Regulatory mechanisms underlying novelty-induced grooming in the laboratory rat

Bouts of pelage cleaning can be readily evoked in laboratory rodents under conditions of exposure to novelty. Such novelty-induced grooming is described as stereotyped and rostro-caudal in its progression. The patterned structure of novelty-induced grooming makes it particularly attractive for research on the organizational and motivational underpinnings of co-ordinated behaviour. Micro-characteristics of stereotyped novelty-induced grooming bouts were studied in 27 female Wistar rats that were exposed to a novel arena with shelters for a period of 15 min. The order of grooming acts within the initial bouts was rostro-caudal, but subsequent bouts became progressively disorganized in their sequencing. The observed pattern of progressive bout disorganization may be attributed to the gradual dearousal from stress. Differences between consecutive bouts in their micro-characteristics suggest that at least some grooming actions emitted within the context of those bouts operate as relatively independent units of behaviour. Those unitary component actions appear to be integrated into protracted pelage cleaning sequences by a separate mechanism. Similar endogenous mechanisms have been proposed for other co-ordinated motor actions, which suggests that the organizational principles identified in the context of novelty-induced grooming may represent general principles that govern co-ordinated behaviour.     

Time-matched grooming in female primates? New analyses from two species

The parcelling model of reciprocity predicts that grooming partners will alternate between giving and receiving grooming within grooming bouts, and that each partner will perform approximately as much grooming as it receives within each bout (‘time matching’). Models of allogrooming based on biological markets theory predict that individuals of lower dominance rank will exchange grooming for tolerance from high-rankers, and therefore an inverse relation will be found between grooming partners' dominance rank distance and how closely they match each other's grooming contributions within each bout. We used weighted logistic regression and weighted least-squares regression to test these predictions using data from female white-faced capuchins, Cebus capucinus, and bonnet macaques, Macaca radiata. Only 5-7% of macaque grooming bouts, and 12-27% of capuchin grooming bouts, were reciprocated. However, (1) the duration of grooming by the first groomer significantly predicted whether the groomee would reciprocate at all, and (2) when bouts were reciprocated, the duration of grooming by the first groomer significantly predicted the duration of grooming by the second groomer. Grooming was most balanced among females of similar dominance ranks. Both the time-matching and rank-related effects were weak, although significant. These results indicate that although some form of time matching may be a general characteristic of grooming in female-bonded primate species, time matching accounts for relatively little of the variation in the distribution of grooming within bouts. We also draw attention to weighted regression as a technique that avoids pseudoreplication while using all available data.     

Female baboons do not raise the stakes but they give as good as they get

We used data from four chacma baboon, Papio cynocephalus ursinus, troops, living in two populations, to test the raise the stakes (RTS) strategy of reciprocity. Female baboons did not raise the stakes either within or across grooming bouts. Instead they time-matched grooming contributions and divided grooming into short episodes. In addition, analysis of the grooming behaviour of frequently versus infrequently grooming dyads did not reveal differences in grooming patterns predicted by the RTS strategy. We suggest time constraints preclude the escalation of grooming bout length as required by RTS; the data were more consistent with a strategy of give as good as you get. However, this strategy could not explain all the patterns observed, and we conclude that biological market theory represents a more appropriate framework for investigating female grooming dynamics than dyadic games based on the iterated prisoner's dilemma. We suggest that competitive altruism among individuals acts as a market force influencing an individual's value as a grooming partner. Copyright 2000 The Association for the Study of Animal Behaviour.     

