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.     

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.     

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.     

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.     

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.     

Signalling of Nutritional Need by Magpie Nestlings

The relationship between begging behaviour, chick nutritional state, and parental distribution of food within broods was studied in 4- and 5-chick magpie Pica pica broods under natural conditions. Three components of the begging display (duration, latency, and posture) were highly correlated with each other and also with the emission and duration of begging calls. Begging performance was strongly influenced by the food intake of nestlings during the preceding 1-h interval, indicating that begging may reliably reflect the nutritional need of nestlings. Daily growth during the preceding day, as well as average cumulative food intake by the brood during the preceding 24 h, seemed not to affect begging in a similar way. Begging signals employed by hungrier nestlings involved a higher degree of muscular activity, thus supporting the prediction that nestlings in greater need should employ more costly signals. Overall, those nestlings who begged more tended to obtain more food, but the relationship between feeding success and begging behaviour was weak due to a high variation between broods in the way that parents seemed to respond to variations in begging behaviour. Possible causes for this variation, and its implications for the evolution of reliable begging displays, are discussed.     

Begging in the absence of parents by nestling tree swallows

Begging by nestling passerine birds has become a model systemfor studies in animal communication. Although most beggingoccurs when parents arrive at the nest to feed (here called"primary begging"), it also occurs between feeding visits andimmediately after parents leave the nest. Begging in thesecontexts (here called "secondary begging") may have relativelylittle influence on the probability of receiving food, but could increase the overall cost of the signal and thus influence nestlingbegging strategies. The purpose of our study was to determinehow often tree swallow (Tachycineta bicolor) nestlings begin contexts other than to parents with food and to examinewhat factors influence the frequency of this begging. Secondarybegging ranged from 7% of measured begging responses at day2 to 30% by day 8 and was more frequent when the interval betweenparental feeding visits was relatively long and when the timeto respond to the arrival of parents with food was short. Increasesin both age and intervisit interval were associated with decreasesin nestling response times, suggesting that secondary beggingmay be related to the speed with which nestlings respond to stimuli. We discuss possible functions of secondary beggingand raise the possibility that it may, in fact, be an error.     

Factors Affecting Vocalization in Tengmalm’s Owl (Aegolius funereus) Fledglings during Post-Fledging Dependence Period: Scramble Competition or Honest Signalling of Need?

Begging behaviour of nestlings has been intensively studied for several decades as a key component of parent-offspring conflict. There are essentially two main theories to account for intensity of food solicitation among offspring: that intensity of begging is related to some form of scramble competition between nest mates or that it offers honest signalling of need to parents. The vast majority of studies which have addressed begging behaviour have been based on observations of, and experiments on, nestlings and have not considered begging behaviour, during the post-fledging period. Begging vocalizations in this post-fledging phase of dependence have rarely been studied, despite the importance of vocalizations as a communication method between offspring and parents, particularly for nocturnal species. We radiotracked 39 fledglings of the Tengmalm’s owl (Aegolius funereus) in two years with different availability of prey: 2010 (n = 29 fledglings) and 2011 (n = 10 fledglings) and made 1320 nightly localizations in which we recorded presence or absence of begging calls. Within years, the most important measures related to the probability of vocalization were body condition at fledging, time of night, number of surviving siblings, age and weather conditions. Begging intensity increased with age in both years; however, in the year with low prey availability fledglings vocalized significantly more often. The main factor causing these differences between years was probably the different availability of prey, affecting breeding success, post-fledging behaviour, and thus also both short- and long-term needs of offspring. We believe that our results suggest honest signalling of their fledgling’s need.     

