Species divergence in offspring begging intensity: difference in need or manipulation of parents?

Conflicts over the delivery and sharing of food among family members are expected to lead to evolution of exaggerated offspring begging for food. Coevolution between offspring begging intensity and parent response depends on the genetic architecture of the traits involved. Given a genetic correlation between offspring begging intensity and parental response, there may be fast and arbitrary divergence in these behaviours between populations. However, there is limited knowledge about the genetic basis of offspring solicitation and parental response and whether these traits are genetically correlated. In this study, we performed a partial cross-fostering experiment of young between pied and collared flycatchers (Ficedula hypoleuca and Ficedula albicollis) and recorded the behaviour of individual offspring and their (foster)parents. We found that nestling collared flycatchers reached a higher phenotypic quality, estimated both as mass at fledging and as intensity of their T-lymphocyte-mediated immune response when raised by heterospecific foster parents. However, although collared flycatchers begged relatively more intensively, we found no evidence of corresponding higher resistance (i.e. lower feeding rate) of adult collared flycatchers than of adult pied flycatchers. Thus, the difference in offspring begging intensity between the two species seems not to be a result of a difference in escalation of the parent-offspring conflict. Instead, the species' divergence in exaggeration of offspring begging intensity 'honestly' matches a difference between the species in offspring need. This interpretation is strengthened by the fact that the difference in begging intensity between the two species increased as the season progressed, coinciding with the higher sensitivity of nestling collared flycatchers to the seasonal decline in food availability. Thus, the behavioural differentiation appears to be a direct consequence of a life-history differentiation (offspring growth patterns).     

A preliminary study on the function of food begging in Sichuan snub-nosed monkeys (Rhinopithecus roxellana): challenge to begging for nutritional gain

Several hypotheses have been developed to explain what benefits a donor may gain from sharing food with another individual, with nutritional gain assumed to be the sole benefit for the beggar. Recently, it has been proposed that begging behaviour serves a social function in non-human primates. In this study, the nutritional-gain assumption was again challenged based on observations on a captive group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana), or golden snub-nosed monkeys. The major findings from this study are that (1) beggars sometimes left their own branches or passed by available branches to beg for similar food from other individuals, (2) beggars occasionally ignored branches that were acquired by begging and (3) food begging occurred more frequently in the all-male unit after the social rank had changed between 2 individuals in this unit. Overall, these preliminary findings suggest that some begging behaviours in captive golden snub-nosed monkeys were not driven by nutritional gain only; instead, we propose that these begging behaviours could be interpreted as attempts at deriving social benefits.     

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 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.     

Trophallaxis in forager honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): resource uncertainty enhances begging contacts?

Trophallaxis among adult worker honeybees is the transfer of liquid food by mouth from one individual to another. Within the colony, nectar foragers perform offering contacts (as food-donors) to transfer the contents of their crops to recipient nest-mates and, in addition, they also perform begging contacts (as food-receivers). The biological relevance of these last interactions remains unknown. Previous evidence suggests that begging may be involved in the exchange of information on food resources that occurs naturally between employed foragers and nest-mates. This work was aimed to reveal possible connections between the information obtained while foraging and the begging behavior displayed inside the nest. Experiments were intended to (1) analyze whether chemosensory information obtained while foraging, i.e., odors and sucrose concentrations, affects begging behavior, and (2) determine whether resource uncertainty enhances begging contacts. Results showed that: (1) most begging contacts lasted less than 1 s, a duration which only allows receiving food samples from nest-mates; (2) the diversity of odors and sucrose concentrations at the feeding place enhances the occurrence of begging contacts; and (3) an increased resource uncertainty enhances the forager begging behavior. In addition, results suggest that foragers may direct their begging contacts frequently to other employed nectar foragers.     

