Leila M. Porter

Enrichment effects on rhesus monkeys successively housed singly, in pairs, and in groups

Abstract Many studies have examined the short-term effects of inanimate environmental enrichment on the behavior of captive primates. Similarly, numerous studies have examined the behavioral effects of manipulations to the social environment. Few analyses have examined the long-term effects of inanimate environmental enrichment or compared the effects of inanimate and social enhancements. The behavior of control ( n = 49) and enriched ( n = 44) rhesus monkeys ( Macaca mulatta ) was observed from 1–4 years, as subjects spent successive years housed singly, in paris, and then in small groups. Social housing condition and/or age of subject significantly affected time spent inactive, grooming, playing, exploring, and behaving abnormally. Frequency of vocalization was similarly affected. Social housing resulted in more species-typical behavior patterns than did single caging. Subjects were more socially oriented when pair-housed than when living in small groups. Inanimate enrichment did not affect behavior over a 3 year period, although enhancements were well-used by singly-caged yearlings and pair-housed juveniles. Subjects used enrichment less frequently when housed in groups. The data suggest that the presence of a social partner(s) led to more beneficial changes in behavior than did the provision of inanimate enhancements for rhesus monkeys in the studied age range. Therefore, it is concluded that social enrichment should be provided when possible and appropriate. Efforts to enrich the inanimate environment will be most beneficial when focused on socially-restricted primates.

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species‐typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species‐typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three‐phase enrichment program and the rest served as controls. Group‐housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self‐grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self‐grooming and exploring than did controls. Among group‐housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially.

Composition and Nutritional Characteristics of Fungi Consumed by Callimico goeldii in Pando, Bolivia

Though ≥22 species of Primates consume fungi, most do so at low rates, comprising <5% of their feeding time. Goeldis monkeys (Callimico goeldii), spend up to 29% of their feeding time year-round consuming fungal sporocarps, the fruiting bodies of fungi. We provide comprehensive data on the nutritional characteristics of 4 species of fungi consumed by Callimico goeldii (Ascopolyporus polyporoides, Ascopolyporus polychrous, Auricularia auricula, and Auricularia delicata). The composition of the fungi is similar to that of other fungi: predominantly fiber (66.2–83.0% dry matter) with small amounts of sugar (2.0–5.6% dry matter) and crude fat (0.9–1.6% dry matter). Though the crude protein content is substantial (5.5–13.4% dry matter), much of the nitrogen in the fungi is not likely to be available to Callimico goeldii because it is associated with indigestible food components or is in nonprotein form. The mineral content of the fungi are within the normal range for fungi generally and the calcium-to-phosphorus ratio is low (0.07–0.25). Fungi appear to be a low-quality food resource for Callimico goeldii and may contribute to their relatively large home ranges and low population density compared to other Callitrichinae. Research on the ability of Callimico goeldii to digest fungi is needed to understand fully the nutritional value of fungi to them. We discuss adaptations Callimico goeldii may have for improving their ability to obtain nutrients from fungi and potential ecological correlates of mycophagy.

Tamarins: Insights into monogamous and non-monogamous single female social and breeding systems.

Tamarins are reported to live in small multimale‐multifemale groups characterized by a single breeding female. Here we present information on the composition and genetic relatedness of individuals in 12 wild‐trapped groups of Weddells saddleback tamarins (Saguinus weddelli) from northern Bolivia to determine if groups are best described as nuclear or extended families suggesting social monogamy or whether groups contain several unrelated same sex adults indicative of social polyandry/polygyny. Mean group size was 6.25 including an average of 2.16 adult males (range 1–4) and 2.08 adult females (1–3). No group contained only one adult male and one adult female and 25% of groups contained two parous females. We estimated the genetic relatedness among individuals using 13 polymorphic microsatellite markers. Across the population, mean relatedness was low and not significantly different among adult males versus among adult females, suggesting that both sexes disperse from their natal groups. Adults of both sexes also tended to have close same‐sex adult relatives within their groups; relatedness among adult females of the same group averaged 0.31 and among adult males was 0.26. This suggests that tamarins of one or both sexes sometimes delay dispersal and remain as adults in their natal group or that emigration of same‐sexed relatives into the same group may be common. Finally, parentage analyses indicated that, whereas the parents of juveniles generally were present in the group, this was not always the case. Based on these data, published reports of the presence of multiple breeding males and occasionally multiple breeding females in the same group, and the fact that less than 10% of groups in the wild contain a single adult male‐adult female pair, we argue that social polyandry best characterizes the composition of tamarin groups and that monogamy is not a common mating pattern in Saguinus weddelli or other tamarin species. Am. J. Primatol. 78:298–314, 2016.

Exudates as a fallback food for Callimico goeldii.

Fallback foods have been defined as resources for which a species has evolved specific masticatory and digestive adaptations, and are consumed principally when preferred foods are scarce. In the present field investigation, we examine fungi, fruit, and exudate consumption in one group of Callimico goeldii in order to determine the importance of exudates as a fallback food for this species. Based on a total of 1,198 hr of quantitative behavioral data collected between mid‐November 2002–August 2003, we found that pod exudates of Parkia velutina accounted for 19% of callimico feeding time in the dry season. This resource was not consumed in the wet season when fruits and fungi were the most common items in the diet. In the dry season of 2005 (July), the same callimico study group did not consume Parkia pod exudates. Instead, the group ate exudates obtained from holes gouged in tree trunks by pygmy marmosets and exudates resulting from natural weathering and insect damage on trunks, roots, and lianas. Pod exudates are reported to contain greater amounts of readily available energy than do trunk and root exudates, and were consumed throughout all periods of the day, particularly in the late afternoon. Trunk and root exudates were consumed principally in the morning. We propose that digestive adaptations of the hindgut, which enable callimicos to exploit fungi (a resource high in structural carbohydrates) year‐round, predispose them to efficiently exploit and process exudates as fallback foods when other resources, such as ripe fruits, are scarce. Am. J. Primatol. 71:120–129, 2009.

