The functions of stotting in Thomson's gazelles: some tests of the predictions

Anita. Behav., 1986, 34, 663-684

The functions of stotting in Thomson's gazelles: some tests of the predictions T. M. C A R O

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

Serengeti Wildl!/e Research Institute, Tanzania National Parks, e/o P.O. Box 3134, Arusha, Tanzania

Abstract. Stotting in Thomson's gazelles (Gazella thomsoni) was found to have a negligible time cost in slow flights and it was normally shown in safe situations when prey were unlikely to be captured. Despite its probable energy cost and time cost during fast flights there was no evidence to show that, once a chase occurred, stotting gazelles were caught more or less often than gazelles that did not stott. Eleven hypotheses concerning the benefits of stotting were tested using a number of predictions about the stotting individual, its conspecifics and the predator (usually cheetahs), some of which were pertinent to several hypotheses. Although a number of hypotheses were supported by some of the predictions, most were refuted by one or more pieces of evidence. Only two were satisfactorily supported by all of them: stotting appears to inform the predator that it has been detected, but it does not invite or deter the predator from pursuing the gazelle. In neonate Thomson's gazelles, stotting probably has a different function, it informs the mother that the neonate has been disturbed and is in need of defence. In addition, mothers whose neonates escaped capture by cheetahs stotted significantly more during the attempt than mothers whose neonates were caught. Hypotheses concerning the prey signalling its health, startling or confusing the predator; group cohesion; anti-ambush behaviour; play in young animals; warning of conspecifics; and pursuit invitation or deterrence were dismissed by data presented here.

Numerous hypotheses have been proposed for the function of stotting because its performance is thought to incur considerable costs for the actor. However, a review (Caro 1986) has pointed out that the three potential costs of stotting, its time, energy, and survivorship costs, have never been measured, only speculated upon. In this paper, I attempt to measure whether there is a time or survivorship cost to stotting in Thomson's gazelles

hypotheses put forward for the function ofstotting. Because many hypotheses have predictions that are not mutually exclusive, several predictions are tested in each case in order to increase or diminish the plausibility of an hypothesis.

(Gazella thomsoni).

The study was conducted on the long, intermediate and short grass plains in Serengeti National Park, Tanzania (see Sinclair 1979 for a general description) intermittently between July 1980 and December 1983. Observations were made, using 8 x40 Zeiss binoculars at a distance of 5-150 m, from a white, long-wheel-base landrover (442 cm long, 180 cm wide and 205 cm in height; bonnet height was 120 cm). Records were made during all months of the year but only in daylight, i.e. 06301830 hours, and were scored on checksheets by hand. Stotting, defined as vertical leaping with all four legs off the ground simultaneously, with the legs being held stiff and straight (see Walther 1969), was recorded in two different situations: in response to

None of the hypotheses concerning the benefits conferred by stotting has been systematically tested, in sharp contrast to the wealth of theories on the subject (Caro 1986). Data on other, related, forms of anti-predator behaviour (notably those collected by Hirth & McCullough 1977; Woodland et al. 1980; Tilson & Norton 1981; Bildstein 1983) are relevant to stotting in that they illustrate potential functions of anti-predator behaviour and can thereby lend weight or cast doubt on the hypotheses that have been put forward for stotting (Caro 1986), but until predictions concerning stotting per se are tested, it will be impossible to dismiss a particular hypothesis with real certainty. The results presented in this paper test all of the

METHODS

663

664

Animal Behaviour, 34, 3

naturally occurring predators, usually cheetahs (Acinonyx jubatus), and in response to the landrover. In cases where the landrover was used as a 'model predator' it was driven at about 10 15 km/h in second gear towards a group of gazelles. When they fled, the brake was quickly applied, the gear usually disengaged and records were taken. In situations involving the vehicle or a predator, the following measures were recorded.

The Group and Identity of its Members The number, age and sex of Thomson's gazelles in a group were recorded (in a very few cases this included Grant's gazelle, Gazella granti, as well). A group was defined in the following way: of all the nearest neighbour distances between group members, the largest distance was less than half the distance between the two closest members of neighbouring groups. I divided the Thomson's gazelles into five age classes. Neonates (less than 2 weeks old) were very small and dark in colour. Unless nursing, they usually lay concealed at some distance from their mother (Lent 1974). Fawns (2 weeks to 4 months) were larger, dependent offspring whose colour had lightened to that of adults; the height of their backs could reach to the adult's black flank stripe. Small horns were not usually visible but a white mane on the breast was a good field characteristic. (This class corresponded to Walther's (1973) fawn and half-grown fawn categories.) Subadults (5-15 months) consisted of horned animals of both sexes whose horn lengths were less, and whose body sizes were smaller, than those of adults. Subadult males never had the S-shaped horns of adult males. (This class corresponded to Walther's adolescent and subadult categories.) Adults (16 months 12 years) were divided into adult males and adult females. The former were of full body size, with ringed Sshaped horns (Walther's young-adult, adult and old categories). The adult females had thin pointed horns without rings and were of full body size (Walther's adult female and old categories); sex in adults was easy to distinguish (see also HvidbergHansen & de Vos 1971; Robinette & Archer 1971; Walther 1978a). Focal stotting in response to cheetahs was not recorded for neonates (see below). In this study, the possibility of recording the stotting behaviour of the same individual or group on more than one occasion was negligible (see Walther 1969) given the size of the Serengeti

Thomson's gazelle population (0.47 million, Sinclair & Norton-Griffiths 1982), the pattern of migration (Bradley 1977), and conscious efforts not to sample in the same area twice within a short interval.

The Predator The number and identity of the predator (cheetah, wild dog (Lycaon pictus), spotted hyaena (Crocuta crocuta) or jackal, with black-back (Canis mesomelas) and golden jackals (Canis aureus) being lumped together, was recorded. For cheetahs, the type of advance was scored: approach consisted of the cheetah walking towards the gazelle; hunting referred to the cheetah trotting or stalking towards the gazelle or crouching at it; while chasing referred to situations where the gazelle fled from a running cheetah that pursued it. Unless stated otherwise, flights involving chasing were not used in the analysis because, from preliminary observation, it appeared that animals stotted less during chases and I wanted to separate hazardous from non-hazardous situations.

The Stotting Individual The remaining measures given here were only recorded when an animal stotted. The first animal to stott was termed the focal individual. Its age and sex were noted; putative mothers of neonates were excluded from the analysis unless stated otherwise (they were identified by proximity and maternal behaviour towards the neonate). Its activity before it fled was noted. The flight distance (distance from the predator or vehicle to the gazelle when it first started to flee; see Hediger 1934) was recorded (this should not be confused with withdrawal or avoidance distance: Walther 1969). The length of the first flight was recorded. Distances here and in the previous measure were estimated to the nearest 5 m by eye. The observer frequently checked distance estimates against measured distances (20, 30, 50, 100, 200 m) back at home. The flight time was recorded on a stop watch to the nearest s. Subsequently the flight speed was derived from these last two measures. The number of stotts performed by the focal animal during its first flight only was recorded and two measures were derived from this: stotts/m and stotts/s. The flight length was divided into five equal segments by eye and the number of stotts that

Caro: Stotting in Thomson's gazelles occurred in each segment was noted, as well as the distance from the predator that the first stott was given. This distance therefore represents the distance from predator to prey before the gazelle's flight started, plus the length of flight before the gazelle first stotted; in the sample used in this paper, the gazelle usually fled from the predator first, without the predator chasing the prey. The direction the gazelle's white rump faced in relation to the predator when most of the stotts occurred was recorded. It should be noted that gazelles often fled in an inverted J-shaped flight path from the source of disturbance; towards the end of their flight the flank and not the rump patch was frequently directed at the predator. It was therefore by no means certain that the rump was directed at the predator during stotting. If a hunt or chase occurred, its success or failure was monitored. Unless stated otherwise, only unsuccessful hunts were used in the analysis because I wanted to separate situations which were extremely hazardous fi'om those that were less dangerous.

Group Members If there was more than one gazelle in the group, the number of other animals in the group that fled was recorded (later calculated as a percentage of group members) as well as the number of fleers that stotted, aside from the focal animal (later calculated as percentage of fleers that stotted). The total number of stotts exhibited by the whole group was also scored. It was relatively easy to record all the measures given above because several were taken before stotting occurred and usually only one animal in the group stotted.

