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。     

Grooming and control of fleas in cats

Oral grooming is common in cats, as in rodent and bovid species where grooming has been shown to be effective in removing lice and ticks. In Experiment 1, we examined the effectiveness of oral grooming in removing fleas which are the main ectoparasite of cats. Elizabethan collars (E-collars) which prevented grooming were fitted on nine cats in a flea-infested household and 3 weeks later, flea numbers on these cats were compared with nine control cats in the same household. Flea numbers dropped in the control cats reflecting an apparent drop in adult fleas in the environment, but in the E-collar cats, flea numbers did not drop, and were about twice as numerous as in control cats. The significantly greater number of fleas on the E-collar cats was attributed to their inability to groom off fleas. In Experiment 2, videotaping of nine different cats from the flea-infested household revealed that these cats groomed at about twice the rate of 10 similarly videotaped control cats from a flea-free colony. These results reveal that flea exposure can increase grooming rate in cats and that grooming is effective in removing fleas.     

The Grooming Invitation Dance of the Honey Bee

The grooming invitation dance is a striking behavior in honey bee colonies that has not been extensively studied. The objectives of this study were (1) to describe the dance through video analysis, (2) to test the functional hypothesis that it is a grooming solicitation signal, and (3) to analyze the stimuli that cause its production. A worker bee producing the grooming invitation dance stands stationary and vibrates her whole body from side‐to‐side at a frequency of 4.2 ± 0.2 Hz for 9.3 ± 1.0 s. Sometimes the bee mixes bouts of body vibration with brief bouts of self‐grooming (average duration = 1.4 s). Bees that perform the grooming invitation dance have a far higher probability of being quickly groomed by a nest mate than do bees that do not perform the dance. Bees that had chalk dust puffed onto the bases of their wings produced significantly more grooming invitation dances than did control bees that received only puffs of air. This shows that it may be the accumulation of small particles at the bases of the wings that normally triggers the dance. We suggest that the evolutionary origin of this signal is self‐grooming behavior.     

Effect of resource competition on the long-term allocation of grooming by female baboons: evaluating Seyfarth's model

Seyfarth (1977, Journal of Theoretical Biology, 65, 671-698) proposed an influential model that explained the long-term patterning of grooming relationships between female primates in terms of an interaction between the idealized grooming objectives of females and competition for valuable grooming partners. A critical test of the model requires a demonstration not only that competition for partners exists, but also that females do have an underlying target for the amount of grooming that they would like to receive relative to the amount they need to give. As it is not possible to stipulate a priori what this target is, or to detect it directly, we assessed its applicability by making a set of predictions, within the framework of Seyfarth's model, as to how observed grooming patterns should change with changes in the intensity of resource competition. We tested these predictions with data from a troop of baboons, Papio hamadryas ursinus, for which the within-bout structure of grooming has already been shown to be sensitive to changes in resource competition (Barrett et al. 2002, Animal Behaviour, 63, 1047-1053). We found no evidence of competition for grooming partners and our results do not support the predictions of the modified model with respect to the existence of underlying grooming objectives. The findings that the grooming of female baboons is more diverse and that the mean rank distance separating partners increases when resource competition is greater, together with the absence of rank effects on long-term patterns, are, however, supportive of the recent biological market approach to social interactions. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Biosocial functions of grooming behavior among the common Indian langur monkey (Presbytis entellus).

An intensive study of the Indian langur monkey (Presbytis entellus) reveals an interplay between biological and social processes. This study which involved captive animals and over 1,500 observation hours suggests that grooming behavior alone cannot be used to measure status differences between the sexes, nor as a means to understand how pathogens carried by ecto-parasites are controlled. It is shown that the type of grooming exhibited in an interactional setting and the region of the body presented by one animal to another for grooming is often determined by the immediate social events and by the nature of the relationship existing between the participants. For these Colobine langur monkeys grooming behavior not only facilitates integration but it also enables an animal to manipulate a tense situation into a peaceful one. Without reference to many of the other patterns of behavior which only relatively, not absolutely differentiate age and sex classes, grooming behavior cannot be entirely understood.     

