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.     

Response to changes in food palatability in tufted capuchin monkeys, Cebus apella

Palatability of plant foods may change over time in relation to the concentration of toxic secondary metabolites. We investigated the behavioural response of capuchin monkeys to this type of change and assessed the influence of social conditions. Twenty-seven tufted capuchin monkeys were presented in Social or Individual conditions with a familiar palatable food (phase 1), with the same familiar food to which pepper had been added, making it unpalatable (phase 2), and with the same familiar palatable food of phase 1 (phase 3). Five sessions were carried out in each phase. The capuchins adapted quickly to the change in food palatability by reducing (phase 2) and increasing (phase 3) the amounts of food eaten. The unpalatable food prompted an increase in olfactory exploration and in food processing. The experimental conditions (Social versus Individual) did not influence consumption, or any of the other behaviours. In addition, capuchins were more often near subjects with food in phases 2 and 3 in which palatability changed than in phase 1. These findings show that capuchins readily adjust to changes in flavour and palatability of a familiar food and that sudden unpalatability has no carry-over effects. Therefore, capuchins behave differently towards a familiar food whose palatability has changed than they do towards novel foods. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Food Transfer and Development of Feeding Behavior and Food-Associated Vocalizations in Cotton-Top Tamarins

Food transfer between adults and infants is common in many marmoset and tamarin monkeys, and is often accompanied by vocalizations. We hypothesized that vocalizations by adults in a food transfer context creates an opportunity for infants to learn not only what foods are appropriate but what vocalizations are appropriate in feeding contexts. We studied the development of feeding behavior and food-associated vocalizations in 10 infant cotton-top tamarins through the first 20 wks of life. Infants obtained solid food through transfers from older group members, primarily the adult male, beginning at weeks 5–6. Both adults and infants vocalized during food transfers with adults, producing rapid sequences of the call types adults normally give when feeding. Infants were usually successful in obtaining food primarily when the adult was vocalizing. The sooner infants were active participants in food transfers, the sooner they began to feed independently. In the early weeks, infants produced a large number of vocal types during food transfers, but with increasing age there was a steady increase in the number of adult-form food calls and a reduction in other, non-food-associated calls. Infants that fed independently at an early age produced fewer non-food-associated calls by the last month of observation. Infants called at higher rates to their most preferred food. Food transfers accompanied by vocalizations may provide an opportunity for infants to learn about appropriate foods as well as the vocalizations that accompany feeding in adults, and may represent a form of 'coaching' or information donation by adults.     

Effect of Removal from the Family Group on Feeding Behavior by Captive Callithrix jacchus

Common marmosets are omnivorous primates with a highly diversified diet. There is no study describing if and how the diet is learned. Infants get their first bits of solid food from other monkeys in the group, which suggests that they may need an introduction to food items by older individuals before including them in their diet. We assessed the acceptance of novel and familiar food items by common marmosets, both isolated and in their family groups. We tested adult, subadults and juveniles from 5 captive families while isolated and in their family groups. The test consisted of presenting for 10 min novel and familiar food items to isolated individuals or to the whole family. We recorded the latency to start eating and the number of food items ingested. When isolated, adults ate more novel and familiar food items than juveniles did. They also started eating sooner than juveniles did. When tested alone, all juveniles, except one, never tasted novel food, and juveniles ingested fewer familiar food items than adults did. When tested in their family groups, juveniles ingested more familiar and novel food than when they were isolated. Our results suggest that: 1. juvenile common marmosets show more food neophobia than adults do, especially when alone; 2. the family group may facilitate the acceptance of novel food items by juveniles; 3. the family group, besides promoting the acceptance of novel food, may also increase its ingestion; and 4. dietary acquisition in Callithrix jacchus involves social facilitation.     

