Predation risk and lek-breeding in Uganda kob

Anim. Behav., 1992, 44, 117-127

Predation risk and lek-breeding in Uganda kob ANDREW

BALMFORD*

& M. T U R Y A H O t

*Large Animal Research Group, Department of Zoology, Downing Street, Cambridge CB2 3E J, U.K. t Uganda Institute of Ecology, P.O. Box 3530, Kampala, Uganda and

College of African Wildlife Management, Mweka, P.O. Box 3031, Moshi, Tanzania (Received26 April 1991; initial acceptance 19 July 1991; final acceptance 15 January 1992; MS. number: 3768)

Abstract. Reduced predation risk has been suggested as a major advantage to males and females of mating on leks rather than elsewhere, and as an explanation of why females often choose to mate on relatively central lek territories. Few studies, however, have yet attempted to quantify predation risk on and away from leks. In this study average per capita predation risk for adult male Uganda kob, Kobus kob thomasi, assessed from the distributions of live kob and skulls, was similar on and off leks. This was apparently due to a trade-off between improved predator detection at leks and a tendency for leks to become foci for predator activity. Within a lek, predation risk to males was relatively high around its periphery, but there was no evidence that the distribution of matings across lek territories was closely related to spatial variation in risk. Thus predation risk is unlikely to be a major factor determining why male kob mate on leks. In lek-breeding species, males defend small territories that do not contain significant resources, and are clustered onto arenas or leks where females come to mate (Bradbury 1981). The adaptive significance of lekking remains poorly understood, but it has been suggested that reduced predation risk may be a major advantage to males of displaying on leks rather than on dispersed territories (Lack 1968; Wiley 1974; Wittenberger 1978; Oring 1982), or to females of mating on leks rather than elsewhere (Wittenberger 1978; Gosling 1986; Gosling & Petrie 1990). Leks may be relatively safe for at least three reasons: the large number of animals present may mean that predators at leks are likely to be detected relatively early (Wittenberger 1978; Oring 1982); leks may be situated in areas of particularly low cover (Gosling 1986; Gosling & Petrie 1990); and dilution of predation attempts at leks may mean that per capita attack rates are relatively low (although the conspicuousness and permanent location of leks may offset such dilution, Rainy & Rainy 1989; Wiley 1991). In addition to overall differences in predation rate on and off leks, fine-scale variation in risk may be important in determining the distribution of matings within leks. If peripheral areas of leks are associated with consistently high predation risk (Hamilton 1971; Wiley 1973), the tendency for 0003-3472/92/070117 + 11 $03.00/0

females to mate on relatively central lek territories (reviewed in Balmford 1991) may reflect female choice for mating at safe locations (Partridge & Halliday 1984). Despite its potential importance, however, few studies have yet attempted to quantify predation risk in lek-breeding species. Moreover, most work to date has concentrated on assessing risk at leks of different sizes (Ryan et al. 1981; Trail 1987; Bradbury et al. 1989), and little is known of the relative risks of mating on versus off leks. Anecdotal reports indicate that predation at leks may be rare (Berger et al. 1963; Moran 1966; Wiley 1973; Lill 1976; Beehler 1988), but predation risk may be equally low away from leks (Lill 1974). In this paper we test the hypothesis that leks are associated with reduced predation risk by investigating levels of predation on male Uganda kob, Kobus kob thomasi, on and off leks. We assess overall predation risk to males by analysing the distribution of skulls and live animals on and away from a lek. We investigate this further by comparing predator detection, visibility and cover on and off leks, and by observing where predators spend time. We then examine fine-scale variation in male predation risk across a lek, and compare this with observed patterns of nonrandom mating.

