- Email: [email protected]
Climate–vegetation dynamics in the fast lane
Update
TRENDS in Ecology and Evolution
equilibrium, small amplitude cycles, or large amplitude cycles that closely approach zero were all possible outcomes for a predator– prey community in a chemostat (L.E. Jones et al., unpublished). Using this result, we predict that the variance of a population in simple communities will itself become smaller as genetic diversity in the prey increases (i.e. the variance of the coefficient of variation will decrease) (Figure 1b). For this reason, communities with low prey genetic diversity will exhibit extreme cycles more frequently than will communities with high prey genetic diversity. Future directions Recent theoretical and empirical research on the biology of predator–prey interactions shows the clear benefit of combining ecology and evolution under the single umbrella of community genetics [14,21]. Within this emerging field, the time is ripe to test questions extending on the work of Yoshida and colleagues. Does coevolution occur on the same time scale as predator–prey cycles, where cycles and evolution in the prey are accompanied by rapid evolution in the offensive traits of the predator [22]? Can the addition of species in the simple two-species community lead to diffuse coevolution [23]? Does increased intraspecific diversity beget ecological stability in ways that are similar to interspecific diversity? Such questions can be challenging to test in natural communities, although their importance is clear. Shertzer et al. [7] and Yoshida et al. [8] have taken a leap forward in our understanding of the ecological consequences of evolutionary processes. Acknowledgements We are grateful for comments and suggestions from P. Abrams, C. Brassil, S. Ellner, W. Godsoe, N. Hairston Jr, L. Jones, K. Shertzer, A. Sih, D. Viswanathan, T. Whitham and T. Yoshida. Our research (http://www. herbivory.com) is funded by grants from the Natural Sciences and Engineering Research Council of Canada to M.T.J.J. and A.A.A., and a Sigma Xi GIAR to M.T.J.J.
References 1 Ehrlich, P.R. and Raven, P.H. (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586– 608
Vol.18 No.11 November 2003
551
2 Ford, E.B. (1949) Mendelism and Evolution, Methuen and Co 3 Pimentel, D. (1961) Animal population regulation by the genetic feedback mechanism. Am. Nat. 95, 65 – 79 4 Rosenzweig, M.L. and MacArthur, R.H. (1963) Graphical representation and stability conditions of predator– prey interactions. Am. Nat. 97, 209 – 223 5 Abrams, P.A. (2000) The evolution of predator– prey interactions: theory and evidence. Annu. Rev. Ecol. Syst. 31, 79 – 105 6 Abrams, P.A. and Matsuda, H. (1997) Prey adaptation as a cause of predator– prey cycles. Evolution 51, 1742 – 1750 7 Shertzer, K.W. et al. (2002) Predator– prey cycles in an aquatic microcosm: testing hypotheses of mechanism. J. Anim. Ecol. 71, 802 – 815 8 Yoshida, T. et al. (2003) Rapid evolution drives ecological dynamics in a predator– prey system. Nature 424, 303 – 306 9 Borass, M.E. (1983) Population dynamics of food-limited rotifers in two-stage chemostat culture. Limnol. Oceanogr. 28, 548– 563 10 Halbach, U. (1970) Influence of temperature on the population dynamics of the rotifer Brachionus calyciflorus. Oecologia 12, 176 – 205 11 Fussmann, G.F. et al. (2000) Crossing the Hopf bifurcation in a live predator– prey system. Science 290, 1358 – 1360 12 Thompson, J.N. (1998) Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329 – 332 13 Fussmann, G.F. et al. (2003) Evolution as a critical component of plankton dynamics. Proc. R. Soc. Lond. Ser. B 270, 1015– 1022 14 Antonovics, J. (1992) Toward community genetics. In Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics (Fritz, R.S. and Simms, E.L., eds), pp. 426 – 449, University of Chicago Press 15 Whitham, T.G. et al. (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84, 559 – 573 16 Whitham, T.G. et al. (1999) Plant hybrid zones affect biodiversity: tools for a genetic based understanding of community structure. Ecology 80, 416– 428 17 Dungey, H.S. et al. (2000) Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54, 1938– 1946 18 Neuhauser, C. et al. (2003) Community genetics: expanding the synthesis of ecology and genetics. Ecology 84, 545 – 558 19 Loreau, M. et al. (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804 – 808 20 Elton, C.S. (1958) The Ecology of Invasions, Methuen and Co 21 Agrawal, A. (2003) Community genetics: new insights into community ecology by integrating population genetics. Ecology 84, 543– 544 22 Karban, R. and Agrawal, A.A. (2002) Herbivore offense. Annu. Rev. Ecol. Syst. 33, 641 – 664 23 Janzen, D.H. (1980) When is it coevolution? Evolution 34, 611 – 612 0169-5347/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2003.09.001
