of general, has often been underrated by many scholars and institu- ecosystems is being constantly eroded by the ongoing environ- tions, and palaeoecological results have traditionally had little mental deterioration because of human activities, resulting in impact on ecological thinking (McGlone, 1996). This has favoured systems that are progressively more vulnerable to changes that the proliferation of reviews and opinion papers from palae- could have previously been absorbed (Folke et al., 2004). Therefore, oecologists trying to convince the general ecological and conser- in conservation ecology, it is essential to know how, when and why vation audience of the need for a palaeoecological approach (Rull, a given ecosystem is approaching a critical resilience threshold to 2010a). adopt more adequate policies (Scheffer et al., 2009). According to Although not properly acknowledged in many recent reviews Rockström et al. (2009), humanity has already transgressed three of and research papers on palaeoecology and conservation, the the nine known critical environmental thresholds, including the eminent palaeoecologist Margaret B. Davis pioneered this field and rates of climate change and biodiversity loss and the interference summarised the contribution of palaeoecological knowledge to with the nitrogen cycle. nature conservation into five lessons related to biotic responses to Palaeoecology provides illustrative examples of ecosystem environmental change as follows (Davis, 1989, 1991): 1) species resilience to environmental change at several temporal domains, respond individually to changing environments, which determines occasionally followed by threshold responses, which are often, but changes in community composition through time (Davis, 1981); 2) not always, linked to climatic surprises and human impact (Carrión biotic responses have a time lag with respect to environmental et al., 2001, 2010; Willis et al., 2007b; Willis and Bhagwat, 2010). A shifts, where the magnitude depends on the duration of the life- detailed analysis of these past records can be useful to identify the cycle of the species involved; 3) disturbance regimes and climate nature, extent and magnitude of external forcings needed to affect changes are not independent, as is shown by the higher fire relevant ecosystem properties (i.e., biodiversity or composition) frequency in drier climates, for example (Davis, 1985); 4) some and improve conservation strategies. Of great interest is the human activities, notably agriculture, can have more impact than potential for palaeoecological records to provide information about climate change on shaping the landscape; and 5) presently, the combinations of biotic and abiotic processes that determine a variety of impacts are occurring that have not been seen in the ecosystem resilience and the multiplicity of potential equilibrium palaeoecological records (warming, UV radiation increase, acid states, which are two aspects considered critical for future biodi- deposition), which may result in new species’ assemblages. The versity conservation (Willis et al., 2007b). first comprehensive account trying to relate palaeoecology and conservation was a special issue of Trends in Ecology and Evolution 4. Palaeoecology and conservation: historical background entitled “Biology and Palaeobiology of Global Climate Change”, coordinated by M.B. Davis. A general conclusion of this special issue Several reviews have been published recently by eminent was that predictions of the effects of climate change on biological scholars on the usefulness of a palaeoecological approach for systems required much more information on environmental nature conservation, with emphasis on biodiversity issues (e.g., physiology and its genetic control, at both organism and commu- Lyman, 2006; MacDonald et al., 2008; Smol, 2008; Dietl and Flessa, nity levels (Davis, 1990). Shortly after, Hazel and Paul Delcourt, who 2009; Davies and Bunting, 2010; Willis et al., 2007a, 2010a, among greatly contributed to the view of palaeoecology as an ecological others). These papers already provide an excellent summary of the discipline, proposed that the mid-Holocene Hypsithermal Interval findings on this subject. Here, we will only summarise them in could be a partial analogue for global warming-induced biotic a historical and conceptual fashion to provide a sound background changes, which would be useful to anticipate the nature and T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2367 geographic patterns of biotic response to the initial 2 C warming study of decade-to-century-scale climate variability (PAGES/CLI- (Delcourt and Delcourt, 1991). After the analysis of several palae- VAR intersection), the mechanisms and consequences of past oecological case studies, these authors have proposed that modern climatic changes using ocean sediments (IMAGES), palaeoclimate communities may disassemble and lose biodiversity by local or and environmental variability in polar regions, and interactions global extinction. Community reassembling is considered, but not between human activities, climate, and environmental processes in the same geographical areas and only after a lag of several (http://www.pages-igbp.org/science/formerfoci.html). millennia, depending on differential migrational rates and the A few years after the creation of PAGES, Huntley (1996) noticed trajectories of species. Additionally, palaeoecological records may that, 30 years before, the understanding of mechanisms by which help to identify more vulnerable areas, which is useful information organisms and communities respond to a changing environment needed to select suitable sites for ecological preserves (Delcourt would have been only of academic interest, whereas today this and Delcourt, 1991). knowledge is essential to nature conservation. During this time, Coincidentally, another outstanding scientist who has led the palaeoecology (mainly pollen analysis and palaeolimnology) field from the beginning, Brian Huntley, has published interesting underwent significant developments in both methods and reviews of palaeoecological case studies oriented to demonstrate approaches in several major areas: chronological accuracy, which is its potential usefulness for biodiversity conservation (Huntley, derived from the application of new radiometric techniques; 1990, 1991). According to this author, one of the main contribu- quantification and modelling of underlying patterns and processes, tions is to provide long-term records that are able to elucidate if the such as pollen dispersal or sedimentation rates; research design, present-day nature of communities, sites and landscapes are the including more precise targets and testable hypotheses; taxonomic result of either stability or change, including human disturbance. accuracy, notably increasing the number of fossil taxa identified; Like Davis (1989, 1991), Huntley (1990) emphasised the temporary spatial and temporal accuracy, by increasing the resolution or nature of communities at a millennial time scale, mainly because of interpretations to meter-scale and yearly records; higher precision the individual character of the biotic response to environmental in the estimation of past environmental variables, such as change and the consequent differential migration rates of species temperature, precipitation, pH, and salinity, by using training (Huntley and Birks, 1983; Huntley and Webb, 1989; Huntley et al., datasets and specific statistical methods; and the use of multi- 1989). Concerning conservation strategies, this author emphas- proxy approaches that combine a variety of independent physico- ised that strategies that rely upon the conservation of isolated sites chemical and biological indicators derived from more reliable in an otherwise inhospitable terrain will likely be unsuccessful. reconstructions (Birks, 1996; Huntley, 1996). Despite these According to Huntley (1990), the main conservation concern should improvements and the potential contribution that palaeoecology be the human pollution of the atmosphere, primarily in the form of would have made to nature conservation, the lack of synergy global environmental change derived from increased amounts of between conservation science and palaeoecology at that time was CO2 and other greenhouse gases. surprising (Birks, 1996). To illustrate the potential usefulness of The Intergovernmental Panel on Climate Change (IPCC) was palaeoecology in this context, Birks (1996), who has been instru- created in 1989 as a joint effort of the World Meteorological mental in the development of modern palaeoecology, discussed Organisation (WMO) and the United Nations Environmental using illustrative examples of how this discipline would be helpful Program (UNEP) to provide the governments of the world with for conservation assessments on the naturalness, fragility, and balanced information and a clear scientific view of climate change status of endangered species, and for supporting ecosystem resto- (http://www.ipcc.ch). The first IPCC assessment report, published ration decisions. However, the lack of detailed autoecological one year later, used palaeodata to show the millennial-scale rela- information for most species of interest was still a handicap tionship between atmospheric CO2 concentration and temperature ( Huntley, 1996). over the last 160,000 years and noted that the projected warming Swetnam et al. (1999) defined “historical ecology” as a discipline for the 21st century would be 15e40 times faster than natural embracing “data, techniques, and perspectives derived from changes (Houghton et al., 1990). Concerning the potential biotic palaeoecology, land-use history from archival and documentary response to warming, the first IPCC report mentioned that palae- research, and long-term ecological research from monitoring and oecological studies were able to provide insights on potential future experiments extending over decades”, and “time series from consequences, emphasising poleward migration and extinction instrument-based observations of the environments”. According to (Tegart et al., 1990). The striking progress of palaeoclimatic and these workers, historical ecology can inform conservation palaeoecological science experienced during the last two decades management by defining baseline conditions of vegetation has produced high-quality historical records, with resolution and communities, their range expansions and contractions through accuracy that make them comparable to actual measurements and, time, and by discriminating between natural and anthropic causes therefore, useful to validate explanatory and predictive models of environmental change. Historical ecology showed that the (Huntley, 1996; Rull, 2010a). Consequently, palaeodata are now unpredictability of biotic responses to environmental change and recognised as a necessary component of climate change studies and the climate-organism non-equilibrium paradigm were key factors its potential impacts, as described in the latest IPCC report (Parry to consider. Therefore, the detection and explanation of historical et al., 2007; Solomon et al., 2007). The following is an account of trends and variability are essential for better nature management the progress towards this realisation. (Swetnam et al., 1999). PAGES began by orienting the palaeo-research efforts towards A review by Gorham et al. (2001) identified the following five three main points: 1) methodological homogenisation to make the major questions linked to conservation that palaeoecology can help records comparable; 2) focus on two temporal scales, namely the to answer: What were the properties of communities, ecosystems, last two millennia (Stream I) and the two glacial cycles (Stream II); and landscapes prior to or following natural or human distur- and 3) the disentangling of natural and anthropic causes of envi- bances? What has been the pattern of recovery from disturbance, ronmental change (Eddy, 1992). From a geographical perspective, and was the prior state re-established? What is the nature and the PAGES research was organised into three main Pole- magnitude of natural variability and the frequency of unusually eEquatorePole (PEP) terrestrial transects (i.e., the PANASH focus): extreme conditions? Were communities and ecosystems relatively the American continent (PEP-I), Asia-Oceania (PEP-II), and stable prior to disturbance, or were there significant trends or EuropeeAfrica (PEP-III). Other PAGES foci were as follows : the fluctuations in some of their properties? Do anthropic disturbances 2368 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 have effects that are different in degree or kind from those of commitment of the US National Ocean and Atmospheric Adminis- natural disturbances? These authors stress the wide range of spatial tration (NOAA), an organisation with a long tradition of involve- and temporal scales at which palaeoecological analyses are useful ment in research on palaeoclimate and management of marine and the variety of environmental problems that it is able to address, fisheries, to take the lead not only in the management of global emphasising freshwater acidification and biodiversity loss. Gorham multi-proxy palaeoenvironmental databases and their forecasting et al. (2001) also discuss what they call the “surprise factor” in potential but also in the incorporation of biotic responses to past palaeoecology (see above). As a general conclusion, Gorham et al. climate changes as a proxy for future predictions (NRC, 2005), a task (2001) stress the need for palaeoecological records to design that is still one of NOAA’s primary mandates (http://www.ncdc. more adequate environmental monitoring programs, and recom- noaa.gov/palaeo/palaeo.html). mend the use of multi-proxy methodologies. The importance of palaeoecology for conservation science A synthesis of the results obtained by PAGES until 2003 was experienced a promising increase, with regard to publications since published in a book entitled “Palaeoclimate, Global Change and the 2007, coinciding with the publication of the fourth IPCC assess- Future” (Alverson et al., 2003). After analysing all the contributions ment, in which palaeoecology played a significant role (Parry et al., of the PAGES book, Bradley et al. (2003) recommended the 2007; Solomon et al., 2007). The formerly limited use of historical following policies: 1) reducing greenhouse gases to reduce global evidence in biodiversity conservation has been attributed to the warming; 2) understanding, monitoring and possibly preventing perception of insufficient resolution in both space and time, the changes in regional climate linked to thermohaline circulation; 3) lack of accessibility of palaeoecological records to non-specialists, sequestering fossil fuel carbon in terrestrial or oceanic reservoirs; and the lack of a positive attitude of many Quaternary scientists 4) developing natural reserves to maintain biodiversity; 5) towards conservation issues (Willis et al., 2007a; Froyd and Willis, detecting and attributing global and regional change to natural or 2008). Since then, a number of palaeoecologists have devoted anthropic forcing; and 6) managing lake catchments, coastal zones important efforts to make evident the direct usefulness of palae- and landcover to protect them for future generations. In the same oecology in conservation, not only from a theoretical perspective, PAGES book, Overpeck et al. (2003) analysed the response of the as occurred previously, but also by providing examples and case biosphere to the known past climate and environmental variability studies and enumerating the areas in which the study of the past to extract information useful to predict potential future biotic would be especially helpful. An interesting contribution, published reactions to ongoing global change. According to these authors, almost at the same time as the fourth IPCC report, was made by “assessments of future conditions without a strong palae- Edwards et al. (2007), who explored the usefulness of palaeoenvironmental component will not be successful”,as“records of oecology to provide more robust estimates of temperature increase past climate and biosphere change are the only information we for this century. They concluded that modelling should benefit from have on the nature and consequences of large environmental the large amount of available palaeodata syntheses and palae- changes”. The resulting recommendations for future palaeoclimatic reconstructions and that model simulations should focus oecological research were as follows: 1) improve the understanding on local rather than regional averages. The Oxford Long-Term of climate variability and biosphere responses and feedbacks; 2) Ecology Laboratory, headed by Katherine J. Willis, has made emphasise high-resolution records that reveal the nature of inter- significant contributions to the utility of palaeoecology in conser- annual climate and biosphere change; 3) increase the number of vation. This research team and several associated co-workers have investigations that examine the ecological consequences of future shown that palaeoecology can significantly help conservation climatic change in light of past records; and 4) enhance the inter- science, especially biodiversity conservation, in the following areas: action among disciplines, such as palaeoenvironmental, ecological 1) the identification of species at risk from extinction, 2) the setting and land-use management, climate and climate modelling, and of realistic goals and targets for conservation, 3) the identification social science communities (Overpeck et al., 2003). Oldfield (2004) of management tools for the maintenance or restoration of a given has provided similar recommendations and added the need for past biological state, 4) the determination of baselines and natural analogues of the ongoing global warming, a better understanding ecosystem variability, 5) the understanding of ecological thresholds of the role of solar variability, more information on hydrological and resilience, 6) the assessment of climate change and conserva- variability, and a better understanding of Holocene eustatic sea- tion strategies, 7) the documentation of biological invasions, 8) the level changes. determination of rates and the nature of biotic response to climate As a result of this previous research and knowledge, the US change, 9) the management of novel ecosystems, and 10) the National Research Council officially recognised the importance of improvement of red lists and similar conservation tools (Willis palaeoecology for nature conservation and published a mono- et al., 2007a,b; 2010a; Froyd and Willis, 2008; Guillson et al., graphy entitled “The Geological Record of Ecological Dynamics: 2008; Willis and Bhagwat, 2010). The usefulness of palae- Understanding the Biotic Effects of Future Environmental Change”, oecological knowledge for ecosystem restoration was emphasized which declared that “the understanding of the patterns, processes, by Jackson and Hobbs (2009). Additionally, Davies and Bunting and principles governing the participation of biological systems in (2010) identified 24 conservation questions, from the 100 posed environmental change e and understanding how those systems by Sutherland et al. (2006), in which palaeoecology can make major respond e is a scientific and societal priority of the highest rank” contributions (Table 1). Concerning conservation strategies for (NRC, 2005). In this sense, three initiatives were proposed: 1) to use protecting biodiversity, historical records can provide significant the geological record as a laboratory to frame and test ecological advice on the following: 1) managing novel ecosystems, as the theories at appropriate scales while encompassing a full range of emergence of unprecedented species’ combinations will likely be earth conditions; 2) to study ecological responses to past climatic favoured by future climate change; 2) retaining ecological memory change to provide a more sound basis for forecasting the ecological in the form of microrefugia; 3) conserving regions of high genetic consequences of future climate change and variability; and 3) to diversity, as they may hold high evolutionary potential; and 4) gain knowledge of the ecological legacies of societal activities to developing resilience to threshold events (Willis et al., 2010b). assess the ecological conditions and variability before human Smol (2008) offered an excellent review and discussion, with impacts and to gather the geohistorical records of how societal many illustrative and convincing examples, on the contribution of activities have affected present-day ecosystem dynamics. An palaeolimnological records to conservation aspects, such as acidi- important consequence of this official pronunciation was the fication, eutrophication, metal and organic pollution, soil erosion, T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2369