9 1992 The Association for the Study of Animal Behaviour 117

Animal Behaviour, 44, 1

118 METHODS Study Area and General Methods

We studied Uganda kob from February 1987 to February 1989 in Queen Elizabeth National Park, South-west Uganda. Territorial males defended either aggregated lek territories or relatively large, isolated, and probably resource-based single territories (Leuthold 1966; Balmford 1990). Confirmation that male aggregations were indeed leks (rather than clustered resource-based territories) was obtained by comparing male mating success with the quality of forage available on different clustered territories: we found no clear relationships between any of our measures of vegetation quality and male mating success (in marked contrast to resource-defending populations of puku, Kobus vardoni, and topi, Damaliscus lunatus; see Balmford 1990, cf. Balmford et al., in press c). Similarly, oestrous female kob generally spent far less time feeding while on leks than when away from them (27% cf. 79%, Balmford 1990), refuting any suggestion that females visited these areas in order to feed. Most of the data reported here were collected from a 28'6-km 2 area surrounding the largest lek in the south of the Park (Ishasha South); additional observations were carried out at two nearby leks and at six leks in the northern part of the Park. The Ishasha study area supported very high densities of kob (ca. 140 animals/km2); females, juveniles and non-territorial males were typically found in large, unstable herds, and travelled widely over extensive home ranges (Balmford, in press). Vegetation consisted principally of open Acacia sieberiana woodland and open, medium height grassland (see Balmford 1990 for further details). The study area overlapped with the home ranges of two prides of lions, Panthera leo (Van Orsdol 1982; Balmford 1990), and lions, spotted hyaenas, Crocuta crocuta, and humans were the major predators on adult kob. In addition, leopards, Panthera pardus, sidestriped jackals, Can& adustus, martial eagles, Polemaetus bellicosus, and rock pythons, Python sebae, killed calves and juveniles. The number ofkob in the study area was assessed by twice-monthly sample counts made while driving along a systematic array of fixed-width transect lines (Caughley 1977). We counted all kob within 100 m either side of each line, but for present purposes totals recorded on each line were then divided by four, since comparable skull counts were only made

within 25 m each side of transect lines (see below). We also carried out censuses at Ishasha South lek, and assessed fine-scale variation in kob density by censusing a 62-5-ha area comprising the lek itself and eight arbitrarily defined sectors of surrounding open grassland. Only standing animals could be counted reliably in distant sectors, but counts of standing animals were considered comparable across sectors since kob spent a similar proportion of their time standing whether on or away from a lek (Balmford 1990). Nearly all males censused on the lek and in surrounding grassland held territories there; we have no data on the proportion of males along census lines that were territorial. We recorded kob activity during 269h of behaviour sampling (Martin & Bateson 1986) across the whole of Ishasha South lek, and during focal animal watches on females on and away from leks, and on males holding either lek or single territories. Lek territories were classified as central or peripheral according to their location and the height of grass that they supported; higher levels of sexual and agonistic activity meant that trampling was generally greater on central territories, which consequently supported somewhat shorter swards (Balmford 1990). All activity records were taken during daylight, but data collected with an image intensifier during nine 12-h night watches indicated that levels and spatial distribution of activity were similar at night. Predation Risk On and Off Leks

To assess predation levels on and off leks, we examined all fresh kob carcasses found at Ishasha for cause of death (Bertram 1979). Signs such as a blood patch or evidence of a physical struggle near the carcass, or grass in the dead animal's mouth, indicated that at least 58 out of 81 carcasses found were almost certainly victims of predation, usually by lions or hyaenas. The distribution of these kills across different areas of the study site probably reflected the approximate origin of depredated animals; although some animals (particularly those killed by hyaenas, Kruuk 1972) will undoubtedly have been chased from one area to another prior to death, it seems improbable that such chasing was consistently towards one particular area, and instead more likely that the number of animals chased from one area and killed in another was approximately balanced by the number chased from the latter area and killed in the former.

