Male behavior through the breeding season in Saimiri boliviensis boliviensis

The Bolivian squirrel monkey (Saimiri boliviensis boliviensis) is a seasonal breeder. Male squirrel monkeys show distinct morphological and behavioral changes prior to and during the breeding season. A “fatting syndrome” includes increased body weight, increased levels of androgens, and in the Bolivian subspecies, an increasingly active role in the social organization of the group. In this study, the behavior of ten adult male Bolivian squirrel monkeys was analyzed over a 6-month period prior to, during, and after the breeding season. Each was housed as the only adult male in a breeding unit with six to ten adult females and one juvenile male. Employing a principle components method, 11 behavioral clusters were generated from 27 responses. Their activity clusters were identified as follows: sexual activity that showed a peak around the time of peak conceptions; excitatory activity that was initially high but decreased throughout the breeding season; and maintenance activity that did not change across the breeding season. The changing social behavior of the male squirrel monkey parallels physiological changes and is correlated with changing androgen levels.     

Phenotypic and Functional Characterization of Lymphocytes from Different Age Groups of Bolivian Squirrel Monkeys (Saimiri boliviensis boliviensis)

Due to many physiological and genetic characteristic similarities to humans, squirrel monkeys provide an ideal animal model specifically for studying malaria, and transmissible spongiform encephalopathies (Creutzfeldt-Jacob disease). While squirrel monkeys three years and older are generally considered adult subjects suitable for use in medical research studies, little is known about the functional properties of lymphocytes in relation to the age of these animals, which could significantly impact the quality and quantity of innate and adaptive immune responses. In this study, we investigated differences in the phenotype and function of lymphocytes subsets of young (3–4 years), adult (8–10 years) and aged (16–19 years) squirrel monkeys. In general, animals in all three age groups exhibited comparable numbers of different lymphocyte subsets except for CD20+ B cells that were significantly lower in aged relative to young animals and T cells subsets expressing both CD4 and CD8 (double positive) were significantly higher in aged relative to young animals. With increasing age, phenotypic differences in central and effector memory T cells subsets were observed, that were more pronounced for the CD8+ T cells. Despite equal proportions of CD3+ T cells among the three age groups, responses of peripheral blood mononuclear cells to T cell mitogens PHA and Con A showed lower IFN-γ producing cells in the aged group than that in the young group. Furthermore, aged animals showed significantly higher plasma levels of inflammatory cytokines IL-6, IFN-γ, TNF-α, IL-10 and IL-12. These findings suggest that while the squirrel monkeys in general share phenotypic and functional similarities of lymphocyte subsets with humans in relation to age, specific differences exist in immune function of lymphocytes between young and old animals that could potentially impact experimental outcomes for which the measurement of immunologic endpoints are critical.     

Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus apella): Developmental and comparative aspects

Adult capuchin monkeys use precision grips during manipulation of small objects, although their thumbs have been classified as pseudo-opposable. We investigated the physical properties of the hands to increase our understanding of manual function in capuchins. Forelimb dimensions and joint mobility (goniometric) measurements were obtained from adult, juvenile, and infant tufted capuchins (Cebus apella). Compared to adult squirrel monkeys, adult capuchins exhibited less flexibility of the wrist and digits. Capuchins of all ages had proportionally longer hands than squirrel monkeys, and capuchins more than 7 weeks old had proportionally longer thumbs than squirrel monkeys. Growth of the arms and hands was asynchronous. The duration of growth of the thumb was particularly prolonged, extending into early adulthood. Age-related changes in flexibility were apparent in most indices, and were greatest at the metacarpophalangeal joints. It is unknown to what extent the characteristics of growth, forelimb dimensions, and goniometry presented by capuchins are shared with other species, or if they contribute to the capuchin's unusual prehensive capacities. However, the marked differences between adult capuchins and squirrel monkeys in these metrics, and between capuchins and rhesus in the growth patterns of the digits, suggest that variation across taxa in these characteristics can be considerable.     

