The functions of stotting: a review of the hypotheses

Anirn. Behav., 1986, 34, 649-662

The functions of stotting: a review of the hypotheses T. M. C A R O

Sub-department of Animal Behaviour, University of Cambridge, Madingley, Cambridge CB3 8AA, U.K.

Abstract. Eleven, non-mutually exclusive hypotheses have been proposed for the function of stotting. After examining the possible time, energy and survivorship costs of stotting, I review each hypothesis in turn, discussing theoretical objections to them and data that are found to support each one. The Pursuit Invitation hypothesis, Pursuit Deterrence hypothesis, Confusion Effect hypothesis and Stotting-as-play hypothesis are unlikely to be correct on theoretical grounds. There are too few data to support or refute a startle effect of stotting, prey signalling its health, the Social Cohesion hypothesis or alarm function of stotting but all require caveats concerning design features or costs of stotting in order to be strong candidates. There are insufficient data to determine the merits of the Anti-ambush hypothesis of stotting or whether it attracts a mother to her fawn. Circumstantial evidence indicates that mothers may invite predators to pursue them instead of their fawns. The Predator Detection hypothesis remains the strongest candidate for the function of stotting and this is supported by evidence concerning related forms of antipredator behaviour. For each hypothesis, predictions are made concerning the stotting individual, its conspecifics, and the predator.

Predation is presumed to be such a keen selective pressure on prey populations that one would expect animals to have evolved a wide variety of anti-predator responses specifically tailored to the hunting techniques of their most able predators (Curio 1976) and, indeed, the array of anti-predator behaviour found in the animal kingdom is awesome (Cott 1957; Edmunds 1974). It thus seems strange that anti-predator behaviour has been investigated so little, despite the considerable challenge posed by questions of its evolutionary maintenance and origin (e.g. Harvey & Greenwood 1978; Dawkins & Krebs 1979). Perhaps the recent demise of mammalian and avian predators in the western world, brought about by man's activities, has been responsible, in part, for the paucity of quantitative data on anti-predator behaviour (but see Schaller 1967; Kruuk 1972 for tropical studies). Fortunately, however, three types of anti-predator behaviour have begun to receive attention in the last 10 years. First, the assumed costs of alarm calling (Maynard Smith 1965) have been questioned both theoretically (e.g. Charnov & Krebs 1975) and empirically (e.g. Owens & Goss-Custard 1976; Shalter & Schleidt 1977; Shalter 1978) while the benefits conferred on alarm callers have come to be increasingly understood in terms of kin selection (e.g. Sherman 1977; Holmes & Sherman 1983; see Klump & Shalter 1984 for a review; but see Sherman 1985). The second area of inquiry, predator mobbing, is also being seen as benefiting

the mobber's kin as well as increasing individual fitness (e.g. Shields 1984) although the precise effects that mobbing has on predators are still largely unknown (see Curio 1978 for a review). The third type of anti-predator behaviour to receive attention is stotting. The assumed costs of stotting incurred by the performer have generated a great number of hypotheses concerning its possible benefits, but unfortunately very few of these have been tested (but see Bildstein 1983). These hypotheses frequently fail to distinguish whether stotting is a signal to other animals; to whom it may be directed, if at all (e.g. predator or conspecifics); the effect it might have on the predator, if any; and whether the stotting individual, its conspecifics, or both, accrue benefits. The purpose of this paper is to clarify each of these issues in relation to each functional hypothesis and to make explicit the predictions that arise from each one. Until this kind of review is performed, it is virtually impossible to tease out different predictions concerning the function of stotting (many of which are not exclusive) and so enable future research workers to test them (see Curio 1978 for a similar view about mobbing behaviour, and Klump & Shalter 1984 for alarm signals). No one study is likely to be able to test satisfactorily all the competing hypotheses ,but it seems productive to set out the important predictions that require testing in each case. Because information on stotting is limited, data on other

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forms of apparent anti-predator behaviour are used in conjunction with information about stotring. In a subsequent paper (Caro 1986), several of these are tested on free-living Thomson's gazelles

( Gazella thomsoni). DEFINITION

Stotting (named by Percival 1928) is a common kind of jumping seen in many species of Cervidae, Antilocapridae and Bovidac (see Byers 1984). Wahher (1969) describes stotting in Thomson's gazelles as follows. 'With front and hindlegs stiffly stretched downward the gazelle bounces up springing from the pastern joints. Right and left frontleg are close together, and so are the hindlegs. In a very long stotting jump the hindlegs can paddle a little bit in the air, but usually they are kept more or less in the same position as the frontlegs. During the jump all four legs are brought forward slightly so that in landing front and hindlegs touch the ground at about the same time. Then, often the animal jumps again in the same manner, and so a chain of stotting actions results. In stotting the tommy keeps the neck erected. Young animals also erect the tail, adults usually stretch it out horizontally. The white hair of the anal region is ruff‚ From their descriptions, pronking and spronking may be different forms of the same type of behaviour. Other authors provide similar definitions; the essential features of stotting are taking all four legs off the ground simultaneously and holding the legs stiff and straight (see Wittenberger 198 l for a clear photograph of this behaviour). The estimated maximum height gained by Thomson's gazelles during stotting is approximately 50 cm (Walther 1969; Kruuk 1972); F. Walther (personal communication) saw an exceptional stott reach 150 cm from hoof to ground. THE COSTS OF STOTTING Stotting usually occurs when the prey is fleeing from the predator and thus has three possible costs in this context: (1) a time cost, (2) an energy cost, and (3) a survivorship cost. Stotting sometimes occurs in other contexts as well as in the presence of predators (Walther 1969; Guthrie 1971; personal observation), but it probably has different survivorship costs and different benefits in these situations (see Caro 1986).

The time cost of stotting has three components. First, the amount of time that stotting takes up that could be spent in other, more beneficial, activities. This cost is rarely considered in the literature because it is tacitly assumed that stotting always displaces high speed running from the animal's repertoire. Smythe (1970) however, recognizes that stotting need not necessarily occur during chases and that its expression could diminish time spent feeding. It therefore needs to be determined whether stotting always occurs in the context of fast chases and, if not, whether it displaces other more beneficial behaviour patterns. Second, most authors assume that stotting occurs in chases and believe stotting reduces the actor's speed of flight. The near unanimity of opinion appears to be derived exclusively from one source, Estes & Goddard (1967), who believe that gazelles would have a better chance of escape (from wild dog, Lycaon pietus) if they broke into a flat gallop at the beginning of their flight. Yet this notion concerns the probability of capture rather than a reduction in flight speed per se (gazelles may get caught whether they stott or not). In contrast, both Brooks (1961) and Kuhme (1965) write that stotting is deceptively slow, and Walther (1969) states that the length of a stott corresponds to the length of a flat jump seen during fast gallops. The reduction in speed that stotting imposes on fleeing individuals needs to be measured irrespective of whether it occurs in the presence of predators. The third time cost of stotting concerns the possible delay in starting the flight arising from stotting. Walther (1969) has stated that stotting often occurs at the beginning of flights and, although it is recognized that stotting individuals probably move away, rather than towards, the predator, the assumed slow gait of stotting is thought to delay the onset of a fast gallop. In one sense, therefore, this component of time cost is a subset of cost due to reduction in flight speed, except that its effect occurs at the start of a flight and may therefore be dangerous because the prey has had no chance to gain distance from the predator during its run. Quantitative assessment of this delay has never been made. Only three authors have discussed the second, energy cost of stotting. Pitcher (1979) believes the energy expended in stotting could be substantial; Walther (1969) argues that stotting is unlikely to be energetically costly because it can occur in play (Martin 1984 has subsequently shown that energy