BalmJbrd & Turyaho : Leks and predation in kob Too few kills were found in areas where we also had detailed information on live animal density for kills themselves to be used as a direct measure of predation pressure. However, when kob (and in particular adult males) are killed, their skulls are usually left behind and can be found after fires (which remove grass cover). We collected 28 skulls from a 50-m strip (25 m either side) along each transect line, and 152 skulls from the 62-5-ha area around Ishasha South lek. The distribution of 13 kob kills across the nine sectors of this latter area (Ishasha South lek and eight off-lek sectors) was correlated with the distribution of skulls across those areas (rs=0-713, N = 9 , P<0'05). Thus, despite the fact that predators and scavengers often scatter skulls quite widely (Kruuk 1972; Schatler 1972), this result indicates that the distribution of skulls can be used to infer the approximate location of predation incidents. To see whether average predation risk was similar on and off leks, we then compared the number of skulls found in on and off-lek areas with that expected solely on the basis of number of live animals present. Statistical analysis could be carried out for adult males only, since we found relatively few skulls of females or younger males (presumably because these were more easily destroyed by predators or scavengers). No difference between observed and expected skull numbers was taken as evidence of no difference in per capita risk to adult males on and offthe lek. Predator Detection

To investigate whether animals on leks detected the approach of a predator sooner than did animals on single territories, we conducted a simple experiment in which an observer walked towards groups of animals on leks and on single territories, and noted the distance at which he was first alerted to by different classes of animals. Poaching was common at Ishasha, and so the observer's approach simulated that of a predator. We performed the experiment 10 times at each of two leks and five times at each of four single territories. On each occasion the observer walked in a predetermined, random direction towards the centre of a lek or single territory and left markers when he could first see animals on it, and when he was first alerted to (defined as being stared at by a standing animal) by: (1) a male on a central lek territory; (2) a male on a peripheral lek territory; (3) a female on a lek

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(effectively always on a central territory); (4) the holder of a single territory; or (5) a female On a single territory. We then measured the distances between these markers and the positions of the corresponding alerting animals. Where necessary, skewness in detection distances and numbers of animals present was removed by log-transformation, and results for leks and single territories were then compared using analyses of variance. F o r each variable (such as distance of detection by females), we first assessed the significance of variation between repeated trials at a particular lek or single territory. Having thereby removed variation within leks or single territories, we then entered territory type (i.e. lek or single territory) as a factor in the analysis, in order to assess whether values differed between them. We investigated factors underlying differences in predator detection ability by comparing vigilant behaviour of individuals on leks and on single territories, using records taken every minute during focal animal watches. We defined vigilance while standing as the percentage of standing time spent with the head above shoulder height (excluding time spent moving or interacting socially), and vigilance while lying as the percentage of lying time spent with the head up. These definitions are equivalent to those used in several recent studies of vigilance in mammals (e.g. Underwood 1982; FitzGibbon 1990; Gosling & Petrie 1990), except that vigilance while standing is usually only recorded during feeding bouts. For kob, feeding bouts were shorter for animals on the lek than off it (Balmford 1990). Because this confounds interpretation of vigilance while feeding, we instead calculated vigilance during all time spent standing. The effect of number of animals on a lek on the number of animals vigilant (defined as the number of animals standing, with heads above shoulder level) was investigated by scan sampling (Martin & Bateson 1986) at six different leks. We recorded head and body positions of all animals present, every 5 min, for 8-12 h at each lek. Data were then pooled across leks and the mean number vigilant was calculated for all scans when the same number of animals were present. Finally, we assessed the possible importance of cover on predator detection by comparing distances at which lek and single territory animals were first sighted during the predator detection experiment, and by comparing grass height on single and lek territories. We measured grass height

120

Animal Behaviour, 44, 1

(defined as the resting height above ground of a polystyrene tile, measuring 30 x 30cm, dropped onto the sward) at monthly intervals, at 10 randomly selected sites in each of 12 lek territories, and at 25 randomly selected sites in each of 10 single territories. As with data from the detection experiment, we then assessed whether grass heights varied between leks and single territories in an analysis of variance, which first took account of variation in grass heights within leks or single territories.

