Non‐territorial Macaques Can Range Like Territorial Gibbons When Partially Provisioned With Food

Human food supplementation can affect components of animal socioecology by altering the abundance and distribution of available food. We studied the effect of food supplementation by comparing the ranging patterns and intergroup interactions of two groups of northern pigtailed macaques (Macaca leonina), a non‐territorial primate species. One group was partially reliant on food provisioning, whereas the other group foraged wild food. We also compared the macaques’ movement with that of a group of white‐handed gibbons (Hylobates lar), a territorial species inhabiting the same site. Home range, core area, and daily path lengths were significantly smaller for the semi‐provisioned group than for the wild‐feeding group. In contrast to wild‐feeding macaques, supplemented macaques showed higher fidelity to home range, core area, and particularly to the region where human food was most accessible and abundant. The relationship of daily path length and home range indicated a low defendability index for wild‐feeding macaques; the higher index for the semi‐provisioned group was consistent with the territorial pattern found in gibbons. Semi‐provisioned macaques showed further traits of territoriality with aggression during intergroup encounters. These findings indicate that human modification of food availability can significantly affect movement patterns and intergroup competition in macaques. The observed ranging dynamics related to food provisioning may decrease the efficiency of macaques as seed dispersers and increase predation on their home range, and thus have important consequences for plant regeneration and animal diversity.     

Effects of provisioning on the social behaviour of Japanese and rhesus macaques: Implications for socioecology

Long-term studies have shown remarkable similarity in the social behaviour and relationships of Japanese and rhesus macaques living in free-ranging groups. The vast majority of these studies have been of provisioned groups and many key principles have been derived from them. Provisioning is known to influence various aspects of life history and demography, as well as quantitative aspects of social behaviour, such as the frequencies of grooming and aggression. It has been widely assumed, however, that the fundamental characteristics of social behaviour and relationships observed in provisioned populations are representative of those that would occur under natural conditions. This paper reviews findings from fieldwork on Japanese macaques living under natural conditions, and compares them with patterns of social behaviour reported by multiple studies of provisioned groups of both species. Differences are apparent in the nature of social relationships between adult females, between adult males, and between adult males and females. Some of these differences can be attributed to the increased levels of aggression associated with provisioning. Others appear to be related to demographic peculiarities of provisioned groups, such as large size and skewed sex ratio. These differences can be used to generate predictions concerning the influence of ecological variables on the dynamics of social relationships and social structure. Ways in which these predictions could be tested by further fieldwork on provisioned and natural populations are discussed.     

Age class differences in the feeding behavior of captive Japanese macaques (Macaca fuscataia) in the forested and nonvegetated enclosure groups

Age class differences in feeding behavior of primates are affected by many factors, including feeding competition, foraging skills, habitat type, food abundance and distribution, body mass, and food types. Two captive groups of Japanese macaques (Macaca fuscata), one housed in a forested enclosure and the other in a nonvegetated enclosure, were studied to examine the effect of environmental enrichment on age class differences in feeding behavior. Although there was no significant age class difference in time spent feeding on provisioned foods in either enclosure, the feeding rate (intake of unit food/minute) of adults consuming provisioned monkey chow was significantly higher than that of immatures in both enclosures, and was faster for both age groups in the nonvegetated than in the forested enclosure. Overall, feeding time was greatly extended for individuals of both age classes in the forested enclosure compared with their counterparts in the nonvegetated enclosure. Immatures in the forested enclosure utilized a significantly greater number of plant species and food items, exploiting many food items available among the terminal branches, and spent significantly more time feeding than adults. Perhaps constrained by larger body size, adults fed more often on the ground or middle height of the trees, likely reducing competition over plant food resources between adults and immatures. The natural vegetation played an important role in extending feeding time and segregating substrate use during feeding by adults and immatures. This study revealed the benefits concerning environmental enrichment of a naturally forested enclosure, which provides captive primates the opportunity to exhibit age class and species-typical feeding behaviors of importance for their dietary maintenance and general health.     