Grooming and Anxiety in Barbary Macaques

Grooming is a fundamental component of sociality in many gregarious animal species, and elucidating the costs and benefits of this behaviour is crucial for understanding its function. There is evidence that animals giving grooming pay a cost in terms of the time and energy they invest, while recipients benefit not just from the removal of dirt and parasites, but also from the relaxing effects of being groomed. Recently, however, studies of primates have indicated that giving grooming may also provide such hedonic benefits, reducing levels of stress or anxiety in the groomer. In this study of free‐ranging adult female Barbary macaques at Trentham Monkey Forest (Stoke‐on‐Trent, UK), we tested the hypothesis that grooming reduces anxiety in the donor and/or the recipient. During focal follows, we quantified females' rates of self‐scratching as a behavioural index of their anxiety levels. Self‐scratching rates in the 2‐min periods after bouts of grooming (given, received and reciprocated) were compared to overall mean self‐scratching rates; we predicted that if grooming reduces anxiety, self‐scratching rates would be significantly lower after grooming bouts than mean levels. We first analysed all grooming bouts and then analysed separately grooming bouts with adult males, with all adult females, with subordinate adult females and with dominant adult females. Contrary to our prediction, self‐scratching rates were never seen to be lower after grooming than mean levels. In fact, for the majority of grooming partner–direction combinations, we found significantly higher rates of self‐scratching after grooming compared to mean levels. The hypothesis that grooming reduces anxiety was therefore not supported. Grooming seems in some cases to increase, not alleviate, anxiety. We explore possible explanations for these unexpected results.     

Description of the behavior of praying mantis with particular reference to grooming

Eighteen behavior patterns, encompassing most of the observable behavior of individually housed praying mantids, Sphodromantis lineola, were recorded using a point sampling technique. The data were sorted into four major behavioral categories: (1) food acquisition, (2) grooming, (3) inactivity, and (4) locomotion and miscellaneous. The mantids spent most of the time in an inactive state, which is consistent with their way of life as ambushing predators. Most of the animals' active time was spent in food acquisition (60%). Grooming behaviors comprised 16.7% of the active time; foreleg grooming represented 82% of grooming, while head grooming represented 14.3%. Analysis of the behavioral states in close temporal proximity to head grooming indicated that head grooming often follows foreleg grooming, occuring in bouts of about 1/2 to 1 min duration. Foreleg grooming is also closely associated with eating and seems to represent a pivotal behavior pattern between food acquisition and grooming, possibly sharing causal factors with both.     

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.     

The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>)

We collected data on grooming, proximity, and aggression in long-tailed macaques (Macaca fascicularis) in Kalimantan, Indonesia. We used this data to study how grooming influenced a receiver's (B) behavior towards the bout's initiator (A). In our first analysis, post-grooming samples were collected after A groomed B. These were compared to matched-control samples of similar conditions but A had not previously groomed B. This comparison was performed on 26 individuals (16 female, 3 male, 7 immature) and tested whether A's initial act of grooming increased the pair's time in proximity and the amount of time B groomed A. We also tested if A's grooming decreased B's aggression towards A per time in proximity. Rates of B-->A aggression per time in proximity with A for 39 individuals (18 female, 5 male, 16 immature) were compared between post-grooming and focal sample data. Finally, we studied 248 grooming bouts to test if the first two grooming episodes were time matched. We assessed the influence of age, sex, rank and inferred kinship on time matching, and controlled for individual variation and tendency to groom using a general linear mixed model. Our results showed that A-->B grooming acted to increase B-->A grooming and the pair's proximity, while lowering B-->A aggression. Despite these effects, episodes in grooming bouts were generally not matched, except weakly among similar partners (i.e., female pairs and immature pairs). Grooming imbalance was greatest across age-sex class (i.e., male-female and adult-immature pairs). In similar pairs, grooming duration was skewed in favor of high-ranking individuals. We conclude grooming established tolerance and increased the likelihood that grooming reciprocation would occur, but grooming durations were not typically matched within bouts. Lack of time matching may be the result of grooming that is performed to coordinate interchanges of other social services.     

Organization rules and timing in kestrel grooming

Grooming bouts were observed for 200 h in two captive American kestrels (Falco sparverius sparverius). Two types of bouts were found, long and short; the bout length distribution for long bouts approximated a geometric distribution, which can be interpreted as a discrete variant of the survival function. Transition rules in long bouts were based on anatomical proximity. Grooming movements clustered together on the basis of anatomical regions and function. Timing processes could either be accounted for by a three-level hierarchy involving two different types of distributions, or a four-level hierarchy of identical distributions. In the former model, grooming acts per cluster, clusters per preening session and preening sessions per bout all yielded frequency distributions of the geometric type, suggesting that grooming could be controlled by a hierarchy of random processes.     