Condition-dependent effects of corticosterone on a carotenoid-based begging signal in house sparrows

Begging is a complex display involving a variety of different visual and auditory signals. Parents are thought to use these signals to adjust their investment in food provisioning. The mechanisms that ensure the honesty of begging displays as indicators of need have been recently investigated. It has been shown that levels of corticosterone (Cort), the hormone released during the stress response, increase during food shortage and are associated with an increased begging rate. In a recent study in house sparrows, although exogenous Cort increased begging rate, parents did not accordingly adjust their provisioning rate. Here, we tested the hypothesis that Cort might affect the expression of other components of begging displays, such as flange color (a carotenoid-based trait). We experimentally increased levels of circulating Cort and investigated the effects of the treatment on (1) the flange coloration of the nestlings, (2) the behavioral response and (3) the parental allocation of food and (4) nestling condition and cell-mediated immune response. We found that Cort affected flange coloration in a condition-dependent way. Cort-injected nestlings had less yellow flanges than controls only when in poor body condition. Parental feeding rate was also affected by the Cort treatment in interaction with flange color. Feeding rate of Cort-injected nestlings was negatively and significantly correlated with flange color (nestlings with yellower flanges receiving more food), whereas feeding rate and flange color were not correlated in control chicks. We also found that nestlings injected with Cort showed a weaker immune response than controls. These results suggest that, indeed, Cort has the potential to affect multiple components of the begging display. As Cort levels naturally raise during fasting, parents have to take into account these multiple components to take a decision as to optimally share their investment among competing nestlings.     

Post-migratory care of young by Crab Plovers Dromas ardeola

The Crab Plover Dromas ardeola is the only waterbird species known to provision offspring well after the post-reproductive migration and through overwintering. A few previous quantitative studies have reported inconclusively that juveniles begged rarely, and also indiscriminately at other juveniles. Here, we describe the feeding behaviour of adult and juvenile Crab Plovers during the first part of the wintering period. Juveniles begged frequently for food, always toward adults, and obtained 0.1 prey items/min from them. Begging birds obtained the largest prey items of those captured by the adults. When foraging alone, juveniles captured prey at the same rate as adults, but captured smaller crabs. The feeding success of adults was not altered by the presence of the begging juvenile. Juveniles depended partly on adults during the first part of the overwintering period, but were almost independent towards the end. Crab Plovers may adopt such unusually prolonged care because they need to abandon their breeding areas quickly, when environmental conditions are extreme. Large numbers of Crab Plovers overwinter in a few areas, now subject to human alteration. Isolated adults may forage on other areas such as narrow and disturbed shores, but juveniles may require wide beaches, suitable for group foraging, that should be considered as key areas for the recruitment of juveniles into the population.     

Coadaptation of Offspring Begging and Parental Provisioning - An Evolutionary Ecological Perspective on Avian Family Life

Offspring begging and parental provisioning are the two central social behaviours expressed during the period of parental care. Both behaviours influence each other and it is, therefore, hypothesized that they should ultimately become (genetically) correlated, stabilized by fitness costs to parents and/or offspring. By reciprocally exchanging entire clutches in canaries (Serinus canaria), we tested (1) whether there is covariation between these behaviours and (2) whether a mismatch - as introduced by cross-fostering - entails costs. Begging was scored in a standardized begging test and parental provisioning was measured via (a) the actual feeding rate and (b) using the growth rate of the foster nestlings as a proxy. Costs were established in terms of future reproductive investment in subsequent clutches and offspring growth. We found a positive and significant phenotypic covariation between offspring begging and parental feeding when using the growth rate as a proxy and, to a lesser extent, in case of the parental feeding rate. Female parents suffered no future reproductive costs when feeding foster nestlings that were more demanding than their own nestlings. Neither growth measured amongst all offspring nor the reproductive investment measured amongst the female offspring as adults was influenced by their begging behaviour. However, the reproductive investment of female offspring tended to depend on the parental qualities of their foster parents. Thus, offspring may only be able to extract resources within the limit of generosity of their foster parents. This suggests parental control of feeding, which is also supported by the positive covariation between offspring begging and parental feeding.     

