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

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 preference or distribution of grooming between partners. Although mothers showed a significant preference to allogroom with their unweaned offspring, this preference practically 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.     

Reciprocal Allogrooming in Wild Impala Lambs

Adult impala engage in a form of reciprocal allogrooming distinguished by a high degree of reciprocity and ***lack of influence of dominance or relatedness on partner preference or distribution of grooming between partners. A previous study on reciprocal allogrooming of captive newborn impala lambs in a zoological park found that the allogrooming emerged as early as the first week after birth and was identical in structure and reciprocity to allogrooming in adults. Because these findings of apparently unique allogrooming behavior of newborn impala could have been a reflection of the effects of being born and raised in a small, stable captive herd, it was necessary to investigate reciprocal allogrooming in newborn impala in the wild. The emergence, reciprocity, rate, and partner distribution of reciprocal allogrooming in wild newborn impala were observed at two study sites: a national park in Zimbabwe and a game farm in South Africa. Maternal one-way grooming between mother and newborn emerged as distinct from reciprocal allogrooming and rapidly declined after week 1 postpartum. Reciprocal allogrooming by lambs was first seen between 5 and 8 d postpartum, and as soon as the behavior occurred it was the same basic pattern as seen in adult impala. The reciprocity index for lambs was near 0.5, indicating that lambs delivered as much grooming during an encounter as the partner. Lambs were grooming frequently with non-mother adults and other lambs by week 1 or 2; by week 3 and onward the allogrooming rate of lambs was more than twice that of their mothers, as predicted by the body size principle of the programmed grooming model. The strong predisposition of neonatal impala lambs to deliver reciprocal allogrooming as early as the first or second week postpartum would appear to reflect a genetically acquired adaptation to the threat of tick infestation in their natural habitat.     

Allogrooming in two species of macaque (Macaca nemestrina andMacaca radiata)

This paper analyzes allogrooming (social grooming) data collected from two large, fully integrated and long established social groups of macaques (one of pigtail macaques and one of bonnet macaques). The data demonstrates a species and sex difference for total allogrooming given with females of both species giving more grooming than the males and with pigtails as a species giving more grooming than bonnets. Also, pigtail females gave more allogrooming to clan members than to nonclan members, but this was not true for pigtail males, bonnet males, and bonnet females. Allogrooming given and allogrooming received by age class for both species showed development of a sexual dichotomy at three to four years. The analysis characterized some of the social structures extant in two closely related species of macaque, particularly the somewhat different use of allogrooming in pigtail females as opposed to the other three categories of animals. Social implications with relation to macaque societies are discussed.     

Nursing behavior and early development of impala at San Diego Wild Animal Park

Because impala are commonly exhibited and handreared in zoos and their natural nursing behavior had not previously been studied, we examined nursing and early development in five impala calves housed in a large, naturalistic enclosure. Calves were observed for the first 5 weeks of life during 12-hr continuous watches and 20-min focal animal samples. Total daily suckling time decreased while time grazing and feeding on concentrates increased from 1–5 weeks of age. An increasing proportion of nursing bouts were terminated by the dam as calves matured, with dams terminating almost 70% of bouts during the first week. Suckling success and maternal grooming also decreased after week I, suggesting that impala mothers cut back early on nursing and grooming of offspring. Rapid decline in mother-young spatial proximity and a concomitant increase in calf association with age-mates over time suggests that the mother-young bond is weak and ephemeral in impala. An example of the implications of our results for improving handrearing programs would be that newborn calves should be started on a daylight feeding schedule of one bottle-feeding every three hours, and that they not be allowed to gorge themselves at any one of these feedings.     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

How Rainfall Variation Influences Reproductive Patterns of African Savanna Ungulates in an Equatorial Region Where Photoperiod Variation Is Absent