Analysis In the Results section, predictions derived from each of the hypotheses are separated according to whether they refer to the individual (I), its conspecitics (C), or the predator (P) (see also Caro 1986). Non-parametric tests were used throughout this paper because some sample sizes were very unevenly matched, others were small, and several correlations necessitated the use of Spearman rank order correlation coefficients because one of the variables had an ordinal scale of measurement (estimated distance; Siegel 1956; Bailey 1959). All statistical tests were two-tailed.

665

R E S U L T S AND D I S C U S S I O N

The Time Cost of Stotting There are three components of the time cost of stotting: (a) the degree to which it interrupts other activities, (b) the degree to which it reduces flight speed, and (c) the delay it imposes at the beginning of a flight. Flights in which stotting occurred did not always appear suddenly to interrupt the beneficial activity of feeding. Table I shows the number of cases in which different activities immediately preceded the flight. In most cases individual gazelles were being vigilant, not feeding, before they fled. Smythe (1970) considers that stotting serves to reduce the time that individuals spend alert because it forces the predator to initiate an unsuccessful hunt; this, he argues, would increase the time during which animals could feed. These results show that stotting does indeed interrupt vigilance but not necessarily through its effect on the predator, as Smythe proposes. If stotting imposes a time cost on individuals, it should reduce the rate of flight. However, when focal flights from the vehicle were separated into those that contained stotts and those flights where no stotts occurred, flight speeds did not differ between the two types of flight in either neonates or fawns (Fig. 1). Indeed, the number of stotts was actually found to be positively correlated with the speed of flight of focal animals when they were fleeing from a cheetah ( N = 75, r~= 0.25, P < 0-05, chases included) or from the vehicle ( N = 178, rs = 0'20, P < 0"05); if stotting reduced flight speed, a negative correlation would be predicted. These results suggest that previous estimates of the time costs of stotting have been exaggerated. Apart from Brooks (1961), Kuhme (1965) and Walther (1969), all other authors have tacitly assumed that stotting slows the individual down in flights in which it occurs. The lack of difference in fight speed between flights in which stotting did or did not occur, and the inability to find a negative correlation between flight rate and the number of stotts, suggests one of two things. Either that the act of stotting per se is no slower than running the same distance, corroborated by Walther (1969) who believes that stott length correspondsAo the length of flat jumps seen in a fast gallop, or that stotting is indeed a slow form of travel but only occurs in slow flights; the implication here is that, if

Animal Behaviour, 34, 3

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Table I. Percentage of instances (and number) in which gazelles (neonates excluded) were found in different activities before a flight containing one or more stotts Scanning* Feed Move Rest Surroundings Observer Unknown Total Cheetah

12.0 (9)

1.3 (1)

1.3 (1)

Vehicle

25.6 (22)

1.2 (1)

3.5 (3)

42-7 (32)

6.7 (5) 59-3 (51)

36.0 (27)

100.0 (75)

10.5 (9)

100.! (86)

* Scanning the surroundings and scanning the observer were combined for vehicle tests. fast flights only were considered, an increased number of stotts might reduce flight speed. When chases only were considered, these being flights that were known to be fast, the number of stotts/m was indeed found to be negatively correlated with flight speed ( N = I 0 , r s = - 0 . 6 6 , P < 0 . 0 5 , Fig. 2). The second proposal therefore appears to be correct: stotting is a slow form of travel normally appearing in slow flights. Stotting might impose a cost by delaying the onset of flights if it occurred at the start of flights. However, Table II shows that few stotts occurred in the first fifth of flights either from a cheetah or from the vehicle; stotts occurred more towards the middle or end of a flight. These results partially disagree with Schaller (1972) and also with Walther

1tNst!Nsi

0.18.

r~= =0.66

0.16, 0.140.12 .

~o 0.10o

}-

0.080.06. 0.040.02-

SPEED OF CHASE (m/s)

Figure 2. Stotts/m plotted against flight speed taking only those flights from cheetahs in which a chase occurred (N= 10).

1.0

0.5

*9

0 STO'CFS NO STOTrS STOTI'S NO STOTTS OCCURRED OCCURRED OCCL~RED OCCURRED

NEONATES

FAWNS

Figure 1. Median rate of flights from the vehicle and interquartile ranges made by neonates and fawns in which stotts did or did not occur. (Only in these age categories were a sufficient number of flights recorded in which stotting did not occur.) Mann-Whitney U-tests: neonates, U= 119.5, ys; fawns, z = - 0 . 6 9 , NS. Numbers in bars refer to sample sizes.

(1969) who states that 'stotting occurs predominantly at the beginning or at the end of a flight'. However, Walther qualifies this by writing 'In the beginning it appears only if the pursuer is not too close to the gazelle. If it is very close the gazelle starts in a flat gallop'. Often, short flights that were over quickly were characterized by a high rate of stotting (see Fig. 12) and this may have led these authors to conclude that stotting occurs at the start of flights. Considering all flights together, these short flights would make it look as if stotts occurred at the beginning as well as at the end of (longer) flights. I could not test whether flights that

Caro." Stotting in Thomson's gazelles

667

Table II. Mean sD of the number of stotts performed in each fifth of the flight from a cheetah and from the vehicle Segment of the flight First

Second

Third

Fourth

Fifth

Cheetah(N=76)

0.63_1"18

1.53-t-1.54

Vehicle(N=179)

0-50_+1.06

1.41_+1.69 1.49_+1-78 2.25+2.09

1.91___2-78 2.32__+1.93 2.42_+2.77 3.52_+2.96

In both flights from a cheetah and from the vehicle, Friedman two-way analysis of variance tests were used to test whether the number of stotts in different segments of the flight were significantly different from each other: cheetah, Z2= 51-47, df= 4, P<0.05; vehicle, X2= 187.82, df=4, P < 0.001. c o n t a i n e d stotts were more delayed t h a n those t h a t did not. I n short, the present evidence suggests t h a t stotting does not interrupt feeding, does n o t reduce flight speed in n o r m a l flights, a n d is unlikely to delay flights because it is n o t usually seen at the start of flights. 10 20 30 40 50 60 70 80 90 100

120

DISTANCE FROM C H E E T A H

The Survivorship Cost of Stotting Survivorship costs of stotting were measured by two methods: (1) by examining the expected features t h a t stotting would h a v e if it did impose a survivorship cost, a n d (2) by examining instances of cheetahs catching gazelles that stotted. I f stotting imposes a survivorship cost one would expect it to occur at safe distances from a cheetah. There are several ways 'safe' can be measured as follows.

According to distance from the predator By examining whether stotts occurred beyond the usual flight distances of those flights which subsequently resulted in prey capture. Figure 3 shows the distribution of estimated distances at which the first stott occurred in 72 flights. T h e m e a n distance (_+ sD) was 67.5_+ 31.1 m a n d the m e d i a n distance was 62.5 m (interquartile range 50 75). F o r a cheetah h u n t to end in the successful capture of a T h o m s o n ' s gazelle, the prey must usually be l~ss t h a n a median o f an estimated 20 m f r o m the cheetah at the start of the chase. F r o m a different sample o f cheetah h u n t s for which I had i n f o r m a tion, Fig. 4 shows that the distance at which gazelles fled from cheetahs in flights t h a t ended in capture was significantly shorter t h a n the distance at which gazelles first stotted to cheetahs (taken from a different set o f data; M a n n - W h i t n e y U-test,

140

160

180

200

220

(m)

Figure 3. Frequency o f estimated distances at which the first stott occurred from cheetahs ( N = 72).

I

80-

~-

uJ -i(3 O rr LL

m

tO

F-P

< ~176176

p < o OOl

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60-

4020-

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88

~

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g Figure 4. Median flight distances from cheetahs in hunts where gazelles were or were not caught, and the distance from the cheetah that the first stott occurred (taken from a different data set). Flight distances taken from flights that ended in capture were significantly shorter than those from flights in which prey escaped, z = -5.12, P<0.001. Numbers in bars refer to sample sizes.

Animal Behaviour, 34, 3

668

z = - 5.22, P < 0.001). Thus the first stott normally occurs a b o u t 40 m b e y o n d this critical distance.