Caro: Functions of stotting costs of play may be low); and Huxley & van Lawick (1984) write that stotting might use less energy than running, especially in long flights from wild dogs. The most productive way to measure the energy cost of stotting may be the one proposed by Martin (1982) for play. This is the amount of extra energy required over that needed for metabolism during running, expressed as a proportion of energy required for all activities over a specified time period. This can be written as ECS = &(sMR--rMR)/ADMR where the energy cost of stotting (ECS) equals the metabolic rate during stotting (sMR) minus the metabolic rate during running (rMR), multiplied by the percentage of time spent stotting (t~) during say a week or month, as stotting is seen infrequently in the wild, and divided by the average daily metabolic rate (ADMR). It is worth noting that ungulates do not just run during chases but may also perform long jumps, high leaps or zigzags (Walther 1969; personal observation); thus stotting is only one of several behaviour patterns that imposes energetic costs on fleeing animals. In practice, measuring the energy cost of stotting is likely to be extremely difficult. The third possible cost of stotting is a survivorship cost. Stotting often occurs in the presence of predators and, when the putative time cost is combined with this fact, a survivorship cost is immediately derived: gazelles would escape predators more easily if they did not stott. This is the form of the argument used by Estes & Goddard (1967). Unfortunately such an assumption has never been checked. For example, stotting might impose a time cost by interrupting feeding or by reducing flight speed but nevertheless only be performed in non-dangerous situations, where the prey has little risk of being caught, i.e. outside the flight distance (Hediger 1934), or in situations where conspecifics stood between the gazelle and the predator (C. FitzGibbon, personal communication). The probability of being captured during chases where stotting occurs needs to be compared with the probability of being caught in chases where no stotting occurs. At present, there are no quantitative data to suggest that stotting animals get caught more often than non-stotters. If any of these costs exist, two functional questions are raised. What is stotting for, and who

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benefits? I shall now attempt to summarize the hypotheses concerning the function of stotting.

BENEFITS TO THE INDIVIDUAL

In this review two points should be borne in mind concerning the term function. First, function refers to the particular consequences of stotting which currently increase the actor's chance of surviving and reproducing, and upon which natural selection could act to maintain stotting (Clutton-Brock 1981). However, stotting probably has a number of consequences and hence may be found to have more than one function. Therefore several of the hypotheses put forward could be correct and proving the importance of one hypothesis says little about the applicability of others. In order to tease out each hypothesis to explain stotting, different predictions are made for each one with the underlying assumption that decisions as to when to stott are perfectly matched to their survival value. Second, selection may currently act on a different set of consequences from those for which stotting was originally selected. In other words, its functions may have altered during the course of evolutionary history. Although it is important to distinguish the current utility (function) of certain forms of anti-predator behaviour from their historical genesis (evolution) (Gould & Vrba 1982; see also Lewin 1982; Caro 1985), the benefits of stotting in this paper only refer to current utility and not to historical origin. Predictions listed below without being followed by evidence indicate that there is no such evidence available.

Signalling to the Predator

Hypothesis" 1: pursuit invitation Smythe (1970, 1977) has put forward the hypothesis that prey animals will both reduce predation risk and decrease time spent being vigilant (and so increase time spent feeding) if they can induce the predator to initiate a chase prematurely (see also Percival 1928). Smythe believes that stotting incites predators to pursue their quarry before the predator is sufficiently close to be able to capture the prey. Coblentz (1980) has severely criticized this hypothesis on the grounds that the Pursuit Invitation hypothesis assumes two things: first, that it is less costly to initiate a chase than to move outside the flight distance and continue to monitor the

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predator. As the estimated energy expenditure of running is almost certainly greater than that of standing, one has to assume that time or survivorship benefits derived from inciting a chase result in a large increase in time spent feeding and/or a greatly reduced probability of the predator making a second attempt at prey capture. Neither of these factors has been measured. Second, the hypothesis also requires that predators can be tricked into initiating a chase outside the normal flight distance, but as Coblentz (1980) points out, predators would probably quickly learn to associate stotting with unsuccessful chases and would thus be deterred from continuing the hunt. Given that predators

readily learn about the behaviour of their prey (Curio 1976), it seems unlikely that pursuit invitation could be maintained by natural selection. A number of predictions, many of which have yet to be tested, arise from Smythe's hypothesis. Individuals (denoted as I in Table I) should (I1A) stott at distances that are safe, i.e. outside the normal flight distance for that particular age class (confirmed by two related studies, see next hypothesis), and should not stott when being chased, but only when moving away from a predator that has not yet decided to hunt. (I2) Individuals should stott irrespective of whether they are alone or in groups, and (I3A) should direct any conspicuous

Table I. Summary of predictions made in the text* Individual stotters (I)

(1) (2) (3) (4) (5) (6) (7) (8) (9) (I 0) (11) (12) (13) (14) (I 5) (16) (17) (18) (19) (20) (21)

Stott more at (A) safe distances (B) any distance Stott whether alone or in groups Direct signals at (A) predator (B) conspecifics Stott more when predator is hunting Stott more to predators using concealed approach Most fleers should stott Sick or easy-to-catch prey should not stott Neonates disturbed farther from their mothers should stott more Neonates should stott if disturbed by predators Neonates should escape capture if defended by their mothers Should not stott in short vegetation Stotting should increase with vegetation height Stotting need not occur in presence of predator Should not occur in short flights in high vegetation Stotts should occur towards end of the flight Should stott more to group-hunting, concealed predators Capture rates decrease with increased stotting in tall vegetation Sex difference in stotting in neonates and fawns Stotting occurs (A) more in females (B) equally in both sexes Females stott more in bigger groups Stotting should occur in conjunction with alarm signals

Cunspeciflcs (C) (1) Stott total should increase with more fleers (2) Members of stotting groups should be captured less (3) Conspecifics should flee with the stotters (4) Mothers should go to their fawn and defend it (5) Stotting incites other neonates to stott (6) Conspecifics should flee if they see others stotting (7) More animals should flee when other individuals stott Predators (P)

(1) (2) (3) (4) (5) (6)

Predators should chase (A) stotters (B) non-stotters Predators should make only one hunting attempt Predators should abandon hunting stotters Predators' rate of approach to prey is reduced by stotting Predators should become visibly confused Predators leave the area in response to stotting

* The applicability of these predictions to each hypothesis is shown in a similar table in a subsequent paper (Caro 1986).