In high temperate latitudes, ungulates generally give birth within a narrow time window when conditions are optimal for offspring survival in spring or early summer, and use changing photoperiod to time conceptions so as to anticipate these conditions. However, in low tropical latitudes day length variation is minimal, and rainfall variation makes the seasonal cycle less predictable. Nevertheless, several ungulate species retain narrow birth peaks under such conditions, while others show births spread quite widely through the year. We investigated how within-year and between-year variation in rainfall influenced the reproductive timing of four ungulate species showing these contrasting patterns in the Masai Mara region of Kenya. All four species exhibited birth peaks during the putative optimal period in the early wet season. For hartebeest and impala, the birth peak was diffuse and offspring were born throughout the year. In contrast, topi and warthog showed a narrow seasonal concentration of births, with conceptions suppressed once monthly rainfall fell below a threshold level. High rainfall in the previous season and high early rains in the current year enhanced survival into the juvenile stage for all the species except impala. Our findings reveal how rainfall variation affecting grass growth and hence herbivore nutrition can govern the reproductive phenology of ungulates in tropical latitudes where day length variation is minimal. The underlying mechanism seems to be the suppression of conceptions once nutritional gains become insufficient. Through responding proximally to within-year variation in rainfall, tropical savanna ungulates are less likely to be affected adversely by the consequences of global warming for vegetation phenology than northern ungulates showing more rigid photoperiodic control over reproductive timing.     

英国惠普斯耐德獐的育幼行为

1993年5-8月在英国惠普斯耐德野生动物园半自然条件下研究了獐（）的单亲育幼行为。描述了母幼獐建立关系,母獐的探访和育幼行为,授幼行为,舔犊行为以及母幼间距离等。研究结果表明,母獐昼夜间仅探访幼兽4-5次。初生獐寻找乳头时往往寻错位置,找向母獐的前胸和颈区。在幼獐出生后的早期,哺乳行为的启动是由母獐启动的,但幼獐一周龄后即为启动者。平均哺乳时段为48.2±10.2s.母獐的舔犊行为常与哺乳同时发生,舔犊的位置最常见于幼獐的头部（62.7%）,其次是肛殖区（13.9%）,再是背部（8.4%）,肋部（7.2%）,胸部（5.6%）和颈部（2.1%）。此外,还讨论了母兽对不同性别的幼獐的投资的差异及其生物学意义。     

Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate

Seyfarth's model assumes that female primates derive rank-related benefits from higher-ranking females in exchange for grooming. As a consequence, the model predicts females prefer high-ranking females as grooming partners and compete for the opportunity to groom them. Therefore, allogrooming is expected to be directed up the dominance hierarchy and to occur more often between females with adjacent ranks. Although data from Old World primates generally support the model, studies on the relation between grooming and dominance rank in the New World genus Cebus have found conflicting results, showing considerable variability across groups and species. In this study, we investigated the pattern of grooming in wild tufted capuchin females (Cebus apella nigritus) in Iguazú National Park, Argentina by testing both the assumption (i.e., that females gain rank-related return benefits from grooming) and predictions (i.e., that females direct grooming up the dominance hierarchy and the majority of grooming occurs between females with adjacent ranks) of Seyfarth's model. Study subjects were 9 adult females belonging to a single group. Results showed that grooming was given in return for tolerance during naturally occurring feeding, a benefit that higher-ranking females can more easily grant. Female grooming was directed up the hierarchy and was given more often to partners with similar rank. These findings provide supporting evidence for both the assumption and predictions of Seyfarth's model and represent, more generally, the first evidence of reciprocal behavioural interchanges driven by rank-related benefits in New World female primates.     