Allomaternal behavior in a group of free-ranging patas monkeys

A free-ranging group of patas monkeys (Erythrocebus patas) containing 18 individually identifiable adult females was observed for approximately 400 hours, equally distributed over two two-month periods corresponding to the breeding and birth seasons, at the La Parguera facility of the Caribbean Primate Research Center. The large number of infants born in the spring and early summer (n = 14) allowed for detailed observations of alloparental behaviors, with a focus on allomothering by the adult females. Seven types of alloparental behaviors were recorded: contact, nuzzling, grooming, agonism, close visual inspection, attempted kidnapping, and kidnapping. Adult females emitted the vast majority of allomaternal behavior, the patterning and frequency of which closely resembled the patterning and frequency of inter-adult female social grooming. Relative dominance status of the participants did not consistently predict the directionality of allomothering. The most commonly observed allomaternal behaviors were contact and nuzzling, which are primarily affiliative behaviors; agonism was rare. Successful kidnapping occurred eight times. Immature monkeys (n = 22) emitted an additional 32 alloparental acts. A propensity towards allomothering by experienced females would be most beneficial to patas infants due to the patas' tendency towards dispersed foraging and rapid flight in the presence of danger. It is possible that direct competition with groups of rhesus macaques for available resources on the island served as a proximal cause for the allomothering observed in this patas group.     

Visualizing the Effects of a Positive Early Experience,Tactile Stimulation,on Dendritic Morphology and Synaptic Connectivity with Golgi-Cox Staining

To generate longer-term changes in behavior, experiences must be producing stable changes in neuronal morphology and synaptic connectivity. Tactile stimulation is a positive early experience that mimics maternal licking and grooming in the rat. Exposing rat pups to this positive experience can be completed easily and cost-effectively by using highly accessible materials such as a household duster. Using a cross-litter design, pups are either stroked or left undisturbed, for 15 min, three times per day throughout the perinatal period. To measure the neuroplastic changes related to this positive early experience, Golgi-Cox staining of brain tissue is utilized. Owing to the fact that Golgi-Cox impregnation stains a discrete number of neurons rather than all of the cells, staining of the rodent brain with Golgi-Cox solution permits the visualization of entire neuronal elements, including the cell body, dendrites, axons, and dendritic spines. The staining procedure is carried out over several days and requires that the researcher pay close attention to detail. However, once staining is completed, the entire brain has been impregnated and can be preserved indefinitely for ongoing analysis. Therefore, Golgi-Cox staining is a valuable resource for studying experience-dependent plasticity.     

A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys

Social grooming in primates is a complex behavior in which monkeys stroke, pick, or otherwise manipulate a companion’s body surface. While grooming has been associated with important social functions, researchers who have examined its physical characteristics, such as body site preferences, have focused on its role in skin care and ectoparasite removal. Whether the form of social grooming is constrained primarily by utilitarian or social functions was empirically tested by directly comparing this behavior with self-grooming, which was assumed to have primarily utilitarian functions. Predictions made concerning social grooming, based on a comparison with self-grooming, were tested by examining site preferences, duration of grooming (overall and to specific body sites), and method of grooming (stroking, picking, or a combination of the two) in rhesus monkeys. None of these predictions was verified. The physical characteristics of social grooming could not be predicted from the way an animal groomed itself. There was no relationship between site preferences in these two types of grooming. Animals groomed others for longer periods of time than they groomed themselves, both overall and when grooming specific sites. The methods these animals used differed markedly in self-and social grooming: they primarily picked at their own hair or skin but, when grooming others, varied their technique across sites, stroking the hair where it was thickest and picking where the hair was sparse. These results suggest that utilitarian functions are not the most important factors constraining the form of social grooming.     

Effects of MDMA Injections on the Behavior of Socially-Housed Long-Tailed Macaques (Macaca fascicularis)

