REVIEWS REVIEWS REVIEWS A Comparison Of Shark And Wolf .
REVIEWS REVIEWS REVIEWSA comparison of shark and wolf researchreveals similar behavioral responses by preyAaron J Wirsing1* and William J Ripple2Marine and terrestrial ecologists rarely exchange information, yet comparing research from both sides of theland–sea boundary holds great potential for improving our understanding of ecological processes. For example, by comparing the interaction between tiger sharks (Galeocerdo cuvier) and dugongs (Dugong dugon) to thatbetween gray wolves (Canis lupus) and elk (Cervus elaphus), we show that top predators in marine and terrestrial ecosystems trigger three similar types of anti-predator behavior: (1) encounter avoidance, (2) escape facilitation, and (3) increased vigilance. By implication, the ecological roles of top predators in both ecosystemsmay be more similar than previously thought, and studies that fail to account for multiple modes of antipredator behavior are likely to underestimate these roles and the consequences of eliminating predators fromecosystems. We encourage more communication between marine and terrestrial ecologists, in the interest ofgenerating further insights into ecosystem dynamics and conservation.Front Ecol Environ 2011; 9(6): 335–341, doi:10.1890/090226 (published online 22 Jul 2010)Acommunication gap exists between marine and terrestrial ecologists (Chase 2000). This divide is due in partto the perception that, because of key chemical and physical differences between marine and terrestrial environments (eg the presence or absence of an aquatic medium),many of the ecological processes operating in these twoecosystems are fundamentally different (Steele 1991; Carret al. 2003). This perception is reinforced by compartmentalization within academic institutions and funding agencies (Raffaelli et al. 2005; Menge et al. 2009). Yet, information sharing across the land–sea boundary has fostered thedevelopment and dissemination of many valuable ecological insights, including concepts such as spatial and temporalscales and trophic cascades (Halley 2005; Menge et al. 2009;Terborgh and Estes 2010), and helped to answer pressingenvironmental questions, such as the nature of global carbon cycling (Cole 2005). Thus, where possible, a healthierexchange of information between ecologists working onIn a nutshell: Traditionally, there has been a communication gap betweenmarine and terrestrial ecologists Using gray wolves and tiger sharks as examples, we show thattop predators in terrestrial and marine ecosystems trigger similar behavioral responses among respective prey species, suggesting that they play similar ecological roles More frequent information exchange between terrestrial andmarine ecologists should provide additional insights into ourunderstanding of ecosystems and will help to guide conservation policy1School of Forest Resources, University of Washington, Seattle, WA(wirsinga@u.washington.edu); 2Department of Forest Ecosystemsand Society, Oregon State University, Corvallis, OR*Beyond the Frontier: Listen to Aaron Wirsing discussing this research on Frontiers’ monthly podcast, at www.frontiersinecology.org. The Ecological Society of Americaeither side of the marine–terrestrial interface should yieldnew insights and general rules that enhance our understanding of each ecosystem, allow for better prediction ofecosystem responses to perturbation, and guide conservation policy (Steele 1991; Chase 2000; Duarte 2007).Predator risk effects – lost foraging opportunities andreduced growth and reproduction experienced by preyinvesting in anti-predator behavior – are now widelyacknowledged as having important implications for preypopulations and ecosystem dynamics (Ripple and Beschta2004; Schmitz et al. 2004; Creel and Christianson 2008;Heithaus et al. 2008). However, few studies have comparedbehavioral responses to predation risk in both marine andterrestrial settings (see Peckarsky et al. [2008] for an example), perhaps inhibiting the formulation of general rules governing the nature and ecological consequences of riskeffects. Here, we highlight several striking examples of similarities between marine and terrestrial anti-predator behavior, paying special attention to parallels between the behavioral responses of dugongs (Dugong dugon) to tiger sharks(Galeocerdo cuvier) in the coastal seagrass ecosystem of SharkBay, Australia, and of elk (Cervus elaphus) to gray wolves(Canis lupus) in the Greater Yellowstone Ecosystem, USA(Figure 1). Our goal is to show how insights can be gainedfrom the “cross-pollination” of ideas from studies in differentecosystems and how this can encourage further communication and collaboration between ecologists tackling similarquestions on either side of the land–sea boundary.n Behavioral responses of dugongs to tiger sharksDugongs are large, marine mammalian grazers thatinhabit warm, coastal waters throughout the Indo–Pacificregion. In Western Australia’s Shark Bay, where dugongsnumber between 10 000 and 14 000 (Gales et al. 2004),shallow banks (water depth 4.5 m) covered by densewww.frontiersinecology.org335
