Adult-infant food transfer in common marmosets: an experimental study

Infant marmosets and tamarins obtain solid food items from adults during and after the time of weaning. In addition to providing nutrients, food transfers may provide infants with the opportunity to learn about diet. The aim of this study was to investigate patterns of begging and food transfer in captive groups of common marmosets during tests with 1) palatable novel food, 2) unpalatable novel food, and 3) familiar food. Infants may gain an opportunity to learn about diet breadth by preferentially begging for novel rather than familiar items, while adults may facilitate infant learning by differing in their willingness to transfer food depending upon the food's novelty or palatability. In this study, infants exhibited more interest and begging with novel food items than with familiar ones. However, food transfers were not more likely to occur with novel foods than with familiar ones, and in fact adults were more likely to refuse infant begging attempts with novel foods. The palatability of the food also did not influence the rates of refusal and transfer: adults transferred palatable and unpalatable novel foods with similar frequencies. These results suggest that infant marmosets gain an opportunity to learn about diet breadth by begging for novel foods, but adults do not preferentially transfer novel or palatable food items.     

Food sharing in lion tamarins: Tests of three hypotheses

Infant marmosets and tamarins (Callitrichidae) frequently receive food from older group members. Three possible functions of food sharing in lion tamarins were examined experimentally. The first hypothesis, that food sharing ensures that infants receive sufficient food even if it is difficult for them to acquire it themselves, was tested by varying the ease with which infants could reach a food source. When access to food was restricted, infants fed themselves less, received more food from others, and had a higher success rate in begging attempts. The second hypothesis, that food sharing helps teach infants an appropriate diet, was tested by presenting fruits that were novel to infants. Although infants fed themselves less under these conditions, adults were less likely to share novel foods than familiar foods. The final experiment compared food sharing when food was abundant with behavior when food items were presented singly. Infants fed themselves less and received more food from others when food items were rare. These results suggest that food sharing in lion tamarins helps to ensure that infants receive adequate amounts of food which is difficult to locate or acquire, but that it is not involved in teaching infants which foods they should eat. © 1993 Wiley-Liss, Inc.     

An experimental analysis of social interaction in the common marmoset (Callithrix jacchus jacchus)

Adult and juvenile common marmosets were introduced to unfamiliar conspecifics individually and in whole groups. In introductions using animals of the same sex, adults were mutually hostile unless they were related or socially familiar; juveniles behaved submissively to adults and little aggression was observed between juveniles. In introductions using animals of the opposite sex, males of all ages solicited females but females did not reciprocate. When whole groups were introduced, in two experiments most of the elder group members behaved aggressively and younger animals did not interact frequently; but in a third experiment, in which the adult males were related, little aggression was observed and younger animals behaved amicably. It is argued that the behavioral reactions shown by individual marmosets are related to territorial hostility and that the behavior of juveniles to adults may aid assimilation of younger animals into new groups.     

Response to novel food and the role of social influences in common marmosets (Callithrix jacchus) and Goeldi's monkeys (Callimico goeldii)

Neophobia, defined as showing caution toward novel features of the environment, is widespread in birds and mammals; it can be affected by ecology, early experience, and social context. In this study, we aimed to (i) investigate the response to novel food in adult common marmosets and Goeldi's monkeys and (ii) assess the role of social influences. We used an experimental paradigm employed previously with capuchin monkeys and children, in which a subject (observer) was presented with a novel food under three conditions: (i) Presence: group members did not have food; (ii) Different color: group members received familiar food whose color differed from that of the observer's novel food; (iii) Same color: group members received familiar food of the same color as the observer's novel food. Although most common marmosets tasted and/or ate the novel food, none of the Goeldi's monkeys ate it and only two sampled it. Differences in home range size and early social experience might explain the divergent behavior of the two species. Observers of both species similarly attended to group members and their visual attention increased with the number of group members eating, especially when the observer's and group members' foods were perceptually similar. However, we observed social influences on explorative behavior in Goeldi's monkeys but not on explorative or eating behavior in common marmosets. This result might be explained by the different pattern of response to novel food observed in the two species. Moreover, social influences on Goeldi's monkeys' behavior were nonspecific, i.e. they were not based on an appreciation that the food is safe because eaten by group members.     

