Ecology, 91(12), 2010, pp. 3563–3571 Ó 2010 by the Ecological Society of America Field evidence for pervasive indirect effects of fishing on prey foraging behavior 1,2,5 3,4 1,3 ELIZABETH M. P. MADIN, STEVEN D. GAINES, AND ROBERT R. WARNER 1Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, California 93106 USA 2Department of Biological Sciences, Macquarie University, Sydney, New South Wales 2019 Australia 3Marine Science Institute, University of California, Santa Barbara, California 93106 USA 4Bren School of Environmental Science and Management, University of California, Santa Barbara, California 93106 USA Abstract. The indirect, ecosystem-level consequences of ocean fishing, and particularly the mechanisms driving them, are poorly understood. Most studies focus on density-mediated trophic cascades, where removal of predators alternately causes increases and decreases in abundances of lower trophic levels. However, cascades could also be driven by where and when prey forage rather than solely by prey abundance. Over a large gradient of fishing intensity in the central Pacific’s remote northern Line Islands, including a nearly pristine, baseline coral reef system, we found that changes in predation risk elicit strong behavioral responses in foraging patterns across multiple prey fish species. These responses were observed as a function of both short-term (‘‘acute’’) risk and longer-term (‘‘chronic’’) risk, as well as when prey were exposed to model predators to isolate the effect of perceived predation risk from other potentially confounding factors. Compared to numerical prey responses, antipredator behavioral responses such as these can potentially have far greater net impacts (by occurring over entire assemblages) and operate over shorter temporal scales (with potentially instantaneous response times) in transmitting top-down effects. A rich body of literature exists on both the direct effects of human removal of predators from ecosystems and predators’ effects on prey behavior. Our results draw together these lines of research and provide the first empirical evidence that large-scale human removal of predators from a natural ecosystem indirectly alters prey behavior. These behavioral changes may, in turn, drive previously unsuspected alterations in reef food webs. Key words: behavior; coral reef; fishing; food web; herbivore; indirect effects; Line Islands, Central Pacific; marine; predator. INTRODUCTION insignificant top-down effects on ecosystems. Alterna- Fishing has long affected marine systems globally tively, it may suggest that the effects of fishing can take different pathways through ecosystems. For example, (Jackson et al. 2001) but has intensified drastically in fishing could potentially have larger effects on prey recent decades (Berkes et al. 2006). Although the direct behavior than on prey density by altering the levels of impacts of fishing (such as declines of harvested species) risk prey face (Dill et al. 2003, Schmitz et al. 2004). are well documented (Myers and Worm 2003), their Small-scale behavioral responses by prey to varying indirect, ecosystem-level consequences are not well predation risk have been shown in other systems to understood. For example, in some systems predator modify community structure (Ripple et al. 2001, Dill et loss has been associated with alternating abundances or al. 2003, Preisser et al. 2005). Theory also suggests that biomasses of lower trophic level species, termed a fishing may indirectly drive comparable food web density-mediated trophic cascade. This simple expecta- alterations over large scales (Walters and Kitchell tion, while commonly observed (McClanahan and 2001). Because these responses can have far greater net Muthiga 1988, Babcock et al. 1999, Dill et al. 2003, impacts (by occurring simultaneously over entire assem- Myers et al. 2007), is not found everywhere (Strong blages) and operate over far shorter temporal scales 1992, Mumby et al. 2006, Newman et al. 2006, Sandin et (with potentially instantaneous response times; Lima al. 2008). The large variability in cascade occurrence and and Bednekoff 1999, Walters and Kitchell 2001) in magnitude could indicate that fishing frequently has transmitting top-down effects than numerical effects alone, it is critical that they be considered in studies of Manuscript received 23 November 2009; revised 3 March the indirect effects of marine predator removal. 