Effects of Relatedness, Dominance, Age, and Association on Reciprocal Allogrooming by Captive Impala

Ethology 94, 207-220 (1993) 0 1993 Paul Parey Scientific Publishers, Berlin and Hamburg ISSN 0179-1613

Animal Behaviour Graduate Group and Department of Physiological Sciences, University of California, Davis

Effects of Relatedness, Dominance, Age, and Association on Reciprocal Allogrooming by Captive Impala

MICHAEL S. MOORING & BENJAMIN L. HART

MOORING, M. S. & HART, E. L. 1993: Effects of relatedness, dominance, age, and association on reciprocal allogrooming by captive impala. Ethology 94, 207-220.

Abstract

Wild impala display a highly reciprocal allogrooming system that, by virtue of its frequency and high degree of reciprocity, is unique among ungulates. A herd of 35 free-ranging captive impala provided opportunity to examine the degree of reciprocity of allogrooming exchanges and the influence of relatedness, dominance, age and association on partner preferences and distribution of grooming between allogrooming partners. As in wild impala, the exchange of allogrooming bouts in the captive impala was highly reciprocal regardless of partners. Kinship and dominance had no influence on partner preferen'ze or distribution of grooming between partners. Although mothers showed a significant preference to allogroom with their unweaned offspring, this preference practi- cally disappeared with older offspring. Age-mates (no greater than 6 mo apart) tended to associate with one another and spatial proximity was positively correlated with grooming partner preference. It was not clear whether impala actively sought out age-mates for grooming, or randomly chose grooming partners from nearby age-mates. The failure to find a role for kinship and dominance is counter to what has generally been found in most Old World terrestrial primate studies. The absence of pronounced social influences, coupled with the known effectiveness of grooming in removing ectoparasites, suggest that a utilitarian role, especially removal of ticks, is an important function of the impala reciprocal allogrooming system.

Corresponding author: Benjamin L. HART, Department of Physiological Sciences, School of Veterinary Medicine, Universicy of California, Davis, CA 95616, USA.

Introduction

Reciprocal allogrooming, in which partners alternately exchange grooming bouts, is a frequent occurrence in impala (Aepyceros melampus) between females of breeding herds and between males of bachelor herds (HART & HART 1992; JARMAN 1979). The frequency and high degree of reciprocity in grooming between

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208 MICHAEL S. MOORING & BENJAMIN L. HART

partners make this behavior unique among ungulates. An analysis from wild impala revealed that allogrooming received on the head and neck of adult females resulted in about half the grooming coverage per m2 surface area that impalas typically deliver to the rest of the body through self oral grooming (HART et al. 1992). The prominence of allogrooming in impala and their tendency to form closely spaced groups invites a comparison of allogrooming in impala with allogrooming in some primate species where social position and relatedness influence choice of grooming partner and distribution of grooming between partners. Among various species of macaques, for example, allogrooming occurs mostly among related individuals (MASSEY 1977; MISSAKIAN 1974; SADE 1972; SILK 1982). Between partners the grooming may be disproportionately directed to the dominant animal and is often seen in the context of diversion of aggressive attacks and reinforcement of alliances. These influences are documented for vervet monkeys (SEYFARTH & CHENEY 1984) and some species of macaques (SILK 1982; DEWAAL & LUTTRELL 1989). There is very little information on the influence of social roles in allogrooming by non-primate species. An examination of the role of kinship and dominance in allogrooming by impala would contribute to understanding the degree to which allogrooming systems in non-primate species involve social functions. An influence of kinship and/or dominance on partner preference and distribution of grooming would suggest that allogrooming could function in social roles in impala, whereas a lack of influence of kinship and dominance would point to more utilitarian functions, namely ectoparasite removal and skin care of body parts that an animal cannot groom with its own mouth. Absence of the social influences of kinship and dominance would also be consistent with the viewpoint that impala allogrooming is one of the few legitimate examples of the tit-for-tat model of evolved cooperation (HART & HART 1992). This study took advantage of a captive herd of impala in a naturalistic setting at the San Diego Wild Animal Park (SDWAP) to address these issues.

