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Resurrection ecology and global climate change research in freshwater ecosystems Author(s): David G. Angeler Source: Journal of the North American Benthological Society, 26(1):12-22. 2007. Published By: The Society for Freshwater Science DOI: http://dx.doi.org/10.1899/0887-3593(2007)26[12:REAGCC]2.0.CO;2 URL: http://www.bioone.org/doi/full/10.1899/0887-3593%282007%2926%5B12%3AREAGCC %5D2.0.CO%3B2 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. J. N. Am. Benthol. Soc., 2007, 26(1):12–22 Ó 2007 by The North American Benthological Society PERSPECTIVES This section of the journal is for the expression of new ideas, points of view, and comments on topics of interest to benthologists. The editorial board invites new and original papers as well as comments on items already published in J-NABS. Format and style may be less formal than conventional research papers; massive data sets are not appropriate. Speculation is welcome if it is likely to stimulate worthwhile discussion. Alternative points of view should be instructive rather than merely contradictory or argumentative. All submissions will receive the usual reviews and editorial assessments. Resurrection ecology and global climate change research in freshwater ecosystems David G. Angeler1 Institute of Environmental Sciences (ICAM), University of Castilla–La Mancha, Avda. Carlos III s/n, E-45071 Toledo, Spain Abstract. The complex effects of global climate change on freshwater ecosystems limit our ability to predict biological responses in a standard way and may compromise ecosystem management with respect to potential changes. I present a theoretical framework that shows the usefulness of resurrection ecology for standardizing cross-system comparisons of ecological responses to global climate change. Resurrection ecology makes use of plant seed and animal resting-egg (propagule) banks that integrate past environmental histories in the gene pools of their organisms. Resurrected organisms that have undergone different periods of dormancy can be studied comparatively using evolutionary/genetic and experimental approaches. Both approaches combined can provide insights into how the dimensions of species’ ecological niches have shifted over time and could help reveal whether direct effects of climate change (increased temperatures and CO2 concentrations and hydrological alterations) or other anthropogenic stressors (e.g., contamination, landuse change) have caused microevolution. Insights gained from resurrection ecology could be used to manage gene flow between populations and to help prevent extinctions of threatened populations. These insights could be used to help manage ecosystem structure and function and maintain ecological sustainability. However, our ability to apply results from resurrection ecology to organisms that do not have long-term dormancy stages in their life cycles may be limited, and the usefulness of resurrection ecology will have to be evaluated along gradients of hydroperiod and flood frequency, which may determine rates of microevolution in aquatic ecosystems. Key words: anthropogenic stress, contemporary evolution, dormancy, seed and resting egg banks, paleolimnology. ‘‘The contribution of climate change to future extinctions depends on how quickly species can respond to change.’’ McCarty (2001) (life-cycle events triggered by environmental cues), geographic range, and physiology have been attributed to climate change. Worst-case scenarios depict increasing rates of extinction and loss of biodiversity resulting from physiological stress, interactions with invading species, habitat loss, and habitat conversion (Vitousek 1994, Hughes 2000, Root et al. 2003, Thomas et al. 2004). The strong consensus in the scientific community is that freshwater ecosystems are particularly vulnerable to projected climate changes (Carpenter et al. 1992, The hypothesis that the Earth currently is undergoing anthropogenic global climate change has accumulated considerable supporting evidence. Global climate change already is generating ecological responses (reviewed by Hughes 2000, McCarty 2001, Walther et al. 2002, Parmesan and Yohe 2003). Shifts in phenology 1 E-mail address: [email protected] 12 2007] GLOBAL CLIMATE CHANGE Firth and Fisher 1992, Magnuson et al. 1997, Lake et al. 2000, Lodge 2001, McCarthy et al. 2001, Schindler 2001, Poff et al. 2002, Alvarez-Cobelas et al. 2005a). Aquatic systems are generally resilient to short- and long-term anthropogenic disturbances, but the pace of climate change is probably too rapid to allow many aquatic organisms to adapt to future environmental conditions. Many species are thought to be at risk because their ability to adapt through natural selection is limited and because anthropogenic alteration of the environment