HERITABILITY OF NESTLING BEGGING INTENSITY IN THE HOUSE SPARROW (PASSER DOMESTICUS)

Evolutionary theory of parent–offspring conflict assumes that offspring food solicitation behavior, known as begging, and parental response to begging are subjected to selection and coevolution. This assumption implies that begging intensity should be heritable, at least to some degree. Although some studies have suggested that begging is heritable, the evidence for this is rare and mostly indirect. To assess the heritability of begging we used artificial selection, sibling analysis, and the monitoring of begging intensity in four generations of cross-fostered captive house sparrow nestlings. We also contrasted the heritability of begging with that of morphological traits, known to be heritable in this species. Our results show that adult wing length and body mass were heritable as expected. The heritability estimates of the visual and vocal components of nestling begging (standardized for food deprivation and body mass) were low to moderate, as expected for behavioral traits in general, and lower than previously reported for passerine birds. Our sibling analysis shows that common environment had much greater effect on begging than genetic origin, suggesting that begging evolution may be strongly influenced by gene–environment interaction, probably through the mechanisms that adjust begging response to environmental and social conditions.     

Not for Parents Only: Begging Calls Allow Nest‐Mate Discrimination in Juvenile Zebra Finches

The benefits of recognition of family members may range from inbreeding avoidance to cooperative and coordinated behaviors within the family group. In birds, recognition of family members has almost exclusively been studied between parents and offspring or within cooperatively breeding societies. Yet, recognition of nest‐mates could be of special importance in recently fledged birds of colonial species by helping in locating the nest, maintaining family group cohesion, or allowing detection of feeding opportunities by recognizing the begging calls nest‐mates produced on the return of a parent. Here we study nest‐mate discrimination based on begging calls in fledglings of domesticated zebra finches (Taeniopygia guttata), a gregarious songbird living in loose colonies in which juveniles may gather in crèches and are fed by parents up to 20 d after fledging. Using playback tests, we show that fledglings called more and spent more time near the loudspeaker in response to the begging calls of their nest‐mates than to the calls of other familiar individuals. Because each fledgling was exposed to the repeated association of the begging calls of its nest‐mates and the subsequent feeding of its parents, this preferential response to the nest‐mates' calls could be a conditioned response to the food reward. Whereas fledglings answered more to male fledgling calls than to female fledgling calls, response to playback was influenced neither by the sex of the subject nor by its brood size. Discriminant function analysis based on acoustic parameters showed that begging calls carried an individual signature as well as a brood signature which might account for such nest‐mate discrimination. Begging signals are major study systems of the evolution of communication in the face of conflicts of interest between signalers and receivers. Our results suggest that eavesdropping and communication networks may be other informative frameworks to understand the design of offspring solicitation signals.     

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.     

Maintenance of Multifemale Social Organization in a Group of <Emphasis Type="Italic">Nomascus concolor</Emphasis> at Wuliang Mountain,Yunnan, China

Many short-term studies have reported groups of black crested gibbons containing ≥2 adult females (Nomascus concolor). We report the stability of multifemale groups in this species over a period of 6 yr. Our focal group and 2 neighboring groups included 2 breeding females between March 2003 and June 2009. We also habituated 1 multifemale group to observers and present detailed information concerning their social relationships over a 9-mo observation period. We investigated interindividual distances and agonistic behavior among the 5 group members. The spatial relationship between the 3 adult members (1 male, 2 females) formed an equilateral triangle. A subadult male was peripheral to the focal group, while a juvenile male maintained a closer spatial relationship with the adult members. We observed little agonistic behavior among the adult members. The close spatial relationship and lack of high rates of agonistic behavior among females suggest that the benefits of living in a multifemale group were equal to or greater than the costs for both females, given their ecological and social circumstances. The focal group occupied a large home range that was likely to provide sufficient food sources for the 2 females and their offspring. Between March 2003 and June 2009, 1 adult female gave 2 births and the other one gave 1 birth. All individuals in the focal group survived to June 2009. A long-term comparative study focused on females living in multifemale groups and females living in pair-living groups would provide insight into understanding the evolutionary mechanisms of the social system in gibbons.     

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.     

Social integration of a bonobo mother and her dependent daughter into an unfamiliar group

In the present study, we obtained quantitative behavioral data on the integration process of an adult female with her dependent daughter into a resident zoo population of six bonobos (Pan paniscus). During the whole observation time of almost two months, the integration happened very peacefully without significant increases of aggressive or agonistic tendencies. The integration was mediated and actively supported mainly by two processes: contacts of resident infants and juveniles towards the immigrating animals and contacts of the immigrating adult female to a “specific senior female” of the resident group. Adult males and adolescent females seemed not to play a role in the social integration of new group members. The new adult female soon became a preferred partner for sexual interactions such as genito-genital rubbing. The social integration of the 18-month-old young was controlled by her mother and finished only after the adult female had reached a stable and safe position in the new group. According to our observations, the exchange of an adult female bonobo including her young between zoos has no negative effects on the animals involved.     

