Social patterns of food sharing in monogamous owl monkeys

Captive owl monkeys (Aotus nancymaae, A. azarai) share food frequently within both families and pairs. In this study food sharing was observed in seven mated pairs and four families (i.e., four mated pairs and their offspring). Patterns of food sharing were examined with respect to age class, sex, and the presence or absence of dependent offspring. Within families, most food transfers were from adult males to developing offspring. Adult males and females transferred food to their mates in caged pairs as well as in family units. Food interactions between adults are as likely to result in food transfers as those between adults and offspring. This pattern of food sharing between mates in a monogamous species may serve both nutritional and social functions that differ from those in polygamous species.     

Rensch's rule, Bergmann's effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina

Some monogamous primates are characterized by biparental care, territoriality, and a reduced level of physical dimorphism. In others, the relationship between those behavioral patterns and dimorphism is less clear. I tested Bergmann's and Rensch's rules using Aotus spp. body mass data and I characterized the extent of sexual dimorphism in body mass, dental and physical measurements in a socially monogamous owl monkey population (n = 91 adults) from the Argentinean Gran Chaco. A. azarai azarai from the Argentinean Chaco is larger than the more tropical owl monkey species (r = 0.7, N = 6 species), but there is no apparent increase in sexual dimorphism with increased body mass. The body masses of adult male and female A. a. azarai were remarkably similar (Mean = 1.26 kg); there were no marked sex differences in most skeletal measurements, but males had higher and wider upper and lower canines than did females. Body mass and neck circumference were positively and strongly related (r = 0.533, n = 52), and the body mass of adults was not a reliable indicator of their age (r = 0.03, n = 10). The data illustrate the complexities inherent in examining and summarizing within population variation in skeletal and nonskeletal measurements and contribute to a better understanding of the relationships between monogamous behavioral patterns and sexual dimorphism.     

The Breeding System of the Acorn Woodpecker in Central Coastal California

Adult spatial relationships and social organization in a marked population of alpine mammals, the pika (Ochotona princeps), were studied over a 3-year period in the Rocky Mountains of Colorado. Home range size, distances between centers of activity of dyads, and weighted overlaps of home ranges of dyads were used to define space use patterns. Disappearance and establishment of individuals reflected the temporal component of space use. Relative frequencies of foraging (haying and feeding), surveillance, and communication (short calling, long calling, cheek rubbing) behaviors were recorded. Social relationships among adults were defined by agonistic interactions (aggression) and affiliative behaviors (social tolerance, vocal duets, copulations). Males and females occupied individual home ranges of equal size on talus, their obligate habitat type. Adjacent home ranges were normally occupied by pikas of the opposite sex. Replacement of home ranges was always by a member of the same sex as the previous occupant. A high degree of affiliative behavior was expressed between spatially contiguous heterosexual dyads. Aggression was greater among intrasexual than heterosexual dyads, and spatial overlaps among intrasexual conspecifics were less than among heterosexual conspecifics. Ecological constraints, such as the distribution of food (primarily located in meadows adjacent to the talus) and the short summer reproductive season (placing a premium on early appropriately timed litter;;) have apparently led to a facultatively monogamous mating system. Males can neither monopolize essential resources sufficiently to attract several females, nor defend groups of females as social repulsion among females further increases their dispersion.     

Begging and social tolerance: Food solicitation tactics in young chimpanzees (Pan troglodytes) in the wild