Table 1 The 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-natural woodlands vs. absence of active management? Fisheries, aquaculture and How long does it take the seabed to recover from disturbance? marine conservation 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 the ecological 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 schemes and would they be cost-effective..? What methods most accurately measure ecological status in the EU Water Framework Directive?

species invasion, and ozone depletion, among others. Potential evolution of palaeo climatology and palaeoecology outcomes. future ocean acidification has also been discussed recently, in the Currently, the PAGES research structure is organised around four context of palaeoecological evidence, by Pelejero et al. (2010). foci and four Cross-Cutting Themes (CCT). Each focus covers a set of Conservation palaeobiology, a term coined by Flessa (2002), has questions of prime importance to the global community. The CCT been recently revived by Dietl and Flessa (2009). It has been defined are more general in their scope and are of fundamental relevance to as “a synthetic field of research that applies the theories and all foci and to palaeoscience in general (Fig. 1). Concerning analytical tools of palaeontology to the solution of problems concerning 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 natural ecological and evolutionary laboratory. According to the same authors, the second approach sets the field apart from historical ecology, which is considered a sister discipline; such an approach is needed to deal with aspects like speciation, extinction or adaptation, which require a longer temporal perspective. The main palae- obiological contributions to conservation highlighted by Dietl and Flessa (2009, 2010) are the potential for defining baselines and natural variability, the identification of more vulnerable species to be protected, and the nature of biotic responses to climate change. Much of the recent progress on the application of palaeoecology to conservation can be attributed to ongoing developments, such as higher chronological resolution, better models on atmospher- eebiosphere system functioning, the incorporation of new chemical and biological proxies to reconstruct past species distributions and past climates, the availability of large geo-referenced databases with biogeographical and climatic data, and new approaches concerning fossil morphology and molecular DNA techniques (MacDonald et al., 2008). All of the previously mentioned authors recognise structural barriers to developing multidisciplinary teams and networks with ecologists and decision makers, but they emphasise the need for such collaboration for suitable nature conservation. Fig. 1. PAGES scientific structure: four thematic foci (coloured circles) are com- PAGES has progressively adapted its structure, objectives, plemented by four circling Cross-Cutting Themes that are of relevance to all foci. programs and priorities according to new findings and the Reproduced from http://www.pages-igbp.org/science/index.html. 2370 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 databases, the NOAA has become the worldwide repository of warmings or coolings within glacial or interglacial conditions, palaeoenvironmental and palaeoecological data, in the form of respectively, and have been proposed as models to evaluate the multi-proxy records on all subjects related to climate change possible consequences of the ongoing greenhouse gas buildup (http://www.ncdc.noaa.gov/palaeo/palaeo.html). Additionally, the (Broecker, 2000). These cycles have been broadly identified, use of both continental and marine core data as the original source correlated and named, and the vegetation response to these cycles for palaeoecological records can be found on the websites of the has been studied using pollen analysis (e.g., Tzedakis et al., 2004; International Continental Scientific Drilling Programme (ICDP), at Fletcher et al., 2010); however, suitable candidates for global http://www.icdp-online.org, and the Ocean Drilling Program, at warming analogues have not been proposed. http://www.icdp-online.org. Researchers can use these sites to Some have also proposed the warming recorded at the Palae- download the palaeodata required for model calibrations and oceneeEocene transition as another past analogue (McInerney and simulations at local, regional and global levels. Wing, 2011). This warming trend initiated around 59 Ma and culminated with the Early Eocene Climatic Optimum, between 53 5. Past analogues for future global change and 51 Ma (Zachos et al., 2008). Within this relatively gradual trend, a sudden acceleration occurred around 55 Ma, known as the Often, it is argued that the global change predicted for this PalaeoceneeEocene Thermal Maximum (PETM), during which the century is unprecedented, mainly because of the high prognosti- temperature increased more than 5 C in less than 10,000 years cated rates at which it will occur. However, palaeoecologists (Zachos et al., 2001). During that time, the Earth was a “greenhouse continue to look for past analogues, for which high-resolution Earth” (i.e., free from ice caps, even in the poles); average temper- records are essential. The latter estimates predict, for this century, atures were between 8 C and 12 C higher than today, and the a likely increase in average temperatures between 2 and 4 C (with atmospheric CO2 concentration was around 1000 ppmv or higher a maximum of up to 6.5 C), a sea level rise of around 1 m and an (Zachos et al., 2008). Apparently, such a scenario could be similar to increase 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 past analogues of such fast trends are changes associated with “abrupt” or “rapid” climate shifts, typically occurring at a centennial scale or below (Broecker, 2000). Willis et al. (2010a) provide several examples of palaeoecological records showing similar rates of change for temperature, sea level and atmospheric CO2. The more recent of these events was the rapid warming that occurred during the transition between the Younger Dryas (YD) cold event and the Holocene, just before 11.5 kyr BP, when Greenland air temperatures increased more than 10 C in about 60 years (Steffensen et al., 2008). According to Jackson and Overpeck (2000),anaverage increase of 5 C in 50 years occurred at the end of the YD. Taken as a whole, the warming at the end of the YD proceeded at a rate of around 4 C/century, which matches with the higher IPCC warming scenarios for the 21st century (Fig. 2). Vegetation responses to this rapid warming have been recorded palynologically in many regions of Europe and North America and include the following (Willis et al., 2010a): rapid expansion of local populations, large-scale species range shifts, community turnover, and formation of novel community assemblages (Williams and Jackson, 2007; Birks and Birks,2008; Birks and Willis, 2008). There is no evidence of large-scale extinction in plants; only local or regional extinctions have been documented (Postigo-Mijarra et al., 2010), which contrasts with the conspicuous and well-documented mammal extinctions (see above). Especially noteworthy are the high-resolution studies around the YD performed in North Europe, which allowed detailed studies of the biotic response to warming. This made the long temporal scales of palaeoecological results compatible with the fine temporal scales of modern observations (Birks and Birks, 2008; Bakke et al., 2009). The response of the Fig. 2. Comparison of the IPCC warming predictions for the 21st century and the different organisms studied, including both plants (pollen, macro- Greenland warming inferred from ice core records for the end of the Younger Dryas reversal. Estimated global temperature trends based on actual instrumental measures fossils, mosses, diatoms) and animals (Chironomidae, Cladocera, are represented by a black solid line. Minimum (B1) and maximum (A2) IPCC average Coleoptera, Trichoptera, Oribatidae), to warming showed clear estimates of 21st century global warming (Solomon et al., 2007) are represented by differences in lags, rates and magnitudes (Birks and Ammann, 2000; blue and red lines, respectively. These trends are attached to the left scale, which is the Birks et al., 2000) that were likely due to different spatial scales, life- temperature change with respect to the 1980e1999 average. Joint confidence intervals history temporal scales, sensitivities and ecological behaviours (Birks for all the IPCC estimates are represented by the gray area. The green line is the e estimated Greenland temperature increase as deduced from ice core records (Alley, and Birks, 2008). The YD Holocene transition seems to be an excel- 2000), which follows the right temperature scale. The estimated rate of change for lent past analogue for the predicted 21st century warming (Cole, the YD warming is 4.1 C/century, which falls within the range of the A1B, A2 and A1FI 2009) because it occurred at very similar magnitudes and rates and scenarios (1.7e6.4 C/century) and coincides with the best estimate for the A1FI acted on the same species that exist today. scenario (4.0 C/century). Data for the YD warming have been downloaded from the NOAA World Data Center for Paleoclimatology at http://www.ncdc.noaa.gov/paleo/ Other potential past analogues are linked to the 1500-year Bond data.html (Alley, R.B. 2004. GISP2 Ice Core Temperature and Accumulation Data. cycles, which occurred during both glacial and interglacial periods IGBP PAGES/World Data Center for Paleoclimatology Data Contribution Series #2004- (Bond et al., 1997). These cycles were manifested as either abrupt 013). T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2371 the scenario predicted under near-future global warming. However, information to the ecological debate and conservation the PETM occurred at rates 100 times lower than the 21st century management. predictions, and they took place during a gradual warming over approximately 10 million years. This is a very different situation 6.1. Gradual changes from today’s “icehouse Earth”, which is characterised by the glacialeinterglacial alternation. Additionally, very few, if any, of the The climate has changed over millennia, and these changes are extant species, and probably few genera, existed by that time (Rull, likely to affect ecosystems and the physical environment, which 2008, and literature therein), which prevents the possibility of often respond at the centennial to millennial scale and encompass applying the niche stability assumption. Therefore, the PETM seems long-term processes like succession, migration, extinction and less powerful than the YD as a past analogue for the global warming landscape changes. However, gradual climate changes can trigger prognosticated for this century. prompt shifts in ecosystems to an alternative state because of a loss A past analogue for the predicted sea level increase has been of resilience (Scheffer et al., 2001). Drastic shifts in climate can also proposed by Virah-Sawmy et al. (2009), using a w3 m rise that occur within a century or less (Dansgaard et al., 2003), triggering occurred in the Indian Ocean 2500e3000 years ago, based on fossil responses from the terrestrial biosphere and the physical envi- corals and higher beaches along the coasts of Madagascar (Camoin ronment in less than 200 years (Allen et al., 2000). et al., 2004). At that time, these coasts were dominated by a highly The ability of humans to recognise and respond to climate biodiverse littoral forest, which was suddenly replaced by a heath- change is related to the limitation of the human scale and depends land in less than 50 years. This heathland remained for thousands upon the culturally conditioned canons of perception and of years until the sea level fell again, and the littoral forest was re- comprehension of the populations involved. Human societies are established with a different composition than the former forest able to respond to climatic signals if they are within the scope of (Virah-Sawmy et al., 2009). This dramatic replacement of the their perceptual time span. Within weeks to decades, rapid climate littoral forest by the heathland has been interpreted in terms of changes can be inferred from perceived or measurable modifica- a threshold response of the forest, determined by changes in tions in direct climatic proxies (Hassan, 2009). Short-term envi- salinity and aridity linked to the higher sea level (Willis et al., ronmental responses (such as resource shortages or habitat loss) 2010b). are visible within the time frame of one to three human generations and prompt adjustments to maintain survival or social stability; 6. Indirect impacts of climate changes: human disturbances however, long-term responses escape human awareness and and humaneclimate synergies cannot be taken into account. In fact, the long-term consequences of any decision to cope with climatic crises are commonly not We still know little about the probable impact of climate within the lifetime of a person or a couple of generations (Hassan, changes on the trajectory of human history, and we are even more 2009). The indirect effects of climate changes deal with the ways uncertain of the environmental impact that human responses to people respond to those changes and have received little attention, those climate changes have had. In response to climate changes, both in policy deliberations and scientific research with regard to human societies make adjustments to maintain their modes of life, current and past climate changes. or they try to lessen the magnitude of the derived impacts, thereby The climate varies gradually on millennial and centennial scales. favouring the emergence of new environmental changes and Such changes are less likely to raise people’s awareness, and distant problems with which future generations will have to cope. memories of how climate was before tend to fade gradually. Even when satisfactory records of climate change and high- However, practices that ensure survival in the face of gradual resolution archaeological data exist for a given region, appro- climate changes are slowly adopted, and cultural changes appear priate and sufficient palaeoenvironmental and/or palaeoecological that can profoundly affect the environment (Hassan, 2009). An information is missing, such as ecosystem recovery after depopu- example might be the climate-driven origin of agriculture proposed lation or stresses on food resources after sedimentary settlement. by many authors (e.g., Reed, 1977; Richerson et al., 2001; Hassan, This information is needed to allow for credible assertions on the 2009; Turner et al., 2010a). This activity probably occurred as causal links between human responses to climate and the derived ecosystems responded to the drastic climate shift during the environmental affectation. To establish such causal links, it is PleistoceneeHolocene transition, together with processes oper- necessary first to show that climate impacts on human activities ating from within human social systems (Piperno et al., 2007). have indeed occurred and subsequently to show that these changes Richerson et al. (2001) hypothesised that, besides the decisive fact in human activities have prompted environmental and ecological that the humans of the Last Interglacial were neither cognitively modifications on a causeeeffect basis. nor culturally able to develop agricultural subsistence, agriculture Human responses to change may alter feedbacks between could not have easily evolved in the Pleistocene because of the climate, ecological, and social systems, producing a complex web of harsh climatic conditions that prevailed. Instead, the beginning of multidirectional connections in time and space (Constanza et al., plant-intensive, resource-use strategies would have started only 2007). Ensuring sustainable future responses to the current global after the gradual amelioration of climate took place during the warming may partly depend on our understanding of this past web PleistoceneeHolocene boundary. In fact, the oldest traces of agri- and how to adapt to future surprises. However, several questions culture date between 11,000 and 9000 cal. BP (Willcox, 2005; become apparent: What is the time span needed by humans to Piperno and Dillehay, 2008; Crawford, 2009). The associated become aware of an ongoing climate change and respond with an changes from an ecological and environmental context would have anticipatory behaviour? What kind of information do we need from created new selective pressures on hunter-gatherer human pop- the past to link the effect of past human responses to predictable ulations and their subsistence, leading to innovative and ultimately human responses