Food Sharing in Pied Bare-Faced Tamarins (Saguinus bicolor bicolor): Development and Individual Differences

We investigated food sharing behavior in 5 litters of pied bare-faced tamarins (Saguinus bicolor bicolor)—8 infants, from 3 families—from 5 to 26 weeks of age. The frequency of sharing by parents in response to infant begging increased steadily from the age of 5 weeks to 16 weeks, and then declined. Offering of food by adults without prior infant begging occurred at very low frequencies throughout observations (1.5% of total items transferred). On average, infants received approximately equal amounts of food from transfers from others and by self feeding until about 20 weeks, after which self feeding began to predominate. Begging success—the proportion of infant begs which resulted in food sharing—remained relatively constant over time, at 60–70%. Overall, therefore, the frequency of food sharing seemed to be governed by changes in infant rather than adult behavior. There were individual differences between adults in their response to infant begging, but two of three fathers transferred significantly more food to infants than mothers did. The results of this study emphasize the existence of specific and individual differences in food-sharing behavior, which must be taken into account in explaining its importance in the reproductive strategies of the Callitrichidae.     

Food sharing in black lion tamarins (Leontopithecus chrysopygus)

Food sharing behavior was investigated by studying 10 captive black lion tamarin (Leontopithecus chrysopygus) infants (six litters) between the ages of four and 26 weeks. The frequency of sharing by parents in response to infant begging increased steadily from the age of five to nine weeks, but then declined gradually, although infants were still receiving food even at 26 weeks. Until the age of 15 weeks, infants received more food items by transfer from other group members than they did from self-feeding. Thereafter, self-feeding predominated. Offering of food by adults without prior infant begging occurred at low frequencies (5.3% of items transferred) and ceased at 20 weeks of age. Begging success (the proportion of infant begs which resulted in food sharing) remained relatively constant, averaging 65%. In common with other lion tamarins, black lion tamarins appear to continue to share food with infants well after weaning, and until at least six months of age.     

Social learning influences the preferences of domestic hens for novel food

It has been argued that social learning helps animals either avoid noxious substances or identify food items, but evidence suggests that avian social learning is fundamentally different from that of mammals. In two experiments, we investigated whether the preferences of domestic hens, Gallus g. domesticus, for novel food were influenced by observing the feeding behaviour of conspecifics. In experiment 1, we attempted to confirm that birds can develop socially learnt aversions to unpalatable foods. Despite demonstrators showing a highly visible ‘disgust reaction’ after eating unpalatable coloured food, observers did not develop aversions to similarly coloured food. In experiment 2, we aimed to determine whether preferences for palatable food were socially learnt, and whether the extent of a demonstrator's preference for novel food affected the magnitude of the observer's socially learned preference. Demonstrators ate coloured food of standard or high palatability, or did not peck food at all. When the demonstrators pecked more frequently or fed more quickly from the food, the observers consumed a greater proportion of food of the same colour; however, this was only when the food was red, not green. We argue this indicates an unlearned aversion to red food, overcome by social learning of the food being highly palatable. The results provide no evidence that adult hens learn aversions through observing disgust reactions, but show that hens are sensitive to the extent of demonstrator preferences for palatable food. The data do not support the hypothesis that avian social learning is fundamentally different from that of mammals. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Food transfer between chimpanzee mothers and their infants

Food sharing among chimpanzees is known to occur particularly between mothers and infants and has been proposed to be a form of parental investment. To explore the function of food sharing, it is essential to know how and what is transferred to an infant from its mother. We investigated details of interactions leading to food transfer and characteristics of items transferred in three mother–infant (<2 years old) pairs in captivity. We gave one kind of fruit or vegetable to a mother and observed interactions between the mother and her infant. Tested items consisted of familiar and novel foods for infants. Two patterns of direct food transfer, so-called sharing, were recognized: (1) infant-initiated sharing in which the infant attempted to take food and the mother did not resist, and (2) mother-initiated sharing in which the mother spontaneously offered a part of her food without the infants attempts to take it. There were clear differences in the characteristics of items transferred in these two patterns of sharing. In infant-initiated sharing, palatable parts of the same food that the mother was eating were transferred. In contrast, in mother-initiated sharing, only unpalatable parts of food in the mothers possession were transferred. Mothers seemed to be reluctant to give nutritious foods to their infants during this study period. Infants, rather than mothers, were responsible for initiating and experiencing the diversity of adult foods in chimpanzees.Electronic Supplementary Material Supplementary material is available in the online version of this article at     

Developmental changes in food transfers in cotton-top tamarins (Saguinus oedipus)

