Social Grooming in Bats: Are Vampire Bats Exceptional?

Evidence for long-term cooperative relationships comes from several social birds and mammals. Vampire bats demonstrate cooperative social bonds, and like primates, they maintain these bonds through social grooming. It is unclear, however, to what extent vampires are special among bats in this regard. We compared social grooming rates of common vampire bats Desmodus rotundus and four other group-living bats, Artibeus jamaicensis, Carollia perspicillata, Eidolon helvum and Rousettus aegyptiacus, under the same captive conditions of fixed association and no ectoparasites. We conducted 13 focal sampling sessions for each combination of sex and species, for a total of 1560 presence/absence observations per species. We observed evidence for social grooming in all species, but social grooming rates were on average 14 times higher in vampire bats than in other species. Self-grooming rates did not differ. Vampire bats spent 3.7% of their awake time social grooming (95% CI = 1.5–6.3%), whereas bats of the other species spent 0.1–0.5% of their awake time social grooming. Together with past data, this result supports the hypothesis that the elevated social grooming rate in the vampire bat is an adaptive trait, linked to their social bonding and unique regurgitated food sharing behavior.     

Benefits, Costs and Constraints of Anti-Parasitic Grooming in Adult and Juvenile Rodents

Grooming behaviour plays various roles in the health care, reproduction, and social life of an individual vertebrate. However, the reasons for the variability in time spent grooming amongst species, populations and individuals are not fully understood. We tested the hypothesis that the main role of grooming is ectoparasite removal and thus that time spent grooming by an animal reflects the costs of parasite infestation offset against the costs of grooming. The test was conducted on a rodent, Meriones crassus, that is parasitised by a flea, Xenopsylla conformis. We monitored behaviour of juvenile and adult rodents before and after flea infestation and quantified the probability of mortality of fleas with respect to the time spent grooming in adults compared with juvenile rodents. We predicted that: (1) increased costs of flea infestation (e.g. in parasitised as opposed to flea‐free rodents and in juveniles as opposed to adults) increases time spent grooming and (2) mortality probability per flea increases with increasing time spent grooming and is higher for fleas on juveniles than for fleas on adult rodents. We were interested to discover at the expense of which activity grooming is increased. Our findings established that the major role of grooming is in flea removal, as exposure to fleas evoked grooming activity in all rodents and grooming activity explained 57–70% of the variation in flea mortality. Furthermore, we showed that the rise in grooming activity was at the expense of resting. However, we found only partial support for the predicted increase in grooming time with increasing costs of flea infestation. Flea infestation did indeed increase the time spent grooming by rodents. Nevertheless, juvenile rodents who incur higher costs of flea infestation spent less time grooming than adults and sustained similar flea densities, suggesting that these hosts are constrained by some other factors, such as feeding time.     

Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support

Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.     

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.     

The Chimpanzee''s service economy: Food for grooming

Evidence is presented that the reciprocal exchange of social services among chimpanzees (Pan troglodytes) rests on cognitive abilities that allow current behavior to be contingent upon a history of interaction. Food sharing within a captive colony of chimpanzees was studied by means of 200 food trials, conducted on separate daus over a 3-year period, in which 6,972 approaches occurred among the nine adults in the colony. The success rate of each adult, A, to obtain food from another adult, B, was compared with grooming interactions between A and B in the 2 hours prior to each food trial. The tendency of B to share with A was higher if A had groomed B than if A had not done so. The exchange was partner-specific, i.e., the effect of previous grooming on the behavior of food possessors was limited to the grooming partner. Grooming did not affect subsequent sharing by the groomer, only by the groomee. The effect of grooming was greatest for pairs of adults who rarely groomed. Nevertheless, the effect was general: 31 dyadic directions showed an increase in sharing following grooming, and only 11 a decrease. Food possessors actively resisted approaches by individuals who had not groomed them. After food trials there was a significant reduction of grooming by previous possessors towards those individuals with whom they had shared.     