to current climate change? Are there really useful successful strategies that included exploitation of plant resources. past analogues? In this section, we combine and discuss some For example, Piperno et al. (2007) illustrate this process for the published palaeoecological, palaeoclimatic and anthropological Neotropic, showing that, during the late-glacial period studies to show how, and to what temporal and spatial extent, (14,000e10,000 BP), three lake beds of the Central Balsas (Mexico) human responses to gradual and abrupt climate changes have were dry and covered by open, cool adapted vegetation, with Zea affected the environment and ecosystems, and we contribute this mays as a constituent element. Strong shifts in climate and 2372 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 vegetation associated with the last phases of tropical deglaciation Additionally, many of the effects are cumulative, which implies that took place as the Pleistocene was ending. Temperature and they only achieved global significance by the widespread nature of precipitation rose and the lakes filled up, becoming active human their effects or because of their cumulative magnitude (Turner foci near water sources and allowing Z. mays to be cultivated at the et al., 1990). In terms of conservation purposes, this means that lake edges, starting between 10,000 and 5000 BP. the large-scale effects of slow environmental changes and the During the Holocene climate conditions allowed the evolution of associated human responses are difficult to foresee and impossible agriculture more or less simultaneously in vast areas with relatively to manage unless appropriate long-term records are available and warm, wet climates in the Near East, along with access to irrigation considered when testing hind- and fore-cast model projections. (Willcox, 2005). The transition from the barest beginnings of wild The application of Quaternary palaeoecology to conservation poli- plant cultivation during the Neolithic to almost full dependence on cies and actions could provide the necessary time perspective to domesticated foodstuffs occurred at a millennial scale (Liu et al., anticipate impacts, such as succession, migration, extinction, and 2007; Piperno et al., 2007; Jones and Liu, 2009). The gradual landscape changes, in a more realistic way. Time scales in conser- climate change taking place was probably imperceptible to people, vation studies are typically limited to relatively short-time intervals and the acquisition of a new innovation or technology happened and commonly ignore the magnitude of human responses and the only after several generations. At each point in time, lifestyle dynamics of long-term processes with high environmental impact. changes most likely seemed a result of traditions unrelated to the gradual warming trend. In contrast to these parts of the planet, 6.2. Abrupt changes intermittent and unpredictable droughts occurred in Southeast Amazonia. Droughts, together with environmental constraints on The palaeoclimatic record details how some climate changes agriculture intensification and reliance on wild sources of protein, were vast and in many cases occurred abruptly (Broecker, 2000; led to the perpetuation of nomadism and hindered cultural devel- Alley et al., 2003). Rapid climate changes have often had opment (Meggers, 2007). profound effects on biological populations by imposing stronger Human occupation and utilisation of plant and animal resources selection and distance from environments to which they are have led to widespread landscape changes all over the world during adapted (Davis and Shaw, 2001). the last 10,000 years. Land use and landcover changed because of The US National Research Council (NRC) study ‘Abrupt climate water withdrawal; agriculture was most likely the primary way in change (ACC): inevitable surprises’ defines ACC from two different which humans affected water regimes; irrigation and deforestation points of view: for agriculture have redistributed global evapotranspiration and “technically, an abrupt climate change occurs when the climate altered the regional climate; the use of fertiliser led to nutrient system is forced to cross some threshold, triggering a transition runoff and promoted eutrophication in aquatic ecosystems around to a new state at a rate determined by the climate system itself the world. These changes have driven a decline in ecosystem and faster than the cause. The cause may be chaotic and thus services other than agriculture, such as fisheries and flood regula- undetectably small (NRC, 2002,p.14)”; tion (Gordon et al., 2008). Environmental impacts derived from the “from the point of view of societal and ecological impacts and post-Neolithic expansion of agriculture have been extremely adaptations, abrupt climate change can be viewed as a signifi- important. Over the long-term, these impacts are probably as cant change in climate relative to the accustomed or background important as those generated by the industrial revolution. In fact, climate experienced by the economic or ecological system being Ruddiman (2003) pushed back the start of the Anthropocene era by subject to the change, having sufficient impacts to make adap- thousands of years based on a wide array of archaeological, cultural tation difficult (NRC, 2002,p.121)”. and geological evidence. The term “Anthropocene” was originally coined to denote the fact that current human activity was indeed Note that “abrupt” does not necessarily mean “severe”. The first changing the Earth on a scale comparable with some of the major definition highlights a fast transition to a new state and the events of the ancient past (Crutzen and Steffen, 2003). The apparent irrelevance of the cause, rather than the magnitude of defenders of the early Anthropocene hypothesis (Ruddiman, 2003; the change. The second definition contrasts the abruptness of the 2007; Ruddiman and Ellis, 2009) proposed that the start of forest change and its effects with the capacity of human and ecological clearance by humans reversed a naturally decreasing CO2 trend systems to adapt and overcome the negative impacts over time or 7000 years ago and promoted a new increase in CO2 values, undergo remedial actions. This capacity depends more on ecolog- whereas early rice irrigation and livestock tending had a similar ical and social features, such as stability, resilience, vulnerability, effect on the methane trend beginning 5000 years ago. In pre- flexibility and scale, than on the severity of the climatic disturbance industrial times, the annual rates of carbon release may have (Hassan, 2009). The level of global climate variability and climate been more than 10 times lower, as populations were much smaller change that is tolerable varies enormously depending upon the and technology was much more primitive than today, but the geographic region and the society or ecosystem. The effect of ACC cumulative emissions could still have been extremely large because may be temporary, and the systems may recover if the environ- of the extended time interval over which they operated. The mental perturbation has not been too large (Alley et al., 2003). associated atmospheric warming was estimated to be 0.8e2 C, on ACC has had profound impacts on ecosystems (Davis and Shaw, average. According to the authors, this would have been large 2001) and civilisations worldwide and is still the subject of much enough to have stopped the glaciation of north-eastern Canada research by Quaternarists. Contrary to non-abrupt climate changes, forecasted by two different climatic models. ACC can be perceived and measured by humans because they take If the hypotheses of climate-driven agriculture and early place in the frame of years or decades. Therefore, people are likely human-induced warming can be demonstrated, it could be to recall and compare extreme events and deviations from “normal assumed that the early human-induced global warming was an conditions” that they have experienced in their lifetimes, or those indirect effect of the onset of agriculture activities, giving rise to reported by previous generations (usually no more than three). a positive feedback mechanism with important environmental Such awareness allows for adaptation or mitigation responses to consequences. The effects of these climate changes on the envi- the new conditions (Hassan, 2009; Turner et al., 2010b). Although ronment could have never been properly anticipated by humans ACC has been blamed on the collapse of complex civilisations (de because of the slow and gradual pace of both phenomena. Menocal, 2001; Weiss and Bradley, 2001), it has been proposed T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2373 that mismanagement of natural resources and the vulnerability of identified three dimensions to accommodate human adaptation to social organisations have played a key role in these outcomes climate changes: the force of change, the properties of the system (Hassan, 2009). One example is the Classic Maya Collapse (AD that may influence its sensitivity, and the type of adaptation that is 750e830), which coincided with the most severe and prolonged undertaken. More concretely, per capita income, inequality in the drought of the last millennium. It happened at or near the time distribution of income, universal health care coverage and high when other South and Mesoamerican cultures experienced access to information have been regarded as important determi- declines, apparently also as a result of severe droughts. For nants of adaptive capacity (Alberini et al., 2006). example, the irrigation-dependent Moche civilisation in Perú Current approaches to ecosystem conservation still rely on the suffered destruction and famines during the 6th century; the city of classic view of predictable and stable point equilibria of ecosystems Teotihuacán (México) was abandoned between AD 750 and 800; (Wallington et al., 2005), and habitat management in most systems and the Tiwanaku civilization, in the central Andes, collapsed traditionally assumes linear succession-like trajectories (Scoones, around AD 1000 (Hodell et al., 2004, 2001; Weiss and Bradley, 1999). Over the past several years, conservation and restoration 2001). Droughts associated with the Maya Collapse occurred in biologists and managers have become aware that the potential for a context of unsustainable use of resources, shifts in organisational sudden shifts in ecosystem states is alarming, indicating that and economic strategies and population movements, which likely a system can be less resilient than expected (Suding and Hobbs, hastened the civilization’s demise (Hassan, 2009). 2009). Non-equilibrium ecology may explain such behaviour. If Worldwide comparisons of the impact of different climate disturbances can cause systems to shift between multiple stable change events on past civilizations indicate that climate has been states, it is reasonable to assume that indirect human impacts of a driving force in some instances, and has played a significant role climate change that are derived from adaptation or mitigation can in others. In societies where environmental impacts of climate widen the range of already vulnerable habitats, where threshold changes are not visible, climate shifts may be perceived simply as dynamics can occur and shift communities into new states that are background noise (Catto and Catto, 2004). It is only recently that difficult to reverse. Human activities to cope with climate change can Quaternarists have looked at historical data to search for analogies incorporate new threshold triggers by converting transient events with the present-day situation, where human emissions of green- into persistent disturbances, by introducing chronic stress and house gases, combined with profound impacts on landscape and starting new disturbances, or eliminating important disturbance ecosystems, are leading to unprecedented transformations in the patterns. The abrupt character of current climate change may earth’s climate and creating new forms of vulnerability to rapid accelerate these processes. The timely recognition of such situations onset disasters and long-term environmental change (Anthes et al., is crucial to ecosystem management and conservation policies 2006; Parry et al., 2007; WBGU, 2008). An increasing number of (Wallington et al., 2005). In this regard, threshold models in resto- observational evidence indicates that climate change is already ration and conservation that are being developed as a response to having effects on biological populations (Walther et al., 2002), such this shift in ecological thinking are central to cope with human as changes in the extension of vegetative periods (Peñuelas and response to climate change Suding and Hobbs, 2009). These authors Filella, 2001) and the upward migrations of plants and animals consider that current utilisation of threshold models in habitat (Peñuelas et al., 2002; Parmesan and Yohe, 2003), and on the management still lacks rigorous testing and underlying assump- environment, such as more frequent and severe hurricanes (Anthes tions, and they suggest a framework for incorporating threshold et al., 2006) and greater fire risk (Flannigan et al., 2000). models that effectively helps decision making and management on Awareness of climate change triggers two types of human relatively short-time scales in human impacted systems. response, namely adaptation (involving actions aimed at There is increasing awareness of the need to assess the indirect preserving those systems of interest) and mitigation (actions to effects of climate change derived from adaptation and mitigation lessen the rate and magnitude of the change) (Turner et al., 2010b). actions: as people adapt to climate change across multiple scales, Most mitigation efforts address the environmental change itself to ranging from local to national and international, a wide range of prevent or mitigate climatic disturbances (Smithers and Smith, new risks to ecosystems and biodiversity will emerge. Nonetheless, 1997). These efforts include seeking a reduction in CO2 emissions, the effects of current climate change have not been pronounced encouraging the use of non-carbon or carbon-neutral energy enough to have prompted significant mitigation or adaptation sources, and the promotion of carbon sinks through land-use and efforts (Turner et al., 2010b). habitat management. In poor and vulnerable populations of the Long-term ecological knowledge needs long-term biodiversity world, climate-induced displacement may be the most likely baselines and palaeoecological data, which are crucial for testing mitigation response because of aridity, sea level rise, melting predictions about ecosystem thresholds and resilience (Dietl and glaciers, coastal subsidence and erosion, which threaten roughly Flessa, 2010; Willis et al., 2010a; Rull and Vegas-Vilarrúbia, 2011). 600 million people (Johnson and Krishnamurthy, 2010). The Some messages have been derived from these initiatives German Advisory Council (WBGU, 2008) identified the following (Wallington et al., 2005; Suding and Hobbs, 2009) that are impor- five regional “hotspots”, where significant climate-induced tant for palaeoecology because the temporal dynamics of ecosys- displacement and conflict are expected to occur, most of them tems have a number of implications for conservation management being the result of flooding, windstorms and rising sea levels: the before considering the indirect human impacts to climate change: Caribbean and the Gulf of Mexico; North Africa, especially the Nile Delta; South Asia, especially the GangeseBrahmaputra Basin; Ecosystems are complex and dynamic, and gradual or sudden Eastern China; and the Sahel zone. In this regard, paleoecological changes in composition and structure can be expected over records have already shown how coasts dominated by a biodiverse time. By understanding the history of a place to be preserved, littoral forest can be quickly replaced by a heathland in less than 50 we may improve our understanding, conservation actions and years (Camoin et al., 2004). prediction of future responses, as it forms part of the essential Depending on the way mitigation actions are performed, they context within which to evaluate current trends and probable can generate unintended environmental and ecological conse- future outcomes of any conflict, adaptation or mitigation quences (Paterson et al., 2008). Adaptation can result in purposeful actions. responses or spontaneous adaptations to shifts in environmental Rates of change can be highly variable and are essential infor- conditions, which can differ from policy. Smithers and Smith (1997) mation that managers need to maintain over the system they 2374 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388

