Learning & Behavior 2004, 32 (1), 131-140

Social about predators: A review and prospectus

A. S. GRIFFIN McGill University, Montreal, Quebec, Canada

In comparison with social learning about food, social learning about predators has receivedlittle at- tention. Yet such research is of potential interest to students of animal cognition and conservation bi- ologists. I summarize evidence for social learning about predators by fish, , eutherian , and marsupials. I consider the proposal that this phenomenon is a case of S–S classical conditioning and suggest that evolution may have modified some of the properties of learning to accommodate for the requirements of learning socially about danger. I discuss some between- differences in the properties of socially acquired predator avoidance and suggest that learning may be faster and more robust in species in which alarm behavior reliably predicts high predatory threat. Finally, I highlight how studies of socially acquired predator avoidance can inform the design of prerelease antipredator training programs for endangered species.

Intuitively, it seems that antipredator behavior should ing acquisition of risky information from others, rather be fully functional upon a first encounter with danger. than at one’sown peril, or an explosion in the amount of Indeed, some stimulus configurations—for example, two research on social learning in the last 2 decades. Two pat- black circles—are inherently aversive and trigger avoid- of social influence on predator avoidance have ance responses in animals with no prior experience of emerged. First, exposure to the alarm behavior of predator- predators (Coss, 1978; Csányi, 1985). On the other hand, experiencedsocial companionscan enhancethe frequency there are reasons to predict that under some environ- (Palleroni, 1999) or the specificity (Cheney & Seyfarth, mental conditions, antipredator behavior should be on- 1990) of antipredator responses of juvenilesor can cause togenetically flexible. First, risk can vary in response specificity to develop more quickly (Mateo, space and time. Learning allows quantitative levels of 1996; Mateo & Holmes, 1997). The second pattern of antipredatorresponses to be fine-tuned to local conditions learning involves the acquisition of responses to previ- (Lima & Dill, 1990). Second, environmental change can ously unfamiliar stimuli and occurs in both juvenilesand expose animals to previously unfamiliar predators, and adults. This process has been termed observational con- learning allows novel dangers to be recognized (Berger, ditioning(Cook, Mineka,Wolkenstein,& Laitsch,1985), Swenson, & Persson, 2001). Third, community structures or releaser-inducedrecognitionlearning(Suboski,1990), can change across generations. Under these conditions, and is the focus of the present review. recognition of stimuli, such as the alarm behavior of Socially acquired predator avoidanceis a taxonomically heterospecifics, may not evolve. Learning allows novel widespread phenomenon that has been found in fish, cues to become associated with predators. In keeping birds, eutherians, and marsupials. The pattern of acqui- with these predictions, there is now abundant evidence sition is similar across groups. Before learning, subjects that learning plays an important role both in the acquisi- show little or no response to a given stimulus. After that tion of antipredator responses and in the adjustment of stimulus has been presented together with an alarm sig- preexisting ones. nal, however, it evokes an avoidance response. Most known examples of predator avoidance learning Several authors have noted the similarity between the involve the use of social information. Unfortunately, the process of predator avoidance acquisition and Pavlovian effects of direct experience with predators have received S–S conditioning (Heyes, 1994; Mineka & Cook, 1993; little attention.It is, therefore, difficult to tell whether the Shettleworth, 1998; Suboski, 1990). Within this frame- apparent importance of social influences on predator work, the predatory cue is considered a conditional stim- avoidance learning reflects an evolutionary trend favor- ulus (CS) to which observers acquire avoidanceresponses after the stimulus has been presented in contiguity with an alarmed demonstrator, the unconditioned stimulus The author thanks Louis Lefebvre, Jeff Galef, and Douglas Chivers (US). Such an analysis is supported by the positive cor- for comments on this paper. A.S.G. is supported by the Swiss National relations between levels of demonstrator and observer Foundation for Scientific Research. Correspondence concerning this article should be addressed to A. S. Griffin, Department of Biology, alarm behavior during training and by the positive correla- McGill University, 1205 Dr Penfield Ave., Montreal, PQ, H3A 1B1 tions between observer fear levels during and after train- Canada (e-mail: [email protected]). ing (Mineka & Cook, 1993). Socially acquired predator