Climate– vegetation dynamics in the fast lane Eric Post Department of Biology, The Pennsylvania State University, 208 Mueller Lab, University Park, PA 16802 USA
Evidence from paleoclimatological research indicates that major climatic changes, such as the rapid increase in temperatures at the end of the Younger Dryas event , 11 000 years ago, can occur over the span of a few decades. Vegetation response to climatic variation and change, is, by contrast, often assumed to occur gradually over much longer timescales. Two recent papers confirm earlier, theoretical predictions that changes in species Corresponding author: Eric Post ([email protected]). http://tree.trends.com
composition of plant communities following climatic shifts can, however, occur with striking rapidity. The predominance of large mammalian grazers at high latitudes during the Pleistocene hints at a vegetation composition that is very different from the chemically defended trees and shrubs that are characteristic of the Arctic and sub-Arctic today [1]. Although the demise in the far north of horses, camels, wooly rhinos, steppe bison and wooly mammoths has been ascribed to many factors, including human exploitation, disease, interspecific
552
Update
TRENDS in Ecology and Evolution
competition and direct adverse effects of climatic change during the Pleistocene–Holocene transition, one hypothesis holds that these specialist grazers saw the disappearance of their foraging niches as the arid steppe was replaced by tundra, boreal forest and muskeg in response to increasing temperatures and precipitation [2]. Efforts to predict responses of extant species to current and future climatic warming can draw clues from the faunal turnovers and redistributions that occurred during the Pleistocene–Holocene transition ,11 000 years ago. Indeed, great strides have been made in monitoring and modeling the geographical range shifts of some animals in response to observed or projected spatial shifts in habitatand plant-community composition associated with climatic warming [3]. Yet, to better understand why some animal species went extinct the last time the Earth warmed up, and why some species, and which species, are likely to go extinct during this episode of rapid warming, we might need to understand just how rapidly plant-community composition can change. Two recent papers [4,5] provide evidence of an intermediate temporal scale of plant-community response to climatic change that is strikingly rapid on a geological timescale and not so out of reach of ecological timescales. Using lacustrine records from multiple sites throughout the North Atlantic region, Williams et al. [4] documented vegetation changes that, in many cases occurred ,100 years after the climatic shift associated with the Younger Dryas event (Box 1). Yu [5] examined pollen- and plant-macrofossil data, together with oxygen isotopic data on climatic variation, from two sites in southern Ontario, Canada, and reported evidence for the immediate replacement of periglacial desert by willow–juniper tundra following glacial retreat, and of replacement of spruce forest by pine by ,100 years after the onset of Holocene warming. These observations reveal the rapidity of vegetation response at the community level to the major climatic shifts that occurred at the Pleistocene–Holocene transition, which, in some cases, occurred as abruptly as, or even more suddenly than, those that are predicted to occur over the next century [6]. In so doing, the authors reveal a response of plant communities to climate change that is of an intermediate temporal scale, more gradual than the immediate phenological response of many species to recent warming [7], but as fast as or faster than the responses predicted by stochastic forest gap models [8] and predictions based on climate projections [9]. Of equal importance, perhaps, is that plant-community shifts in response to climatic fluctuation of the order of decades [4],
