Detection of insect prey by wild common marmosets: The effect of color vision

Most species of New World primates have an unusual color vision pattern that can affect an individual's ability to detect food. Whereas males can only be dichromatic, females can be either dichromatic or trichromatic. Trichromats are expected to have an advantage in detecting conspicuous food whereas dichromats should be better at locating cryptic resources. Here we aimed to understand how color vision phenotype influences insect foraging by five groups of common marmosets living in a semiarid environment. We recorded insect predation events, noting morphotype and color of the captured insect, and the substrate from which it was captured. Color modeling suggested that, for all values of chromatic contrast resulting from comparing the measured insect–substrate pairs, trichromats outperformed dichromats. Females showed an overall higher insect capture rate than males. Females also showed a higher capture rate of conspicuous insects but there was no sex difference for the capture of cryptic insects. When we compared only dichromatic individuals there was no difference between sexes. These findings suggest that differences found in capture rate related not only to sex but also to visual polymorphism and that the latter is a crucial factor determining insect capture rate in common marmosets. Nevertheless, these results should be interpreted with caution because of the small number (three) of dichromat females and the unknown phenotype of the remaining females. Our results support the balancing selection hypothesis, suggesting that the advantage of one phenotype over the other may depend on environmental circumstances. This hypothesis has recently been considered as the most plausible for the maintenance of visual polymorphism in New World primates.     

Group size,composition, and reproductive success in wild common marmosets (Callithrix jacchus)

Data from published sources about size and composition of wild common marmoset groups (Callithrix jacchus) were analyzed to see if the number of juveniles in a group is closely related to the number of other group members. Mean group size was 8.7 members including 4.4 adults (1.8 females, 2.5 males), 2.9 subadults, and 1.4 juveniles. The number of juveniles was significantly positively correlated to the number of adult males. Groups with one or two adult males had significantly fewer juveniles (mean: 1:1 juveniles) than groups containing more than two adult males (mean: 2.0 juveniles). Apart from a different number of subadults, results showed obvious similarities between common marmosets and tamarins of the genus Saguinus in size and composition of subgroups of adults as well as the key role of adult males in mediating the reproductive success of a breeding female. Common marmoset females seem to gain direct fitness benefits in increased reproductive success from the presence of a larger number of adult males. Whether or not other group members get fitness benefits depends on the reproductive strategy of adult males (monogamy vs. polyandry), their kinship, and on the genetic relationship of nonbreeders to the offspring of the breeding female. © 1995 Wiley-Liss, Inc.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

Time course of vocal modulation during isolation in common marmosets (Callithrix jacchus)

Common marmosets vocalize phee calls as isolation calls, which seem to facilitate their reunion with family groups. To identify multiple acoustic properties with different time courses, we examined acoustic modulations of phees during different social contexts of isolation. Subject marmosets were totally isolated in one condition, were visually isolated and could exchange vocalizations in another condition, and were visually isolated and subsequently totally isolated in a third condition. We recorded 6,035 phees of 10 male–female marmoset pairs and conducted acoustic analysis. The marmosets frequently vocalized phees that were temporally elongated and louder during isolation, with varying time courses of these changes in acoustic parameters. The vocal rates and sound levels of the phees increased as soon as the marmosets saw their pair mates being taken away, and then gradually calmed down. The phee duration was longer in conditions during which there were no vocal responses from their pair mates. Louder vocalizations are conspicuous and seem to be effective for long‐distance transmission, whereas shorter call duration during vocal exchanges might avoid possible vocal overlap between mates. Am. J. Primatol. 72:681–688, 2010. © 2010 Wiley‐Liss, Inc.     

Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus)

Social peer groups of callitrichid monkeys [marmosets and tamarins] exhibit intrasexual dominance hierarchies in captivity. This laboratory study employed two-choice behavioral discrimination bioassys to test the hypothesis that scent from female common marmosets contains chemical cues that permit discrimination between dominant females in the peri-ovulatory versus luteal phase of the ovarian cycle and females holding dominant versus subordinate status. When scent from only dominant females was presented, marmosets directed significantly greater amounts of investigatory behavior toward peri-ovulatory scent versus scent collected during the luteal phase of the ovarian cycle. Animals of both sexes demonstrated significant discriminatory behavior between scent deposited by dominant versus subordinate females, but only when the dominant female was in the peri-ovulatory phase of the ovarian cycle. Test animals directed equal amounts of investigative behavior toward scent from luteal-phase dominant females and subordinate females. Female test subjects deposited significantly more scent marks over presented scents than did male subjects, particularly when the scent had been donated by a peri-ovulatory female. Chemical odors specific to the peri-ovulatory and luteal phases of the ovarian cycle may play a role in mediating behavioral interactions among marmosets. Am. J. Primatol. 46:265–284, 1998. © 1998 Wiley-Liss, Inc.     