3,4-methylenedioxy-N-methyl amphetamine (MDMA) is one of the few known molecules to increase human and rodent prosocial behaviors. However, this effect has never been assessed on the social behavior of non-human primates. In our study, we subcutaneously injected three different doses of MDMA (1.0, 1.5 or 2.0mg/kg) to a group of three, socially housed, young male long-tailed macaques. More than 200 hours of behavioral data were recorded, during 68 behavioral sessions, by an automatic color-based video device that tracked the 3D positions of each animal and of a toy. This data was then categorized into 5 exclusive behaviors (resting, locomotion, foraging, social contact and object play). In addition, received and given social grooming was manually scored. Results show several significant dose-dependent behavioral effects. At 1.5mg/kg only, MDMA induces a significant increase in social grooming behavior, thus confirming the prosocial effect of MDMA in macaques. Additionally, at 1.5 and 2.0 mg/kg MDMA injection substantially decreases foraging behavior, which is consistent with the known anorexigenic effect of this compound. Furthermore, at 2.0 mg/kg MDMA injection induces an increase in locomotor behavior, which is also in accordance with its known stimulant property. Interestingly, MDMA injected at 1.0mg/kg increases the rate of object play, which might be interpreted as a decrease of the inhibition to manipulate a unique object in presence of others, or, as an increase of the intrinsic motivation to manipulate this object. Together, our results support the effectiveness of MDMA to study the complex neurobiology of primates’ social behaviors.     

Establishing Meal Patterns by Lickometry in the Marmoset Monkey (Callithrix jacchus): Translational Applications From the Bench to the Field and the Clinic

The ability to measure and interpret variables associated with feeding behavior and food intake is essential to a variety of nonhuman primate study modalities. The development of a technique to accurately and efficiently measure food intake and meal patterning in captivity will enhance both the interpretation of foraging behavior in the wild as well as our ability to model clinically relevant human feeding pathologies. In this study, we successfully developed the use of a rodent lickometer system to monitor meal patterning in captive common marmosets. We describe the modifications necessary for this type of instrumentation to be used successfully with marmosets. We define variables of interest that relate to both previous rodent literature and human clinical measures. Finally, we relate our findings to potential translational value for both primate field research and biomedical applications. Am. J. Primatol. 74:901‐914, 2012. © 2012 Wiley Periodicals, Inc.     

Market powers predict reciprocal grooming in golden snub-nosed monkeys (Rhinopithecus roxellana)

Social grooming is a common form of affiliative behavior in primates. Biological market theory suggests that grooming can be traded either for grooming or other social commodities and services. When no other services are exchanged, grooming is predicted to be approximately reciprocated within a dyad. In contrast, the amount of reciprocal grooming should decrease as other offered services increase. We studied grooming patterns between polygamous male and female in golden snub-nosed monkeys (Rhinopithecus roxellana) from the Qinling Mountains of central China and found that about 29.7% of grooming bouts were reciprocated. However, the durations of grooming bouts offered and returned was asymmetrical within dyads. In bisexual dyads, more grooming was initiated by females than males, which became more pronounced as the number of females per one-male unit increased. The rate of copulation per day for each female was positively correlated with the total duration of grooming time females invested in males.. Females without an infant (non-mothers) directed more grooming towards females with an infant (mothers) and were significantly more likely to be non-reciprocated. There was a significant negative relationship between non-mother and mother grooming duration and the rate of infants per female in each one-male unit. High-ranking females also received more grooming from low-ranking females than vice versa. The rate of food-related aggressive interactions was per day for low-ranking females was negatively correlated with the duration of grooming that low-ranking females gave to high-ranking females. Our results showed that grooming reciprocation in R. roxellana was discrepancy. This investment-reciprocity rate could be explained by the exchange of other social services in lieu of grooming.     

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。     

Peptide-induced excessive grooming in the rat: The role of opiate receptors

We have investigated the possibility that opiate peptides induce excessive grooming behavior in the rat via a direct action on an opiate receptor by comparing the opiate agonist dynorphin(1–13) with its non-opioid fragment des-tyrosine¹-dynorphin(1–13) (dT-Dyn). We have shown that both peptides are capable of inducing grooming and that this behavior can be suppressed by pretreatment with naloxone. Analysis of the grooming pattern revealed that the response induced by dT-Dyn is qualitatively similar to that induced by ACTH(1–24) and dynorphin(1–13). Cross-tolerance was demonstrated among the various peptides. We conclude that peptide-opiate receptor interaction is not the primary event in the induction of grooming and that the opiate receptor(s) involved are located at another site underlying peptide-induced grooming.     

