The functional correlates of jaw‐muscle fiber architecture in tree‐gouging and nongouging callitrichid monkeys

Common (Callithrix jacchus) and pygmy (Cebuella pygmaea) marmosets and cotton‐top tamarins (Saguinus oedipus) share broadly similar diets of fruits, insects, and tree exudates. Marmosets, however, differ from tamarins in actively gouging trees with their anterior dentition to elicit tree exudates flow. Tree gouging in common marmosets involves the generation of relatively wide jaw gapes, but not necessarily relatively large bite forces. We compared fiber architecture of the masseter and temporalis muscles in C. jacchus (N = 18), C. pygmaea (N = 5), and S. oedipus (N = 13). We tested the hypothesis that tree‐gouging marmosets would exhibit relatively longer fibers and other architectural variables that facilitate muscle stretch. As an architectural trade‐off between maximizing muscle excursion/contraction velocity and muscle force, we also tested the hypothesis that marmosets would exhibit relatively less pinnate fibers, smaller physiologic cross‐sectional areas (PCSA), and lower priority indices (I) for force. As predicted, marmosets display relatively longer‐fibered muscles, a higher ratio of fiber length to muscle mass, and a relatively greater potential excursion of the distal tendon attachments, all of which favor muscle stretch. Marmosets further display relatively smaller PCSAs and other features that reflect a reduced capacity for force generation. The longer fibers and attendant higher contraction velocities likely facilitate the production of relatively wide jaw gapes and the capacity to generate more power from their jaw muscles during gouging. The observed functional trade‐off between muscle excursion/contraction velocity and muscle force suggests that primate jaw‐muscle architecture reflects evolutionary changes related to jaw movements as one of a number of functional demands imposed on the masticatory apparatus. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Species differences in response to conspecific intruders inCallithrix jacchus andSaguinus oedipus

In this study, the first performed on two species of callitrichid primates under identical conditions, the responses elicited in newly mated individuals by conspecific intruders were compared in four pairs of Callithrix jacchusand four pairs of Saguinus oedipus.Intruders were systematically varied in terms of sex and the social context in which they were met. Clear sexual dimorphism was observed in the behavior of Saguinus oedipus,but the behavior of males and females was less dimorphic in Callithrix jacchus.Males and females of both species showed an increase in agonistic and display behavior in the presence of same-sex intruders, but the mode of behavior varied both with sex and species. Social facilitation, as indicated by increased frequencies of agonistic and display responses in the presence of a mate, was observed only in males of both species. Neither C. jacchusnor S. oedipusdisplayed clear evidence of a monogamous mating system like that of Callicebusor of a polygynous mating system like that of Saimiri.Observed differences in the responses to conspecifics between these two species in the laboratory may be explained by facultative differences in mating systems resulting from differences in ranging and foraging behavior under freeranging conditions.     

Age of epiphyseal closure in tamarins and marmosets

Estimates of the chronological age for animals of unknown age provide useful information for medical, demographic, and evolutionary studies. Skeletal development, as indicated by epiphyseal closure, can be used to estimate an animal's chronological age or specify its stage of development. Many studies of Primate skeletal development have used animals of unknown age, with the order of epiphyseal closure providing a relative age for each animal. This study examines the age of epiphyseal closure at 22 epiphyseal sites using animals of known age at death in three calitrichid species (Saguinus fuscicollis, Saguinus oedipus, and Callithrix jacchus). The observed average age of epiphyseal closure is similar in these tamarins and marmosets. There is a significant difference in rate of development between the species. Regression equations can predict the age of unknown animals to within 4.8 months for S. fuscicollis, 8.6 months for S. oedipus, and 7.6 months for C. jacchus (twice the standard error of the estimate). These age estimates allow us to determine if an animal is relatively mature or immature, but are largely unacceptable for studies in which precise age estimates are necessary. The order of epiphyseal closure is similar across 11 monkey species (using additional data from published literature) and supports the suggestion of a general pattern in Primate skeletal development. Am. J. Primatol. 41:129–139, 1997. © 1997 Wiley-Liss, Inc.     

Moving laboratory rhesus monkeys (Macaca mulatta) to unfamiliar home cages

Removing a three-year-old rhesus monkey from its home cage and placing it into a second but unfamiliar cage of similar size produces increases in vocalizations and stereotyped behaviors, and decreases in cage shaking and manual and oral exploration of the cage. Males and females respond differently to a cage change, particularly in regard to visual exploration and locomotor activity. This research was supported by N. I. H. grants RR00169, HD04335, MH22253, and MH19760.     

