Tutoring in Wild Golden Lion Tamarins

Among most nonhuman primates, juveniles must acquire most of their solid food independently. Information gleaned from adults results from efforts initiated by the juveniles. Donation of food or foraging information by adults to immatures is rare among apes and virtually unknown among monkeys. We report 3 observations in which wild adult golden lion tamarins appear to have directed their immature offspring to a location where a hidden prey item was located. According to the definition of Caro and Hauser (1992), the tamarins were tutoring their young.     

Food-Offering Calls in Wild Golden Lion Tamarins (<Emphasis Type="Italic">Leontopithecus rosalia</Emphasis>): Evidence for Teaching Behavior?

Many animals emit calls in the presence of food, but researchers do not always know the function of these calls. Evidence suggests that adult golden lion tamarins (Leontopithecus rosalia) use food-offering calls to teach juveniles which substrate (i.e., microhabitat) to forage on, or in, for food. However, we do not yet know whether juveniles learn from this aspect of the adults’ behavior. Here we examine whether juveniles learn to associate food-offering calls with a foraging substrate, as a step toward assessing whether these calls qualify as teaching behavior. We compared the performance of four wild juvenile golden lion tamarins that were introduced to a novel substrate while exposed to playbacks of food-offering calls (experimental condition) to the performance of three juveniles that were exposed to the novel substrate without the presence of food-offering playbacks (control condition). We varied the location of the novel substrate between trials. We found that food-offering calls had an immediate effect on juveniles’ interactions with the novel substrate, whether they inserted their hands into the substrate and their eating behavior, and a long-term effect on eating behavior at the substrate. The findings imply that juvenile golden lion tamarins can learn through food-offering calls about the availability of food at a substrate, which is consistent with (but does not prove) teaching in golden lion tamarins through stimulus enhancement. Our findings support the hypothesis that teaching might be more likely to evolve in cooperatively breeding species with complex ecological niches.     

Social influences on foraging behavior in young nonhuman primates: Learning what,where, and how to eat

Human infants rely on social interactions to acquire food‐related information. 1 , 2 Adults actively teach children about food through culturally diverse feeding practices. Characteristics we share with the other primates, such as complex diets, highly social lives, and extended juvenile periods, suggest that social learning may be important during ontogeny throughout the order. Although all young primates typically pay attention to feeding adults, great apes and callitrichids, in particular, acquire new foraging techniques through abilities unknown in other nonhuman primates; that is, they learn by imitation. However, ape social learning is almost exclusively infant‐initiated, while adult callitrichids actively teach their young. It is unlikely that the same selective forces have acted to favor sophisticated social‐learning mechanisms in both taxa. 3 , 4 Equipped with an ape brain, complex foraging methods, and a cooperative infant‐care system, early hominins were uniquely poised to take social learning about food and foraging techniques to a new level.     

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.     

Foraging Ontogeny is not Linked to Delayed Maturation in Squirrel Monkeys (Saimiri sciureus)

The acquisition of complex foraging behaviors by young is a proposed cause of a prolonged juvenile phase in many vertebrates, including primates. I compared the foraging behaviors of infant, juvenile and adult squirrel monkeys to determine if significant age‐related differences in foraging behavior and efficiency were present. Infants and juveniles differed from each other in patterns of prey and fruit foraging, but few differences existed between juveniles and adults. Despite differing in the use of foraging substrates, young juveniles (8–12 mo) were as efficient as older juveniles (1–4 yr) and adults at capturing and processing large prey. Young juveniles (<1 yr) were limited in their ability to consume husked palm fruits due to an inability to peel them to obtain pulp. By 1 yr of age, however, foraging behaviors of adults and juveniles were nearly indistinguishable. The absence of meaningful differences between adults and juvenile foraging is not consistent with the hypothesis that the need to develop foraging skills accounts for the pattern of extended juvenility in squirrel monkeys.     

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.     