Social Behavior of Callimicos: Mating Strategies and Infant Care

Callimico (Callimico goeldii) is the only species of tamarin or marmoset to regularly produce one infant, possibly representing a derived trait. Studies of adult–infant interactions among callimicos, therefore, offer important insights into the evolution of cooperative infant care in callitrichids. We studied a group of callimicos consisting of one adult female (FH), two adult males (MR and MJ), and one young female (FS), at a Bolivian field site. Opportunistic data on infant care and mating behavior were taken for 3 months following FS’s birth. Then, for 8 months, behavioral data and nearest neighbor distances were collected using focal animal sampling for 1,199 observation hours. Nearest neighbor distances among group members varied significantly (p < 0.001): on average the breeding female was found 2.7 m from her infant, 2.8 m from adult male MJ, and 3.5 m from adult male MR. The frequency of grooming behaviors varied significantly among adults (p < 0.001): FH was groomed most (8.4% of observations) and spent the least time grooming others (3.4%), while MR was groomed least (5.9%) and groomed others most (10.7%). Although FH was observed mating with both males within 2 months after the birth of FS, she did not give birth to additional offspring. All adults shared food with and carried the infant. Adults also shared food with each other. Aggressive behavior among adults was extremely rare (n = 8) and occurred six times in a feeding context and twice in a non-feeding context. These data demonstrate that despite producing singletons, callimicos like many other callitrichids are characterized by a polyandrous mating pattern, spatially cohesive groups, and high levels of social cooperation.

The Ecology of Exudate Production and Exudate Feeding in Saguinus and Callimico

Callitrichines are small-bodied New World primates characterized by anatomical, behavioral, and/or physiological adaptations that enable individuals to exploit plant exudates. However, little is known concerning rates of exudate production and availability of exudates to primate consumers. In this investigation, we present data on patterns of exudate feeding in a mixed species troop of tamarins (Saguinus mystax and S. fuscicollis) in northeastern Peru, and a group of callimicos (Callimico goeldii) in northwestern Bolivia. In addition, we collected data on the amount and renewal rate of exudates produced from naturally occurring and experimentally induced wounds to tree species exploited by Saguinus and Callimico. Our results indicate that exudates are available to nongouging primate foragers during most or all months of the year. In Saguinus, exudates from tree trunks, Parkia pods, and holes gouged by pygmy marmosets (Cebuella pygmaea) accounted for 16.3% of total plant feeding and foraging time. In the case of Callimico, stilt root exudates, Parkia pod exudates, and trunk exudates accounted for 35% of plant feeding time. Daily exudate production on individual trees in Bolivia (n = 17) varied from 0 to 10.75 g/day. Total monthly trunk exudate production in naturally occurring wounds present on sample trees in Peru (n = 5) ranged from 0 to 369 g. Pod exudates were available principally during the dry season, whereas trunk exudates were available during all months of the year. We argue that exudates represent a reliable and renewable resource for nongouging callitrichines, and that tamarins and callimicos effectively track the location, availability, and productivity of trunk, stilt root, and pod exudate sources in their home range.

Mycophagy and its influence on habitat use and ranging patterns in Callimico goeldii

Mycophagy has been documented in a number of species of marmosets and lion tamarins (Callitrichinae) but its effect on ranging behavior is not known. We present the results of 10 years of research on five groups of Goeldis monkey (Callimico goeldii) at a field site in northwestern Bolivia. We studied the diet and ranging behavior of two of the groups. On average, groups contained 4.5 individuals (range 2.0-9.0), but they gradually decreased in size until only the breeding female remained in the home range. The annual diet was composed of fungi (31.1-34.9%), fruits (34.0-40.6%), prey (17.4-30.1%), and exudates (1.0-10.9%). They had large home ranges (114-150 ha) and over time individuals tended to shift their core areas of use. They used secondary and bamboo forest and forest with dense understories more than expected based on availability. We suggest that the large home ranges and shifting core areas used by C. goeldii are components of a foraging strategy to track patchy, low density, and ephemeral fungal fruiting bodies. Our results, along with data published on other callitrichines, indicate that groups of Leontopithecus, Callithrix, and Callimico that eat fungi have larger home ranges than those that do not. Mycophagy is one of the several factors that evidently affect home range size in callitrichines. Fungi are clearly an important food source for a number of populations, but additional studies are needed to determine why some eat fungi frequently while others do not.

Mother's little helpers: What we know (and don't know) about cooperative infant care in callitrichines

Since Darwin ( ), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamiltons ( ) theory of inclusive fitness provided an explanation by showing how cooperative behaviors could be adaptive if directed at closely related kin. Recent studies, however, have begun to question whether kin selection is sufficient to explain cooperative behavior in some species (Bergmüller, Johnstone, Russell, & Bshary, ). Many researchers have instead emphasized the importance of direct fitness benefits for helpers in the evolution of cooperative breeding systems. Furthermore, individuals can vary in who, when, and how much they help, and the factors that affect this variation are poorly understood (Cockburn, ; Heinsohn, ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, ).

Group Demographics and Dispersal in a Wild Group of Goeldi’s Monkeys (Callimico goeldii)

Callimico goeldii is one of the least studied South American primates, as its cryptic nature and low density make it difficult to observe in the wild [1]. Callimico differs from the other members of its subfamily, the Callitrichinae, in that it usually has single rather than twin offspring [2]. Here, we present the first documentation of dispersal and group formation among wild C. goeldii and discuss our observations in the context of breeding strategies and social organization.