Trabecular bone structure in the mandibular condyles of gouging and nongouging platyrrhine primates

The relationship between mandibular form and biomechanical function is a topic of significant interest to morphologists and paleontologists alike. Several previous studies have examined the morphology of the mandible in gouging and nongouging primates as a means of understanding the anatomical correlates of this feeding behavior. The goal of the current study was to quantify the trabecular bone structure of the mandibular condyle of gouging and nongouging primates to assess the functional morphology of the jaw in these animals. High‐resolution computed tomography scan data were collected from the mandibles of five adult common marmosets (Callithrix jacchus), saddle‐back tamarins (Saguinus fuscicollis), and squirrel monkeys (Saimiri sciureus), respectively, and various three‐dimensional morphometric parameters were measured from the condylar trabecular bone. No significant differences were found among the taxa for most trabecular bone structural features. Importantly, no mechanically significant parameters, such as bone volume fraction and degree of anisotropy, were found to vary significantly between gouging and nongouging primates. The lack of significant differences in mechanically relevant structural parameters among these three platyrrhine taxa may suggest that gouging as a habitual dietary behavior does not involve significantly higher loads on the mandibular condyle than other masticatory behaviors. Alternatively, the similarities in trabecular architecture across these three taxa may indicate that trabecular bone is relatively unimportant mechanically in the condyle of these primates and therefore is functionally uninformative. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

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

Since Darwin ( 1859 ), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamilton's ( 1964 ) 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, 2007 ). 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, 1998 ; Heinsohn, 2004 ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, 2012 ).     

Monitoring ovarian function in marmosets and tamarins by the measurement of urinary estrogen metabolites

Practical aspects of urinary estrogen analysis were considered with regard to establishing simple and reliable methods for monitoring ovarian function in marmosets and tamarins. Changes in the hormone:creatinine ratio in small volumes of urine from the common marmoset were significantly correlated with changes in 24-h excretion. Comparison of the metabolism and excretion of estrogens during the ovarian cycle in the common marmoset and cottontop tamarin revealed interesting species differences. High concentrations of conjugated estrone were measured in marmoset plasma, but estradiol 17β was the predominant estrogen in urine. In contrast, estrone was the most abundant estrogen measured in tamarin urine. Both species excreted very little estriol. Sulfates and glucuronides were present in urine in similar proportions before ovulation in the marmoset, although after ovulation sulfates were the more abundant. Conversely, most of the estrogens in tamarin urine appeared to be conjugated as glucuronides. Direct assay for estrone sulfate was applied to the measurement of urinary estrogen excretion during the ovarian cycle in a marmoset. The results compared well with those for total estradiol 17β after hydrolysis and ether extraction. The use of direct assays for conjugated estrogens in small volumes of urine is suggested as a practical method for monitoring ovarian function in marmosets and tamarins.     

Diseases of the Callitrichidae: a review.

The Callitrichidae contains four genera that embrace up to 50 species and subspecies found in neotropical habitats. Certain members have either naturally occurring or induced conditions that serve as important models of human disease. They include viral, bacterial, and parasitic infections, nutritional deficiencies, neoplasia, and various other conditions. The spontaneous diseases of captive callitrichids and those to which these species are experimentally susceptible were reviewed.     

Does the milk of callitrichid monkeys differ from that of larger anthropoids?

The generalization that anthropoid primates produce dilute milks that are low in protein and energy is based primarily on data from large monkeys of the families Cebidae and Cercopithecidae, as well as humans. The marmosets and tamarins (Callitrichidae) are not only much smaller in body size, but also typically raise multiple offspring during a relatively brief lactation. We hypothesized that selection for small body size and high reproductive rate might favor secretion of milk of higher energy and protein concentrations. To test this hypothesis, 46 milk samples collected from 10 common marmosets (Callithrix jacchus, ca. 350 g) were assayed for dry matter (DM), crude protein (CP), fat, and sugar; and gross energy (GE) was calculated from these constituents. We also assayed five samples collected from three golden lion tamarins (Leontopithecus rosalia, ca. 700 g) and six samples collected from a single pygmy marmoset (Cebuella pygmaea, ca. 150 g) over two lactation periods. All samples were collected between days 10 and 57 post partum, representing mid lactation for these species. The milks of these three species were similar, containing 14.0%, 16.1%, and 13.7% DM; 2.7%, 2.6%, and 2.9% CP; 3.6%, 5.2%, and 3.7% fat; 7.4%, 7.2%, and 7.8% sugar; and 0.76, 0.90, and 0.82 kcal/g for common marmosets, golden lion tamarins, and the pygmy marmoset, respectively. These species produced milks with energy values that were within the range reported for large anthropoids, albeit with slightly higher protein concentration. However, milk composition did vary substantially among individual common marmoset females, especially in the proportion of milk energy derived from fat. In contrast, CP as expressed as a percent of GE was remarkably constant among common marmoset females. Callitrichid milk appeared to be similar to that of larger anthropoid primates in GE, but was higher in CP and in the proportion of GE from CP. However, the small sample sizes for the golden lion tamarin and the pygmy marmoset, and the wide variation in milk composition found among common marmoset females cautions against definitively characterizing the milks of callitrichids from these data.     

