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Transdisciplinary research is needed to predict plant invasions in an era of global change
Update Letters
Transdisciplinary research is needed to predict plant invasions in an era of global change Christoph Kueffer Institute of Integrative Biology, Plant Ecology Group, ETH Zurich, CH-8092 Zu¨rich, Switzerland
The recent article by Bradley et al. [1] provides a valuable overview of the challenges for plant invasion biology posed by global change. While the authors acknowledge the importance of human agency in shaping future plant invasions, they do not consider the implications for research or forecasting of invasion risks. As someone who believes that societal factors should be given more attention, I wish to state the case for transdisciplinary research that draws upon the expertise of social scientists, economists and bioengineers. Invasions are strongly influenced by the way humans move species, manage the land, and value nature and nonnative species. All of these processes will be affected by global change, with important implications for predicting and managing invasion risks [2,3]. Indeed, because many biological aspects of invasions are contingent upon the anthropogenic context of the invasion, global change may challenge some of the most basic assumptions of invasion biology. Generalizations about traits of invasive species (invasiveness) and characteristics of invaded habitats (invasibility) are based on observations of past invasions that happened under particular conditions. To better understand whether these results are transferable to other anthropogenic contexts, and thus provide a basis for predicting future invasions risks, we need to know more about the ways in which societal factors have shaped past and present invasions. However, relatively few studies have explicitly considered societal factors [2], and most of these have been based on a narrow range of socio-political settings [4]. In their article, Bradley et al. [1] argue that it is helpful to characterise invasive plants as opportunistic, well-dispersed and fast-growing species with a high demand for resources, and they implicitly assume the risk of invasion comes only from non-native species. However, this characterization may be insufficient in the future. This is because, as the following examples show, there might be changes not only in the processes driving invasions, but also in human perceptions of what constitutes an invasion. First, because invasions are strongly affected by the way humans select and move species, new invasion risks emerge as patterns of introduction change [3,5]. Some of the most problematic invasions on oceanic islands, for example, occurred on resource-poor soils and were caused by deliberate, large-scale introductions of non-native species that were pre-adapted to such conditions [6]. In contrast, many mountainous regions have not been heavily invaded. This might have less to do with harsh conditions Corresponding author: Kueffer, C. ([email protected]).
at high elevation than with the fact that few mountain specialists have been introduced to these areas [7]. If there were to be a shift from winter to summer tourism in certain regions, more pre-adapted non-native mountain plants might be introduced for horticulture, and such a societal response to climate change could well increase the invasion risk more than a change in climate per se ([7] and www. miren.ethz.ch). Second, invasion risks in the future may come from altogether novel organisms produced through genetic engineering or synthetic biology [8]. Such artificial organisms might have novel traits that do not fit into the classical picture of a typical invader outlined by Bradley et al. [1]. For instance, biofuel plants selected for growing on marginal land in order to mitigate climate change could pose a risk, even under harsh environmental conditions [9]. Third, the analysis of processes underlying invasions cannot be fully separated from stakeholder valuation [2]. Indeed, many concepts that lie at the foundation of invasion biology (for example, the ‘unnatural’ speed of spread or the relevance of the non-native origin of a species) are strongly tinged by human values. If global change causes shifts in the distribution and abundance of species, the distinction between native and non-native could become blurred, with some ‘native’ species being regarded as invasive [10]. The vigorous debate surrounding the assisted migration of threatened species [11,12] provides an illustration of just how value-laden our perceptions of what constitutes an invasion risk can be. Based on these arguments, I suggest that to predict risks in an era of global change we must treat plant invasions as an inherently socio-ecological phenomenon, and this implies new types of research collaboration. In particular, we must be able to anticipate the characteristics of species, whether native, non-native or artificial, that will be introduced to or spread to new areas, the scale and timing of these introductions (propagule pressure), and the disturbance regimes and landuse patterns that will characterise recipient habitats. Each of these aspects will depend upon social, economic, and political factors as well as upon advances in bioengineering of novel organisms. Acknowledgements I thank Peter Edwards for valuable comments on earlier versions of this letter.