By examining whether stotts occurred less often in dangerous situations. Gazelles gave significantly

By examining whether stotts occurred late on in flights. If stotting was dangerous it m i g h t be

fewer s t o t t s / m and fewer stotts/s w h e n they were chased by a cheetah c o m p a r e d with when they were a p p r o a c h e d or h u n t e d by a cheetah (Fig. 6). In s u m m a r y , stotting during flights from predators occurred approximately 40 m b e y o n d the

expected to occur m o r e towards the end o f a flight t h a n at the beginning. As s h o w n above in the section on time costs o f stotting, this was f o u n d to be true (Table II).

By examining whether stotts were more delayed (in terms of distance). One measure o f the delay to

16

stott is to subtract the flight distance from the first stott distance; larger values denote greater delays, W h e n this measure was correlated with flight distance, there was some indication t h a t small flight distances were associated with greater delays (cheetah: N = 7 0 , r ~ = - 0 " 2 0 , NS; vehicle: N = 175, r s = - 0 " 1 9 , P < 0"05).

By situation By examining where stotts occurred in dangerous situations. A l t h o u g h the m e d i a n first stott distance did show an increase with increasing d a n g e r (Fig. 5) there were n o significant differences between the distances that gazelles first stotted w h e n they were chased, h u n t e d or a p p r o a c h e d by a cheetah. This was in c o n t r a s t to the flight distance which was smaller in chase situations because cheetahs were rapidly reducing the distance between p r e d a t o r and prey. Despite starting flight distances close to a cheetah in chases, gazelles stotted far from them.

0 r - - - P < 0.001

P
0.5

~ 0.3

o.1 i

'- P ( 0 . 0 0 1 - - I

2.0P(0.003

100

[-P(O.O9

8O

1.5- t 1.0-

0.50

0 APP

HUNT CHASE

FIRST STOTT DISTANCE

APP

HUNT CHASE

FLIGHT DISTANCE

Figure 5. Median first stott distances and flight distances from cheetahs and their interquartile ranges. Advancing cheetahs were separated into instances of approaching (APP), hunting (stalk, crouch and trot; HUNT), and chasing (CHASE). First stott distances: approached versus hunted, Mann Whitney U-tests, z~l.10, Ns; hunted versus chased, z=0.18, NS; approached versus chased, z = 0.64, NS. Flight distances: approached versus hunted, z = -0"80, NS; hunted versus chased, z = -- 1.73, P<0'09; approached versus chased, z = - 1 - 6 2 , NS. Numbers in bars refer to sample sizes.

APP

HUNT

CHASE

Figure 6. Median measures of stotting performed by gazelles towards cheetahs that approached (APP), hunted (HUNT) and chased (CHASE) them, and interquartile ranges. Number of stotts: approached versus hunted, Mann-Whitney U-tests, z=0.74, NS; hunted versus chased, z = - 1 . 4 2 , NS; approached versus chased, z = - 0 . 9 2 , NS. Stotts/m: approached versus hunted, z = - 0 . 7 6 , NS; hunted versus chased, z = - 3 . 9 8 , P<0.001; approached versus chased, z = - 4 . 2 7 , P < 0.001. Stotts/s: approached versus hunted, z = -0.31, NS; hunted versus chased, z = - 2 . 9 8 , P<0.003, approached versus chased, z = - 3 . 4 4 , P < 0 0 0 1 . Numbers in bars refer to sample sizes.

Caro." Stotting in Thomson's gazelles critical distance at which gazelles were likely to be captured; stotting occurred towards the middle and end of flights; and the first stott was delayed further into the flight when the vehicle or the cheetah was close by when the flight started, a finding supported by Walther (1969). To reinforce this last point, there was some indication that the first stott was delayed in more dangerous situations, when gazelles were chased or hunted by cheetah (see Fig. 5 and Walther 1969). Thomson's gazelles could, without doubt, recognize a cheetah pursuing them and they stotted less in these situations. Stotting appeared to be an activity that occurred towards the end of risk-free flights. The second method of measuring survivorship cost was to determine whether stotting animals were captured more often than non-stotters. A sample of 31 flights from cheetahs (Table III) showed that no stotting gazelle was caught by a cheetah (neonate gazelles are known to be preferentially chosen and easily caught (personal observation) and were excluded; they are dealt with below). Indeed, in response to stotting, cheetahs either abandoned the hunt, or they chased but subsequently failed to capture their quarry significantly more often than they caught it (binomial test, N = 7, P < 0.03). In addition, I could not demonstrate, given that a chase occurred, that stotting individuals were caught more often than adults that did not stott (Fisher exact probability test, P=0-40). To summarize, adult gazelles that stotted were no more likely to get caught than non-stotters, once a chase was initiated. No stotting gazelle was caught in the sample from which I systematically collected data, although neonates were very occasionally caught, and once or twice, during 389years of observations, I saw an adult gazelle that stotted get captured by a cheetah. Results Showed that cheetahs were more likely to a b a n d o n the hunt or

669

fail to catch their quarry in response to stotting. For example, a single territorial male might be approached by a cheetah in open cover, the latter stalking it every time it lowered its head to feed. Adult cheetahs usually freeze in a standing position when their prey looks directly at them or scans the surroundings but, if cheetahs do not halt in time, they can be suddenly sighted by the gazelle. This is the situation in which I frequently witnessed stotting: the gazelle would see the cheetah, run about 15-20 m and stott a variable number of times, and the cheetah would then lie down in a relaxed position, or continue to walk normally towards the prey but not stalking it. The hunt had obviously ended.

The Benefits of Stotting Table VI summarizes the results concerning the hypothesized benefits of stotting found in this paper. A quick glance shows that no one hypothesis is wholly supported, or refuted, by all the predictions. If a prediction is supported, it does not necessarily show that the hypothesis is correct because some predictions apply to several hypotheses. A n u m b e r of predictions need to be supported before an hypothesis gains credence. If a prediction is not supported it could mean three things: the hypothesis is incorrect; the hypothesis only explains the benefits of stotting in certain situations; or it is even possible that the prediction is inapplicable to that particular hypothesis. With these points in mind, I discuss the results pertaining to each hypothesis in turn.

Hypothesis 1: pursuit invitation The Pursuit Invitation hypothesis states that ungulates stott at safe distances in order to make predators initiate an (unsuccessful) hunt prematurely and thus allow the prey to return to feeding

Table IlL Outcomes of 31 cheetah hunts in response to different gazelles (adults, subadults and fawns) that did or did not stott Chase occurred Chase Hunt successful Chase failed abandoned Totals Quarry stotts Quarry does not stott Totals

0 5 5

2 7 9

5 12 17

7 24 31

670

Animal Behaviour, 34, 3

instead of maintaining vigilance (Smythe 1970, 1977). Gazelles should therefore (I1; numbers for this and other predictions refer to Table VI) stott at safe distances from the predator (confirmed above) and (I2) should stott alone as well as when they are in groups. First, I saw single Thomson's gazelles stott to predators numerous times in the course of 389years in the Serengeti, often in situations when no other gazelles were visible at all. Second, gazelles were no more likely to stott to the vehicle when they were in groups than when they were alone (Z2= 0-02, df= l, >as;records were only made in response to the vehicle). Third, there were no differences between focal animals stotting alone (N=34) or in groups (N=41) in the number of stotts, stotts/m, or stotts/s directed at cheetahs (median no. stotts: alone=8.0, groups=7.0, Mann-Whitney U-test, z = - 0 - 8 9 , >as; median stotts/m: alone=0.29, groups=0.30, z=0.32, >as; median stotts/s: alone= 1.21, groups= 1.00, z = -0.74, >as) or at the vehicle (median no. stotts: alone=4-0 (N=9), groups= 7.0 ( N = 171), z-= 1.01, >as; median stotts/m: alone = 0-21 ( N = 9), groups =0.40 (N= 168), z = 1-33, ys; median stotts/ s: alone=0-75 (N=9), groups=0-71 (N=170), z = -0.56, Ns). (I3) The Pursuit Invitation hypothesis would predict that stotting should be specifically directed at the predator. As the white rump patch of a Thomson's gazelle is particularly prominent during stotting (see also Walther 1969), it might be expected that individuals would preferentially direct their rump towards predators. This was found to be true against cheetahs (binomial test N = 86, P<0.001) and against the vehicle (N=179, P < 0.001) when flights of stotting gazelles predominantly displaying their rumps to predators were compared with those in which the flank was displayed to the predator during stotting. (I4) Gazelles should stott more when cheetahs were hunting but there were no differences in measures of stotting in flights from approaching or hunting cheetahs (Fig. 6) despite a possible ability to distinguish between these two sorts of cheetah behaviour as indicated by the somewhat greater flight distances and first stott distances shown to bunting cheetahs (Fig. 5). (P1) Hypothesis l predicts that predators should preferentially chase stotters. Contrary to the hypothesis, I could not show that adult stotting had the effect of making a cheetah take part in a chase more often that it made a cheetah abandon a hunt