Social contributions to the foraging behavior of young wild golden lion tamarins (Leontopithecus rosalia): Age-related changes and partner preferences

In cooperatively breeding species, group members other than the parents contribute to the care of the young. The costs and benefits to caregiving may vary with the type of care provided and with caregiver characteristics such as age, sex, reproductive status, and foraging ability. Here I examine the relative contributions of parents, helpers and same-aged twins to the foraging and feeding activities of the young in a longitudinal study of wild golden lion tamarins, specifically with regard to direct food transfer, tolerance for coforaging or cofeeding by immatures and signaling young as to the location of profitable prey-foraging sites. I found that the type of food-related assistance varied as a function of the age of the immature and among group members. Rates of food transfer steadily declined as immatures aged, while coforaging rates peaked when juveniles were in the middle age group. Mothers and fathers were the most generous in terms of providing food to begging young. Mothers most often directed juveniles to productive foraging sites, and female helpers never did. Older siblings did not vary caregiving effort according to sex or age. Adult and subadult foraging ability was not a strong predictor of the rates at which prey was given to the young or the rates at which caregivers tolerated coforaging by immatures on plant and prey resources. Thus, foraging ability did not appreciably influence generosity to or tolerance of the young.     

Disparity between Adult and Juvenile American Robins Turdus migratorius Foraging for Ground Invertebrates and Cherry Fruits

Although it has long been known that juveniles often have foraging skills inferior to those of adults, it has generally been assumed that animal prey are more difficult to capture than fruit, and thus that juveniles foraging on fruit should be similar to adults in their efficiency. To examine these ideas, we investigated the abilities of juvenile and adult American robins Turdus migratorius to forage for ground invertebrates and fruits of the black cherry tree Prunus serotina. We hypothesized that juveniles, lacking the experience of adults, would not have the skills of adults and therefore would be less proficient invertebrate and fruit foragers. Juveniles captured 69% of invertebrates at which they struck compared with 80% of adults’ strikes that ended in capture. However, juveniles made more strikes than adults, so mean prey capture per minute was the same. Juveniles were also less skilled fruit foragers. Juveniles were twice as likely as adults to fail to pick a cherry (55% of adults’ vs. 28% of juveniles’ attempts ended in success). However, there was no significant difference in the proportion of juveniles and adults that dropped a cherry once it was picked. As a result of their low levels of success, juveniles consumed about half the number of cherries per minute as did adults. Contrary to prior assumptions, skills involved in fruit foraging may not be so easily acquired and many omnivorous species, like the American robin, must learn both invertebrate and fruit foraging skills.     

Age and seasonal effects on predator-sensitive foraging in squirrel monkeys (Saimiri sciureus): a field experiment

A field experiment was conducted to examine the effect of perceived predation risk on the use of foraging areas by juvenile and adult primates under different conditions of local food abundance. Wild squirrel monkeys, Saimiri sciureus, were observed in an experiment conducted during the dry and the wet seasons at a site in Eastern Amazonia, Brazil. Animals were presented with feeding platforms that differed in food quantity and exposure to aerial predators through varying vegetative cover. In the dry season, juveniles and adults chose platforms based solely on food quantity. However, in the wet season, juveniles foraged preferentially on high-reward platforms only if cover level also was high (i.e., potentially offered greater concealment from predators). In contrast, adults showed the same pattern of platform use regardless of season. These results indicate that age and local resource availability based on seasonality affect whether primates forage in a predator-sensitive manner. Juveniles may be more sensitive to predation risk when foraging, and individuals may take fewer risks when resource abundance is high in their environment.     

Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest

The feeding ecology of two small-bodied primate species—saddle-back ( Saguinus fuscicollis auilapiresi ) and moustached tamarins ( S. mystax pileatus )—occurring in stable, mixed-species groups was studied in a terra firme forest site in the upper Urucu River, Amazonas, Brazil. Ecological data are based primarily on one mixed-species group of 5–8 saddle-back and 8–10 moustached tamarins. The overall vegetative and animal-prey components of each tamarin species' diet, their selection of food species, and the seasonal variation in their use of plant resources are described, and compared to those of callitrichids elsewhere. The extremely diverse diet of tamarins included at least 136 tree, 33 vine and liana, 12 epiphyte and nine shrub species, as well as a wide range of prey items. They fed primarily on ripe fruit pulp of most of these species for most of the year, but shifted to floral nectar and plant exudates of a few key plant species during the dry season. Taxonomic overlap in plant diet was nearly complete between the two tamarin species, but they diverged considerably in their prey capture techniques. Saddle-backs used the low forest understorey, and manipulatively searched for sedentary prey concealed within discrete, usually rigid, microhabitats, whereas moustached tamarins used the midstorey where they visually searched for mobile prey well exposed on foliage. These and other feeding and foraging patterns are discussed in the light of other callitrichid species studied to date.     