are watching. The kind of managerial response to slow or fast rely on the findings of macroscopic and/or microscopic charcoal in changes as part of mitigation action may be very different and recent sediments and in older sedimentary rocks (Scott, 2000; may determine the success of a given conservation strategy. Whitlock and Larsen, 2001). Fires appear in the geological record Natural disturbance is an integral part of ecosystems with in the Devonian (onset at 416 million years ago or Ma). The absence human assets and livelihoods and are important to consider. of both humans and fire-prone plant species provides an excellent Natural disturbances plus anthropic initiatives may precipitate opportunity to address the relationship between fire and envi- threshold dynamics of the ecosystem to be preserved. Adap- ronmental parameters. In these conditions, atmospheric O2 tation strategies should take this synergy into account when concentration (O2 hereafter) has been proposed as the main forcing trying to accommodate the new climate or climate derived factor promoting fire, even on a priori non-flammable biological situation. material. Combustion occurs when O2 is over 13%, and variations in History of landscape use and human disturbance legacies may O2 levels correlate with fire activity throughout Earth’s history be important elements in shaping the current composition and (Scott, 2000). For instance, the Carboniferous (359.2e303.4 Ma) structure of a particular ecosystem in such a way that the links was modelled as the period of highest O2 (Berner and Canfield, between biotic assemblages and abiotic settings are not 1989), and many studies have shown extensive Carboniferous straightforward, thereby complicating the development of charcoal deposits throughout the Earth, interpreted as the product conservation actions. of major and extensive wildfires (Scott, 2000)(Fig. 3). Subsequently, an interval of lower fire incidence followed until the early Creta- 7. Past fire records ceous (onset at 145.5 Ma), when an increase in fire events coincided with a new increase in O2. In the CretaceouseTertiary boundary (K/ Fire is a natural and/or anthropic element present in all vege- T, at 65.5 Ma), consistent evidence for a global fire event, as would tated lands. The main drivers of fire are the following: 1) the be expected by the meteorite impact hypothesis (Alvarez et al., environment, mainly temperature, precipitation and the balance of 1980), is lacking, and fire records at that time have been inter- atmospheric gas concentrations; 2) the flammability of fuels, preted as the result of normal fire regimes or fires of regional mainly vegetation; 3) the existence of ignition sources; and 4) character (Scott, 2000). For the purposes of the present review, the human activities (Flannigan et al., 2009; Whitlock et al., 2010). focus will be on the Quaternary, especially the last glacial cycle, Understanding the complex mechanisms involved in fire ecology is when modern ecosystems were shaped with the help of anthropic not an easy task because internal and external variables act in fires. a complex and non-linear fashion, resulting in synergies and The YD reversal has already been discussed as an example of positive feedbacks that lead to unexpected results (Bowman et al., rapid climatic change between 13 and 11.5 cal ky BP and as 2009; Krawchuk et al., 2009). For example, vegetation flammability a potential historical model for present and future climatic shifts. increases in dry climates because of a decrease in internal water The YD reversal also provides examples of increased fire incidence content and the common occurrence and increased concentration and their natural or anthropic nature. For example, Marlon et al. of flammable metabolites, which may lead to fire events of unex- (2009) have reviewed the patterns of fire incidence and biomass pected virulence. This is the case of the so-called pyrophilous burning during the YD in North America and have shown an vegetation types, common in Mediterranean ecosystems, where increasing trend at both the onset and the end of this interval, with fire is considered an important part of their ecological dynamics the last one being the more intense. The authors favoured a climatic (Carrión et al., 2010). Bond et al. (2005) proposed that fire has been origin for both, although they did not neglect other direct (delib- and is currently a major factor in the worldwide biome distribution. erate or accidental burning) and indirect causes linked to the arrival For example, it has been suggested that, in the absence of fires, and dispersion of human populations after crossing the Bering cloud forests would double their global cover, mostly at the passage, such as the increase in flammable vegetation cover expense of ecosystems dominated by C4 grasses, as is the case in because of the decrease of herbivores, attributable to the well- most tropical savannas (Bond et al., 2005). Non-linear responses documented megafaunal extinction prior to the YD. According to and spatially heterogeneous fire patterns should be considered to Marlon et al. (2009), the main climatic drivers of YD fires would predict future ecological scenarios (Cochrane and Barber, 2009; have been the increase in average temperatures recorded since the Flannigan et al., 2009; Krawchuk et al., 2009). In this sense, posi- onset of the Bølling-Allerød interstadial, which began approxi- tive feedback between climate and vegetation, non-homogeneous mately 14.7 cal kyr BP, just before the YD, and the abrupt warming effects of global warming on the different climatic regions, and local peculiarities in the hydrological balance have been considered the most relevant factors for more accurate predictions (Hoffmann et al., 2002; Cardoso et al., 2003). Fire has been a significant driver of ecological changes in the biosphere through its history, especially during the last millennia, when the human impact on ecosystems increased dramatically. It has also been predicted that fire will be a crucial factor in the near- future because of the ongoing global warming, especially in those regions where the hydrological balance (precipitation/evapotranspiration 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 becomes more puzzling over the last w20,000 years, when human societies have become outstanding factors in burning. In this sense, important challenges include the identification of the potential causes for past fires (i.e., natural or anthropic) and the potential influence of fi environmental conditions on re occurrence, both directly and Fig. 3. Estimated atmospheric oxygen levels over the last 600 Ma; adapted from indirectly, by modifying human behaviour. Past fire records mostly Berner and Canfield (1989), and Scott (2000). T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2375 at the YD/Holocene transition, which has been considered a past since the LGM. Using this database, Power et al. (2008) have analogue for ongoing global warming. This climatic hypothesis has observed that fire activity has varied globally and continuously since also been supported by other studies worldwide (e.g., Haberle and the LGM in response to long-term changes in global climate and Ledru, 2001; van der Hammen and Van Geel, 2008). Moreover, short-term regional changes in climate, vegetation, and human land Daniau et al. (2010) observed that, during the last glaciation, fire use. Fire frequency has been continuously increasing since the LGM regimes varied synchronously with millennial-scale climate until the present, with a significant increase in spatial heterogeneity changes associated with DansgaardeOeschger (D/O) events, which beginning around 12 cal kyr BP. The hope is that this database will are part of the above-discussed 1500-year Bond cyclicity. According contribute to a better understanding of fire patterns at global, to the same authors, fire incidence increased during D/O warmings regional and local scales to optimise conservation practices. and decreased during rapid coolings, thus supporting the climatic hypothesis. The defenders of this hypothesis argue that, globally, 8. Neotropical examples climate has been the major control on fire regimes, even during the last two millennia, despite the dramatic increase in human pop- The Neotropics is a key region from a conservation perspective ulation and the associated disturbances resulting from land use. because of its amazing biodiversity and endemism patterns and the They also argue that anthropic fires became more important after occurrence of extensive rainforests, some of which are in nearly AD 1870 (Marlon et al., 2008). This contrasts with the proposal that, pristine states; the Neotropics contain several conservation hot- in the tropics, historical fire incidence has been regulated mainly by spots (Myers, 2001; Huber and Foster, 2003). This region is less well human activities and climateehuman synergisms (Power et al., known than the northern temperate areas from a palaeoecological 2008). For example, ENSO variability coupled with human migra- point of view, but several studies are available showing its suit- tions and settlement shifts have been proposed as the main drivers ability to provide case studies with conservation significance and for neotropical fire regimes since the mid-Holocene (Meggers, highlighting the need for further studies (e.g., Bush, 1996, 2002; 1994; Uhl, 1998); However, now, and likely in the near-future, Bush and Silman, 2007; Mayle et al., 2007; Figueroa-Rangel et al., anthropic fires dominate the scene (Cochrane and Barber, 2009). 2010; McKey et al., 2010). The examples provided here have been Fires of human origin have also been proposed as important in the selected from our own research in northern South America. Neotropics during the Lateglacial, including the YD interval, and the Holocene (Bush et al., 2007; Rull, 2009b). As noted above, at 8.1. The YD coolingewarming shift in the northern Andes: biotic a global scale, human fires would have been responsible for the responses earlier increase in atmospheric CO2 concentration and the onset of the Anthropocene in the early Holocene (Ruddimann, 2003, 2007). As stated above, the rapid warming initiated at the end of the YD The importance of Quaternary charcoal records as proxies for is a potential analogy for the predicted future global warming, and past fires and the associated changes in vegetation composition, its study may help forecast near-future biotic responses and facil- diversity or local extinctions has been widely recognised (Whitlock itate the adoption of conservation policies. The occurrence of the and Larsen, 2001). These palaeorecords can be used not only to YD cooling in the Neotropical region has been debated for decades. observe how past fires have disturbed the vegetation but also Several palaeoecological records favoured its existence, whereas as modelling inputs to derive realistic scenarios of future others did not (Hansen, 1995; van der Hammen and Hooghiemstra, fireeclimateevegetationehuman relationships for management 1995; Rull et al., 2010a). Some records reported a cooling around purposes. Whitlock et al. (2010) show the complexity of under- the YD dates, but the dating was not good enough to provide the standing fire behaviour at different levels and the need to incor- necessary bracketing for accurate correlations (van’t Veer et al., porate long-term studies to obtain a more accurate view of fire 2000; Mahaney et al., 2008). The first clear record was obtained events as a part of Earth-system dynamics. According to these in the Cariaco Basin (Fig. 4), where both palaeoclimatic recon- authors, the following important points should be considered in struction and dating supported a cool and dry event coinciding the study of past fires: 1) fire regimes operate at different spatial with the YD (Haug et al., 2001; Lea et al., 2003). On the continent, and temporal scales, with distinct drivers at each scale; 2) clima- the first undisputed YD equivalent has been found recently in the teefire, fuelefire, and humanefire relationships also act at different sediments of a high-altitude Andean lagoon (Los Anteojos) after scales; 3) there is a huge impact from human practices where a multi-proxy study. Sedimentological and geochemical indicators climate and fuel are not limiting factors, such as occurs in extreme documented a sudden cooling and a glacier advance initiated at conditions like desserts (no fuel) or rainforests (no favourable 12.85 cal ky BP, with a maximum of around 3 C below present climate for ignition); and 4) the “fire regime” concept should be average temperatures at 12.65 cal ky BP, followed by a rapid revised. The current definition of fire regime only considers short- warming initiated at 12.3 cal ky BP, which ended near the term studies that are unable to capture the full range of fire vari- YDeHolocene boundary. As in Cariaco, the Anteojos cooling was ability in many ecosystems. Whitlock et al. (2010) have introduced also characterised by dry climates (Stansell et al., 2010). the “super-fire regime” concept to better address the characteristic The response of vegetation to the cooling was heterogeneous, nature of fire within a biome by taking into account all the forcing where the more sensitive taxa were Podocarpus (a genus of trees factors involved, including humans at the appropriate temporal living at the upper altitudinal forest levels), Polylepis sericea (a tree scales. This concept, with an important palaeoecological compo- that forms almost monospecific stands above the upper forest line, nent, is more powerful to anticipate future variability within or UFL, within the “páramo” open vegetation), Huperzia (a genus of a given biome because it considers long-term ecosystem behaviour ferns typical of humid “páramos”), and Isoëtes (an aquatic pteri- and humans as part of ecosystems and “climate changers” dophyte growing submerged in shallow waters, including lake (Whitlock et al., 2010). shores) (Fig. 5). Other taxa that responded to the cooling were the As an effort to manage the available information on fire families Asteraceae and Poaceae, but the homogeneous pollen palaeorecords, the Global Palaeofire Working Group (GPWG) morphology of their genera and species prevented the necessary was established to follow the rules of the IGBP Fast Track taxonomic resolution to analyse their detailed responses to climate Initiative on Fire (http://www.gpwg.org). The open-access Global shifts. However, these families characterise the open “páramo” Charcoal Database (http://www.ncdc.noaa.gov/palaeo/impd/gcd. vegetation in the northern Andes and increased during the cooling, html), created in 2003, gathers the available fire palaeorecords which indicates an increase in this vegetation type. All the sensitive 2376 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388

