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.     

The function of allogrooming in domestic cats (Felis silvestris catus); a study in a group of cats living in confinement

Grooming interactions (n=83) occurring in a group of non free-ranging adult neutered male (n=14) and female (n=11) domestic cats (Felis silvestris catus) were analysed. Grooming was not induced by the proximity (distance <=0.5 m) of another animal. Grooming was in general directed at the head-neck area. Higher ranking animals groomed lower ranking animals more often than the other way round. Groomers tended to adopt ‘higher’ (standing, sitting upright) postures than groomees (sitting, lying). Agonistic behaviour occurred in 35% of interactions. Groomers showed offensive behaviour more often than groomees, most often after grooming a partner. Furthermore groomers often groomed themselves after grooming a partner. The degree of relatedness of animals did not affect the frequencies or durations of grooming. These results are consistent with the hypothesis that allogrooming in domestic cats may be a way of redirecting (potential) aggression in situations in which overt aggression is too costly. The data were previously presented at the 29th International Congress of the International Society for Applied Ethology (van den Bos, R. (1995) Allogrooming in domestic cats in confinement, Proceedings of the 29th International Congress of the International Society for Applied Ethology, S.M. Rutter et al. (Eds.), pp. 109–110)     

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 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.     

Grooming patterns in Verreaux's sifaka

Lemur grooming has received very little attention in the literature. Nevertheless, allogrooming in lemurs has been suggested to be fundamentally different from the grooming of anthropoids. One reason is that lemurs generally rely on oral rather than manual grooming. Lemur allogrooming has also been suggested to serve less of a social function than has been attributed to anthropoid grooming. I analyzed the allogrooming behaviors of 29 Verreaux's sifaka (Propithecus verreauxi) living in five social groups in the Kirindy Forest of Madagascar. Based upon 1,586 observation hours, I found that sifaka, like anthropoids, spend very little time mutual grooming (2±3%). Half of all allogrooming involved parts of the body that could have been easily groomed by the recipient, such as the limbs. Even though ectoparasite loads are expected to be greater during the rainy season, allogrooming did not increase during the rainy season. Allogrooming rates were influenced by both rank and sex, and increased by 50–100% during the mating season. The results of this study suggest that allogrooming in Verreaux's sifaka plays an important social function, even though it is performed with a toothcomb. Am. J. Primatol. 72:254–261, 2010. © 2009 Wiley‐Liss, Inc.     

Stimulating effect of sugar dusting on honey bee grooming behaviour

The aim of this research was to investigate whether or not sugar dusting can stimulate the grooming behaviour in Apis mellifera L. (Hymenoptera: Apidae), an important defensive mechanism against Varroa destructor Anderson & Trueman (Acari: Varroidae), and to assess the most effective dose and frequency of treatment. The criterion for evaluation of grooming potential was the percentage of damaged mites (PDM) among the total number collected on the bottom boards of the hives. In each sugar‐treated group PDM was significantly higher in comparison both with the negative control (no treatment) and with the values preceding the treatment. The results point to a stimulating effect of sugar on the grooming behaviour at all doses and frequencies tested. Treatment frequency influenced the stimulating effect of sugar: treatments at 3‐ and 7‐day intervals with 30 and 40 g resulted in significantly higher PDMs than the least frequent treatment (every 14 days); dusting with 20 g influenced PDM only when repeated at 3‐day intervals. Because treatments at 3‐day intervals are time‐consuming, those with 40 or 30 g repeated every 7 days may be recommended. In the positive control (hives treated with amitraz), average PDM was significantly lower than in the negative control and all sugar‐treated groups. Possible causes of the stimulating effect of sugar dusting on bee grooming behaviour are discussed.     

Reciprocal Allogrooming in Dam-reared and Hand-reared Impala Fawns

Among adult females and males of African antelope impala are unique in their performance of reciprocal allogrooming. The occurrence of this behaviour in neonatal impala fawns was explored in a free-ranging impala herd at the San Diego Wild Animal Park where 5 dam-reared fawns were observed from birth through 10 weeks of age. One-way maternal grooming and reciprocal allogrooming with the dam and non dam partners emerged as distinct behavioural systems. Maternal grooming, directed mostly to the anogenital area, was typical of that seen in other ungulates, and sharply declined over the first two weeks. Reciprocal allogrooming, characterized by alternate exchanges of grooming bouts with a partner in the same manner as in adults, was seen as early as 3–8 d after birth. All fawns were grooming with unrelated adult females by the end of the second week. By week 2 virtually every measure of reciprocal allogrooming by fawns (grooming delivered per hour, reciprocity, and percent of encounters initiated) was as high as for adults. The appearance of this reciprocal allogrooming pattern, especially at such an early age, appears to be unique among ungulates, and possibly mammals in general. Three hand-reared impala fawns, deprived of the opportunity to interact with older herdmates, but having access to impala fawns and heterospecific fawns, were observed from 1–3 mo of age. The hand-reared impala showed no alteration in the occurrence of reciprocal allogrooming behaviour compared with the dam-reared control fawns, indicating that allogrooming experience with older animals was not required for the appearance of reciprocal allogrooming at an early age. Interestingly, hand-reared fawns persisted in grooming heterospecific fawns despite the fact that heterospecifics rarely reciprocated grooming. We postulate that the strong predisposition for impala young to groom others may be related to the threat of tick infestation in the impala's ecotone habitat.     