8o "5

9 Observed D Expected

60

zo E z

o

Lek

Off-lek gress

Figure l. Observed and expected numbers of adult male Behaviour of Predators

As the major predators of kob were largely nocturnal, we rarely observed predation attempts, and spatial variation in their distribution was instead inferred from observations of where predators spent time. We noted the number of lions present on our arrival whenever we visited three different leks, and then calculated the proportion of time that lions spent at each lek by comparing the number of lions sighted (summed across all visits) with the maximum possible if all lions in the local pride had been on that lek every day (calculated as the product of number of visits and pride size). We also estimated the proportion of night time that lions spent at Ishasha South lek, using continuous records of lion presence made during night watches. Pride size was determined by individual recognition of all members (after Pennycuick & Rudnai 1970). The proportion of its time that a pride spent on a lek was then compared with that expected on the basis of lek area relative to pride home range (given in Van Orsdol 1982), and of kob numbers on the lek and elsewhere in the pride range. We could not carry out similar quantitative analyses on where hyaenas spent time, since we lacked accurate estimates of hyaena numbers. Variation in Predation Risk Around the Lek

We assessed fine-scale variation in predation risk across leks by analysing the distribution of adult male skulls across different sectors of the 62.5-ha area around and including Ishasha South lek. The numbers of skulls collected in off-lek sectors adjacent to and more distant from the lek, and in the lek centre and periphery, were compared with those expected solely from the distribution of standing males, assuming predation risk to be identical across sectors. We compared these results

skulls found on Ishasha South lek and in open grassland off-lek areas along transect lines. Expected figures are derived from 339 lek censuses (using the mean of 12 monthly means) and 22 counts along transect lines. with differences in predator detection by central and peripheral lek males, determined during the predator detection experiment. We then investigated the relationship between spatial variation in predation risk to males and the distribution of matings across Ishasha South lek by comparing the risk associated with different lek territories with the mean ejaculation rates of their holders. We estimated mean ejaculation rates of territory holders from behaviour sampling data, during which the locations of all ejaculations were noted. The predation risk associated with each territory was measured in two ways: as the number of male skulls on the territory; and, to estimate risk only when the territory was occupied, as that number divided by the proportion of time for which the holder of the territory was present. RESULTS Predation Risk On and Off Leks

The number of adult male skulls found on Ishasha South lek and in the surrounding area of open grassland did not differ from that expected from counts of standing males, assuming uniform predation risk (;(2= 1-21, df= 1, NS). Similarly, the distribution of adult male skulls between the lek and the census lines was similar to that predicted solely from live animal distribution (Z2=0.93, df= 1, NS), particularly when the lek, which was in open grassland, was compared with open grassland areas along census lines (Z2=0.0075, df= 1, NS; Fig. 1). Mean per capita predation risk to adult males (most of whom were probably territorial, see

Balmford & Turyaho : Leks and predation in kob

121

I0

250

5

. • 200

I 55

~0 15o .~ 100 ID

c~ 50

Leks

Single territories

Figure 2. Mean detection distances (_+SE) from the predator detection experiment, for peripheral males on two leks, and males on four single territories. Figures above bars give the number of successful trials at each lek or single territory.

Table I. Vigilance of individual kob, recorded during focal animal watches on and offleks Median vigilance while Mannstanding (%) Whitney (inter-quartile range) U-test

Kob class

Sample size

Lekmales Single territory males

21 13

10.53 (8.30-15.24) } 10.64(5.59-11.59)

Lekfemales Off-lek females

8 10

13-80(9.47 20.84)} 13.04 (5.47-21-44)

Central lek males Peripheral lek males

13 8

11.17 (8.30-15.56) } 9.43(6.86-12.11)

Methods) therefore did not appear to differ on and off the lek. While this result may be confounded by the fact that lek males were in better physical condition than off-lek males (Balmford 1990), and so may have been better able to escape predators (FitzGibbon & Fanshawe 1988), it does suggest that holding a lek territory was on average no safer than holding a single territory. Predator Detection

In the predator detection experiment even peripheral lek males (who detected approaches later than did central males; see below) detected the observer sooner than did single territory males (significance of territory type as a factor in A N O V A of log-transformed detection distances: F1,33 = 25.53, P < 0.001; Fig. 2). Similarly, females on leks detected predators sooner than did females on single territories (significance of territory type in ANOVA, using log-transformed data:

z= 1.05 U= 36 U=38

P

Median vigilance while Mann lying (%) Whitney (inter-quartile range) U-test

P

NS

16.06 (3.31-32.18) } 11"22 (4"44--18"15) z=0-58

MS

NS

9.79 (6.82-19.72)} 17-72(10.71-26.32)