Differential grooming rate and tick load of territorial male and female impala, Aepyceros melampus

During the breeding season in Zimbabwe territorial male impalawere found to engage in much less self oral grooming and allogroomingthan females, presumably as a reflection of the need to remainvigilant in herding females and repulsing challenging bachelormales. Territorial males spent an average of 11 min engagedin all types of grooming during a 12-h day, compared with 40min grooming by females. Rutting activity and time spent scanningpeaked in May, while self oral grooming and feeding by territorialmales was lowest at this time. The decrement in grooming bymales (relative to females) represented half of all time devotedto rutting behaviors. Territorial males appeared to sacrificefeeding and grooming time in exchange for more time devotedto vigilant activities essential to mating success. In a comparableregion of Zimbabwe, territorial males were also found to harborabout six times as many adult ticks as the females on the sameterritories during the breeding season. Because grooming isunderstood to be effective in removing ticks, the higher tickload of territorial males was attributed to their reduced groomingbehavior. However, testosterone and adrenal cortical steroids,which are elevated in territorial male impala, are known todepress the immune system, and so may be important in controllingparasite infections. Sexually active males of many species aregenerally found to harbor more parasites than females. The differencein tick load between territorial male and female impala mayreflect both behavioral and hormonal parameters.     

Impala social behaviour: birth behaviour

Data collected from observations of eighteen parturient impala females are presented. Females attempt to isolate from the breeding herds 2 to 3 h before parturition. They have a characteristic appearance and behaviour at this stage and are having obvious labour contractions. Nearly all the females sought some cover and a vegetation type including many bushes was used frequently as a birth site. Only four of eleven females left the herd and found cover without harassment by either the territorial male or bachelor males. Many were also followed by impala females. The birth process is described; final expulsion of the foetus occurs in a recumbent position. All birth fluids and membranes are eaten by the mother. Much attention is paid to cleaning up the birth site, baby and herself. Time from birth to expulsion of the placenta is variable and the placenta is normally eaten as soon as it is expelled. Impalas can stand at about 15 min after birth and attempt to suckle soon after this. Only some mothers help the baby to find the udder. Unsteady running occurred at about 25 min after birth. Impalas have a preference for giving birth between 10·00 and 14·00 hours. The significance of this behaviour and the other behaviours shown as anti-predator devices are discussed. Individual differences in behaviour and early care of the young are noted.     

The evolution of parasite-defence grooming in ungulates

Grooming repertoires are exhibited by all terrestrial mammals, and removal of ectoparasites is an important ancestral and current function. Parasite‐defence grooming is regulated both by a central control mechanism (programmed grooming model) and by cutaneous stimulation from bites (stimulus‐driven model). To study the evolution of parasite‐defence grooming in ungulates, we compared species‐typical grooming behaviour with host morphology and habitat to test predictions of the programmed grooming model while taking into account phylogenetic relatedness. We observed grooming in 60 ungulate species at ectoparasite‐free zoological parks in which the confound of differential tick exposure was controlled for and stimulus‐driven grooming was ruled out. Concentrated‐changes tests indicated that sexually dimorphic grooming (in which breeding males groom less than females) has coevolved with sexual body size dimorphism, suggesting that intrasexual selection has favoured reduced grooming that enhances vigilance of males for oestrous females and rival males. Concentrated‐changes tests also revealed that the evolution of complex oral grooming (involving alternate use of both teeth and tongue) and adult allogrooming (whereby conspecifics oral groom body regions not accessible by self grooming) was concentrated in lineages inhabiting closed woodland or forest habitat associated with increased tick exposure, with such advanced grooming being most concentrated in Cervidae. Regression analyses of independent contrasts indicated that both host body size and habitat play a role in the evolution of species‐typical oral grooming rates, as previously reported. These results indicate that the observed grooming represents centrally driven grooming patterns favoured by natural selection in each lineage. This is the first phylogenetically controlled comparative study to report the evolution of parasite‐defence grooming behaviours in response to selection pressures predicted by the programmed grooming hypothesis. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81 , 17–37.     

Allogrooming as mutualism in diurnal lemurs

Recent work on allogrooming in Primates has demonstrated the value of considering both its physical and its social aspects. Most studies have been conducted on anthropoid primates only. Here, the grooming interactions of anthropoids and those of diurnal lemurs are contrasted, with special reference to their mutuality. It is shown that lemur grooming appears more intimate and has a far greater component of mutuality than is the case among anthropoids. It is argued that the latter finding reflects a difference between the two taxa in the forms of their agonistic interactions: in anthropoid primates, grooming is thought to be related to patterns of agonistic support in triadic interactions, while in lemurs, agonistic interactions are dyadic and allogrooming is more directly reciprocal.     