Caro." Functions of stotting aspects of stotting at the predator. (I4) If the prey can recognize when predators are hunting, stotting should occur more often-when the predator is hunting than when it is not. Predators (denoted as P in Table I) should (P1A) preferentially chase stotters rather than non-stotters; it is known from qualitative records that stotters are occasionally attacked (see Pitcher 1979). Stotters should not be captured by predators, or at least captured far less often than non-stotters. (P2) Predators should make one hunting attempt only and not return to attack the stotter again. Circumstantial evidence does support the Pursuit Invitation hypothesis in one context. Both Walther (1969) and Kruuk (1972) report Thornson's gazelle mothers running between a spotted hyaena (Croeuta crocuta) and the fawn it was pursuing, or else very close to or alongside the predator. Kruuk also describes gazelles stotting at pursuing hyaenas; I have seen presumed mothers stotting at a spotted hyaena while it was chasing fawns. Thus stotting behaviour in this context could be construed either as pursuit invitation by the female, or as distracting the predator's attention, or also having consequences such as informing offspring of the dangerous nature of the pursuer. Parents of other species show similar behaviour to that described above: some groundnesting birds perform distraction displays, such as feigning a broken wing, which lures predators away from vulnerable offspring (e.g. Simmons 1955; Brown 1962). If fawn survivorship were greatly enhanced by mothers' behaviour despite energy, time and possible survivorship costs to the mothers, then Coblentz's first objection (see above) could in theory be circumvented and parental care of this sort might be favoured. Nevertheless predators should still learn not to pursue the mother and to focus their attention on the fawn alone (as seen in the cheetah, Aeinonyxjubatus, personal observation). In summary, the Pursuit Invitation hypothesis for stotting can only be expected to apply to parents with young fawns. Stotting will only be maintained through invitation if fawns are occasionally saved because predators unsuccessfully pursue the mother because she stotts.

Hypothesis 2: predator detection This hypothesis states that stotting, and related behaviour patterns such as rump patch flashing, serves to inform the predator that it has been

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detected (Bildstein 1983). A more elaborate version of the hypothesis (hypothesis 3: Pursuit Deterrence) states that stotting conveys the message that detection has occurred and that further approach would result in an unsuccessful predatory attack because the predator has been detected prematurely (Woodland et al. 1980). Woodland and colleagues were able to show that eastern swamphens (Porphyrio porphyrio) tail-flick at approaching humans (and so display their white tail feathers) before eventually flying away when the distance between them and the 'predator' becomes less than 20 m. In groups, birds most vulnerable to the predator tail-flicked most; moreover, solitary birds also tail-flicked. When humans approach, white-tailed deer (Odocoileus virginianus) lift their tail to expose its white ventral surface. Bildstein (1983) made predictions about a number of competing hypotheses concerning the function of such tail-flagging. He found that singletons tail-flagged as much as those in groups, flagging was directed towards the human (not other deer), and it was more likely to occur during the first flight and at safe distances from the 'predator'. These findings led him to reject two out of five hypotheses and, of the other three, the Predator Detection hypothesis was best supported b y t h e data. Although tail-flicking and tail-flagging are used as indirect evidence to support or refute some of the predictions made in this paper, it is premature to conclude the benefits derived from these activities are necessarily the same as those derived from stotting because the former activities probably involve little or no time cost and a negligible energy cost, whereas the greater potential cost of stotting could imply greater and qualitatively different benefits. Moreover, the interpretation of tail-flicking by Woodland et al. (1980) is not accepted by Craig (1982), who believes that this activity signals submission to conspecifics.

Hypothesis 3: pursuit deterrence The Pursuit Deterrence hypothesis states that stotting serves to inform the predator that it has been seen and that its chances of capturing the prey are now so low that it is always worth the predator abandoning its hunt. Neither of the two studies quoted under hypothesis 2 can separate the Predator Detection hypothesis from the Pursuit Deterrence hypothesis because the predator was human and did not retreat, nor

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can a study of barking in captive Reeve's muntjac (Muntiacus reevesi) given in response to novel objects (Yahner 1980). For theoretical reasons though, it is difficult to see how pursuit deterrence could operate without being susceptible to cheating. Selection will clearly favour predators who do not embark on hunts that are sure to end in failure, but it will also favour prey who attempt to deceive predators about their ability to escape easily (Bildstein 1983). Prey animals might stott every time they ran anywhere, for example. Cheating notwithstanding, there is another reason why pursuit deterrence is unlikely to be operating: predators might still be expected to try to capture prey that stott because some prey may occasionally misjudge the situation and so not be immune from capture (young prey for instance). F o r both these reasons it is difficult to conceive of situations in which probability of hunting success will be reduced to virtually zero, as required by hypothesis 3. Despite these caveats, it could be argued that a study of the klipspringer (Oreotragus oreotragus) gives a degree of support to hypothesis 3. Klipspringer pairs give loud repeated calls (duets) from high, and presumably, unassailable vantage points after they have successfully fled from an approaching predator (usually black-backed jackals, Canis mesomelas; Tilson & Norton 1981). These authors report that 'In five approaches a jackal closed to within 10 m, rushed out, and just missed catching one of the group. A single call was given four out of five times. After the group had reached safety, the adults immediately gave loud alarm duets. In all 18 situations, the jackal showed no interest in pursuing the group once they reached rocks. Also, as soon as alarm duetting started, the jackal-turned away and left the area'. Tilson & Norton (1981) rejected the notion that klipspringers were warning conspecifics because the population density was low; yet in other, higher density areas (Dunbar & Dunbar 1974; Dunbar 1978) it would be less easy to dismiss this possibility. However, it is not entirely clear whether an attack had or had not yet occurred in the other 13 cases where jackals turned away, which is the information required to distinguish the Predator Detection from the Pursuit Deterrence hypothesis. Hypotheses 2 and 3 both predict the following. (I 1A) individuals should begin stotting outside the flight distance, as a close approach is not necessary to inform the predator it has been seen (Bildstein 1982); this prediction is supported by data from

swamphens and white-tailed deer. (I2) Individuals should stott whether they are alone or in groups (supported by data from swamphens, and for tailflagging in white-tailed deer by Hirth & McCullough 1977; Bildstein 1983; personal observation). (I3A) Signals should be directed at the predator (again supported by Woodland et al. 1980; Bildstein 1983; personal observation). (14) If prey can recognize hunting predators, they should preferentially stott in hunting contexts. In support of this, Smythe (1970) reports eliciting stotting in Dolichots patagonium (Caviidae) at 30-40 m when he rode obliquely towards them, but they would only flee if he rode at them directly (or approached to 20m). According to the Predator Detection hypothesis, (15) prey should stott more to predators using a concealed approach than to other predators; predators using an unconcealed approach will probably be seen by prey most of the time. (P1B) Predators should preferentially chase non-stotters. (P3) From the Predator Detection hypothesis there is no strong prediction as to whether predators will continue their approach but stotters should not usually be captured. According to the Pursuit Deterrence hypothesis, predators should abandon their hunt or change their direction of approach in response to stotting, a prediction possibly supported by Tilson & Norton's (1981) klipspringer study, but not always in other studies (Pitcher 1979). Stotters should never be captured.

