Social Learning About Predators: a Review and Prospectus
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Learning & Behavior 2004, 32 (1), 131-140 Social learning 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, birds, eutherian mammals, 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-species 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- terns 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, predation 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 pheromones. 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.