Provisioning in wild golden lion tamarins (Leontopithecus rosalia): benefits to omnivorous young

Provisioning may act to cushion weaned young from dietary insufficiencyand errors during the period in which they are mastering complexforaging techniques or learning to identify appropriate dietaryitems. That is, young mammals who receive food from others maygain nutritional and/or informational benefits. I conducteda longitudinal study of 13 wild golden lion tamarins 11–56weeks of age in six groups to evaluate hypotheses regardingthe functions of provisioning. All members belonging to thisprimate taxonomic family (the Callitrichidae) are cooperativebreeders and are known to provision their young more frequentlythan do other primate species, except humans. My results, togetherwith experimental findings, suggest that juveniles receive bothnutritional and informational benefits from being provisioned.My juvenile study subjects received animal prey (invertebratesand small vertebrates) from others more frequently than plantresources (fruits and hardened exudates). Apparently difficult-to-handlefruits were more likely to be transferred than readily processedfruits. These results support the nutritional benefits hypothesisbecause the young received items, particularly lipid- and protein-richprey, that they might not otherwise have acquired. That juvenilesfed independently on, and were provisioned with, the same fruitson the same day is counterevidence to the nutritional benefitshypothesis, however. The informational benefits hypothesis wassupported because juveniles received a large variety of foods(including more than 20% of fruit species eaten) and receiveduncommon fruits that were easily acquired. Adults emitted food-offeringcalls to encourage the transfer of prey to juveniles, particularlywhen the prey was whole and alive.     

Influence of environmental variables on foraging by juvenile American Robins

ABSTRACT.   Juvenile birds lack the experience of adults and, as a result, are typically less efficient foragers. Environmental factors can influence how birds forage and the outcome of foraging bouts, but few investigators have considered the effects of such factors on the foraging behavior of juveniles. We examined the effects of two environmental factors, sunlight and soil moisture, on the foraging behavior of juvenile and adult American Robins ( Turdus migratorius ). Both factors had a significant effect on robin foraging, with robins more effective at capturing arthropods in the sun and worms in moist soils. However, juveniles were less successful than adults across all conditions. Juveniles were less successful than adults at capturing arthropods and were less efficient at capturing worms. Juveniles captured an average of one worm per minute, whereas adults captured nearly two worms per minute. Additionally, the high failure rates of juveniles (0.44/min) as compared to adults (0.20/min) may be indicative of their inability to choose suitable prey items. Finally, we found that juveniles tended to forage with other robins more than did adults, suggesting that they may use other individuals as cues for locating favorable foraging sites.     

Seasonal Effects on Play Behavior in Immature <Emphasis Type="Italic">Saimiri sciureus</Emphasis> in Eastern Amazonia

Play behavior is prevalent among most mammalian young, particularly primates. Though several hypotheses address the function of play, researchers have documented information on the potential costs of play and of environmental effects on the occurrence of primate play less well during long-term field studies. I examine seasonal changes in play behavior of immature squirrel monkeys (Saimiri sciureus) across 4 age classes: infants, young juveniles, mid-juveniles, and late juveniles. I observed individuals during 12 mo in Eastern Brazilian Amazonia, an area characterized by highly seasonal rainfall. Play was strongly tied to seasonality, food availability, and changes in diet. The percentage of time spent playing was reduced in the dry season, a period characterized by low fruit availability and an increase in time spent foraging for prey. I suggest that the decrease in play behavior in the dry season is related both to a higher need for energy conservation and to increased time expended in foraging activities.     

Social influences on the acquisition of sex-typical foraging patterns by juveniles in a group of wild tufted capuchin monkeys (Cebus nigritus)

Foraging traditions in primates are becoming the subject of increasing debate. Recent evidence for such a phenomenon was recently provided for wild Cebus capucinus [Fragaszy & Perry, 2003]. To better understand the bases of animal traditions, one should examine intrapopulation behavioral variability and the influence of social context on within-group transmission of specific foraging patterns. We studied the variability of foraging patterns across age and sex classes, and the proximity patterns of juveniles to adults of both sexes in a group of wild tufted capuchin monkeys (Cebus nigritus) living in the Iguazu National Park, Argentina. Foraging activity was examined for a period of 9 months in terms of proportions of focal samples devoted to foraging on certain food targets, microhabitats, and supports, and using specific foraging patterns. Proximity analyses were performed to reveal patterns of association between juveniles and adults. Sex differences in foraging behavior were present and overrode age differences. Overall, males ate more animal foods, foraged more for invertebrates on woody microhabitats (especially large branches), palms, and epiphytes, and used lower and larger supports than females. Females ate more fruits, foraged more on leaves and bamboo microhabitats, and used smaller supports than males. Juveniles were similar to adults of the same sex in terms of food targets, foraging substrates, and choice of supports, but were less efficient than adults. Proximity patterns indicated that juvenile males stayed in close spatial association with adult males and preferentially focused their "food interest" on them. This phenomenon was less evident in juvenile females. The degree to which juveniles, especially males, showed some of the sex-typical foraging patterns correlated positively with their proximity to adults of the same sex. These findings suggest that the acquisition of foraging behaviors by juvenile males is socially biased by their closeness to adults of the same sex.     

