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Interspecific Relationships Between Body Size and Response to Predation Risk 1, 2 EVAN L

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Interspecific Relationships Between Body Size and Response to Predation Risk 1, 2 EVAN L The allometry of fear: interspecific relationships between body size and response to predation risk 1, 2 EVAN L. PREISSER AND JOHN L. ORROCK 1Department of Biological Sciences, University of Rhode Island, Kingston, Rhode Island 02881 USA 2Department of Zoology, University of Wisconsin, Madison, Wisconsin 53706 USA Citation: Preisser, E. L., and J. L. Orrock. 2012. The allometry of fear: interspecific relationships between body size and response to predation risk. Ecosphere 3(9):77. http://dx.doi.org/10.1890/ES12-00084.1 Abstract. Body size is associated with fundamental biological processes such as metabolism, movement, and the rate of reproduction and evolution. Although allometric principles should also influence the range of potential behavioral responses for a given organism, evidence for such large-scale and cross-taxon relationships is lacking. If they exist, scaling-related changes in behavior should be prominent in predator- prey interactions: body size affects the likelihood of attack and the costs of predator avoidance. We take a interspecific perspective on a traditionally intraspecific topic by using a 142-species data set containing organisms ranging over seven degrees of magnitude in body size to analyze the relationship between mean response to predation risk and both prey size and the predator : prey size ratio. We found a weak but significant relationship between two metrics of prey size (mean species-level prey mass and mean species- level predator : prey size ratio) and two of the five prey response variables: risk-induced changes in prey habitat use and prey fecundity were significantly correlated with prey body size and the predator : prey ratio. Risk-induced reductions in prey activity were positively correlated with prey mass. In contrast, there was no correlation between prey mass or the predator : prey size ratio and risk-induced changes in either prey growth and survival. We also document considerable variation in response to predation risk among taxa, highlighting that many additional factors contribute to the effects of predation risk on prey behavior, growth, fecundity, and survival. The weak but significant large-scale relationships we documented in our work suggest that allometric relationships may play a subtle role in structuring some of a prey organism’s response to predation risk. Key words: allometry; anti-predator behavior; body size; non-consumptive effects; predator-prey interactions. Received 21 March 2012; revised 18 June 2012; accepted 17 July 2012; final version received 24 August 2012; published 18 September 2012. Corresponding Editor: J. Drake. Copyright: Ó 2012 Preisser and Orrock. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits restricted use, distribution, and reproduction in any medium, provided the original author and sources are credited. E-mail: [email protected] INTRODUCTION responses to climate change (Gardner et al. 2011) as well as alter food web structure and dynamics Body size is associated with many of the most (Brose 2010, Thierry et al. 2011). Predator-prey fundamental processes of biology: metabolism interactions are particularly affected by size and movement (Peters 1983, Schmidt-Nielsen considerations (Jackson and Dial 2011, Thierry 1984, Brown et al. 2004), rates of reproduction et al. 2011); size can prove a refuge for both small (Blueweiss et al. 1978, Peters 1983) and evolution and large prey (Brooks and Dodson 1965, Urban (Allen et al. 2006), and the likelihood of 2007b), and comparative studies have found extinction (Gaston and Blackburn 1995, Allen et broad support for a similar range of body-size al. 2006). Size-related properties can also affect ratios among consumers and their resources v www.esajournals.org 1 September 2012 v Volume 3(9) v Article 77 PREISSER AND ORROCK (Brose et al. 2006). questions may provide important insights into Anti-predator behavior often plays an integral the underlying impact of body size on behavior. role in predator-prey interactions (Lima and Dill We report the results of the first comprehen- 1990, Peacor and Werner 2001, Caro 2005), and sive inter-taxon analysis on the role of body size the relationship between prey body size and in affecting predation-induced changes in behav- predation risk has been extensively explored in a ior, growth, and fitness. Specifically, we use number of taxa (e.g., Urban 2007b and references meta-analysis to examine species-level responses cited therein). Within a given taxa, there are a of prey to predation risk (e.g., visual, chemical, range of potentially interactive reasons why and/or tactile predator cues; Preisser and