Impala are a common, medium-sized antelope of savannah-woodland ecotones in eastern and southern Africa. Females are sedentary and highly gregarious, living in large, cohesive clans of 30-150 animals and occupying annual home ranges averaging 52 ha in Zimbabwe (MURRAY 1981, 1982). Females with unweaned young and juveniles live in breeding herds, while subadult and adult males form bachelor herds, and mature, high-ranking males hold territories during the breeding season (JARMAN 1979). In Zimbabwe, the average relatedness among clan females was estimated to be relatively low, between 0.03-0.07 for all females, and between 0.04-0.12 among age peers (MURRAY 1981). Bachelor herds are made up of dispersed juvenile males or displaced territorial males and are not related (JARMAN 1979; MURRAY 1981). JARMAN (1979) noted no evidence of a female dominance hierarchy in Serengeti impala.

The allogrooming behaviour consists of oral grooming delivered to the head or neck of the partner by means of scraping or “combing” with the lower incisor- canine complex, which is the same type of oral grooming utilized by impala during self-grooming. Like self oral grooming, allogrooming is delivered in bouts of usually 5-10 grooming episodes. Allogrooming in adults is delivered to the head and neck of the partner. A typical allogrooming encounter begins with one

Reciprocal Allogrooming in Captive Impala 209

individual approaching another and delivering a bout of oral grooming. The recipient then usually returns a bout, and the exchange of bouts is continued in the alternating fashion until one partner fails to return a bout (HART & HART 1992). In a previous study, newborn impala were found to reciprocally allogroom with other fawns and unrelated adults by the second week after birth, exchanging grooming bouts at the same rate as adults (MOORING & HART 1992).

Methods

Subjects

The impala herd, which numbered 35 individuals in Year 1 (1988) and 38 in Year 2 (1989), was housed in the 50-ha East Africa enclosure at SDWAP, along with 13 other species of East African ungulates. All animals were individually marked, and ages were known through zoo records. During this time the herd size and composition approximated that found in the wild. One mature sire male was present, and the area of the enclosure fell within the natural home range size (MURRAY 1982). The impala were free to graze ad libitum on Kikuyu grass (Pennisetum caldenzsetum) found throughout the enclosure, and their diet wa:; supplemented with herbivore pellets. Vegetation sampling and examination of animals within the enclosure indicated that it was tick-free. Observations were made from mid- Jun. through Aug. in each year.

Sampling

Daylight observations were made with a 15-60 X zoom spotting scope primarily between the hours of 06.00 and 12.00 h, from a point overlooking the herd at a distance of 5&200 m. Age classes were designated according to age at the start of observations each year: fawns, < 6 mo; juveniles, 6-17 mo; adults, > 17 mo. Observations were made on 20 adult females, 5 juveniles, and 9 fawns in Year 1 and on 23 adult females, 9 juveniles, and 5 fawns in Year 2. The herd male was never observed to allogroom and was not included in the observations. The sampling methods were focal animal sampling (Year 1 only) and sampling all occurrences of certain behaviours (ALTMANN 1974). Focal samples were used to record individual differences in allogrooming; they were 20 min in duration and totalled 181 h. Group observations (sampling all occurrences of reciprocal allogrooming) were designed to maximize the number of reciprocal allogrooming encounters recorded. During group observations all or part of the herd was observed and occurrences of reciprocal allogrooming among partners recorded. Group observations totalled 243 h. For data analysis one partner was designated as focal. The ear notches and ear tags of individual impala could be identified through the spotting scope. The data were recorded on a Tandy 102 portable computer.

Grooming Definitions

Reciprocal allogrooming was directed to the partner’s head, neck, or ears in alternating bouts. A single grooming scrape is cermed a grooming episode, and a sequence of episodes by one partner comprises a bout. A reciprocal allogrooming exchange between a pair is termed an encounter. The individual who delivered the first bout of allogrooming was the initiator, and the partner, whose failure to return a bout resulted in the termination of the encounter, was the terminator.