Experimental analyses of patch selection by foraging black surfperch (Embiotoca jacksoni Agazzi)

The dynamics of microhabitat use by foraging adult and juvenile black surfperch (Embiotocajacksoni Agazzi) were explored. Detailed observations of black surfperch feeding at Santa Catalina Island, California, revealed that adults and young-of-year juveniles co-occurred in the same habitat but used different algal substrata as foraging sites. Juveniles selected invertebrate prey almost exclusively from the surface of foliose algae. The occurrence of young E. jacksoni was highly correlated with that of foliose algae. Adults tended to bite most frequently from turf, a low-growing matrix of plants, colonial animals, and debris covering the rocky substratum. The abundance of adults was negatively correlated with the occurrence of foliose algae. Adults and juveniles showed marked, but different, preferences in their utilization of taxa of algae as foraging substrata. Certain algae (e.g., Zonaria farlowii Setchell & Gardner) were preferred while other taxa (e.g., Sargassum palmeri Grun) were avoided by both age groups. However, most types of algae were preferred by one group but not the other. To test the hypothesis that knowledge of algal substratum composition allows prediction of fish occurrence and foraging behavior in a patch, algal cover on 2 × 2 m² areas of bottom was manipulated creating plots dominated by turf, Zonaria farlowii, or Sargassum palmeri. Fish occurrence could be accurately predicted on the basis of abundance of foliose algae, but foraging activity of fish was highly dependent on the algal taxon that dominated the patch. Differential prey availabilities among foraging substrata provided some insight into the patterns of foraging patch preferences displayed by adult and juvenile Embiotoca jacksoni.     

Antipredator vigilance of juvenile and adult thirteen-lined ground squirrels and the role of nutritional need

Juvenile thirteen-lined ground squirrels, Spermophilus tridecemlineatus, are less vigilant (i.e. they spend less time visually scanning the environment) than adults. To determine whether nutritional need was a potential cause of this difference, we supplemented two groups of free-ranging juveniles during the predispersal stage, while juveniles were still near and around the natal burrows. The high-energy food group (HEF: 11 squirrels) received peanut butter and oats while the low-energy food group (LEF: seven squirrels) received lettuce. Adults (14 squirrels) were also supplemented, but due to their greater home range sizes, it was not feasible to classify them as either HEF or LEF. To evaluate the effect of supplementation on antipredator vigilance, the behavioural act of visually scanning for predators, we videotaped individuals while they were foraging above ground during 5-min observation periods. Each squirrel was observed and weighed during three time periods over 23 days. From the videotape, we extracted measures of time spent vigilant, locomoting and foraging. All three categories of squirrels gained mass over the study period, but the HEF juveniles rapidly exceeded that of the LEF juveniles. Early in the study, LEF and HEF juveniles did not significantly differ in either body mass or time budgets, and, initially, both juvenile groups were similar to adults in the amount of time devoted to vigilance. Later in the study, the behaviour of HEF juveniles closely resembled that of adults (increased time devoted to vigilance and decreased time devoted to foraging), while LEF juveniles decreased vigilance and increased their foraging time. This study indicates that for thirteen-lined ground squirrels the lower vigilance of juveniles is due, at least in part, to the greater nutritional needs of young animals with consequent increases in foraging, which is largely incompatible with vigilance. Copyright 2000 The Association for the Study of Animal Behaviour.     

