To Olfactory and Visual Cues from Multiple Predators

Oecologia (2010) 162:893–902 DOI 10.1007/s00442-010-1564-x BEHAVIORAL ECOLOGY - ORIGINAL PAPER DiVerential habitat use and antipredator response of juvenile roach (Rutilus rutilus) to olfactory and visual cues from multiple predators Charles W. Martin · F. Joel Fodrie · Kenneth L. Heck Jr. · Johanna Mattila Received: 16 June 2009 / Accepted: 6 January 2010 / Published online: 3 February 2010 © Springer-Verlag 2010 Abstract The indirect, behavioral eVects of predation and open-water habitat, but entered structured habitat when predator–predator interactions can signiWcantly alter the presented with a vision cue of this predator. Opposite trophic ecology of many communities. In numerous responses were elicited from roach for both olfactory and instances, the strength of these eVects may be determined visual cues of perch. Interestingly, roach defaulted to selection by the ability of prey to identify predation risk through of structured habitat when presented with vision + olfaction predator-speciWc cues and respond accordingly to avoid cues of either predator. Moreover, when presented individ- capture. We exposed juvenile roach (Rutilus rutilus), a ual cues of both predators together, roach responded by common forage Wsh in many brackish and freshwater envi- choosing open-water habitat. Upon being presented with ronments, to vision and/or olfactory cues from two preda- vision + olfaction cues of both predators, however, roach tors with diVerent hunting methods: northern pike (Esox strongly favored structured habitat. DiVerences in habitat lucius, an ambush predator) and European perch (Perca selection of roach were likely in response to the alternative Xuviatilis, a roving predator). Our results demonstrated that foraging strategies of the two predators, and suggest that responses of roach to perceived risk (as evidenced by their prey species may not always use structured habitats as pro- selection of structured or open-water habitats) were highly tection. This appears particularly true when a threat is per- dependent on cue type and predator identity. For instance, ceived, but cannot immediately be located. These results roach responded to olfactory cues of pike by entering provide insight to the complex and variable nature by which prey respond to various cues and predators, and oVer a mechanistic guide for how behaviorally mediated and Communicated by Anssi Laurila. predator–predator interactions act as structuring processes in aquatic systems. C. W. Martin (&) · K. L. Heck Jr. Dauphin Island Sea Lab, 101 Bienville Boulevard, Dauphin Island, AL 36528-0369, USA Keywords Antipredator behavior · Predator–prey e-mail: [email protected] interactions · Olfaction · Vision · Multiple predator eVects · Non-consumptive eVects C. W. Martin · K. L. Heck Jr. University of South Alabama, 307 University Boulevard N, Mobile, AL 36688-0002, USA Introduction F. J. Fodrie The non-consumptive eVects of predation (also referred to Department of Marine Sciences, Institute of Marine Sciences, as trait or behaviorally mediated indirect interactions) are University of North Carolina at Chapel Hill, increasingly recognized to be an important, yet understud- 3431 Arendell Street, Morehead City, NC 28557, USA ied, component of predator–prey interactions and food-web dynamics (Dill et al. 2003; Grabowski 2004). Recent meta- J. Mattila Husö Biological Station, Åbo Akademi University, analyses have indicated that the mere threat of predation Tykistökatu 6, 20520 Turku, Finland can have impacts that are as strong, if not stronger, than 123 894 Oecologia (2010) 162:893–902 direct consumption (Dill et al. 2003; Werner and Peacor predator eVects on shared prey, especially relative to the 2003; Pressier et al. 2005). For instance, indirect interac- impacts of predator species operating alone (Sih et al. tions that alter the foraging behavior of mid-trophic-level 1998). In some cases, multiple predators can operate syner- species can initiate trophic cascades (Trussell et al. 2002; gistically, resulting in enhanced risk for their shared prey Schmitz et al. 2004). A key element of these non-lethal (Fodrie et al. 2008). Nearly all reports of predator facilita- predator–prey exchanges is the ability of prey to recognize tion that result in enhanced risk for a shared prey are based and evade risk once a threat is perceived through visual, on two elements: one predator alters the habitat selection of olfactory, mechanoreception, electroreception, or social prey, and this makes prey highly vulnerable to attacks from cues. Thus, separating the behavioral responses of prey to another predator (Sih et al. 1998). In other scenarios, preda- various cue types should lead to a better understanding of tors interfere with one another resulting in reduced risk for the circumstances in which trait-mediated interactions will prey (Crowder et al. 1997). Often, this occurs if prey are dominate trophic exchanges and regulate energy Xow capable of rapidly switching between predator-speciWc through food webs. defense behaviors/mechanisms (Sih et al. 1998). Regard- Although the roles of all antipredator sensory cues have less of the outcome, the ability of prey to receive, process, been evaluated in aquatic systems [e.g., mechanoreception and act upon multiple cues is put to a stern test in instances via lateral line sensitivity (Montgomery and MacDonald when there is more that one threatening predator species. 