U=25

NS

NS

16.06 (2.78-30.40)} 17"54 (4"76-52'32)

U=43

NS

F1,23 = 13-91, P<0.01). Other things being equal, such early warning of a predator's approach should reduce relative attack success on leks. Earlier predator detection by lek males was not due to lek individuals devoting more time to vigilance (Table I). Data from one watch (of 4 h or longer) for each of 21 lek territorial males and 13 single territory males showed there were no differences in their vigilance either while standing or while lying (Table I). Similarly, there were no differences in the vigilance of females watched on and off the lek. Nonetheless, scan sampling data from several leks revealed that the number of animals vigilant increased dramatically with number of animals present on the leks (rs=0-968, N = 17, P<0"001). Moreover, more animals were present during trials on leks than on single territories (significance of territory type in A N O V A of n u m b e r of animals present: F1,33 =9-24, P<0"01). Thus, if the effect of group size on n u m b e r vigilant is a general one, and if greater total vigilance does

Animal Behaviour, 44, 1

122

result in earlier predator detection, then earlier detection by lek animals may be partly explained by the greater numbers of animals present on leks than on single territories. Any effect of number of animals vigilant on predator detection may have been compounded by differences in cover between leks and single territories. Grass was generally shorter on the former (significance of territory type in ANOVA of grass heights, using data for all months and after taking account of variation between months and within leks and single territories: F1,18o4 = 15.05, P<0.001). However, differences in grass height were small (across all months: mean on lek= 194 mm; mean on single territories =246 mm) and were significant within only 2 months (significance of territory type in ANOVAs, by month: September 1988:F1,324 3.76, P < 0.10; October t988: F1,348=10.05, P<0.01; December 1988: Fl,a4s=27-35, P<0-001; January 1989: F1,34s = 3.69, P<0-10). Moreover, immediately after an extensive fire, lek territories in fact supported longer grass than did single territories (significance of territory type in ANOVA of February 1989 grass heights: F1,348 = 13.40, P < 0.001). A clearer indication of differences in cover between leks and single territories comes from the predator detection experiment, where the observer first sighted lek animals at greater distances than he sighted single territory animals (significance of territory type in ANOVA of sighting distances: F1.33=12.18, P < 0.01). This suggests that topographical and/or vegetative cover was less around leks than single territories. =

Behaviour of Predators

Based on data from daytime visits, lions spent far more time on leks than predicted either from lek area or number of kob present on leks (Fig. 3a). This result was not an artefact of idiosyncratic behaviour by a few individual lions, as it was repeated by both prides, and at both leks in the range of the Southern pride. Lions also spent a greater proportion of the night at Ishasha South lek than predicted (Fig. 3b); indeed, lions or hyaenas visited the lek during at least eight of the nine 12-h night watches. These estimates of predator presence are conservative in that they assume all predators were observed whenever they were on the lek (obviously optimistic for nocturnal observations). Thusifpredators make predation attempts

in approximate proportion to where they spend time, the results suggest that kob on leks experience higher per capita rates of predation attempts than do those off leks. Variation in Predation Risk Around the Lek