Context and sex differences exist in the acoustic structure of phee calls by newly–paired common marmosets (Callithrix jacchus)

Captive common marmosets of all ages robustly produce a “separation” phee call during brief separations from their group. In contrast, a second structural variant, which may function as an intergroup call, is produced in the home cage primarily by the reproductive adults. A previous study found that postpubertal but nonreproductive offspring rarely produce phee calls when in the home cage with the natal group, yet these marmosets call frequently after pairing with an opposite‐sex partner. The sudden increase in home cage phee calls may indicate the rapid onset of intergroup calling. Alternatively, marmosets may be producing the separation phee variant as a result of separation from the natal group. The present study investigated whether phee calls produced by recently paired individuals in the home cage were structurally distinguishable from their calls recorded in a separation paradigm. We also tested whether sex differences, known to exist in the calls of mature adults, could be found in calls recorded from younger, nonreproductive animals separated from their natal groups. We analyzed 18 acoustic parameters of phee calls produced in the home cage after pairing and of calls produced during separation both from the natal group and from a new mate. Discriminant function analyses found that home cage calls were clearly discriminable from separation calls (average 91.7% correctly classified), indicating that the rapid increase in home cage phee call production shortly after pairing is not a consequence of separation from the family group. Postpubertal marmosets appear to show a rapid behavioral adjustment to separation from their natal groups. Additionally, sex was clearly discriminable in calls recorded both before and after pairing (average 86.8% correctly classified). Like calls recorded from well‐established paired marmosets, phee calls produced by recently paired, postpubertal marmosets are discriminable by context and sex. Am. J. Primatol. 49:165–181, 1999. Published 1999 Wiley‐Liss, Inc.     

Insect prey foraging strategies in Callicebus oenanthe in northern Peru

Titi monkeys (genus Callicebus) are small-bodied platyrrhines that supplement their predominantly frugivorous diet with variable amounts of leaves, seeds, and/or arthropod prey. Notable interspecific variation in the amount of insect prey in the diet has been observed in Callicebus, ranging from 0% to 20%. In this study, I investigate the degree and type of prey foraging in a little-known species, Callicebus oenanthe inhabiting a fragmented, secondary forest on the foothills of the Andes in northern Peru. I present data on prey type, prey search and capture techniques, substrate/vegetation use, foraging height, prey capture efficiency, and seasonal variation of insect prey foraging in one group of C. oenanthe observed from January to August 2005. Insect prey accounted for 22% of the diet, the highest amount reported for any Callicebus species to date, and insects from at least six different orders were included. C. oenanthe was mainly an investigative forager of hidden prey, manipulating easy-to-open substrates such as rolled up leaves, and hunted ant swarms and larger insects opportunistically. Insect foraging was predominant during the dry season (26%) and decreased during the wet season (13%). The study group foraged mostly in the understory (2-6 m) within vine-laden shrubs and trees, which may conform to an anti-predator strategy of crypticity. Overall the group had an 83% insect capture success rate. These data suggest that insect prey is an important part of the diet of C. oenanthe and may be especially notable during periods of resource scarcity. This study adds to the knowledge concerning insect prey foraging in Callicebus, which can have an important role in defining ecological strategies in the selection of secondary protein food resources within a given ecosystem.     

Avian prey-dropping behavior. I. The effects of prey characteristics and prey loss

Numerous species of birds break hard-shelled prey items by droppingthem from a height. This intriguing prey-extraction method providesan excellent opportunity for studying foraging behavior becausea single, easily measurable quantity—height of drop—maybe influenced by a wide variety of identifiable characteristicsof the prey (e.g., breakability, weight) and social environment(e.g., alone or in the presence of kleptoparasites). Using adynamic, state variable modeling approach, this paper presentsthe first theoretical framework for avian prey-dropping systemsthat incorporates the diversity of prey characteristics andsocial situations. The model yielded a series of qualitativepredictions about prey-dropping behavior that can be testedreadily in any prey-dropping system. In particular, the results indicatedthat quantitative and qualitative differences in item breakability andpotential kleptoparasitism should have a significant effecton the height and pattern of prey dropping.     

