Ecological Impacts of an Invasive Predator Explained and Predicted by Comparative Functional Responses
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Ecological impacts of an invasive predator explained and predicted by comparative functional responses Jaimie T. A. Dick, Kevin Gallagher, Suncica Avlijas, Hazel C. Clarke, Susan E. Lewis, Sally Leung, Dan Minchin, Joe Caffrey, et al. Biological Invasions ISSN 1387-3547 Volume 15 Number 4 Biol Invasions (2013) 15:837-846 DOI 10.1007/s10530-012-0332-8 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media B.V.. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Biol Invasions (2013) 15:837–846 DOI 10.1007/s10530-012-0332-8 ORIGINAL PAPER Ecological impacts of an invasive predator explained and predicted by comparative functional responses Jaimie T. A. Dick • Kevin Gallagher • Suncica Avlijas • Hazel C. Clarke • Susan E. Lewis • Sally Leung • Dan Minchin • Joe Caffrey • Mhairi E. Alexander • Cathy Maguire • Chris Harrod • Neil Reid • Neal R. Haddaway • Keith D. Farnsworth • Marcin Penk • Anthony Ricciardi Received: 11 May 2012 / Accepted: 27 August 2012 / Published online: 7 September 2012 Ó Springer Science+Business Media B.V. 2012 Abstract Forecasting the ecological impacts of a recent and ecologically damaging invader in Europe invasive species is a major challenge that has seen and N. America, in comparison to the local native little progress, yet the development of robust predic- analogues Mysis salemaai and Mysis diluviana in tive approaches is essential as new invasion threats Ireland and Canada, respectively. This was conducted continue to emerge. A common feature of ecologically in a novel set of experiments involving multiple prey damaging invaders is their ability to rapidly exploit species in each geographic location and a prey species and deplete resources. We thus hypothesized that the that occurs in both regions. The predatory functional ‘functional response’ (the relationship between responses of the invader were generally higher than resource density and consumption rate) of such those of the comparator native species and this invasive species might be of consistently greater difference was consistent across invaded regions. magnitude than those of taxonomically and/or trophi- Moreover, those prey species characterized by the cally similar native species. Here, we derived func- strongest and potentially de-stabilizing Type II func- tional responses of the predatory Ponto-Caspian tional responses in our laboratory experiments were freshwater ‘bloody red’ shrimp, Hemimysis anomala, the same prey species found to be most impacted by H. anomala in the field. The impact potential of J. T. A. Dick (&) Á K. Gallagher Á H. C. Clarke Á J. Caffrey S. Leung Á M. E. Alexander Á C. Maguire Á Inland Fisheries Ireland, Swords Business Campus, C. Harrod Á N. Reid Á K. D. Farnsworth Swords, Co. Dublin, Ireland School of Biological Sciences, Queen’s University Belfast, Belfast, Northern Ireland BT9 7BL, UK C. Harrod e-mail: [email protected] Instituto de Investigaciones Oceanolo´gicas, Universidad de Antofagasta, Avenida Angamos 601, S. Avlijas Á A. Ricciardi Antofagasta, Chile Redpath Museum, McGill University, 859 Sherbrooke Street West, Montreal, QC H3A 0C4, Canada N. R. Haddaway Institute of Integrative and Comparative Biology, S. E. Lewis Faculty of Biological Sciences, University of Leeds, Carroll University, 100 North East Avenue, Leeds LS2 9JT, UK Waukesha, WI 53186, USA M. Penk D. Minchin School of Natural Sciences, Trinity College Dublin, The Coastal Research and Planning Institute, Dublin, Ireland University of Klaipeda, Klaipeda, Lithuania 123 Author's personal copy 838 J. T. A. Dick et al. H. anomala was further indicated when it exhibited Ricciardi et al. 2012). However, given that the rapid similar or higher attack rates, consistently lower prey exploitation of resources is a trait commonly associ- handling times and higher maximum feeding rates ated with high-impact invaders (Strayer et al. 1999; compared to those of the two Mysis species, formerly Byers et al. 2002; Johnson et al. 2008; Morrison and known as ‘Mysis relicta’, which itself has an extensive Hay 2011), valuable insights into their ecological history of foodweb disruption in lakes to which it has impact could conceivably be derived from inter- been introduced. Comparative functional responses specific comparisons of their ‘functional response’— thus merit further exploration as a methodology for i.e., the relationship between resource density and predicting severe community-level impacts of current consumer uptake rate. Recently, it