Grooming partner preference of a particular animal for another animal was defined as the number of encounters observed between the two animals, divided by the total number of encounters observed between the first partner and all partners, multiplied by 100. There were 1971 encounters in Year 1 and 4446 encounters in Year 2 and preference was calculated from all encounters. Encounters that were prematurely ended by interruption or disturbance, and one-way grooming of females directed towards their fawns were discarded from the analysis unless otherwise indicated. The reciprocity index was a measure of grooming symmetry between partners within an encounter, and was calculated as the numtier of bouts or episodes delivered by an impala divided by the number of bouts or episodes delivered and received by that impala. Reciprocity could range between 0 and 1 , with perfect svmmerry reflected as 0.5.

Echolog!, Vol. 94 ( 3 ) 15

210 MICHAEL s. MOORING & BENJAMIN L. HART

Dominance

In the context of this paper, dominance refers to dyadic relationships and not to a hierarchical rank within the herd. Dominance relationships among adult females were determined on the basis of the supplanting that occurred while feeding and during aggressive interactions such as head-butting or chasing. The individual that moved away after being supplanted o r butted was deemed subordinate.

Relatedness

Relatedness among all impala was calculated from genealogical records kept by SDWAP since the establishment of the herd in 1971. At that time, the founder females were transferred to the park from the San Diego Zoo where impala were first introduced from wild Kenyan populations in 1960. Family trees were constructed based upon the SDWAP records of maternal and paternal parentage and the coefficient of relatedness was calculated between every pair of individuals appearing in the dataset (n = 1332). Because the herd contained only one sire male at a time, impala born into the same cohort were usually half-siblings. For purposes of analysis, the coefficients of relatedness (r) were categorized as follows: closely related, r = 0.5-0.25; intermediately related, r = < 0.25-0.0625; distantly related, r = < 0.0625.

Age and Association

The birthdate of each animal was known from SDWAP records. The age difference in months was calculated for the 1332 pairs in the dataset. For analysis, age difference was categorized as follows: small, < 6 mo; medium, 6-12 mo; large, > 12 mo. Because birthing was relatively synchronous in both years, with most fawns born in Jun. and JuI., all individuals falling within the small age difference category were age-mates.

Nearest neighbor scans were performed at 5-min intervals throughout all focal observations. The nearest neighbor was designated as the individual that was closest to the focal, measured head-to- head (but no more than four body lengths away) in the previous 5-min period. In order to separate nearest neighbor data from grooming partner preference, if a neighbor engaged in reciprocal allogrooming with the focal animal during the previous 5-min scan period, it was not counted as a nearest neighbor. This procedure had the effect, however, of underestimating the degree to which nearest neighbors were a preferred grooming partner. Association was an index of spatial proximity to the focal, defined as the number of nearest neighbor scans in which a particular animal was the nearest neighbor of the focal animal divided by the total number of scans made on the focal, multiplied by 100. Based upon the empirical distribution of association values, association was categorized as low, < 5; medium, 5-10; and high, > 10.

Data Analysis

Data were statistically analyzed using non-parametric procedures (DANIEL 1990). Mann- Whitney, Wilcoxon signed-rank and Spearman rank correlations were performed on the StatView programme (FELDMAN & GAGNON 1986), while the Sign and Binomial tests were done by hand. Analysis of Variance (ANOVA) was performed on the mainframe SAS version 6.06 (SAS INSTITUTE 1989). Multiway ANOVA on ranks for unbalanced designs (CONOVER 1980) were performed by using the SAS GLM procedure on ranked data with random and test options to calculate the quasi-F statistics and Satterthwaite approximate degrees of freedom. Unless otherwise stated, all tests were two-tailed with the level of significance set at 0.05.

ANOVA was used to analyze the relationship between relatedness, dominance, age, and association on grooming partner preference, and on parameters of allogrooming between specific grooming partners consisting of grooming delivered and received, reciprocity, and percentage of encounters initiated and terminated by either partner. The dataset for partner preference consisted of the preference values for every animal in the herd for which data were collected (Year 1 : n = 951 dyads; Year 2: n = 1206 dyads). For parameters of allogrooming, a subset of dyads for which at least four encounters were observed was selected on the dataset (Year 1: n = 48 dyads; Year 2: n = 125 dyads), with each dyad unique in the dataset (i.e., dyad AB, in which A was the focal and B was the partner, did not also appear as dyad BA).