Comparing shark and wolf research(a)(b)(c)(d)Yellowstone National ParkYellowstone National ParkM HeithausN Hammerschlag336AJ Wirsing and WJ Rippleing tactic – excavation – that gives accessto relatively nutritious seagrass rhizomes(roots), but inhibits vigilance by requiringa head-down posture. Instead, they switchalmost entirely to a less rewarding but safertactic – cropping – that facilitates head-upsurveillance, but only allows for the acquisition of nutrient-poor terminal leaves fromseagrass plants (Wirsing et al. 2007c; Figure2c). In other words, dugongs are only willing to take advantage of opportunities toharvest seagrass rhizomes through excavation behavior when there is less need toscan their surroundings for sharks.n Behavioral responses of elk to graywolvesElk are one of the largest terrestrial mammalsFigure 1. (a) Tiger shark (Galeocerdo cuvier); (b) dugong (Dugong dugon); in North America. Inhabiting grasslands and(c) gray wolf (Canis lupus); and (d) elk (Cervus elaphus).forest, these generalist herbivores can func-seagrass meadows (predominantly Amphibolis antarctica) lieamidst deeper channels (depths 6 m) with sandy substrates. Because they are seagrass specialists, dugongs in thissubtropical ecosystem spend the majority of their time foraging in shallow water (Wirsing et al. 2007a). However, thestrength of this large-scale (hundreds of meters to kilometers) habitat preference is not temporally consistent.Rather, it varies over time because dugongs in Shark Baymust cope with the risk of predation by tiger sharks, whichshow a preference for shallow banks over deep channels(Heithaus et al. 2002) and fluctuate in abundance with seasonal water temperature from a high in February to a low inJuly (Wirsing et al. 2006). When sharks are abundant,dugongs sacrifice food that might otherwise be acquired inshallow waters by increasing their time spent in deeperwater, where seagrass is relatively scarce but the encounterrate with sharks is lower (Wirsing et al. 2007a; Figure 2a).Tiger sharks do not hunt shallow seagrass banks uniformly. Instead, they spend more time patrolling peripheral (edges) than internal (interiors) portions of banks(Heithaus et al. 2006). Dugongs foraging on shallowbanks when sharks are present manifest a surprisingsmall-scale (tens of meters) shift. Namely, they increasetheir relative use of edges, where encounters with sharksare more likely, and thereby leave behind interior seagrassplants that they might otherwise have harvested (Wirsinget al. 2007b; Figure 2b). In doing so, dugongs benefit froman improved ability to escape to the safety of deep channels, where predators are far less numerous and increasedwater volume confers a maneuverability advantage overattacking sharks (Heithaus et al. 2006) that outweighs thecost of additional predator encounters.Dugongs also alter their fine-scale behavior at foraginglocations over shallow banks. When tiger sharks arenumerous, dugongs virtually abandon a profitable foragwww.frontiersinecology.orgtion as both grazers and browsers and are theprimary prey of gray wolves in the Rocky Mountains ofsouthern Canada and the northern US. Following the reintroduction of wolves into Yellowstone National Park in1995 and 1996, researchers have documented behavioraleffects associated with trophic cascades, whereby elk, underthe risk of predation by wolves, alter their habitat use andforaging patterns, vigilance, movements, group size dynamics, and other traits (Laundré et al. 2001; Ripple andBeschta 2004; Creel et al. 2005; Hernández and Laundré2005; Fortin et al. 2005). For example, when wolf packs arenearby, Yellowstone Ecosystem elk move from open grasslands – where food quality is highest – to coniferous forestcover, where encounters with wolves are less likely (Creel etal. 2005; Figure 2d).Elk vulnerability to wolf predation is heightened bynumerous features of the terrain, including deeply incisedchannels, multiple channels, oxbows, cut banks, terraces,and woody debris accumulations, each of which maycause fleeing ungulates to lose speed and maneuverabilityduring a chase (Bibikov 1982; Bergman et al. 2006;Ripple and Beschta 2006). Accordingly, elk exposed tothe risk of predation by wolves have been found to avoidsites near streams, where these impediments are common,at all times of the day and night (Beyer 2006), presumably to improve their ability to escape. Furthermore, afterthe return of wolves, elk browsing on aspen (Populustremuloides) was found to be lower in the vicinity ofdowned logs, which could impede fleeing elk (Ripple andBeschta 2007; Figure 2e).Elk respond to increases in predation risk with correspondingly higher vigilance rates, and this results inreduced foraging time (Laundré et al. 2001; Childress andLung 2003). Thus, high levels of elk vigilance can represent a response to an amplified level of fear and theincreased expectation of an attack by predators. Studies The Ecological Society of America