The Hand That Feeds the Monkey: Mutual Influence of Humans and Rhesus Macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) in the Context of Provisioning

Historically, humans and other primates (primates henceforth) have coexisted across cultures and contexts, and many primate populations use anthropogenic food sources as their main or supplementary food. While primates may actively forage for such food, they are also directly provisioned by humans in many regions. Ethnoprimatology views humans and primates as cohabitants of integrated socioecological spaces who mutually influence each other’s ecologies and social lives. We contextualized provisioning of primates by humans within an ethnoprimatological framework and examined if the availability of anthropogenic food affected primate diets or the amount of time primates spent in anthropogenic habitats and whether primates influenced the human act of provisioning. To this end, we used scan sampling on a group of rhesus macaques across a year, and conducted interviews with 86 people who paused at a nearby tea shop for refreshments. We found that the macaques’ consumption of natural resources and dietary diversity decreased, and they spent more time in human-modified habitats when provisioned food was available. We also found that particular behaviors of the provisioned macaques stimulated provisioning by humans. Our findings show that provisioning influences macaque feeding ecology and habitat use, and that the behavior of the macaques themselves drives people to provide them with food subsidies, illustrating a complex web of interactions between the sympatric species.     

Social effects on foraging behavior and success depend on local environmental conditions

In social groups, individuals' dominance rank, social bonds, and kinship with other group members have been shown to influence their foraging behavior. However, there is growing evidence that the particular effects of these social traits may also depend on local environmental conditions. We investigated this by comparing the foraging behavior of wild chacma baboons, Papio ursinus, under natural conditions and in a field experiment where food was spatially clumped. Data were collected from 55 animals across two troops over a 5‐month period, including over 900 agonistic foraging interactions and over 600 food patch visits in each condition. In both conditions, low‐ranked individuals received more agonism, but this only translated into reduced foraging performances for low‐ranked individuals in the high‐competition experimental conditions. Our results suggest one possible reason for this pattern may be low‐ranked individuals strategically investing social effort to negotiate foraging tolerance, but the rank‐offsetting effect of this investment being overwhelmed in the higher‐competition experimental environment. Our results also suggest that individuals may use imbalances in their social bonds to negotiate tolerance from others under a wider range of environmental conditions, but utilize the overall strength of their social bonds in more extreme environments where feeding competition is more intense. These findings highlight that behavioral tactics such as the strategic investment of social effort may allow foragers to mitigate the costs of low rank, but that the effectiveness of these tactics is likely to be limited in certain environments.     

Influence of Human Food Consumption on the Time Budget of Vervets

In nonhuman primate groups that utilize crop and food-raiding strategies, the inclusion of human food in the diet can have a pervasive impact on the activity budget. Human food is usually of higher quality and energy per unit than wild food. Thus, metabolic demands may be reached sooner on a human food diet, which in turn leads to improved foraging efficiency. In particular, a reduction in time spent feeding is associated with an increase in time spent resting. We investigated changes in time budget in a group of vervets (Chlorocebus aethiops pygerthrus) living in a tourist and cultivated area of Entebbe, Uganda (Zoo group). Saj collected 123 hr of focal observations on 17 individuals. Human food constituted half of the diet of Zoo group. Access to human food resulted in a high proportion of time resting and a low proportion of time feeding. The group had a small average daily range and a small home range in relation to other reports on unprovisioned groups. The time budget differences suggest that the juveniles spent more time moving and feeding and less time resting than adults did, and that adult females were more social than adult males were. These patterns have been observed in both provisioned and unprovisioned vervet groups. In contrast to a report from an unprovisioned group (Harrison, 1983), lactating females in this provisioned situation were able to maintain feeding and activity levels similar to those of other adults. However, adult females spent significantly less time consuming human food than juveniles did. We suggest that the risk associated with human food consumption may explain the low consumption of human food by females with dependent offspring. The differences may also reflect the different nutritional requirements of lactating females or the tendency for juveniles to be more exploratory than other group members.     