Blackcap Sylvia atricapilla nestlings do not produce begging calls until they are able to escape from predators

Nest predation is a major source of reproductive failure in birds and thus it can exert selection on both parental and offspring strategies. Begging calls are known to be a powerful component of parent–offspring communication but these calls can also increase predation risk. Here we demonstrate a sophisticated strategy for the development of begging vocalization in a species under high nest predation. Blackcap Sylvia atricapilla nestlings spend most of their nesting period silent, and develop begging calls just before they are able to fledge. The onset of begging vocalization matches the onset of endothermy, which enables Blackcap chicks to leave the nest. We demonstrate experimentally that begging calls function as a signal of the increased needs of homeothermic nestlings. Playback of begging calls conducted in nests with silent nestlings resulted in a significant increase in feeding rates and a decrease in brooding. Development of begging calls only at the age of endothermy allows species under high nest predation to keep the risky period of begging vocalizations and frequent feeding to a minimum. This strategy may constitute an evolutionary solution to high predation pressure in some open nesting passerines. This is the first study to demonstrate the existence of silent begging in a passerine.     

Individual benefits of nestling begging: experimental evidence for an immediate effect, but no evidence for a delayed effect

The evolutionary stability of honest signalling by offspring is thought to require that begging displays be costly, so the costs and benefits of begging--and whether they are experienced individually or by the whole brood--are crucial to understanding the evolution of begging behaviour. Begging is known to have immediate individual benefits (parents distribute more food to intensely begging individuals) and delayed brood benefits (parents increase provisioning rate to the brood), but the possibility of delayed individual benefits (previous begging affects the current distribution of food) has rarely, if ever, been researched. We did this using playback of great tit Parus major chick begging and a control sound from either side of the nest. Male parents fed chicks close to the speaker more when great tit chick begging, but not other stimuli, was played back. In contrast, there was no effect of playback at the previous visit on the chicks that male parents fed. We have thus demonstrated an immediate individual benefit to begging, but found no evidence of a delayed individual benefit in this species.     

Sex differences in responsiveness to begging in a cooperative mammal

In species where young are provisioned by both parents, males commonly contribute less to parental care than females, and are less responsive to variation in begging rates. Similar differences in the care of young occur among adults in cooperative breeders, but fewer studies have investigated whether these are associated with differences in responsiveness. Here, we present results from a playback experiment investigating responsiveness to begging in the meerkat (Suricata suricatta), a cooperatively breeding mammal. Although increased begging rate raised the feeding rate of adults of both sexes, there was no consistent tendency for females to be more responsive than males. However, when we examined changes in the proportion of food items found that were fed to pups (generosity), we found that females were more responsive than males to increased begging rate. These results can be explained in terms of sex differences in dispersal: in meerkats, females are philopatric and receive considerable benefits from investing in young, both directly, by increasing group size, and indirectly, by recruiting helpers if they inherit the breeding position. In addition, they emphasize that generosity provides a more sensitive measure of responsiveness to begging than feeding rate, as it accounts for variation in foraging success.     

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.     

Begging in Common Redstart Nestlings: Scramble Competition or Signalling of Need?

Begging behaviour by the young affects parental food distribution among nestlings of altricial birds. We present an analysis of two types of begging behaviour (assuming the front nest positions and gaping) based on videotaped natural nestling feeding in European common redstart (Phoenicurus phoenicurus). We test whether these types of begging support the predictions of two mathematical models: scramble competition with competitive asymmetries between nestlings [Anim. Behav. 27 (1979) 1210] or honest signalling model [Nature 352 (1991) 328]. None of the measured variables of nestling or parental behaviour were affected by body weight differences between siblings. In contrast, both gaping and nest positioning were affected by individual differences in nestling hunger. In agreement with the honest signalling model, hungrier nestlings gaped with higher probability and started to gape sooner after the arrival of the parent than did their less hungry nestmates. Those nestlings with the shortest latency to gape also received food more often. Nest positioning was related to nestling hunger in a way unforeseen by the existing models. The intervals between nestling position changes were several times longer than the intervals between parental feeding visits, and parents preferred to feed nestlings in front positions, so nestlings in front positions were always less hungry than nestlings in back. Hence the pattern of movements influenced the feeding decision in favour of the more satiated nestlings and acted against the effect of gaping. Nestling movement seemed to be caused by the less hungry nestlings moving actively from front to rear positions. Low mortality of individual nestlings within broods that survived to fledging and small within‐brood variation in fledging weights indicated low competition among nestmates. We suggest that there are two behavioural mechanisms that contribute to the equalization of fledging weights in common redstart nestlings: the signalling of need through gaping and the regular turnover of nestlings at front positions.     