Grooming and group cohesion in primates: implications for the evolution of language

It is well established that allogrooming, which evolved for a hygienic function, has acquired an important derived social function in many primates. In particular, it has been postulated that grooming may play an essential role in group cohesion and that human language, as verbal grooming or gossip, evolved to maintain group cohesion in the hominin lineage with its unusually large group sizes. Here, we examine this group cohesion hypothesis and test it against the alternative grooming-need hypothesis which posits that rates of grooming are higher in species where grooming need (i.e. the motivation to groom for hygiene and its associated psychological reward) is more pronounced. This alternative predicts that the derived social function of grooming evolved mostly in those lineages that had the highest exposure to ectoparasites and dirt, i.e. terrestrial species. A detailed comparative analysis of 74 species of wild primates, controlling for phylogenetic non-independence, showed that terrestriality was a highly significant predictor of allogrooming time, consistent with the prediction. The predictions of the group cohesion hypothesis were not supported, however. Group size did not predict grooming time across primates, nor did it do so in separate intra-population analyses in 17 species. Thus, there is no comparative support for the group-cohesion function of allogrooming, which questions the role of grooming in the evolution of human language.     

Interommatidial sensilla of the praying mantis: Their central neural projections and role in head-cleaning behavior

The compound eye of the praying mantis is covered with approximately 600 bristles and campaniform sensilla. Their afferents project to the brain, and to the suboesophageal and prothoracic ganglia. Cutting the eye branch of the dorsal tegumentary nerve (DTN), the peripheral nerve innervating the corneal sensilla, makes it impossible to initiate head grooming by tactile stimulation of the eye. This stimulus is a strong releaser of grooming behavior in normal animals. Head grooming can be initiated, after cutting the eye branch of the DTN, by stimulation of the frons (the operation leaves the sensory innervation of this part of the cuticle intact). Frame-by-frame analysis of films of head grooming after cutting the nerve reveals a reduction of the speed at which the forelimb is brushed across the surface of the head and eye. The significance of this finding is discussed in terms of a putative feedback loop from the corneal sensilla to the motor neurons controlling the grooming movements.     

Thermal constraints on activity scheduling and habitat choice in baboons

The importance of thermoregulation as a constraint on behavior has received comparatively little attention in relation to other ecological factors. Despite this, a number of studies suggested that high temperature may represent an important ecological constraint. This paper examines the impact of temperature on activity scheduling in a troop of chacma baboons (Papio hamadryas ursinus) at De Hoop Nature Reserve, South Africa. Once the daily, seasonal, and individual effects were controlled for, the "perceived environmental temperature" (PET), which accounts for the relative contributions of solar radiation, wind speed, and humidity on shade temperature, was a significant constraint on behavior. With high PET, feeding declines, and there is an increase in grooming and particularly resting behavior. Baboons thus engage in more sedentary behaviors as temperature increases, with significantly higher levels of resting and grooming when temperature exceeds the approximate thermal neutral zone for baboons. Seeking shade is an important behavioral response to thermal stress, and PET was a significant determinant of whether an animal was in shade while engaged in either resting or grooming behavior. Furthermore, the proportion of time spent in shade increased across air temperatures that were below, within, and above the thermal neutral zone for baboons. Finally, since resting and grooming are conducted preferentially in certain habitat types, thermoregulatory considerations also impact on patterns of habitat choice and day-journey routes. This suggests that the thermal environment is an ecological variable that should be given greater consideration in future studies of primate behavior.     

Group size, grooming and fission in primates: a modeling approach based on group structure

In social animals, fission is a common mode of group proliferation and dispersion and may be affected by genetic or other social factors. Sociality implies preserving relationships between group members. An increase in group size and/or in competition for food within the group can result in decrease certain social interactions between members, and the group may split irreversibly as a consequence. One individual may try to maintain bonds with a maximum of group members in order to keep group cohesion, i.e. proximity and stable relationships. However, this strategy needs time and time is often limited. In addition, previous studies have shown that whatever the group size, an individual interacts only with certain grooming partners. There, we develop a computational model to assess how dynamics of group cohesion are related to group size and to the structure of grooming relationships. Groups’ sizes after simulated fission are compared to observed sizes of 40 groups of primates. Results showed that the relationship between grooming time and group size is dependent on how each individual attributes grooming time to its social partners, i.e. grooming a few number of preferred partners or grooming equally or not all partners. The number of partners seemed to be more important for the group cohesion than the grooming time itself. This structural constraint has important consequences on group sociality, as it gives the possibility of competition for grooming partners, attraction for high-ranking individuals as found in primates’ groups. It could, however, also have implications when considering the cognitive capacities of primates.     