Neighbor effects in marmosets: social contagion of agonism and affiliation in captive Callithrix jacchus

Researchers have demonstrated the neighbor effect for affiliative and agonistic neighbor vocalizations in captive chimpanzees. We extend the investigation of the neighbor effect to New World monkeys, Callithrix jacchus. We collected data on vocalizations and behaviors of 31 focal individuals and concurrent neighbor vocalization within three behavioral categories: intragroup and intergroup aggression and intragroup affiliation. We investigated whether there was an influence of neighbor vocalizations on focal behavior within the same behavioral category. For data analysis we used approximate randomization of paired‐sample t‐tests. We found that marmosets performed intergroup aggressive behavior (bristle, anogenital present for neighbor loud shrill only) for significantly longer, and emitted significantly more intergroup agonistic vocalizations (twitter, loud shrill), at a high frequency of intergroup agonistic neighbor vocalizations (twitter, loud shrill) than at low. The marmosets were also significantly more likely to engage in bristle behavior immediately after hearing a neighbor intergroup aggressive call (twitter, loud shrill) than directly beforehand. High neighbor intragroup agonistic calls (chatter) were associated with significantly longer spent in related behavior (composite of: attack, chase, steal food). Affiliative behaviors (share food, grooming invite) were engaged in by marmosets for significantly longer at higher frequencies of affiliative neighbor chirp calls than at low. Marmosets were also significantly more likely to perform food sharing and active affiliative contact immediately after rather than before hearing a neighbor chirp call. Our findings suggest that neighbor vocalizations influence marmoset behavior through social contagion and indicate that the neighbor effect for affiliation and aggression generalizes to the marmoset. Am. J. Primatol. 72:549–558, 2010. © 2010 Wiley‐Liss, Inc.     

Foraging behaviour and prey discrimination in the bluespotted maskray Dasyatis kuhlii

A study observing the foraging behaviours and prey discrimination of a common demersal stingray, the bluespotted maskray Dasyatis kuhlii was performed under controlled laboratory conditions. A selection of prey species and masses were offered at depths of 10 and 50 mm in sand. Foraging efficiency and prey selection at both burial depths were compared. Dasyatis kuhlii selected the ghost shrimps, Trypaea australiensis and T. australiensis >2·5 g, range ± 0·2 g though foraging errors represented by prey being excavated and not consumed suggested a limited discriminatory ability at the point of detection. Burial depth did not influence prey species, mass selection or discriminatory ability.     

Male parenting and response to infant stimuli in the common marmoset (Callithrix jacchus)

Callithrix jacchus infants are raised in complex family environments where most members participate in rearing the young. Many studies examining male parental behavior have focused on the carrying of infants with observations made within the family context. However, interference from family members can make it difficult to assess the father's motivation to care for infants. Our goals were to develop a testing paradigm for determining an individual's response to infant stimuli separate from family influences, compare a male's motivation to respond to an infant stimulus outside the family with his paternal behavior within the family, to compare responses to infant stimuli of parentally experienced versus inexperienced males and finally to develop a reproducible and standardized method of testing male responsiveness to infant stimulus that could serve to evaluate hormonal manipulations. Fifteen experienced common marmoset fathers were evaluated using three different measures of parental behavior: (1) instantaneous scan sampling, (2) continuous focal sampling in the family, and (3) continuous focal sampling of males presented with four infant stimuli: familiar and unfamiliar infants, familiar and unfamiliar infant vocalizations. Six parentally inexperienced males (non-fathers) served as controls. Males that carried the most in the family were typically the same males that responded most to the infant vocalization tests. Experienced fathers did not differ in their latency to enter the stimulus cage for any of the four infant stimuli response tests while inexperienced males took significantly longer to enter the stimulus cage. In addition, fathers expressed a greater frequency of infant-directed behavior than did the inexperienced males during the unfamiliar infant and unfamiliar vocalization tests. These studies show that experienced male marmosets are highly motivated to interact with infant stimuli and that there is interindividual variability in response to infant vocalizations. Testing males outside of the family allows for a clear assessment of male's interest in infant stimuli in both parentally experienced fathers and inexperienced males.     