1987) and social cues via schooling (Hager and Helfman Although tests of multiple predator eVects have thus far 1991; Brown et al. 2009)], many experiments have focused focused on prey mortality as the response variable, multiple on the role of vision (Mathis et al. 1993; Heithaus et al. predator eVects should be equally important determinants 2002, 2006; Wirsing et al. 2007) and olfactory cues in of non-consumptive eVects. To our knowledge, the speciWc mediating predator–prey exchanges (Smith 1992; Kats and cues used by prey in multiple predator scenarios and Dill 1998; Chivers and Smith 1998; Brown 2003; Amo subsequent eVects on habitat selection have not been et al. 2004; Kusch et al. 2004; Ylönen et al. 2007). Within evaluated. aquatic environments, we still know little about the relative To investigate cue-mediated predator–prey interactions, roles of each in governing predator–prey interactions we designed an experiment to address the following ques- (Wahle 1992; Mathis and Vincent 2000; Hickman et al. tions: (1) what are the relative roles of olfactory and visual 2004; Kim et al. 2009), even though it could be expected cues from two common predators on the habitat selection of that prey rely heavily on olfaction within relatively turbid a widespread prey species, and (2) do interspeciWc combi- environments. In the future, eutrophication (Utne-Palm nations of predator cues induce responses in prey habitat 2002; Engström-Öst and Mattila 2008) and the loss of sedi- selection that could be predicted by averaging the responses ment-stabilizing foundation species such as submerged of prey to each predator individually? aquatic vegetation (Waycott et al. 2009) should lead to increasingly turbid conditions. This may force prey to rely even more heavily on olfaction for guiding defensive Materials and methods responses to predator detection (Lehtiniemi et al. 2005). Therefore, data are needed to evaluate the relative eVects of Study organisms vision and olfaction, which are recognized as the most important sensory cues used by prey within shallow-water We explored cue-driven predator–prey interactions using environments (Mikheev et al. 2006), on the predator-avoid- commonly encountered species in brackish and freshwater ance responses of prey. Moreover, quantifying the magni- habitats throughout Europe. Juvenile roach (Rutilus ruti- tude and direction of prey responses elicited by these cues, lus), a numerically dominant forage Wsh that inhabits both both individually and in combination, has the potential to open-water and structured habitats [e.g., emergent reeds reveal new insights for predicting how food webs will (Phragmites australis) as well as numerous species of sub- respond to anthropogenic stressors aVecting water quality merged aquatic vegetation], were used as prey. While roach (sensu Lindquist and Bachmann 1982; Shivik 1998). are known to school, especially under threat of predation Since omnivory is common in natural systems (Pimm (Christensen and Persson 1993; Eklöv and Persson 1995), and Lawton 1978), most species at lower and intermediate we used individual roach in this experiment to tease apart positions in food webs (i.e., forage Wsh in estuarine envi- their responses to various cue inputs as a starting point to ronments) not only receive multiple cues from single preda- understanding their behavior. We selected northern pike tors, but also simultaneous threat stimuli from multiple (Esox lucius) and European perch (Perca Xuviatilis), two of predator species. Therefore, prey must respond to an amal- the most commonly encountered piscivores in this region gam of risk cues. Where predator species diVer in foraging (BonsdorV and Blomqvist 1993; Ådjers et al. 2006) as pre- behaviors, there is growing interest in quantifying multiple dators. These two species have diVerent foraging strategies: 123 Oecologia (2010) 162:893–902 895 northern pike hide in vegetation and ambush prey (Savino drained, rinsed thoroughly, and reWlled with Wltered water and Stein 1989), while perch forage by continually roving to eliminate any lingering olfactory cues from previous

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