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 tabular mountains 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. genera and species mentioned reacted to the Anteojos cooling by the different individual requirements of each taxon. It is also decreasing their percentages, but the most sensitive taxa were notable that sensitive taxa showed immediate responses to both Polylepis and Isoëtes, with pollen and spores that disappeared from the cooling and the subsequent warming, without any time lag at the sediments during the maximum cooling and did not re-appear the resolution of the study, which is decadal to centennial (Fig. 6). until the onset of the warming that initiated at 12.3 cal BP. This was This indicates that these taxa not only are the more sensitive but interpreted as a downslope migration of the sensitive taxa and also react quickly to climate shifts, even the rapid ones. Conse- a decrease in lake levels because of cool and dry climates (Rull et al., quently, they would be useful to monitor the biotic responses to 2010b). ongoing warming to prognosticate the expected biotic changes in Among the trees from the upper forest levels recorded through the near-future. It is known that high-altitude biomes are highly palynological analysis (including other well known indicators of sensitive to climate changes and are therefore preferred environ- this vegetation type, such as Alnus, Hedyosmum and Weinmannia), ments for global change studies (Ives, 1999). Also, the Andean only Podocarpus has reacted to the YD climate shifts. This indicates forests are known to be among the more biodiverse ecosystems on that the taxonomic composition of these forests changed because of the planet, holding outstanding hotspots for conservation (Myers, T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2377