Provisioning of Young in Golden Lion Tamarins (Callitrichidae, Leontopithecus rosalia): A Test of the Information Hypothesis

Provisioning of young after weaning or fledging is a highly variable phenomenon. Among cooperative breeders, such as marmosets and tamarins, both parents and natal adults may provision immatures. Experiments designed to measure the effects of food familiarity on food-transfer interactions were conducted on zoo-living golden lion tamarin, Leontopithecus rosalia , families to test one proposed benefit of provisioning to recipient young — that immature callitrichids learn food preferences through exposure to food items obtained from older group members. Adults transferred to immatures foods that were known to adults, but novel to immatures, and foods that were novel to all more frequently than foods that were familiar to both adults and immatures. Results suggest that adults alter their behavior such that learning by immatures is fostered. Immatures also were less likely to reject new foods acquired from other group members, compared with those obtained independently, suggesting the possibility that immatures attend to food transfer to facilitate incorporation of new foods into the diet. In contrast, anecdotal accounts of wild marmoset and tamarin food transfer have indicated that infants receive from adults foods that primarily are high in lipids and/or protein, as expected if provisioning acts to supplement nutrition. These apparently contradictory findings may reflect the differing effects of the captive and wild environment on food-transfer behavior or may point to a dual function of provisioning dependent on age of the recipient.     

Seeing group members eating a familiar food enhances the acceptance of novel foods in capuchin monkeys

In primates, social context is one of the factors that increases the acceptance of novel foods. Previous experiments showed that tufted capuchins, Cebus apella, eat significantly more of novel foods when in the presence of group members eating the same novel foods. Several processes may have led to these results. The mere presence of group members may reduce the individual's stress of being alone, or its neophobic response and, consequently, may increase its food consumption. The individual may be influenced by what group members do, and local/stimulus enhancement and/or social facilitation may occur. To investigate the above processes, we assessed whether an individual capuchin monkey's consumption of novel foods is lower when (1) the individual is alone with nobody in the nearby cage than when (2) group members are present in the nearby cage with no food or when (3) they are present and eating a familiar food. We tested 15 subjects with three novel foods, each presented in one condition. In both social conditions, the more group members there were by the food box the more the experimental subject ate. In addition, when group members were present and eating food, there was a significant increase in the acceptance of the three foods, regardless of what group members were eating. We argue that social facilitation of eating is a quicker way to overcome neophobia and only social facilitation of eating what the others are eating can be considered a safe way to learn about a safe diet. Copyright 2000 The Association for the Study of Animal Behaviour.     

Exploratory behavior and learning in laboratory marmosets (Callithrix jacchus jacchus): Comparisons between experimental-cage and home-cage activity

In this paper I examine exploratory behavior and learning in two groups of common marmosets (Callithrix jacchus jacchus), both living under laboratory conditions. The main aim of my studies was to compare behavior occurring in an experimental testing situation with home-cage behavior, and to assess conditions under which exploration is enhanced. One group of marmosets was tested individually in an experimental room away from a larger animal holding room, and a second group was observed in their own home cages, surrounded by other marmosets. Marmosets in both groups were given the opportunity to learn simple tasks, such as pressing a lever for food or jumping on to a wire grid to open a door and see a neighbouring marmoset, and were provided with sets of novel or familiar objects to encourage play and exploration. In the isolated experimental cage, marmosets which learnt a lever-pressing task showed higher general activity levels than controls; in the home cages the mere addition of novel objects resulted in enhancements in exploratory behavior (measured in terms of contacts with the objects). Although the activities associated with learning tended to decline over time, the novel objects remained a constant interest throughout the experiment. The results have implications for maintaining marmosets in captivity, especially in situations when they are housed separately.     

Diet,intestinal morphology,and nitrogen assimilation efficiency in the damselfish,Stegastes lividus,in Guam

Synopsis Analysis of stomach contents of Stegastes lividus revealed a shift from omnivory in juveniles to herbivory in adults. Red algae, primarily Polysiphonia spp., Gelidiopsis intricata and Ceramium spp., formed the bulk of the diet in all size classes. Foraminifera and small crustaceans were of particular importance in the diet of juveniles. Net nitrogen assimilation efficiency of field-fed S. lividus was approximately 61%, and did not vary with fish size. The net assimilation efficiencies of fish fed on Enteromorpha in the laboratory ranged from size-class means of 36–79% for nitrogen and from 29–72% for total organic material, and increased from juveniles to adults. Apparently, juveniles compensate for a lower efficiency in assimilating plant food by including a higher percentage of animal material in their natural diets. The ratios of intestine length to standard length (IL/SL) and to intestine diameter (IL/ID) increased rapidly in juveniles and leveled off in adults. The retention time for ingested food items may only be about one-half as long in juveniles as in adults. The combination of observed IL/ID ratios and estimated retention times proved most valuable in the interpretation of ontogenetic changes in feeding habits and assimilation efficiency.     