Plasticity of grooming behavior against entomopathogenic fungus Metarhizium anisopliae in the ant Lasius japonicus

Social insects employ many types of defense mechanisms against parasites and pathogens because they face high risks from infections due to crowded living conditions with closely related nestmates. Grooming behavior, including self-grooming and allogrooming, can remove fungal spores on the cuticles of social insects and may be a behavioral defense mechanism to improve survivorship. Allogrooming between nestmates has been predicted to be especially important as a defense against ectoparasites. However, little is known about the plasticity of grooming behavior in susceptible environments. Here, we show that the ant Lasius japonicus increases the frequency of allogrooming rather than self-grooming to improve survivorship against the entomopathogenic fungus Metarhizium anisopliae. We found that increasing fungal dosage and ant group size influenced the plasticity of grooming behavior. Additionally, the survival rate of the ants over 30 days improved with increased group size. Our results suggest that social insects opt for altruistic behavior to prevent the spread of diseases. This study illustrates how ants maintain colonies through grooming behavior in the presence of fungal spores.     

Grooming site preferences in wild white-handed gibbons (Hylobates lar)

During a four-month study of wild white-handed gibbons in Thailand one group was observed for 131 hr. The individuals spent 5.2% of their activity period allogrooming. Several body sites received more respectively less allogrooming than expected. Surface areas easy to clean by autogrooming such as the belly received significantly less allogrooming than expected. Upper body areas which are likely to be infested by parasites and other matter received significantly more allogrooming than lower body parts. Thus, grooming in gibbons seems to reflect a primarily hygienic function.     

Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama

I investigated the effect of the density of louse eggs (Pedicinus obtusus andP. eurygaster) on grooming site preferences in Japanese macaques (Macaca fuscata). Louse eggs were more often found on the outer side of the body (upper back, lower back, outer arms, and outer legs) than on the inner side of the body (chest, belly, inner arms, and inner legs). Japanese macaques were more likely to be groomed on the outer side than the inner side of the body by allogrooming and autogrooming. Such grooming site preferences correlated with the distribution of louse eggs but not with the areas of body parts. Thus, the ecology of lice might affect grooming behavior of Japanese macaques. Five hundred and fifty louse eggs were estimated to parasitize an adult female Japanese macaque. Considering the intrinsic rate of natural increase of lice, monkeys need to be groomed almost every day. This suggests that Japanese macaques need grooming partners and form social bonds with others for everyday grooming.     

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.     

Weaving a tight social net: Allogrooming in free-ranging female langurs (Presbytis entellus)

We studied grooming among adults of a one-male multifemale troop of free-ranging Hanuman langurs (Presbytis entellus)living near Jodhpur, India, for 9 years. The 11–13 females devoted about 6% of their day to allogrooming. Adult males, whose tenures averaged 2.2 years, were transient figures in the troop's history, as reflected by their rather peripheral role in the grooming network. Females groomed males 4–40 times more frequently (1006 episodes) than vice versa- (176 episodes). Adult females received 97% of all grooming from other adult females (6655 episodes). Although females exhibited an age- inversed dominance hierarchy, they did not compete for grooming access to particular troop mates. Dyads of all possible rank differences occurred as frequently as expected: 51% of grooming was directed up the hierarchy and 49% down it. Young, high- ranking individuals gave and received significantly more grooming than the oldest, low- ranking females did. The pattern seemed to be influenced by kin selection because of the presumably high degree of female relatedness. They invested most in troopmates with the highest reproductive value, i.e., the youngest individuals. This trend was coupled with a preference of closest kin (mothers and daughters). Reciprocity was the outstanding feature since all adult females groomed and were groomed by all others. Such a tight social net might establish the necessary cohesion during frequent territorial disputes with neighboring troops.     