131 Copyright 2004 Psychonomic Society, Inc. 132 GRIFFIN avoidance has recently been demonstrated in tammar a second category of chemicalalarm substances, referred wallabies (Macropus eugenii), an Australian macropo- to as disturbance cues, has also been identified (for a re- did marsupial (Griffin & Evans, 2003). This finding ex- view, see Chivers & Smith, 1998). These chemicals are tended the existence of such learning to a new taxonomic released when a fish detects a predator. Although prior group and provided the impetus for the present review. exposure to these substances and unfamiliar predators My objectives here are both to provide an overview of appears to enhance survival in staged predatory encoun- past work and to suggest new research approaches to ters (Mirza & Chivers, 2002),it is not known whether dis- mechanisms of socially transmitted predator avoidance. turbance cues facilitate predator recognition learning, as First, I will summarize the evidence for socially trans- do damage-released alarm cues. mitted predator avoidance in fish, birds, and eutherian Conspecific alarm substances that trigger avoidance and marsupial mammals. I chose this taxonomic focus responses in fish with no prior experience of them (Göz, because the vast majority of studies on socially acquired 1941; Magurran, 1999; Suboski et al., 1990) may func- predator avoidancehave been conductedin these groups, tion as USs during training (Suboski, 1990). The associ- even thoughsuch learning might occur in other taxa, such ation of a chemical US and a predatory CS resembles the as amphibians and reptiles (Suboski, 1992). Second, I association of carbon disulfide and a food odor that me- will examine whether the properties of learning support diates learning about novel foods in rats (Galef, 1996). In the idea that socially acquired predator avoidance is me- contrast to chemically induced food preferences, how- diated by asocial learning mechanisms, rather than by ever, visual stimuli produced by alarmed conspecifics some independent social learning process. Third, I will can also facilitate predator recognition. Naive individu- highlight some species differences and discuss possible als observing fearful demonstrators through a clear bar- reasons for them. Finally, I will briefly illustrate how the rier while simultaneously experiencing novel predator findings from basic studies of socially acquired predator cues acquire antipredator responses to these predator avoidance can inform the design of prerelease anti- cues (Chivers & Smith, 1994a; Suboski et al., 1990). In predator training programs for endangered species. the case of visual cues, it is more difficult to specify the nature of the US producing predator avoidance.Specific FISH movement patterns of the demonstrator, such as dashing (Chivers & Smith, 1994a), or positionrelative to the sub- Predator avoidance learning in fish has been the focus strate might be important, but there have been no at- of much basic research. There is some evidence that di- tempts to investigatethe role of such features in learning. rect experience with predators (being startled or chased) The recent developmentof movement analysisalgorithms can inculcate antipredator responses or enhance preex- allows dynamic stimuli to be encoded quantitatively isting ones (Järvi & Uglem, 1993). However, social cues (Peters, Clifford, & Evans, 2002),and video-editingcom- seem to be particularly effective for triggering predator puter software can be used to build dynamic video stim- avoidance learning in this group. uli and to manipulate movement cues while controlling for morphology. Test stimuli are then presented to ob- Social Stimuli That Trigger Learning servers on high-resolution monitors, a technique known in Observers to evoke biologically meaningful responses in several The most intensively studied associative paradigm in species of fish (see, e.g., Kodric-Brown & Nicoletto,2001; fish has involved paired presentations of unfamiliar Trainor & Basolo,2000). Such an approach could, hence, predator cues with alarm . VonFrisch (1938) be used to understand which aspects of a fearful demon- discovered that the skin of an injured fish releases chem- strator trigger learning in their observers. ical substances that evoke alarm responses in receivers. Social transmission of predator avoidance is not re- Shortly thereafter, Göz (1941) showed that these sub- stricted to conspecifics. Both chemical alarm substances stances facilitate predator avoidancelearning. Göz found and the sight of alarmed shoalmates in mixed species ag- that blindedEuropean minnows (Phoxinusphoxinus) dis- gregations facilitate antipredator learning in hetero- played an alarm response to a predator odor to which specifics. For