Species and subspecies specificity in urine and scent marks of saddle-back tamarins (Saguinus fuscicollis)

Saguinus fuscicollisproduces scent marks which consist mainly of a mixture of urine and the secretions of circumgenital scent glands. The present study investigates the ability of saddle-back tamarins to discriminate between scent material from conspecifics and corresponding material from other species and to differentiate material from two subspecies of Saguinus fuscicollis.When choices between urine samples from conspecifics and from guinea pigs and choices between urine samples from conspecifics and from common marmosets were offered, the tamarins investigated samples from conspecifics more frequently. Similar responses were obtained when choices between scent marks from saddle-back tamarins and from common marmosets and between scent marks from saddle-back and red-chested moustached tamarins were offered. The tamarins also discriminated between scent marks and between extracts of scent marks from Saguinus f. fuscicollisand Saguinus f. illigeri.In these choice tests, subjects of both subspecies tended preferentially to investigate material from Saguinus f. fuscicollis.The results of these studies show that urine and scent marks contain chemical cues on which recognition of conspecifics can be based. Moreover, the scent marks of closely related subspecies also offer cues which could enable the tamarins to discriminate between them.     

Use of a radioimmunoassay technique to measure the titer of anti-cow-zona antibodies in marmoset monkeys

A double antibody radioimmunoassay technique is described for the measurement of anti-zona antibodies in the peripheral plasma of marmosets actively immunized against intact cow zonae pellucidae. The method has been shown to be a reliable, repeatable indicator of antibody titer, enabling direct comparison of the response obtained between marmosets. This is the first report of a procedure describing the active immunization of a primate against zona antigens, and the first time a radioimmunoassay technique has been used to monitor profiles of anti-cow zona antibody production following active immunization. The method should prove to be a useful tool in the evaluation of zona antigens as agents for immunocontraception.     

Social enrichment of the environment with infants for singly caged adult rhesus monkeys

The practicability of social enrichment for singly caged adult rhesus monkeys was examined. Twenty-nine weaned rhesus monkey infants were removed from breeding troops to avoid overcrowding and were placed with unfamiliar singly caged adults. An adult-infant pair was considered compatible when (1) the two animals started huddling with each other within the first 5 days after pair formation and (2) the infant showed no signs of depression and took its share from a limited amount of favored food. Adult-infant pairs were compatible in 90% (26/29) of cases. Compatibility depended neither on the sex, age, and origin of the adult nor on the sex of the infant. There was no evidence that partners lost interest in each other during 7–11 months of follow-up observations. Three adults exhibiting stereotypical behavior abandoned their peculiar habits after they had lived with their young companions for 4 months. It was concluded that the often-heard notion that rhesus monkeys are highly aggressive should not prevent simple attempts to provide singly caged animals with a companion.     

Breeding of the cotton-top tamarin Saguinus oedipus oedipus: A comparison with the common marmoset

A colony experienced in the successful breeding of thecommon marmoset acquired 15 cotton-top tamarins for breeding purposes over a period of 2 yrs. Data are presented on the breeding of the cotton-top and compared with the breeding of the common marmoset. The tamarins did not breed as successfully as the common marmosets. There were several reasons for this: Cotton-tops took longer to produce young on initial pairing, had a longer birth interval, and showed a high incidence of suspected infanticide and parental neglect. These factors are thought to be largely responsible for the relatively low reproductive potential of the cotton-top in captivity.     

Physical Environmental Effects on Infant Care and Development in Captive Callithrix jacchus

Environmental enrichment may affect infant care and development in captive primates. We investigated the effects of this factor in laboratory common marmosets (Callithrix jacchus). An enriched physical environment enhanced the social activities of the marmosets and elicited a greater repertoire of behaviors, without negatively affecting the provision of infant care. In addition, infants in enriched cages displayed certain behaviors sooner than infants in non-enriched cages did, which suggests an increased developmental rate. Infants in enriched cages also ate more solid food and engaged in solitary play and exploration more than ones in non-enriched cages did. Play and exploration probably improve spatial cognition and motor skills, which, together with a higher degree of independence, may allow infants to cope better with laboratory routines and general social interactions later in life than their counterparts reared in less complex enclosures. We conclude that laboratories can significantly increase the welfare of marmosets by providing a more complex physical environment.     

