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.     

Influence of availability of perches on the behavioral well-being of captive,group-living mangabeys

Environmental enrichment is expected to increase the well-being of animals. Changes in well-being can be measured by variations in behavioral patterns. This study reports on behavioral changes induced, in arboreal monkeys, by progressively increasing the number of perches, from none to five, in an “experimental cage.” A cage equipped with five perches was used as the control cage. The behaviors of a group of seven gray-cheeked mangabeys in the control cage and in the “experimental” cage were compared. A total deprivation of perches yielded an increase in aggressive behaviors and locomotion, and a decrease in cohesiveness. Placing perches progressively in the experimental cage restored the level of all the variables to levels found in the control cage. This restoration to control levels actually occurred only when the number of perches in the experimental cage was close or equal to that in the control cage. Therefore perches constitute a necessary feature of an adequate environment for mangabeys. We suggest that this restoration is a consequence of providing appropriate structure of the utilizable space for the monkeys. This structure might increase the control and the predictability that monkeys should have over social events. © 1996 Wiley-Liss, Inc.     

Contrasting effects of living in heterosexual pairs and mixed groups on the structure of social attraction in squirrel monkeys (Saimiri).

The structure of social attraction was assessed in pair- and group-living squirrel monkeys (Saimiri) using paired-comparison and single-stimulus preference tests. Effects of the social environment were most prominent in females. Females housed with a single male showed sharply increased attraction to like-sex strangers and less pronounced increase in attraction to opposite-sex strangers, as compared to group-living females. Differences between pair- and group-living males were in the same direction found with females, but less extreme. Most group-living monkeys strongly preferred familiar animals to strangers regardless of sex, and like-sex to opposite-sex familiars. Change in the structure of social attractions in response to variations in the composition of the social environment appears to be an important factor in the maintenance of the species-typical grouping pattern in the squirrel monkey.     

Androgen resistance in squirrel monkeys (Saimiri spp.)

The goal of this study was to understand the basis for high androgen levels in squirrel monkeys (Saimiri spp.). Mass spectrometry was used to analyze serum testosterone, androstenedione, and dihydrotestosterone of male squirrel monkeys during the nonbreeding (n = 7) and breeding (n = 10) seasons. All hormone levels were elevated compared with those of humans, even during the nonbreeding season; the highest levels occurred during the breeding season. The ratio of testosterone to dihydrotestosterone in squirrel monkeys is high during the breeding season compared to man. Squirrel monkeys may have high testosterone to compensate for inefficient metabolism to dihydrotestosterone. We also investigated whether squirrel monkeys have high androgens to compensate for low-activity androgen receptors (AR). The response to dihydrotestosterone in squirrel monkey cells transfected with AR and AR-responsive reporter plasmids was 4-fold, compared with 28-fold in human cells. This result was not due to overexpression of cellular FKBP51, which causes glucocorticoid and progestin resistance in squirrel monkeys, because overexpression of FKBP51 had no effect on dihydrotestosterone-stimulated reporter activity in a human fibroblast cell line. To test whether the inherently low levels of FKBP52 in squirrel monkeys contribute to androgen insensitivity, squirrel monkey cells were transfected with an AR expression plasmid, an AR-responsive reporter plasmid, and a plasmid expressing FKBP52. Expression of FKBP52 decreased the EC50 or increased the maximal response to dihydrotestosterone. Therefore, the high androgen levels in squirrel monkeys likely compensate for their relatively low 5 alpha-reductase activity during the breeding season and AR insensitivity resulting from low cellular levels of FKBP52.     

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.     

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.     

Hormonal and behavioral changes at puberty in the squirrel monkey

Developmental changes in the reproductive behavior and physiology of 9 male and 15 female juvenile squirrel monkeys were evaluated in a 20-month study. Plasma levels of gonadal steroids remained relatively low for this species until most animals reached puberty between 2.5 and 3 years of age. Longitudinal assessment of plasma progesterone levels indicated that the onset of ovarian cycles tended to be synchronized between females although the 5 heaviest females began to cycle earlier than the rest. The heavier females reached puberty at a time which was appropriate to their birth in the wild, whereas most of the remaining females conceived 6 months later during a second period of reproductive activity that coincided with the laboratory mating season. Pubescent males underwent their first seasonal elevation in plasma testosterone levels during the second period and its onset was synchronized across all males. Thus, even in the absence of adults, pubertal processes in the squirrel monkey were strongly influenced by the seasonal breeding pattern. In addition, behavioral observations revealed that social maturation closely parallels reproductive ability in females, whereas males enter a protracted subadult stage after puberty.     