example, the alarm pheromones (Chivers, they had previouslybeen indifferent after experiencingthat Brown, & Smith, 1995) or the sight (Mathis, Chivers, & odor in the presence of injured conspecifics. Decades Smith, 1996) of fathead minnows (Pimephales prome- later, the effects of alarm substanceswere isolated by ex- las) mediate acquired antipredator responses in brook tracting them from the skin of donor fish, and it was shown stickleback (Culaea inconstans). Unlike responses to that chemical substances alone are sufficient to trigger conspecific alarm substances, which appear to be expe- learning (Magurran, 1989; Suboski et al., 1990). Today, rience independent (Magurran, 1999), there is evidence the role of injury-released chemical cues in socially ac- that responses to heterospecific alarm substances are quired predator avoidance has been demonstrated in a learned (Chivers, Mirza, & Johnston, 2002; Chivers & range of species, including several outside the super- Smith, 1994b). In fathead minnows, responses to hetero- order Ostariophysi, to which such learning was origi- specific alarm substances are acquired socially through nally thought to be restricted (for reviews, see C. Brown associations with conspecific alarm substances (Mirza & Laland, 2001; Chivers & Smith, 1998). More recently, & Chivers, 2001). Social learning thus allows both for SOCIAL LEARNING ABOUT PREDATORS 133 novel predators to be recognized and for novel cues to and posttested in the laboratory but trained in the field become associated with predators. show significant acquired responses to a novel predator (G. E. Brown, Chivers, & Smith, 1997; Chivers & Smith, Content of Learning 1995b). Fish can acquire fear responses to a range of stimuli, Transmission across chains of individuals and including biologically meaningful olfactory and visual through populations. The transmission of socially ac- cues, such as the odor (Chivers & Smith, 1994c;Magurran, quired predator avoidance across chains of individuals 1989) or sight (Chivers & Smith, 1994a) of predators. has been documentedin several species of fish (D. Hall & Fish can also learn to avoid specific habitats after these Suboski, 1995; Suboski et al., 1990). Initial demonstra- have become associated with the presence of chemical tors are conditioned using paired presentations of preda- alarm substances (Chivers & Smith, 1995a). A range of tor cues and chemical alarm substances, whereas subse- arbitrary olfactory and visual cues, such as morpholine quent groups can be trained by mixing naive individuals (Suboski et al., 1990) or red lights (D. Hall & Suboski, with experienced demonstrators and presenting predator 1995; Yunker, Wein, & Wisenden, 1999), can also ac- cues (Suboski et al., 1990). Under laboratory conditions, quire control over fear responses, once they have been transmission occurs across at least three groups of naive reliably associated with predation risk. To my knowl- observers (Suboski et al., 1990). Alarm responses to edge, only one study has shown that acquired responses risky habitatscan also be transmitted to naiveshoal mates are specifically evoked by the training stimulus (Chivers from individualstrained with chemical alarm substances & Smith, 1994a). Fathead minnows trained to respond (Chivers & Smith, 1995a). fearfully to predatory pike respond to pike but do not dis- In addition to chain transmission experiments in the play a fear response to goldfish. Similarly, minnows that laboratory, there has been one attempt to quantify the have been conditioned to respond fearfully to goldfish spread of acquired predator avoidance through a natural do not generalize their acquired response to pike. population.Predator awareness spreads rapidly through a predator-naivepopulationafter introductionof a predatory Properties of Learning species (Chivers & Smith, 1995b). Ten predatory pike Preferential learning. Despite the apparent flexibil- were released into a predator-free population of approx- ity in the kind of information that can be acquired, there imately 20,000 fathead minnows. Laboratory measures is some evidence that socially acquired predator avoid- showed that each pike consumed from 2 to 5 minnows ance is adaptively biased. Magurran (1989) found that per day. Fathead minnows showed no alarm responses to European minnows can be conditionedto respond to odors pike odor before the introduction. Tested only 14 days of both nonpredatory tilapia (Tilapia mariae) and preda- later, the minnows displayed high-levelresponses to pike tory pike but that the magnitudeof the acquired response odor. Field studies have the obvious disadvantage that to the predator is higher than that to the nonpredator. At- mechanisms of transmission cannot be specified. In par- tempts to determine which stimulus features are more ticular, the effects of individual learning cannot be