Hypothesis 4: prey is healthy An hypothesis related to Pursuit Deterrence states that, by stotting, prey inform the predator they are healthy enough to outrun the predator, and therefore attempts at capture beyond the initial approach will be unrewarding (Zahavi, personal communication to Dawkins, quoted in Dawkins 1.976). Theoretical application of Zahavi's model specifically to stotting (Nur & Hasson 1984) shows that such signalling to predators can evolve and be maintained in a prey population. However the energy cost of stotting must be sufficiently high or else it will be subject to cheating, because if stotting imposes only a negligible energy cost, unfit as well as fit individuals will (try to) stott in order to deceive the predator about their health and so avoid pursuit. There are no data to support or discredit Zahavi's hypothesis. It is not clear as to where prey would be predicted to stott in relation to the predator (I1). Although

Caro: Functions of stotting prey might be expected to stott at safe distances, they might also stott at less safe distances if their health allowed them a good chance of escape (D. Gibbons, personal communication). Predictions (I2 I4) derived from the previous hypothesis also apply to this one. Hypothesis 4 predicts (I6) that, given only one member of a herd will be captured during a hunt, then most fleeing individuals should stott in order that each one can show the predator that it is too healthy to be worth pursuing. In effect, if one individual stotts then all the other potential victims should compete with each other not to be chosen, and stott as well. If the energy costs of stotting are high and stotting is an honest signal of the ability to evade capture then (I7) sick prey should not be able to stott. In addition, young or very old individuals should stott less than other age classes because they are poor at evading capture (see Schaller 1972). (P1B) Predators should not hunt stotting gazelles, and (P3) should abandon hunts in response to stotting or, if all individuals stott, selectively attack low-jumping stotters (Harvey & Greenwood 1978). Predictions such as this last one would be untenable if energy costs of stotting were low and cheats could invade the population.

Hypothesis 5: startle behaviour The Startle hypothesis was put forward to explain abrupt displays of white hair patches in response to predators but it could also apply to stotting. The argument is that the sudden onset of a behaviour, tail-flagging for example, startles the predator, causing it to hesitate momentarily and so allowing the prey extra time to escape, in a similar fashion to protean displays (Humphries & Driver 1967). At the end of the flight the tail is dropped quickly and the prey suddenly appears to blend in with the surrounding vegetation (Edmunds 1974). The Startle hypothesis is unlikely to be relevant to stotting in those species of ungulate that have large rump patches that are always on display (Guthrie 1971), or that jump high when they normally run because, in such cases, predators will have had the opportunity to habituate to both of these conspicuous aspects of stotting. However, the intermittent nature of stotting might preclude rapid habituation, so it is conceivable that the act of stotting could temporarily startle some predators into hesitating especially during the first chases they attempted. Stotting should be shown by individuals (I 1B) at

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all distances from the predator but possibly more when the predator is within the flight distance, i.e. the prey is in real danger of capture. This prediction is not supported by a related study: Bildstein (1983) showed that white-tailed deer flagged more when they fled at greater distances, did not flag when approached from close distances, and some fled to a distance greater than the mean flight distance before tail-flagging. (P4) If the predator's rate of approach towards prey is reduced because of being startled (which seems unlikely in view of the absence of any mention of this in published accounts, and from personal observation), then predictions (I2), (I3A) and (I4) should hold for startle behaviour.

Hypothesis 6." confusion effect If several members of an ungulate group stott simultaneously while fleeing, the predator may become confused (Walther 1969; Bertram 1978). This effect is not restricted to stotting per se: it would also apply if many brilliant white rump patches are seen to move in unpredictable directions (see Guthrie 1971). Jarman (1974) considers that this could be one of the functions of leaping amongst fleeing impalas (Aepyceros rnelampus) and, to reinforce the point, impalas themselves do not stott (M. Murray, personal communication). There is evidence from several species to show that both aquatic predators (see Neill & Cullen 1974; Poole & Dunstone 1976; Ohguchi 1978; Treherne & Foster 1982) and terrestrial predators (Gillett & Gonta 1978) become confused by the activities of their prey. The confusion effect has been stated in three ways. First, stotting or jumping could benefit the individual alone regardless of whether other group members stott. Benefits would be accrued because predators would be unable to follow the animal's unpredictable movements (Humphries & Driver 1967). Such a conservative phrasing of the effect is unusual, as confusion is normally regarded as arising from the activity of several individuals (Milinski 1977). But if the confusion effect requires more than one individual to stott simultaneously, it is difficult to see how it could have evolved: the predisposition to stott would have to arise in a number of individuals at the same time. Nevertheless, it is quite possible that confusion effects could easily have been co-opted from another function of stotting (Gould & Vrba 1982). In the second phrasing of the effect, only a

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certain number of individuals are required to confuse the predator; perhaps only 50% of the group stotting are enough to disorient a predator and cause it to give up. In this case, it is difficult to see how confusing the predator could be immune from cheating because individuals could benefit from the stotting of others without incurring its costs. In its third, strongest form, every group member is required to stott for the confusion effect to operate. Focusing on the second and third interpretations of the hypothesis, (I 1B) individuals are expected to begin stotting at any distance from the predator (not supported by tail-flagging in white-tailed deer). (I2) Individuals should never stott when they are alone because this hypothesized benefit relies on other individuals stotting (or at least fleeing) simultaneously and it would be difficult to argue that anti-predator behaviour shown by individuals found alone was merely 'carried over' from the group context. If the anti-predator bebaviour is presumed to carry costs in every situation then the actor should accrue benefits in the context in which it is shown (but see Craig 1982 for an alternative view). In addition, (I6) most individuals that flee should stott (true for tail-flagging in deer and swamphens), and (I4) prey should usually stott to hunting predators. (C 1) The total number of stotts shown by the group should increase with increasing numbers of fleers; this is supported by observations of stotting spreading contagiously in herds of Thomson's gazelles that are being pursued by wild dogs (Estes & Goddard 1967). (C2) Members of groups in which stotting occurs should be captured less often than members of groups in which less or no stotting occurs. (P5) Predators should become visibly confused when they attack groups that stott. This appears unlikely in view of well reported anecdotal data on hunting in a variety of carnivores: a number of predator species such as the cheetah, (although not the wild dog: Estes & Goddard 1967), appear to pick out their victim from a group before commencing a chase, then relentlessly pursue it no matter what (e.g. Kruuk 1972; Schaller 1972; personal observation).