Vol.18 No.11 November 2003
coupled with the possibility of rapid extinction of plant species [10], might pose consequences for the persistence of animal species, because they respond both directly to climatic changes and indirectly to lagged, climate-induced changes in vegetation [11]. The strength of the study by Williams et al. [4] is their incorporation of quantitative time-series analysis of data from areas of varying topographical relief. They assembled records from 11 lake cores on both sides of the North Atlantic, with resolutions ranging from 16–93 years. Although, to a certain extent, the temporal resolution of the data will constrain the minimum observable lag in the response to climatic fluctuation, these data are of fairly high and consistent temporal resolution among samples. The lake records used by Williams et al. [4] contained proxies for both vegetation composition (pollen) and past climate (d18O and chironomid assemblages), and these time-series were compared using cross-correlation analysis. Remarkably, the median of the most highly significant cross-correlations among sites indicated a vegetation response time of 60 years, whereas, among all significant cross-correlations, the median lag occurred at 90 years. On a geological timescale, this is less than the blink of an eye, whilst, in an ecological perspective, such responses represent no more than a couple of population cycles for large herbivores [12] and many arboreal taxa. In contrast to Williams et al. [4], Yu [5] examined both pollen and plant macrofossil stratigraphic data from two proximal sites in southern Ontario, Canada, to reconstruct the late Quaternary vegetation history of the Niagara Escarpment. Importantly for this study, the Niagara Escarpment was only recently deglaciated, ,13 000 years before present (Bp). Hence, Yu’s cores, one of which penetrated to bedrock, and one of which penetrated to outwash gravel, facilitated an analysis of periglacial vegetation colonization and succession following retreat of the ice at the onset of the Holocene. Treeless boreal vegetation, a mix of Alnus– Dryas –Cyperaceae tundra, was evident initially after the retreat of the ice sheets, and dominated from ,12 000– 13 000 years Bp. Interestingly, the subsequent shift from treeless tundra to spruce forest might have been rapid and perhaps facilitated by migration from nearby refugia, because Picea glauca cones from proximate sites were dated to 12 320 ^ 360 years Bp [13]. Yu’s [5] detailed ordination analysis comparing the results of multivariate analyses of pollen assemblages to independent
Box 1. What was the Younger Dryas event? The Pleistocene (, 1.8 million–11 000 years ago) was not an ice age; rather, it was a series of waxing and waning ice ages characterized by dramatic climate fluctuations across a broad range of temporal frequencies. As global temperatures increased near the end of the Pleistocene, and as the ice sheets that covered much of North America and Northern Europe began to enter their final stages of retreat, there was a sudden decline in temperatures detectable by climate proxies throughout the northern hemisphere at between , 11 500 and 13 000 years before present. This sudden cooling phase, which lasted , 1000 – 1300 years, is known as the Younger Dryas event [17]. Its termination marked the end of the last ice age and the transition from the Pleistocene to the Holocene, a period of much warmer and more stable climate. http://tree.trends.com
The abruptness with which the Younger Dryas ended, and with which northern hemisphere temperatures rose, is dramatic. Isotopic evidence from Greenland ice cores has been interpreted as indicating that temperatures increased by , 78C in the span of little more than ten years [18]. Although the causes of such abrupt climatic change as the Younger Dryas event remain disputed, one hypothesis maintains that cold water from the melting ice sheets entered the Gulf of Mexico, through the St Lawrence Seaway, the North Atlantic, temporarily impeding the northward flow of warm water from the southern Atlantic via the Gulf Stream. Regardless of the mechanisms involved, abrupt climatic changes have occurred often, and have probably had major ecological repercussions [19].