reduces the dispersal and migration potential of organisms, thereby limiting their ability to find suitable habitat (Poff et al. 2002). Moreover, the synchronization between life-cycle events and seasonal changes in habitats may be disrupted (Winder and Schindler 2004, Harper and Peckarsky 2006), limiting the ability of organisms to reproduce. Cumulative effects and complex interactions of climate-driven environmental changes (chiefly alterations of natural hydrological cycles) and other anthropogenic disturbances (e.g., contamination, habitat fragmentation, introductions of exotic species) limit our ability to forecast with certainty how aquatic ecosystems and their biota will change in response to novel environmental conditions (e.g., Dale 1997, Magnuson et al. 1997, Schindler 2001), thereby leading to ecological surprises (Paine et al. 1998). This problem limits our ability to manage aquatic ecosystems in a way that will be sustainable and will conserve ecosystems services for human populations that are projected to increase over the next several decades (Magnuson et al. 1997, IPCC 2001). Mechanistic relationships between environmental changes and biological responses must be understood if we are to adopt sound mitigation and conservation strategies in the future. I provide a theoretical framework that shows how resurrection ecology (Kerfoot et al. 1999) could be used to predict evolutionary responses of organisms to environmental changes caused by global warming. Resurrection ecology has the potential to enable us to determine whether higher temperatures, higher CO2 concentrations, and hydrological alterations (direct effects of climate change) or other anthropogenic stressors (contamination, exotic species, landuse change) could exert strong selection pressure on biota in aquatic ecosystems. Comparisons of results obtained from local studies of lake and wetland sediments could enable freshwater ecologists to assess the consistency of evolutionary responses across regional and climatic domains. Remedial actions intended to mitigate the impacts of global climate change could include artificial management of gene flow between isolated populations that have different abilities to adapt to environmental change (as AND RESURRECTION ECOLOGY 13 revealed by resurrection ecology), which could help counteract effects that might lead to extinction. Back to the Future: What Can We Learn from Past Adaptations to Rapid Climatic Change? The Pleistocene–Holocene Transition ‘‘Paleolimnological reconstructions . . . can provide evidence of the past environmental and climatic conditions that impacted [aquatic] communities.’’ Porinchu et al. (2003) Current rates of global warming are unprecedented based on the last 10,000 y of paleoclimatological evidence. Global mean surface temperature increased by ;0.68C during the 20th century, and modeling approaches using different CO2 emission scenarios suggest that temperature will increase another 1.4 to 5.88C by 2100 (IPCC 2001), depending on the willingness of humans to reduce current CO2 emissions. Independent of which scenario will have happened in 100 y, managing ecosystems to guarantee sustainability will be challenging. Paleoclimatologists advocate learning from the past to estimate future shifts in ecological systems related to the projected range of temperature increases. We can use the paleoecological record to trace other relatively abrupt changes in Earth’s climate history and determine biological responses to those events. Those records might enable us to generalize about the rate and degree of biological adaptation to global warming (but see Ammann et al. 2000 for methodological difficulties). The abrupt change in climate between the Pleistocene and the Holocene is an instructive example. According to paleoclimatological data (e.g., Brauer et al. 1999), temperatures (derived from O2 isotopic concentrations) appear to have increased ;78C (Johnsen et al. 1992, Alley et al. 1993) in ;50 y during the transition from the Younger Dryas cold period to the Preboreal warm period ;11,600 calibrated y (paleoclimatological reconstructions calibrated to calendar years) ago. Reconstructions of terrestrial habitats using remains of plants (summary in Hoek 2001) and beetles (Atkinson et al. 1987) and aquatic studies using remains of chironomids (Ammann et al. 2000, Porinchu et al. 2003, Massaferro et al. 2005), cladocerans (Ammann et al. 2000), algae, or plant seeds (Brauer et al. 1999) suggest that many ecosystems responded very quickly to the transition. Many systems showed no lag or responded in ,20 y, whereas other systems had slower response times (hundreds of years). However, most of the biological shifts must be understood as catastrophic collapses of ecosystem structure or as switches between different stable states. Only a few systems