Cage design and configuration for an arboreal species of primate

The squirrel monkey (genus Saimiri) is an arboreal primate from equatorial South America. This species forms large social groups that consist of multiple females and males of varying ages, from infant to adult. As the use of squirrel monkeys in research continues to grow, an understanding of optimal cage design and environment is essential. The University of South Alabama Primate Research Laboratory houses a breeding colony of 350 squirrel monkeys. Each group cage, measuring 4.5 X 2.5 X 1.5 meters, can contain up to 20 animals. A breeding group consists of one adult male, eight to ten adult females, and varying numbers of infant and juvenile animals. In order to determine the most suitable cage environment for the squirrel monkey, a series of studies were carried out to compare various perch materials and cage configurations. Squirrel monkeys preferred a poly-vinyl-chloride pipe perch (rigid) over rope perches (non-rigid). When provided with multiple levels of perches, all levels were used. Males tended to distribute their activities randomly at different levels. In a two tiered perch arrangement, females concentrated 67% of their social activity on the top tier. In a triple tier configuration, females concentrated 66% of their travel on the top tier. These results indicate that by creating a cage environment with multiple tiers of horizontal perches the effective cage space can be doubled or tripled. This provides an effective means of reducing population density without enlarging the dimensions of the cage or reducing social group size.     

A comparative analysis of subgroup structure and spatial relationships in captive baboons and squirrel monkeys

Subgroup structure, spacing patterns, and the relationship between spatial and behavioral interations were compared for captive baboons and squirrel monkeys. Analysis of the structure, intensity, and permanence of subgroups revealed that the baboons formed low intensity, overlapping subgroups which were relatively flexible while the squirrel monkeys segregated into permanent, high intensity, mutually exclusive cliques. Clique associations and social proximity relationships were found to be better predictors than dominance rank of the nature and frequency of behavioral interactions in the two colonies.     

Experimental analysis of the nature of social context in captive groups of squirrel monkeys (Saimiri sciureus)

The nature of social context as a factor affecting grouping behavior is experimentally examined in captive groups of squirrel monkeys by recording the effects of systematic removal and return of individuals on the distributions of non-agonistic interactions and prolonged (huddle) contacts among the remaining group members. Observed changes in the distributions of these interactions among the remaining individuals are analyzed in terms of the age-sex class of the individual(s) removed, age-sex distributions of the individuals remaining, and the classes of dyadic relationships severed by the removals. Results indicate that, at least so far as these spacing-related behaviors are concerned, (1) the social environment does not act as a configurational whole on the grouping behavior of individuals, (2) the effect of social context on grouping behavior may be analyzed as the effects of specific dyadic relationships upon others, and (3) not all dyadic relationships significantly affect all others in a social group, i.e., not all of the social environment is relevant to the interactions between all pairs of individuals.     

Social organization and social behavior in two subspecies of squirrel monkeys (Saimiri sciureus).

Social organization and social behavior were examined in two subspecies of squirrel monkeys which differ markedly in the degree of sexual dimorphism. The Bolivian squirrel monkeys, the subspecies with greater sexual dimorphism, manifested a sexually segregated form of social organization, while the social organization of the Guyanese monkeys was sexually integrated. Dominance relationships were found to reflect these patterns of sexual segregation or integration; in the Bolivian social groups separate linear dominance hierarchies were established within each sex while the Guyanese monkeys established a single linear hierarchy which included both males and females. Relationships between males and females in the two subspecies appear to be regulated by two distinct mechanisms, dominance in the Guyanese monkeys and sexual segregation in the Bolivians.     