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 to the YD, was deﬁned according to independent sedimentary and geochemical proxies. The left column is the summary of all pollen taxa subdivided into three categories representing forest 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).

2001). Therefore, the information obtained in the Anteojos case normally forested Guayana landscape. These savannas form large study on the biotic responses of high-altitude ecosystems to rapid extensions of treeless grasslands and are intermingled in some warming should be considered for management purposes. places with forests and shrublands, developing typical forest- savanna mosaics (Huber, 1994a). The GS is the homeland of the 8.2. Fire, climate change, and savanna expansion in the Gran Pemón indigenous group, from the Carib-speaking family. It has Sabana (Guayana region) been postulated that this culture reached the GS relatively recently, or approximately 300 years ago (Thomas, 1982; Colson, 1985), but The Gran Sabana (GS) is a vast region of approximately some archaeological evidence may suggest an earlier human 18,000 km2 located in SE Venezuela, between the Orinoco and the occupation beginning in the early Holocene (Gassón, 2002). A Amazon Basins. The GS is a huge island of savannas within the deﬁnitive assessment on the age of human settlements in the GS is

Fig. 6. Correlations of the Pollen Index (PI) and the Polylepis curves with selected physico-chemical palaeoclimatic proxies measured in the same core and referential palaeoclimatic reconstructions containing the YD event (Cariaco and GISP). The PI was calculated as the ratio between sensitive taxa: ( Podocarpus þ Polylepis þ Huperzia)/(Asteraceae þ Poaceae). Gray bands represent the stadials based on the GISP isotopic curve. The glacier advance defined by Stansell et al. (2010) in the Anteojos core is indicated by a box around the MS and Ti curves. Note the parallelism among the curves of physico-chemical proxies for climate change, and the PI, and especially, the rapid response of Polylepis to environmental shifts; Redrawn from Rull et al. (2010b). 2378 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 not yet possible. Fire is an important component of the Pemón replacement of either forests or shrublands by savannas during the culture. They use it every day to burn great expanses of savannas Lateglacial and the early Holocene, thus bringing into question the and occasionally forests (Fig. 7). However, the high fire incidence of climatic proposal. In the Mapaurí locality, a mountain cloud forest between 5000 and 10,000 observed fires per year (Huber, 1995; dominated the landscape until approximately 10.2 cal ky BP, when Leal, 2010) contrasts with the nearly inexistent agriculture or it was replaced by a treeless savanna (Rull, 2007a)(Fig. 8). In the cattle e raising practices typical of other cultures strongly linked to Lake Chonita catchment, the Lateglacial was characterised by fire. In the Pemón culture, fire practices are initiated for various a shrubland with no modern analogues, which persisted during the reasons, such as for hunting, shifting agriculture, fire prevention, entire YD and was substituted with a treeless savanna in the communication, savanna cleaning, firewood drying, aesthetics, and YDeHolocene transition (Montoya et al., 2011)(Fig. 9). In both magic (Kingsbury, 2001; Rodríguez, 2004, 2007). cases, the treeless savannas persist until today. These biotic shifts The GS is also important from an economic point of view coincided with the late YDeearly Holocene global warming because it lies on the headwaters of the Caroní River, which is the (Kaufman et al., 2004; Kaplan and Wolfe, 2006) and were locally main provider of hydroelectrical power for the country (Castro and characterised by a decrease in the hydrological balance. In the case Gorzula,1986). The organisation in charge of the exploitation of this of Lake Chonita, the disappearance of the shrubland coincided with energy (EDELCA) has developed a conservation program for the a charcoal peak, indicating a sudden increase of fire incidence Caroní River Basin that includes the control of fire in the headwa- (Montoya et al., 2011). In Mapaurí, local forests appeared slightly ters to protect its ecosystems (Castro and Gorzula, 1986). In addi- after the vegetation replacement, when the savannas were already tion, the GS is part of several national and international official established, but regional forests were already increasing during the protection areas, such as national parks, biosphere reserves and vegetation replacement (Rull, 2009b). Therefore, a synergistic world heritage sites (Huber, 1995, http://whc.unesco.org/en/list/ effect between climate and fire seems to have been the driver of the 701). Despite this, only about 13% of fires lighted by the Pemón establishment of present-day savannas in these areas. The origin of are controlled and extinguished (Sletto, 2008; Bilbao et al., 2010). these fires (natural or anthropic) is still unknown, but their This low success is due to the large extension of the GS, the high temporal patterns and intensity are very similar to recent records of number of daily fires compared to the available prevention and anthropic fires. In addition, it has been proposed that the consistent extinction resources, and the unpredictability of fire locations occurrence of high charcoal concentrations is a strong indicator of (Rodríguez, 2007; Bilbao et al., 2010). There is a vivid debate human presence, even in the absence of other obvious evidence of between EDELCA and several local ecologists, on one hand, and the land use (as is the case of the GS) (Bush et al., 2007). Therefore, Pemón and their defenders, on the other, about fire dynamics in the a Lateglacial to early Holocene establishment of human populations GS. The first defend the current protection rules and the ecological using fire cannot be dismissed, though more clear evidence is still knowledge, whereas the second argue in favour of the indigenous needed (Montoya et al., 2011). traditional practices, in which fire is an essential element (Rull, 2009a). A subjacent question in this debate concerns the origin of the GS savannas, given their isolated nature among the extensive Guayana and Amazon rainforests, in a climate more favourable for forest formations. It has been postulated that the open vegetation type of the GS may be due either to the action of anthropic fires or to palaeoclimatic and edaphic factors (Fölster, 1986; Fölster and Dezzeo, 1994; Huber, 2006). Palaeoecological records can help to address these problems by providing additional tools for conservation purposes. The proposal of the climatic hypothesis predated the palaeoecological study of the region and was based on palaeoclimatic and biogeographic assumptions. According to this hypothesis, the GS is a relic of the former extension of savannas that dominated the Neotropics during the LGM because of the prevalence of drier climates (Eden, 1974). Recent palaeoecological studies have documented the

Fig. 8. Summary percentage pollen diagram and charcoal concentration for the Holocene recorded from the Mapaurí peat bog sediments (Gran Sabana). The forest assemblage at the base of the diagram is dominated by Catostemma pollen, whereas most of the pollen of herbaceous plants corresponds to Poaceae. Charcoal particles were classified into two categories: small (<100 mm), as a proxy for regional fires, and large (>100 mm), as a proxy for local fires (Rull, 1999). Note the good temporal match between forest reduction and savanna establishment and charcoal increase; Modified Fig. 7. Savanna fires in the Gran Sabana near Stanta Elena de Uairén (Photo: V. Rull). from Rull (2009b). T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2379

Fig. 9. Summary percentage pollen diagram and charcoal concentration for the Lateglacial recorded from the Lake Chonita sediments (Gran Sabana). Charcoal I corresponds to small charcoal 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 the coincidence between the establishment of treeless savannas at the expense of the YD shrublands and the dramatic ﬁre increase; Modiﬁed from Montoya et al. (2011).