showed gradual biological change in response 14 D. G. ANGELER to abrupt warming. Abrupt shifts in community structure probably disrupted functional interactions among species and destabilized ecosystems (Ammann et al. 2000). Paleoecological evidence also suggests that the biological changes varied from site to site and were influenced by local and regional environmental characteristics. Hoek (2001) suggested that the magnitude of responses to temperature change might also have been strongly influenced by nonclimatic variables including migration lags, edaphic characteristics, landscape settings, dryness, and windiness. Global Climate Change in Freshwater Ecosystems: Projected Impacts and Biological Responses ‘‘Investigations into climate change have begun to highlight the importance of strongly nonlinear, complex, and discontinuous responses.’’ Schneider and Sarukhan (2001) Examples from the Pleistocene–Holocene transition show that biological responses to climate change were highly variable, even within similar ecosystem types. Highly variable responses also are expected as a result of present-day anthropogenic interference with the climate, despite differences in the spatiotemporal pattern (abrupt in the past vs creeping in the present) and nature (shifting from cold to warm in the past vs warm to warmer in the present/future) of the 2 transitions. Moreover, humans have inflicted other forms of stress that were not a factor for ecosystems in the past and that will make the biological responses of freshwater ecosystems to climate change even more complex and unpredictable (IPCC 2001). Many modeling studies indicate that slight increases in temperature will have profound effects on the amount and frequency of precipitation and that these effects will alter runoff patterns and hydrological functioning of aquatic ecosystems (IPCC 2001, Poff et al. 2002). A detailed review of these effects is beyond the scope of my paper, but the hydrological alterations (precipitation patterns, evapotranspiration, hydroperiods, flood frequency, lake mixis, etc.) may vary strongly between different regions and climatic domains (IPCC 2001, Poff et al. 2002). Anthropogenic stressors will continue to degrade aquatic ecosystems through unsustainable land uses (e.g., habitat fragmentation, contamination) and other practices that alter hydrology (e.g., overexploitation of ground water, dam construction). New combinations of anthropogenic stress and climate change will affect ecosystems at the local scale, and these combinations could be more deleterious than the effects arising from climate change alone (Przeslawski et al. 2005, Xenopoulos et al. 2005, Franco et al. 2006). These effects [Volume 26 will depend on local, regional, and climatic conditions and will affect ecological responses across the biological hierarchy from organisms to communities (Fig. 1). Several mechanisms are thought to influence responses of aquatic organisms to climate change and other anthropogenic stressors (Fig. 2). Migration and dispersal are likely to be especially important because climate change will pose significant challenges to aquatic organisms seeking suitable new habitat (e.g., Poff et al. 2002). Natural genetic adaptation also is likely to be a key mechanism because organisms may be able to adapt rapidly to environmental change through contemporary evolution (i.e., adaptation occurring within time periods of years and decades; reviewed by Ashley et al. 2003, Stockwell et al. 2003). The potential for rapid adaptation to climate change is encouraging because reduced gene flow between populations caused by habitat destruction and fragmentation may force populations to rely more on genetic adaptation than on migration/dispersal to new habitats (Etterson and Shaw 2001). Contemporary evolution in plants and animals has occurred in response to a wide range of anthropogenic disturbances, including exotic species introduction, contamination, and overharvesting (Thompson 1998, Ashley et al. 2003, Stockwell et al. 2003). Most of our understanding of rapid evolutionary responses to climatic change relates to adaptation to temperature at the molecular level for some cellular processes (Clarke 2003). How these molecular adaptations to changes in temperature will be reflected in organism performance and fitness and how these adaptations will affect population, community, and ecosystem processes are not well understood (Clarke 2003). A few recent studies have shed light on how ecological systems may adapt evolutionarily to climate change. Studies of evolutionary responses of model organisms (e.g., Drosophila, Arabidopsis) to increases in temperature or CO2 over multiple generations in the laboratory (e.g., Cavichi et al. 1995, Ward and Kelly 2004) indicate that adaptation to selective agents can be rapid (Ward et al. 