Seasonal Variation in the Activity Patterns and Time Budgets of <Emphasis Type="Italic">Trachypithecus francoisi</Emphasis> in the Nonggang Nature Reserve,China

Activity patterns and time budgets are 2 important aspects of animal behavior that researchers use to investigate ecological influences on individual behavior. We collected data on activity patterns and time budgets in 1 group of François’ langurs (Trachypithecus francoisi) from August 2003 to July 2004 in the Nonggang Nature Reserve, Guangxi Province, China, via instantaneous scan sampling method with 15-min intervals. The diurnal activity pattern of François’ langurs showed morning and afternoon feeding peaks, with a midday resting peak. Seasonal change was apparent in the activity pattern: 2 significant feeding peaks occurred in the dry season and only 1 significant feeding peak in the rainy season. The group spent an average of 51.5% of the daytime resting. Feeding and moving accounted on average for 23.1% and 17.3% of the activity budget, respectively. Subjects spent little time on social activities, averaging 2% for grooming and 5.5% for playing. Their time budgets showed significant seasonal variation: they spent a greater proportion of time on feeding and less time on resting and grooming in the dry season than in the rainy season. They also differed among different sex-age classes: immatures spent more time playing, whereas adults devoted more time to resting, feeding, and grooming. Correlations between time budgets and food items or food availability clearly indicated that François’ langurs might adopt an energy-maximizing strategy when preferred foods were scarce in the dry season.     

Affiliation promotes the transmission of a social custom: handclasp grooming among captive chimpanzees

Handclasp grooming is a unique social custom, known to occur regularly among some, but not all populations of chimpanzees (Pan troglodytes). As with other cultural behaviors, it is assumed that this distinctive grooming posture is learned socially by one individual from another. However, statistical comparisons among factors thought to influence how a behavior spreads within a group have never, to our knowledge, been conducted. In the present study, the origination and spread of handclasp grooming in a group of captive chimpanzees was followed throughout more than 1,500 h of observation over a period of 12 years. We report on the frequency, bout duration, and number and demography of performers throughout the study period, and compare these findings to those reported for wild populations. We predicted that dyads with strong affiliative ties, measured by time spent in proximity to and grooming one another, were likely to develop a handclasp grooming partnership during the study period. A quadratic assignment procedure was used to compare correlations among observed frequencies of grooming and proximity with handclasp grooming in all possible dyads within the group. As predicted, the formation of new handclasp grooming dyads was positively correlated with the rate of overall grooming and proximity within a dyad. In addition, in nearly all dyads formed, at least one individual had been previously observed to handclasp groom. We concluded that affiliation and individual experience determines the transmission of handclasp grooming among captive chimpanzees.     

Reciprocal altruism in bats and other mammals

In this paper five conditions are specified which must be met before reciprocal altruism, rather than kin selection, should be invoked. Four purported mammalian examples— social grooming in coati, cluster position in roosting pallid bats, information exchange among greater spear-nosed bats, and blood regurgitation among vampire bats—are examined to determine if reciprocal altruism is necessary to plausibly explain each situation. Results from a computer simulation which apportions the relative selective advantage of vampire bat food sharing to kin selection and reciprocal altruism are then presented. The results demonstrate that the increase in individual survivorship due to reciprocal food sharing events in this species provides a greater increase in inclusive fitness than can be attributed to aiding relatives. This analysis suggests that reciprocal altruism can be selectively more important than kin selection when altruistic behaviors in a relatively large social group occur frequently and provide a major fitness benefit to the recipient even when that recipient is related to the donor.     

Enclosure environment affects the activity budgets of captive Japanese macaques (Macaca fuscata)