灵长类相互理毛的影响因素、功能及其利益分析

理毛行为是动物行为学研究的主要内容之一,根据理毛的对象可分为自我理毛(Autogrooming)和相互理毛(Allogrooming),其中相互理毛是灵长类重要的社会行为。现在认为相互理毛可能与社会参量(亲缘关系、性别、年龄、等级制度、繁殖状况等)有联系,并且有一定的社会功能。本文论述了理毛行为的分类、影响相互理毛的因素、相互理毛功能假说及其相互理毛的投入-收益分析,以便人们对相互理毛的行为进行更深入的研究。     

滇金丝猴雌性个体间的理毛行为

相互理毛行为广泛存在于社会性群居灵长类动物中,通常具有清洁卫生和社会交往功能。2012 年10 月至2013 年6 月,我们在云南白马雪山国家级自然保护区对一人工辅助投食滇金丝猴群,采用全事件取样法和焦点动物取样法收集了雌性个体间相互理毛的行为数据,包括理毛的部位、理毛的姿势、理毛的时间和回合数。研究结果表明:滇金丝猴雌性个体之间每次相互理毛的平均时间为5. 7 min。相互理毛部位较多的发生在自我理毛不能进行(达到)的部位(61.1% );在不能自我理毛部位的相互理毛行为持续时间长,平均9.7 min;在个体能够进行自我理毛部位的相互理毛持续时间短,平均为3. 2 min。相互理毛的姿势以对坐为主(48. 4% ),不同理毛姿势的理毛时间差异显著。新迁入家庭单元的雌性个体为理毛的首先发起者,但其获得被理毛的时间却并不多。滇金丝猴雌性个体相互理毛部位、理毛姿势和理毛时间的差异表明,它们之间的相互理毛行为符合卫生功能假说和社会功能假说。     

Altruism among non-relatives: alternatives to the 'Prisoner's Dilemma'

Triver's model of reciprocal altruism, and its descendants based on the Prisoner's Dilemma model, have dominated thinking about cooperation and altruism between non-relatives. However, there are three alternative models of altruism directed to non-relatives. These models, which are not based on the Prisoner's Dilemma, may explain a variety of phenomena, from allogrooming among impala to helping by non-relatives in cooperatively breeding birds and mammals.     

Allogrooming by adult Callithrix jacchus in relation to postpartum oestrus

The allogrooming behaviour of the parents (= α-animals) of three family groups of Callithrix jacchus has been studied during 25 days following birth. A total of 22 postpartum periods has been analysed. We recorded significant increase of grooming activity beginning with the 5th day postpartum. Allogrooming initiated by invitation gesture dropped to one-tenth of the total allogrooming frequency within one week, starting from day 5 postpartum. As a rule, allogrooming activity increased abruptly, whereas the decrease was mostly continuous, lasting several days. The maximum of postpartum allogrooming frequency preceded to some extent the maximum of copulatory activity and sexual willingness of the ♀. The ♂ made more attempts to groom the ♀ than vice versa. Up to the 18th day postpartum the ♀ ♀ ended more grooming sessions than the ♂ and than during anoestrus. The ♀ ♀ refused more invitations to grooming than did the ♂ ♂. The analysis of postpartum grooming behaviour in C. jacchus does not allow for accurate determination of the first and last day of the postpartum oestrus.     

Techniques for evaluating humoral and cell-mediated immunity in mule deer fawns (Odocoileus hemionus).