Signalling to Conspecifics Hypothesis 7." social cohesion McCullough (1969; Hirth & McCullough 1977) has proposed that the function of tail-flagging,

which normally exposes the white rump patch, is to act as a signal to conspecifics to group together in the face of a predator and so accrue group-related benefits (Bertram 1978). Although the hypothesis was initially proposed for individuals in cryptic species signalling the necessity to group together when they had been detected by a predator, it is also claimed to operate in species that have white patches displayed permanently: individuals are supposed to signal continuously to conspecifics about the importance of forming groups (Hirth & McCullough 1977). Benefits for the individual from being in a group could arise from dilution effects (if only one prey individual is captured: e.g. Mech 1970; Malcolm & van Lawick 1975); from deterring the predator because of group defence (Mech 1970) or mobbing (see Curio 1978); from avoiding detection if animals can hide behind others (Estes 1976); or from avoiding being on the periphery of the group (Hamilton 1971); see Bertram (1978) for a review. Rather weak supportive evidence for the hypothesis is claimed by Hirth & McCullough who showed that nearly all white-tailed deer groups tailflagged, be they male or female groups, whereas significantly more female groups alarm snorted. This was said to support the Social Cohesion hypothesis because tail-flagging was unlikely to have an alarm function like snorting (presumably maintained by kin selection, see below) and it refuted Guthrie's (1971) hypothesis concerning the role of white rump patches used in intraspecific encounters. It would be unwise to use this evidence alone to support hypothesis 7. Other reasoning speaks against stotting being a signal to individuals to form a group. Both stotting and tail-flagging are probably directional forms of communication because the white rump patch or tail is particularly prominently displayed in both activites (Walther 1969; personal observation). A non-directional signal such as an alarm call would probably be a far better promoter of group cohesion than a visual signal, especially in wooded areas where visibility is low (D. Gibbons, personal communication). In a slightly modified variation of the theory, McCullough (personal communication to Bildstein, quoted in Bildstein 1983) proposed that deer tail-flag in order to bring individuals together to form a group, rather than keep them together as in the previous version. This form of the Social Cohesion hypothesis predicts (I2) that solitary

Caro: Functions of stotting individuals will tail-flag (as well as those in groups predicted by the previous version). Bildstein (1983) showed that solitary white-tailed deer do tail-flag to approaching humans and was therefore unable to refute the hypothesis. How observations on tailflagging might relate to stotting with respect to this hypothesis remains unclear. Other predictions are as follows. (I3B) The signal should be directed at conspecifics in the presence of a predator (not supported by Bildstein 1983) and possibly after the signalling individual has passed them by as suggested by Harvey & Greenwood (1978), and (I4) should occur in hunting situations. (C2) Members of groups should be captured less often than solitary individuals. In support of this, Schaller (1972) showed that lions (Panthera leo) had a higher success rate hunting solitary Thomson's gazelles, wildebeest (Connochaetes taurinus), or zebras (Equus burchelli) than they did hunting groups of intermediate size. (C3) Conspecifics should flee with the stotter (version 1), or move to it and flee together (version 2).

Hypothesis 8: attracting the mother's attention Many species of ungulates hide their neonates in tall vegetation during the first weeks of life ('hider' species: e.g. Underwood 1979; see Lent 1974 for a review), while the young of other species accompany their mothers at heel ('follower' species). Typically, hidden neonates will not move from predators unless the predator approaches very close to where they are hidden. It has been suggested that stotting in Thomson's gazelle neonates serves to inform the mothers that their offspring are changing hiding positions in response to disturbance (R. Estes, personal communication). Such disturbance is usually caused by predators because fawns rarely move unless they are approached by their mothers, and other herbivores normally avoid them (Walther 1969; Kruuk 1972). A second suggestion is that stotting in a neonate or fawn attracts the mother's attention so that she will come to its aid. Thomson's gazelle mothers, and even other females (Estes 1967; Kruuk 1972) are known to defend fawns against black-backed and golden jackals (Canis aureus) (Estes 1967; Wyman 1967; Walther 1969; Packer 1983). Also, mothers are thought to try to attract the predator's attention away from their fawns by repeatedly running obliquely across the line described between the fleeing fawn and the predator pursuing it (Walther 1969; Kruuk 1972; see discussion under hypothesis 1).

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This Attention Attracting hypothesis predicts that (18) neonates disturbed from their hiding place should stott more the further they are from their mothers. (I9) In the first proposal, disturbed neonates should stott regardless of the cause of disturbance as they are signalling their whereabouts to their mother. In the second proposal, they should only stott if disturbed by predators (assuming they can recognize a predator) because they are calling for their mother's aid. (I10) Fawns defended by their mothers should escape capture more often (supported by Wyman 1967) than those receiving no aid, and fawns should more often escape if their mothers run in front of the predator. The young of follower species should, of course, not stott. (C4) Mothers should move to the neonate if it stotts (first proposal) and (second proposal), should defend it against predators after it stotts. Signalling not Involved

Hypothesis 9: anti-ambush behaviour Steinhardt (1921) and subsequently Pitcher (1979) proposed that the height gained during stotting allowed individuals to check more accurately the surrounding vegetation, and the vegetation along their flight path. Although this hypothesis has not been tested, the springbuck (Antidorcas marsupialis) lowers its head towards the ground while pronking, which probably limits visual orientation. The predictions concerning this hypothesis are as follows. (I11) Individuals should not stott in short vegetation. (I12) Stotting should increase with vegetation height, and (I3) should not necessarily occur in the presence of predators. Both these predictions are supported by Schaller's (1967) observations of Indian blackbuck (Antilope cervicapra) which were seen to stott through patches of long grass in the absence of predatory attack. (I 14) If it is assumed that individuals are constantly monitoring surrounding vegetation for predators, then stotting should be less likely to occur in short flights (in medium-high vegetation at least) because the prey already knows this area is predator-free. (115) For similar reasons, stotts should occur more frequently towards the end of a flight when prey move into a new area (partially supported by the description provided by Walther 1969). (I16) Individuals should stott more in response to species of predators that use a concealed approach and that normally hunt in groups, because social predators are more likely to have

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concealed conspecifics lying in wait than are asocial predators. Finally, (I17) prey individuals should escape capture more easily in medium or tall vegetation the more they stott.