References 1 Bradley, B.A. et al. (2010) Predicting plant invasions in an era of global change. Trends Ecol. Evol. 25, 310–318 619
Update 2 Kueffer, C. and Hirsch Hadorn, G. (2008) How to achieve effectiveness in problem-oriented landscape research: the example of research on biotic invasions. Living Rev. Landscape Res. 2, 2. http://www.livingreviews.org/ lrlr-2008-2 3 Hellmann, J.J. et al. (2008) Five potential consequences of climate change for invasive species. Conserv. Biol. 22, 534–543 4 Pysek, P. et al. (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol. Evol. 23, 237–244 5 Wilson, J.R.U. et al. (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol. Evol. 24, 136–144 6 Kueffer, C. et al. (2010) A global comparison of plant invasions on oceanic islands. Persp. Plant Ecol. Evol. Syst. 12, 145–161 7 Pauchard, A. et al. (2009) Ain’t no mountain high enough: plant invasions reaching new elevations. Frontiers Ecol. Environ. 7, 479–486
Trends in Ecology and Evolution Vol.25 No.11 8 Sutherland, W.J. et al. (2008) Future novel threats and opportunities facing UK biodiversity identified by horizon scanning. J. Appl. Ecol. 45, 821–833 9 Barney, J.N. and DiTomaso, J.M. (2008) Nonnative species and bioenergy: are we cultivating the next invader? BioScience 58, 64–70 10 Vale´ry, L. et al. (2009) Invasive species can also be native. Trends Ecol. Evol. 24, 585 11 Ricciardi, A. and Simberloff, D. (2009) Assisted colonization is not a viable conservation strategy. Trends Ecol. Evol. 24, 248–253 12 Schwartz, M.W. et al. (2009) The precautionary principle in managed relocation is misguided advice. Trends Ecol. Evol. 24, 474
0169-5347/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2010.08.001 Trends in Ecology and Evolution, November 2010, Vol. 25, No. 11
Letters
Biodiversity ‘‘surpluses’’ and ‘‘deficits’’ are not novel issues Kees (C.J.) Nagelkerke Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, NL-1098 XH Amsterdam, The Netherlands
Jackson and Sax (JS, [1]) provided a conceptual framework to analyze biodiversity dynamics after environmental change. They discuss transients caused by lags in extinction and immigration, rightly seen as of major importance for the future of biodiversity. Borrowing terms from accountancy, they discuss concepts such as ‘‘extinction debts’’, ‘‘immigration credits’’, ‘‘biodiversity surpluses’’ and ‘‘biodiversity deficits’’. For example, when time scales of immigration and extinction differ, temporary biodiversity surpluses or deficits may arise. Accidentally, JS overlooked my earlier work [2] covering much of the same ground. This work also corroborates, and adds to, the mainly conceptually oriented approach of JS by using an explicit evolution-based mechanistic model. Thereby it fulfills some of their expressed needs for further research and helps with the understanding and prediction of the kinds of transient dynamics JS discuss. I applied dynamic metapopulation modeling to multispecies-multi-habitat landscapes. The landscapes consisted of a mosaic of habitat types differing in disturbance frequency. With my modeling I aimed to investigate biodiversity transients occurring after various types of landscape change. I introduced the term ‘‘colonization credit’’ for lagged immigration, closely related to the ‘‘immigration credit’’ of JS. It was assumed that evolution had moulded dispersal rates to local extinction rates [3,4]. As a result, dispersal, and hence colonisation rate, increased with the natural disturbance rate of a species’ habitat. Evolution was taken to be slow enough to not modify dispersal during landscape change. These assumptions resulted in systematic differences between species in the speed of their reaction to landscape changes. The reaction speeds were set by the pristine habitat disturbance frequencies, but their Corresponding author: Nagelkerke, Kees (C.J.) ([email protected]).
620
ranking depended strongly on the type of landscape change. When habitat availability was affected, species from frequently-disturbed habitats were responding the fastest. Consequently, when landscape degradation increased the amounts of frequently-disturbed habitats relative to infrequently-disturbed ones, immigration of new, disturbancedependent, species occurred faster than extinction of species from the declining infrequently-disturbed habitats. This gave a temporary increase in biodiversity, a ‘‘surplus’’. In contrast, landscape recovery produced a ‘‘deficit’’, because (re)immigration of species using re-expanding, infrequently-disturbed, habitats occurred at a slower pace than the extinction of species from declining, frequently-disturbed, habitats. Hence, there was a strong asymmetry between degradation and recovery. Other modes of landscape change, such as increasing the disturbance rate of all habitats, or increasing dispersal resistance, produced transients completely different in the trajectory of the number of species as well as in composition. Figure 18.5 from [2] depicts some results. Note the close resemblance to Figure 2 of JS. In general, time lags depend critically on the characteristics of species and habitats and on the mode of environmental change. For example, response to increased dispersal resistance is much slower than to habitat destruction or increased disturbance (Figure 18.3 in [2]). The longest time-lags occur when species with low colonization and local extinction rates react to the impediment of dispersal. Conservationists should note this. However, those same species are the first to go extinct when disturbance rate is increased (Table 18.1 in [2]). My results show, firstly, that deficits and surpluses can arise from mechanistic models based on general assumptions. The necessary systematic differences between rates