Age differences and developmental trends in alarm peep responses by squirrel monkeys (Saimiri sciureus)

Alarm calls can code for different classes of predators or different types of predatory threat. Acoustic information can also encode the urgency of threat through variations in acoustic features within specific alarm call types. Squirrel monkeys (Saimiri sciureus) produce an alarm call, known as the alarm peep, in highly threatening situations. Infant squirrel monkeys appear to have an innate predisposition to respond to alarm peeps but require experience to associate alarm peeps with the appropriate type of predatory threat [Herzog & Hopf, American Journal of Primatology 7:99-106, 1984]. Little is known about age-related differences in the type or frequency of response to alarm peeps, or the development of alarm peep response in infants. The purpose of this study was to test experimentally the response strategies of different age classes of squirrel monkey to the playback of alarm peeps that were produced by infants, juveniles, or adults. Results suggest that infants, juveniles, and female subadults respond more frequently to alarm peeps than do adult females. Infant squirrel monkeys showed different behavioral strategies in response to alarm peeps as a function of age. Adult females differentiate between infant and adult alarm peeps by responding more frequently to the alarm peeps of adult females. These data demonstrate that squirrel monkeys use acoustic information to discern when to respond to the alarm peeps from conspecifics, and that infants gradually develop an adult-like response to alarm peeps over the first year of development.     

The role of play in social organization: Comparative observations on squirrel monkeys (Saimiri)

Various functional theories of play stress that social play is essential for the practice and learning of sex roles, dominance relationships, troop culture, integration of individuals into the troop structure, the control of aggression, etc. Data on squirrel monkeys (Saimiri) in natural environments indicate that social interaction and troop integration can develop in various manners in the absence of social play.Comparative observations were made on squirrel monkeys in a seminatural environment in Florida and 43 natural environments in Panama, Colombia, Peru, and Brazil. There was a broad range of variance in the data on ecology, troop size, troop cohesiveness, average individual distances, frequency of play, etc. In some environments, individuals in the infant and juvenile age classes engaged in social play for approximately 1.5 to 3 hours a day. However, in one environment, not a single incidence of social play occurred during 261 hours of close range observation. The troops in which no play occurred were very cohesive (i.e., they seldom fragmented), and the animals traveled at close individual distances. Agonistic interactions were not uncontrolled. Copulations were observed; and 85 percent of the adult females were accompanied by infants, which indicates a normal rate of reproductive success for the species.Data are presented on friendly, aggressive, sexual, and spacing behavior in squirrel monkeys. These data indicate that (1) social play is not necessary for the development and/or learning of an adaptive modicum of social interaction patterns and troop cohesion, but (2) the opportunity to play provides learning experiences in which young animals can develop more complex, varied social interaction patterns and stronger habits for engaging in frequent social exchanges.     

Quantitative genetics of costly neonatal sexual size dimorphism in squirrel monkeys (Saimiri boliviensis)

Offspring size is often an intimate link between the fitness of parents and offspring. Among mammals, neonate mass is also related to adult levels of dimorphism and intrasexual competitive mating. We describe the sex‐specific genetic architecture of neonate mass in captive squirrel monkeys (Saimiri boliviensis), a small Neotropical primate. Best fitting quantitative genetic models show strong maternal genetic effects with little difference between sexes offering limited opportunity for neonatal dimorphism to respond to observed or hypothetical selection. Heritabilities that are approximately zero also imply it is unlikely that neonatal dimorphism can evolve as a correlated response to selection on adult size. However, male mass is also more dependent on maternal condition (age and parity) making dimorphism plastic. Finally, we hypothesize that large maternal genetic effects reflect income breeding and tightly synchronized seasonal reproduction in squirrel monkeys, both of which require strong maternal control of offspring growth and timing of birth.     

Postnatal changes of IgG and IgM levels in squirrel monkeys (Saimiri sciureus)

Serum IgG and IgM levels were measured in domestically bred squirrel monkeys (Saimiri sciureus) ranging in age from 0 days to 42 months, as well as in adult squirrel monkeys from the wild estimated to be 60 months or older. The results indicated that the transplacental transfer of IgG occurs in the squirrel monkey but the transferability is lower in the squirrel monkey than in the cynomolgus monkey. Immune response in the squirrel monkey occurs just after birth, as shown by IgM production.     