By analyzing dyadic data with ANOVAS, a problem of non-independence arises. Because there can be allogrooming measurements for n-1 dyads per animal, none of those n-1 measurements are

Reciprocal Allogrooming in Captive Impala 21 1

independent. Furthermore, even though there are potentially n(n- 1)/2 pairwise combinations in the herd, there are only n degrees of freedom (for example, the 1206 preference dyads in Year 2 are based upon n = 36 animals). An alternative method of analysis would have been to perform randomization tests by generating hypothetical distributions of no association for comparison with the observed distributions. However, this procedure would not have allowed multivariate analysis which we felt was essential for teasing out the effect of concurrently operating social factors by controlling for different factors simultaneously. Nor would it have allowed interaction effects to be examined. Therefore, we dealt with the issue of independence in the following way: For ANOVAS that tested preference, the identity of the focal animal (to whom the preference values referred) was included as a classification factor in the ANOVA in order to control for the individual animal effect. When testing parameters of allogrooming based upon a subset of grooming partners, the identity of both partners was included as a category in the ANOVA in order to control for the individual effects of both partners. As an additional precaution against pseudo-replication by inflating the degrees of freedom in the ANOVAS, a fixed-effects analysis was performed. Ranked data were used because we were not confident that the stringent as:jumptions required for parametric analysis were met by our dataset. We felt justified in using ranked ANOVAS because ANOVAS performed on the raw data (transformed and untransformed) produced qualitatively the same results. Residual plots from the ranked analysis produced a “shotgun effect” of randomly scattered residuals, indicating that the assumption of homogeneity of variance was met.

Results General Observations

Allogrooming was directed to the head, ears, and neck of the partner as bouts of usually 6-2C episodes, with partners alternating in delivering bouts (Fig. 1). Although limited visibility made it impossible to distinguish between licking and teeth scraping in every case, in all those encounters in which tongue and teeth could be seen (about 50 %), allogrooming was performed with the lateral incisor-canine complex. Reciprocal allogrooming encounters involved a mean of 4.7 bouts per encounter and 14 episodes per bout (weighted means of both years). In Year 2 (the year in which the most encounters were observed), the impala were observed to allogroom with a mean (+ SE) of 21.7 (+ 0.9) partners, which was almost % of the available 36 partners in the herd. Overall grooming symmetry within encounters was close to perfect (Fig. 2 ) . Taking the individual mean reciprocity scores of 20 adults and five juveniles observed during both years, the grand mean reciprocity was 0.51 (k 0.02) for bouts, and 0.50 (k 0.03) for episodes, which was not significantly different from 0.5 (one-sample t-test: p > 0.5).

Fig. 1: Typical allogrooming exchange as shown between a jiivenile and an adult female impala. Illustra- tion drawn from a photograph by

Emma ALLEN

, 5::


cn 3 CI

8

8 -

0 2 4 6 8 i a

Fig. 2: Illustration of the degree of reciprocity of grooming bouts delivered and received by all impala. The 45" line represents perfect reciprocity. Only one animal of a pair is plotted; there are fewer points than allogrooming encounters because in several encounters the same number of bouts were

exchanged

Bouts received

The mean percent of allogrooming initiations that were reciprocated was 70.5 (2 2.1) YO. The initiator did not generally continue to deliver grooming unless the partner reciprocated. Considering all reciprocal allogrooming encounters observed among juveniles and adults in both years, 355 initiations were not reciprocated. Of these, the initiator terminated grooming upon failure of the would-be partner to reciprocate in 85.4 % of cases. In only 12.4 % of non- reciprocated initiations did the initiator deliver a second bout, and in 2.3 % of instances three to five bouts were given before terminating.