Age differences in neophilia, exploration, and innovation in family groups of callitrichid monkeys

The prevailing assumption in the primate literature is that young or juvenile primates are more innovative than adult individuals. This innovative tendency among the young is frequently thought to be a consequence, or side effect, of their increased rates of exploration and play. Conversely, Reader and Laland's [International Journal of Primatology 22:787-806, 2001] review of the primate innovation literature noted a greater reported incidence of innovation in adults than nonadults, which they interpreted as (in part) a reflection of the greater experience and competence of older individuals. Within callitrichids there is contradictory evidence for age differences in response to novel objects, foods, and foraging tasks. By presenting novel extractive foraging tasks to family groups of callitrichid monkeys in zoos, we examined, in a large sample, whether there are positive or negative relationships of age with neophilia, exploration, and innovation, and whether play or experience most facilitates innovation. The results indicate that exploration and innovation (but not neophilia) are positively correlated with age, perhaps reflecting adults' greater manipulative competence. To the extent that there was evidence for play in younger individuals, it did not appear to contribute to innovation. The implications of these findings for the fields of innovation and conservation through reintroduction are considered.     

Cutting costs in response to predatory threat by Geoffroy's marmosets (Callithrix geoffroyi)

Ideally, prey should respond to their predators efficiently, without over- or underreacting to the threat. This may be particularly important for small-bodied species for whom metabolic demands are high and predatory risk is great. In the current study, two family groups of Callithrix geoffroyi living outside in a rural setting at the Center for Reproduction of Endangered Species, San Diego Wild Animal Park, were observed before, during, and after ten presentations of a great horned owl model. The owl was mounted on a post on a nearby hillside, simulating a situation in which a real but nonimminent threat is posed. As controls, a model of a crow and a cloth bag were also presented, each for ten trials. During the 10 min presentations of the owl, rates of play and foraging decreased, and rates of locomotion and vigilant looking increased from baseline rates. Data on occupation of the best viewing area suggest that the marmosets shared the job of monitoring a potential threat. After the owl was removed, behavior quickly returned to baseline rates, with the exception of looking at the place where the owl had been, and play. Neither the bag nor the crow generated significant differences from the baseline condition that preceded it. Marmosets may reduce the costs of antipredator behavior by appropriately assessing the degree of risk and by quickly resuming important activities once a potential threat has passed. Am. J. Primatol. 46:187–196, 1998. © 1998 Wiley-Liss, Inc.     

Social context affects phee call production by nonreproductive common marmosets (Callithrix jacchus)

Common marmosets produce two variants of their long call (phee call) in different situations. Intergroup calls are produced in territorial situations, and intragroup separation calls are produced by marmosets isolated from group members. Marmoset groups frequently include postpubertal, nonreproductive members; their roles in the spontaneous production of territorial vocalizations is unclear. This study analyzed the production of home cage phee calls by nonreproductive, postpubertal marmosets while they were housed in their natal groups and after pairing with an opposite-sex conspecific. Additionally, the production of the separation phee call variant was assessed in both social conditions. The results indicated that the marmosets rarely produced home cage, or territorial, phee calls while they were natally housed. In contrast, both males and females produced the territorial phee call at a much higher rate as early as 4 days after pairing. Age-matched females remaining in their natal groups throughout the study produced home cage phee calls infrequently. Most marmosets produced separation phee calls at a high rate after separation from either their natal group or a partner, suggesting that the makeup of a social group has little effect on an animal's motivation to reunite with conspecifics. These results suggest that the social environment has an important influence on the production of territorial phee calls. Am. J. Primatol. 43:135–146, 1997. © 1997 Wiley-Liss, Inc.     

Opportunistic predation on birds trapped in mist nets in two areas in the Atlantic Forest of southeastern Brazil

Mist netting is the most popular method for capturing birds, but it can increase the predation rates of individuals trapped in the nets. From 2008 to 2017, we recorded eight instances of opportunistic bird predation from mist nets (MNs) in a matrix mixing restored forest and fragments of semideciduous seasonal forest in southeastern Brazil, three times (37.5%) by exotic primates and five times (62.5%) by birds of prey. Overall predation rates (1.17–1.20%) at these two sites were considered high but were lower than in other Brazilian studies. Placing MNs near the edges of forest fragments may have allowed attacks by either forest predators or marmosets, which are exotic edge species. Some previously described precautions may decrease the predation rates of birds in MNs, such as shorter observation intervals, greater attention to given site selection and maintaining a safe distance between the MNs and the ground.