(g2= 0'33, df= 1, >as; Table III). Cheetahs, at least, very often appeared to pick out their victim from a group of gazelles before the prey fled, thus they would be unable to use stotting as a cue (personal observation). Young gazelles appeared to be chosen frequently prior to attacks (see also Schaller 1972); indeed groups seemed to he stalked sometimes simply because a neonate suddenly stood up and came into view (personal observation). Thus predatory attempts appeared to be decided on the basis of group composition, not on any measure of stotting. (P2) For Smythe's hypothesis to be supported, predators should not attempt prey capture more than once because of stotting behaviour. Cheetah hunting technique relies on a close approach to unwary prey. I have no quantitative data on the rate at which cheetahs attacked groups of gazelles a second time but it appeared to be very infrequent. An approaching cheetah would make Thomson's gazelles very alert and once the predator had been sighted, vigilance was constantly maintained until the cheetah had disappeared from view. A second attack appeared to be prevented by increased vigilance and had nothing to do with whether a group member stotted or not. The Pursuit Invitation hypothesis is unlikely to be correct on theoretical grounds. Coblentz (1980) has pointed out that predators would quickly come to learn to associate stotting with unsuccessful hunts. The hypothesis also requires that the energy cost of running (let alone stotting), as opposed to standing still monitoring the predator, must be outweighed by substantial benefits; only in the case of females with fawns can this second criticism be challenged because fawn survivorship could, theoretically, be greatly enhanced at relatively little cost to the mother (Caro 1986). To summarize, gazelles stotted at safe distances, whether they were alone or in groups, and they directed their rump patches towards predators. Support for these predictions does not convincingly demonstrate hypothesis 1 to be correct because these predictions apply to several other hypotheses as well (see Table VI). Gazelles did not stott more to hunting than to approaching cheetah, which would lend weight to the hypothesis, but the proximity of a cheetah may of course pose a threaf regardless of its behaviour. I could find no evidence that stotters were caught less often than nonstotters, or that cheetahs picked their victim on the basis of its stotting, both of which are demanded by

Caro: Stotting in Thomson's gazelles the hypothesis. Cheetahs rarely attacked gazelle groups twice but this appeared to be due to enhanced vigilance, not because a gazelle had stotted and thereby initiated an unsuccessful chase. (Results concerning mothers are addressed in hypothesis 8.) Theoretical reasoning and results presented here concerning non-mothers therefore dismiss the Pursuit Invitation hypothesis as a serious candidate for the function of stotting.

Hypothesis 2: predator detection The Predator Detection hypothesis states that stotting serves to inform the predator that it has been seen (Bildstein 1983). Stotting individuals should therefore (I 1) stott at safe distances from predators (confirmed), (I2) stott when they are alone as well as in groups (confirmed), and (I3) direct their rump patches at the predator while stotting (confirmed). (I5) The prediction that stotts should occur more often in hunting situations applies only to the approaching-hunt comparison. Chased gazelles would be expected to stott far less under the Predator Detection hypothesis because cheetahs are already aware that they have been seen (they are chasing their prey!), and gazelles were found to stott less during chases (Fig. 6). However, gazelles did not stott more often to a hunting cheetah than an approaching cheetah (see hypothesis 1), despite a possible ability to discriminate between these two sorts of behaviour (Fig. 5). This finding does not refute the hypothesis because gazelles may need to signal to any cheetah appearing in close proximity that they have seen it. (I5) If, by stotting, the prey is signalling that it has seen the predator, then, once a predator has been seen, prey might be expected to direct more stotts to predators that use concealed approaches to prey (e.g. cheetah) than those that run their prey down without using cover (e.g. wild dog, spotted hyaena and jackals). Figure 7 shows that this was not the case. Although there were no significant differences between the canids and hyaenids, as predicted by the hypothesis, gazelles stotted less to a cheetah than they did to a wild dog (MannWhitney U-test, z=2.26, P<0"03) and showed fewer stotts/m to both wild dog and spotted hyaena (z=3-04, P<0.003; z = - 3 . 0 8 , P<0-002 respectively) than they did to a cheetah. Although these numbers are small and require corroboration, they do support reports of gazelles stotting vigorously to wild dogs (Estes & Goddard 1967; Walther 1969;

671 ,

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Figure 7. Median stotts, stotts/m and stotts/s and interquartile ranges shown in flightsfrom cheetahs (CH), wild dogs (DOG), spotted hyaenas (HY) and black-backed and golden jackals combined (JACK). Numbers in bars refer to sample sizes. H. van Lawick, personal communication) and to hyaenas (Kruuk 1972). However, these results do not necessarily refute the Predator Detection hypothesis because it also predicts that gazelles would stott most to predators that have the highest rates of hunting success and so pose the greatest threat to them. The Detection hypothesis does not make predictions about conspecifics or whether a cheetah should preferentially attack non-stotters. The hypothesis predicts that (P3) those predators

672

Animal Behaviour, 34, 3

whose capture rate depends on closely approaching unwary prey, should usually, but not always, abandon hunting when the prey stotts. Table III shows that cheetahs usually did this, but not invariably, thus strongly supporting the hypothesis. In summary, stotting gazelles were not caught less often than gazelles that did not stott (see above); if one or the other were caught more often, the Detection hypothesis would be falsified. Thus, with two caveats, both of which are open to question on independent grounds, that gazelles signal to a cheetah regardless of its behaviour and that they signal to predators without regard to their hunting method but to some other criterion (perhaps average hunting success of each species), the Predator Detection hypothesis is supported by all the tests made of it. Similar conclusions about other forms of antipredator behaviour have been reached in studies of eastern swamphens (Porphyrio porphyrio) tail-flicking at humans (Woodland et al. 1980; but see Craig 1982), white-tailed deer (Odocoileus virginianus) tail-flagging at humans (Bildstein 1983), and klipspringer (Oreotragus oreotragus) calling to predators (Tilson & Norton 1981). All these studies showed that animals called from safe positions and that signals were directed at the predator. Taken together with the results on stotting presented here, there is growing evidence that one function of several forms of anti-predator behaviour is to signal to predators that they have been detected. C. FitzGibbon (personal communication) has questioned why gazelles should stott at all when being chased; gazelles stott at low rates during chases but stotting is not absent (Fig. 6). One interpretation may be that because gazelles often flee from conspecifics (Walther 1969; personal observation), the act of fleeing itself may be insufficiently unambiguous to inform the predator it has been detected. In support of this, I never saw a cheetah abandon a hunt in response to a quarry that was unaware of its presence yet happened to be fleeing from another gazelle during the cheetah's concealed advance.

Hypothesis 3." pursuit deterrence This hypothesis is a variant of hypothesis 2; it proposes that predators will be deterred from continuing to approach prey once they have been seen (Woodland et al. 1980). Many of the same predictions apply to this hypothesis as to the last:

(I1) stotting should occur at safe distances, (I2) alone or in groups, and (I3) be directed at the predator (all confirmed). (I4) Stotters might be predicted to discriminate hunting from approaching cheetahs but they did not. (15) Stotting did not occur more in response to predators using a concealed approach. As in pursuit detection, these last two findings could be argued in other ways and do not refute the hypothesis. There are two predictions concerning predators. (Pl) Cheetahs should only chase non-stotters, but they did pursue stotting gazelles on some occasions (Table III), and from other, unsystematic observations I noted that gazelles (usually neonates) that stotted were very occasionally captured by cheetahs. Stotting therefore does not absolutely ensure that pursuit will not follow, although it reduces the chances of this occurring for adults. (P3) Predators should always abandon hunts in response to stotting (not confirmed, Table III). Clearly deterrence does not always work and it would be difficult to see how it could without being cheated upon. For prey that could easily be captured there would also be selection to attempt to deter pursuit. Prey might even misjudge their ability to escape. For both these reasons predators would be selected to attempt the capture of stotting individuals occasionally. In short, the Pursuit Deterrence hypothesis, stated in its strong form, cannot be responsible for the expression of stotting in Thomson's gazelles.