The structure of allogrooming exchanges among impala at SDWAP appeared to be virtually identical in organization to that engaged in by impala in the wild including the high degree of reciprocity and tendency of the initiator to not deliver a second bout if its first bout was not reciprocated (HART & HART 1992). The only difference noted in allogrooming compared with wild impala was that SDWAP female adults commonly (40 Yo of encounters) appeared to solicit allogrooming by approaching a potential partner and lowering the head and neck, thus making the head and neck region accessible to grooming. The characteristic neck presentation posture was observed in about 75 % of encounters.

Relatedness

In order to test whether close relatives were preferred as grooming partners over more distant relatives, we examined whether allogrooming was distributed according to the coefficient of relatedness. A three-way ranked ANOVA was conducted with the focal animal, relatedness, and age difference as the classification factors, and preference as the response variable. Mother-offspring dyads were omitted from the analysis because they were expected to exhibit high preferences. However, subsequent inclusion of mother-offspring data did not change the significance. As revealed in Fig. 3, degree of relatedness had little influence on partner preference. ANOVA revealed no significant effect of relatedness on preference value in either Year 1 [F(2,77) = 0.64, p = 0.531 or Year 2


Fzg. 3: Grooming partner preference as function of degree of relatedness expressed as X (2 SE) for Year 1 and Year 2. Partners are categorized as closely (C). in- rermediately (I) or distantly (D) related. The number above tach bar represents number of dyads. There were no significant effects of relatedness on preference. Preference, defined in the text, reflects the degree to which an impala groomed with one partner compared with all other groom-

ing partners

55 ' t 1

C I D C I D

Year 1 Year 2

[F(2,94) = 1.20, p = 0.311. If anything, there was a tendency for impala to prefer to groom with more distant relatives or non-relatives.

Although close relatives were not preferentially chosen as partners, preferential treatment might be given when the partner is closely related, for example by delivering more grooming bouts or episodes. The possibility that relatedness affected parameters of allogrooming within an encounter was tested by conduct- ing a four-way ranked ANOVA with focal animal and partner (to control for individual animal effect of the partners), relatedness, and age difference as classification factors, and the following as response variables: number of bouts or episodes delivered or received per encounter, total bouts or episodes delivered plus received per encounter (an index of encounter duration), reciprocity for bouts and episodes, and percentage of encounters initiated or terminated by the focal. Mother-offspring dyads were omitted from the analysis, but subsequent inclusion did not change the significance. Neither relatedness nor age difference had a significant effect on any of the grooming parameters in either year.

It is possible that impala may not be capable of distinguishing among grooming partners with different degrees of relatedness other than mothers and their offspring. To test this possibility, a two-way ranked ANOVA was performed with focal animal and class of partner (mother-fawn offspring, mother-adult offspring, non-mother-offspring) as classification factors. Maternal one-way grooming directed to a fawn was omitted. Mother-offspring relationship had a significant effect on preference in both years [Year 1: F(2,1107) = 18.8, p = 0.0001; Year 2: F(2,1143) = 8.4, p = 0.00021. Schefft multiple comparisons showed that mothers and their fawn offspring preferred one another as grooming partners over non-offspring in both years, and mothers and fawn offspring preferred one another as partners over mothers and adult offspring in Year I , but not in Year 2 (Fig. 4). Comparing preference among mother-offspring dyads only, mother-fawn offspring exhibited a significantly higher preference (about twice as much) over mothers and their adult offspring in both years [Year 1: F(1,40) = 8.4, p = 0.006; Year 2 : F(1,49) = 5.2, p = 0.031.

214 MICHAEL. s. MOORING & BENJAMIN L. HART

"I, t I 5

15

8

5

C

t 10

n

5

0 F A N F A N

Year 1 Year 2

Fig. 4: Comparison of grooming partner preference for mothers with fawn offspring (F}, mothers with adult or juvenile offspring (A), and mothers with non-offspring partners (N), expressed as mean (k SE) preference. Compari- sons are shown for Years 1 and 2. The number above each bar represents number of dyads. Differences are significant between mother-fawn offspring and non-offspring for both years and between mother-fawn and mother-adult offspring in Year 1 only. Preference, defined in the text, reflects the degree to which an impala groomed with one partner compared with all other grooming