sep- readily associated with fear have shown that motion, but arated from the effects of social learning. Nevertheless, not shape, triggers preferential learning (Wisenden & the rapidity with which predator awareness spread in this Harter, 2001). study suggests that learning did not rely solely on indi- Evidence for a slightly different kind of constraint vidual exposure to the predators. comes from work on fathead minnows. Predator-naive Functional benefits of socially acquired predator individuals acquire fear responses to the sight of preda- avoidance. The functional benefits of socially acquired tory northern pike (Esox lucius) that are similar to those predator avoidancehave been examined in several species acquired to nonpredatory goldfish (Carassius auratus), by comparing survival of trained and nontrainedfish dur- but 2 months after conditioning, learned responses to ing staged encounters with predators (Berejikian, Smith, pike are greater than responses to goldfish (Chivers & Tezak,Schroder, & Knudsen, 1999; Chivers et al., 2002; Smith, 1994a). Järvi & Uglem, 1993; Mirza & Chivers, 2000). Trained Behavior of observer during training, speed of fish had consistently higher survival rates than did un- acquisition, duration of acquired responses, latent trained fish in both laboratory and field studies. inhibition, and context specificity. Studies of socially acquired predator avoidance in fish have shown consis- BIRDS tently that both chemical and visual cues evoke alarm re- sponses in observers during training (Chivers & Smith, Predator avoidance learning has received less atten- 1994a; Suboski et al., 1990). Predator recognition is typ- tion in birds than in fish. Most recent work has been mo- ically acquired in a single paired presentation of social tivated by efforts to enhance survival rates of endangered and novel stimuli and is retained for up to 2 months avian species bred in captivity and released into the wild (Chivers & Smith, 1994a). Effects of prior habituation (Maloney & McLean, 1995; McLean, Hölzer, & Strud- to the CS on acquisition have not been investigated in holme, 1999;van Heezik, Seddon,& Maloney,1999).For this taxonomic group. Acquired antipredator responses conservation purposes, experiments are not designed to are not context specific. Groups of fathead minnows pre- enhance the understanding of mechanisms of acquisition 134 GRIFFIN but, rather, to maximize the likelihoodof learning. Con- tious after having seen a predator holding a dead con- sequently, training regimes usually engage both individ- specific. Acoustic playbacks of conspecific alarm calls ual and social acquisitionprocesses. As in fish, basic re- are known to trigger predator avoidance learning in ob- search has revealed evidence for individuallearning about servers (Vieth, Curio, & Ernst, 1980). predators (Kramer & von St. Paul, 1951) but has focused Just as chemical alarm substances emitted by one fish primarily on elucidating the mechanisms of socially ac- species can trigger predator avoidance learning in an- quired predator avoidance (Curio, 1988, 1993; Curio, other species, heterospecific alarm calls can initiate Ernst, & Vieth, 1978). After anecdotal observations by cross-species learning. Paired presentationsof an unfamil- Lorenz (1952, 1969) in corvids and preliminary tests of iar model and a multispecies alarm chorus inculcate socially transmitted avoidanceof feeding dishes in ducks antipredator responses in blackbirds that are similar to (Klopfer, 1957), Kruuk (1976) was the first to investi- those of birds trained with a conspecific demonstrator gate whether predator avoidance could be socially trans- (Vieth et al., 1980). Responses to heterospecific alarm mitted in birds. However, Curio et al. (1978) provided calls might be acquired, perhaps through direct associa- the first compelling demonstration of socially acquired tions with predators (Shriner, 1999) or, as in fish (Mirza predator avoidance. Since then, a handful of other stud- & Chivers, 2001) and (Hauser, 1988),secondary ies have demonstrated socially acquired predator avoid- associationswith conspecific alarm calls. However, there ance in other species, including starlings (Sturnus vul- have been no direct tests of this hypothesis. garis; Conover & Perito, 1981), ring-billed gulls (Larus delawarensis; Conover, 1987), and New Zealand robins Content of Learning (Petroica australis; Maloney & McLean, 1995; McLean Both basic and applied research programs have shown et al., 1999). Curio’s work remains, however, the most consistently that birds acquire fear responses to model detailed study of socially acquired predator avoidancein vertebrates, both predatory and nonpredatory, and that avians. such acquired responses are specific to the training stim- ulus. For example, Kruuk (1976) found that sea gulls Social Stimuli That Trigger Learning in alighted