Progressive parenting behavior in wild golden lion tamarins

Young primates in the family Callitrichidae (the marmosets and tamarins) receive extensive and relatively prolonged care from adults. Of particular note, callitrichid young are routinely provisioned until well after weaning by parents and helpers, which is in stark contrast to typical juvenile primates, who must acquire most of their food independently once they are weaned. Adults of some callitrichid species produce a specialized vocalization that encourages immature group members to take proffered food from the caller. Here, I report that wild adult golden lion tamarins (Leontopithecus rosalia) not only used this food-offering call to encourage young, mobile offspring to approach and take captured prey from them, but as the young began to spend significant time foraging for themselves and to acquire prey by independent means, the frequency of these vocalizations in the context of food transfer declined. Adults then began to use food-offering calls in a novel context: to direct juveniles to foraging sites that contained hidden prey that the adults had found but not captured. During the period of these most frequent adult-directed prey captures, the independent prey-capture success rates of juveniles improved. Thus, adults modified their provisioning behavior in a progressive developmentally sensitive manner that may have facilitated learning how to find food. I hypothesize that as a result of these demonstrations by adults, juveniles either may be encouraged to continue foraging despite low return rates or to learn the properties of productive prey-foraging substrates in a complex environment.     

Close Proximity of the Heterosexual Partner Reduces the Physiological and Behavioral Consequences of Novel-Cage Housing in Black Tufted-Ear Marmosets (Callithrix kuhli)

The present studies assessed the extent to which heterosexual pairmates could buffer marmosets (Wied's black tufted-ear marmoset,Callithrix kuhli)against stress. Six male and six female marmosets from established groups were exposed to two experimental manipulations together with a control condition. Each condition lasted a total of 4 days. For the two experimental conditions, animals were removed from the family group and housed in a novel cage for 48 h in either the presence or the absence of the heterosexual pairmate. During the 48-h novel-cage housing period and for 48 h upon reunion of the subjects with the family group, concentrations of urinary cortisol were measured in the first void sample of the day and behavioral observations were conducted. When animals were housed alone in a novel cage they exhibited significant elevations in levels of urinary cortisol after 24 and 48 h of novel-cage exposure. In contrast, when marmosets were housed in the novel cage in the presence of the pairmate, levels of urinary cortisol did not change across the 4-day period. The presence of the social partner also reduced the behavioral manifestations of exposure to novelty. Upon reunion with the family group, animals that had been housed in the novel cage alone spent significantly more time in close proximity to the pairmate than animals that had been housed with the partner. A second experiment was conducted to determine the effect that separation from the pairmate, only (independent of any effects of novelty), had on levels of cortisol. Concentrations of urinary cortisol were measured in subjects housed in the familiar home cage, but in the absence of the pairmate, over a 48-h period and compared to concentrations of excreted cortisol immediately prior to separation. Separation from the pairmate did not elevate cortisol levels when the subject was housed in the home cage, suggesting that elevated cortisol levels in animals housed alone in the novel cage were in response to novelty exposure rather than to separation from the pairmate. Since the physical presence of the heterosexual partner reduced the physiological and behavioral effects of novel-cage housing, social attachments might function as homeostatic regulators of HPA function in marmosets.     

Food Acceptance and Social Learning Opportunities in Semi‐Free Eastern Chimpanzees (Pan troglodytes schweinfurthii)

When confronted with novel foods, chimpanzees’ responses combine a mixture of curiosity and cautiousness. Once the item is in the mouth, the initial cautiousness is followed by an aversion to bitter taste that is mediated mainly by the TAS2R gene family. For instance, variations on the TAS2R38 locus which has been studied extensively in humans have been associated with different acceptance of bitter substances. Surprisingly, while cautiousness and bitter taste aversion were selected to prevent any risk of poisoning, very few studies on novel food acceptance have included the vegetative parts of plants. Moreover, the studies were usually carried out with captive apes faced to a very restricted variety of non‐toxic plants, hardly making the results representative. This study aims to replicate previous findings obtained in zoos while controlling for these limitations. We provided nine subgroups of eastern chimpanzees (Pan troglodytes schweinfurthii) living in the Ugandan sanctuary of Ngamba Island with novel plants known to be consumed by wild chimpanzees of the same subspecies, as well as domestic plants, wild sapota fruit and grey clay used by human local communities. We also genotyped their TAS2R38 gene. Our results confirm the very low genetic heterogeneity for TAS2R38 in this chimpanzee subspecies. Chimpanzees were particularly cautious towards the vegetative parts of novel plants, likely reflecting their behavioural strategy for avoiding toxic compounds. We also confirmed their higher propensity towards testing sapota and clay, reflecting their ability to expand their diet. In contrast with the results found in zoos, familiar and novel less‐palatable vegetative parts of plants did not elicit many interindividual observations. This may be explained by the items presented, which could have been so novel to be considered as enrichment in captive conditions, where the apes are rarely exposed to plants.     