B E N E F I T S TO O T H E R I N D I V I D U A L S Signalling to Conspecifics

Hypothesis 11: warning conspecifics Hypothesis 10: play Hypothesis 10 is not a functional hypothesis in the strict sense; it states that stotting is a form of play, another activity with no obvious short term benefits (see Martin & Caro 1985 for evidence relating to the functions of play). Earlier this century, hunters referred to adult stotting as being a category of play. However such an hypothesis can probably be dismissed because adult ungulates rarely show other forms of play. Immature ungulates stott in the presence of predators but they also stott in the context.of play as noted by Estes (1967) and Walther (1969). Play is a category of behaviour observers find relatively easy to distinguish from other types of behaviour (Caro et al. 1979), and it normally comes to an abrupt halt in hazardous situations (Fagen 1981). The fact that both adult and juvenile stotting does occur in response to predators and not at predictable times of day like most aspects of ungulate play (Byers 1984), indicates that stotting in the presence of predators is unlikely to be a category of play. To demonstrate that all stotting in young ungulates is play would be particularly difficult because it would require proving a negative, and showing that none of the other hypothesized functions applied to stotting. Yet if stotting were play, it might have some of the features of others forms of play in ungulates, such as being more likely to occur after rain or when immatures are wellnourished (Muller-Schwarze et al. 1982). Specifically, (I18) there might be a sex difference in stotting among fawns, as has been found for aspects of play in Siberian ibex kids (Capra ibex: Byers 1977) and bighorn sheep (Ovis eanadensis: Berger 1980). (C5) Stotting in one individual might be contagious and incite other young to stott at the same time (as reported by Walther 1984), so it would be more likely to be shown by pairs or groups of fawns than by single ones (see Byers 1984). These predictions refer to stotting only in the presence of predators, however. There is no reason to suppose that immature gazelles do not stott in the context of playful interactions when predators are absent, and they may show sex differences or contagious effects in this context.

This hypothesis proposes that individuals stott to warn conspecifics of the predator's presence (Estes & Goddard 1967). Such altruism is only likely to be favoured between close kin (Hamilton 1964) or in situations where unrelated individuals are known to each other and repeatedly interact over a protracted time period (Trivers 1971). In ungulate groups containing very large numbers of individuals, alarm behaviour could probably only spread by kin selection (but see below). Ungulates have a well developed vocal and, possibly, behavioural repertoire of what are thought to be alarm signals. In contrast to many alarm signals, however, stotting is often a repetitive activity and for this reason Pitcher (1979) has correctly questioned its role in warning others of danger. Bildstein (1983) pointed out that alarm behaviour could theoretically be divided into risk-free and risk-prone alarm signals, the former conferring no survivorship cost on the sender in the presence of a predator. (I1A) If stotting does impose a survivorship cost, individuals should only stott at safe distances (greater than average flight distance) from predators (supported by evidence from swamphens) and provided kin are nearby (supported by white-tailed deer), Only the first animal to see the predator should stott. (12) Alarm signals that increased the signaller's rate of capture would be unlikely to occur if the animal was alone. Yet tail-flagging in white-tailed deer was found to occur both in groups and in singletons; Bildstein (1983) could thereby refute his risk-prone alarm signal hypothesis for tail-flagging (but not the risk-free signal function). (I3B) Signals should be directed at conspecifics rather than at predators (not supported by tail-flagging in white-tailed deer, which direct the signal to humans and not conspecifics). (I19A) Stotting should occur in female ungulates but not in males because members of female groups are more likely to be related to each other due to differential dispersion of the sexes (Greenwood 1980). This prediction is not supported for tailflagging in white-tailed deer where most animals flag (Hirth & McCullough 1977). (I20) Females should stott more in bigger groups because they can help more relatives escape danger (see Cheney & Seyfarth 1981), or more during the breeding

Caro: Functions ofstotting season when they have young to protect (Curio 1975). (I21) Stotting might occur as an alternative to auditory alarm signals, such as snorting (M. Murray, personal communication), when it is windy or during the heat of the day when auditory signals are difficult to detect (Waser & Waser 1977; Klump & Shalter 1984). Stotting should also occur in conjunction with other probable alarm signals like foot-stamping (Walther 1969) or flank-flashing (Brooks 1961; Estes 1967) if it increases the probability that a warning signal will be perceived by conspecifics. (C6) Conspecifics should flee or increase vigilance (M. Borgerhoff Mulder, personal communication) upon seeing another animal stott. (C7) More animals should flee when other group members perform more stotts, because the certainty of hidden danger is increased. All of these predictions assume stotting to be an altruistic warning signal, but it could be used in a manipulative way, alerting conspecifics regardless of kin (Charnov & Krebs 1975). If the predator moves out of the signaller's view, the behaviour of alerted conspecifics could provide the signaller with valuable information about danger if others can see the predator from their positions (M. Murray, personal communication). (P6) In addition, alerting conspecifics to the predator could provide benefits for the individual if it ensured that the predator left the area to hunt elsewhere because so many prey animals were aware of its presence. A warning function mediated through individual selection has at least one different prediction from that mediated through kin selection: (I19B) stotring should occur in both sexes equally often.

CONCLUSIONS Five points are relevant to the hypotheses put forward to explain the functions of stotting. First, the issue of multiple benefits needs reiteration. Stotting probably has a number of consequences and could confer a number of benefits on the individual and its conspecifics and so incremently affect reproductive success of many individuals. It may be difficult to decipher the most important consequences by which stotting is currently maintained within the population. Second, it is clear that no single test is likely to refute a particular hypothesis alone. Rather, several different tests will generally be required,

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each of which excludes one of the several predictions made by each hypothesis and thus narrows the range of plausibility. The third point is that the function, or functions, of stotting may change as an individual grows older (e.g. Oppenheim 1980) or as its reproductive state changes. Some of the proposed functions may only apply during certain stages of the animal's life history, as is the case of the Play hypothesis for example, since it is known that adults play little. Functions could also differ between gazelle mothers stotting in front of a cheetah which was pursuing their fawn, and adult females in a large herd stotting at an approaching cheetah. Fourth, the function of stotting may differ according to which species of predator is involved. It would be foolhardy to generalize the importance of different consequences of stotting across predators that use a wide variety of hunting techniques, without repeated observations of stotting in response to each species' different style of predatory behaviour. Finally, results from one species cannot necessarily be assumed to apply to other species or other possibly related forms of behaviour. Stotting in open country species may serve a different function from that in woodland species. Stotting in species with white rump patches may have different consequences in species that lack those markings. Last, the causes and consequences of stotting could be quite different from apparently functionally similar behaviour such as tail-flagging or tail-flicking in other species, which makes comparisons between studies difficult. One of the most urgents tasks in the study of stotting is to quantify its exact costs so that we can understand the approximate magnitude of the proposed benefits. The three types of time cost and possibly the survivorship cost are likely to be relatively easy to measure; the energy cost will be more difficult because stotting probably involves only an incremental increase in metabolic rate above that of running. It may be more practical to assume that stotting requires similar amounts of energy to that of jumping or leaping and thereby make use of energy estimates of these activities taken from other studies. This review suggests that hypotheses for the function ofstotting are on a continuum of plausibility which can be divided approximately into five levels, based on a combination of theoretical reasoning and available data.