Bolnick body size might affect anti-predator behavior: 2008) as a function of both prey body size and the body size determines energetic demands (Kleiber predator : prey body size ratio. A broad literature 1947, Schmidt-Nielsen 1984, Brown et al. 2004) attests to the importance of examining intraspe- that, in turn, determine the cost of anti-predator cific patterns: we complement this work with an behavior. For instance, larger or better-fed interspecific analysis of data from 142 prey organisms should experience a lower cost of species from 11 taxonomic classes and 74 foraging reductions in response to predation risk predator species from 12 classes whose body than smaller or hungry organisms (Stephens and size ranges over seven orders of magnitude. Our Krebs 1986, Lima and Bednekoff 1999). Larger aim in examining the relationship between prey body size also alters the likelihood of detection, size, predator : prey ratio, and responses to attack, and capture by a predator (Brooks and predation risk is to explore whether allometric Dodson 1965, Urban 2007b, Thierry et al. 2011) as principles provide an underlying framework for well as predator-mediated competitive interac- large-scale interspecific patterns of prey response tions (Peacor and Werner 2001). As one example, to predation risk. increased body size can increase the likelihood of prey detection but decrease the probability of METHODS capture by gape-limited predators (Urban 2007a). A key question emerging from studies that Literature search document a strong intraspecific signal of body We analyzed a large data set containing size on predator-prey interactions is whether information on the strength of nonconsumptive similar interspecific patterns also exist and, if so, effects (NCEs) of predation risk on prey. The data the nature of the relationship(s). set includes information from 196 papers pub- A recent review (Dial et al. 2008) highlighted lished prior to 2006. Our search methods are the fact that while broad allometric patterns have presented in detail elsewhere (Preisser et al. been explored in fields such as biogeography, 2007); briefly, we began by carrying out key community ecology, and evolutionary ecology word searches in three online databases (BIOSIS, (e.g., Brown et al. 2004), research into the effect of JSTOR, and Web of Knowledge Science Citation body-size scaling on behavior has lagged behind. Index) for papers that reported the results of They identify two factors as particular impedi- manipulative experiments reporting the respons- ments to such efforts. First, inter-taxon compar- e(s) of prey organisms to non-lethal predation isons are difficult because the type and range of risk (e.g., visual and/or olfactory cues, a caged or available behavioral data often varies widely nonlethal predator, etc.). In each paper identified between taxa. Second, the high degree of using this method, we searched both the cited intraspecific variability that many organisms literature and subsequent literature that cited it. exhibit is likely to obscure any broader interspe- Because we were primarily interested in popula- cific relationships. Despite these challenges, it is tion-level consequences of NCEs, we only used likely that ‘‘...size-related functional influences papers that include measurements of one or more on performance profoundly influence many of the following prey variables that have been aspects of animal behavior, such as how animals shown to respond strongly to the risk of forage, fight, flee, perceive danger, respond to predation (Preisser and Bolnick 2008): somatic risk and interact with other individuals’’ (Dial et growth (i.e., mass gain per time), fecundity (i.e., al. 2008:394). If so, research addressing such offspring per individual, brood size), density, and v www.esajournals.org 2 September 2012 v Volume 3(9) v Article 77 PREISSER AND ORROCK survival. Because so little data were available on tors, we found that information regarding pred- prey density, we chose not to analyze this ator mass was often lacking or ambiguous (e.g., response variable. We recorded data from any reporting only the sex of the predator; Trussell papers containing information on one or more of and Nicklin 2002). Only 24 of 196 papers these variables. In addition, we recorded data (accounting for 100 of 1042 records in the from these papers regarding prey activity (dis- database) provided data on predator mass; of tance moved, moves/hr, or other metrics assess- the remainder, 60 papers (309/1042 records) ing prey mobility) or open (i.e., non-refuge) provided data on predator developmental stage habitat use (proportion of time spent in open sufficient to estimate predator mass, 64 papers versus refuge habitats, percentage of individuals (296/1042 records) provided data on some aspect in predator-accessible areas, or other metrics of predator
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