Hypothesis 4: prey is healthy Zahavi's hypothesis (personal communication to Dawkins, quoted in Dawkins 1976) is similar to the Pursuit Deterrence hypothesis; it states that individuals stott to inform the predator that they are healthy enough to outrun it. Predictions (I2~4) apply here: gazelles should stott alone and in groups (confirmed); direct rump patches at the predator (confirmed); and stott more during hunts (not confirmed; the rule of thumb again might be 'stott to any cheetah nearby'). Hypothesis 4 predicts (I6) that most fleeing members of a group should stott because each one competes with conspecifics in its attempt to inform the predator that it is not worth pursuing. However, Fig. 8 shows that the percentage of fleers in a group who stotted from a cheetah ()?_+sD=14.6_+28-9~; median 0'0~o, interquartile range 0-14-8~) or from the vehicle ()?_+SD= 5"3 _+18" 1~ ; median 0.0~, interquartile range 0 0~) was usually very low. A

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further prediction is (I7) that sick animals should not stott; I have no data on this. In addition, young gazelles should not stott, or at least stott less than adults because very young gazelles appear to be easy targets for predators (e.g. Kruuk 1972). Table V (see hypothesis 11) shows that young gazelles were more likely to stott in response to the vehicle, rather than less likely as proposed by the prediction, but I have no information on probability of stotting to a cheetah. However, given stotting occurred, I could compare all the age classes of Thomson's gazelles on three measures of stotting to both a cheetah and to the vehicle using M a n n -

673

Whitney U-tests to compare all categories with each other. There were no significant differences between the number of stotts shown by adults ( N = 6 0 , median 7"0), subadults ( N = 7 , median 13.0) and fawns ( N = 5, median 16.0) to a cheetah, nor were there significant differences on the measures of stott/m (medians 0.30, 0-33, 0.32 respectively) and stotts/s (medians 1-12, 1-75, 1.78 respectively). Again no significant differences were found when adults ( N = 9 ) , subadults ( N = 3 7 ) , fawns ( N = 57) and neonates ( N = 7 7 ) were compared on the three measures of stotting in response to the vehicle (median stotts: 8.0, 7.0, 8.0, 7.0 respectively; median stotts/m: 0-21,0.29, 0.40, 0.40; median stotts/s: 0.75, 0.52, 0-83, 0.71), except that neonates showed significantly more stotts/m than adults ( z = - 1 . 9 9 , P < 0 - 0 5 ) and fawns showed more stotts/s than subadults (z = - 2 . 1 7 , P = 0.03). Thus, there may have been a slight tendency for younger animals to stott more frequently than older ones, the reverse of the prediction, but even this was not borne out by consistent statistical differences across any measure. Nevertheless, neonate gazelles may stott for other reasons (see hypothesis 8), so perhaps a better test of the hypothesis would be to check whether stotting neonates were caught less often than neonates that did not stott. F r o m the small number of hunts from which such data were specifically taken, there was no indication that stotting neonates escaped capture more often than non-stotters (Fisher exact probability test, P = 0.80; Table IV). (P 1) Predators should not chase stotting animals (not confirmed), and (P3) should abandon hunts when stotting occurs (not confirmed). In addition, it has already been shown that stotters were not caught significantly less often than non-stotters. I have no data as to whether predators attack individuals that do not stott high off the ground. To conclude, the hypothesis is damaged primar-

Table IV. Outcomes of tO cheetah hunts in response to different neonate gazelles that did or did not stott Chase occurred Chase Hunt successful Chase failed abandoned Totals Quarry stotts Quarry does not stott

1 7

0 2

0 0

1 9

Totals

8

2

0

10

674

Animal Behaviour, 34, 3

ily because so few fleeing members of a group stott in response to cheetahs, implying that they are not informing cheetahs of their comparative health in relation to other gazelles. Also stotters do not get caught less often than non-stotters, and young easy-to-catch gazelles stott as much as adults. (My results confirm Walther's (1969) finding that fawns stott; his assertion that 'stotting is especially often used by fawns' may be based on the high probability that fawns will stott during flights from vehicles (Table V). Taking only flights in which stotting occurred however, there were few consistent differences between age classes.) Zahavi's hypothesis also demands that predators abandon hunts of gazelles that signal their health by stotting but some stotting gazelles were pursued by cheetahs. Primarily for these reasons, but also for the theoretical difficulty that stotting would not be immune from cheating if its energy costs were low (e.g. Caro 1986) because individuals would be selected to stott irrespective of whether they had the ability to outrun the predator or not, the Prey Signalling its Health hypothesis is rejected.

Hypothesis' 5: startle behaviour This hypothesis states that signals given by prey may startle the predator momentarily, allowing the prey extra time to escape. It is unlikely to apply to Thomson's gazelles, which have white rumps permanently displayed, but it is conceivable that stotting startles predators. If so, (I1) stotting should occur at all distances from the predator but more especially when the predator is close. The reverse was found to be true. Animals should stott (I2) alone and in groups, (I3) direct their rumps at predators, and (I4) stott particularly often when hunted. The first two have been confirmed, the last refuted. (P4) Predators' rate of approach should be reduced when their prey stott. I saw no evidence of this; if individuals stotted, cheetahs either abandoned their hunt or, more rarely, continued their advance at a steady pace. If stotting served to startle cheetahs it was not wholly successful, because stotters were very occasionally caught. Lastly, neither I, nor any cheetah I saw were ever visibly startled by stotting. These equivocal results suggest that stotting in Thomson's gazelles does not startle the predator. It is also difficult to see how stotting could startle predators, given that pursued prey normally jump as high as animals that stott (Walther 1969) and that no concealed part of the body is suddenly

revealed by stotting. Although the white rump patch is large (Guthrie 1971), and is prominently displayed during stotting, especially in fawns and neonates, it is always on display. For these reasons the Startle hypothesis seems untenable.

Hypothesis 6: confusion effect With several members of a group stotting simultaneously, the predator might become confused (Walther 1969; Bertram 1978). If this were true, (I1) then gazelles should stott at any distance but more often when they were close to the predator (not confirmed) and especially when being chased; the converse was found to be true. (I2) Individuals should only stott when they were in groups (not confirmed), (I3) should direct their rumps to the predator (confirmed), and (I4) preferentially stott to hunting predators (not confirmed). In addition, (16) most members of a group who fled would be expected to stott but the percentage of fleers that stotted was normally very low (Fig. 8). (C1) If the confusion effect is operating, the total number of stotts shown by all members of the group should correlate significantly with the number of fleeing animals in the group, but it did not (cheetah: N=41, rs =0"01, NS; vehicle: N = 171, rs=--0'01, ys). (C2) I have no data on whether members of groups in which stotting occurred were captured less often than members of groups in which no stotting occurred. However, my impression was that stotting by group members had no effect on the outcome of a hunt. (P5) Neither I, nor F. Walther (personal communication) ever saw a cheetah become visibly confused as a result of stotting, for example chasing one quarry and then switching to another. The hypothesis that predators might become confused by many white rump patches moving up and down in front of them is another hypothesis susceptible to cheating. If it only required a few stotting members of the group to cause the predator to reach some threshold at which it becomes confused, then individuals would be selected to delay stotting, and thus delay incurring its time or energy costs, given that others might stott first (Caro 1986). Added to this theoretical problem are the practical difficulties outlined above: gazelles did not stott when the cheetah was close to them, single gazelles stotted, and they did not stott more to cheetahs that chased them. In addition very few fleers stotted from either the vehicle or a cheetah, and in neither case did the number of stotts shown

Caro: Stotting in Thomson's gazelles by the group correlate with the number of animals fleeing. Both the theoretical problem and empirical data therefore preclude the confusion effect from being further considered as a function of stotting in Thomson's gazelles in relation to cheetahs.

Hypothesis 7: social cohesion This hypothesis proposes that stotting (or more normally rump-patch signalling) serves to tell other group members to move towards each other in the presence of a predator and then flee together and so accrue group-related benefits (Hirth & McCullough 1977). Therefore (I2) both solitary Thomson's gazelles and those in groups should stott (confirmed) in order to bring and keep conspecifics together, (I3) they should preferentially direct signals at conspecifics (refuted), and (I4) should stott more when being chased (refuted). (C2) Group members should be captured less often than solitary individuals. Quantitative data on cheetahs hunting gazelles suggest that this is true (personal observation) and it is supported by data from other predators hunting a variety of prey species (Schaller 1972). (C3) I never saw Thomson's gazelles bunch together when being chased by a cheetah, as this hypothesis would predict, and there was no evidence to suggest the percentage of fleeing animals in the group was correlated with the number of stotts performed by the focal individual (usually the only stotter, see above; cheetah: N=41, r~=0'21, NS; vehicle: N = 171, r s = - 0 . 0 2 , NS).