Food restricted Tufted Puffin (Fratercula cirrhata) nestlings increase vocal activity during handling without modulating total or free corticosterone

In some species, corticosterone (CORT) appears to play a role in the control of begging behavior. Because of the potentially high costs associated with chronic elevation of CORT, it has also been proposed as a mechanism to ensure begging is an honest signal. We determined the effects of moderate food restriction (50% of high calorie treatment) on vocal behavior during handling, and on baseline levels of both total and ‘free’ unbound CORT in Tufted Puffin (Fratercula cirrhata) nestlings. Chick vocalizations during handling were similar to begging calls, and we assumed they were representative of begging behavior. We also measured total and free CORT in free-living Tufted Puffin chicks to determine if hormone levels in our experiment were comparable to natural levels. We found no effect of caloric restriction on either total or free baseline CORT, yet food-restricted nestlings vocalized more intensely during handling than chicks in the high calorie group. Mean plasma concentrations of total and free CORT in experimentally manipulated birds did not differ from levels in free-living nestlings. These results suggest that CORT does not play a role in modulating begging behavior in this species.     

Features of begging calls reveal general condition and need of food of barn swallow (Hirundo rustica) nestlings

Altricial offspring of birds solicit food provisioning by complexbegging displays, implying acoustic and visual signals. Differentcomponents of begging behavior may function as reliable signalsof offspring state and thus reproductive value, on which parentsbase optimal parental decisions about allocation of criticalresources (e.g., food). We experimentally manipulated componentsof general condition of nestling barn swallows (Hirundo rustica)by (1) altering brood size by cross-fostering an unbalanced number of nestlings between pairs of synchronous broods andthus manipulating the level of within-brood competition forfood, (2) injecting some nestlings with a harmless immunogen,simulating an infection, and (3) preventing part of the nestlingsfrom receiving food for a short period while establishing controlgroups. We recorded rate of begging response by individual nestlings as parents visited the nest and recorded begging calls usinga DAT recorder to analyze six sonagraphic features of vocalizations.Our factorial experiment revealed that nestlings deprived offood begged more frequently when parents visited the nest comparedto their non—food-deprived nest mates. Food deprivationincreased duration of syllables forming begging calls, whereas brood size enlargement resulted in increased latency of responseto parental calls. Heavy nestlings in good body condition vocalizedat a relatively low peak frequency. To our knowledge, thisis the first study in which begging rate and sonagraphic structureof begging calls are shown to reliably reveal a diverse setof components of offspring general state, on which parental decisions may be based.     

Social patterns of food sharing in monogamous owl monkeys

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

Flexible social structure of a desert rodent, Rhombomys opimus: philopatry, kinship, and ecological constraints

We tested hypotheses based on philopatry, kinship, and ecologicalconstraints to explain sociality in a semifossorial desert rodent,the great gerbil, Rhombomys opimus. Data were collected in thefield in Uzbekistan in the spring and fall of 1996 and 1998–2004.Population densities fluctuated dramatically with high turnoverin both males and females to reveal that dispersal and socialstructure were density dependent. Fewer gerbils dispersed athigher densities and members of family groups dispersed together.A majority of females lived in groups at high densities, butas population densities declined, proportionally more femaleswere solitary. DNA analysis revealed that group-living femaleswere genetically similar, whereas solitary females visited bythe same male, as well as adult males and females in the samefamily group, were usually not genetically similar. Reproductivesuccess as measured by the number of emergent pups and survivalof juveniles during the summer drought was not related to groupsize or whether females were philopatric. A majority of femalesin family groups reproduced, and all females engaged in cooperativebehaviors. We accepted three hypotheses to explain fluctuationsin group formation in the great gerbil: variation in food abundanceand distribution, habitat saturation, and kinship. We concludethat great gerbils are facultatively social. Flexible socialbehavior may be adaptive in unpredictable desert conditions.Females live solitarily under conditions of limited food andhigh mortality that disrupt social behavior and group formationand share territories with female kin under favorable conditionsfor survival and reproduction when kin groups can be maintained.Males adjust to the distribution of females.     