Update
TRENDS in Ecology and Evolution
proxies of climatic variation from the same sites inferred from d18O data reveal complex community responses to climatic fluctuations. For example, vegetation at one of Yu’s sites (Crawford Lake, Ontario) had begun to shift to spruce forest by ,500 years after the Bølling–Allerød warming phase (,12 700 years Bp). However, there was a rapid increase in herb pollen percentages at the onset of the Younger Dryas event that was indicative of differential responses among the arboreal and herbaceous components. With the onset of rapid warming at the termination of the Younger Dryas event, however, there is a dramatic change in vegetation that is evident from Yu’s data: spruce-dominated forests shifted to pine-dominated forests within a span of ,100 years or less, spurred by the onset of Holocene warming. Such variability in the rate and nature of vegetation responses to climatic events might reflect the importance of factors such as baseline climatic conditions at various sites, biological inertia in the process of succession, facilitation of invasion by some species through the earlier presence of nitrogen fixers, and the proximity of refugia from which species can migrate to recently exposed sites. This last factor might be of particular relevance to Yu’s results for post-glacial expansion of spruce, because independent plant macrofossil data indicate that spruce occurred at the very edge of the ice sheet during the Last Glacial Maximum, ,18 000 ^ 1500 years Bp [14], and spruce migration rates have been estimated to vary between 0.05 and . 1 km y21, with a median rate of 0.10 km y21 [15,16]. The importance of these two studies lies in their ability to put a finger on just how quickly plant communities appear to have responded, and might continue to respond, to climate change.The beauty ofthe approachestaken byWilliams etal. [4] and Yu [5] lies in the fact that, not only do they confirm earlier theoretical predictions of the potential rapidity with which plant community composition might respond to abrupt climate changes, but they also complement the many studies of both plant and animal response to climatic events, variability and change that focus on spatial fluxes (e.g. [3]). The information provided by this pair of new papers, and the others that they will no doubt spawn, will prove valuable in future efforts to model the responses of plant and animal species to predicted climate change. In particular, the quantitative insights provided by these papers might facilitate the mechanistic modeling of climate change-related geographical range shifts and community
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dynamics at higher trophic levels, including large herbivores that survived the Pleistocene–Holocene transition [11]. Acknowledgements I would like to thank David Post, Jack Williams and two anonymous referees for helpful comments and discussions that greatly improved this article.
References 1 Guthrie, R.D. (2000) Origin and causes of the mammoth steppe: a story of cloud cover, woolly mammal tooth pits, buckles, and inside-out Beringia. Quat. Sci. Rev. 20, 549 – 574 2 Guthrie, R.D. (1996) Four late Pleistocene large mammal localities in interior Alaska. In American Beginnings: The Prehistory and Palaeoecology of Beringia (West, F.H., ed.), pp. 119–129, University of Chicago Press 3 Parmesan, C. and Yohe, G. (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37 – 42 4 Williams, J.W. et al. (2002) Rapid and widespread vegetation response to past climate change in the North Atlantic region. Geology 30, 971–974 5 Yu, Z. (2003) Late Quaternary dynamics of tundra and forest vegetation in the southern Niagara Escarpment, Ontario. New Phytol. 157, 365–390 6 Alley, R.B. (2000) Ice-core evidence of abrupt climate changes. Proc. Natl. Acad. Sci. U. S. A. 97, 1331 – 1334 7 Walther, G-R. et al. (2002) Ecological responses to recent climate change. Nature 416, 389 – 395 8 Lischke, H. et al. (2002) Untangling a Holocene pollen record with forest model simulations and independent climate data. Ecol. Model. 