Despite the overall similarity in predation risk to males on and off leks, the fine-scale distribution of skulls around the lek was very different to that predicted from the distribution of standing males (~2 -- 22-75, dr=3, P<0.001; Fig. 4), suggesting substantial spatial variation in per capita predation risk to males in the immediate vicinity of leks. In particular, males on central lek territories were safer than those on the lek periphery, while off-lek predation risk was higher immediately adjacent to the lek than in more distant off-lek sectors (pairwise comparisons: lek centre versus periphery, ~2 =9.41, dr= 1, P<0.01; lek periphery versus offlek adjacent, ~2= 0.98, dr= l, ys; off-lek adjacent versus distant, ~2 = 15.59, dr= l, P<0.001). To investigate this fine-scale variation in predation risk further, we compared our detailed information on risk across the lek with data on overall off-lek risk along census lines. The distributions of male skulls versus live animals indicated no difference in predation risk between the lek centre and areas along census lines (~z=0.28, dr= 1, Ns), or between more distant off-lek sectors and census lines (~2 = 1-37, dr= 1, Ns). In contrast, both the lek periphery and off-lek sectors immediately adjacent to the lek were significantly more dangerous than areas along census lines (pairwise comparisons: lek periphery versus census lines, ~2=6.05, df= 1, P<0.05; off-lek adjacent versus census lines, ~2=6.43, dr=l, P<0-05). These analyses suggest that fine-scale variation in risk across the lek arose principally because the area around the lek periphery was particularly dangerous, rather than because the lek centre was particularly safe. The higher risk associated with the periphery of our lek was probably because predators concentrated their attacks at leks, and were more likely to get within striking distance of peripheral rather than central lek males before being detected. In the predator detection experiment, the first peripheral lek males to alert to the observer did so at shorter distances than did the first central lek males (pairwise t-test on log-transformed detection distances: t15=-2.86, P<0.05; X for peripheral

Balmford & Turyaho." Leks and predation in kob 2"0

123

(e)

1.5 -lO

I,L

I-0

0-5

Ishasha S (433)

Gatogota (44)

S pride

2-0

Ishasha N (26) N pride

(b) 9 Observed n Expected from lek oreo

1.5

E= r "E

[] Expected from kob numbers 1.0

2 o~

0.5

Ishasha S (9 nights)

Figure 3. The percentage of day time (a) and night time (b) that lions spent on leks, compared with that predicted from lek area or kob numbers on and offleks, There were too few data on kob numbers in the range of the Northern pride for this latter value to be calculated for Ishasha North lek. Day time spent on leks was based on instantaneous recording when leks were first visited (number of visits in parentheses); night time calculations use data from nocturnal watches. Pride h o m e ranges were taken from Van Orsdol (1982).

80

9

Observed

~= o~ 60

[]

Expected

~n

~ eo 5 z

Lek centre

Lek periphery

Off-tek adjacent

Off-lek distant

Figure 4. The distribution of adult male skulls across different sectors of a 62.5-ha area of open grassland around and including Ishasha South lek, compared with that expected on the basis of live animal distribution.

Animal Behaviour, 44, 1

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males=201.9 m, .Y for central males=248-8 m). This difference was not due to any difference in vigilance between peripheral and central lek males (Table I): it occurred simply because geometry ensures that if an approaching predator is first detected at any distance from the lek it will always be nearer to a peripheral male than to a central male. Mating patterns seen at Ishasha South lek were apparently not closely related to local variation in predation risk. Males that held relatively safe, central lek territories did have far higher rates of ejaculation (median=0-089/h, N = 2 2 territories) than males on riskier, peripheral territories (median=0-014/h, N=18; z=4-43, P<0-001). However, there was no fine-scale association between mean ejaculation rate and estimated predation risk for holders of different tek territories, even when risk was adjusted for male absenteeism (rs=0-085 and -0.010, respectively, N = 4 0 territories, NS).

DISCUSSION The analysis of skull distribution suggests that, for adult male kob, there is little difference in average predation risk between holding a lek territory and holding an isolated territory. The better physical condition of lek males may mean that, holding condition constant, leks are slightly riskier than single territories, but it seems unlikely that reduced predation risk is a major benefit of lek territory defence in kob (see also de Vos 1979; Bradbury & Gibson 1983; Beehler 1988; Clutton-Brock 1989). The same conclusion was reached for Lawe's parotia, Parotia lawesii, where annual mortality was similar for males that displayed on lek territories and males that held isolated display sites (Pruett-Jones 1985). High levels of predation by owls at mating aggregations of Antechinus stuartii have led to the suggestion that, in some years, increased predation risk may even be a considerable cost of lekking in this marsupial (Lazenby-Cohen & Cockburn, in press). At first glance, the results on overall predation risk to males on and off kob leks are paradoxical. Not only should larger group size on leks dilute predation there, but results from the predator detection experiment support earlier suggestions (e.g. Oring 1982) that, through a combination of reduced cover and increased total vigilance, males on leks detect predators sooner than do off-lek