Feeding Competition and Group Size in Alouatta pigra

Researchers consider group size in primates to be determined by complex relationships among numerous ecological forces. Antipredator benefits and better resource defense are the primary pressures for large groups. Conversely, intragroup limited food availability, can result in greater intragroup feeding competition and individual energy expenditure in larger groups, creating energetic advantages for individuals in small groups and placing an upper limit group size. However, the extent to which food availability constrains group size remains unclear for many species, including black howlers (Alouatta pigra), which ubiquitously live in small social groups (≤10 individuals). We studied the relationship between group size and 2 key indices of feeding competition—day journey length and activity budgets—in 3 groups of wild Alouatta pigra at a hurricane-damaged site in Belize, Central America. We controlled for differences in food availability between home ranges (food tree density) and compared both indicators of feeding competition directly with temporal variation in food availability for each group. Our results show no consistent association between resource availability, group size, and either index of competition, indicating that feeding competition does not limit group size at the site—i.e., that larger groups can form without increased costs of feeding competition. The results support the search for other explanations, possibly social ones, for small group size in the primates, and we conclude with suggestions and evidence for such alternative explanations.     

One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy

In this paper I examine behavioral strategies used by male and female tamarins to increase individual reproductive opportunities while continuing to maintain a high level of group cohesion and social cooperation. Tamarins of the genus Saguinus are characterized by social groups generally composed of more than one adult of each sex, but a breeding system in which only a single female in each group gives birth. The breeding sovereignty of a single dominant female limits the reproductive opportunities of subordinate females as well as the reproductive opportunities of resident adult males.^1-3 Despite extreme variability in year-to-year reproductive success among members of the same social group, field studies indicate that within-group intrasexual aggression and fighting are rare, and that both breeding and nonbreeding individuals expend time and energy cooperatively caring for young, defending productive feeding sites, and assisting in food harvesting activities.^4-11 In fact, Caine¹² has argued that “co-operation, tolerance, and flexibility” are the primary themes of tamarin social interactions (p. 218). A major question that remains unanswered, however, is how such high levels of cooperation could have evolved in a social system characterized by emigration of both adult males and females from the natal group, polyandrous mating, and intense reproductive competition.     

人工投食行为对非人灵长类社会生态的影响

近年来,国内开展了对几种非人灵长类投食群的研究。借鉴日本猴(Macaca fuscata)、恒河猴(M.mulatta)和黑猩猩(Pan troglodytes)长期积累的研究经验,有利于我们减少人工投食对非人灵长类带来的不利影响,也有利于推动国内非人灵长类社会生态学的深入研究。本文通过比较这三种灵长类野生群和投食群之间的差异,量化地分析了人工投食对灵长类动物社会生态学方面的影响。结果表明在社会行为方面,人工投食会导致灵长类动物的聚集、增加争斗频率、改变个体间等级关系、延缓分群现象、影响活动域和增加新兴行为。在种群数量方面,人工投食会缩短雌性性成熟时间、增加出生率和婴猴存活率、减少成年猴死亡率。而人工投食对雄性性成熟、出生间隔等方面的影响仍需要进一步考证。最后我们讨论了人工投食行为的利弊,并建议应谨慎和妥善地实施人工投食,和对非人灵长类投食群进行合理的监管。     