Sexual segregation and its ontogeny in squirrel monkey social structure

Four groups of squirrel monkeys were observed to determine the primary basis of adult group structure. These studies included observations on (1) intact and gonadectomized males and females during and after breeding; (2) intact adults only; (3) subadults only; and, (4) a mixed group of adults and subadults. The spatial distribution of subjects in each group was used as a basic measure of social organization. It was found that for adults, regardless of hormonal status, between-sex distances were consistently greater than within-sex distances. This sexually segregated adult structure was largely attributable to the females' attaction to one another and overt rejection of the males. Subadults by themselves did not show any clear sexual segregation. However, in the presence of an adult structure, the subadults gradually manifested the segregated pattern of the adults by gravitating toward same-sex adults. These results indicate that the socialization process, rather than endogenous hormonal status, is the major determinant of adult social structure in squirrel monkeys.     

Age related variation in male–male relationships in wild spider monkeys (Ateles geoffroyi yucatanensis)

In social organizations characterized by male philopatry, social relationships between males are argued to be the strongest. Little is known about the social relationships of philopatric male spider monkeys. To address this limitation, we investigated social relationships among individually recognized wild adult male spider monkeys from two well-habituated communities in the Yucatan Peninsula, Mexico, focusing on affiliative behaviors important in regulating male social relationships, including grooming, embracing, arm-wrapping, and grappling. We examined whether behaviors were reciprocated between male partners and whether age was a factor in how the behaviors were distributed or reciprocated, by examining differences between younger adult males (<10 years) and older adult males (≥14 years). Although we found evidence that affiliative behaviors were overall reciprocated between spider monkey adult males, there were pronounced differences in the interactions depending on their relative age. Reciprocation in grooming and embraces between same-age males suggests their relationships are valuable to both partners. Among different-age dyads, younger males gave more embraces than they received, were the initiators of grappling and arm-wrapped more often than with same-age males, suggesting relationships between younger and older males are more risky. This confirms that younger males are attracted to older males, probably because they value relationships with older males more than the reverse, but they are also at risk.     

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 context as a structuring mechanism in captive groups of squirrel monkeys (Saimiri sciureus)

Various classes of individuals were removed from three captive groups of squirrel monkeys and effects measured on the frequencies of nonagonistic interactions of the remaining individuals. Results indicated that there are regularities in the effects of certain classes of dyadic relationships on others which may be considered species-typical structuring mechanisms ofSaimiri social groups and which account for in consistencies which have appeared between experimentally identified social preferences of adults of this species and their actual behavior in social groups. A tentative process model ofSaimiri social structure and its seasonally changing character is presented and implications of this kind of analytical model for studies of evolution and adaptation are briefly discussed.     

Social grooming between squirrel monkeys and uakaris in a seminatural environment

Young squirrel monkeys (Saimiri sciureus) were reported grooming an adult female uakari (Cacajao calvus rubicundus) on four different occasions. Furthermore, the uakari was noted grooming two squirrel monkeys in separate instances. These observations took place in a seminatural rainforest (The Monkey Jungle; Goulds, Florida, U.S.A.) where provisions are provided. Some possible hypostheses tendered to account for this unusual behavior included (a) the unaverted interaction of food-seeking and fur-cleaning behavior, and (b) the compatibility of play-curiosity activities by squirrel monkeys with the uakaris' need for social contact.     

Enteric trichomonads of squirrel monkeys (Saimiri sp): Natural infestation and treatment

In a large breeding colony of squirrel monkeys, a previous study demonstrated apparent universal infestation of adult animals with enteric trichomonads. The potential of these organisms to act as a source of experimental variability and the potential pathogenic effects of parasitism in this species stimulated this study of organism acquisition and treatment. Age of natural infestation with trichomonads was determined from results of microscopic examination and culture of fecal samples from infants of different ages. A majority of squirrel monkey infants showed first evidence of trichomoniasis at 2 to 4 weeks of age, with apparent 100% infestation by 8 weeks of age. Treatment of adult monkeys was investigated. In vitro techniques were utilized to determine sensitivity to metronidazole of a number of isolates. An effective regimen for treatment of adult monkeys was determined to be 25 mg/kg body weight of metronidazole given orally, twice daily for 5 days.     