Food and foraging behaviour of the lizard,Ctenotus taeniolatus

A sample of 261 Ctenotus taeniolatus revealed that this species of skink is principally insectivorous, the most common foods being lepidopteran and coleopteran larvae, orthopterans and formicids. The occurrence of these foods in the diet followed seasonal patterns. The prey of adults and juveniles did not differ qualitatively, although adults were capable of eating a greater diversity of prey sizes than juveniles. Lizards used both sit-and-wait and active foraging strategies, with adults and juveniles exhibiting these behaviours in different ratios.     

Ontogeny of Feeding Behavior of Eulemur fulvus in the Dry Forest of Mayotte

Captive data show that juvenile mammals usually reproduce the diet of the adult. However, it is not known whether, in natural environments, the process of feeding maturation varies according to available foods and to adult choices. I examined the feeding ontogeny of Mayotte brown lemurs (Eulemur fulvus), a presumed introduced species, from birth to 12 mo old in the southern dry forest of Mayotte. The study focused on activities and diets of 4 mothers and their juveniles from 2 groups in 1999 and 2000. In 2001, we also observed 2 other dyads from each group for 2 mo (March/April). I assessed plant phenology in each group's home range. There are 4 phases of feeding ontogeny: (1) the 3 mo following birth are characterized by lactation, early bouts of exploration, and consumption; (2) the next 2 mo are characterized by feeding and social weaning; (3) during the sixth and seventh mo, the daily feeding activity rhythms of the mother and her juvenile are synchronized and diets largely overlap; (4) at 10–12 mo of age, the feeding juvenile is closer to other group members than to its mother. During their first year of life, especially before being weaned, juveniles eat several food items that are not ingested by their mothers. It appeared that the progressive overlap in dietary items and feeding synchrony between mother and juvenile depends on several types of leaming. There is a correlation between the availability of particular food resources with high nutritional quality and timing of reproduction and infant maturation.     

Lower foraging efficiency of offspring constrains use of optimal habitat in birds with extended parental care

After reproducing successfully, birds with extended parental care form family groups. Despite being the dominant social unit, such family groups have been reported to switch to alternative habitat earlier than adults without offspring, with potential negative carry‐over effects for the next breeding season. Here we test a proposed mechanism for this earlier habitat switch, namely a low foraging efficiency in juveniles. Such a test is best performed under controlled conditions because in the field families may occupy food patches of a different quality than singles or pairs without young. We studied this mechanism in Bewick's Swans Cygnus columbianus bewickii, which trample (or ‘treadle’) for food buried in the sediment. The gross intake rate of juveniles was as low as 60% of that of adults, depending on the burial depth of the food. Trampling effort did not differ between age classes, but differences in intake rate were related to body size, suggesting that larger or heavier birds were trampling more efficiently. Corresponding giving‐up densities in the field were calculated to be c. 60% higher for juveniles than for adults. Our findings are consistent with the hypothesis that the lower foraging efficiency of juveniles may be responsible for the segregation of family groups from adults without offspring.     

尼日利亚热带雨林池塘中茄氏旗鳉的食性

本文逐月研究了尼日利亚Mfangmfangpond中茄氏旗鳉全年的食性。其食谱按优势多寡出现的次序分别是陆生无脊椎动物、大型植物、水生无脊椎动物、小型甲壳动物、沙粒和藻类。我们将膜翅目、鞘翅目和双翅目昆虫作为其食性的次级项,而全年都出现的有机体碎屑作为初级项。雄鱼较雌鱼捕食了更多的陆生无脊椎动物。茄氏旗在雨季有16项食物组成,但旱季只有7项。就相对重要性而言,陆生和水生无脊椎动物在旱季更大,而大型植物碎屑、小型甲壳动物、沙粒和藻类则在雨季更大。成鱼较幼鱼更多地以外源性无脊椎动物为食。雌鱼较雄鱼有更强的觅食能力;同样,成鱼较幼鱼的觅食能力强得多.     