东方田鼠家群个体体重、攻击性及胆量对其扩散的影响

扩散作为动物适应生存环境的重要特征之一,受到自身生物学特征及环境等方面的制约。以家群形式生活和子代雄鼠扩散为主的东方田鼠,其成员个体是否因领地食物和空间资源竞争导致体重小、攻击性弱及胆小个体先行扩散。以新鲜马唐叶片构建三块密集均质的食物斑块,在食物斑块周边以透明玻璃设置观测箱,采用透明塑胶管连接三块食物斑块作为动物扩散的通道,构建东方田鼠扩散行为观测装置。将东方田鼠家群子代成员投放至带有自身家群气味的食物斑块,测定成员个体在食物斑块上的觅食行为序列过程和参数,以及向其他食物斑块扩散的行为过程和参数以及家群中先行扩散个体体重、攻击性及胆量占所有家群数的比率,检验成员个体的体重、攻击性及胆量对扩散的影响。结果发现,体重小、攻击性弱和胆小个体的觅食启动时间极显著地大于体重大、攻击性强和胆大个体的,但其先行扩散的比率却显著地大于体重大、攻击性强和胆大个体的;然而体重小、攻击性弱及胆小个体的扩散开始时间显著或极显著地大于体重大、攻击性强及胆大个体的。结果揭示,东方田鼠家群成员随着年龄的增长和对食物及空间资源竞争的加剧,体重大、攻击性强及胆大个体会迫使体重小、攻击性弱及胆小个体先行扩散。     

Increased Frequency of Intergroup Encounters in Wild Bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>) Around the Yearly Peak in Fruit Abundance at Wamba

Intergroup interactions in primates vary from nonagonistic to severely aggressive. Food resources and fertile females cause intergroup aggression when groups defend resources and mates from other groups. Peaceful intermingling during intergroup encounters is rare but has been reported in several primates, including bonobos (Pan paniscus). Although intergroup encounters in bonobos occur at both nonprovisioned and provisioned sites, provisioning may be one factor responsible for frequent intergroup encounters. We studied intergroup encounters between one bonobo group (PE) and its neighboring groups, one semihabituated and two habituated groups, under nonprovisioned conditions in 2010–2015 at Wamba, Democratic Republic of Congo. We examined whether fruit abundance and females with sexual swellings influenced encounter frequency. PE group encountered the other groups on 7.1 days (mean, range: 0–19) per month. Up to four different groups met simultaneously at one location. Encounter frequency was highest around the yearly peak in fruit abundance, suggesting that reduced food competition is linked to increased encounter frequency. During periods of relatively low fruit abundance, the probability of an encounter was higher when a higher number of adult females with maximum sexual swellings were present, suggesting that the attractiveness of females with sexual swellings promoted group encounters during periods of relatively low fruit abundance. These findings suggest that both competition for food and the availability of females with sexual swellings influence encounter frequency in bonobos.     

Does social status within a dominance hierarchy mediate individual growth,residency and relocation?

The availability of food, and hence energy, is known to influence the abundance, habitat choice and growth of individuals. In contrast, there is a paucity of knowledge on how the interaction of energy supply and social status determines patterns of residency and movement. This study tests whether the presence of conspecifics and an individual’s social status in relation to food supply influence the fitness and movement of a drift-feeding fish (Galaxias fasciatus). Using an information-theoretic approach (AIC), our analysis indicated that the most parsimonious model of fish movement among pools was one that included food supply, social rank and fish relative growth rate. Our results indicated that subordinate fish relocated more frequently compared to dominant fish, most likely as a consequence of intra-specific competition that limited the access of these smaller fish to resources and constrained their growth. Our results suggest that energy constraints may force individuals to explore new habitats in an effort to find more energetically profitable patches. We conclude that intra-specific competition mediated through the social hierarchy amongst closely interacting individuals plays a key role in determining individual growth, residency and relocation.     

Symmetrical patterns in non-agonistic social interactions found in unprovisioned Japanese macaques

Non-agonistic social interactions in an unprovisioned troop of Japanese macaques (Macaca fuscata yakui) were analyzed with the spacing between individuals, leading-following interactions, and exchange of social grooming. The most frequent interactions were found between kin-related females. Unrelated females stayed with one another rather frequently, but rarely exchanged social behaviors. Interactions between males and females were infrequent though they were occasionaly observed between high-ranking males and high-ranking females. Very frequent exchange of grooming was observed between males, and even high-ranking males exchanged grooming more frequently with males than with females. Most non-agonistic social interactions in the study troop were based on bidirectional exchange of social behaviors, in which no clear tendency relevant to dominance or sex was found; while in provisioned Japanese macaque troops, associations between males and females, between unrelated females, and between males were formed mainly be subordinates' active roles in associative behaviors. This seems relevant to the idea that dominance grealty influence social life in provisioned troops. The present study provides guidelines for interspecific comparison of social interaction patterns of macaque species.     