The GS forests and shrublands did not recover, resulting in modern GS inhabitants with common burning practices (Montoya, a clearance that remains today. This is true even in the absence of 2011)(Figs. 11 and 12). further increases in fire intensity, as is shown in the palae- In summary, fire and its synergies with climate are largely oecological record of Laguna Encantada covering the last 7500 responsible for the present-day GS landscape. Palaeoecological years (Montoya et al., 2009). According to present-day ecological reconstructions reveal a progressive forest clearance and savanna studies, the burning of GS forests triggered an irreversible degra- expansion since the YD, mainly because of the low resilience of GS dational sequence leading to the establishment of savannas, and forest recovery was prevented by edaphic impoverishment, both in nutrients and water retention capacity (Fölster, 1986, 1992; Fölster and Dezzeo, 1994). This low forest resilience is supported by the Urué record, through the palaeoecological reconstruction of a secondary succession after a fire event that eradicated the forest from the site. The detailed record of the last millennium showed a degradational sequence from the original forests to open secondary forests of different composition, followed by shrublands, fern communities and, finally, treeless savanna, in the absence of further local fires (Rull, 1999). There were also increases in the moisture balance in the last centuries that were not followed 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 GS lakes during the last two millennia (Rull, 1992). In all cases, the Mauritia arrival and expansion coincided with a remarkable charcoal increase, which likely represents the establishment of Fig. 10. Morichal (Mauritia flexuosa) stands around Lake Encantada (Photo: V. Rull). 2380 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388

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

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

8.3. Biotic responses to environmental change in the Guayana Highlands’ undisturbed ecosystems Fig. 11. Summary percentage pollen diagram and charcoal concentration for the last millennia recorded from Lake Chonita sediments (Gran Sabana). Note the coincidence The Guayana Highlands (GH) are an assemblage of more or less fi between the sudden appearance and increase of Mauritia pollen and the onset of re flat summits of the quartzite/sandstone table mountains, locally incidence, interpreted as the establishment of the present-day indigenous culture. “ ” Modified from Montoya (2011). called tepuis , located in the neotropical Guayana region of northern South America (Figs. 13 and 14). From a biogeographic point of view, the GH summits above 1500 m (which are the forests, which were unable to recover after fire, even under highest) constitute a biogeographic province called Pantepui favourable climatic conditions. Forest clearance has accelerated (Huber, 1987, 1994b). The tepui summits can reach extensions up to during the last two millennia because of an intensification of about 1000 km2 and altitudes up to 3000 m, and they contain human-driven fire incidence. Therefore, it could be predicted that amazing levels of diversity and endemism, as manifested in the savanna expansion at the expense of forest and shrub formations approximately 2500 known species of vascular plants, of which will continue in the GS if the current fire management continues. almost 30% are Pantepui endemics and around 25% are local Fire extinction practices are not a solution because of their above- endemics or restricted to one single mountain (Berry et al., 1995; mentioned low efficiency. Forest conservation should focus on Berry and Riina, 2005). The Pantepui biomes have lasted in an preventive rather than corrective policies; however, the deep almost-pristine state of conservation because of their remoteness rooting of fire practices in the Pemón culture is a handicap. At and inaccessibility and, probably more importantly, the lack of natural resources to exploit (Huber, 1995). This makes them unique environments to record natural climatic variability and the corresponding ecosystem responses (Rull, 2007b, 2010c). The GH have

Fig. 12. Fires affecting a morichal community near Santa Elena de Uairén. Note that Mauritia ﬂexuosa palms are not burnt because of the rapidity in which ﬁre propagates through herbs (Photo: V. Rull). Fig. 14. General view of the Ilú-Tramen tepuian massif (Photo: V. Rull). T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2381 been free from direct human disturbances, such as mining for gold Pantepui taxa prevent an inference of their potential response to and diamonds, logging and burning, shifting cultivation, population this warming acceleration, but similar rates have been measured pressure, and tourism, which are common in the surrounding for recent upward migrations forced by the ongoing global warm- lowlands and midlands (Huber, 1995). However, one of the main ing in other mountain regions (e.g., Kelly and Goulden, 2008; Lenoir concerns for Pantepui biota is the potential effect of the ongoing et al., 2008). To test the ability of Pantepui species to migrate at global warming if the IPCC predictions for this century are accurate similar rates in response to global warming, a comparison of the (Rull and Vegas-Vilarrúbia, 2006). Recent studies suggest that, present-day situation with historical botanical records is needed under this scenario, a drastic reduction in the available habitat for (Rull et al., 2009). summit taxa because of warming-driven upward migration would The available palaeoecological information for the tepui result in the extinction by habitat loss of around 80% of the Pan- summits refers mainly to the Holocene. Most records proceed from tepui species (Rull et al., 2009, Nogué et al., 2009a). the Chimantá tepuian massif, except for two from the Guaiquinima Palaeoecological records may help to evaluate the reliability and massif. In the Chimantá massif, three tepuis (Acopán, Amurí and the eventual impact of such estimates by comparing them with the Toronó) showed an outstanding vegetation constancy over the last natural upward migration rates since the LGM. Based on two 6000 years, with only minor local reorganisations between Steg- sequences from the lowlands and midlands around the Guayana olepis meadows and Bonnetia gallery forests, which is likely due to Highlands, it has been estimated that natural rates of temperature lateral migration of water currents along the extensive alluvial increase since the LGM have been approximately 0.025 C/century, plains (Rull, 2005a). In the Eruoda-tepui, of the same massif, which corresponds to upward shifts of around 5 m/century (Bush vegetation constancy was also the norm during the Holocene et al., 2004; Rull, 2007a). The estimated rates for the projected (Nogué et al., 2009b)(Fig. 15). However, a gentle vegetation shift at global warming of the 21st century in northern South America are approximately 100e200 m elevation has been linked to an upward 3 C/century (Solomon et al., 2007), which is equivalent to an displacement of the altitudinal ecotone between the Stegolepis upward migration of approximately 500 m/century (Rull and meadows and the Chimantaea shrublands in the Churí-tepui, Vegas-Vilarrúbia, 2006; Nogué et al., 2009a). Therefore, global approximately 2.5 cal ky BP (Rull, 2004a,b,c)(Fig. 16). The Guai- warming rates would be 100 times the natural rates for Pantepui quinima records showed successive replacements of three vege- species. Unfortunately, the lack of autoecological studies for the tation types e Stegolepis meadows, Archytaea gallery forests and

Fig. 15. Percentage pollen diagram from the summit of the Eruoda-tepui, in the Chimantá massif. Note the constancy of the pollen assemblages throughout the whole diagram during the Holocene; Modiﬁed from Nogué et al. (2009b). 2382 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388