AJ Wirsing and WJ Ripple0.500.0002.001.501.000.500.000.01 0.02 0.030.04(b)0Probability ofconifer occurence1.000.80Vigilance(a)1.50Percent aspenbrowsedEscapefacilitation2.000.01 0.02 0.0350403020100(c)0.600.400.200.00(d)Wolves absent Wolves present60(e)40200Riparianwithout logs0.0430Time spentvigilant (%)EncounteravoidanceProp in edge/Prop in shallows/prop food in edge prop food in shallows337Prop of timeexcavatinghave shown increased average female elkvigilance levels following wolf reintroduction and greater female elk vigilance levelsin high wolf-density than in low wolf-density areas (Laundré et al. 2001; Childress andLung 2003). Elk vigilance was also significantly higher near escape impediments( 30 m) than at locations away from suchimpediments (Halofsky and Ripple 2008;Figure 2f). This pattern of vigilance hasapparently triggered a cascade effect characterized by reduced elk browsing and tallerwillows (Salix sp) and aspen within Yellowstone’s valley bottoms, especially whereescape impediments occur in relatively closeproximity to these woody species (Rippleand Beschta 2006, 2007).Comparing shark and wolf researchRiparianwith logs(f)201000.010.020.030.04Tiger sharks caught h–1Beyond 30 mWithin 30 mDistance to escape impedimentn Similarity between anti-predatorbehavior elicited by tiger sharks andwolvesFigure 2. Manifold risk effects of tiger sharks on dugongs and gray wolves onelk. (a) As relative shark abundance (catch rate h–1) increases, the proportionDespite their shared role as top predators, (prop) of dugongs foraging over shallow seagrass meadows decreases successivelylarge elasmobranchs (the taxonomic sub- more than expected, based on the proportion of food (seagrass) in the shallowsclass that includes sharks) and canids have (dashed black line), indicating a predator-induced shift into deeper water wherenot been the subject of comparative studies. encounters with sharks are less likely. (Adapted from Wirsing et al. 2007a.) (b)Yet, we show that the presence of tiger With rising shark abundance, the proportion of foraging dugongs along the edgessharks and wolves sparks an analogous set of of shallow seagrass meadows begins to exceed that expected, based on theanti-predator behaviors in a large marine proportion of food at the edges (dashed black line), indicating a shift from interior(dugong) and a large terrestrial (elk) herbi- portions of meadows to peripheral areas, where the probability of escape into deepvore, respectively. This close match between water is elevated. (Adapted from Wirsing et al. 2007b.) (c) The proportion ofdugong and elk defensive behaviors suggests time dugongs devote to excavation, a foraging tactic that inhibits vigilance,that predator risk effects can be transmitted declines as tiger shark abundance increases. (Adapted from Wirsing et al.through marine and terrestrial communities 2007c.) (d) When wolves are present, elk often shift from open grasslands toin a remarkably similar manner. Further- conifer forests (ie probability of conifer occurrence at locations of elk with GPSmore, the magnitude and variety of these collars increases), possibly to decrease encounters with wolves. (Adapted frombehavioral responses underscore the strong Creel et al. 2005.) (e) Elk browse more aspen at sites without downed logspotential for anti-predator behavior to influ- (escape impediments), likely to enhance escape possibilities in case of wolf attack.ence patterns of prey distribution and forag- (Adapted from Ripple and Beschta 2007.) (f) Elk vigilance is highest near escapeing in both ecosystems, even if the intensity impediments, likely in response to enhanced vulnerability to wolf predation.of predator-induced mortality (ie direct pre- (Adapted from Halofsky and Ripple 2008.) In (a–d), bars show means and 95%dation) is low. Anti-predator responses by confidence intervals. In (f), bars show means and standard errors.dugongs and elk lie along at least threebehavioral axes, corresponding to different spatial scales(Figure 2). At the largest spatial scale, both herbivoresapparently shift habitats to avoid encounters with predators when exposed to risk, with dugongs decreasing theiruse of shallow banks where sharks are abundant in favorof deeper water and elk moving away from open grasslands that are monitored by wolves and into the protective cover of coniferous woodlands. At an intermediatespatial scale, both prey species altered their foraging location to facilitate escape from would-be attackers, whenusing areas where encounters with predators were likely.Specifically, with sharks present, dugongs foraging overshallow seagrass banks increased their use of peripherallocations (edges), which provide for increased maneuver The Ecological Society of Americaability and easy access to deep water. Similarly, whileusing areas patrolled by wolves, elk concentrated theirforaging at locations away from escape impediments (egdowned logs). At a fine spatial scale (the foraging location), both herbivores apparently invest more heavily invigilance when under increased threat of predation, withdugongs increasing their use of a foraging tactic – cropping – that enables more effective surveillance whensharks are abundant and elk increasing their use of awatchful, head-up posture when feeding near obstaclesthat could impede their escape. More anti-predatorbehavioral parallels not considered in this paper are possible; for example, elk adjust their group dynamics inresponse to wolf predation risk (Winnie and Creel 2007),www.frontiersinecology.org