In conclusion, some evidence gives weak support to the hypothesis: gazelles stott when they are alone, supporting the idea that they are signalling to conspecifics to join them, and they stott in groups perhaps to signal to keep together (C. FitzGibbon, personal communication). Yet, the number of fleeing animals was not significantly correlated with the percentage of stotts performed by the focal individual and Thomson's gazelles did not flee from a cheetah in groups, although they sometimes did from wild dog packs (personal observation), which suggests that the Social Cohesion hypothesis is a weak contender for the function of stotting.

for mothers to aid them against predators (Walther 1969). In testing both versions (I8) I found that concealed neonates that I disturbed in the car stotted more frequently than did neonates which were standing and could presumably be seen by their mothers (ManmWhitney U-test, z = - 2 - 3 1 , P < 0.02) although the number of stotts and stotts/ m did not differ significantly (Fig. 9; z = -- 1.49, NS; z= 0.14, NS, respectively). Second, concealed (but not unconcealed) neonates showed more stotts in their flights and stotted more frequently the further they were away from their mothers (N= 21, rs = 0.49, P < 0-05; rs = 0-59, P < 0.02 respectively; see Fig. 10). (I9) I could not tell whether neonates stotted more when disturbed by predators (second version) but (I10) preliminary data suggest that mothers were instrumental in promoting their fawn's survival. In chases of neonates by a cheetah in which neonates were not caught, mothers stotted significantly more per m in between the neonate and the cheetah than they did in chases where the neonate was captured (Mann Whitney U-test, U = 0 , P<0.05; Fig. 11). To add support to this finding based on such a small sample size, I compared measures of stotting of mothers with those of adult females. Mothers who were successful stotted significantly more than adult females (stotts/m: U=2, P<0"002; stotts/s: U=6-5, P<0'02; Fig. ll). Moreover these results are conservative because they include all flights by adult females from cheetahs; if there had been sufficient data to allow the more appropriate measure of flights in which adult females were chased by cheetahs to be considered, then differences between females and successful mothers would have been even greater (see Fig. 6). Mothers who were unsuccessful in 16-

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675

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Animal Behaviour, 34, 3

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measures of stotting from the vehicle in concealed (N= 21)neonates. One star: P < 0.05; two stars: P < 0.02. saving their offspring did not differ from adult females (stotts: U = 16.5, NS; stotts/m: U = 12, NS; stotts/s: U = 15, NS). (C4) A mother often ran to her offspring if a predator appeared but I have no evidence to show that she did this more if it stotted. Mothers were seen defending their fawns against jackals, sometimes successfully. In conclusion, there is strong evidence to support the notion that neonate Thomson's gazelles signal to their mother by stotting. (In other contexts, too, stotting is seen in response to the behaviour of other gazelles, see Conclusions.) Walther (1984) concurs by stating that 'when a gazelle fawn which has been lying out leaves its resting place stotting it

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Figure 11. Medians and interquartile ranges of three measures of stotting in mothers whose neonates successfully evaded capture (ESC), mothers whose neonates were caught by a cheetah (CAPT), and adult females (FEM) stotting to a cheetah (see text). Numbers in bars refer to sample sizes. has a strong alarm effect upon the mother'; thus stotting can notify the mother of the neonate's new position and inform her whether it is in danger. Concealed neonates stotted more than unconcealed ones and stotted more the farther they were from their mothers. I could not tell whether

Caro: Stotting in Thomson's gazelles neonates stotted more when disturbed by predators than by herbivores, nor whether mothers came to the aid of stotters more than non-stotters, but mothers were seen to defend their fawns and neonates against jackals (see also Packer 1983). By stotting at high rates, Thomson's gazelle mothers appeared to help their neonates escape capture from a cheetah. However, this finding does not necessarily support the Pursuit Invitation hypothesis in gazelle mothers. A cheetah did not fail to capture a neonate because its mother intercepted the cheetah and caused it to chase the mother instead; rather, the cheetah failed because it was outrun by the young gazelle or lost sight of it in tall vegetation (see also Walther 1969; Kruuk 1972). Thus mothers may distract the predator's attention in some way by vigorously stotting in front of it so that, if the neonate abruptly hides in thick vegetation during the chase, which is its best defence against predators, the cheetah appears to be unable to locate the precise patch of herbs in which to search for it.

Hypothesis 9: anti-ambush behaviour Stotting might simply allow gazelles to get a better view of their surroundings (Pitcher 1979). If this were true, (I11) individuals should not stott in short vegetation. However, Thomson's gazelles often stotted both at the vehicle and at the cheetah in very short vegetation (less than 20 cm in height). (112) Furthermore, there was no evidence to suggest that stotting increased in higher vegetation when stotts, stotts/m and stotts/s were all compared in three different vegetation heights (less than 20 cm, 20-40 cm, more than 40 cm). No significant differences were found on any comparison when individuals stotted at the vehicle (no. stotts: N = 131, 41, 8; medians=7.0, 7.0, 6.5 respectively across increasingly high vegetation; stotts/m: N=128, 41, 8; medians=0.4, 0,4, 0-4; stotts/s: N = 130, 41, 8; medians= 0.75, 0-53, 1.00) or in the presence of a cheetah (N=53, 14, 9 for all measures; no. stotts: medians---8.0, 6.0, 10.0; stotts/m: medians=0.30, 0"34, 0-25; stotts/s: 9medians = 1.25, 1.00, 1.13), except that more stotts were shown in vegetation more than 40 cm high than in 20--40-cm vegetation with cheetahs ( M a n n Whitney U-test, U=22-5, P<0.02); however, the median number of stotts for very short (less than 20 cm) grass lay in between these two figures and these results were in no way borne out in the other two measures of stotting. In summary, no consistent

677

differences in stotting could be found in the vegetation types measured. (I 13) Hypothesis 9 predicts that stotting in high vegetation need not occur in the presence of predators. Although gazelles do stott in response to the behaviour of other gazelles and not always in the presence of predators, I was not aware that gazelles stotted in high grass (more than 1 m high). Thomson's gazelles moved quickly through high vegetation, often making arched jumps (Walther 1969) which could be confused easily with stotting (but the front legs are not held out parallel to the ground in stotting). Arched jumping appeared to afford a greater visual field than the extremely restricted view gained from walking in high grass. (I14) After feeding for some time in an area, gazelles will probably know that the vegetation close by contains no predators. If stotting increases a gazelle's visual field, then flights that take the prey further away from its latest feeding area should contain more stotts/m. However, exactly the opposite was found to occur: short flights were characterized by more stotts/m than other flights (cheetah: N = 76, rs = -0.42, P < 0.002; vehicle: N = 177, rs=--0.38, P<0.002; Fig. 12). (I15) For similar reasons, stotting should be more prevalent towards the end of a flight (confirmed; Table II). I have no evidence to test whether 016) gazelles stotted more to lions (Panthera leo), often a grouphunting predator using a concealed approach, than to cheetahs (adults are often solitary: Caro & Collins 1986), as would be predicted by the hypoth-

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678

Animal Behaviour, 34, 3

esis or whether 017) prey animals suffered lower capture rates in tall vegetation when they stotted. This hypothesis suggests that stotting does not involve signalling, but is simply a means of achieving greater visual orientation. However, gazelles are able to gain height in other ways, through arched jumping and during flat gallops (see Walther 1969 for definitions), so it is difficult to see why gazelles should have evolved a particular form of behaviour to achieve this end. Indeed gazelles stotted in very low vegetation which provided excellent views of the surroundings and stotting did not increase with vegetation height, at least up to 60 cm. However, it could be argued that such an effect would only be seen when vegetation was very high (e.g. more than 1 m, or at least well above gazelle eye level) but in these conditions gazelles appeared to perform arched jumps to obtain a better view (personal observation). Other results were equivocal: gazelles showed most stotts/m during short runs but stotted more in the last three-fifths of their runs. Nevertheless, the fact that gazelles frequently stott in grass less than 20 cm high is sufficiently damaging to discard the Anti-ambush hypothesis; stotting almost certainly confers benefits other than increased visual orientation on its bearers.