2010; accepted 22 April 2010. Corresponding Editor: S. R. Across a wide diversity of aquatic and terrestrial Thorrold. systems, including marine, freshwater, and terrestrial 5 Present address: Department of Environmental Sciences, University of Technology Sydney, Sydney, New South Wales systems, prey are known to respond to predators by 2007 Australia. E-mail: [email protected] altering their activity levels and spatial habitat uses (see 3563 3564 ELIZABETH M. P. MADIN ET AL. Ecology, Vol. 91, No. 12 reviews by Lima and Dill [1990] and Dill et al. [2003] and risk driven by fishing: the bullethead parrotfish (Chloru- meta-analysis by Preisser et al. [2005]). Such responses rus sordidus), a large, mobile herbivore; the whitecheek reflect the inherent trade-off between obtaining food and surgeonfish (Acanthurus nigricans), a medium-bodied, avoiding predators (Lima and Dill 1990), as described mobile, herbivore; the blackbar damselfish (Plectrogly- by the ‘‘ecology of fear’’ model of Brown et al. (1999). phidodon dickii), a small, site-attached omnivore; and Nonetheless, ecological studies and models often ignore the bicolor chromis (Chromis margaritifer), a small, site- behavioral responses of prey (Peckarsky et al. 2008), attached zooplanktivore. We quantified excursions (i.e., even though many prey behaviors (e.g., grazing on distance or area of reef over which individuals move benthic algae) play key roles in structuring natural during 5-min observations; see Appendix C) as a key systems. There is a growing body of theoretical (Brown metric of prey behavior. Excursions provide access to et al. 1999, Walters and Kitchell 2001, Frid et al. 2008, food and, in some cases, mates, yet necessarily impose Orrock et al. 2008) and empirical (Ripple et al. 2001, risk, because the probability of encountering predators Heithaus and Dill 2002, Dill et al. 2003, Werner and scales with the magnitude of the excursion (Anholt and Peacor 2003, Schmitz et al. 2004, Preisser et al. 2005, Werner 1995). As such, they provide a useful means of Heithaus et al. 2008, Peckarsky et al. 2008, Stallings determining how these prey fishes titrate for resources 2008) evidence for nonconsumptive effects and resultant and safety (Brown and Kotler 2004). behaviorally mediated trophic cascades, whereby a predator affects the resources of its prey via changes in Predation risk the prey’s behavior. Behavioral responses can mediate Both predation risk and prey behavioral responses top-down effects by altering per capita foraging rates were quantified at 11 sites within the three atolls and/or the spatial distribution of foraging effort (Palmyra, N 5; Tabuaeran, N 3; and Kiritimati, N (Schmitz et al. 2004, Preisser et al. 2005), as observed 3). Sites were¼ located at least 1¼ km apart and ranged in the Rocky Mountains of North America following ¼from two to 10 m depth. Both of our key metrics of the reintroduction of wolves to areas in which they had predation risk are based on biomass, rather than previously been eradicated by hunting (Ripple et al. abundance, of piscivorous fishes. Biomass has been 2001). Importantly, this mechanism can act in concert demonstrated to be a more meaningful metric for with or independently of numerical changes in prey (Dill detecting the effects of fishing on coral reefs, particularly et al. 2003, Werner and Peacor 2003, Schmitz et al. for areas in which larger and less abundant fish are 2004). Peckarsky et al. (2008) recently reevaluated a targeted by fishing (Russ and Alcala 1998). Importantly, number of classic textbook examples of (purportedly this underlying metric incorporates the sizes, in addition density-mediated) predator–prey interactions and found to abundance, of predators facing prey fishes, an that nonconsumptive effects played a key role in driving important factor in determining perceived predation some of the observed patterns. This evidence, coupled risk. In order to determine whether results could with global declines of marine predators due to fishing, potentially be idiosyncratic to this biomass-based metric suggests that large-scale empirical exploration of the of risk, however, an alternative metric of risk based on behavioral consequences of fear-released systems is both predator abundances filtered by a size threshold was also vital and timely (Heithaus et al. 2008). We set out to test used (see Appendix D). All fishes known to be primarily whether fishing has the potential to invoke this piscivorous were included in our predator counts. mechanism in natural reef systems by determining if Individuals of Scomberoides lysan ,30 cm total length and how prey fishes alter their foraging behavior in (TL) were excluded from our counts because juveniles of response to fishing-induced predator loss. Here we this species are not primarily piscivores and feed instead quantitatively examine these behavioral consequences on fish scales torn from schooling fishes (Lieske and across the remote northern Line Islands archipelago of Myers 1994), and their location at the surface of the the central Pacific, where the landscape of risk differs water