Individuals adapt to changes in their environment, such as food availability and temperature, by adjusting the amount of time spent in different behavioral activities. These adjustments in behavior should vary across age-sex class according to specific physiological and social needs. We studied the activity budgets of three social Japanese macaque groups inhabiting either vegetated or nonvegetated enclosures in order to compare the effects of access with vegetation, as both food and substrate on resting, feeding, grooming and moving activities over a 12-month period. Daily access to natural foods for monkeys in the vegetated enclosure seems to be largely responsible for the differences in daily time budgets of these three groups. Resting time in all three groups was longer than the time devoted to other activities. Resting and moving time in the two nonvegetated enclosures was significantly longer than in the vegetated enclosure. In contrast, feeding and grooming time was significantly longer in the vegetated enclosure. Seasonal variation in time spent feeding, resting and grooming was significantly effected by enclosure type. In all three enclosures, immatures, particularly females, spent more time feeding and moving, whereas adults spent more time resting. Significant monthly variation in time spent by age-sex class was noted only for feeding and resting. Interestingly, in the vegetated enclosure, time spent feeding on natural vegetation was equal to the amount of time spent feeding on provisioned food. This suggests that factors other than energetic and nutritional needs may be important determinants of the activity budget of the species. These results have important implications for the enrichment of captive primates and our understanding of the maintenance of activity patterns by primates in the wild.     

Grooming reciprocity in female tibetan macaques macaca thibetana

Grooming among nonhuman primates is widespread and may represent an important service commodity that is exchanged within a biological marketplace. In this study, using focal animal sampling methods, we recorded grooming relationships among 12 adult females in a free-ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China, to determine the influence of rank and kinship on grooming relationships, and whether females act as reciprocal traders (exchange grooming received for grooming given) or interchange traders (interchange grooming for social tolerance or other commodities). The results showed that: (1) grooming given was positively correlated with grooming received; (2) kinship did not exert a significant influence on grooming reciprocity; and (3) grooming reciprocity occurred principally between individuals of adjacent rank; however, when females of different rank groomed, females tended to groom up the hierarchy (lower ranking individuals groomed higher ranking individuals more than vice versa). Our results support the contention that both grooming reciprocity and the interchange of grooming for tolerance represent important social tactics used by female Tibetan macaques.     

Effect of female group size on harem male roosting behavior of the Indian short-nosed fruit bat <Emphasis Type="Italic">Cynopterus sphinx</Emphasis>

Mate guarding has been known to incur costs and cause constraints for harem males in many polygynous species. However, the effect of female group size on the harem male’s time budget in bats has received very limited attention. The Indian short-nosed fruit bat, Cynopterus sphinx, exhibits resource defense polygyny, in which tent roosting males construct tents and defend multiple female bats. We studied the effect of female group size on three aspects of harem male behavior: social grooming by reciprocal licking, tent maintenance, and tent guarding in the mast tree Polyalthia longifolia. In the process of reciprocal licking, all the bats in the harem were drenched in saliva before emergence, and this activity was positively and significantly correlated with female group size. Once females departed for foraging, harem males remained in their respective tents at night-time between intermittent foraging bouts and engaged in tent maintenance and tent guarding. Time invested by harem male bats in tent maintenance and tent guarding were positively and significantly correlated with female group size. Harem males extended their presence in tent by utilizing tents as feeding roosts. Female group size also influenced the emergence time of harem male bats, where males with largest group emerged later than did the smallest group. Likewise, harem male with the smallest group had more time available for foraging than the male with the largest group. Findings of this study suggest that having a larger harem may indeed be costly for the males by reducing their foraging time.     

Dominance hierarchy and social grooming in female lion- tailed macaques (Macaca silenus) in the Western Ghats, India

This article reports the structure of dominance and its relationship with social grooming in wild lion-tailed macaque females. The strength of dominance hierarchy was 0.79 on a scale of 0 to 1 indicating a moderate linearity in the ranking system. Dominance scores were converted into an ordinal as well as an interval scale. Grooming scores were also converted into interval scales using standard scores. Grooming received and grooming given correlated positively and negatively respectively with dominance ranks indicating that high ranking females received more and gave less grooming. Grooming was also positively related to encounter rates for dyads of females. More grooming among adjacent ranks, and grooming being more reciprocal, occurred only in the case of dominant females. The grooming patterns, therefore, appeared to be more of despotic than egalitarian nature. While ranking macaques into different Grades of social systems ranging from despotic to egalitarian, Thierry (2004) has placed lion-tailed macaques in Grade 3 corresponding to the ‘relaxed’ social system. Our results indicate that the grooming and dominance relationships in this species are more despotic, and hence, the Grade for this species requires to be shifted toward 2 or 1.     