at a greater distance from a model stoat after Observers training but found no changesin behaviortoward a hedge- Mobbing is a compound social stimulus that incorpo- hog, suggesting that the acquired wariness was specific rates both visual (tail and wing flicks and predator- to the predator. Similarly, birds trained to respond to directed dives) and acoustic (alarm calls) signals in re- model vertebratesdo not respond to arbitrary control stim- sponse to predators. The results from several studies sug- uli after training (empty box, Curio et al., 1978; plastic gest that mobbing acts as a US that triggers learning in bottle, McLean et al., 1999). observers (Conover, 1987; Curio et al., 1978; Kruuk, 1976; Maloney & McLean, 1995; McLean et al., 1999). For ex- Properties of Learning ample, Kruuk found that, relative to control birds, both Preferential learning. There is evidence for prefer- lesser black-backed (Larus fuscus) and herring (Larus ential learning in birds. The initial presentation of a argentatus) gulls alight at a significantly greater dis- model Australian honeyeater (Philemon corniculatus) tance from a model stoat after they have seen the model evokes a greater response from blackbirds than does a stoat holding a dead gull and have participated in mob- plastic bottle, and when each of these stimuli is paired bing aggregations around the predator. Unfortunately, with the experience of a conspecific appearing to mob Kruuk’s experimental situation made it impossible to them, the magnitude of the acquired antipredator re- separate the role of mobbing conspecifics from that of sponse to the honeyeater is much greater (Curio et al., the dead bird itself in acquired predator avoidance.Curio 1978). et al. subsequentlydemonstratedthat Europeanblackbirds Behavior of observer during training, speed of ac- (Turdus merula) learn to mob a species of bird to which quisition, duration of acquired responses, latent in- they are initially indifferent (Australian honeyeater,Phile- hibition, and context specificity. As in fish, observer mon corniculatus), once they have seen a conspecific ap- alarm levels reflect those of the demonstrators during pear to mob it. training (Curio et al., 1978). Predator recognition is ac- Both visual and acoustic cues alone suffice to trigger quired after one paired presentation of the social and the predator avoidance learning. Conover and Perito (1981) novel stimuli and has been shown to be retained for at found that significantly fewer starlings alighted at food least 8 days (Curio et al., 1978). Blackbirds acquire fear placed close to a model owl (Bubo virginianus) after responses to a CS even if they have received repeated they had seen the predator holding a struggling starling presentations of the stimulus before social conditioning in its talons and that latencies to land were significantly (Curio et al., 1978). The context specificity of acquired longer. During training, the live conspecific was tethered responses has not been tested in avians. to the predator model but did not vocalize, suggesting Transmission across chains and functional bene- that visual alarm cues alone facilitated predator avoid- fits of learning. Curio et al. (1978) tested transmission ance learning. Kruuk’s (1976) work on free-living sea across a chain of 6 blackbirds and found no decline in gulls also suggeststhat observers may become more cau- acquired responses. However, the acquired responses of SOCIAL LEARNING ABOUT PREDATORS 135 the observers were higher during posttraining tests than presented in conjunction with experimental playbacks of during their subsequent service as demonstrators, sug- conspecific terrestrial alarm yaps (Herzog & Hopf, 1984). gesting that acquired responses are less robust in black- birds than in the fish species tested to date. Content of Learning Only one applied study has addressed the question of Alarm behavior can be conditioned to both model and whether socially acquired predator avoidance enhances live predators (Herzog & Hopf, 1984; Mineka & Cook, the likelihoodof survival. Survival rates of houbara bus- 1988), and acquired responses are relatively specific to tards (Chlamydotis undulata) conditioned to respond to the conditionedstimulus. After training, rhesus monkeys a live predator were higher than those of untrained birds conditioned to respond fearfully to did not gen- (van Heezik, Seddon, & Maloney, 1999). Conditioning eralize their acquired response to control stimuli, such engaged, however, both individual (being chased by a as wood blocks and electrical cords (Mineka & Cook, predator) and social (presence of predator-experienced 1988).Similarly,a squirrel monkey,conditionedto avoid demonstrator) learning processes. a model cat paired with conspecific alarm calls, did not respond fearfully to a model that, during training, EUTHERIAN MAMMALS had been presented