Zfp462 deficiency causes anxiety‐like behaviors with excessive self‐grooming in mice

Zfp462 is a newly identified vertebrate‐specific zinc finger protein that contains nearly 2500 amino acids and 23 putative C2H2‐type zinc finger domains. So far, the functions of Zfp462 remain unclear. In our study, we showed that Zfp462 is expressed predominantly in the developing brain, especially in the cerebral cortex and hippocampus regions from embryonic day 7.5 to early postnatal stage. By using a piggyBac transposon‐generated Zfp462 knockout (KO) mouse model, we found that Zfp462 KO mice exhibited prenatal lethality with normal neural tube patterning, whereas heterozygous (Het) Zfp462 KO (Zfp462^+/?) mice showed developmental delay with low body weight and brain weight. Behavioral studies showed that Zfp462^+/? mice presented anxiety‐like behaviors with excessive self‐grooming and hair loss, which were similar to the pathological grooming behaviors in Hoxb8 KO mice. Further analysis of grooming microstructure showed the impairment of grooming patterning in Zfp462^+/? mice. In addition, the mRNA levels of Pbx1 (pre‐B‐cell leukemia homeobox 1, an interacting protein of Zfp462) and Hoxb8 decreased in the brains of Zfp462^+/? mice, which may be the cause of anxiety‐like behaviors. Finally, imipramine, a widely used and effective anti‐anxiety medicine, rescued anxiety‐like behaviors and excessive self‐grooming in Zfp462^+/? mice. In conclusion, Zfp462 deficiency causes anxiety‐like behaviors with excessive self‐grooming in mice. This provides a novel genetic mouse model for anxiety disorders and a useful tool to determine potential therapeutic targets for anxiety disorders and screen anti‐anxiety drugs.     

Ecological determinants of the behavior and social structure of Japanese monkeys: A synthesis

A review is presented of the results of the various studies in this volume and an attempt is made to establish connections among several features of the ecology, behavior, and social structure of Japanese monkeys. Several studies in this volume suggest that intergroup direct feeding competition has been much more severe in Yakushima, in the warm-temperate region, than in Kinkazan, in the cool-temperate region of Japan. This result is consistent with the predictions that moderate abundance and clumped distribution of food incur more severe intergroup direct competition. However, the number of adult females within a group in Yakushima was smaller than that in Kinkazan even though severe intergroup direct competition should favor large groups. This contradiction can be mainly explained by the less severe intergroup indirect competition in Kinkazan than in Yakushima. By contrast, some studies in this volume also indicate that adult male to female ratio within a group has been higher in Yakushima than in Kinkazan. This result can be explained in two ways: the females in Yakushima might have recruited more males to increase the competitive ability of the group under conditions of severe intergroup direct feeding competition; alternatively, it might be profitable that the males in Yakushima defend females cooperatively as group males against the males in other groups at a moderate density of females. Some studies in this volume suggest that grooming frequency was higher in Yakushima than in Kinkazan. The higher grooming frequency in Yakushima might have been partly due to a constant increase in engaging in social behavior from a decrease in feeding time. Another reason might be that there is a stronger effect of grooming on promotion of formation of coalitions among adults under conditions of severe intergroup direct and intragroup direct competition.     

Reciprocity and partner preference in grooming of female blue monkeys

Grooming among adult and older juvenile females in a wild group of blue monkeys (Cercopithecus mitis stuhlmanni) is analyzed and related to agonistic behavior. Both grooming and agonistic behavior were less frequent than would be expected in baboon and macaque groups. Fair shares of grooming were given and taken, both within and between interactions, in amost dyads, and all females were seen to groom with at least half the others. The reciprovity of grooming was its most outstanding feature. There was no evidence that grooming was preferentially directed at kin. Frequent grooming partnerships fell into two clusters, one of which ranked higher than the other. We suggest that grooming throughout the group helps to establish a coherent team of females which effectively, defends its territory in daily encounters at the boundaries with neighboring groups.