Population recognition of infant isolation peeps in the squirrel monkey

Infants from three populations of squirel monkeys with different pelage, behaviour patterns and physiological patterns emitted two forms of isolation peeps. Offspring from Peruvian and Bolivian stock produced isolation peeps previously described as belonging to ‘Roman Arch’ monkeys, whereas the Guyanese population produced isolation peeps previously described as belonging to ‘Gothic Arch’ monkeys. Playbacks of isolation peeps from, infants of each population to groups of adult monkeys revealed a population specificity in the response to infant calls. Peruvian, and Bolivian adults responded with increased activity, decreased huddling and increased approach to the speaker only when isolation peeps of Peruvian and Bolivian infants were broadcast. Guyanese adult monkeys showed similar responses to the isolation peeps of Guyanese infants. These are the first reported data indicating that the long-recognized vocal differences in squirrel monkey populations are responded to differentially. The results also support a major taxonomic division between the Gothic Arch and Roman Arch populations with the other morphological and physiological differences within these populations reflecting secondary divisions.     

Increased production of 11beta-hydroxysteroid dehydrogenase type 2 in the kidney microsomes of squirrel monkeys (Saimiri spp.)

In squirrel monkeys (Saimiri spp.), cortisol circulates at levels much higher than those seen in man and other Old World primates, but squirrel monkeys exhibit no physiologic signs of the mineralocorticoid effects of cortisol. These observations suggest that squirrel monkeys have mechanisms for protection of the mineralocorticoid receptor (MR) from these high levels of cortisol. We previously showed that the serum cortisol to cortisone ratio in these animals is low relative to that in human serum, suggesting that production of the MR protective enzyme, 11beta-hydroxysteroid dehydrogenase type 2 (11beta-HSD2), is increased in squirrel monkeys. Here, we directly evaluate whether increased production of 11beta-HSD2, which inactivates cortisol to cortisone, is a mechanism for protection of MR. In vitro assays showed that 11beta-HSD2 activity in squirrel monkey kidney microsomes was 3 to 7 times higher than that seen in kidney microsomes from pig or rabbit. 11beta-HSD2 protein detected by Western blot analysis was 4 to 9 times greater in squirrel monkey microsomes than in pig or rabbit microsomes. Comparison of the effect of expression of either human or squirrel monkey 11beta-HSD2 on MR transactivation activity showed similar inhibition of MR response to cortisol by both enzymes, indicating that the intrinsic activities of the human and squirrel monkey enzymes are similar. These findings suggest that one mechanism by which squirrel monkeys protect the MR from activation by high cortisol levels in the kidney is by upregulation of 11beta-HSD2 activity through increased production of the enzyme.     

Comparison of rectal and tympanic core body temperature measurement in adult Guyanese squirrel monkeys (Saimiri sciureus sciureus)

Background Measuring core body temperature in a manner that is safe for animals and veterinary personnel is an important part of a physical examination. For nonhuman primates, this can involve increased restraint, additional stress, as well as the use of anesthetics and their deleterious effects on body temperature measurements. The purpose of this study was to compare two non‐invasive methods of infrared tympanic thermometry to standard rectal thermometry in adult squirrel monkeys. Methods Tympanic temperatures were collected from 37 squirrel monkeys and compared to rectal temperatures using a human and veterinary infrared tympanic thermometer. Results Compared with rectal temperature measurements, the human tympanic thermometer readings were not significantly different, while the veterinary tympanic thermometer measurements were significantly higher (P < 0.05). There were no differences between sexes. Conclusions The tympanic thermometer designed for use in humans can be used in adult squirrel monkeys as an alternative to rectal thermometry for assessing core body temperature.