2000). Rates of natural genetic change in annual plants (Etterson and Shaw 2001), Drosophila (Rodrı́guez-Trelles and Rodrı́guez 1998, Levitan 2003, Levitan and Etges 2005), other dipterans (Bradshaw and Holzapfel 2001), or mammals (Berteaux et al. 2004) have been measured in field studies. A detailed review of these studies is beyond the scope of my paper, but the available evidence highlights several important features: 1. As in the Pleistocene–Holocene transition, biological responses may be complex, hierarchical, and multivariate, making generalizations across ecological 2007] GLOBAL CLIMATE CHANGE AND RESURRECTION ECOLOGY 15 FIG. 1. Conceptual model summarizing impacts in freshwater ecosystems that will arise as a result of disruption of natural hydrological functioning mediated by global climate change and other anthropogenic stressors as influenced by local, regional, and biome characteristics. systems difficult. The type of response will vary among populations and communities depending on dispersal strategies and natural (latitudinal and altitudinal boundaries) and anthropogenic constraints (e.g., dams, land use) on dispersal, migration, and natural selection (Fig. 2). The type of response and the constraints on dispersal will affect population genetics, source–sink dynamics, metapopulations and metacommunities, and other community-structuring concepts. 2. Adaptation to climate change is taxon and context specific and difficult to predict (Holt 1990, Gomulkiewicz and Holt 1995, Grant and Grant 1995, Abrams 1996, Stockwell et al. 2003). Some species may adapt to change, but with negative consequences. For example, microevolutionary changes could result in depauperate genomes and loss of fitness at the population level (Rodrı́guez-Trelles and Rodrı́guez 1998, Stockwell et al. 2003), leading to reduced evolutionary potential because of reduced gene flow or genetic drift. In other cases, rates of adaptive evolution may be unable to keep pace with the predicted rate of climate change (Etterson and Shaw 2001). 3. Our inability to assess mutation rates in relation to climate change (a technical limitation) will influence our ability to measure the degree to which natural selection will determine responses to climate change (Fig. 2; Berteaux et al. 2004). 4. Methods problems associated with field studies limit our ability to attribute observed changes unambiguously to global warming. Variables other than climate can easily confound the effects of climate change (Hughes 2000). The degree of certainty with which we can predict how biological systems in nature will respond directly or indirectly to climate change depends on how well we 16 D. G. ANGELER [Volume 26 FIG. 2. Conceptual model showing biological responses to global climate change across different spatial scales and the potential uses of resurrection ecology for assessing those responses. The model emphasizes contemporary evolution and adaptation to novel ecosystem characteristics that may arise from complex biotic and abiotic changes across different spatial scales. can integrate disturbance histories, biological interactions, and evolution in experiments. I provide arguments below that will show the usefulness of resurrection ecology for this task. Finding the Cause of Change: The Potential of Resurrection Ecology ‘‘Lake sediments store genotypes and species from the past and so can provide insight into the rates and trajectories of past ecological and evolutionary changes.’’ Hairston and Kearns (2002) The complex impact–response patterns caused by global climate change in aquatic ecosystems limit our understanding of biological responses to climate change. However, this knowledge will be essential for deriving sound management options in the future. Determining the forces that drive natural selection in ecosystems in response to change could be especially helpful. However, Conner (2003) pointed out the difficulty of assigning specific causes of natural selection in the wild. These difficulties arise because the present-day adaptations of many organisms cannot be attributed unambiguously to one or more selective forces acting within the multidimensional selection regimes in nature. Our inability to benchmark autecological traits of present-day organisms against those of their evolutionary ancestors further complicates the issue. Resurrection ecology has strong potential to overcome these limitations. Resurrection ecology is based on the notion that plant seed and animal resting-egg (propagule) banks are spatiotemporal integrators of genetic-, phenotypic-, species-, and community-level variation, which can serve as important biodiversity surrogates in aquatic ecosystems. Traditionally, the record of organism remains in the propagule bank has been used descriptively to reconstruct paleoenvironments and 2007] GLOBAL