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Author's Personal Copy Author's personal copy Biol Invasions (2014) 16:735–753 DOI 10.1007/s10530-013-0550-8 PERSPECTIVES AND PARADIGMS Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach Jaimie T. A. Dick • Mhairi E. Alexander • Jonathan M. Jeschke • Anthony Ricciardi • Hugh J. MacIsaac • Tamara B. Robinson • Sabrina Kumschick • Olaf L. F. Weyl • Alison M. Dunn • Melanie J. Hatcher • Rachel A. Paterson • Keith D. Farnsworth • David M. Richardson Received: 1 August 2013 / Accepted: 16 September 2013 / Published online: 26 September 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Invasion ecology urgently requires predic- functional responses. We show that functional response tive methodologies that can forecast the ecological analyses, by describing the resource use of species over impacts of existing, emerging and potential invasive a range of resource availabilities, avoids many pitfalls species. We argue that many ecologically damaging of ‘snapshot’ assessments of resource use. Our frame- invaders are characterised by their more efficient use of work demonstrates how comparisons of invader and resources. Consequently, comparison of the classical native functional responses, within and between Type II ‘functional response’ (relationship between resource and III functional responses, allow testing of the likely use and availability) between invasive and trophically population-level outcomes of invasions for affected analogous native species may allow prediction of species. Furthermore, we describe how recent studies invader ecological impact. We review the utility of support the predictive capacity of this method; for species trait comparisons and the history and context of example, the invasive ‘bloody red shrimp’ Hemimysis the use of functional responses in invasion ecology, anomala shows higher Type II functional responses then present our framework for the use of comparative than native mysids and this corroborates, and could J. T. A. Dick (&) Á R. A. Paterson Á K. D. Farnsworth H. J. MacIsaac School of Biological Sciences, Institute for Global Food Great Lakes Institute for Environmental Research, Security, Queen’s University Belfast, M.B.C., 97 Lisburn University of Windsor, Windsor, ON N9B 3P4, Canada Road, Belfast BT9 7BL, Northern Ireland, UK e-mail: [email protected] O. L. F. Weyl South African Institute for Aquatic Biodiversity (SAIAB), M. E. Alexander Á T. B. Robinson Á S. Kumschick Á Grahamstown 6140, South Africa D. M. Richardson Centre for Invasion Biology, Department of Botany and O. L. F. Weyl Zoology, Stellenbosch University, Private Bag X1, Centre for Invasion Biology, SAIAB, Grahamstown, Matieland 7602, South Africa South Africa J. M. Jeschke A. M. Dunn Á M. J. Hatcher Department of Ecology and Ecosystem Management, School of Biology, University of Leeds, Restoration Ecology, Technische Universita¨tMu¨nchen Leeds LS2 9JT, UK (TUM), 85350 Freising-Weihenstephan, Germany A. Ricciardi Redpath Museum, McGill University, 859 Sherbrooke Street West, Montreal, QC H3A0C4, Canada 123 Author's personal copy 736 J. T. A. Dick et al. have predicted, actual invader impacts in the field. The Jeschke et al. 2012; Ricciardi et al. 2013). This may, in comparative functional response method can also be part, be due to a lack of rigour in defining these used to examine differences in the impact of two or hypotheses (Heger et al. 2013) and lack of focus on more invaders, two or more populations of the same demographic processes. These two major challenges invader, and the abiotic (e.g. temperature) and biotic need to be simultaneously addressed to advance the (e.g. parasitism) context-dependencies of invader fundamental science of invasion ecology and to impacts. Our framework may also address the previous provide practical methodologies that prioritize and lack of rigour in testing major hypotheses in invasion mitigate invasion threats by, for example, refining risk ecology, such as the ‘enemy release’ and ‘biotic assessment protocols (Ricciardi and Rasmussen 1998; resistance’ hypotheses, as our approach explicitly Parker et al. 1999; Byers et al. 2002; Andersen et al. considers demographic consequences for impacted 2004; Kumschick et al. 2012; Leung et al. 2012) and resources, such as native and invasive prey species. managing biological communities to provide maxi- We also identify potential challenges in the application mum biotic resistance (Taylor and Duggan 2012). of comparative functional responses in invasion ecol- There have been several attempts to develop ogy. These include incorporation of numerical frameworks for conceptualizing the mechanisms responses, multiple predator effects and trait-mediated whereby invasive species cause ecological impacts, indirect