partners Dominant-subordinate Status

88 % of all supplantation and agonistic interactions among adult females (n = 98) were directed from older to younger animals, indicating that dominance in the SDWAP herd was basically age-graded. To examine the influence of dominance we used the larger dataset of Year 2. Dyads were selected in which the dominance relationship had been observed and in which four or more allogrooming encounters were observed. The 21 dyads which emerged were analyzed pairwise (dominant vs. subordinate) using the sign test to examine the one-tailed prediction that (a) preference values of subordinates for dominants would exceed preferences of dominants for subordinates, and (b) reciprocity values would be greater for subordinate partners, indicating that subordinates delivered more grooming than they received. As shown in Table 1, preference, reciprocity and

Table 2: Comparison of dominant and subordinate members of allogrooming pairs with regard to measures (2 ? SE) of preference of dominant for subordinate or subordinate for dominant, and

distribution of grooming during an encounter (n = 21)

I Measure Dominant Subordinate I Preference for Partner'' 13.9 (k 9.9) 13.3 ( 2 9.6) Reciprocity

Bouts 0.48 (? 0.13) 0.52 (? 0.13) Episodes 0.48 (? 0.15) 0.52 (k 0.15)

Bouts delivered per encounter 2.9 (? 1.4) 3.0 ( 2 1.3) Episodes delivered per encounter 46 (k 31) 48 (k 33) % Encounters initiated 0.43 (k 0.31) 0.57 (? 0.31) % Encounters terminated 0.52 (k 0.19) 0.48 (2 0.19)

Preference, defined in the test, reflects the degree to which an impala groomed with one partner compared with all other grooming partners.

Eeciprocal Allogrooming in Captive Impala 215

other measures of distribution of grooming for dominants and subordinates were very close to being tht: same and were not significantly different (p > 0.2). In other words dominance appeared to have no influence of partner choice or distribution of grooming within an encounter.

Impala were occasionally observed to interrupt an allogrooming encounter already in progress. I n Year 2 (for which the most data were available) 71 interruptions (4.1 %) were observed out of a total of 1713 encounters. Of these, in 28 instances the interrupting individual was dominant and supplanted one of the grooming partner:;, and in eight of these supplantations the interrupter initiated grooming with a remaining partner (which in three cases was reciprocated by the remaining partner). In five instances the interrupter was groomed first by the remaining partner. In the other 15 supplantations, the interrupter was not groomed by either of the original partners.

Age Difference

In contrast to the absence of an effect of relatedness, Fig. 5 reveals that impala clearly preferred partners with a small age difference over those with a medium or large difference. The three-way ANOVA for preference involving relatedness and age difierence as classification factors revealed that age difference had a highly significant effect on preference in both Year 1 [F(2,81) = 28.3, p < O.OOOI] and Year 2 [F(2,79) = 29.4, p < O.OOOI]. There was a significant interaction effect between age class of focal animal and age difference as well (p < 0.005). To investigate whether this effect differed among age classes, we ran separate three-way ANOVAS on fawns, juveniles, and adults. Age difference was significant for all age classes (Table 2), but the F statistic was much larger, and the p-value generally smaller, for fawns [Year 1: F(2,16) = 284.5, p < 0.0001; Year 2: F(2,8) = 144.2, p < O.OOOl] compared with juveniles [Year 1: F(2,lO) = 5.6, p < 0.02; Year 2: F(2,16) = 9.2, p < 0.0021 or adults [Year 1 : F(2,41) = 3.9, p < 0.03;

169 f

h t g . 5: Grooming preference as function of age difference expressed a X (+ SE) for Y e n 1 and Year 2. The numbcr above each bar represents number of dyads. Preference for age peers with a small difference (S: < 6 mo) was si:- nificantly greater than for partners with a medium (M: 6-12 mo) o r large (L: > 12 mo) age difference. Prefer- ence, defined in the text, reflects the degree to which .in impala groomed with one partner compared with ,111

other grooming partners

S M L S M L

Year 1 Year 2


Year 2: F(2,26) = 14.4, p < 0.00011. Scheffe multiple comparisons showed that fawns initiated grooming more often with age-mates than with any other partner, and did not distinguish between partners of medium or large age differences in Year 2, although they did so in Year 1 (Table 2). O n average, fawn preference for age-mates was between 9-25 times greater than preference for other partners.