simultaneously with a control sound (Herzog & Hopf, 1984). Findings from field experiments with mammals strongly suggest that social learning plays a role in ac- Properties of Learning quired predator avoidance. Free-living mother moose Preferential learning. In monkeys, as in birds, anti- (Alces alces) behave more cautiously in response to wolf predator responses are associated with some stimuli (Canis lupus) howls once they have lost an offspring to preferentially. For example, rhesus monkeys failed to ac- this predator (Berger et al., 2001). It is possible, however, quire fear responses to a toy rabbit or flowers even after that experience with wolves involves both social (observ- watching video sequences of conspecifics behavingfear- ing a predatory event on a social companion) and indi- fully toward these stimuli (Cook & Mineka, 1989, 1990). vidual (being chased) experience. Field studies do not Interestingly, second-order avoidance conditioning does allow identification of the mechanism of transmission. not seem to be subject to such constraints.Monkeys con- However, field studies are very important because they ditioned to respond fearfully to snakes later acquire fear indicate the biological significance of phenomena ob- responses to an arbitrary object (striped box, a second- served in the laboratory. Socially acquired object avoid- order CS) when it was reliably associated with presenta- ance has been demonstrated under controlled conditions tion of a snake (a first-order CS; Cook & Mineka, 1990). in several eutherian mammals, including rats (Rattus Behavior of the observer during training, speed of norvegicus; Lore, Blanc, & Suedfeld, 1971), pata mon- acquisition, duration of acquired responses, latent keys (Erythrocebus patas; K. R. L. Hall, 1968), squirrel inhibition, and context specificity. As in other taxo- monkeys (Saimiri sciureus; Herzog & Hopf, 1984; nomic groups, the alarm behavior of observer rhesus Huebner, Lentz, Wooley, & King, 1979), and rhesus monkeys correlates positivelywith that of demonstrators monkeys (Macaca mulatta; Mineka & Cook, 1988). But during training (Mineka & Cook, 1993). Observer fear the most compelling evidence for socially acquired responses reach asymptotic levels after only one condi- predator avoidance in eutherian mammals is that pro- tioning trial and are maintained over the course of five vided by Mineka, Cook, and their colleagues in studies subsequenttrainingsessions.However, responseslearned of rhesus monkeys (for a review, see Mineka & Cook, in two training trials are retained for at least 3 months, 1988), the only eutherian system in which mechanisms longer than those learned in one training trial (Mineka & of social learning of predator avoidance have been ex- Cook, 1993). As in birds, there is evidence that latent in- plored systematically. hibition does not impair learning. Monkeys exposed to six presentations of a snake and food before fear condi- Social Stimuli That Trigger Learning in tioning nevertheless acquire fear responses to the snake Observers after watching a demonstrator respond fearfully to it Mineka, Cook, and colleaguesdemonstratedin a series (Mineka & Cook, 1986). Finally, by conditioning rhesus of papers that juvenile rhesus monkeys fear snakes after monkeys in one context and testing them in another, watching a social companionrespond fearfully to a snake. Mineka, Davidson, Cook, and Keir (1984) demonstrated Like the mobbing behavior of birds, alarm responses of that acquired fear responses are not context specific. rhesus monkeys are compound signals containing both Transmission across chains and through popula- acoustic (e.g., vocalizations and teeth chattering) and vi- tions. Cook et al. (1985) demonstrated that individuals sual (e.g., piloerection and specific body postures) com- that have acquired fear responses to snakes after watching ponents,bothof which appear to function as USs (Mineka wild-reared demonstrators respond fearfully to them can & Cook, 1993). There is also evidence that an acoustic be used as demonstrators for yet another group of naive on its own is sufficient to trigger predator observers. However, fear responses tended to decline in avoidance learning. Two juvenile squirrel monkeys be- laboratory-conditioned individuals over the course of came more fearful of a model predator once it had been their use as demonstrators, and acquired responses in ob- 136 GRIFFIN servers were somewhat lower than they were after the training model (fox) and to another morphologically first round of conditioning (Cook et al., 1985). Trans- similar predator (cat, Felis catus), although the learned mission across longer chains has not been tested. response to the cat was transient. Wallabies did not behave differently in response to a model nonpredator (goat, MARSUPIAL MAMMALS Capra hircus) after training with a fox model.