Transdisciplinary research is needed to predict plant invasions in an era of global change Christoph Kueffer Institute of Integrative Biology, Plant Ecology Group, ETH Zurich, CH-8092 Zu¨rich, Switzerland
The recent article by Bradley et al. [1] provides a valuable overview of the challenges for plant invasion biology posed by global change. While the authors acknowledge the importance of human agency in shaping future plant invasions, they do not consider the implications for research or forecasting of invasion risks. As someone who believes that societal factors should be given more attention, I wish to state the case for transdisciplinary research that draws upon the expertise of social scientists, economists and bioengineers. Invasions are strongly influenced by the way humans move species, manage the land, and value nature and nonnative species. All of these processes will be affected by global change, with important implications for predicting and managing invasion risks [2,3]. Indeed, because many biological aspects of invasions are contingent upon the anthropogenic context of the invasion, global change may challenge some of the most basic assumptions of invasion biology. Generalizations about traits of invasive species (invasiveness) and characteristics of invaded habitats (invasibility) are based on observations of past invasions that happened under particular conditions. To better understand whether these results are transferable to other anthropogenic contexts, and thus provide a basis for predicting future invasions risks, we need to know more about the ways in which societal factors have shaped past and present invasions. However, relatively few studies have explicitly considered societal factors [2], and most of these have been based on a narrow range of socio-political settings [4]. In their article, Bradley et al. [1] argue that it is helpful to characterise invasive plants as opportunistic, well-dispersed and fast-growing species with a high demand for resources, and they implicitly assume the risk of invasion comes only from non-native species. However, this characterization may be insufficient in the future. This is because, as the following examples show, there might be changes not only in the processes driving invasions, but also in human perceptions of what constitutes an invasion. First, because invasions are strongly affected by the way humans select and move species, new invasion risks emerge as patterns of introduction change [3,5]. Some of the most problematic invasions on oceanic islands, for example, occurred on resource-poor soils and were caused by deliberate, large-scale introductions of non-native species that were pre-adapted to such conditions [6]. In contrast, many mountainous regions have not been heavily invaded. This might have less to do with harsh conditions Corresponding author: Kueffer, C. ([email protected]).
at high elevation than with the fact that few mountain specialists have been introduced to these areas [7]. If there were to be a shift from winter to summer tourism in certain regions, more pre-adapted non-native mountain plants might be introduced for horticulture, and such a societal response to climate change could well increase the invasion risk more than a change in climate per se ([7] and www. miren.ethz.ch). Second, invasion risks in the future may come from altogether novel organisms produced through genetic engineering or synthetic biology [8]. Such artificial organisms might have novel traits that do not fit into the classical picture of a typical invader outlined by Bradley et al. [1]. For instance, biofuel plants selected for growing on marginal land in order to mitigate climate change could pose a risk, even under harsh environmental conditions [9]. Third, the analysis of processes underlying invasions cannot be fully separated from stakeholder valuation [2]. Indeed, many concepts that lie at the foundation of invasion biology (for example, the ‘unnatural’ speed of spread or the relevance of the non-native origin of a species) are strongly tinged by human values. If global change causes shifts in the distribution and abundance of species, the distinction between native and non-native could become blurred, with some ‘native’ species being regarded as invasive [10]. The vigorous debate surrounding the assisted migration of threatened species [11,12] provides an illustration of just how value-laden our perceptions of what constitutes an invasion risk can be. Based on these arguments, I suggest that to predict risks in an era of global change we must treat plant invasions as an inherently socio-ecological phenomenon, and this implies new types of research collaboration. In particular, we must be able to anticipate the characteristics of species, whether native, non-native or artificial, that will be introduced to or spread to new areas, the scale and timing of these introductions (propagule pressure), and the disturbance regimes and landuse patterns that will characterise recipient habitats. Each of these aspects will depend upon social, economic, and political factors as well as upon advances in bioengineering of novel organisms. Acknowledgements I thank Peter Edwards for valuable comments on earlier versions of this letter.