Social foraging in vampire bats is predicted by long-term cooperative relationships

Stable social bonds in group-living animals can provide greater access to food. A striking example is that female vampire bats often regurgitate blood to socially bonded kin and nonkin that failed in their nightly hunt. Food-sharing relationships form via preferred associations and social grooming within roosts. However, it remains unclear whether these cooperative relationships extend beyond the roost. To evaluate if long-term cooperative relationships in vampire bats play a role in foraging, we tested if foraging encounters measured by proximity sensors could be explained by wild roosting proximity, kinship, or rates of co-feeding, social grooming, and food sharing during 21 months in captivity. We assessed evidence for 6 hypothetical scenarios of social foraging, ranging from individual to collective hunting. We found that closely bonded female vampire bats departed their roost separately, but often reunited far outside the roost. Repeating foraging encounters were predicted by within-roost association and histories of cooperation in captivity, even when accounting for kinship. Foraging bats demonstrated both affiliative and competitive interactions with different social calls linked to each interaction type. We suggest that social foraging could have implications for social evolution if “local” within-roost cooperation and “global” outside-roost competition enhances fitness interdependence between frequent roostmates.

A combination of captive experiments and proximity sensing in the wild show that social bonds in vampire bats that are typically defined by cooperative interactions within the roost also extend beyond the roost and may provide benefits during foraging.     

Roost switching, roost sharing and social cohesion: forest-dwelling big brown bats, Eptesicus fuscus, conform to the fission-fusion model

We used radiotelemetry to quantify roost switching and assess associations between members of maternity colonies of forest-dwelling big brown bats. Bats remained loyal to small roosting areas of forest within and between years and switched trees often (). For radiotagged bats from the colony in one of these areas, roost-switching frequency was positively correlated with the number of different individuals with which tagged bats shared roosts. We quantified associations between pairs of bats using a pairwise sharing index and found that bats associated more often than predicted when roost and roostmate selection were random but that all tagged bats spent at least some days roosting in different trees, apart from preferred roostmates. Our results suggest that forest-dwelling big brown bats conform to a fission-fusion roosting pattern. Roost switching in forests may reflect the maintenance of long-term social relationships between individuals from a colony that is spread among a number of different trees on a given night. In this fission-fusion scenario, switching between trees, within a local area, could serve to increase the numbers of individuals with which bats maintain associations. We contend that roosting areas in forests are analogous to spatially large roosts in caves, mines and buildings.     

Interplay between various aspects in social relationships of young rhesus monkeys: Dominance,agonistic help,and affiliation

Relationships between group-living primates depend strongly on their position in the group dominance hierarchy and on their relationships with other group members. The influence of various behaviours on social relationships of immature rhesus monkeys (Macaca mulatta) was investigated here. Dominance ranks were established and related to the degree of affiliation in a dyad. Older monkeys were mostly dominant to the younger ones, regardless of kinship. Subordinate monkeys left proximity of their dominant members more often than they were left by them both among siblings and non-siblings, but the effect of dominance rank on the amount of play initiation and grooming in a dyad differed between these two types of dyads. The amount of agonistic help two individuals provided for each other was low among immatures. Nevertheless, pairs of siblings gave help to each other in agonistic conflicts more often than non-siblings, and such help was more often reciprocated between siblings than between non-siblings. Help in agonistic conflicts was positively correlated with the amount of time monkeys spent playing, grooming, or in proximity. Adults tended to interfere less in conflicts of frequent sibling play partners or non-sibling grooming partners. No evidence was found for young monkeys to exchange reciprocally grooming for agonistic help. It is argued that the time monkeys spend interacting with each other in affiliative interactions increases their familiarity and thus promotes close relationships between them. On the whole, young monkeys' relationships, like those between adults, are influenced strongly by their kinship, and position in the dominance hierarchy.     