Diet overlap among size classes of Colorado River cutthroat trout (Oncorhynchus clarki pleuriticus) in a high-elevation mountain stream

We examined the taxonomic composition, abundance, and size of food items consumed by young-of-year, juvenile, and adult Colorado River cutthroat trout (Oncorhynchus clarki pleuriticus) in order to determine the degree of diet overlap occurring in a relatively unproductive, high-elevation, mountain stream. Overall, we identified 49 Families of insects representing nine Orders, and 4 other Classes of organisms in the diets of the trout sampled and saw no evidence of piscivory. Each size class of fish consumed significantly different taxa and significantly different sizes of food items. However, despite these differences, the proportional similarity index (PSI) indicated that there was considerable overlap in taxa and sizes of organisms consumed by the three size classes. The greatest overlap occurred between young-of-year and juveniles, and between juveniles and adults. Both the relatively high proportion of small items in the adult diet and the slow growth rate of adults in these streams indicate that food may be limiting for adults and that intraspecific competition between adults and smaller size classes may be high.     

Variation among juvenile capuchins in social influences on exploration

The exploratory or feeding activities of others might influence the timing, the place, or both, of exploratory activities among young group-living individuals, and this influence might affect the information gained by individuals during exploration. This study examined the temporal and spatial aspects of adults' influence on the exploratory behavior of juvenile capuchins, and on the juveniles' acquisition of a novel behavior. Two experimental apparatus, which were initially novel to the juvenile subjects but familiar to the adults, and which provided food when a tool was used properly, were presented to group-housed capuchin monkeys. The apparatus were presented (a) in a central area, in which all animals could interact with the apparatus and in which several older group members regularly solved the tasks (group site), and (b) in a protected site within the home cage (crèche) that only juveniles could enter, but from which the rest of the cage, including the group site, could be viewed. Juveniles contacted the apparatus at the crèche more often when there was no apparatus at the group site, but only half the individuals made greater use of the apparatus at the group site than at the crèche when an apparatus was present at both sites. Seven of nine used an apparatus more often when adults also had an apparatus, than when adults did not have an apparatus. These results indicate that juveniles' exploratory activity is only weakly related to adults' activity. The linkage appears closer for younger juveniles (20 months or less) than for older juveniles. Moreover, as only older juveniles learned to solve the tasks, coordination of exploration with adults was evidently not related to learning a new skill. © Wiley-Liss, Inc.     

Shoaling preference and evidence for maintenance of sibling groups by juvenile black perch Embiotoca jacksoni

Group sizes in free‐living juvenile black perch Embiotoca jacksoni were quantified and predictions of the hypothesis that such groups comprise sibling brood‐mates were tested. Group sizes in the field were within the range of female brood sizes and often occurred close to each other but did not merge. In captivity, juveniles formed groups immediately after birth. In laboratory experiments, they also associated significantly more with chambers containing familiar members of their own brood than empty chambers but did not associate more with chambers containing similar‐sized juveniles from a different brood. Juvenile E. jacksoni also associated significantly more with chambers containing familiar brood‐mates than with chambers containing unfamiliar members of a different brood. The strength of this preference increased with the number of days fish had been together since birth. When two broods were placed in a large outdoor tank, all individuals from both broods directed significantly more aggressive acts towards members of the other brood than towards members of their own brood. While the relative effects of familiarity and relatedness cannot be completely separated in this viviparous species, associating with familiar individuals would facilitate the maintenance of sibling groups in the field.     

Age-dependent patterns of intensive observation on elders by free-ranging juvenile Japanese macaques (Macaca fuscata yakui) within foraging context on Yakushima

Early learning about edible food in the environment is a critical survival task for young nonhuman primates. Social learning and social facilitation are often cited to explain how youngsters learn to select and find their food. In this framework, we observed eight mother-youngster pairs of free-ranging Japanese macaques divided into two sets according to the age of the young (infants aged between 7 and 12 months and juveniles aged between 1.5 and 2 years) during three winter months. We systematically investigated the intensive observation directed by the youngsters toward elders by recording the target's identity (e.g. mother, subadult), the items manipulated by the elder and those items closely observed by the youngster, along with the behavior of the youngster preceding and immediately following an intensive observation period. The diet of the mothers and juveniles was estimated from time records of each feeding occurrence for each food item (identified to species level) and from the quantity of fresh matter ingested. The results show that intensive observation by both infants and juveniles were directed toward those elders engaged in plant and invertebrate foraging. Such behavior was age-dependent, being more frequent in infants than in juveniles. The majority of the intensive observations were directed toward the mother. Intensive observations also shaped a change in the behavior of infants by significantly stimulating the investigation of food items and locations otherwise not investigated by juveniles. Moreover, infants showed a particular interest in rare food items and especially invertebrates. Age differences between the two sets of young and their interest in rare foods are discussed with reference to the occurrence of intensive observation within the framework of kin relationships, social organization, and social transmission of information about food type and food location and its survival values.     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.