animals. However, from the perspective of predators, leks are essentially stationary aggregations of prey animals and so represent exceptionally reliable food patches. Lions from both prides at Ishasha spent disproportionate amounts of time at kob leks, suggesting that they concentrated their predation effort there. Presumably, for predators, benefits such as reduced search costs, familiarity with local cover opportunities, and the high chance of finding vulnerable animals such as fighting males (Modha & Eltringham 1976; P. M611er & W. M611er, personal communication; personal observation), offset the disadvantage of the increased probability of detection at leks. Similar concentrations of predator activity have been reported at leks of topi (Rainy & Rainy 1989; Gosling & Petrie 1990) and Antechinus (Lazenby-Cohen & Cockburn, in press). A striking parallel with the situation at leks is found in the spatially fixed nests of colonial spiders, in which higher conspicuousness means that per capita risks of predation or egg parasitism are independent of, or even increase with, increasing nest size (Lubin 1974; Rypstra 1979; Smith 1982; Spiller & Schoener 1989; Hieber & Uetz 1990). While overall predation risk to males is apparently similar on and off kob leks, there is nevertheless substantial fine-scale variation in risk in the immediate vicinity of leks. As predicted by the selfish herd model (Hamilton 1971) we found that per capita risk for males was considerably higher around the periphery of our study lek than at its centre. Higher predation levels around the edges of stationary prey aggregations have also been reported for colonially nesting Ad61ie penguins, Pygoscelis adeliae (Tenaza 1971) and spiders (Rayor & Uetz 1990) (although the generality of higher risk around the periphery of such groups will depend on the mode of predator attack, see Trail 1987; Parrish 1989). Variation in predation risk at leks may have important consequences for the profitability of holding different lek territories. For instance, males on peripheral territories experience lower mating success than central lek males, and are also permanently exposed to a higher risk of predation. Net benefits of territory defence are presumably therefore lower for peripheral than for central territory holders (although this may be partially offset by relatively low fighting rates on peripheral territories, Balmford 1990). This in turn raises the question of why peripheral males join leks at all.

Balmford & TutTaho : Leks and predation in kob However, in the case of kob (unlike topi or fallow deer, Dama dama; Gosling & Petrie 1990; Thirgood 1991), it is clear that peripheral lek males achieve far higher long-term mating success than holders of single territories (Balmford 1990). Thus while defending a peripheral lek territory may be less profitable for a male kob than defending a central lek territory, it may still be associated with higher net benefits than defence of an isolated territory. Since male ungulates often experience higher predation risk than females (Kruuk 1972; Schaller 1972; FitzGibbon 1990), the data presented here permit firm conclusions about overall risk only for adult males. None the less, our results still shed some light on the hypothesis that reduced predation risk is a major benefit to females of mating on leks rather than on dispersed territories (Wittenberger 1978; Gosling 1986; Gosling & Petrie 1990). Like males, female kob detect predators sooner on leks than on single territories. Furthermore, oestrous females may be especially vulnerable to predation away from leks if harassment by young males forces them to leave large mixed-sex herds and travel in very small groups (Clutton-Brock 1989). Sexually receptive female kob might therefore minimize their risk of predation by mating on leks, particularly since they tend to aggregate on central territories. Against this suggestion it should be noted that predators also aggregate at kob leks, that lek centres are apparently no safer than areas distant from leks, and that in order to get to the centre of a lek, oestrous females must pass through an area of enhanced risk around the lek periphery (Fig. 4). The distribution of the few female skulls that we did find provides some indication of the danger associated with the lek periphery: six of the 11 collected along census lines and on and around Ishasha South lek were in off-lek sectors immediately adjacent to the lek, even though on average only 10% of the live females in those areas were found around the lek (this sample was too small for meaningful statistical analysis). A further problem with the hypothesis that females mate on leks in order to avoid predators is that it fails to explain the wider issue of the intraspecific and interspecific distribution of lek-breeding, and in particular, the variable incidence ofleks (present in some years but not in others) in a number of ungulate populations (such as fallow and sika deer, Cervus nippon, in Europe) that lack predators altogether (Langbein & Thirgood 1989; Balmford et al., in press b). In view of these problems, we would tentatively

