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.     

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.     

Age and Sex-Based Differences in the Use of Prey Sensory Cues in Wolf Spiders (Araneae: Lycosidae)

Differences in foraging patterns mediated by sensory cues were examined between adult and juvenile male and female wolf spiders (Schizocosa rovneri; Lycosidae). Patch residence time for thirty-one spiders were tested among juveniles and adults in artificial foraging patches. Patches varied in sensory information provided by live prey (crickets) as follows: visual stimuli alone; vibratory stimuli alone; visual and vibratory stimuli together; and control (no stimuli). Spiders moved between patches for one hour, but could not feed. Adult Schizocosa rovneri use primarily visual information to determine patch residence time, but juveniles use vibratory cues as well. Significant age and sex-based differences in the use of sensory cues suggest that observed divergent foraging strategies are partly due to the use of different perceptual cues in prey detection.     

DIFFERENCES IN THE FORAGING OF JUVENILE AND ADULT BIRDS: THE IMPORTANCE OF DEVELOPMENTAL CONSTRAINTS

Juvenile birds differ from conspecific adults in their diet and methods of prey capture and prey handling. Juvenile-adult differences in foraging result from (1) immaturity of the beak, skeleto-muscular and neurological systems and (2) the time required to learn foraging skills. These conclusions are largely based on field observations. More experimental studies to assess the relative importance of the various constraints are needed.
Juvenile birds appear to be under strong selection to reach adult form and function as rapidly as possible. Remaining differences between juveniles and adults are largely attributable to constraints. In contrast to many other taxa there are few examples in which juvenile-adult differences in foraging have been accentuated by selection on the juvenile behaviours.     

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.     

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.     

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.     

Detection of elevated antibody against calreticulin by ELISA in aged cynomolgus monkey plasma

Calreticulin (Crt) is a molecular chaperone ubiquitously present in the endoplasmic reticulum. In non-human primates, age-related occurrence of anti-Crt antibody has not been reported. We developed an ELISA assay for an anti-Crt antibody and determined the age-related increase in the levels of anti-Crt antibody in three groups of cynomolgus monkeys: juvenile (1.5 yr), young adults (5-10 yr) and aged adults (20-34 yr). Mean ± SD auto-antibody levels at 450 nm in juvenile, young adults and aged groups were 0.23 ± 0.18, 0.30 ± 0.28, and 0.55 ± 0.33, respectively. Statistically significant differences were noted in the autoantibody levels to Crt among the aged group and juvenile or young adults. This is the first report to demonstrate the expression of anti-Crt autoantibody in aged monkeys and indicates that cynomologous monkeys may serve as an appropriate nonhuman primate model for studies of age-related alteration of immune function in elderly humans. Though preliminary, this finding merits further investigation to determine the relationship between immunosenescence and expression of antibodies to Crt.     

FORAGING OF JUVENILE MONK SEALS AT FRENCH FRIGATE SHOALS, HAWAII

Emaciation and poor survivorship of juvenile Hawaiian monk seals at French Frigate Shoals atoll prompted a study of their foraging, using video camera technology ( crittercam ). Nine juveniles between the ages of 1 and 3 yr (six males, three females) were fitted with crittercam to identify their foraging habitat and feeding behavior. All feeding was directed at small (≤ 10 cm), cryptic, benthic prey. Older seals (ages 2 and 3), varied in their foraging intensity with most of their attention directed at shallow atoll depths (10–30 m). In contrast, the three yearlings focused all their feeding in the sand fields (50–100 m) on the atoll's outer slope. Bottom trawls were used to assess the prey abundance of the sand habitat and found 70% of the numerical catch was flounder ( Bothidae ). Extrapolating the yearlings' prey capture rate (0.13/min, derived from the crittercam video) over their total bottom time yielded an estimated 1–1.3 kg/day of flounder. The mean size of flounder (5 ± 1.7 cm) caught in the bottom trawls was close to the size at which larval flounder settle from the plankton (3 cm), suggesting that localized changes in oceanography could directly impact the seals' prey supply. Extensive use of sand communities by young seals may be the strongest link yet identified between juvenile survivorship and oceanographic dynamics.     

Progressive parenting behavior in wild golden lion tamarins

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

Ontogenetic variation in the autecology of the greater earless lizard Cophosaurus texanus

We investigated the potential for ontogenetic resource partitioning within a population of the Texas earless lizard Cophosaurus texanus Results from focal samples, line transects, haphazard observations, and stomach flushes compiled in summer (July 1993) and autumn (September 1995) revealed differences in microhabitat use and diet between adults and juveniles Juveniles use rock perches more frequently than adult males, and consume smaller prey than adults No ontogenetic differences in thermal ecology were observed Diet differences between juveniles and adults may be attributed to the inability of juveniles to handle large prey items Differences between juveniles and adults in prey size and microhabitat use suggest ontogenetic variation in foraging, predator avoidance, and territory defense     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Foraging behavior predicts age at independence in juvenile Eurasian dippers (Cinclus cinclus)