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

9. Conclusions

Palaeoecological knowledge provides valuable clues to understand biotic responses to natural and human disturbances, as well as the synergies between them, and is a necessary input for nature conservation because it furnishes essential tools to anticipate potential biological consequences of ongoing global change, thereby contributing to better conservation policies. From the above literature review on the subject, the following lessons have Fig. 16. Summary percentage pollen diagram from the summit of the Churí-tepui been highlighted: (Chimantá massif). Assemblage A is dominated by Stegolepis (S) and corresponds to the herbaceous meadows typical of this massif. Assemblage B is dominated by Chimantaea fi (Ch), an endemic genus of the Chimantá and a few adjacent tepuis, and represents the The signi cance of palaeocological studies for nature conser- unique shrublands of the Chimantá. The upper altitudinal limit of Stegolepis is around vation issues could be considered a manifestation of the 2300 m, whereas the Chimantaea shrublands grow above this elevation. The vegetation importance of past records for the elucidation of long-term shift before 1450 cal yr BP was interpreted as an upslope biotic migration, likely ecological processes, which are difficult to resolve with only because of a gentle warming; Redrawn from Rull (2004a). neoecological surveys that only cover several decades. Indeed, processes such as ecological succession, secular migration, upland forests-during the last 8 cal ky BP, which were attributed to extinction, adaptation, and microevolution may take centuries moisture changes, probably of regional extent (Rull, 2005b). Based or even millennia to occur, depending on the duration of the on these tepuian records, palaeoecological and palaeoclimatic lifecycle of the involved species. Therefore, predictions about correlations have been elusive, and the norm seems to be an potential biological consequences of near-future environ- extended biotic constancy spiked with local ecological rearrange- mental changes rely on an appropriate knowledge of biotic ments or a spatial heterogeneity in the responses to minor responses to past, secular to millennial, environmental temperature and moisture changes experienced during the Holo- changes, which are only available from palaeoecological cene (Rull, 2010c). Another factor to be considered is the sensitivity records. of the studied sites to climatic changes and variations. For example, The available palaeoecological knowledge shows that potential the Churí site, the only one in which an altitudinal ecological shift biotic responses to environmental changes transcend the has been recorded, is in a key ecotone. Other Chimantá localites, framework of neoecological studies. For example, the old notably Acopán, Amurí amd Toronó, are near the middle of the ecological debate about individual or collective responses to meadows’ altitudinal range, where a small climatic oscillation is not environmental disturbances has been recently resolved in enough to determine a significant vegetation change. favour of the first option in the context of palaeoecological The observed spatial heterogeneity of vegetation responses to records. An interesting consequence is the possibility of new Holocene climatic changes in the tepuian summits prevents any unknown species combinations with no modern analogues generalisation and complicates forecasts relating to global warm- resulting from future environmental shifts. Past records have ing. On the one hand, local moisture changes seem to have been the already shown similar situations and provided useful decisive factor for biotic change, except for Churí, where a slight analogues for hypothesis testing about potential future temperature shift seems to have played a role in vegetation scenarios. replacement. This complicates the predictions of future responses Acclimation and/or adaptation, with the first relying on of Pantepui biota to global warming and suggests that forecasting phenotypic plasticity and the second involving genetic changes based only on temperature changes may overestimate the magni- of potential evolutionary significance, have been proposed as tude of projected extinctions by habitat loss. In addition, the two possible reactions to future global warming and as alter- potential existence of microsites with suitable environmental natives to extinction by habitat loss. Genetic adaptation seems conditions for the persistence of the potentially threatened species to be an unlikely option given the short temporal frame would relax environmental stresses and favour the survival of involved. However, palaeoecological and molecular phyloge- a number of theoretically endangered species. Indeed, the potential netic studies would support the possibility of rapid evolu- occurrence of glacial and late-glacial microrefugia was first tionary changes resulting from the existence of pre-adapted proposed for the tepuian summits (Rull et al., 1988; Rull, 2009c). genomes that would eventually be successful under the new In summary, modelling based on present-day biogeographical predicted climatic conditions. patterns, physiography and an average IPCC scenario for the 21st In the context of the palaeoecological data available so far, the century suggest catastrophic extinctions by habitat loss in the response of organisms and communities to future global Pantepui vascular flora, which involves the extinction of a signifi- warming is not expected to be homogeneous but rather highly cant number of endemic species; however, palaeoecological dependent on local and regional environmental conditions. records provide a more optimistic view, suggesting the possibility This highlights the importance of conducting micro- and meso- of survival for a number of species because of their ecological scale surveys that consider local particularities for conservation tolerance and/or ability to thrive in microrefugia. In the first case, planning. only ex situ conservation strategies (botanical gardens, seed and Current predictions of species extinction by habitat loss would germoplasm banks, etc.) would be able to guarantee species’ overestimate these risks and should be revised because they conservation, whereas in the second, in situ practices would rarely consider the possibility of survival within small local T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388 2383

microsites with favourable conditions (microrefugia) for the between palaeoecology and anthropology may furnish the involved species. Past records suggest that microrefugia would necessary information to establish causal links, not only on the have been decisive for the preservation of particular genetic influence of climate changes in human activities but also on combinations during significant environmental changes, such how the resulting changes in human practices may in turn as the Pleistocene glaciations, and contribute to an under- affect the environment and ecological function. This, together standing of the present-day genetic structure of species and with a sound knowledge of where and how sensitive ecosys- their populations. To properly revise the existing extinction tems develop, would greatly improve forecasting and antici- forecasts, models using spatial grids as small as possible are pation skills when confronted with current climate change. recommended to capture local topographical and microcli- Mismanagement of natural resources combined with vulner- matic conditions as potential future microrefugia. From this able social organisation seem to have played a key role in perspective, and accounting for the palaeoecological back- precipitating the collapse of complex past civilisations under ground, some authors propose that spatial reorganisations climatic stress. Present drawbacks, such as the exponential without extinction will be the dominant biotic response to the growth of human population under a globalised economy near-future global changes. based on market rules and consumerism, promote social Predictions about future biotic responses to future changes injustice and cause the overexploitation of natural resources, commonly rely on an implicitly assumed equilibrium between the uncontrolled increase of greenhouse gas emissions, and organisms, their communities, and the environment. However, other environmental damages. Using historical examples as palaeoecological records show that biotic reactions would be analogues would illustrate the structural weaknesses of much more complex because of the non-linearity of the modern societies, leading to the inability to appropriately cope ecological processes involved, which would lead to unexpected with current and future climate change. The non-linearity of biotic responses through enhanced feedback. The more ecological processes would be an additional handicap to common mechanism for the occurrence of these “surprises” is successfully adapt to or mitigate these unprecedented trans- the existence of inherent biotic thresholds that, once sur- formations of Earth’s climate. Indeed, negative synergisms passed, may lead to different potential stable states of the would cause the appearance of new threshold triggers, affected ecosystems. Environmental changes need not be promoting chronic stresses, which may result in the appear- necessarily abrupt to produce threshold responses; even subtle ance of new disturbances and the elimination of others. The and gradual shifts may determine ecological surprises. It is also timely recognition of such situations is crucial for ecosystem possible that ecosystems never attain equilibrium, and tran- management and conservation policies. sient states perpetuate because of the recurrent action of The correct assumptions of threshold conservation models will environmental change. strongly rely on knowledge about key indicator parameters and The resilience of an ecosystem, or its capacity to absorb their spatial and temporal patterns of change. Ecological disturbances with no significant changes, is a critical feature in monitoring and surveys spanning weeks to decades are able to the biotic response to environmental reorganisations. Past provide relevant indicator variables and threshold patterns. records provide examples of the type and magnitude of However, as noted above, many ecological processes occur over external drivers needed to modify significant ecosystem timescales that exceed the so-called long-term observational properties and determine threshold responses. One of the main ecological datasets. Real long-term ecological knowledge needs lessons from this is that ecosystems may express their resil- long-term biodiversity baselines and paleoecological data, ience when confronted with environmental shifts by attaining which are crucial for testing predictions about ecosystems several possible equilibrium states, as manifested in changes in thresholds and resilience. Paleoecological records may help biodiversity and/or composition, without losing their ecolog- answer key questions about the threshold dynamics of ical functions. Palaeoecological reconstructions also show that ecosystems, such as the following: What is the capacity for such ecological changes are often irreversible (hysteresis). rebuilding an ecosystem? Have there been several stable states Palaeoecology is able to provide past analogues for projected over time? What is the biotic capacity of a given ecosystem to global warming and the corresponding biotic responses, which cope with disturbance triggers? Are there particularly resilient is of high relevance for delineating successful conservation species? Which situations have increased the vulnerability of policies. The global warming recorded at the end of the a system in the past, favouring a change of state? Can transient Younger Dryas (ca 13.0 to 11.5 kyr BP) emerges as one of the states be recognised? Where and when are thresholds more more powerful of these analogues because both magnitude and frequent? rates of change parallel those predicted for the present century. One of the main drivers of ecological change introduced by We should also note that the main biotic response to this humans has been fire incidence, through increases in both palaeoclimatical event seems to have consisted of ecological frequency and intensity. The occurrence of wildfires has been reorganisations and changes in community composition extensively documented through the history of the biosphere because of differential species migration patterns and rates. So before humans and has been related to the flammability of far, it has not been possible to associate large-scale extinctions vegetation, which is dependent on the O2 atmospheric to the YD climatic reversal. High-resolution studies of the YD concentration, climate, internal water content and the accu- would be decisive, not only to improve our knowledge on biotic mulation of flammable compounds. Fire has been considered responses of present-day species to climate shifts but also an important factor for the distribution of vegetation because, because it would provide the necessary link between paleo- in the absence of burning, forests would double their present ecology and modern observations. global cover at the expense of open vegetation dominated by Throughout history, humans have not always been aware of grasses. ongoing climate changes. Gradual shifts have occurred imper- Fire incidence has increased and coincided with the rise of ceptibly but have promoted profound and irreversible cultural human populations and their geographical dispersal, especially changes, whereas abrupt changes have prompted adaptation or from approximately 20,000 years ago. Fire events recorded mitigation responses. In both cases, new environmental during the last glaciation seem to have been synchronous with changes and problems have emerged. A suitable collaboration millennial-scale warmings associated with D/O events, thus 2384 T. Vegas-Vilarrúbia et al. / Quaternary Science Reviews 30 (2011) 2361e2388

suggesting that climate shifts have favoured their occurrence. Acknowledgements The same is true for the YD, when an increase in fire incidence has been documented, especially during the YDeHolocene The authors would like to thank the QSR Editorial Office for the global warming. Since that time, the causes of fires docu- invitation to write this review. Funding has been provided by the mented in the palaeoecological records e either natural or Banco de Bilbao Vizcaya Argentaria Foundation (FBBVA, project anthropic e are difficult to ascertain, but there is a general BIOCON-08-031), the Spanish Ministry of Science and Innovation consensus that human activities have been the main drivers of (MICINN, project CGL2009-07069/BOS), and the Higher Council for fire during the last millennia, especially since the 19th century. Scientific Research (CSIC, project 200830I258). We acknowledge Another important element to consider is the occurrence and Simon Connor for his help regarding the human impact bibliography. suitability of the available fuel (mostly vegetation). Synergistic effects among climate, human activities and fuel characteristics References have also been considered decisive factors because of the occurrence of positive feedbacks. Alberini, A., Chiabaib, A., Muehlenbachsa, L., 2006. Using expert judgment to assess The neotropical case studies presented here emphasise the adaptive capacity to climate change: evidence from a conjoint choice survey. importance of concentrating efforts on the YD shift and the Global Environmental Change 16, 123e144. Albright, R., Mason, B., Miller, M., Langdon, C., 2010. Ocean acidification compro- associated biotic responses as an analogue for ongoing global mises recruitment success of the threatened Caribbean coral Acropora palmata. warming, the potential role of fire in the development of Proceedings of the National Academy of Sciences USA 107, 20400e20404. present-day neotropical landscapes, the spatial heterogeneity Allen, J.R.M., Brandt, U., Brauer, A., Hubberten, H.-W., Huntley, B., Kellerk, J., Kramlk, M., Mackensen, A., Mingra, J., Negendank, J.F.W., Nowaczyk, N.R., of biotic responses to climate changes, and the need for Oberhänsli, H., Watts, W.A., Wulf, S., Zolitschka, B., 2000. Rapid environmental revising current habitat loss estimates as a consequence of changes in southern Europe during the last glacial period. Nature 400, 740e743. global warming predicted for the 21st century. Another inter- Alley, R.B., 2000. 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