Adaptive attunement to the sex of individuals at a competition: the ratio of opposite- to same-sex individuals correlates with changes in competitors' testosterone levels

Evolutionary theories (e.g., the challenge hypothesis) suggest that testosterone plays an important role in intrasexual competition. In addition, those theories suggest that testosterone responses during competition should depend upon the presence of potential, immediate mating opportunities associated with the competition. The current research tested the hypothesis that the sex composition of individuals at a competition (ratio of opposite-sex, potential mates to same-sex individuals) would influence changes in competitors' testosterone levels. Consistent with our hypotheses, higher ratios of opposite- to same-sex individuals at an ultimate frisbee tournament were associated with greater increases in salivary testosterone among competitors. The relationship between sex ratio and increased salivary testosterone was observed for both male and female competitors and occurred regardless of whether competitors won or lost. Findings are consistent with the hypothesis that testosterone responses during competition are influenced by cues of potential, immediate mating opportunities.     

Food calling in wild ravens (Corvus corax) revisited: Who is addressed?

Numerous birds and mammals use vocal signals to advertise feeding opportunities but often such signals vary with individual and contextual factors. Non-breeding ravens call at food that is difficult to access, resulting in the attraction of nearby conspecifics. Although callers may benefit from group formation in various ways, we recently found substantial individual variation in food calling. We here explored whether this variation can be partly explained by the social dynamics in raven foraging groups, together with already known effects of age class and sex. Specifically, we expected ravens to respond to the presence or absence of affiliates that could act as cooperative partners in the forthcoming feeding event, that is they should call when other ravens were present but they themselves were alone rather than when they were also in company of an affiliation partner. We observed the vocal behaviour of individually marked wild ravens and, simultaneously, categorized their affiliative behaviour with other ravens in the minutes before experimentally controlled feedings. In line with our prediction, individuals were less likely to produce food-associated calls when they were in close contact with an affiliation partner prior to feeding as compared to when they were alone. Furthermore, sex and age class influenced food calling as females called more often than males and younger birds called more often than adult ravens. In conclusion, these results suggest that ravens attempt to find support from a particular cooperative partner by broadly advertise feeding opportunities via food-associated calls, especially when they have low chances in contest competition due to their age and sex. These findings lend further support to the assumption of raven flocks being structured by social relationships and individual birds flexibly controlling their vocal signalling according to the current flock composition.     

Sociality in Callithrix penicillata: II. Individual Strategies During Intergroup Encounters

In social animals, intergroup interactions, whether through agonistic and competitive behaviors or affiliative ones, can influence important parameters such as home range, territory sizes, and access to resources, which may directly affect both female and male fitness. We studied the intergroup interaction patterns of a wild group of black-tufted-ear marmosets (Callithrix penicillata) in central Brazil. Agonistic interactions occurred at low frequencies during intergroup encounters. The marmosets directed agonistic interactions without physical aggression primarily against same-sex individuals, suggesting that male and female aggression patterns are shaped by their sexual interests. However, females of the focal group also directed agonistic behavior toward extragroup males that attempted copulation. The marmosets appeared to use intergroup encounters to gather information about possible partners and extragroup reproductive opportunities. Intergroup sexual interactions occurred mainly in the form of copulations or attempted copulations by all adults, with the exception of the dominant female. Our results suggest that a possible reproductive strategy used by males is to attempt fertilization of extragroup females. Adult males copulated with the same extragroup female during several opportunities, which suggests sperm competition or the establishment of social bonds with neighboring females.     