Infradian rhythmicity in milk leukocyte activity together with plasma cortisol and prolactin levels throughout the lactation period in high-yielding crossbred cows

Infradian rhythmicity in milk leukocyte activity together with plasma cortisol and prolactin levels throughout the lactation period in high-yielding crossbred cows has been studied in 10 high-yielding (milk production: 5000 l per lactation) Karan Fries crossbred (Holstein Friesian × Tharparkar) cows. Milk and blood samples were collected from all the experimental animals. Isolation of milk phagocytes (neutrophils and macrophages) and lymphocytes were done by density gradient centrifugation. In vitro phagocytic index of milk neutrophils and macrophages was performed by colorimetric NBT reductive assay. Mitogen-induced milk lymphocyte blastogenic response was estimated by colorimetric MTT (tetrazolium) assay. Total plasma cortisol and prolactin were estimated by enzyme immune assay. Highest value of plasma cortisol and prolactin was observed at calving which decreased significantly (p < 0.01) on 15th day postpartum for both prolactin and cortisol. Immune activity of milk leukocytes was highest on day 0 colostrum and decreased significantly (p < 0.01) on 7th day postpartum. A significant (p < 0.01) rise of plasma prolactin was observed around 135th and 225th days postpartum, whereas a peak level of plasma cortisol was observed at 105th, 180^th, and 270th days postpartum. Phagocytic index of milk neutrophils and macrophages remains almost in a steady state during mid-lactation period (between 100 and 200 days postpartum). A decline in increasing trend of milk phagocytic activity was observed during late lactation. Mitogen-induced milk lymphocyte blastogenic response was highest on day 0 colostrum which decreased significantly (p < 0.01) on 15th day postpartum. Con A-induced milk lymphocyte blastogenic response showed an increasing trend from 120th to 210th days postpartum. Upon correlation study, it showed that the plasma cortisol has a negative effect on milk leukocyte activity, while prolactin has a positive effect, though the effect is lactation stage specific.     

Pre-copulatory behaviour in the male Mongolian gerbil: I. Differences in dependence on androgen of component patterns

Male behaviour patterns, including ultrasonics, olfactory investigation, grooming and sequences of following of oestrous females during the pre-copulatory period, were described for the Mongolian gerbil. Differences in dependence of these patterns on gonadal hormones were examined by measuring the rates of decline after castration and the degree of restoration following the subcutaneous injection of testosterone propionate (20 μg/2 days/animal). Castration and androgen therapy did not influence the performance of male genital grooming, allogrooming and the olfactory investigation of both female secretory products and the female's body, excluding the posterio-dorsal area. The other male patterns differed in the extent to which they were affected. Thus ventral gland marking, foot-stomping and sequences of follow/dart interactions declined rapidly and were not restored to pre-castration levels by androgen; whereas the upsweep ultrasonic vocalization and olfactory investigation of the female's perineal area declined more gradually, and were completely restored. These consistent differences in both decline and restoration suggest that mechanisms underlying some pre-copulatory patterns are influenced by androgen to a greater degree than others.     

Differential effects of kinship,dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata

An analysis of allogrooming (total times spent grooming individual partners) of 8 sexually mature females (3–12 years of age) in a captive group of 17 Japanese macaques, shows that during the nonmating season, grooming distributions were characterized by high proportions of grooming given to family members and/or higher ranking nonkin. During the mating season, all eight females showed significant shifts in their grooming distributions, and four females showed significant shifts in grooming between their nonestrous and estrous periods (defined behaviorally). Fox six of eight females, mating season grooming was characterized by either high proportions of grooming given to family members and/or heterosexual and homosexual partners. It was found that within dyadic sexual relationships, dominants gave more grooming to subordinates than the former received, in contrast to a reversal of this pattern in the majority of these same dyads during the nonmating season. This is interpreted as one short-term function of grooming: a dominant asymmetrically grooms a subordinate sexual partner to maintain proximity with (or reduce tension in) the latter. The two remaining focal females (middle ranking, nulliparous) differed from the other females in that they shifted their mating season grooming to subordinate nonkin, despite the lack of evidence that this was a result of sexual interactions, patterns of partner availability, competition, patterns of grooming reciprocity, or agonistic alliance support. From these results, it is suggested that in some contexts, grooming of subordinate nonkin may function to reduce tension in thegroomer. In the Japanese macaque, this latter possibility and the asymmetric grooming of subordinate homosexual partners may prove to be exceptions to the general rule that female cercopithecine grooming of nonkin flows up the dominance hierarchy.     

Relation of Intergroup Variation in Allogrooming to Group Social Structure and Ectoparasite Loads in Red Howlers (Alouatta seniculus)

We compare the allogrooming behavior of 5 troops (average size = 8.2) of red howlers (Alouatta seniculus) from the Venezuelan Llanos with that of other A. seniculus and Alouatta spp. of the genus. In 126.9 observation hr, we recorded 118 allogrooming events, with an average bout length of 109 sec. Females groomed more frequently than males did, but as groomees there is no significant differences between sexes. Adult males groomed adult females mostly in a sexual context (before copulation). Allogrooming rates differ significantly among groups. There are also significant differences among members of the same troop both as groomers and groomees, which we explain in the context of the social behavior and history of each troop. There is no significant correlation between weight of the groomee and duration of the grooming bout. However, the examination of grooming rates and ectoparasite load suggests that allogrooming may have hygienic consequences. Differences in allogrooming rates among species of Alouatta are related to differences in group kin structure and patterns of female competition, in particular, coalition formation. We conclude that the social structure and the degree of relatedness among individuals within a group (or among individuals in a population in interpopulation comparisons) is a more important determinant of allogrooming rate than body size or group size. Our results emphasize the importance of considering intergroup and interpopulational variation in behavior.     