Female grooming markets in a population of gray-cheeked mangabeys (Lophocebus albigena)

Primate female allogrooming models based on biological marketstheory predict that grooming is "time matched" within bouts,that is, the amount of time the first female grooms predictsthe amount of time the second one grooms. The models also predictthat when female–female contest competition is weak, groomingis traded for grooming, but when female–female contestcompetition is strong, grooming may be traded for other commoditiessuch as feeding tolerance, and grooming discrepancy betweenmembers of dyads is rank related. We tested these predictionsusing data collected from adult and subadult female gray-cheekedmangabeys (Lophocebus albigena) (N = 26) in 5 groups in KibaleNational Park, Uganda. We found that, overall, females reciprocatedin 33% of grooming bouts. Among reciprocated bouts, femalesin all 5 groups showed time matching. In 2 groups, we also foundrank-related grooming discrepancies but showing opposite patternsto each other. Consistent with predictions based on biologicalmarkets theory, these groups may have been under greater feedingcompetition, revealed more by adjustments in ranging behaviorthan increased agonistic rates. Although these results supportcurrent allogrooming models, they also suggest that the modelsmay become more robust if the influence of scramble competitionis incorporated. In addition, they emphasize the flexibilityand dynamic nature of female competitive relationships withinthe same population of primates.     

Decision making in grooming by Japanese macaques (Macaca fuscata)

I analyzed the temporal organization of individual Japanese macaques’ (Macaca fuscata) grooming sequences in 14 mothers and 13 offspring of different age/sex classes and 4 nonkin females. I hypothesized that preceding grooming affects subsequent grooming by the same individual. Grooming bouts were likely to be terminated as the bouts became longer when females groomed nonrelatives. Moreover, the duration of first bouts was longer than that of following bouts. These effects were also seen in grooming of mothers by their offspring > 1 year old and that of adult and adolescent female offspring by their mothers. In contrast, neither the duration of first bouts nor the number of preceding bouts had much effect on the occurrence or duration of subsequent bouts in any subject.     

Grooming, social bonding, and agonistic aiding in rhesus monkeys

An analysis of simultaneous grooming bouts in a captive group of rhesus monkeys (Macaca mulatta) failed to provide evidence of competition to groom high ranking partners. Not only were grooming supplantations rare, but the highest ranking individuals performing grooming did not groom the highest ranking animals receiving grooming. Lower ranking partners, however, did more grooming in nonkin dyads. Grooming partners aided one another in agonistic episodes, but the individual receiving the aid did not groom the individual providing the aid more than vice versa. Kin dyads did aid and groom one another at greater than expected rates, but the aider did not receive the greater proportion of grooming in the dyad. Males participated in more grooming than expected, but their grooming was not related to aiding either with regard to one another or female partners. Animals that were targeted in joint aggression, or aided against, received significantly less grooming from their opponents. A general social relationship expressed in partner preferences, social grooming, and agonistic aiding better explained the observed pattern than any model based on the exchange of services for favors in different currencies.     

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.     

Grooming in brown howler monkeys,Alouatta fusca

The grooming behavior of a group of brown howler monkeys was studied for one year in an Atlantic forest reserve of southeastern Brazil. A total of 290 grooming bouts were recorded and analyzed. The two adult females directed most of the grooming (91%), while the adult male was the major recipient (37%). Grooming between females, and between them and their siblings, also occurred quite often. On average, the group spent 2% of its daily time grooming, with a higher frequency around noon. There were significant differences, however, in time spent grooming between seasons; grooming was more abundant during the coldest seasons (autumn–winter) and rarer in hotter ones (spring–summer). A significant negative correlation was found between grooming time and temperature, but contrary to expectations, grooming time failed to correlate with both the group' diet and the demands of food-gathering, as measured by travelling time and day range length. A comparison of grooming behavior with other species of the genus suggests that brown, red (A. seniculus), and black howler monkeys (A. caraya) are more similar to each other than to mantled howlers (A. palliata), a result that probably is linked with the differing social structure and group size of the latter species. © 1995 Wiley-Liss, Inc.     