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(1) In all age-classes except mothers, pursuit invitation is unlikely to maintain stotting in a population because it requires the predator making only one predatory attempt and relies on the predator's inability to learn what stotting signifies. The Pursuit Deterrence and Confusion Effect hypotheses appear untenable on theoretical grounds because both are subject to cheating. Individuals could lie about their chances of escape and might fail to stott if stotting by only a certain proportion of group members led to predator confusion. Stotting being play appears unlikely as play normally terminates in the presence of predators. (2) The startle effect of stotting cannot be tested because data are lacking but it seems improbable that stotting could startle a predator given that sudden jumping or turning often occurs in flights anyway. There is no information on prey signalling their health to the predator by stotting but this hypothesis requires stotting to have a high energy cost in order to be immune from cheating. The Social Cohesion hypothesis could apply to stotting but supporting evidence is weak and there are arguments against the use o f a visual signal in this context. The repetition of behaviour involved in stotting is not one of the usual design features of alarm signals. Furthermore if the alarm function of stotting is maintained by means other than through kin selection, it must be shown that the predator leaves the area in response to stotting. However all four hypotheses require additional data to be tested satisfactorily. (3) There is insufficient evidence to support or refute the Anti-ambush hypothesis, or whether stotting attracts a mother to her fawn. (4) Circumstantial evidence supports the notion that mothers may invite predators to follow them, rather than follow their fawns, but it is unclear whether predators follow stotting mothers or are distracted by them. (5) There are no theoretical grounds for dismissing the idea of stotting being a behaviour that informs a predator it has been detected, and evidence concerning other aspects of anti-predator behaviour lends credence to this hypothesis. Indeed, predator detection rather than deterrence or invitation seems intuitively correct because the decision to continue to approach prey or to give up a hunt rests with the predator, not with the prey. However, all l 1 hypotheses require data to support or refute them convincingly.

ACKNOWLEDGMENTS Support from the Max-Planck [nstitut f/.ir Verhaltensphysiologie provided the impetus for writing this review, By chance, a Royal Society travel grant gave me the opportunity to see white-tailed deer tail-flag in the wild. I thank Monique Borgerhoff Mulder, Clare FitzGibbon, David Gibbons, Martyn Murray, Fritz Walther and two referees for thoughtful comments and helpful suggestions on the manuscript. REFERENCES Berger, J. 1980. The ecology, structure and function of social play in bighorn sheep (Ovis eanadensis). J. Zool. Lond., 192, 531-542. Bertram, B. C. R. 1978. Living in groups: predators and prey. In: Behavioural Ecology: An Evolutionary Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 6496. Oxford: Blackwell Scientific Publications. Bildstein, K. U 1982. Response of northern harriers to mobbing passerines. J. Field Ornithol., 53, 7-14. Bildstein, K. L. 1983. Why white-tailed deer flag their tails, Am. Nat,, 121, 709-715. Brooks, A. C. 1961. A Study of the Thomson's Gazelle (Gazella thomsonii Gunther) in Tanganyika. Colonial Research Publication no, 25. London: Her Majesty's Stationery Office. Brown, R. G. B. 1962. The aggressive and distraction behaviour of the western sandpiper Ereunetes mauri. Ibis, 104, 1-12. Byers, J. A. 1977. Terrain preferences in the play behavior of Siberian ibex kids (Capra ibex sibiriea). Z. Tierpsychol., 45, 199-209. Byers, J. A. 1984. Play in ungulates. In: Play in Animals and Humans (Ed. by P. K. Smith), pp. 43-65. Oxford: Blackwell Scientific Publications. Caro, T. M. 1985. Intersexual selection and cooption. J. theor. Biol., 112, 275-277. Caro, T. M. 1986. The functions of stotting in Thomson's gazelles: some tests of the predictions. Anita. Behav., 34, 663-684. Caro, T. M., Roper, R., Young, M. &Dank, G. R. 1979. Inter-observer reliability. Behaviour, 69, 303 315. Charnov, E. L. & Krebs, J. R. 1975. The evolution of alarm calls: altruism or manipulation? Am. Nat., 109, 107-112. Cheney, D. L. & Seyfarth, R. M. 1981. Selective forces affecting the predator alarm calls of vervet monkeys. Behaviour, 76, 25-61. Clutton-Brock, T. H. 1981. Function. In: The Oxford Companion to Animal Behaviour (Ed, by D. McFarland), pp. 220-223. Oxford: Oxford University Press. Coblentz, B. E. 1980. On the improbability of pursuit invitation signals in mammals. Am. Nat., 115,438-442. Cott, H. B. 1957. Adaptive Coloration in Animals. London: Methuen. Craig, J. L. 1982. On the evidence for a 'pursuit deterrent" function of alarm signals of swamphens. Am. Nat., 119, 753-755.

Caro: Functions o f stotting Curio, E. 1975. The functional organization of antipredator behaviour in the pied flycatcher: a study of avian visual perception. Anim. Behav., 23, 1 115. Curio, E. 1976. The Ethology of Predation. Berlin: Springer-Verlag. Curio, E. 1978. The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Z. Tierpsychol., 48, 175 183. Dawkins, R. 1976. The Selfish Gene. Oxford: Oxford University Press. Dawkins, R. & Krebs, J. R. 1979. Arms races between and within species. Proc. R. Soc. Lond. B, 205,489-511. Dunbar, R. I. M. 1978. Competition and niche separation in a high altitude herbivore community in Ethiopia. E. Afr. Wildl. J., 16, 183 199. Dunbar, R. I. M. & Dunbar, E. P. 1974. Social organization and ecology of the klipspringer (Oreotragus oreotragus) in Ethiopia. Z. Tierpsychol., 35, 481-493. Edmunds, M. 1974. Defenee in Animals. Harlow, Essex: Longman. Estes, R. D. 1967. The comparative behavior of Grant's and Thomson's gazelles. J. Mammal., 48, 18%209. Estes, R. D. 1976. The significance of breeding synchrony in the wildebeest. E. Afr. Wildl. J., 14, 135-152. Estes, R. D. & Goddard, J. 1967. Prey selection and hunting behavior of the African wild dog. J. Wildl. Mgmt, 31, 5~70. Fagen, R. 1981. Animal Play Behavior. New York: Oxford University Press. Gillett, S. D. & Gonta, E. 1978. Locust as prey: factors affecting their vulnerability to predation. Anim. Behav., 26, 282-289. Greenwood, P. J. 1980. Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav., 28, 1140-1162.

Gould, S. J. & Vrba, E. S. 1982. Exaptation: a missing term in the science of form. Paleobiology, 8, 4-15. Guthrie, R. D. 1971. A new theory of mammalian rump patch evolution. Behaviour, 38, 132-145. Hamilton, W. D. 1964. The genetical evolution of social behaviour. I, II. J. theor. Biol. 7, 1 52. Hamilton, W. D. 1971. Geometry for the selfish herd. J. theor. Biol., 31, 295 311. Harvey, P. H. & Greenwood, P. J. 1978. Anti-predator defence strategies: some evolutionary problems. In: Behavioural Ecology: An Evolutionary Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 129 151. Oxford: Blackwell Scientific Publications. Hediger, H. 1934. Zur Biologic und Psychologic der Flucht bei Tieren. Biol. Zbl., 54, 21-40. Hirth, D. H. & McCullough, D. R. 1977. Evolution of alarm signals in ungulates with special reference to white-tailed deer. Am. Nat., 111, 31-42. Holmes, W. G. & Sherman, P. W. 1983. Kin recognition in animals. Am. Seient., 71, 46-55. Humphries, D. A. & Driver, P. M. 1967. Erratic display as a device against predators. Science, N.Y., 156, 17671768. Huxley, E. & van Lawick, H. 1984. Last Days in Eden. London: Harvill Press. Jarman, P. J. 1974. The social organisation of antelope in relation to their ecology. Behaviour, 48, 215 267. Klump, G. M. & ShaRer, M. D. 1984. Acoustic behaviour