150, 1–21 9 Overpeck, J.T. et al. (1991) Potential magnitude of future vegetation change in eastern North America: comparisons with the past. Science 254, 692–695 10 Jackson, S.T. and Weng, C. (1999) Late Quaternary extinction of a tree species in eastern North America. Proc. Natl. Acad. Sci. U. S. A. 96, 13847 – 13852 11 Schmitz, O.J. et al. Ecosystem responses to global climate change: moving beyond color mapping. Bioscience (in press) 12 Peterson, R.O. et al. (1984) Wolves, moose, and the allometry of population cycles. Science 224, 1350– 1352 13 Terasme, J. and Matthews, H.L. (1980) Late Wisconsin white spruce (Picea glauca (Moench) Voss) at Brampton, Ontario. Can. J. Earth Sci. 17, 1087–1095 14 Jackson, S.T. et al. (2000) Vegetation and environment in Eastern North America during the last glacial maximum. Quat. Sci. Rev. 19, 489–508 15 Clark, J.S. et al. (1998) Reid’s paradox of rapid plant migration: dispersal theory and interpretation of paleoecological records. Bioscience 48, 13 – 24 16 Ritchie, J.C. and MacDonald, G.M. (1986) The patterns of post-glacial spread of white spruce. J. Biogeog. 13, 527 – 540 17 Dansgaard, W. et al. (1989) The abrupt termination of the Younger Dryas climate event. Nature 339, 532 – 534 18 Alley, R.B. et al. (1993) Abrupt increase in Greenland snow accumulation at the end of the Younger Dryas event. Nature 362, 627–629 19 Alley, R.B. et al. (2003) Abrupt climate change. Science 299, 2005–2010 0169-5347/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2003.08.008
| Letters
Controlling the false discovery rate in ecological research Luis V. Garcı´a Departamento de Geoecologı´a, IRNAS-CSIC. P.O. Box 1052, E41080-Sevilla, Spain
A controversial question when analyzing outcomes of ecological research has been whether the increase of type I Corresponding author: Luis V. Garcı´a ([email protected]). http://tree.trends.com
error under repeated testing should be taken into account for evaluating the scientific soundness of the results [1–3]. The traditional strong control of the familywise error rate (FWER) (i.e. the probability of obtaining one or more
TRENDS in Ecology and Evolution
equilibrium, small amplitude cycles, or large amplitude cycles that closely approach zero were all possible outcomes for a predator– prey community in a chemostat (L.E. Jones et al., unpublished). Using this result, we predict that the variance of a population in simple communities will itself become smaller as genetic diversity in the prey increases (i.e. the variance of the coefficient of variation will decrease) (Figure 1b). For this reason, communities with low prey genetic diversity will exhibit extreme cycles more frequently than will communities with high prey genetic diversity. Future directions Recent theoretical and empirical research on the biology of predator–prey interactions shows the clear benefit of combining ecology and evolution under the single umbrella of community genetics [14,21]. Within this emerging field, the time is ripe to test questions extending on the work of Yoshida and colleagues. Does coevolution occur on the same time scale as predator–prey cycles, where cycles and evolution in the prey are accompanied by rapid evolution in the offensive traits of the predator [22]? Can the addition of species in the simple two-species community lead to diffuse coevolution [23]? Does increased intraspecific diversity beget ecological stability in ways that are similar to interspecific diversity? Such questions can be challenging to test in natural communities, although their importance is clear. Shertzer et al. [7] and Yoshida et al. [8] have taken a leap forward in our understanding of the ecological consequences of evolutionary processes. Acknowledgements We are grateful for comments and suggestions from P. Abrams, C. Brassil, S. Ellner, W. Godsoe, N. Hairston Jr, L. Jones, K. Shertzer, A. Sih, D. Viswanathan, T. Whitham and T. Yoshida. Our research (http://www. herbivory.com) is funded by grants from the Natural Sciences and Engineering Research Council of Canada to M.T.J.J. and A.A.A., and a Sigma Xi GIAR to M.T.J.J.