Hypothesis 10."play The benefits of stotting in young animals might differ from those of adults (Walther 1969); several authors report that young gazelles stott during play bouts. From the outset, however, it seems unlikely that stotting is a form of play because other forms of play normally stop abruptly in hazardous situations when predators are present. Yet if stotting in the presence of predators was a form of play in young gazelles, and had no obvious short-term benefit, then it might be expected to have the characteristics of play seen in other species, such as the different types and amount of play seen in the two sexes (e.g. Caro 1981). Unfortunately, I could not test for (I18) sex differences in stotting in neonates or fawns because the sexes are difficult to tell apart (see Walther 1973). Play in many species of ungulates consists of mutual behaviour (Byers 1984). I therefore looked at (C5) whether young gazelles were more likely to stott from the vehicle when peers (neonates or fawns) were stotting. There was no evidence to suggest that instances of neonates stotting were more likely to occur when peers were stotting than when peers were not stotting in flights from the

vehicle (binomial test, N = 24, Ns). The same was true of fawns (N= 14, Ns). Nor were there any differences in the number of stotts, stotts/m or stotts/s shown by focal neonates or focal fawns, when peers were or were not stotting simultaneously from the vehicle (Mann-Whitney U-tests; neonates: peers stotting, N = 8; peers not stotting, N-- 12; median no. stotts=8.0, 5'5 for peers stotting and not stotting respectively; U=39.5, Ns; median stotts/m= 0.34, 0.45 respectively; U=39, ys; median stotts/s=0.86, 0.77 respectively; U=40, NS; fawns: median no. stotts (N=3, 11 respectively)= 13.0, 8'0 respectively; U = 12.5, Ns; median stotts/m (N=2, 11 respectively)--0.21, 0.60 respectively; U=2, Ns; median stotts/s (N=2, 11 respectively) = 0.67, 0.75 respectively; U = 8.5,

NS). In summary then, it is unlikely that stotting is a form of play because it occurs in potentially dangerous situations. In addition, stotting does not have some of the characteristics of play because stotting in neonates or fawns was no more likely to occur when peers were stotting, and stotting was no more frequent in these situations. This is not altogether surprising given that only one adult usually stotts in the presence of predators (although very many gazelles may simultaneously stott to wild dogs). Numerous accounts, however, suggest that stotting does occur during play in the absence of predators especially in the early morning and after rain (Brooks 1961; Walther 1964; Estes 1967; C. FitzGibbon, personal communication; personal observation). In these situations it appears to conform to solitary locomotor play seen in many other ungulate species (Byers 1984).

Hypothesis 11: warning conspecifics This last hypothesis proposes stotting to be an alarm signal (Estes & Goddard 1967) by means of which an individual warns conspecifics of the predator's presence. This proposed alarm behaviour might or might not, in theory, incur risks for the signaller. If there are survivorship costs of stotting, gazelles should only stott at safe distances from the predator (I1, confirmed), solitary individuals should not stott (I2, not confirmed), and signals should be directed at conspecifics and not at the predator (I3, not supported). In the first version of hypothesis 11, altruistic benefits will only be mediated through kin selection given the structure of gazelle society (see Caro 1986). Thus females should stott more than males

679

Caro: Stotting in Thomson's gazelles

because Thomson's gazelle females are far more likely to be in the presence of close kin than are males (Walther 1977, 1978b). (I19A) There were almost no significant differences in the n u m b e r of stotts given, stotts/m or stotts/s between adult males stotting in groups and adult females stotting in groups containing conspecifics only ( M a n ~ Whitney U-tests, vehicle: males N = 5 , females N = 4 ; median no. stotts=3.0, 9.5 respectively; U = 6, Ns; median stotts/m = 0.21,0.18 respectively; U = 8, NS; median stotts/s = 0.75, 0-59 respectively; U = 9, Ns. Cheetah (gazelle mothers with neonates excluded): males N = 23, females N = 7; median no. stotts = 6.0, 7-0 respectively; z = - 0 - 7 7 , NS; median stotts/m=0'30, 0.20 respectively; z - - - - 2 . 0 3 , P < 0 . 0 5 ; median stotts/s= 1.00, 0.78 respectively; z = - 1 " 9 5 , NS). The only significant difference showed that males stotted more often per m to cheetahs than did females, the reverse of the prediction. What is more, in a second test of the hypothesis, it was found that there were no differences between group sizes in situations in which neonates and fawns either did or did not stott (Mann Whitney U-test, N = 2 7 , 34, medians 3'0, 4.0 respectively; z = - 0 . 4 9 , NS); these individuals were very likely to have relatives, mothers and usually yearling half-siblings, in the group. (I20) There was no positive correlation between group size and n u m b e r of stotts (N = 7, r~ = - 0-46, NS), stotts/m ( r s = - - 0 ' 2 3 , NS), and stotts/s (r~= --0-22, ys) shown by female gazelles; indeed the evidence suggested that they stotted less as group size increased. Across all age classes of Thomson's gazelles, measures of focal stotting did not correlate with group size (excluding group sizes of one) either for cheetahs (no. stotts, N = 41, rs= 0"00, NS; stotts/m, rs=--0"01, NS; stotts/s, r~=--0"08, NS) or for the vehicle ( N = 1 7 1 , rs=--0"06, NS; N = 1 6 8 , &=--0-021 NS; N = I 7 0 , rs=--0.02, NS). Nor did the arguably better measure of the total number of stotts shown by all members of the group correlate with group size (cheetah: N = 4 1 , rs=0.05, Ns; vehicle: N = 1 7 1 , rs = --0'05, NS) as might be expected if individuals were trying to warn relatives in the group. Nevertheless, in the second version of the hypothesis, where alarm behaviour is mediated through individual selection and individuals warn conspecifics of the predator's presence so as to reduce its hunting success, then (II9B) no sex differences would be predicted, which is confirmed by these results.

Hypothesis 11 also predicts that, if stotting is an alarm signal, it might occur in conjunction with other known alarm signals such as snorting, or putative alarm signals such as flank flashing or stamping, because these alarm signals often occur together. However, it is difficult to see why a relatively low-cost auditory signal would not suffice for warning nearby conspecifics of danger. (I21) The aforementioned signals were rarely shown by Thomson's gazelles in the presence of a cheetah or the vehicle and did not occur in conjunction with stotting. In 76 recorded instances of gazelles stotting in response to cheetahs they stamped the front foot only once, and flank-flashed once. (I could not be sure that gazelles had not snorted at cheetahs if I was far away so I dropped this comparison from the analysis.) Similarly, stamping was seen only once in 178 stotting flights from the vehicle and no snorting occurred. Taking flights from the vehicle that did not contain a stott as well as those that did contain one or more, the probability of stotting decreased with age while flank flashing increased (Table V). When age groups were combined, flank flashes and stotts occurred together in the same flight less often than expected by chance ( ) ( = 7.44, d f = 1, P < 0.01). If stotting serves to warn conspecifics of danger, conspecifics might be more likely to look up if an individual in the group stotts. I could not test for this but group members were usually alert to danger before any animal stotted. I could test whether (C6) conspecifics were more likely to flee if an individual stotted. Taking the age classes for which I had large enough samples (fawns and neonates combined), there were no differences in the percentage of fleeing animals in the group (no stott, N = 3 4 ; stott N = 2 7 , medians=10.0, 10.0 respectively, M a n n - W h i t n e y U-test, z = - 0-64, NS) when the flights where fawns and neonates did not stott were compared to situations in which they did. Table V. Changes in probability of stotting and flank-