interactions, replacement versus non-replace- with a common theme being how invaders alter ment study designs and the inclusion of functional communities and ecosystems through resource use responses in risk assessment frameworks. In future, the (Vitousek 1990; Chapin et al. 1996; Parker et al. generation of sufficient case studies for a meta-analysis 1999). In particular, Parker et al. (1999) opined the could test the overall hypothesis that comparative need for ‘operational generalizations’ about impact functional responses can indeed predict invasive spe- and stressed the difficulty of assessing the per capita cies impacts. effects of invaders. Not all invaders have a major impact because of their per capita effects; for Keywords Invasive species Á Type II and III example, many invasive plants, through their great functional responses Á Resource use Á Impact abundance or biomass, affect fire regimes (Brooks prediction Á Predator–prey Á Invasion hypotheses Á et al. 2004). Nonetheless, many invaders do generate Species-trait comparisons Á Global change Á impacts directly because of per capita effects, and a Population stability and viability Á Biological major obstacle to testing impact theories is the lack of control Á Parasitism Á Biotic resistance Á Context- standardized methods for determining such effects on dependency Á Enemy release Á Risk assessment use of resources, such as native prey (Ricciardi et al. 2013). Furthermore, we require methods that can reliably explain the ecological impacts of existing invaders, and predict impacts of emerging and future invaders under different or changing environmental Introduction circumstances; understanding the corollary, patterns of resistance of natives towards invaders, would also Invasion biology faces two major challenges with be welcome. Ideally, such methods should be rapid, respect to increasing our ability to forecast the reliable, inexpensive and applicable across taxonomic ecological impacts of invasive species. Firstly, the and trophic groups, with data collection possible from discipline needs to move beyond describing and a variety of laboratory and field-based studies, as cataloguing case studies of impact towards the devel- appropriate to the organisms and systems involved. opment of a mechanistic understanding of impact that Here, we review and provide a framework for a would allow for more predictive power, and this in the promising emerging field in invasion ecology that can context of global change (Walther et al. 2009; Dick address these issues: the use of comparative functional et al. 2013; Simberloff et al. 2013). Secondly, robust responses, whereby the relationship between resource tests of major hypotheses in invasion ecology are often consumption rate (e.g. by a predator) and resource lacking, as evidenced by equivocal support for many density (e.g. prey) is compared between invader and such hypotheses (e.g. Catford et al. 2009; Davis 2011; native species to reveal ecological impact (e.g. see 123 Author's personal copy Comparative functional responses 737 Dick et al. 2013; Fig. 1a–d). Specifically, we: (1) examine species trait comparisons in invasion ecology and explore advantages of the functional response method in this context; (2) review the historical use of functional responses in invasion ecology and its major hypotheses; (3) introduce our comparative functional response framework and its advantages as a predictive tool in invasion ecology; and (4) outline future challenges of implementing this framework in pre- dicting invader impacts and testing hypotheses, and identify research priorities. Species traits comparisons and the utility of functional responses Comparisons of species traits between invaders and natives (or unsuccessful/less successful invaders) have in some circumstances been successful in identifying broad determinants of invasiveness in terms of estab- lishment and spread (e.g. Mack 1996; Remanjek and Richardson 1996; Sakai et al. 2001; van Kleunen et al. 2010), however, numerous exceptions to any derived rule dilute the predictive power of such techniques for any one known or potential invader. Trait-based predictions have had some success in predicting plant establishment, invasiveness and impact (e.g. Pysˇek et al. 2009; but see Palacio-Lopez and Gianoli 2011), but the distribution of success of such trait compar- isons is patchy among animal taxa (Hayes and Barry 2008), with some good predictors of invasion success for birds (Sol et al. 2002; Blackburn et al. 2009), fishes (Marchetti et al. 2004a, b) and mammals (Jeschke and Strayer 2006), often based on propagule pressure and human affiliation. However, consistent predictors of invasion success across animal and plant taxa remain elusive (Hayes and Barry
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