Marsupial species were traditionallyincorporatedinto Properties of Learning studies of learning so that the performance of eutherian Preferential learning. There have been no attempts mammals could be compared with that of a group pre- to determine whether socially acquired predator avoid- sumed to be evolutionarily less “complex” (for a review, ance in marsupials is biased toward some kinds of stim- see Wynne & McLean, 1999). Phylogenetic analyses uli. It is known, however, that individually trained tam- have now revealed that marsupial mammals diverged mar wallabies preferentially associate predators with from placental mammals about 100 million years ago fear (Griffin, Evans, & Blumstein, 2002). Possibly, so- and represent a parallel evolutionary lineage (Springer, cial learning about predators will show a similar bias. Westerman, & Kirsch, 1994). Consequently, the suppo- Behavior of the observer during training, speed of sition that marsupials might be in some way “inferior” to acquisition, duration of acquired responses, latent eutherians is no longer justified. inhibition, and context specificity. As in other species, Australian kangaroos and wallabies (Macropodidae) the vigilancelevels of observer wallabies correlated pos- display clear antipredator responses that involveboth vi- itively with those of their demonstrators during training sual (erect bodypostures and fleeing) and acoustic(alarm (Griffin & Evans, 2003). Observer responses reached foot thumping) cues. Griffin and Evans (2003) investi- maximum levels after two training trials, suggesting that gated the potential of such stimuli to trigger predator social learning about predators is as rapid in marsupials avoidancelearning in tammar wallabies, a medium sized as in all the other species tested to date. However, in wal- (4–7 kg), moderately social kangaroo. First, they en- labies, unlikein rhesus monkeys(Mineka & Cook,1988), hanced the responses of individual wallabies to a taxi- the responses of observers declinedover the course of two dermically prepared model predator (fox, Vulpesvulpes) subsequent training trials, despite the fact that demon- by presenting it in conjunction with a simulated capture strators continued to respond fearfully to the predator. by a human. After training, the wallabies responded to The duration and context specificityof acquired responses, the fox with high levels of alarm behavior, including as well as the effects of latent inhibition, have not been fleeing and alarm foot thumping.Repeated presentations investigated in marsupials. of the model fox alone were used to habituate another group to the predator. After training, the wallabies in this GENERAL CONCLUSIONS ON SOCIALLY group responded to the fox by briefly orientingtoward it. ACQUIRED PREDATOR AVOIDANCE Both groups of wallabies (fox fearful and fox indiffer- ent) were then used as demonstrators to test whether ac- The propertiesof socially acquired predator avoidance quired responses could be socially transmitted. Naive are remarkably similar across groups (Table 1). The in- observers given the opportunity to watch trained demon- tensity of observer alarm responses increases with the strators respond fearfully to the fox watched the preda- intensity of demonstrator responses during training, ac- tor significantly more after training than did control ob- quisition occurs in one to two trials, and there is prefer- servers that had watched an indifferent demonstrator ential learning about particular kinds of stimuli. These respond to the predator stimulus. properties provide support for the idea that socially ac- Attempts to test whether acoustic alarm stimuli alone quired predator avoidance is mediated by individuallearn- are sufficient to trigger learning have yielded variable re- ing processes and not by any independent social learning sults. McLean, Lundie-Jenkins,and Jarman (1996) showed mechanism (Heyes, 1994; Mineka& Cook, 1993; Suboski that rufous hare wallabies(Lagorchestes hirsutus) watch et al., 1990). First, traditional studies of classical condi- a model fox more after they have experienced it in con- tioning have shown that the intensityof an unconditioned junction with playbacks of conspecific alarm thumps. response (UR) usually increases with that of the US. The However, similar experiments with tammar wallabies positive relationship between observer and demonstrator found no effect of this acoustic signal on learning, but alarm thus supports the idea that social alarm cues function this may have been due to the small number of subjects as USs that evoke URs in observers. Second, it is known in the study (Griffin, 2003). that stimuli associated with arbitrary aversive events, such as an electric shock, can be acquired significantly Content of Learning in one trial and reach asymptotic levels after very few To determine whether socially acquired responses CS–US pairings (Young & Fanselow, 1992). Rapid ac- were specific to the predator with which wallabies were quisition is, therefore, not particular to socially acquired trained, Griffin and Evans (2003) measured responses to predator avoidance but, rather, to fear conditioning in an array of stimuli both before and after training. They general. Third, selective associationsare present not only found that the acquired response was specific to the in socially acquired fear, but also in individually condi- SOCIAL LEARNING ABOUT PREDATORS 137