Table 2: Preference of female impala fawns, juveniles, and adults for grooming with partners of small, medium, or large age difference (number of animals is indicated)

Grooming partner preference Partner age difference Year 1 Year 2

Preference n Preference n

Fawns Small (< 6 mo) Medium (6-12 mo) Large (> 12 mo)

Small (< 6 mo) Medium (6-12 mo) Large (> 12 mo)

Small (< 6 mo) Medium (6-12 mo) Large (> 12 mo)

Juveniles

Adults

7.2 0.6 0.8

6.0 2.7 1.9

4.4 2.8 2.5

81 45 b

145 c

36 a 66 b 77 b

37 a 53 b

411 b

16.2 0.8 0.7

5.6 2.9 1 . 1

4.5 4.4 2.0

20 a 40 b

110 b

80 a 82 ab

144 b

69 a 112 a 549 b

‘i Preference, defined in the test, reflects the degree to which an impala groomed with one partner compared with all other grooming partners.

‘f’t Different letters in the same column indicate significance (p < 0.05).

Association

In order to examine whether impala preferentially groom with those partners with whom they associate in most, a 3-way ranked ANOVA was performed using focal, age difference, and association as classification factors. Data from Year 1 only (n = 951 dyads) were included because this was the only year that focal observations were made. Mother-offspring dyads were omitted. With age difference controlled for, association had a highly significant effect on grooming partner preference [F(2,105) = 11.3, p < O.OOOI]. Likewise, age difference remained highly significant with association controlled for [F(2,86) = 14.9, p < O.OOOl]. Scheffi multiple comparisons showed that high, medium, and low association levels predicted corresponding levels of preference. Spearman’s correlation revealed a positive correlation between preference and association (rs = 0.35, p < O.OOO1) and a negative correlation between age difference and association (rs = -2.22, p < O.OOOl) , indicating that age peers were the most frequent nearest neighbors. Association was not correlated with relatedness (rs = 0.01, p = 0.4), showing that close kin did not preferentially associate. This was because,


although half-sibling age-mates showed a preference to associate and allogroom with one another, other close relatives, namely mothers and weaned offspring, or full siblings, did not.

Discussion

Impala in the SDWAP herd performed reciprocal allogrooming in a pattern that was almost identical to that observed in wild populations. The same high degree of reciprocity evident in Kenyan impala (HART& HART 1992) was found in SDWAP impala. One notable difference between SDWAP and Kenyan impala was that SDWAP female adults frequently made use of the neck presentation posture to solicit grooming prior to the start of an encounter; this behaviour was not observed in Kenyan impala.

Because of the absence of comparable data it was not possible to tell if the social structure or social relationships in the captive herd were more pronounced than in wild impala herds. Certainly with a closed herd one could expect, if anything, stronger soci.xl influences than the ephemeral kinship bonds and weak dominance hierarchy reported for wild female impala (JARMAN 1979; MURRAY 1981). Yet at SDWAP there appeared to be little influence of social factors on impala allogrooming. The coefficient of relatedness did not predict grooming partner preference among herd members, nor did it influence distribution of grooming bouts or episodes within allogrooming encounters. Mothers and fawn offspring showed a high preference for one another as grooming partners, as seen in other ungulates (equids: TYLER 1972; cattle: REINHARDT & REINHARDT 1981; mule deer: MOORING 1989). However, mothers and their older, weaned offspring preferred to groom one another only half as much as mother-fawn pairs, and their grooming preference approached the average shown among non-kin. This would indicate that the preferential grooming relationship that existed with young, nursing offspring diminished as the offspring matured. In another study (MOOR- ING & HART 1992) of impala fawn allogrooming at SDWAP it was found that by the second week after birth most fawns engaged in much more reciprocal allogrooming with non-mother adults than with mothers. In SDWAP adult female impala, dominance status between partners had no effect on grooming partner preference, reciprocity, initiation or termination of encounters, o r grooming bouts and episodes delivered. Although comparable data are not available for wild females, in Kenyan impala dominance status between bachelor males had no influence on initiation or distribution of grooming (HART & HART 1992).