Ecological Risk Aversion and Foraging Behaviors of Juvenile Squirrel Monkeys (Saimiri sciureus)

The ‘ecological risk aversion hypothesis’ [C.H. Janson and C.P. van Schaik, Juvenile Primates, Oxford Univ. Press, New York (1993), pp. 57–74] proposes that the pattern of slow growth characteristic of juvenile primates is a response to ecological risks (predation and starvation) experienced by juveniles. Juveniles are thought to avoid predation risk by positioning themselves near conspecifics, therefore experiencing high levels of feeding competition with older individuals, reduced access to resources and, consequently, high starvation risks during periods of food scarcity. The present study compared the foraging behaviors of juvenile and adult squirrel monkeys, a small neotropical primate characterized by a long juvenile period, to determine how predation and starvation risks affected juvenile behaviors. The study was conducted in Eastern Amazonia, in a seasonal environment. Due to their slow development, small body size and large group sizes, it was expected that juveniles in this species would behave in a manner consistent with the risk aversion hypothesis. However, age differences in foraging efficiency and foraging success were smaller than predicted. There was also no evidence that juveniles sacrificed access to food for predator protection. Adults did not have preferential access to fruit patches and direct competition was rare. Feeding competition for prey, the most common resource in the troop's diet, was negligible. Therefore, the slow growth and long juvenile period of squirrel monkeys do not correspond with evidence of predation or starvation risk, as predicted by the risk aversion hypothesis.     

Maintenance of cotton-top tamarins fed an experimental pelleted diet versus a highly diverse sweetened diet

The future study of colon disease in captive callitrichid colonies may require manipulation of diets. The limited knowledge of the nutritional requirements for these species and the varied diets and supplementations fed to these animals in various colonies suggest the importance of testing the palatability and acceptability of diets for these primates. Individually housed cotton-top tamarins (Saguinus oedipus) were given either the regular Oak Ridge Associated Universities (ORAU) diet (monkey chow slurry, canned diet and supplements), a similar slurry using an experimental natural ingredient diet plus supplements, or the experimental diet without supplements. Neither dry food consumption, body weight, fecal output, nor the histological evaluation of the colons were affected by these diets. Daily intake of protein and calories were higher than previously reported estimates for the species. These results demonstrate that a natural ingredient non-sweetened pelleted diet is palatable for cotton-top tamarins for a period of 3.5 months, however, further testing over longer time periods is necessary. The nonnutritional (e.g. psychological) advantages of providing a highly diverse diet to primates housed in a relatively monotonous environment should be considered before adopting such a diet for an entire colony.     

Nest and foraging‐site selection in Yellowhammers Emberiza citrinella: implications for chick provisioning

Capsule Vegetation structure and invertebrate abundance interact to influence both foraging sites and nestling provisioning rate; when invertebrate availability is low, adults may take greater risks to provide food for their young.

Aims To investigate nesting and foraging ecology in a declining farmland bird whose fledging success is influenced by the availability of invertebrate prey suitable for feeding to offspring, and where perceived predation risk during foraging can be mediated by vegetation structure.

Methods Provisioning rates of adult Yellowhammers feeding nestlings were measured at nests on arable farmland. Foraging sites were compared with control sites of both the same and different microhabitats; provisioning rate was related to habitat features of foraging‐sites.

Results Foraging sites had low vegetation density, probably enhancing detection of predators, or high invertebrate abundance at high vegetation density. Parental provisioning rate decreased with increasing vegetation cover at foraging sites with high invertebrate abundance; conversely, where invertebrate abundance was low, provisioning rate increased with increasing vegetation cover.

Conclusions Vegetation structure at foraging sites suggests that a trade‐off between predator detection and prey availability influences foraging site selection in Yellowhammers. Associations between parental provisioning rate and vegetation variables suggest that where invertebrate abundance is high birds increase time spent scanning for predators at higher vegetation densities; however, when prey are scarce, adults may take more risks to provide food for their young.     

Prolonged Parental Feeding in Tool‐Using New Caledonian Crows

According to life‐history theory, the duration of extended parental feeding is determined by the costs and benefits of maximising reproductive success. Therefore, the length of regular parental provisioning should be correlated with the time required for juveniles to acquire the skills that they need to be independent. The relatively few cases of extremely prolonged parental feeding in both land and sea birds appear to be consistent with this prediction because they are associated with learning‐intensive foraging techniques. New Caledonian crows have the most intricate tool manufacture techniques amongst non‐human animals and juveniles take over 1 yr to reach adult‐like proficiency in their tool skills. We investigated the prediction that this species also should have prolonged parental provisioning. We found that these crows have one of the longest known periods of regular extended parental provisioning in birds. Some parents regularly fed juveniles for up to 10 mo post‐fledging. Humans also stand out amongst primates because of their learning‐intensive foraging strategies and an extended period of juvenile dependence. The independently evolved association between a relatively high level of technological skill in foraging and prolonged juvenile provisioning in both humans and New Caledonian crows raises the possibility that these two characteristics might be causally related.