On the evolution of delayed recruitment to food bonanzas

Whereas food sharing by immediate recruitment to food bonanzasis relatively common, especially among birds, delayed recruitmentfrom overnight roosts is comparatively rare, although it hasbeen studied extensively in the common raven (Corvus corax).Two hypotheses have been advanced to explain the evolution ofdelayed recruitment. Under the status-enhancement hypothesis,delayed recruiting is favored because the recruiter's social statusincreases with the number of followers it leads to a food source.The posse hypothesis also focuses on the number of individualsrecruited to a site, but in this case aggregation is favoredbecause larger groups are more likely to usurp a carcass defendedby a pair of territorial adult ravens. We used a game-theoreticmodel to explore the logic of immediate versus delayed recruitmentin the light of these hypotheses. In particular, we identified threecritical values of the probability of immediate recruitment:that below which delayed recruitment is a cooperative strategy,that below which delayed recruitment is an evolutionarily stablestrategy, and that below which a mutant strategy of delayedrecruitment will invade a population of immediate recruitersto reach fixation. The model demonstrates that either status enhancementor the posse effect may alone suffice for the evolution of delayed recruitmentto food bonanzas via mutualistic information sharing at communal roosts.     

Kin selection,social grooming and the removal of ectoparasites: A theoretical investigation

This paper considers how individuals should apportion their altruism among their relatives, with particular reference to social grooming in primates. It is concluded that there are no good reasons to expect an altruist to deploy its altruism among other individuals in proportion to its coefficients of relatedness to them. Various factors may cause an individual to be altruistic not just to its closest relative. One factor which is probably of widespread importance is when altruism reaches a point of diminishing returns, so that an increase in aid given is not accompanied by a proportional increase in benefit received. Quantitative predictions are made for social grooming with special reference to its possible function of ectoparasite removal.     

The influence of behavioral context and social characteristics on the physical aspects of social grooming in rhesus monkeys

The extent to which dominance status and sex can influence the physical act of grooming was examined in two groups of rhesus monkeys. Both the sex and the dominance status of the groomee, but not of the groomer, were found to affect the body sites groomed and the positions assumed by the animals during the grooming bout. Females were groomed more on the back and head and less on the tail, rump, upper leg, and lower arm than males. Females with infants tended to face away from the groomer. Higher-ranking groomees were groomed more on the tail and rump and less on the upper leg and back than lower-ranking groomees. Higher-ranking groomees spent more time lying down during grooming than lower-ranking groomees, while lower-ranking groomees faced away from the groomer more then higher-ranking groomees. The behavioral interactions just prior to and immediately after grooming were also recorded. Although the onset of grooming was preceded by social interactions between the partners, the end of grooming was followed by a complete break in interactions. Particular types of social signals displayed by the groomee just prior to grooming were highly correlated with the grooming of specific body sites. These results suggest that the groomee controls the behavior of the groomer by the social signals it displays and the positions it maintains during the grooming bout. Thus, the grooming act itself may play an important role in the social relationships between group members.     

Variability of foraging and roosting activities in adult females of Daubenton’s bat (<Emphasis Type="Italic">Myotis daubentonii</Emphasis>) in different seasons

We radio-tracked fifteen reproductive females (5 pregnant, 5 lactating, 5 in post-lactation) of the Daubenton’s bat in summer 2005 in order to reveal the effect of reproductive state on their foraging and roosting activity. Spatial activity of females decreased from pregnancy to lactation and increased again in the post-lactation period. Overall time spent foraging did not differ among the three study periods. However, while pregnant and lactating females spent similar proportion of the night length foraging, females in the post-lactation period were foraging for shorter part of night. The frequency of nightly visits to roosts was highest during lactation but there was a trend towards shortening of particular visits during that period. All but one roost were in tree hollows excavated by woodpeckers in spatially restricted area of ca 0.7 km². Tree cavities used during pregnancy were located higher on a tree trunk and had larger entrance area than the cavities used in the two later periods. Bats switched roosts every 2–3 days (range 1–8) and moved to a new roost up to 800 m apart. Pregnant females tended to switch roosts more frequently than females in the two later periods. We did not observe a significant effect of minimum nightly temperature on the activity of radio-tracked Daubenton’s bats. Therefore, we suggest that observed seasonal changes in the pattern of behaviour of Daubenton’s bat females were driven by their changing energetic demands rather than by some extrinsic factors (e.g. weather conditions).