Twenty mule deer fawns (Odocoileus hemionus) were removed from their dams 48 h after birth, and hand-reared. Methods for monitoring their immune capability are described. Passive humoral immunity was determined by serum protein electrophoresis. Active humoral immunity following Clostridium toxoid vaccination was determined by immunodiffusion. Cell-mediated immunity was assayed using contact sensitization to 1-nitro, 2,4-dichlorobenzene (DNCB).     

Social behaviour and infant carrying in a group of moustached tamarins,Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla,Peruvian Amazonia

The social behaviour of a group of eight moustached tamarins,Saguinus mystax, (five males, three females) was studied on Padre Isla in northeastern Peru. About 60% of all allogrooming was done by the two adult males in the group, and about 11% by a young adult female. All other group members groomed very little. The adult breeding female received more grooming than any other group member. After the death of the adult female (preyed upon by an anaconda) the amount of active allogrooming remained constant for all group members except for the young adult female, who increased her contribution to about 30%. Her preferred grooming partner was the subadult female, which generally screamed when being groomed by the young adult female and terminated grooming by going away. This kind of grooming relation is termed “forced grooming” and is interpreted as a possible social control mechanism. The young adult female groomed the adult males more often after the death of the adult female than before. This might have had the function of strengthening the social bond with the adult males and in obtaining the breeding position in the group. After the death of the adult female, the vulva of the young adult female grew to full adult size. Agonistic behaviour was less frequent than allogrooming. Most aggressive interactions (50%) originated from the subadult male of the group. The young adult female was the target of most of these aggressions. Extremely little aggression occurred between the three females. The young adult female was the only individual who tried to emigrate from the group during the study period. Her attempt to join a neighbour group failed due to rejection by all four members of this group. All group members participated in carrying an infant, but the adult males and the young adult female carried most frequently. Contribution to infant carrying varied with the infant's age.     

Allogrooming, partner choice, and dominance in male anubis baboons

This study was designed to test the hypothesis that among unrelated male baboons (Papio cynocephalus anubis) in single-gender social groups there is no significant association between dominance status and allogrooming performance. The hypothesis was tested using behavioral measures obtained by focal animal sampling techniques. The results indicate that unrelated male baboons established well-defined linear dominance hierarchies, formed allogrooming relationships with one another, and exhibited a nonrandom distribution of allogrooming; however, there were no significant relationships between dominance rank and the frequency of allogrooming. We further tested our results by grouping individuals into three dominance status classes (high, middle, and low) and comparing the classes. Analysis of variance demonstrated no significant differences in rates of allogrooming by dominance class. These results suggest that dominance did not account for the variation in observed allogrooming behavior: Dominance status did not appear to determine the frequency with which animals groomed others, the number of grooming partners, or frequency of grooming that any individual received in comparison to that performed. High-ranking animals did not have significantly more grooming partners than low-ranking animals, and there appeared to be little competition within the groups for subordinates to groom high-ranking animals. When age, kinship, and group tenure are controlled, performance and reception of allogrooming are not strongly associated with dominance in single-gender social groups of male anubis baboons.     

Effects of cohort,sex, and birth date on body development of roe deer (Capreolus capreolus) fawns

We investigated the effects of the year of birth (cohort effect), sex and birth date on the variations observed in birth weight and postnatal growth rate in 209 newborn fawns marked during eight consecutive fawning seasons from a highly productive roe deer population under good nutritional conditions. Roe deer exhibited a fast body development with a birth weight of 1628 g and a postnatal growth rate of 139 g/day constant over the first 20 days of their life. As previously reported for dimorphic and polygynous ungulates, there was a marked cohort effect on the rate of body development. This variability was partly explained by climatic conditions during late gestation. When fewer than 5 days with rainfall over 5 mm occurred in April, fawns were heavier. High temperatures during April and during the winter could also be involved in fast body development of roe deer fawns. Sex of fawn did not affect roe deer growth pattern. This was expected on the basis of low sexual dimorphism in size and low polygyny level characteristic of roe deer. Lastly, the date of birth did not affect the body development of roe deer fawns. High constancy of mean birth dates and high synchrony of births observed in this population could account for this result.