was suggested that and future invasive species and could be entered into introduced predators that are damaging to native risk assessment protocols. communities might display higher functional responses than comparator native species (Bollache Keywords Biological invasion Á Ecological impact Á et al. 2008). We propose that comparative functional Functional response Á Prediction Á Risk assessment responses of invaders and natives offer a methodology to forecast the impacts of present and future invaders. Further, strong impacts may be predictable when new invaders exhibit functional responses that are consis- Introduction tently equivalent to, or higher than, those of known harmful invaders across different biogeographical Invasive species continue to jeopardize biodiversity and regions. Should this be the case, comparative func- disrupt ecosystems (Lockwood et al. 2007;Davis2009; tional responses may also be a useful metric to include Ricciardi et al. 2012). The most cost-effective approach in risk assessment protocols (see Andersen et al. 2004). to managing invasion threats is prevention (Leung et al. To further explore this concept and its application, 2002), but effective allocation of limited resources we conducted a novel inter-regional experiment to towards this goal requires reliable forecasts of invasive- examine the functional responses of an invasive ness and impact (Byers et al. 2002). Although there has predator of emerging global significance, the Ponto- been some progress in linking species characteristics to Caspian mysid ‘bloody red’ shrimp, Hemimysis ano- invasiveness (Kolar and Lodge 2001; van Kleunen et al. mala G.O Sars, which is spreading across continental 2010;Kelleretal.2011), few advances have been made Europe (Ketelaars et al. 1999; Ricciardi et al. 2012) in developing methods for predicting the ecological and has recently invaded the UK (Holdich et al. 2006), impacts of invaders (Byers et al. 2002;NRC2002; Ireland (Minchin and Holmes 2008) and the North Ricciardi 2003;Lockwoodetal.2007;Davis2009;but American Great Lakes (Ricciardi et al. 2012). In order see Nentwig et al. 2009). Some physiological and life to assess the potential ecological impact of this history correlates of ecological impact have been species, we compared its functional responses with identified for terrestrial plants (McIntyre et al. 2005; those of other mysids, Mysis salemaai Audzijonyte & Pysek et al. 2009), but attempts to use species traits to Va¨ino¨la¨, 2005 (native to Ireland) and M. diluviana predict the outcomes of invasions in general have had Audzijonyte & Va¨ino¨la¨, 2005 (native to boreal North modest success to date (Cronk and Fuller 1995; America). The latter are sister species in the Mysis Lockwood et al. 2007;Davis2009; van Kleunen et al. relicta complex, which itself has an extensive invasion 2010). history and has caused biodiversity loss and foodweb Further, variation in morphological, genetic and disruptions in many lakes to which it has been behavioural characteristics across their invasive ranges introduced (Nesler and Bergersen 1991). We predicted have frustrated attempts to identify species traits that that these crustacean predators would display Holling consistently predict invader impacts on recipient Type II functional responses, as such responses are communities (Hayes and Barry 2008; Tecco et al. most likely to be de-stabilizing with respect to prey 2010). Presently, the only general predictive method populations (Murdoch and Oaten 1975) and thus available is to reference an invader’s history of impact, would concur with observed patterns of prey species an approach limited to invaders whose effects are displacement in invaded systems (see Ketelaars et al. already well documented (NRC 2002; Ricciardi 2003; 1999; Ricciardi et al. 2012). 123 Author's personal copy Invader functional responses 839 Materials and methods asymptote at prey density 30, densities were increased to 40, 80 and 140 with this prey species (Fig. 1a) and In Ireland, we collected H. anomala (8–14 mm body for all subsequent experiments, which were conducted length) from Loughs Derg and Ree and the native M. for 12 h overnight in darkness (when mysids forage salemaai (16–21 mm) from Loughs Derg and Neagh. most actively). These methods were repeated with In Canada, we collected H. anomala and Mysis H. anomala and M. diluviana in Canada. diluviana (of similar respective size ranges as above) Mean prey eaten at 12 h was examined for each from the St. Lawrence River and Lakes Memphrem- prey species in two-Factor ANOVAs with respect to agog and Oneida, respectively. All mysids