Comparing shark and wolf research338and dugongs responding to tiger sharks may do so as well.By implication, anti-predator responses by prey in bothmarine and terrestrial environments can be complex,meaning that studies in either domain that neglect one ormore of the kinds of responses documented here are likelyto underestimate or fail to detect risk effects and, consequently, result in an incomplete understanding of theroles played by predators in ecological communities.The multiple types of anti-predator behavior exhibitedby dugongs and elk suggest that predators may indirectlyaffect species that serve as food for their prey (typicallyproducers like plants, but also smaller consumers if theprey species is a carnivore) via diverse and sometimes conflicting pathways (Figure 3). That is, behavioral responses,such as encounter avoidance and enhanced vigilance,would be expected to benefit producers in areas wherepredators are abundant by displacing or reducing the timedevoted to foraging by prey. In contrast, efforts by prey toimprove their chances of escape could lead to eitherdiminished or heightened exploitation of producers,where predators are relatively numerous, depending onthe degree of spatial correlation between predator abundance and the ability of the prey species to escape attack.In Shark Bay, for example, shifts into deep water(encounter avoidance) and increased reliance on cropping (investment in vigilance) by dugongs responding totiger sharks likely benefit shallow seagrass meadows byreducing both the number of foragers and the extent towhich seagrass plants are destroyed by excavation. On theother hand, heavy use of edges (escape facilitation) bydugongs under threat of predation has mixed consequences for seagrass meadows, diminishing pressure oninterior seagrass plants but intensifying herbivory alongthe meadow periphery (Heithaus et al. 2007).In general, the net response of a prey individual to apredator is the product of several modes of behavioraladjustment. When these modes of adjustment have different consequences for producers, the overall nature of apredator’s indirect effect on any particular producer (iepositive or negative) should be contingent upon their relative magnitude. Accordingly, we suggest that studiesthat compare the strength of multiple types of prey antipredator responses may facilitate prediction of whetherproducers subject to the indirect effects of predators arewinners or losers (Schmitz et al. 2000).n Other examples of similarity between marine andterrestrial anti-predator behaviorMany other features of anti-predator behavior also appearto transcend the land–sea boundary. Here, we discussthree that should serve as a basis for fruitful exchangebetween marine and terrestrial ecologists: (1) the dependence of anti-predator behavior on prey body conditionor energetic state; (2) the dependence of anti-predatorbehavior on prey escape mode; and (3) the influence ofsuch behavior on community properties relative to that ofwww.frontiersinecology.orgAJ Wirsing and WJ Rippleconsumptive predator effects (ie reduction of prey densityvia direct predation). Each of the following three sectionscompares a pair of case studies drawn from the marineand terrestrial literature to demonstrate the generality ofone of these features.Prey body condition (energetic state)Studies from marine and terrestrial systems reveal an analogous relationship between prey body condition, or energeticstate, and investment in anti-predator behavior. In SharkBay, for example, green sea turtles (Chelonia mydas) at risk ofpredation by tiger sharks invest more heavily in anti-predator behavior (ie take fewer risks) as their body conditionimproves, spending more time foraging along the perimeterof seagrass meadows, where the quality of the plants onwhich they rely is reduced but escape to deeper water is easier (Heithaus et al. 2007). Similarly, common wildebeest(Connochaetes taurinus) under threat from lions (Pantheraleo) and spotted hyenas (Crocuta crocuta) on the AfricanSerengeti take greater risks when in poor condition and, as aresult, succumb to predation more often than individuals inbetter condition (Sinclair and Arcese 1995). By implication,risk effects in both marine and terrestrial ecosystems probably work synergistically with direct predation and bottom-upforces (eg food supply) to c
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