flashing to the vehicle with age

Age class Adult Adult females Subadults Fawns Neonates

Probability of stotting

Probability of flank-flashing

N

0.03 0 0.02 0-23 0.52

0.48 0.40 0.38 0.10 0-03

31 30 48 30 31

680

Animal Behaviour, 34, 3

(C7) Similarly there was no evidence to show that the number of fleers or percentage of fleers increased with an increasing number of focal stotts (N= 41, r~-~0.13; rs = 0.21 respectively; see hypothesis 7), focal stotts/m (rs = -- 0.12, -0-24 respectively) or focal stotts/s (rs = -- 0.17, -- 0' 16 respectively; all NS) in the presence of a cheetah, or of the vehicle (stotts: N - 171, r~= -0.08, NS; r~= --0"02, NS respectively; stotts/m: N = 168, rs=--0.16, NS; r~=--0"16, NS respectively; stotts/s: N=170, r~=-0"30, P<0-02; r ~ = - 0 - 2 5 , P<0.05 respectively). In most cases, the focal individual was the only animal to stott; in flights from the vehicle, it appeared that there were actually fewer fleers when the focal animal stotted more. To sum up these results, many predictions can be derived from this hypothesis only one of which is supported: gazelles were found to stott at relatively safe distances from cheetahs. The following were detrimental to the hypothesis: gazelles stotted alone and at predators and did not preferentially stott at a hunting cheetah. If alerting others is maintained through kin selection, stotting should only be seen in the relatively philopatric females, However, no adult sex differences were found in measures of stotting, and there was no relationship between group size and stotting, as might be predicted. Further refutation comes from observations showing that stotting very rarely occurred in conjunction with other alarm signals. Also the number of animals fleeing was not affected by whether a young animal stotted or not, and did not increase with an increasing number ofstotts shown by the focal individual. In addition, it is unlikely that the function of stotting is to alert other gazelles so that hunting becomes unprofitable and the predator is forced to leave the area. Single gazelles often stotted at a cheetah when no other gazelles were visible (see hypothesis 1). Second, most gazelles were often alert, watching the cheetah, before any individual stotted, and third, (P6) cheetahs did not tend to leave the general vicinity in response to a failed attack on a group of gazelles. A cheetah that had been seen might lie down and rest, or walk over a rise out of view of the herd. It might or might not attack that group again later, but the pertinent point is that an individual cheetah might remain in the same square kilometre for periods up to a week in length (personal observation); indeed I frequently used location as an initial cue in identifying individual cheetahs. The prey's knowledge of the

predator did not appear to make a cheetah move location; rather the prey's movements determined cheetah ranging behaviour. In short, although stotting could, in theory, be maintained in the Thomson's gazelle population by dint of its alarm function, the weight of evidence suggests that this is not the case.

CONCLUSIONS The time cost of stotting from reduction in flight speed appears to be negligible in situations in which stotting normally occurs. Thomson's gazelles stott in safe situations when they are not being pursued and stott well beyond the distance at which they are likely to be captured. This implies that stotting must have potential costs, and there is a hint that stotting does reduce flight speeds when high-speed chases occur. Indeed measures of stotting are low during chases. The energy cost of stotting was not measured in this study but the reduction in stotts with increasing length of flight (Fig. 12) indicates that there may be an appreciable energy cost to this behaviour. Stotting would certainly be more costly than standing still monitoring the predator, but it might be no more costly than the leaping that is often seen in flights. Thus stotting probably imposes a time cost at high speeds and an energy cost in any flight; together these would result in an overall survivorship cost ifstotting were employed in inappropriate situations. Normally however, stotting does not result in increased mortality for the individuals that show it. The results presented in this study strongly suggest that stotting has two consequences upon which natural selection acts to maintain it. A third function is implicated. Stotting in adult and subadult Thomson's gazelles appears to inform the predator that it has been detected. Stotting provides an unambiguous signal to the predator that the prey is wary of it. The predator can then decide whether further approach will be unproductive: it can continue or give up. In most cases it gives up because, in the case of a cheetah, it is unlikely to catch the gazelle unless it can begin the chase less than 30 m from its victim. However, this decision will depend on a number of factors such as the cheetah's level of hunger, the necessity of feeding cubs, and the likelihood of making a successful capture in the future, which, in

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turn, will depend on predatory competence and prey availability. If the predator decides that the effort of a long chase will probably not result in prey capture and that unwary prey are available nearby, it will give up. In such cases the probability of capture for the gazelle will be reduced to a very low level. Stotting in adult Thomson's gazelles in response to a cheetah is therefore maintained by natural selection because cheetahs usually abandon hunts in response to it. Although benefits may primarily accrue through the prey signalling to the predator that it has been detected, incidental benefits may also be garnered through an increased time spent feeding, if the predator moves off. Also, gazelles may occasionally startle conspecifics (possibly kin) into looking up and seeing the predator (personal observation); Thomson's gazelles become very alert if any conspecific stotts. This helps to explain why only one member of a group normally stotts. Cheetahs do not usually abandon hunts if a gazelle stares directly at it but they do if the gazelle both stotts and stares at it. If several gazelles all stare but only one stotts, this appears to provide sufficient information to tell the cheetah that it has been seen by all group members. Stotting is therefore maintained by natural selection because, in the majority of cases, predators abandon hunts in response to it. Of course there are situations in which predators do not abandon hunts because of hunger or other factors and these may represent some of the observations made on packs of wild dogs hunting Thomson's gazelles (Estes & Goddard 1967; Walther 1969). Quantitative observations on gazelle anti-predator behaviour in response to wild dogs are lacking but the hunting success of wild dogs appears to be very high (Schaller 1972; Malcolm & van Lawick 1975), and it is worth noting that, unlike cheetahs, wild dogs may pick out their victim only after starting the chase (Estes & Goddard 1967). This suggests that one consequence of the high rates of stotting to wild dogs is to prevent the predator 'locking on' to an individual, possibly by confusing it in some way. F. Walther saw this occur a number of times in response to wild dogs (personal communication); however, the subject requires further investigation. Stotting in Thomson's gazelle neonates appears to have a different function from that of informing the predator it has been seen. Neonates apparently inform their mother that they have been disturbed and thereby notify her of their new position. If

danger threatens, she has the option of trying to defend the neonate in a number of different ways. It seems unlikely that stotting in neonates could be selected through the effect it has on the predator. Young Thomson's gazelles are captured at high rates (Schaller 1972; personal observation) without apparent regard to whether they stotted or not. Cheetahs will start an unconcealed rush towards fawns or neonates far earlier than towards adult or subadult Thomson's gazelles because young gazelles appear unable to outrun cursorial predators, have poor zig-zagging ability (personal observation), and even fail to recognize some predators (personal observation). Informing a predator that a neonate has seen it therefore appears very unlikely to cause a predator to abandon a hunt. Rather, stotting in young gazelles is selected through the information it conveys to its mother. A third function of stotting is also implicated. Mothers whose neonate escaped capture by a cheetah, stotted significantly more than did those whose offspring were caught. This implies that the high rates of stotting shown by mothers act either as a distraction display (e.g. Simmons 1955) that distracts the predator's visual attention or, possibly, in a similar way to the hypothesized confusion effect. However, they do appear to deflect the predator's direction of attack (personal observation) in a manner akin to that required by the Pursuit Invitation hypothesis. More work needs to be done on this aspect of stotting. Finally, it should be noted that stotting also occurs during intraspecific encounters, in situations where there is no predator present. Walther (1969) mentions that, if anoestrous females or bachelor males are being driven by a male, they will sometimes stott to it, especially after a fight. These descriptions do have similarities to stotting in the presence of a predator: stotting to a conspecific that has harassed you could inform it that continued disturbance will only end in an unproductive chase. However, Walther also occasionally saw pursuing gazelles stott in intraspecific encounters, so this subject clearly requires further analysis.

ACKNOWLEDGMENTS I thank the Government of Tanzania for permission to carry out research and the Coordinator and Acting Director of the Serengeti Wildlife Research Institute for help and cooperation during the study.

Caro. Stotting in Thomson's gazelles I was s u p p o r t e d by a Royal Society Scientific Investigations grant, the D e p a r t m e n t of Zoology and S u b - d e p a r t m e n t of A n i m a l Behaviour, Cambridge. I particularly wish to t h a n k the MaxPlanck Institut ffir Verhaltensphysiologie for specifically funding this project. ! a m grateful to Monique Borgerhoff Mulder, Peter Hetz, A n d r e w Hill, Sue Praill a n d A l a n a n d J o a n R o o t for logistical support, to M o n i q u e Borgerhoff M u l d e r for discussion in the field a n d during writing, a n d for n u m e r o u s critical c o m m e n t s o n the manuscript. Steve Albon, Clare F i t z G i b b o n , D a v i d G i b b o n s , M a r t y n Murray, Fritz W a l t h e r a n d two referees also kindly provided thoughtful c o m m e n t s . This is S.R.I. c o n t r i b u t i o n No. 345.

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(Received21 December 1984,"revised22 March 1985,"MS. number: 2647)