The substantial role of food sharing in human evolution has been widely recognized, and food-soliciting tactics may have been critical in facilitating these transfers. Great apes, our closest living relatives, also use different food-soliciting tactics to obtain food from both kin and non-kin. However, the individual and social factors involved in requests for and subsequent transfers of food have been relatively little studied. Here, we examined which tactics (e.g., tactile gestures, taking actions, and vocalizations) infant chimpanzees (Pan troglodytes) employ to solicit food as well as the success of obtaining food from their conspecifics. Using a multimodal approach, we focused on food-related interactions in 14 chimpanzee infants of two different subspecies (P. t. schweinfurthii/verus) living in the communities of Kanyawara, Uganda, and Taï South, Côte d'Ivoire. Overall, we found that infants' solicitation tactics included mainly visual or tactile gestural requests and taking attempts, while vocalizations and gestures involving auditory components were rarely used. With increasing age, infants used more visual gestures when soliciting food from conspecifics other than the mother. If food was solicited from mothers or maternal kin, infants predominantly begged for food via (mechanically effective) taking attempts. In terms of subsequent food transfers, taking attempts were more successful than gestures. In light of the prevalent use of non-contact begging despite low rates of success, food solicitation in young great apes might also function to facilitate social tolerance and gain social information. We thus conclude that the food sharing context might represent a critical platform to learn and practice social rules underlying cooperative interactions, which can later be generalized across collaborative domains.     

Perseverance and food sharing among closely affiliated female chimpanzees

Chimpanzees (Pan troglodytes) have been frequently observed to share food with one another, with numerous hypotheses proposed to explain why. These often focus on reciprocity exchanges for social benefits (e.g., food for grooming, food for sex, affiliation, kinship, and dominance rank) as well as sharing based on begging and deterring harassment. Although previous studies have shown that each of these hypotheses has a viable basis, they have only examined situations in which males have preferential access to food whereby females are required to obtain the food from males. For example, studies on male chimpanzee food sharing take advantage of successful crop-raids and/or acquisitions of meat from hunting, situations that only leave females access to food controlled by male food possessors. This begs the question how and with whom might a female chimpanzee in sole possession of a high-quality food item choose to share? In two large captive groups of chimpanzees, we examined each of the hypotheses with female food possessors of a high-quality food item and compared these data to a previous study examining food transfers from male chimpanzees. Our results show that alpha females shared significantly more with closely affiliated females displaying perseverance, while kinship and dominance rank had no effect. This positive interaction between long-term affiliation and perseverance shows that individuals with whom the female possessor was significantly affiliated received more food while persevering more than those with neutral or avoidant relationships towards her. Furthermore, females with avoidant relationships persevered far less than others, suggesting that this strategy is not equally available to all individuals. In comparison to the mixed-sex trials, females chose to co-feed with other females more than was observed when the alpha male was sharing food. This research indicates that male and female chimpanzees (as possessors of a desired food item) share food in ways influenced by different factors and strategies.     

Food transfers in wild and reintroduced golden lion tamarins,Leontopithecus rosalia

We collected data from wild and reintroduced golden lion tamarins (Leontopithecus rosalia) to describe the behavior of donor and recipient during food transfers, evaluate the effect of supplemental feeding on food transfer behavior, and examine various hypotheses concerning the function of food transfers in primates. Behavioral observations were conducted on 12 groups of tamarins with young (N = 30) between the ages of 1 week and 1 year old. Results show that food transfers involve various behaviors, from steals by recipients to offers by donors; transfers mostly derive from adults and are directed at immature weaned young (between 3 and 9 months old); and that most items transferred were prey or fruits that require skill to process. Eleven percent of food transfers were preceded by an adult vocalization specific to that context, whereas 86% were preceded by conspicuous infant vocalizations and begging behavior. The most common vocalizations were loud and atonal (rasps) and broad banded frequency modulated (trills). Infants born to reintroduced parents vocalized less, whereas reintroduced adults vocalized more before transferring food than their wild counterparts. Reintroduced adults and young received more food transfers (4.4 per hr) than did wild‐born adults and young (2.2 per hr). Our findings suggest that food transfer in golden lion tamarins is best understood as provisioning of young that have not fully developed foraging skills to ensure they get the necessary resources for growth and survival. Am. J. Primatol. 48:305–320, 1999. © 1999 Wiley‐Liss, Inc.     