CLIMATE CHANGE historical environmental changes. However, propagule banks contain resting stages that can remain viable for decades to centuries (Hairston et al. 1995). Therefore, resurrection of organisms that have been dormant for known lengths of time, extraction and analysis of their DNA, and comparisons of autecological traits along different niche axes offer great promise for experimental determination of microevolution. This combination of paleoecological, genetic, and experimental disciplines has given rise to the promising research area of resurrection ecology (Kerfoot et al. 1999). The techniques have been used successfully with Daphnia to assess evolutionary responses to metal contamination (Kerfoot et al. 1999), morphological (Kerfoot and Weider 2004) and phototactic behavioral responses to predation (Cousyn et al. 2001), and responses to toxic cyanobacteria during eutrophication (Hairston et al. 1999, 2001). When, Where, and How Will Resurrection Ecology Work in Climate-Change Research? Constraints on resurrection ecology Life-history traits.—Use of resurrection ecology is limited to organisms that remain dormant in sediments for long periods, e.g., protists (Fryxell 1983, McQuoid et al. 2002) and microinvertebrates (Hairston et al. 1995, Belk 1998, Thorp and Covich 2001). Macrophytes (Baskin and Baskin 1998) and many aquatic insects (Williams 2006) also have dormant stages (e.g., seeds, turions, eggs, and pupae) in their life cycles. However, we do not know how long many of the species in these groups can survive in resting stages, rendering the application of resurrection ecology to them uncertain. Many other important biota in aquatic ecosystems (reptiles, amphibians, birds, and fish) do not produce long-lived resting stages, and resurrection ecology cannot be applied to these groups (Fig. 3A). Abiotic.—Propagule banks are present in many types of aquatic ecosystems, including lakes of all depths, permanent and temporary ponds, riverine floodplains, swamps, and coastal marshes. Riverine floodplains are integral parts of many fluvial systems. If the signatures of anthropogenic stress in fluvial systems can be read in floodplain propagule banks, resurrection ecology may offer the potential for determining responses to climate change in fluvial systems as well as in lentic systems. Thus, resurrection ecology could provide useful and easily standardized tools for making crosssystem comparisons of evolutionary change and could be useful for comparing responses to environmental stress across regions and climatic domains. However, potential abiotic constraints to contempo- AND RESURRECTION ECOLOGY 17 rary evolution must be considered if we are to evaluate further the usefulness of resurrection ecology for crosssystem comparisons. Organisms must be able to undergo full life cycles constantly for microevolution to take place. Thus, the ability to respond evolutionarily to environmental change is expected to diminish along gradients of habitat permanence and flood frequency (Fig. 3B). The prerequisite of constant reproduction is met in permanently flooded systems such as lakes (left end of the gradient in Fig. 3B). However, climate change could outpace the rate of adaptive genetic responses in ephemeral wetlands that flood only sporadically on a temporal scale of decades (right end of the gradient in Fig. 3B). In such habitats, resurrection ecology is unlikely to be useful for detecting evolutionary responses to change. Temporary wetlands have been traditional choices for conversion to agricultural use, a practice that will pose an increased threat as global climate changes push aquatic ecosystems toward shorter hydroperiods and reduced flood frequencies (Alvarez-Cobelas et al. 2005b). Once the structure of the propagule bank is destroyed by agricultural practices, potential responses to environmental change can no longer be studied using resurrection ecology. Moreover, some evidence suggests that disruption of natural hydroperiods and flood frequencies can degrade propagule banks over time (M. Brock, University of New England, Armidale, Australia, personal communication). This evidence suggests that propagule banks can deteriorate to a point that could reduce the usefulness of resurrection ecology unless adaptive management helps to counteract excessive ecological degradation (Hulme 2005). Because resurrection ecology can be applied only to a limited set of organisms in specific kinds of environments, the inferences that can be drawn from resurrection studies may be limited. For example, many aquatic vertebrates have longer life spans and generation times than organisms with long-term dormancy stages in their life cycles. Therefore, evolutionary responses of aquatic vertebrates to environmental stress could be decoupled from the responses of organisms banked in