Grooming Patterns in the Primitively Eusocial Wasp Polistes dominulus

Grooming is a commonly observed behavior in many animals. One function of grooming is to clean the body of debris and parasites. An additional function may be to homogenize chemical cues present on the body. This latter purpose is especially likely in species in which contact‐based chemical communication occurs, such as in eusocial insects. In this study we address the context, sequence, frequency and duration of 683 acts of self‐grooming performed by the paper wasp, Polistes dominulus. In general, individuals groomed heads after cell inspections, and abdomens after sitting, suggesting that grooming serves to remove debris from the body. Although no differences were observed in the total amount of time spent grooming, foundresses groomed significantly more often than did workers. Wasps were equally likely to groom thoraces or abdomens following heads, but were more likely to groom abdomens after thoraces and heads after abdomens. Interestingly, the appendages used to groom individual body parts were highly specific (e.g. the prothoracic legs were used for the head), thus indicating that grooming is not used to homogenize chemical cues across the body surface of the wasp.     

Group harmony in gibbons: Comparison between white-handed gibbon (Hylobates lar) and siamang (H. syndactylus)

The siamang (Hylobates syndactylus) is exceptional among gibbons in that its area of distribution almost completely overlaps those of other gibbons, namely the white-handed gibbon (H. lar) and the agile gibbon (H. agilis) of the lar group. The siamang has almost twice the body weight of the gibbons of the lar group (ca. 11 kg vs. 5–6 kg), and it has been suggested that distinct ecological and behavioural differences exist between the siamang and its two sympatric species. The siamang has been claimed to differ from the white-handed gibbon “in the closer integration and greater harmony of group life” (Chivers, 1976, p. 132). However, few quantitative data exist to support this hypothesis. In the present study, intra-group interactions in captive family groups of white-handed gibbons and siamangs (two groups of each species) were recorded by focal-animal sampling. These data failed to show a consistent association between species and most of the behavioural patterns recorded, such as frequency of aggression, percentage of successful food transfer, frequency of social grooming bouts, and duration of social grooming/animal/hr. A significant difference was found for only two of the variables: Individual siamangs in this study showed longer grooming bout durations, and made fewer food transfer attempts than lar individuals. Only the first of these two differences is consistent with the hypothesis mentioned above, whereas the lower frequency of food transfer attempts in siamangs is the opposite of what should be expected under the hypothesis. On the other hand, two of these behavioural patterns showed a significant correlation with the parameters group size and individual age: Both individuals in larger groups and younger individuals tended to show shorter grooming bouts and a smaller proportion of successful food transfers. Our findings indicate that social cohesion within these gibbon groups may be much more flexible according to and depending on social or ecological influences and less rigidly linked to specific gibbon taxa than previously assumed. A considerably larger number of gibbon groups would have to be compared to provide reliable evidence for or against species-specific differences in group cohesion. Another finding of this study—a positive correlation between the frequency of aggression and grooming—is discussed in the light of the functional interpretations commonly attributed to allogrooming behaviour in primates.     

Age-related differences in social grooming among adult female Japanese monkeys ( Macaca fuscata)

The present study investigated the influence of dominance rank in combination with kinship on age-related differences in social grooming among adult females in a free-ranging group of Japanese monkeys (Macaca fuscata). Eighty-three adult females were divided into six sub-groups according to age-class (younger: 5–9 years old; middle: 10–14 years old; older: 15–22 years old) and dominance rank (high and low rank). The ratio of the number of unrelated females that each female groomed to the total number of available unrelated females and grooming bouts which she gave to unrelated females decreased with increasing age for both high- and low-ranking females, whereas age did not appear to affect corresponding values for related females. On the other hand, compared with low-ranking females, high-ranking females of all age-classes received grooming more often from a larger number of unrelated females. Moreover, older females of low rank received grooming less often from a smaller number of unrelated females than younger females of low rank. These results indicate that with increasing age females are more likely to concentrate on related females when they have grooming interactions with other females. This tendency seems to be more apparent for low-ranking females. Moreover, the present findings also indicate that older high-ranking females could maintain their social attractiveness as high as younger high-ranking females.     