An observation of between-mates feeding behaviour in chick-guarding chinstrap penguins

Courtship feeding has not been reported for chinstrap penguins (Pygoscelis antarctica). However, we observed a male chinstrap penguin fed to his mate during the guard stage of chick. After being fed, the female regurgitated the food to her chick. Our observation suggests that the chicks’ behaviour of begging for food may be retained in adults, but it is usually restrained.     

Biology of <Emphasis Type="Italic">Cheirogaleus major</Emphasis> in a Littoral Rain Forest in Southeast Madagascar

Greater dwarf lemurs (Cheirogaleus major) are small nocturnal primates from the rain forests of eastern Madagascar. I investigated a population of Cheirogaleus major in a littoral rain forest of Southeast Madagascar during 2 rainy seasons to supplement the sparse information available for the species. I collected data on morphology, group composition, sleeping behavior, home range, and social organization via mark/recapture, radio telemetry, and focal individual observations. I identified 2 presumed family groups, and my data from radiotracking revealed a monogamous social organization. In each group, I found an adult pair and its presumed offspring sharing home ranges and sleeping sites together. I also observed gregarious behavior of group members during their nocturnal activity. I found no difference in body measurements between sexes, but body mass and tail circumference increased significantly from November to February, indicating a fatting period before hibernating.     

Social behaviour and infant carrying in a group of moustached tamarins,Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla,Peruvian Amazonia

The social behaviour of a group of eight moustached tamarins,Saguinus mystax, (five males, three females) was studied on Padre Isla in northeastern Peru. About 60% of all allogrooming was done by the two adult males in the group, and about 11% by a young adult female. All other group members groomed very little. The adult breeding female received more grooming than any other group member. After the death of the adult female (preyed upon by an anaconda) the amount of active allogrooming remained constant for all group members except for the young adult female, who increased her contribution to about 30%. Her preferred grooming partner was the subadult female, which generally screamed when being groomed by the young adult female and terminated grooming by going away. This kind of grooming relation is termed “forced grooming” and is interpreted as a possible social control mechanism. The young adult female groomed the adult males more often after the death of the adult female than before. This might have had the function of strengthening the social bond with the adult males and in obtaining the breeding position in the group. After the death of the adult female, the vulva of the young adult female grew to full adult size. Agonistic behaviour was less frequent than allogrooming. Most aggressive interactions (50%) originated from the subadult male of the group. The young adult female was the target of most of these aggressions. Extremely little aggression occurred between the three females. The young adult female was the only individual who tried to emigrate from the group during the study period. Her attempt to join a neighbour group failed due to rejection by all four members of this group. All group members participated in carrying an infant, but the adult males and the young adult female carried most frequently. Contribution to infant carrying varied with the infant's age.     

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.     

Families on the spot: sexual signals influence parent–offspring interactions

In 1950, Tinbergen described the elicitation of offspring begging by the red spot on the bill of parent gulls, and this became a model system for behavioural studies. Current knowledge on colour traits suggests they can act as sexual signals revealing individual quality. However, sexual signals have never been studied simultaneously in relationship to parent–offspring and sexual conflicts. We manipulated the red-spot size in one member of yellow-legged gull pairs and observed their partners'' feeding efforts in relationship to offspring begging. In the enlarged-spot group, partners doubled their effort compared with the other groups. Furthermore, in the reduced-spot group, partners provided food in relationship to offspring begging, contrasting with the fixed effort of the partners of enlarged-spot gulls. Manipulated gulls, independently of treatment, provided food in relationship to chicks begging only when the partner''s investment was low, and performed a fixed effort when the partner''s contribution was high. Results demonstrate that the red spot in yellow-legged gulls functions as a sexual signal and indicate that parental rules are plastic, depending on the information on offer. Previous evidence and this study indicate that this signal is used by all family members to adjust decision rules. The incorporation of sexual signals in parent–offspring interactions can be crucial in understanding intra-familial conflicts.