The interaction of surface and dust particle size on the pick-up and grooming behaviour of the German cockroachBlattella germanica

The relationship between the particle size of an inert silica dust, its up-take from different surfaces and the grooming behaviour of males, gravid females, and fifth and sixth instar nymphs of the German cockroachBlattella germanica (Dictyoptera: Blattellidae) (L.) was investigated. The normal grooming behaviour of gravid females, nymphs and males differed according to sex and age. The gravid females and nymphs exhibited greater grooming activity than the males, especially of the antennae and the legs. Gravid females, nymphs, and adult males exhibited increased grooming activity after exposure to dust in the size range 0.5–63 μm, but there was no significant difference in grooming behaviour from the control when cockroaches were exposed to dust sizes greater than 70 μm. Antennal grooming by males was greater than leg grooming when exposed to all dust sizes, except size particles ranging 4.5–7.5 μm. A dust pick-up experiment indicated that the average amount of dust transferred toB. germanica is affected by particle size, the porosity of the treated surface, and the sex and age of the cockroaches. Gravid females picked up greater amounts of dust than fifth and sixth instar nymphs, which in turn picked up more dust than males. Silica dust particles (0.5–7.5 μm) were picked up more effectively than larger particle sizes, by all three categories, males, females and fifth and sixth instar nymphs of cockroach on all three test surfaces plastic, ceramic and unpainted plywood. Plywood was the least effective surface for transfer of dust, of all sizes, to males, females and nymphs.     

Protein synthesis in interspecies hybrid embryos of the amphibian Xenopus

The newly synthesized abundant proteins of early Xenopus laevis and Xenopus borealis embryos have been examined by two-dimensional electrophoresis after labelling with [³⁵S]methionine. Six prominent polypeptides specific to Xenopus laevis embryos and a further six specific to Xenopus borealis have been identified. Overall, embryos of the two species are estimated to differ by approx. 15% in their protein synthetic patterns from blastula to tailbud stage. Interspecific hybrid embryos (Xenopus laevis (♀)/Xenopus borealis (♂)) synthesise only the maternally specified set of proteins until gastrulation after which they produce the full complement of both Xenopus laevis and Xenopus borealis specific proteins. The possible use of such molecular markers of parental genome activity in facilitating further embryological study is discussed.     

A Quantitative Analysis of Secretion-Grooming Behaviour in the Water Bug Plea minutissima Leach (Heteroptera,Pleidae): Control by Abiotic Factors

The pigmy backswimmer, Plea minutissima, from time to time leaves the water to apply its antimicrobial metathoracic gland secretion to its water-repellent ventral pubescence (“secretion-grooming”) which is enclosed by an air sheath when submerged and has a respiratory function. Secretion-grooming keeps the hairs free of microbial contamination and thus hydrophobous and functional. The grooming behaviour is regulated by abiotic factors. It is released by an increase in light intensity or water temperature, with a sudden rise in temperature being particularly effective. The higher the temperature and light intensity, the faster the grooming act is performed and completed. The grooming motivation is higher at a higher ambient temperature, but declines once the behaviour has been brought to completion. As a consequence the highest grooming activity in the field is observed in summer on the first sunny day after a prolonged period of overcast days. The tying of secretion-grooming to abiotic factors probably serves to destroy epizoic microorganisms before they begin to multiply more rapidly at higher temperatures. The mechanisms regulating the secretion-grooming behaviour of Plea may be of significance also for the regulation of certain other insect behaviours (e.g., flight behaviour).     

The relative roles of kinship and reciprocity in explaining primate altruism

Several hypotheses have been proposed to explain the evolution of altruistic behaviours. Their relative roles in explaining actual cases of animal altruism are, however, unclear. In particular, while kin selection is widely believed to have a pervasive influence on animal behaviour, reciprocity is generally thought to be rare. Despite this general agreement, there has been no direct test comparing the relative roles of kinship and reciprocity in explaining animal altruism. In this paper, we report on the results of such a test based on a meta-analysis of allogrooming in primates, grooming being probably the most common altruistic behaviour among mammals. In direct contrast to the prevailing view, reciprocity played a much larger role than kinship in explaining primate allogrooming. These results point to a more significant role of reciprocity in the evolution of animal altruism than is generally acknowledged.
Ecology Letters (2010) 13: 45–50