We investigated the development of food transfer and independent feeding in cotton-top tamarin (Saguinus oedipus) families. We studied the relationship between infant-directed vocalizations and food transfers on the development of independent feeding in infants. We experimentally tested ten infants (eight twins and two singletons) three times a week for 17 weeks from before weaning through 20 weeks. Food transfers and vocalizations made during tests were recorded and analyzed to determine (1) the role of vocalizations (C- and D- chirps and D-chirp series) in food acquisition, (2) the relationship between food transfers and individual food acquisition, and (3) whether, owing to energetic costs of nursing and carrying twins, food is transferred to twins sooner than to singletons. Infants were more successful in acquiring food via begging when adults produced repeated vocalizations than when adults did not vocalize. Adults emitted more food-related vocalizations in rapid series when in the presence of infants, whereas during feeding in the absence of infants only single unit vocalizations were produced. Begging occurred frequently. Changes over infant age were not significant when all infants were included in analysis. However, when twin data were analyzed alone, begging success changed significantly over months, with successful begging peaking in month 3 (week 12). Begging success rate did not differ between twins and singletons, although twins fed independently sooner and at a higher rate than did singletons.     

Ultrasonic vocalization by female mice in the presence of a conspecific carrying food cues

In female mice, Mus domesticus, reunion with a same-sex conspecific is associated with intense ultrasonic vocalization. We examined whether the palatability of a familiar food eaten by a demonstrator mouse and the motivational state of the conspecific observer could modulate the number of ultrasonic calls uttered during female-female interaction in NMRI mice. A pilot study indicated that these calls were uttered almost exclusively by the observer member of the pair. Observers were either food deprived or not deprived and demonstrators were offered either no food, a palatable diet or an unpalatable diet. We monitored both the number of ultrasounds (range 65-75 kHz) uttered and a series of behavioural parameters during the first 3 min of social interaction after 24 h of separation. Observers investigated the nose area of demonstrators fed on the unpalatable diet more than the same area of demonstrators not given food. No differences were found in demonstrators' behaviour. Ultrasonic calls were given immediately after female-female reunion and were affected by both the motivational state of the observer and the salience of the information carried by the conspecific. These results suggest that the motivational state of the observer affects ultrasonic calling towards a demonstrator conspecific. Nondeprived animals produced more calls towards demonstrators fed on palatable food, whereas food-deprived subjects vocalized more to fed conspecifics, independently of the palatability of the food eaten by the demonstrator. We suggest that ultrasonic vocalization in female mice can facilitate proximity with a conspecific and the number of these calls is modulated by the salience of the information carried by the companion. Copyright 2000 The Association for the Study of Animal Behaviour.     

Response to novel food in infant chimpanzees: Do infants refer to mothers before ingesting food on their own?

We investigated infant response toward novel food in captive chimpanzees under the condition in which they can explore such items freely together with their mother. Infants first approached novel foods rather than familiar ones when presented simultaneously. However, they did not ingest novel food immediately, but always sniff-licked it first. Infants tended to pay attention to their mothers before mouthing or ingesting novel foods themselves, but never did so with familiar ones. In response to the infant's activity, mother chimpanzees were tolerant rather than actively interfering. Those results imply that chimpanzee infants respond to novel foods in a neophobic way and refer to their mother for some kind of cue before attempting to ingest them.     

Aversive Learning in the Praying Mantis (<Emphasis Type="Italic">Tenodera aridifolia</Emphasis>), a Sit and Wait Predator

Animals learn to associate sensory cues with the palatability of food in order to avoid bitterness in food (a common sign of toxicity). Associations are important for active foraging predators to avoid unpalatable prey and to invest energy in searching for palatable prey only. However, it has been suggested that sit-and-wait predators might rely on the opportunity that palatable prey approach them by chance: the most efficient strategy could be to catch every available prey and then decide whether to ingest them or not. In the present study, we investigated avoidance learning in a sit-and-wait predator, the praying mantis (Tenodera aridifolia). To examine the effects of conspicuousness and novelty of prey on avoidance learning, we used three different prey species: mealworms (novel prey), honeybees (novel prey with conspicuous signals) and crickets (familiar prey). We sequentially presented the prey species in pairs and made one of them artificially bitter. In the absence of bitterness, the mantises consumed bees and crickets more frequently than mealworms. When the prey were made bitter, the mantises still continued to attack bitter crickets as expected. However, they reduced their attacks on bitter mealworms more than on bitter bees. This contrasts with the fact that conspicuous signals (e.g. coloration in bees) facilitate avoidance learning in active foraging predators. Surprisingly, we found that the bitter bees were totally rejected after an attack whereas bitter mealworms were partially eaten (~35%). Our results highlight the fact that the mantises might maintain a selection pressure on bees, and perhaps on aposematic species in general.     