Biparental care and obligate monogamy in the rock-haunting possum, Petropseudes dahli, from tropical Australia

Monogamy is rare among mammals, including marsupials. I studied the social organization of the little-known rock-haunting possum in Kakadu National Park in Northern Australia. Preliminary field observations revealed that the majority of possums live in cohesive groups consisting of a female-male pair and young, suggesting a monogamous mating system. I used radiotracking to determine home range patterns, and observations to measure the degree of symmetry between the sexes in maintaining the pair bond and initiating changes in group activity. I also measured the extent of maternal and paternal indirect and direct care. Nocturnal observations and radiotelemetric data from 3 years showed that six possum groups maintained nonoverlapping home ranges with long-term consorts and young sharing dens. Males contributed more than females to maintaining the pair bond but they contributed equally to parental care. For the first time, the parental behaviours of bridge formation, embracing, marshalling of young, sentinel behaviour and tail beating are reported in a marsupial. Males participated to a high degree in maintaining relationships with one mate and their offspring. Collectively, these results suggest that the mating system of this wild population of rock-haunting possums is obligate social monogamy. Copyright 2000 The Association for the Study of Animal Behaviour.     

Territorial cooperation and social monogamy: factors affecting intersexual behaviours in pair-living snapping shrimp

Among the factors that may contribute to the evolution of social monogamy are selection for extended mate guarding of females and selection for territorial ‘cooperation’. Many socially monogamous taxa are also territorial, with ‘partners’ sharing a single territory, suggesting that one or both partners may benefit by sharing territorial maintenance. Snapping shrimp (genus Alpheus) are socially monogamous and territorial, living in excavated burrows or with host organisms, with females performing all parental care. The territorial cooperation hypothesis predicts that male and female partners share (1) territorial defence, resulting in a reduction in the risk of eviction from the burrow, (2) burrow construction duties, such that individuals in pairs spend less time in burrow construction relative to solitary individuals, and/or (3) foraging duties, by returning food to the burrow, where it is consumed by both partners. UsingA. angulatus as a model species, a territorial defence experiment revealed that females in pairs were significantly less likely than solitary females to be evicted by female intruders, but males in pairs were not significantly less likely than solitary males to be evicted by male intruders. A subsequent experiment revealed that paired males were significantly less likely to be evicted by an intruding male if paired with sexually receptive females than if paired with nonreceptive females. Another experiment revealed that (1) paired females spent significantly more time in burrow construction than paired males, and (2) both males and females consistently returned food items to the burrow, perhaps incidentally provisioning their mates. These data suggest that social monogamy may have been selected for in part because of the advantages of territorial cooperation, as both males and females are likely to benefit by dividing the labour of territorial defence and maintenance. These tests of the territorial cooperation hypothesis are synthesized with data from tests of the extended mate-guarding hypothesis to place snapping shrimp pairing behaviour into a larger construct incorporating both the influence of ecological pressures (territoriality) and mating interactions between the sexes. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Environmental determinants of butterflyfish social systems

Synopsis Butterflyfishes (Chaetodontidae) display a variety of social systems, including monogamous pair-bonds, harems, and schooling with group spawning. The range of reproductive options available to butterflyfishes is shaped by their general life history characteristics, such as broadcast spawning with widely dispersed pelagic larvae, large body size and low adult mortality. The distribution and quality of food resources are major determinants of group size and mobility, thereby influencing the relative costs and benefits of available options, and determining specific social systems. Planktivorous and corallivorous butterflyfishes exemplify the relationship between food resources and social systems. Pelagic plankton is a patchy, but temporally and spatially unpredictable food resource which is efficiently exploited by fish in mobile schools. Neither sex is able to monopolize food resources necessary for the other sex, and plantivorous butterflyfishes appear constrained to spawn in groups. In contrast, corals are stable and predictable in space and time, favoring residence in one area and territorial defense of that space by coral-feeding butterflyfishes. Females defend food resources from other females, and males defend territories containing a female from other males. Males attempt to defend areas containing more than one female, but are unsuccessful. A monogamous social system results. This system favors the evolution of cooperative behavior between mates to increase female fecundity, as long as the male has an opportunity of sharing in that reproduction. Mate removal experiments conducted on two monogamous coral-feeding species,Chaetodon multicinctus andChaetodon quadrimaculatus reveal a division of labor between male and female pair-mates. Paired males assume most of the territorial defense activities, allowing their mates to feed more.     

Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.     

Spoiled Brats: Is Extreme Juvenile Agonism in Ring‐Tailed Coatis (Nasua nasua) Dominance or Tolerated Aggression?

Ring‐tailed coatis exhibit an extreme form of juvenile agonism not found in other social mammals. Two groups of habituated, individually recognized, coatis were studied over a 2.5‐yr period in Iguazu National Park, Argentina. Dominance matrices were divided by year and group, resulting in four dominance hierarchies which were analyzed using the Matman computer program. Strong general patterns were seen in both groups during both years. Adult males (one per group) were the highest ranking individuals, followed by male juveniles, female juveniles, adult females, and male and female subadults. The pattern in which young, physically inferior individuals were able to outrank larger adults is different from other social mammal species in that the juvenile coatis aggressively defended food resources and directed aggression towards older individuals. These agonistic interactions may not reflect ‘dominance’ in the traditional sense, and appear to be a form of ‘tolerated aggression.’ This tolerated aggression leads to increased access to food, and should help juveniles during a period in which they need to rapidly gain weight and grow. Because this tolerance of juvenile aggression is reinforced through coalitionary support of juveniles by adult females, agonistic patterns are also consistent with the hypothesis that juvenile rank is being influenced by high degrees of relatedness within coati groups. Although some interesting parallels exist, there is little evidence indicating that these dominance patterns are the same as those found in other social mammals such as hyenas, lions, meerkats, or Cercopithicine primates.     

Extrapair paternity in the common sandpiper, Actitis hypoleucos, revealed by DNA fingerprinting

The prevalence of extrapair paternity in many socially monogamous passerines has not been mirrored in most monogamous nonpasserines studied to date. Here, we investigated the reproductive behaviour of a socially monogamous shorebird, the common sandpiper, using multilocus DNA fingerprinting. Given the high level of paternal care in the species, and the likely high costs in allocating care between kin and nonkin in species with precocial young, we predicted low levels of extrapair paternity similar to other monogamous shorebirds. We found the social mating system to be predominantly monogamous although one polyandrous pairing was identified. Of 83 offspring from 27 broods, 13 (15.7%) young from five (18.5%) broods were identified as being extrapair. There was no evidence of intraspecific nest parasitism or quasiparasitism. In this population, territorial intrusions were carried out largely by males but did not appear to be related to seeking extrapair copulations (EPCs). Seventy copulation attempts were observed and most were within-pair (84%). Six of eight EPC attempts occurred outside the territory of the female's social mate. Copulation rates were significantly higher just before and during egg laying than at other times during the study. At least two females that reared extrapair young had associated with males other than their eventual mates on arrival, suggesting that some females use rapid mate switching as a mating tactic, facilitated perhaps by the asynchronous arrival among both sexes in this population. Why some female sandpipers mate promiscuously remains unresolved.     

Begging for information: mother-offspring food sharing among wild Bornean orangutans

Transfer of solid food from mothers or other adults to dependent offspring is commonly observed in various primate species and both nutritional and informational benefits have been proposed to explain the function of such food sharing. Predictions from these hypotheses are tested using observational data on wild orangutans (Pongo pygmaeus wurmbii) at Tuanan, Central Borneo, Indonesia. In 1,145 hr of focal observation and 458 recorded food interactions between four pairs of females with offspring it was found that virtually all transfers were initiated by the offspring and that younger infants solicited food more often and did so for a greater variety of items than older offspring. All offspring primarily solicited food that was difficult to process, i.e., inaccessible to them. Furthermore, the amount of food solicitation was negatively correlated with ecological competence. Hence food sharing seemed to be related to an offspring's skill level, as suggested by the informational hypothesis. In contrast, offspring did not solicit high-quality items more than low-quality items and food sharing did not peak around the age of weaning, as predicted by the nutritional hypothesis. Mothers were usually passively tolerant, allowing offspring to take food but hardly ever provisioned. Parent-offspring conflict concerning food sharing was only observed well after weaning. Thus, by taking food directly from the mother, young orangutans were able to obtain information about the affordances and nutritional value of food items that were otherwise out of their reach and could familiarize themselves with the mother's diet. In species such as orangutans or other apes, characterized by a broad diet that requires extractive foraging, informational food transfer may be vital for an immature to acquire complex feeding skills and adult diet.     

