Alarm Calls As Costly Signals of Antipredator Vigilance: the Watchful Babbler Game

ANIMAL BEHAVIOUR, 2001, 61, 535–543 doi:10.1006/anbe.2000.1636, available online at http://www.idealibrary.com on Alarm calls as costly signals of antipredator vigilance: the watchful babbler game CARL T. BERGSTROM* & MICHAEL LACHMANN† *Department of Biology, Emory University †Santa Fe Institute, Santa Fe (Received 28 January 2000; initial acceptance 9 March 2000; final acceptance 10 August 2000; MS. number: A8703) Alarm-calling behaviour is common in many species that suffer from predation. While kin selection or reciprocal altruism are typically invoked to explain such behaviours, several authors have conjectured that some alarm calls may instead be costly signals sent by prey to inform approaching predators that they have been detected. We develop a general game-theoretical model, the watchful babbler game, in which prey signal awareness to predators. We derive necessary and sufficient conditions for alarm calls to function as honest signals. We show that signals can honestly reveal prey awareness if (1) the prey’s sense of predation risk accurately reflects the probability that the predator is present, and (2) greater awareness of the predator allows the prey a greater chance of escape. When honest signalling is possible, the model predicts that prey will be more willing to signal when predators are common than when predators are rare, and that greater pursuit costs to the predator will allow cheaper signals by the prey. 2001 The Association for the Study of Animal Behaviour Alarm-calling behaviour has provided a persistent puzzle sharing this information, the prey avoids pursuit; by to behavioural biologists. Why should an individual risk receiving it the predator avoids wasting time and energy its own survival to produce costly ‘warnings’ of a preda- in the chase. A prey individual may be ‘undesirable’ for tor’s presence (Maynard Smith 1965)? Evolutionary biol- any of a number of reasons: it may be particularly fast and ogists have typically invoked kin selection and/or skilled at escape, it may be particularly dangerous once reciprocal altruism to explain such behaviours (reviewed caught, it may be of relatively low nutritional value, or it by Hauser 1996, pp. 413–433). While a calling individual may already be aware of the predator’s presence and thus may suffer some direct cost, it may also reap inclusive more likely to escape (or to cause harm to the attacking fitness benefits by warning relatives of danger, or predator) than an unsuspecting prey individual (Hasson anticipate direct fitness benefits from future reciprocity. 1991). Previous theoretical work has focused on the first However, several authors have argued that alarm calls of these reasons, examing ‘quality advertisement’ models may serve an alternative function (Perrins 1968; Smythe in which prey of varying qualities use costly signals to 1970; Zahavi 1977, 1987; Woodland et al. 1980). Calls convey their skill at evading pursuit (Nur & Hasson 1984; may not be directed to conspecifics, but instead to the Vega-Redondo & Hasson 1993; Yachi 1995). Motivated by predators themselves. Hasson (1991) and Caro (1995) the growing literature on signalling of awareness, we review numerous empirical studies testing this class focus in this paper on the last of these possibilities: a prey of hypotheses, and examine the role of signal cost in individual is confronted with imperfect information ensuring signal honesty under such circumstances. about the predator’s presence, and signals its ‘awareness The basic logic of these explanations is as follows. of the predator’ rather than its strength, speed, or other Consider a prey individual that is for some reason an physiological correlates of escape ability. ‘undesirable’ target for a predator. Thus, both the pred- Putative signals of awareness from prey to predator ator and the prey have a common interest in communi- have been described in kangaroo rats (Randall & Stevens cating information about the prey’s ‘undesirability’. By 1987; Randall & Matocq 1997), deer (Caro et al. 1995), lizards (Leal & Rodriguez-Robles 1997; Leal 1999), gup- Correspondence and present address: C. T. Bergstrom, Department of Zoology, University of Washington, Box 351800, Seattle, WA 98195- pies (Godin & Davies 1995), skylarks (Cresswell 1994), 1800, U.S.A. (email: [email protected]). M. Lachmann is at tetras (Brown et al. 1999), primates (Zuberbu¨hler et al. the Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501- 1999), and numerous other species from a diverse range 8943, U.S.A. of taxa (Caro 1995). For illustration, we detail here an 0003–3472/01/030535+09 $35.00/0 535 2001 The Association for the Study of Animal Behaviour 536 ANIMAL BEHAVIOUR, 61, 3 avian example presented by Zahavi & Zahavi (1997, function as honest signals from prey to predator in this Chapter 1), describing several curious features of alarm- game. In the following section, we describe the structure calling behaviour in babblers. When a member