Table 1 Summary of the Principal Properties of Socially Acquired Predator Avoidance Property Fish Birds Eutherians Marsupials Social cues that trigger Chemical alarm substances Compound visual and Compound visual and Compound visual and learning in observers Visual alarm cues acoustic alarm cues acoustic alarm cues acoustic alarm cues (mobbing) Alarm vocalizations Acoustic alarm thumps Visual cues Alarm vocalizations Cross-species learning Yes Yes Not known Not known Speed of learning One CS–US presentation One CS–US presentation Two CS–US presentations Two CS–US presentations Content of learning Olfactory predator and Visual predator and Visual predator stimuli Visual predator stimuli arbitrary stimuli nonpredator stimuli Visual predator and arbitrary stimuli Habitats Specificity of learning No generalization to No generalization to No generalization to No generalization to nonpredator fish inanimate object inanimate object or nonpredator to morphologically different predator Duration of learning 2 months 8 days 30 days Not known Preferential learning Yes Yes Yes Not known Effect of latent inhibition Not known None None Not known Context specificity of None Not known None Not known acquired responses Observer–demonstrator Positive relationship Positive relationship Positive relationship Positive relationship alarm behavior during training

tioned fear. Rats learn to recognizea tone more readily than ditioningto accommodate for the requirements of learn- a light as a signal for an electric shock. In recent years, ing socially about danger. general models of learning have been adjusted to incor- Despite an overall similarity, there are some species porate parameters accounting for stimulus associability. differences in the properties of socially acquired predator Consequently, preferential associations are not consid- avoidance (Table 1). In fish, one presentation of a preda- ered to reflect any specialized learning process. tory CS together with a chemical alarm US appears to Only one property points to a difference between clas- induce robust antipredator behavior. Propagation occurs sical fear conditioning and socially acquired predator along chains of individuals with no apparent decline in avoidance.In both blackbirds and rhesus monkeys, prior either demonstrator alarm or learned responses (Suboski habituation to the CS does not seem to affect subsequent et al., 1990). In contrast, in rhesus monkeys, one training acquisition of a fear response to that stimulus (Curio trial induces fear responses that are less robust than those et al., 1978; Mineka & Cook, 1986). In contrast,CSs that induced by two training trials. In addition, even though signal the absence of a frightening US in classical aver- responses acquired in two trials are retained longer, they sive conditioning do not subsequently acquire control are not resistant to extinction.Fear acquired by observers over conditioned fear (Young & Fanselow, 1992). The tends to decrease when these individuals are used as idea that socially acquired avoidance might not be af- demonstrators for another set of naive observers (Cook fected by phenomena known to influence the likelihood et al., 1985). In blackbirds, the situation is somewhat in- of classical conditioning is consistent with the results of termediate. Although one-trial learning appears to lead other studies of social learning (Galef & Durlach, 1993). to robust responses that can be transmitted along chains Tests of the effect of CS–US presentation order might with no apparent decline, subjects show lower responses reveal another difference between individually and so- during their use as demonstrators than immediately after cially acquired fear. It is known that backward condi- training (Curio et al., 1978). It is not known whether so- tioning,in which the US is presented before the CS, does cially acquired fear responses are resistant to extinction not always lead to conditionedfear responses (e.g., Kalish, in tammar wallabies, because there have been no chain 1967; but see Arcediano & Miller, 2002). One might pre- transmission experiments with wallabies. There is some dict that this order of presentation should have no effect evidence, however, that observer responses tend to reach on socially acquired predator avoidance, because it em- maximum levels after two training trials and to decrease ulates a natural situation in which an individual first ob- over the course of further training sessions (Griffin & serves an alarmed conspecific and then identifies the Evans, 2003). Together, these results suggest that the so- source of alarm. Future studies are needed to test whether cial acquisition of fear in fish is rapid and robust. Other evolutionhas modified other properties of classical con- species may require more numerous, more varied, and/or 138 GRIFFIN more temporally spaced out learning opportunities for tality rates of hatchery-reared young are considerably acquisition to be robust. Interactions between social and higher than those of wild-reared individuals (Maynard, individual learning might also consolidate information Flagg, & Mahnken,1995), and predation is the principal acquired socially,as has been shown for sociallyacquired cause of death (Howell, 1994). Antipredator training has food preferences (Galef & Whiskin, 2001). the potential to make hatchery-reared fish more predator Functional considerations might help explain why aware and, hence, to improve their survival. The design learning may be more robust in some species than in oth- of antipredator training techniques has benefited hugely ers. Intuitively,it seems that predator avoidancelearning from the procedures and findings from basic work on should be extremely rapid and, once acquired, should al- predator recognitionlearning(C. Brown & Laland, 2001). ways be retained. On the other hand, one might predict In particular, the findingsthat (1) sociallyacquiredpreda- that learning shouldbe fast and lead to permanentchanges tor avoidance is widespread, (2) social training can lead in behavior only if social alarm cues are reliably associated to recognition of target predators, (3) acquired predator with danger and threat is very high. As risk decreases, awareness can propagate through a population, and opportunity for repeated learning trials increases, par- (4) learning enhances the likelihoodof survival have en- ticularly in social learning that does not entail a direct couraged developmentof antipredatortraining programs. risk to the observer. 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