Timing of foraging independence may be controlled by parents,offspiing, or both and may have consequences for dispersal,reproduction, and survival In a study of juvenile Eurasian dippers(Cinclus cinchus), I examined the relationship between individualdifferences in parental provisioning, the development of foraging,and the timing of independence. Young dippers forage very differentlyfrom adults, specializing on small, stationary pre such as simuliidlarvae (Diptera), and avoiding energetically costly and highlyskilled foraging techniques, such as diving, by which adultsobtain larger prey In my Welsh study area, age at independencevaried substantially within and between broods. Juveniles thatrelied more on simuliids and less on larger prey were independentsooner, as were juveniles with higher rates of intake whileforaging the effect was obvious 3–4 days after fledging.Provisioning rate and total caloric intake over the dependentperiod was unrelated to age at independence, although greaterreliance on parental feeding was associated with higher totalcaloric intake. Higher rates of intake from begging were correlatedwith reduced foraging time. The results demonstrate that theacquisition of the adult foraging strategy is not a prerequisitefor independence or, hence, dispersal. In fact, mastering theskills necessary to capture larger prey may delay independence.Individual juvenile dippers seem to find different solutionsto the trade-off between gaining sufficient food (either frombegging or from foraging for simuliids) and the eventual necessityof learning to forage like an adult.     

Vigilance during play in squirrel monkeys

Play by young squirrel monkeys (Saimiri boliviensis) may put them and other troop members at risk for predation because youngsters are noisy, separated from adults, and not vigilant when at play. In a study using separated groups of adults and 1-year-old juveniles caged outdoors, we found that adult female squirrel monkeys become more vigilant during periods of spontaneous play among juveniles. This behavioral response could be obtained with auditory cues (play vocalizations) alone. Five times as much vigilance activity was directed toward an area from which threat or disturbance was likely to come as was directed toward the juveniles themselves. These results suggest both an adaptive, compensatory increase in adult vigilance during play and a function for play vocalizations. Additional functions for play vocalizations remain to be investigated.     

Social learning of hunting skills in juvenile marsh harriers <Emphasis Type="Italic">Circus aeruginosus</Emphasis>

The impact of social factors on the improvement of hunting skills of juvenile marsh harriers during their first autumnal migration were studied in SE Poland. While foraging with adult birds, juveniles performed more dives on prey both in terms of number of trials and rates. Hunting sessions of juveniles were more efficient in the presence of adults than in the absence of adults. Juveniles hunting with adults and other juveniles could select adequate habitat patches in which access to prey is easier. The role of vertical and horizontal transmission of information in the development of hunting skills in juvenile marsh harrier were confirmed because faster development of hunting ability was achieved in the social hunting after the end of their postfledging dependency period.     

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.     

Prey use and nutritional differences between reproductive states and age classes in Atlantic spotted dolphins (Stenella frontalis) in the Bahamas

Nutritional quality of prey is a significant driver of predator foraging patterns. In mammals, nutritional needs are known to change across ontogeny and reproductive state; however, little is known about nutrition in marine mammals. For this study, we used observational data of diurnal foraging events, collected annually from 1992 to 2009, to investigate nutrition and prey use in Atlantic spotted dolphins (Stenella frontalis) on Little Bahama Bank, Bahamas, between reproductive states (lactating, pregnant, nonreproductively active [NRA]. We also investigated the impact of age class association (various calf age groups [ages 1–6], older “noncalf” juveniles, and adults) on foraging group nutrition and prey use. To obtain representative nutrient values, we measured calories, lipids, proteins, and moisture in common prey. Using nutritional values and observational data, we investigated the influence of nutritional value on prey use. Results indicated that specific nutrients were targeted by different reproductive states and age class groups. Nutritional intake of all nutrients was higher for lactating females than pregnant females, but lower than NRA females. Investigation of age group associations revealed that nutritional intake of all four nutrients was higher for noncalf than calf‐associated groups. This study represents one of the first investigations of intraspecific prey use and nutritional differences in cetaceans.     

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.     

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.     

Size and experience matter: diving behaviour of juvenile New Zealand sea lions (Phocarctos hookeri)

The diving ability of juvenile animals is constrained by their physiology, morphology and lack of experience, compared to adults. We studied the influences of age and mass on the diving behaviour of juvenile (2–3-year-old females, n = 12; 3–5-year-old males, n = 7) New Zealand (NZ) sea lions (Phocarctos hookeri) using time–depth recorders (TDRs) from 2008 to 2010 in the NZ subantarctic Auckland Islands. Diving ability (e.g. dive depth, duration and bottom time per dive) improved with age and mass. However, the percentage of each dive spent at the bottom, along with percentage time at sea spent diving, was comparable between younger and lighter juveniles and older and heavier juveniles. These suggest that younger and older juveniles expend similar foraging effort in terms of the amount of time spent underwater. Only, 5-year-old male juveniles dove to adult female depths and durations and had the highest foraging efficiency at depths >250 m. It appears that juvenile NZ sea lions attain adult female diving ability at around 5 years of age (at least in males), but prior to this, their performance is limited. Overall, the restricted diving capabilities of juvenile NZ sea lions may limit their available foraging habitat and ability to acquire food at deeper depths. The lower diving ability of juvenile NZ sea lions compared to adults, along with juvenile-specific constraints, should be taken into consideration for the effective management of this declining, nationally critical species.