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suggest that the overall balance between improved predator detection and increased predator pressure at leks may apply to female kob as well as males, and that oestrous females may therefore gain no net anti-predator benefits by mating on leks. However, more data on predation of oestrous females on and off leks are clearly required. Our results also allow us to consider the hypothesis that fine-scale variation in predation risk is important in determining patterns of female mate choice within leks (Partridge & Halliday 1984). In so far as predation risk to males does reflect risk to females, higher risk around the periphery of leks suggests that the tendency of females to mate on central lek territories might in part reflect choice for spending time in areas of lower predation risk. However, on a finer scale, we found no evidence that within-lek variation in predation risk was closely correlated with the distribution of matings at Ishasha South lek; indeed, three of the four busiest territories were immediately adjacent to bushes in which lions were seen to hide. Our failure to find a detailed correlation between the distribution of matings and predation risk may in part have been due to fine-scale scattering of skulls by predators and scavengers (which could have introduced considerable noise into our measures of risk on each territory, but still not affected the coarse-scale relationship between skull and carcass distribution reported in the Methods; S. Boutin, personal communication). Nevertheless, given the marked differences in mating success seen even between males holding adjacent lek territories of apparently similar anti-predator value (Gosling & Petrie 1990; personal observation), it seems unlikely that variation in predation risk alone is capable of explaining mating patterns seen at leks. Lastly, although our results indicate that predator avoidance may not be the principal factor favouring lek-breeding in kob, spatial and temporal variation in risk may be important in finetuning certain aspects of lekking behaviour. For example, the greater visibility around leks than single territories suggests that minimization of risk may in part account for the location of leks; leks were usually sited in areas of open grassland, whereas single territories were often in woodland (Buechner 1961; Balmford 1990; see also McKaye et al. 1990). Moreover, a detailed analysis of mating patterns seen at Ishasha South lek revealed, not surprisingly, that male mating success declined

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markedly in response to the immediate presence of lions on the lek (Balmford et al., in press a). Similar effects of temporal variation in predation risk on patterns of lek activity have been reported for a variety of lekking birds, fish and frogs (Hartzler 1974; Tuttle et al. 1982; M c K a y e 1983; Trail 1987; Green 1990).

ACKNOWLEDGMENTS We thank the National Research Council of U g a n d a and the Boards of Trustees of U g a n d a National Parks and the Uganda Institute of Ecology for permission to live and work at Ishasha. We are very grateful to Tim Clutton-Brock for suggesting the study, and to Steve Albon, Sarah Blakeman, Mike Evans, Mary Holt, Tony Katende and Roland Stevens for help with data collection. M.T. was supported by the U g a n d a Institute of Ecology, and fieldwork was funded by a N E R C Overseas Studentship to A.B. and by grants from Clare College, the Department of Zoology and the Board of Graduate Studies, Cambridge University; Sigma Xi; the Percy Sladen Memorial Fund; the Company of Biologists; and the H. E. D u r h a m Fund. Peter and Willi M r l l e r kept us mobile at Ishasha. Steve Albon and Sarah Blakeman helped in collating and analysing data. Steve Albon, Sarah Blakeman, Stan Boutin, Juan Carranza, Tim Clutton-Brock, Andrew Cockburn, James Deutsch, Clare FitzGibbon, Morris Gosling and Nigel Leader-Williams kindly commented on various drafts of this manuscript. This paper was written while A.B. was supported by a Research Fellowship at Girton College, Cambridge.

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