References 1 Bradley, B.A. et al. (2010) Predicting plant invasions in an era of global change. Trends Ecol. Evol. 25, 310–318 619
Update 2 Kueffer, C. and Hirsch Hadorn, G. (2008) How to achieve effectiveness in problem-oriented landscape research: the example of research on biotic invasions. Living Rev. Landscape Res. 2, 2. http://www.livingreviews.org/ lrlr-2008-2 3 Hellmann, J.J. et al. (2008) Five potential consequences of climate change for invasive species. Conserv. Biol. 22, 534–543 4 Pysek, P. et al. (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol. Evol. 23, 237–244 5 Wilson, J.R.U. et al. (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol. Evol. 24, 136–144 6 Kueffer, C. et al. (2010) A global comparison of plant invasions on oceanic islands. Persp. Plant Ecol. Evol. Syst. 12, 145–161 7 Pauchard, A. et al. (2009) Ain’t no mountain high enough: plant invasions reaching new elevations. Frontiers Ecol. Environ. 7, 479–486
Trends in Ecology and Evolution Vol.25 No.11 8 Sutherland, W.J. et al. (2008) Future novel threats and opportunities facing UK biodiversity identified by horizon scanning. J. Appl. Ecol. 45, 821–833 9 Barney, J.N. and DiTomaso, J.M. (2008) Nonnative species and bioenergy: are we cultivating the next invader? BioScience 58, 64–70 10 Vale´ry, L. et al. (2009) Invasive species can also be native. Trends Ecol. Evol. 24, 585 11 Ricciardi, A. and Simberloff, D. (2009) Assisted colonization is not a viable conservation strategy. Trends Ecol. Evol. 24, 248–253 12 Schwartz, M.W. et al. (2009) The precautionary principle in managed relocation is misguided advice. Trends Ecol. Evol. 24, 474
0169-5347/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2010.08.001 Trends in Ecology and Evolution, November 2010, Vol. 25, No. 11
Letters
Biodiversity ‘‘surpluses’’ and ‘‘deficits’’ are not novel issues Kees (C.J.) Nagelkerke Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, NL-1098 XH Amsterdam, The Netherlands
Jackson and Sax (JS, [1]) provided a conceptual framework to analyze biodiversity dynamics after environmental change. They discuss transients caused by lags in extinction and immigration, rightly seen as of major importance for the future of biodiversity. Borrowing terms from accountancy, they discuss concepts such as ‘‘extinction debts’’, ‘‘immigration credits’’, ‘‘biodiversity surpluses’’ and ‘‘biodiversity deficits’’. For example, when time scales of immigration and extinction differ, temporary biodiversity surpluses or deficits may arise. Accidentally, JS overlooked my earlier work [2] covering much of the same ground. This work also corroborates, and adds to, the mainly conceptually oriented approach of JS by using an explicit evolution-based mechanistic model. Thereby it fulfills some of their expressed needs for further research and helps with the understanding and prediction of the kinds of transient dynamics JS discuss. I applied dynamic metapopulation modeling to multispecies-multi-habitat landscapes. The landscapes consisted of a mosaic of habitat types differing in disturbance frequency. With my modeling I aimed to investigate biodiversity transients occurring after various types of landscape change. I introduced the term ‘‘colonization credit’’ for lagged immigration, closely related to the ‘‘immigration credit’’ of JS. It was assumed that evolution had moulded dispersal rates to local extinction rates [3,4]. As a result, dispersal, and hence colonisation rate, increased with the natural disturbance rate of a species’ habitat. Evolution was taken to be slow enough to not modify dispersal during landscape change. These assumptions resulted in systematic differences between species in the speed of their reaction to landscape changes. The reaction speeds were set by the pristine habitat disturbance frequencies, but their Corresponding author: Nagelkerke, Kees (C.J.) ([email protected]).
620
ranking depended strongly on the type of landscape change. When habitat availability was affected, species from frequently-disturbed habitats were responding the fastest. Consequently, when landscape degradation increased the amounts of frequently-disturbed habitats relative to infrequently-disturbed ones, immigration of new, disturbancedependent, species occurred faster than extinction of species from the declining infrequently-disturbed habitats. This gave a temporary increase in biodiversity, a ‘‘surplus’’. In contrast, landscape recovery produced a ‘‘deficit’’, because (re)immigration of species using re-expanding, infrequently-disturbed, habitats occurred at a slower pace than the extinction of species from declining, frequently-disturbed, habitats. Hence, there was a strong asymmetry between degradation and recovery. Other modes of landscape change, such as increasing the disturbance rate of all habitats, or increasing dispersal resistance, produced transients completely different in the trajectory of the number of species as well as in composition. Figure 18.5 from [2] depicts some results. Note the close resemblance to Figure 2 of JS. In general, time lags depend critically on the characteristics of species and habitats and on the mode of environmental change. For example, response to increased dispersal resistance is much slower than to habitat destruction or increased disturbance (Figure 18.3 in [2]). The longest time-lags occur when species with low colonization and local extinction rates react to the impediment of dispersal. Conservationists should note this. However, those same species are the first to go extinct when disturbance rate is increased (Table 18.1 in [2]). My results show, firstly, that deficits and surpluses can arise from mechanistic models based on general assumptions. The necessary systematic differences between rates