References 1 Ehrlich, P.R. and Raven, P.H. (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586– 608
Vol.18 No.11 November 2003
551
2 Ford, E.B. (1949) Mendelism and Evolution, Methuen and Co 3 Pimentel, D. (1961) Animal population regulation by the genetic feedback mechanism. Am. Nat. 95, 65 – 79 4 Rosenzweig, M.L. and MacArthur, R.H. (1963) Graphical representation and stability conditions of predator– prey interactions. Am. Nat. 97, 209 – 223 5 Abrams, P.A. (2000) The evolution of predator– prey interactions: theory and evidence. Annu. Rev. Ecol. Syst. 31, 79 – 105 6 Abrams, P.A. and Matsuda, H. (1997) Prey adaptation as a cause of predator– prey cycles. Evolution 51, 1742 – 1750 7 Shertzer, K.W. et al. (2002) Predator– prey cycles in an aquatic microcosm: testing hypotheses of mechanism. J. Anim. Ecol. 71, 802 – 815 8 Yoshida, T. et al. (2003) Rapid evolution drives ecological dynamics in a predator– prey system. Nature 424, 303 – 306 9 Borass, M.E. (1983) Population dynamics of food-limited rotifers in two-stage chemostat culture. Limnol. Oceanogr. 28, 548– 563 10 Halbach, U. (1970) Influence of temperature on the population dynamics of the rotifer Brachionus calyciflorus. Oecologia 12, 176 – 205 11 Fussmann, G.F. et al. (2000) Crossing the Hopf bifurcation in a live predator– prey system. Science 290, 1358 – 1360 12 Thompson, J.N. (1998) Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329 – 332 13 Fussmann, G.F. et al. (2003) Evolution as a critical component of plankton dynamics. Proc. R. Soc. Lond. Ser. B 270, 1015– 1022 14 Antonovics, J. (1992) Toward community genetics. In Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics (Fritz, R.S. and Simms, E.L., eds), pp. 426 – 449, University of Chicago Press 15 Whitham, T.G. et al. (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84, 559 – 573 16 Whitham, T.G. et al. (1999) Plant hybrid zones affect biodiversity: tools for a genetic based understanding of community structure. Ecology 80, 416– 428 17 Dungey, H.S. et al. (2000) Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54, 1938– 1946 18 Neuhauser, C. et al. (2003) Community genetics: expanding the synthesis of ecology and genetics. Ecology 84, 545 – 558 19 Loreau, M. et al. (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804 – 808 20 Elton, C.S. (1958) The Ecology of Invasions, Methuen and Co 21 Agrawal, A. (2003) Community genetics: new insights into community ecology by integrating population genetics. Ecology 84, 543– 544 22 Karban, R. and Agrawal, A.A. (2002) Herbivore offense. Annu. Rev. Ecol. Syst. 33, 641 – 664 23 Janzen, D.H. (1980) When is it coevolution? Evolution 34, 611 – 612 0169-5347/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2003.09.001
Climate– vegetation dynamics in the fast lane Eric Post Department of Biology, The Pennsylvania State University, 208 Mueller Lab, University Park, PA 16802 USA
Evidence from paleoclimatological research indicates that major climatic changes, such as the rapid increase in temperatures at the end of the Younger Dryas event , 11 000 years ago, can occur over the span of a few decades. Vegetation response to climatic variation and change, is, by contrast, often assumed to occur gradually over much longer timescales. Two recent papers confirm earlier, theoretical predictions that changes in species Corresponding author: Eric Post ([email protected]). http://tree.trends.com
composition of plant communities following climatic shifts can, however, occur with striking rapidity. The predominance of large mammalian grazers at high latitudes during the Pleistocene hints at a vegetation composition that is very different from the chemically defended trees and shrubs that are characteristic of the Arctic and sub-Arctic today [1]. Although the demise in the far north of horses, camels, wooly rhinos, steppe bison and wooly mammoths has been ascribed to many factors, including human exploitation, disease, interspecific
552
Update
TRENDS in Ecology and Evolution
competition and direct adverse effects of climatic change during the Pleistocene–Holocene transition, one hypothesis holds that these specialist grazers saw the disappearance of their foraging niches as the arid steppe was replaced by tundra, boreal forest and muskeg in response to increasing temperatures and precipitation [2]. Efforts to predict responses of extant species to current and future climatic warming can draw clues from the faunal turnovers and redistributions that occurred during the Pleistocene–Holocene transition ,11 000 years ago. Indeed, great strides have been made in monitoring and modeling the geographical range shifts of some animals in response to observed or projected spatial shifts in habitatand plant-community composition associated with climatic warming [3]. Yet, to better understand why some animal species went extinct the last time the Earth warmed up, and why some species, and which species, are likely to go extinct during this episode of rapid warming, we might need to understand just how rapidly plant-community composition can change. Two recent papers [4,5] provide evidence of an intermediate temporal scale of plant-community response to climatic change that is strikingly rapid on a geological timescale and not so out of reach of ecological timescales. Using lacustrine records from multiple sites throughout the North Atlantic region, Williams et al. [4] documented vegetation changes that, in many cases occurred ,100 years after