The lack of influence of relatedness and dominance is in contrast to allogrooming in other ungulate species where dominance influences reciprocity and partner preference (equids: CLUTI-ON-BROCK et al. 1976; TYLER 1972; WELLS & VON GOLDSCHMIDT-ROTHSCHILD 1979; cervids: HALL 1983; HIRTH 1977; MILLER 1971). The lack of these influences on allogrooming in impala is also in contrast to the typical pattern seen in some Old World primate species where, as mentioned in the introduction, kinship and dominance influence the distribution of grooming within the troop. It should be mentioned, however, that other studies have cast doubt upon the universal influence of kinship (DE WAAL & LUTI-RELL 1989;


EHARDT 1988; ROWELL 1991) and dominance rank (COELHO et al. 1983; STAMM- BACH 1978) on allogrooming relationships in primate species.

Impala of all age classes at SDWAP preferred to groom and to associate with age-mates. In a previous study of SDWAP impala, fawns born in the same season preferentially interacted among themselves through group play activities, resting together in nursery groups, and reciprocally allogrooming (MOORING & RUBIN 1991). The same pattern of association was also noted in wild impala of Zim- babwe (MURRAY 1981) and the Serengeti (JARMAN 1979). It is not clear whether impala mostly allogroom with age-mates, and therefore preferentially associate with age peers, or if they associate with age peers for some other reason, and allogroom at random with the nearest animal.

Various lines of evidence suggest that the unusual features of impala reciprocal allogrooming may have evolved in response to the threat of tick infestation in their natural environment. Ticks deplete body resources, thereby presenting a strong selective force for the occurrence of grooming which is effective in removing ticks (reviewed by HART 1990). The brushy, open woodland habitat favored by impala throughout Africa is reported to support high densities of ticks (LONDT & WHITEHEAD 1972; NORVAL 1977; PETNEY & HORAK 1987). Impala are unique among the smaller antelope in being attended by oxpeckers (HART et al. 1990), and because oxpeckers depend upon ticks foraged from their hosts for the mainstay of their diet, oxpecker attendance can be taken as an indirect measure of relative tick infestation. Impala possess an incisor-canine dental comb aligned so as to effectively comb the pelage with the upward sweeping head movement characteristic of oral grooming (MCKENZIE 1990). Cementing over the dental comb on one side of the body in wild impala resulted in an 8-fold increase in adult ticks on the affected side compared with the uncemented side (MCKENZIE, pers. comm.). The same type of teeth combing seen in self-oral grooming is seen in allogrooming.

Regular bouts of self-grooming supplemented with reciprocal allogrooming to the head and neck may be important in order to remove ticks before they can attach and engorge. As argued elsewhere (HART et al. 1992), natural selection could have favored impala that engaged in a baseline level of programmed self- grooming and allogrooming independent of immediate tick stimulation in order to remove ticks before they attach and engorge. Thus, the fact that SDWAP impala allogroomed in a tick-free environment cannot be taken to mean that allogrooming does not have a tick-control function in the wild. SDWAP impala also engaged in regular bouts of self-grooming (HART et al. 1992). If impala engage in reciprocal allogrooming in order to remove ticks from body regions not accessible to self-grooming with the incisor-canine dental comb, then social factors may not be of primary importance in determining with whom to allogroom.

Acknowledgments

We are grateful to the Zoological Society of San Diego for granting us access to the impala of the San Diego Wild Animal Park, and in particular for the assistance of L. KILMAR, D. LINDBURG, R. MASSENA, R. RIECHES and their staff. M. OWREN modified the computer sampling programme to our


needs, and N. WILLITS provided statistical advice. MSM was funded by a Distinguished Scholar Award and a Regents Fello~vship from the University of California, Davis, as well as by awards from Sigma Xi, the Scientific Research Society, and Graduate Research Awards from the University of California, Davis.

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Documents

Effects of Relatedness, Dominance, Age, and Association on Reciprocal Allogrooming by Captive Impala