Negotiations over Grooming in Wild Vervet Monkeys (Chlorocebus pygerythrus)

Mutual grooming plays a central role in the establishment and maintenance of social relationships in primates. Allogrooming has two main functions: hygiene and bonding with partners. The duration of grooming bouts is commonly used in studies of the functional aspects of grooming, but few reflect on the proximate mechanisms that determine grooming bout lengths. As it is highly unlikely that groomer and groomee prefer exactly the same bout length, we are likely to observe the result of some form of negotiation. We currently lack information about the signals that primates employ to inform others about their intentions and desires concerning grooming interactions. From October 2006 until April 2007 we studied three behaviors shown in grooming interactions that could potentially have a signaling function in the negotiation process over the initiation and length of grooming bouts among adult females of two vervet groups freely ranging in the Loskop Dam Nature Reserve, South Africa: approaching another individual as far as that resulted in a grooming session, changing of the body position by the groomed individual, and lip smacking. We found that “approach” did not reliably predict which individual would receive grooming first, although approaching individuals groomed significantly more than those approached. Thus, in the context of grooming interactions, moving toward a group member may signal the willingness to invest. Body part presentations appeared to be the main signal used to demand a prolongation of the grooming by the partner. Finally, lip smacking was used under potentially stressful circumstances, notably shortly before using the mouth to groom the partner or an attempt to touch a mother’s infant. Our exploratory study hopefully inspires colleagues to start looking at the role of communication during cooperative interactions for a better appreciation of how animals manage cooperation and negotiate exchange rates.     

The organization of grooming in budgerigars

Structural rules for grooming are examined in the budgerigar (Melopsittacus undulatus). Two types of bouts are found: short bouts with no predictable temporal pattern and long bouts with some degree of periodic occurrence. Transitions in long bouts are mostly based on anatomical proximity. Grooming movements cluster together according to function and body region. Evidence for hierarchical organization obtained by clustering is confirmed by the proportion of occurrence of movements in long and short bouts. Individual birds are similar enough on measures of occurrence, transition and hierarchica structure for pooling of subjects to be justified; this suggests that the organizational rules found here are to a large extent species-typical.     

Social relationships among adult female baboons

Adult female baboons were studied over a 15-month period which included sexual cycling, pregnancy, and lactation. Females could be ranked in a linear dominance hierarchy which accurately predicted the direction, but not the frequency, of agonistic interactions. Females were most attractive to others during lactation, receiving less aggression, more friendly gestures, more grooming, and grooming by more different individuals than females in other reproductive states. In all three reproductive states high-ranking females were more attractive than others. When differences in behaviour related to changes in reproductive state were factored out, individual females groomed animals next to themselves in the dominance hierarchy more than others. A model is presented showing how rank-relaed access and attractiveness may interact to perpetuate this distribution of grooming over time.     

The D1 family dopamine receptor,DopR, potentiates hind leg grooming behavior in Drosophila

Drosophila groom away debris and pathogens from the body using their legs in a stereotyped sequence of innate motor behaviors. Here, we investigated one aspect of the grooming repertoire by characterizing the D1 family dopamine receptor, DopR. Removal of DopR results in decreased hind leg grooming, as substantiated by quantitation of dye remaining on mutant and RNAi animals vs. controls and direct scoring of behavioral events. These data are also supported by pharmacological results that D1 receptor agonists fail to potentiate grooming behaviors in headless DopR flies. DopR protein is broadly expressed in the neuropil of the thoracic ganglion and overlaps with TH‐positive dopaminergic neurons. Broad neuronal expression of dopamine receptor in mutant animals restored normal grooming behaviors. These data provide evidence for the role of DopR in potentiating hind leg grooming behaviors in the thoracic ganglion of adult Drosophila. This is a remarkable juxtaposition to the considerable role of D1 family dopamine receptors in rodent grooming, and future investigations of evolutionary relationships of circuitry may be warranted.