Impact of Translocation,Provisioning and Range Restriction on a Group of Macaca thibetana

We examined the possible long-term impact of translocation and subsequent provisioning and range restriction on recruitment rates in a group of rare Tibetan macaques (Macaca thibetana) in Anhui Province, China. We compared demographic data recorded in the group (and in its fission products) during the 6 years before and after translocation and in a group with no history of management. We also compared preliminary data related to nutritional condition, habitat characteristics, and group activities. Infant losses markedly increased following translocation and management. Estimated measures of nutritional condition varied more among adults in the managed group than among those in the never managed group, suggesting that members of the managed group may have experienced higher levels of intragroup competition. We hypothesize that increased levels of intragroup competition for provisioned food may have put infants at increased risk.     

神农架川金丝猴投食群的母婴关系

灵长类动物母亲的育婴行为不仅对后代的存活起着关键作用,而且对婴猴的发育和成年后的社会交往有着重大影响,因此母-婴关系一直是灵长类学研究的热点之一。为了解川金丝猴的母-婴关系,探讨川金丝猴母-婴关系个体差异的影响因素,我们于2013年3月至2014年10月,以母-婴间相对距离表示照料强度,对神农架川金丝猴的母-婴照料关系以及母亲照料强度个体差异的影响因素进行了定量研究。结果表明：母亲照料行为强度、母亲对阿姨行为的容忍与婴猴年龄相关,限制行为与婴猴年龄不相关。身体接触与婴猴年龄不相关;腹部接触以及母-婴相对距离小于1 m与婴猴年龄呈负相关;相对距离1 m至5 m、相对距离5 m至10 m和相对距离大于10 m与婴猴年龄呈正相关;母亲对阿姨行为的拒绝与婴猴年龄呈负相关;母亲对婴猴的限制行为与年龄不相关。总的来说,即随着婴猴成长,母婴间距离越来越远,母亲也逐渐减少对婴猴的保护。母亲的生育经验、婴猴性别、婴猴出生先后和社会单元大小对神农架川金丝猴母婴关系没有显著影响,补食群丰富的食物资源和群内雌性友好的关系可能是导致本结果的原因。     

The evolution of social philopatry and dispersal in female mammals

In most social mammals, some females disperse from their natal group while others remain and breed there throughout their lives but, in a few, females typically disperse after adolescence and few individuals remain and breed in their natal group. These contrasts in philopatry and dispersal have an important consequence on the kinship structure of groups which, in turn, affects forms of social relationships between females. As yet, there is still widespread disagreement over the reasons for the evolution of habitual female dispersal, partly as a result of contrasting definitions of dispersal. This paper reviews variation in the frequency with which females leave their natal group or range (social dispersal) and argues that both the avoidance of local competition for resources and breeding opportunities and the need to find unrelated partners play an important role in contrasts between and within species.     

You are Not Welcome: Social Exchanges between Female Spider Monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)

Group living leads to competition for food between group members. Two types of intragroup food competition may occur: scramble competition, in which all group members use the same resource, such that feeding opportunities are equal for everyone; and contest competition, in which some group members monopolize resources through aggression and dominance. In species in which females disperse from the natal group and immigrate into other groups, immigrant females increase group size and thus possibly food competition. Under these circumstances, other females may use aggression to discourage new females from joining the group. We assessed the distribution of aggression, embraces, and kisses among female spider monkeys (Ateles geoffroyi) in relation to group tenure. We recorded social interactions during 1688 10-min focal animal samples on 11 females in Santa Rosa, Costa Rica. We found that aggression was rare between long-term resident females and aggression rates were not higher during feeding than in other contexts, suggesting there was little contest competition. Long-term residents and less recently immigrant females showed higher aggression rates toward the most recent immigrants than toward other females, especially during the first months after a female immigrated, which coincided with the dry season. We did not find similar patterns for embrace and kiss. These results suggest that other females target aggression toward the most recent immigrants to reduce scramble competition. This finding suggests that group tenure should be included in socioecological models for species with female dispersal.