the climatic shift associated with the Younger Dryas event (Box 1). Yu [5] examined pollen- and plant-macrofossil data, together with oxygen isotopic data on climatic variation, from two sites in southern Ontario, Canada, and reported evidence for the immediate replacement of periglacial desert by willow–juniper tundra following glacial retreat, and of replacement of spruce forest by pine by ,100 years after the onset of Holocene warming. These observations reveal the rapidity of vegetation response at the community level to the major climatic shifts that occurred at the Pleistocene–Holocene transition, which, in some cases, occurred as abruptly as, or even more suddenly than, those that are predicted to occur over the next century [6]. In so doing, the authors reveal a response of plant communities to climate change that is of an intermediate temporal scale, more gradual than the immediate phenological response of many species to recent warming [7], but as fast as or faster than the responses predicted by stochastic forest gap models [8] and predictions based on climate projections [9]. Of equal importance, perhaps, is that plant-community shifts in response to climatic fluctuation of the order of decades [4],
Vol.18 No.11 November 2003
coupled with the possibility of rapid extinction of plant species [10], might pose consequences for the persistence of animal species, because they respond both directly to climatic changes and indirectly to lagged, climate-induced changes in vegetation [11]. The strength of the study by Williams et al. [4] is their incorporation of quantitative time-series analysis of data from areas of varying topographical relief. They assembled records from 11 lake cores on both sides of the North Atlantic, with resolutions ranging from 16–93 years. Although, to a certain extent, the temporal resolution of the data will constrain the minimum observable lag in the response to climatic fluctuation, these data are of fairly high and consistent temporal resolution among samples. The lake records used by Williams et al. [4] contained proxies for both vegetation composition (pollen) and past climate (d18O and chironomid assemblages), and these time-series were compared using cross-correlation analysis. Remarkably, the median of the most highly significant cross-correlations among sites indicated a vegetation response time of 60 years, whereas, among all significant cross-correlations, the median lag occurred at 90 years. On a geological timescale, this is less than the blink of an eye, whilst, in an ecological perspective, such responses represent no more than a couple of population cycles for large herbivores [12] and many arboreal taxa. In contrast to Williams et al. [4], Yu [5] examined both pollen and plant macrofossil stratigraphic data from two proximal sites in southern Ontario, Canada, to reconstruct the late Quaternary vegetation history of the Niagara Escarpment. Importantly for this study, the Niagara Escarpment was only recently deglaciated, ,13 000 years before present (Bp). Hence, Yu’s cores, one of which penetrated to bedrock, and one of which penetrated to outwash gravel, facilitated an analysis of periglacial vegetation colonization and succession following retreat of the ice at the onset of the Holocene. Treeless boreal vegetation, a mix of Alnus– Dryas –Cyperaceae tundra, was evident initially after the retreat of the ice sheets, and dominated from ,12 000– 13 000 years Bp. Interestingly, the subsequent shift from treeless tundra to spruce forest might have been rapid and perhaps facilitated by migration from nearby refugia, because Picea glauca cones from proximate sites were dated to 12 320 ^ 360 years Bp [13]. Yu’s [5] detailed ordination analysis comparing the results of multivariate analyses of pollen assemblages to independent
Box 1. What was the Younger Dryas event? The Pleistocene (, 1.8 million–11 000 years ago) was not an ice age; rather, it was a series of waxing and waning ice ages characterized by dramatic climate fluctuations across a broad range of temporal frequencies. As global temperatures increased near the end of the Pleistocene, and as the ice sheets that covered much of North America and Northern Europe began to enter their final stages of retreat, there was a sudden decline in temperatures detectable by climate proxies throughout the northern hemisphere at between , 11 500 and 13 000 years before present. This sudden cooling phase, which lasted , 1000 – 1300 years, is known as the Younger Dryas event [17]. Its termination marked the end of the last ice age and the transition from the Pleistocene to the Holocene, a period of much warmer and more stable climate. http://tree.trends.com
The abruptness with which the Younger Dryas ended, and with which northern hemisphere temperatures rose, is dramatic. Isotopic evidence from Greenland ice cores has been interpreted as indicating that temperatures increased by , 78C in the span of little more than ten years [18]. Although the causes of such abrupt climatic change as the Younger Dryas event remain disputed, one hypothesis maintains that cold water from the melting ice sheets entered the Gulf of Mexico, through the St Lawrence Seaway, the North Atlantic, temporarily impeding the northward flow of warm water from the southern Atlantic via the Gulf Stream. Regardless of the mechanisms involved, abrupt climatic changes have occurred often, and have probably had major ecological repercussions [19].