lake and wetland sediments, i.e., genetic adaptation to stress is expected to be slower in many vertebrates than in most invertebrates. As a further example, inferring ecosystem responses (arguably the sum of responses of all biotic [benthic and pelagic] constituents of the system) directly from the responses of a small subset of taxa with specific life-history traits will be problematic. Nevertheless, the responses of propagules banked in wetland and lake sediments may be useful surrogates for ecosystem responses to global climate change (Fig. 3C), and resurrection ecology offers a number of 18 D. G. ANGELER [Volume 26 FIG. 3. Conceptual model showing the influences of life-history traits of organisms (A) and hydrological characteristics of aquatic ecosystems (B) on potential uses of resurrection ecology and the potential contributions of resurrection ecology to global climate change research (C). The dotted lines indicate speculative applications of resurrection ecology. important advantages over conventional methods of investigating responses to environmental change (Table 1). Advantages Rapid response times.—Many of the organisms banked in the sediments of aquatic ecosystems grow quickly and have short generation times, so their evolutionary responses to environmental change should be detectable within years or decades (Kerfoot et al. 1999, Hairston et al. 1999, 2001, Cousyn et al. 2001, Kerfoot and Weider 2004), and trends in responses could be identified relatively quickly. The impacts of future climate change will depend on the specific combination of direct effects of climate change and other anthropogenic stressors imposed on an ecosystem (Fig. 1). Organism responses to these specific combinations should be registered over time in the genotypes stored in the historical archives of the propagule banks, and this biological memory could help us to determine the specific forces driving natural selection. More specifically, propagule banks of aquatic ecosystems could act as useful indicators of Red Queen dynamics (the idea from Alice in Wonderland that organisms must run just to remain in place; Van Valen 1973) and help to GLOBAL CLIMATE CHANGE 2007] TABLE 1. AND RESURRECTION ECOLOGY 19 Advantages and limitations of resurrection ecology in global climate change research. Advantage Allows cross-system comparisons in ecosystems that contain propagule banks Serves as a standardized indicator for environmental change across local, regional, and biome scales Probably could be used to manage gene flow between populations and to help prevent extinction Could help inform management of ecosystem services Integrates paleoecological, evolutionary/genetic, and experimental disciplines, allowing straightforward determination of ecological responses determine the impacts in aquatic ecosystems to which organisms must adapt evolutionarily. Potential for experimental manipulation.—Autecological studies of organisms obtained from past and contemporary resting eggs are probably the most powerful tools for identifying evolutionary responses to climate change. Manipulations of present-day and past niche dimensions could be useful for determining evolutionary responses of organisms to direct or indirect effects of climate change (Fig. 2). Specifically designed manipulative experiments could be used to address questions such as: 1) Do species in natural environments adapt to higher temperatures or CO2 levels? 2) Do species evolve to cope with the hydrological alterations of the ecosystems they inhabit? 3) How will species respond to anthropogenic stressors such as introduced species, contamination, or change in land uses? 4) Will species have evolutionary priorities if different stressors act in concert, i.e., will evolutionary responses to subtle and slower changes in temperature be similar to their responses to other anthropogenic and more-incisive perturbations? 5) If yes, will these priorities be the same across ecosystems, regions, and climatic domains? Additional paleolimnological studies based on radiometric dating, pollen, diatoms, and invertebrate remains could provide information on the nature and magnitude of environmental change that have acted on genotypes. Resurrection Ecology: Managing Gene Flow and Mitigating Impacts of Climate Change ‘‘We may not be able to prevent accidents, but we may be able to diminish their impact.’’ Rosenzweig (1995) A long history of ecological experimentation and theory supports the hypothesis that ecosystem goods and services and the ecosystem properties from which they are derived depend on biodiversity (Hooper et al. 2005). The available evidence suggests that biodiversity will decrease because of the interactive effects of Limitation Gradients of hydroperiod and flood frequency could affect the rate of contemporary evolution Limited to organisms that have long-term dormancy stages in their life cycles (not applicable to many aquatic vertebrates) Probably high budgetary and personnel demands climate change and other disturbances (Thomas et al. 2004, Lovejoy and Hannah 2005). Decreased biodiversity, in turn, will affect ecosystem services (Metzger et al. 2005, Schröter et al. 2005) and could compromise human welfare. Resurrection ecology has the potential to be an indicator of possible organismal responses to climate change and other anthropogenic stressors across ecosystem types. However, its contributions to climate-change research could go beyond simple detection of evolutionary responses to mitigation of the effects of global climate change through artificial management of gene flow between populations (Fig. 3C). Research related to natural genetic selection and artificial management of gene flow in natural systems (Conner 2003, Stockwell et al. 2003) is still preliminary. Thus, the ideas presented here must be considered speculative (reflected by the dotted arrows in Fig. 3C). However, results obtained from resurrection ecology studies of the rates and magnitudes of evolutionary responses to selection forces have some potential to inform artificial management of gene flow between populations. If we were able to manage gene flow among populations with different degrees of evolutionary adaptation to the selective forces accompanying climate change, we could help increase evolutionary potential, help species resist environmental change, and reduce the risk of extinction. Of course, artificial management of gene flow within the context of the results of resurrection ecology studies would be limited to species with long-term dormancy in their life cycles. Nevertheless, if the goal of artificial management of gene flow were to help preserve the ability of ecosystems to provide ecosystem services, resurrection ecology could target those services that are provided directly by organisms with long-term dormancy as a life-history trait. Application of resurrection ecology to the management of services that are provided by the sum of aquatic biota is less straightforward. 20 D. G. ANGELER Global Climate Change Research and Resurrection Ecology: A Synthesis The nonlinear, complex, and discontinuous nature of global climate change and biological response patterns limits our understanding of how ecosystems will change under projected climate-change scenarios and how these changes will be distributed across geographical regions and biomes. This lack of knowledge currently limits our ability to manage ecosystems and implement strategies that could help mitigate the effects of global climate change. The strongest application of resurrection ecology lies in the use of comparative studies of propagule banks that can be standardized across systems at local, regional, and biome scales. Resurrection ecology also has some potential to provide useful insights into ways to manage gene flow between populations to help counteract factors that might lead to extinction. However, the use of resurrection ecology is inherently limited to organisms with long-term dormancy in their life cycles, so that results obtained from resurrection ecology probably cannot be applied to other aquatic biota (chiefly vertebrates). Thus, resurrection ecology is less likely to be helpful in efforts to determine ecosystem responses to global climate change or to manage ecosystem services derived from the sum of all biotic constituents of aquatic ecosystems. Given that future scenarios of the effects of global climate change are pessimistic regarding loss of biodiversity and sustainability of ecosystem services, politicians, scientists, and managers should exploit every tool available that could help conserve our environment (Osmond et al. 2004). Resurrection ecology could be very useful for some of these tasks. Acknowledgements The input of 2 anonymous referees, W. H. Clements, and P. Silver helped to strengthen the message of this research and is gratefully acknowledged. Financial support was provided by EU and JCCM/FEDER research grants (EVG1-2002-00019 and PAI-05-020). This paper is dedicated to the memory of my grandfather, Joseph Camilleri (1920–2005). Literature Cited ABRAMS, P. A. 1996. Evolution and the consequences of species introductions and deletions. Ecology 77:1321– 1328. ALLEY, R., D. A. MEESE, C. A. SHUMAN, A. J. GOW, K. C. TAYLOR, P. M. GROOTES, J. W. C. WHITE, M. RAM, E. D. WADDINGTON, P. A. MAYEWSKI, AND G. A. ZIELINSKI. 1993. Abrupt increase in Greenland snow accumulation at the end of the Younger Dryas event. Nature 362:527–529. [Volume 26 ALVAREZ-COBELAS, M., J. CATALAN, AND D. GARCÍA DE JALÓN. 2005a. Impacts on inland aquatic ecosystems. Pages 113– 146 in J. M. Moreno (editor). 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