Sibling competition and siblicide in asynchronously-hatching broods of the cattle egret Bubulcus ibis

Feeding behaviour and sibling competition were observed in nine families of the cattle egret (Bubulcus ibis) from blinds during 1359 nest-h throughout the nestling period. During days 0–19, size differences among siblings were clear; begging behaviour of chicks changed with time. At least one parent always attended the nest. Food boluses regurgitated early within a feeding period were received by senior chicks more often than by juniors. When any two siblings begged for food at the same time, the elder and younger received the first bolus on 65% and 35% of occasions respectively. Between days 20 and 39, the frequency of begging reached a peak. Begging behaviour became intense and stereotyped. The number of boluses received per begging declined rapidly, especially for junior chicks. In large broods, the success rate of begging was lower and fights occurred among siblings, especially among juniors. Out of 256 dyadic fights, the elder sibling won 85, lost one, and tied 171. The youngest chick died in two broods, apparently as the result of these fights (siblicide). No parents interfered in fights among their offspring. After day 40, the frequency of begging decreased gradually and ceased by day 80, No chicks died in the last period, although the frequency of fights in all large broods remained high.     

Why brown-headed cowbirds do not influence red-winged blackbird parent behaviour

Brown-headed cowbirds, Molothrus ater, frequently parasitize red-winged blackbirds,Agelaius phoeniceus . The presence of a brood parasite, unrelated to both host nestlings and parents, has provoked speculation regarding within-brood food allocation and parental provisioning. This study is the first to compare directly the effect of brood parasitism on host parent and offspring behaviour in younger and older broods. We videotaped 28 unparasitized red-winged blackbird broods and compared them to 22 parasitized broods. Red-winged blackbird nestling begging appears largely unaffected by cowbird parasitism. The presence of the cowbird in the nest affected neither the latency nor duration of host nestling begging, but stimulated more frequent begging by red-winged blackbird nestlings following food distribution. Begging by cowbirds was unique in two ways: (1) cowbirds maintained a consistent begging effort throughout the nestling period (but did not receive a consistent food share); and (2) cowbirds begged longer and more frequently following the allocation of food. Persistent begging by the cowbird following the allocation of food has implications for the division of parental care, if by doing so the brood parasite is able to provoke the foster parent to increase provisioning, at the expense of brooding. We found no evidence for the adjustment of parental care. Neither the foraging rates nor the lengths of the parental feeding visits differed markedly between parasitized and unparasitized broods. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake

Parent black-legged kittiwakes (Rissa tridactyla) and their dependent chicks respond to food shortages by increasing circulatinglevels of corticosterone. To examine the behavioral significanceof corticosterone release, we experimentally increased levelsof circulating corticosterone in parents and chicks up to thelevels observed during food shortages. We found that corticosterone-implantedchicks begged more frequently than sham-implanted controls.Corticosterone-implanted chicks in broods of two begged morefrequently than singletons. Parent kittiwakes then respondedto the increase in corticosterone levels in their chicks byincreasing chick-feeding rates. However, feeding rates werenot different among corticosterone-implanted chicks in broodsof two and singletons. We also found that corticosterone-implantedparents spent more time away from the nest—perhaps foraging—andless time brooding/guarding chicks than sham-implanted controls.Untreated mates of the corticosterone-implanted bird did notcompensate for the change in their partner's behavior; consequently, chicks were left unattended about 20% of the time compared to1% at the control nests. However, corticosterone-implantedparents did not decrease their chick-feeding rates. Our findingssuggest two functional implications of the increased corticosteronesecretion during food shortages in the black-legged kittiwake:it facilitates begging in chicks, and it affects time allocatedby parents to guarding young at the nest. Thus, release of corticosterone might provide a mechanistic link between physiological condition and behavioral interactions among adults and theiryoung.