Update
TRENDS in Ecology and Evolution
proxies of climatic variation from the same sites inferred from d18O data reveal complex community responses to climatic fluctuations. For example, vegetation at one of Yu’s sites (Crawford Lake, Ontario) had begun to shift to spruce forest by ,500 years after the Bølling–Allerød warming phase (,12 700 years Bp). However, there was a rapid increase in herb pollen percentages at the onset of the Younger Dryas event that was indicative of differential responses among the arboreal and herbaceous components. With the onset of rapid warming at the termination of the Younger Dryas event, however, there is a dramatic change in vegetation that is evident from Yu’s data: spruce-dominated forests shifted to pine-dominated forests within a span of ,100 years or less, spurred by the onset of Holocene warming. Such variability in the rate and nature of vegetation responses to climatic events might reflect the importance of factors such as baseline climatic conditions at various sites, biological inertia in the process of succession, facilitation of invasion by some species through the earlier presence of nitrogen fixers, and the proximity of refugia from which species can migrate to recently exposed sites. This last factor might be of particular relevance to Yu’s results for post-glacial expansion of spruce, because independent plant macrofossil data indicate that spruce occurred at the very edge of the ice sheet during the Last Glacial Maximum, ,18 000 ^ 1500 years Bp [14], and spruce migration rates have been estimated to vary between 0.05 and . 1 km y21, with a median rate of 0.10 km y21 [15,16]. The importance of these two studies lies in their ability to put a finger on just how quickly plant communities appear to have responded, and might continue to respond, to climate change.The beauty ofthe approachestaken byWilliams etal. [4] and Yu [5] lies in the fact that, not only do they confirm earlier theoretical predictions of the potential rapidity with which plant community composition might respond to abrupt climate changes, but they also complement the many studies of both plant and animal response to climatic events, variability and change that focus on spatial fluxes (e.g. [3]). The information provided by this pair of new papers, and the others that they will no doubt spawn, will prove valuable in future efforts to model the responses of plant and animal species to predicted climate change. In particular, the quantitative insights provided by these papers might facilitate the mechanistic modeling of climate change-related geographical range shifts and community
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dynamics at higher trophic levels, including large herbivores that survived the Pleistocene–Holocene transition [11]. Acknowledgements I would like to thank David Post, Jack Williams and two anonymous referees for helpful comments and discussions that greatly improved this article.
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| Letters
Controlling the false discovery rate in ecological research Luis V. Garcı´a Departamento de Geoecologı´a, IRNAS-CSIC. P.O. Box 1052, E41080-Sevilla, Spain
A controversial question when analyzing outcomes of ecological research has been whether the increase of type I Corresponding author: Luis V. Garcı´a ([email protected]). http://tree.trends.com
error under repeated testing should be taken into account for evaluating the scientific soundness of the results [1–3]. The traditional strong control of the familywise error rate (FWER) (i.e. the probability of obtaining one or more