Quantification of hair cortisol concentration in common marmosets (Callithrix jacchus) and tufted capuchins (Cebus apella)

Quantifying cortisol concentration in hair is a non‐invasive biomarker of long‐term hypothalamic‐pituitary‐adrenal (HPA) activation, and thus can provide important information on laboratory animal health. Marmosets (Callithrix jacchus) and capuchins (Cebus apella) are New World primates increasingly used in biomedical and neuroscience research, yet published hair cortisol concentrations for these species are limited. Review of the existing published hair cortisol values from marmosets reveals highly discrepant values and the use of variable techniques for hair collection, processing, and cortisol extraction. In this investigation we utilized a well‐established, standardized protocol to extract and quantify cortisol from marmoset (n = 12) and capuchin (n = 4) hair. Shaved hair samples were collected from the upper thigh during scheduled exams and analyzed via methanol extraction and enzyme immunoassay. In marmosets, hair cortisol concentration ranged from 2,710 to 6,267 pg/mg and averaged 4,070 ± 304 pg/mg. In capuchins, hair cortisol concentration ranged from 621 to 2,089 pg/mg and averaged 1,092 ± 338 pg/mg. Hair cortisol concentration was significantly different between marmosets and capuchins, with marmosets having higher concentrations than capuchins. The incorporation of hair cortisol analysis into research protocols provides a non‐invasive measure of HPA axis activity over time, which offers insight into animal health. Utilization of standard protocols across laboratories is essential to obtaining valid measurements and allowing for valuable future cross‐species comparisons.     

Dangerous prey and daring predators: a review

How foragers balance risks during foraging is a central focus of optimal foraging studies. While diverse theoretical and empirical work has revealed how foragers should and do manage food and safety from predators, little attention has been given to the risks posed by dangerous prey. This is a potentially important oversight because risk of injury can give rise to foraging costs similar to those arising from the risk of predation, and with similar consequences. Here, we synthesize the literature on how foragers manage risks associated with dangerous prey and adapt previous theory to make the first steps towards a framework for future studies. Though rarely documented, it appears that in some systems predators are frequently injured while hunting and risk of injury can be an important foraging cost. Fitness costs of foraging injuries, which can be fatal, likely vary widely but have rarely been studied and should be the subject of future research. Like other types of risk‐taking behaviour, it appears that there is individual variation in the willingness to take risks, which can be driven by social factors, experience and foraging abilities, or differences in body condition. Because of ongoing modifications to natural communities, including changes in prey availability and relative abundance as well as the introduction of potentially dangerous prey to numerous ecosystems, understanding the prevalence and consequences of hunting dangerous prey should be a priority for behavioural ecologists.     

Prey size, prey nutrition, and food handling by shrews of different body sizes

We tested some predictions relating metabolic constraints offoraging behavior and prey selection by comparing food handlingand utilization in four sympatric shrew species: Sorex minutus(mean body mass = 3.0 g), S. araneus (8.0 g), Neomys anomalus(10.0 g), and N. fodiens (14.4 g). Live fly larvae, mealwormlarvae, and aquatic arthropods were offered to shrews as smallprey (body mass <0.1 g). Live earthworms, snails, and smallfish were offered as large prey (>0.3 g). The larvae werethe high-nutrition food (>8 kJ/g), and the other prey werethe low-nutrition food (<4 kJ/g). The smallest shrew, S.minutus, utilized (ate + hoarded) <30% of offered food,and the other species utilized >48% of food. The largerthe shrew, the more prey it ate per capita. However, highlyenergetic insect larvae composed 75% of food utilized by S.minutus and only >40% of the food utilized by the other species. Thus, inverse relationships appeared between shrewbody mass and mass-specific food mass utilization and betweenshrew body mass and mass-specific food energy utilization:the largest shrew, N. fodiens, utilized the least food massand the least energy quantity per 1 g of its body mass. Also,the proportion of food hoarded by shrews decreased with increase in size of shrew. With the exception of S. araneus, the sizeof prey hoarded by the shrews was significantly larger thanthe size of prey eaten. Tiny S. minutus hoarded and ate smallerprey items than the other shrews, and large N. fodiens hoardedlarger prey than the other shrews.