Reproduction and survival of polygynous and monogamous Blue Tit Parus caeruleus

In a seven-year study of Blue Tits in optimal habitat near Antwerp, Belgium, 45 polygynous broods involving 22 males out of 667 successful first broods were found. In another 43 nests no male was found, although a major effort was made to trap all adults. The estimated proportion of polygynous males is 3.4%, if only confirmed cases are considered, but 10.8% if all possible cases are included. One male was paired simultaneously to three females.
Primary females (laying earliest in a triangle) were as successful as monogamous ones. Secondary (laying later in a triangle) and deserted females (nests in which no male was trapped), although still quite successful, raised fewer young and in one plot had a lower probability of recruiting offspring.
Both in males and females, the frequency of polygyny was independent of age. Adult survival did not differ between monogamous and polygynous males. Among females no effect of pairing status on survival was found in one plot, but in a second plot monogamous females survived better than others. It is concluded that in any study of Blue Tits in optimal habitat one could expect to find polygyny.     

Chick growth and survival in northern lapwings Vanellus vanellus indicate that secondary females do the best of a bad job

The polygyny threshold model predicts that monogamous and secondary females on average settle at the same time and have similar reproductive success. This is not generally found. Incorporating varying female competitive strength into the model, changes the predictions to state that secondary females should breed later and show a reduced success compared to that of monogamous and primary females. We examined if this was the case by investigating growth and survival in chicks of northern lapwings Vanellus vanellus from mothers of monogamous, primary and secondary mating status. Chicks where monitored from hatching to the age of 15–18 d. Growth and survival in secondary chicks was lower than in monogamous and primary chicks. Primary chicks survived significantly better than secondary chicks. Survival of monogamous chicks was comparable to primary chicks and close to significantly higher than in secondary chicks (p = 0.086). Among surviving chicks, daily weight gain in monogamous chicks was significantly higher than in secondary chicks. Growth rates of primary chicks were comparable to monogamous chicks and tended to be higher than in secondary chicks (p = 0.11). Monogamous and primary females both bred significantly earlier than secondary females, and chick survival and body‐mass growth decreased significantly with hatching date. Given the premium on early breeding in lapwings, secondary females appeared to do the best of a bad job, and their later onset of breeding could have been caused by poorer condition and/or lower breeding experience. Additional costs might also have accrued from sharing breeding resources with primary females that presumably were stronger competitors.     

Social Mating System and Sex-Biased Dispersal in Mammals and Birds: A Phylogenetic Analysis

The hypothesis that patterns of sex-biased dispersal are related to social mating system in mammals and birds has gained widespread acceptance over the past 30 years. However, two major complications have obscured the relationship between these two behaviors: 1) dispersal frequency and dispersal distance, which measure different aspects of the dispersal process, have often been confounded, and 2) the relationship between mating system and sex-biased dispersal in these vertebrate groups has not been examined using modern phylogenetic comparative methods. Here, we present a phylogenetic analysis of the relationship between mating system and sex-biased dispersal in mammals and birds. Results indicate that the evolution of female-biased dispersal in mammals may be more likely on monogamous branches of the phylogeny, and that females may disperse farther than males in socially monogamous mammalian species. However, we found no support for a relationship between social mating system and sex-biased dispersal in birds when the effects of phylogeny are taken into consideration. We caution that although there are larger-scale behavioral differences in mating system and sex-biased dispersal between mammals and birds, mating system and sex-biased dispersal are far from perfectly associated within these taxa.     