of a of this game. We then find the necessary conditions for feeding flock spies a potentially dangerous predator, it existence of an honest signalling equilibrium (see Analy- lets out a shrill ‘barking’ alarm call; the others in the flock sis), and consider how changes in the system will affect may initially dive for cover but often the entire flock joins the equilibrium signalling behaviour. Finally, we describe the initial signaller atop the tree, all loudly issuing alarm the predictions made by the model, discuss the general calls. As Zahavi & Zahavi point out, this behaviour is not conclusions and consider possible extensions (see easily explained by the conspecific-warning theories of Discussion). alarm calling. If the intended receivers of the alarm calls are the other flock members, why do the birds continue THE WATCHFUL BABBLER GAME calling long after the entire flock has assembled and joined the barking? Why do the babblers employ such a A small bird is feeding alone in the bushes when it loud alarm call, which may attract the attention of the catches a glimpse of something soaring overhead. A predator in question, or even the attention of yet unseen hawk? A heron? A falcon? A shadow? A simple trick of predators, when a much softer call would seemingly be the light? Sometimes the small bird, which we will call sufficient to alert the members of the flock? the ‘prey’, gets a good look before its view is obstructed Zahavi & Zahavi conjecture that the answer to these by the bushes and trees of the forest. Other times, it questions is that the alarm calls are actually directed to merely catches a glimpse of a swiftly moving form in the predator, rather than to conspecifics. By barking the sky. loudly, the babblers inform the predator, say, a raptor, In either case the prey can attempt to deter pursuit by that it has been seen, and that any attack will probably be issuing an alarm call, loudly proclaiming that it has seen unsuccessful. Sharing this information is to the advan- the predator (and, thus, implying that it has the knowl- tage of both predator and prey. The raptor does well edge and forewarning needed to escape; see below). How- moving on, and waiting for a chance at unsuspecting ever, such a signal is not without cost. The act of prey; the babblers are better off avoiding the attack even signalling takes time and energy, and exposes the prey to if they are aware of the raptor beforehand (Zahavi & detection and potential pursuit by other ‘secondary’ pred- Zahavi 1997). ators. There are no conspecifics nearby for the prey to If alarm calls actually deter the raptor’s attack, why warn (or to warn the prey, for that matter), so the only would a babbler not gain from calling indiscriminately, function of a signal would be to deter predation. If the even before sighting a predator, on the off-chance that ‘primary’ predator is actually present in the vicinity of the one is present? Zahavi & Zahavi offer an answer to this prey, this predator takes into account any alarm call that puzzle as well: ‘A babbler who would cheat by going to may have been sent, and decides whether or not to the top of the canopy and barking before it saw a predator pursue the prey. would expose itself to raptors it might not have noticed. Of course, no two prey–predator interactions will be That risk helps ensure that if a babbler goes to the top of precisely the same. The sensory stimuli observed by the the tree and declares it has seen a raptor, it has indeed prey will vary from moment to moment. Sometimes the seen one’ (Zahavi & Zahavi 1997, page 5). That is to say, prey will perceive a high likelihood of attack by a pred- if the signal of awareness is sufficiently costly, prey will ator; other times the prey will not realize that a predator benefit from sending this signal only when they are quite is nearby. Furthermore, some situations will afford the certain that they have spotted a predator. predator a better chance of catching the prey than others; While this verbal argument seems plausible, it is diffi- the predator’s chance of successful pursuit will naturally cult to evaluate without a formal mathematical model. vary from one interaction to the next. Similarly, to qualify as a proper hypothesis, the predator- To take these variations into account, we draw two deterrence explanation for alarm calling must make clear random variables at the beginning of each iteration of the predictions (ideally, as specific as possible) based on some game. The stimuli observed by the prey are summarized underlying model of prey-to-predator signalling (Caro by a random variable x. Since these stimuli may depend 1995). Under what circumstances, if any, will this costly on whether the predator is present, x is drawn from one signalling mechanism allow honest communication of distribution when the predator is absent and from a awareness from prey to predator? And how are changes in separate (but overlapping) distribution when the predator the environment (e.g.

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