661

of birds and mammals in the predator context. Z. Tierpsychol., 66, 189-226. Kruuk, H. 1972. The Spotted Hyena: a Study o f Predation and Social Behavior. Chicago: University of Chicago Press. Kuhme, W. 1965. Freilandstudien zur Soziologie des Hyaenenhundes (Lycaon pictus lupinus Thomas 1902). Z. Tierpsychol., 22, 495-541. Lent, P. C. 1974. Mother-infant relationships in ungulates. In: The Behaviour of Ungulates and its Relation to Management (Ed. by V. Geist & F. R. Walther), pp. 1455. Morges, Switzerland: International Union for the Conservation of Nature. Lewin, R. 1982. Adaptation can be a problem for evolutionists. Science, N.Y., 216, 121~1213. McCullough, D. R. 1969. The tule elk: its history, behavior, and ecology. Univ. Calif. Publ. Zool., 88, 1 209. Malcolm, J. R. & van Lawick, H. 1975. Notes on wild dogs (Lycaon pictus) hunting zebras. Mammalia, 39, 231-240. Martin, P. 1982. The energy cost of play: definition and estimation. Anita. Behav., 30, 294-295. Martin, P. 1984. The time and energy costs of play behaviour in the cat. Z. Tierpsychol., 64, 298 312. Martin, P. & Caro, T. M. 1985. On the functions of play and its role in behavioral development. Adv. Study Behav., 15, 59-103. Maynard Smith, J. 1965. The evolution of alarm calls. Am. Nat., 94, 59 63. Mech, L. D. 1970. The Wolf." The Ecology and Behavior of an Endangered Species. New York: Natural History Press. Milinski0 M. 1977. Do all members of a swarm suffer the same predation? Z. Tierpsychol., 45, 373-388. Muller-Schwarze, D., Stagge, B. & Muller-Schwarze, C. 1982. Play behavior: persistence, decrease, and energetic compensation during food shortage in deer fawns. Science, N. Y., 215, 85-87. Neill, S. R. St. J. & Cullen, J. M. 1974. Experiments on whether schooling by their prey affects the hunting behaviour of cephalopods and fish predators. J. Zool. Lond., 172, 549-569. Nur, N. & Hasson, O. 1984. Phenotypic plasticity and the handicap principle. J. theor. Biol., 110, 275 297. Ohguchi, O. 1978. Experiments on the selection against colour oddity of water fleas by three-spined sticklebacks. Z. Tierpsychol., 47, 254-267. Oppenheim, R. W. 1980. Metamorphosis and adaptation in the behavior of developing organisms. Devl Psychobiol., 13, 353-356. Owens, N. W. & Goss-Custard, J. D. 1976. The adaptive significance of alarm calls given by shorebirds on their wintering feeding grounds. Evolution, 30, 392398. Packer, C. 1983. Sexual dimorphism: the horns of African antelopes. Science, N.Y., 221, 1191-1193. Percival, A. B. 1928. A Game Ranger on Safari. London: Nisbet. Pitcher, T. 1979. He who hesitates, lives. Is stotting antiambush behavior. Am. Nat., 113, 453-456. Poole, T. B. & Dunstone, N. 1976. Underwater predatory behaviour of the American mink (Mustela vison). J. Zool. Lond., 178, 395-412.

662

Animal Behaviour, 34, 3

Schaller, G. B. 1967. The Deer and the Tiger." A Study of Wildlife in India. Chicago: University of Chicago Press. Schaller, G. B. 1972. The Serengeti Lion." A Study of Predator-Prey Relations. Chicago: University of Chicago Press. ShaRer, M. D. 1978. Localization of passerine sceet and mobbing calls by goshawks and pigmy owls. Z. Tierpsychol., 46, 260-267. Shalter, M. D. & Schleidt, W. M. 1977. The ability of barn owls Tyto alba to discriminate and localize avian alarm calls. Ibis, 119, 22-:27. Sherman, P. W. 1977. Nepotism and the evolution of alarm calls. Science, N. Y., 197, 1246 1253. Sherman, P. W. 1985. Alarm calls of Belding's ground squirrels to aerial predators: nepotism or self-preservation? Behav. Ecol. Sociobiol., 17, 313 323. Shields, W. M. 1984. Barn swallow mobbing: selfdefence, collateral kin defence, group defence, or parental care? Anim. Behav., 32, 132-148. Simmons, K. E. L. 1955. The nature of the predatorreactions of waders towards humans; with special reference to the role of the aggressive, escape- and brooding-drives. Behaviour, 8, 130 173. Smythe, N. 1970. On the existence of 'pursuit invitation' signals in mammals. Am. Nat., 104, 491~494. Smythe, N. 1977. The function of mammalian alarm advertising: social signals or pursuit invitation? Am. Nat., 111, 191-194. Steinhardt, J. 1921. Vom wehrhaften Riesen und seinem Reiehe. Hamburg: Alster Verlag. Tilson, R. L. & Norton, P. M. 1981. Alarm duetting and pursuit deterrence in an African antelope. Am. Nat., 118, 455~462.

Treherne, J. E. & Foster, W. A. 1982. Group size and antipredator strategies in a marine insect. Anim. Behav., 32, 536-542. Trivers, R. L. 1971. The evolution of reciprocal altruism. Q. Rev. Biol., 46, 35-57. Underwood, R. 1979. Mother-infant relationships and behavioural ontogeny in the common eland (Taurotragus oryx oryx). S. Afr. J. Wildl. Res., 9, 2745. Walther, F. R. 1969. Flight behaviour and avoidance of predators in Thomson's gazelle (Gazella thomsoni Guenther 1884). Behaviour, 34, 184-221. Walther, F. R. 1984. Communication and Expression in Hoofed Mammals. Bloomington: Indiana University Press. Waser, P. M. & Waser, M. S. 1977. Experimental studies of primate vocalization: specializations for long-distance propagation. Z. Tierpsychol., 43, 239-263. Wittenberger, J. F. 1981. Animal SocialBehavior. Boston: Duxbury Press. Woodland, D. J., Jaafar, Z. & Knight, M.-L. 1980. The 'pursuit deterrent' function of alarm signals. Am. Nat., 115, 748 753. Wyman, J. 1967. The jackals of the Serengeti. Animals, 1967, 79-83. Yahner, R. H. 1980. Barking in a primitive ungulate, Muntiacus reevesi: function and adaptiveness. Am. Nat., 116, 157 177.

Received 21 December 1984; revised 22 March 1985; MS. number: 2646)