Willow tit Parus montanus extrapair offspring are more heterozygous than their maternal half‐siblings

Through extrapair matings, males can sire additional offspring with low cost and females may look for direct benefits in form of food or additional paternal care or gain genetic benefits that increase offspring fitness. We studied the patterns of female mate choice and frequency of extrapair paternity in the socially monogamous willow tit Parus montanus using microsatellites. We also examined the effect of heterozygosity on the growth rate and survival of the chicks. We found 25 mixed‐paternity broods out of 117 broods of which both parents were sampled. Altogether, 6.7% of sampled chicks were classified as extrapair young. The pairwise relatedness of social pairs did not correlate with the percentage of extrapair young in the brood and there was no difference in heterozygosity between promiscuous and monogamous parents. However, the extrapair young were more heterozygous than the within‐pair young in the mixed‐paternity broods. The maternal half‐siblings in mixed paternity broods were similar in body size. Thus, there was no indication for different growth rate between the siblings, but there were indications that heterozygosity affects survival.     

Communal breeding in the mara, Dolichotis patagonum

Mara social organization involves a combination of monogamous territoriality and co-operative, communal breeding that has not otherwise been described among mammals.
Some pairs reared their young in communal warrens, and pup survival was greater in warrens with larger memberships.
Pairs visited their young once daily, and females resisted, sometimes unsuccessfully, the attempts of interloping youngsters to nurse. Stolen nursing facilitated the survival of orphans.
More adults were present at larger creches, and total vigilance was thus increased despite each pair spending less time sitting-alert and less time at the warren. The proportion of the day for which at least one pair was vigilant at the warren increased to 90% with larger creche sizes.
Pups were much more likely to emerge from the warren when adults were present, and in the absence of adults were more likely to be sitting-alert close to the entrance.
These observations are compatible with hypotheses explaining the mara's social system in terms of resource dispersion, anti-predator behaviour and thermoregulation.     

Female extra-pair behaviour and environmental quality in the serin (Serinus serinus): a test of the 'constrained female hypothesis'

Recent behavioural and molecular studies have shown that in most monogamous bird species extra-pair copulations and fertilizations outside the pair bond occur routinely. The consequences of female extra-pair behaviour might comprise effects on important life-history traits, such as the extent of male parental care. In this study we test the assumption that, within a species, females'' options for extra-pair mating depend on female quality and the environments that females occupy. This ''constrained female hypothesis'' predicts that females in good environments or high-quality females are able to resist males'' control efforts better than females in poor environments or low-quality females. We test the idea in the socially monogamous serin. We found that the likelihood of extra-pair paternity is significantly higher in territories with high availability of food. There was a negative relationship between environmental quality (food availability) and paternity both in natural and in experimentally manipulated habitats. Male feeding rates were negatively related to food availability and positively related to paternity. These data and the additional result that in better environments all of a females'' offspring were sired by one extra-pair male provide support for Gowaty''s ''constrained female hypothesis''.     

Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch)

The purpose of this study was to describe patterns of infant care and development in family groups of the monogamous titi (Callicebus moloch). Three infant titis were observed with their natal family groups over the first six months of life. Field observations of extensive male involvement with infants were confirmed. Adult males were clearly the infants' primary social companions, and infants spent more time in contact with adult males at all ages than with mothers or older siblings. However, mothers and siblings also carried infants at times and interacted with them in affiliative ways (e.g., grooming, nuzzling, play). Mothers often invited nursing, but otherwise it was infants who primarily initiated transfers between carriers and approaches to parents, reminding us that the infants' own activities and their effects on caregivers should not be overlooked in considerations of the patterns of infant care. This is particularly important for those species exhibiting extensive parental involvement by males. It is suggested that substantial male care of young titi infants leads to several important consequences for the infant's social development, including the development of a stronger attachment to the father than the mother.