A Behavioral Mechanism for Incorporating an Unpalatable Food in the Diet of a Generalist Herbivore (Orthoptera: Acrididae)

We investigated mechanisms that could lead to incorporation of unpalatable foods into the diet of a generalist grasshopper, Schistocerca americana: nutritional stress, habituation, learning, and attraction to novelty. The model system involved mesquite, a palatable but inferior food, and mulberry, an unpalatable but adequate food. Nutritional stress, due to prolonged intake of the inferior food, mesquite, did not increase the acceptability of mulberry. Habituation to the deterrent compounds in mulberry and associative learning of the nutritional benefits of mulberry also did not occur. However, mulberry became more acceptable after a day of restriction to a single food type other than mulberry, and even deterrent and nutritionally worthless alternatives such as filter paper became acceptable after a day on any one food type. A tendency to feed on novel food types may be a proximate mechanism for the incorporation of relatively unpalatable, but nutritionally valuable foods into the diet. Novelty and the apparent need for diversity of foods are discussed in the context of exploratory foraging behavior by generalist herbivores.     

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.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

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.     

An analysis of avoidance generalization and food preference transitivity in goldfish,Carassius auratus

To examine the effect of novelty in food selection by fishes, goldfish were trained by feeding them on red or green food pellets. Individual fish and fish in shoals of two, three, and five were then given a choice between equal numbers of familiar pellets and novel (yellow) pellets. In experimental groups, the yellow pellets were soaked in 15% quinine hydrochloride to make them unpalatable. Fish were next presented with equal numbers of familiar and a second novel pellet. It was expected that fish would generalize from their experience with the unpalatable pellets and demonstrate avoidance to sampling a second novel food item. However, as groups, neither controls nor experimentals were reluctant to sample the second novel pellets. Also, fish did not eat significantly more familiar than novel pellets when both were palatable. A third set of experiments examined food preference transitivity in which each pellet type was presented alone and in three pair-wise combinations to individual fish. Although red and yellow pellets were preferred over green, they were preferred equally, indicating an absence of transitivity in pellet choice and, perhaps, a “preference” for a mixture of red and yellow pellets.     

Foliage acceptability to browsing ruminants in relation to seasonal changes in the leaf chemistry of woody plants in a South African savanna

Summary We investigated seasonal changes in food selection by hand-reared kudus and impalas in savanna vegetation in northern Transvaal, South Africa. The acceptability of the leaves of woody plants to these animals was compared with leaf concentrations of nutrients, fibre components and old leaf phenophases. No consistently significant correlation was found between acceptability and any single chemical factor. Based on an a priori palatability classification, discriminant function analysis separated relatively palatable species from unpalatable species in terms of a linear combination of protein and condensed tannin concentrations. The high acceptability of certain otherwise unpalatable species during the new leaf phenophase was related to elevation of protein levels relative to condensed tannin contents. Species were added to the diet during the dry season approximately in the order of their relative protein-condensed tannin difference.     

Cross-generic Food Sharing in Tamarins

Adult-infant food-sharing behavior is a major component of the infant care strategies of callitrichids (marmosets and tamarins). It is particularly well-developed in cotton-top tamarins (Saguinus Oedipus) and lion tamarins (Leontopithecus spp), which show frequent adult-initiated food offering, as well as sharing of food in response to begging by infants. This report documents a case of cross-generic food sharing, in which a male golden-headed lion tamarin (Leontopithecus chrysomelas) shared food with an infant cotton-top tamarin. The lion tamarin provided more food to the infant than its mother did. This emphasizes the importance of this behavior in the reproductive strategies of the communally-rearing Callitrichidae and raises questions about mechanisms that underly it.