Progesterone as a predictor of cyclicity in Bolivian squirrel monkeys during the breeding season

In a squirrel monkey breeding colony, two distinct groups of females were observed during the breeding season, December through March. One had low and the other had high estradiol (E2) and progesterone (P) concentrations. The conception rate in females with high E2 and P values was 74%. However, only 25% of monkeys with low steroid concentrations became pregnant during the breeding season. This study showed that all mature females in a colony may not be cycling concurrently and that two serum P measurements obtained at four-day intervals may be utilized to detect noncycling monkeys during the breeding season.     

Mating-related estradiol fluctuations during the estrous cycle of the Bolivian squirrel monkey (Saimiri boliviensis boliviensis)

The female squirrel monkey, Saimiri boliviensis, a New World monkey, has 10-day estrous cycles during the annual breeding season. Measurements of serum estradiol (E) concentrations in females housed with males in breeding pens revealed markedly higher levels than previously reported. Additionally, females in breeding pens appeared to have two distinct patterns of serum E peaks relative to the LH surge. Serum estrogen peaks averaging 5-fold greater than levels on the preceding day were observed on the same day as the LH surge, whereas other females had only a small E rise on the day of the LH surge followed by a 6-fold E rise on the next day. The serum progesterone (P) levels in all animals were depressed for 1-2 days before the LH surge but frequently started to rise on the day of the LH surge. The effect of the presence of a breeding male was examined by studying females housed in a group pen without exposure to a breeding male. In contrast to breeding-pen patterns, relatively small E rises were found in the 10 cycles observed. To further elucidate estrus-related E rises, a limited male-access paradigm was used to isolate mating-related hormone fluctuations. Pre-mating E levels had no marked rises; however, 4 h after mating, whether on the day of the LH surge or the next day, large E rises were found. These studies indicate that the LH surge in cycling squirrel monkeys is consistently preceded by a marked P nadir and associated with relatively small E rises.(ABSTRACT TRUNCATED AT 250 WORDS)     

Annual cyclicity in the squirrel monkey (Saimiri sciureus): The relationship between testosterone, fatting, and sexual behavior

The relationship between seasonal sexual activity, endogenous testosterone, and weight changes (fatting) in the squirrel monkey (Saimiri sciureus) was assessed. Adult males were shown to have an annual rhythm in testosterone levels which coincides with peak sexual activity. Fatting was shown to occur in both adult males and adult females seasonally. However, fatting preceded both heightened sexual activity and increases in endogenous testosterone concentrations. In addition the frequency of eating and drinking do not show a consistent correlation with weight change in males and females. Therefore, the seasonal fatting response in squirrel monkeys must be due to mechanisms other than altered rate of consumption or increased production of testosterone.     

Variation in age at puberty in monkeys.

5 female and 3 male patas monkeys and 6 female and 3 male talapoin monkeys matured in a captive breeding colony. Age at puberty is given, and some variation discussed. The talapoin, a very small monkey, becomes adult at 4 1/2 years for females, 1 or 2 years later for males. The patas, a rather large monkey, becomes adult at 2 1/2 years, for females, and 1 or 2 years later for males. Both these ages for puberty differ from data for the rhesus monkey which has been accepted as generalizable to all Old World monkeys. Possible causes of differences between species in average age at puberty are discussed, including nutrition, environmental inconstancy, and relative size of infant and mother. It is suggested that age at first conception, a biologically more relevant index than menarche, should be considered as a potentially important adaptive variable when describing primate species.     

Factors influencing perch selection by communally roosting Turkey Vultures

ABSTRACT Many birds roost communally during at least part of their annual cycle, suggesting that for them the advantages of living in a group outweigh the disadvantages. However, perch sites within a roost may vary in quality because of differences in degree of exposure to the elements, predators, and fecal droppings. Individuals should select perches in the roost that minimize costs while enabling them to experience the benefits of communal roosting. We studied communally roosting Turkey Vultures (Cathartes aura) in northeastern Iowa (USA) from late August to mid‐October, when hatching‐year (HY) birds had joined the roost and were distinguishable from after‐hatching‐year (AHY) birds. On 82 d during our 4‐yr study (2004–2007), we noted the age class and perch position of vultures on two communication towers used as a preroost site. Perches used by vultures were classified as top‐level (with no perches above them) or lower‐level (with other perches above them). Top‐level perches were preferred by Turkey Vultures. Of 1713 birds recorded, 71% were on top‐level perches, even though only 39% of available perches were top‐level. Vultures did not use lower perches if top perches on that tower were unoccupied. The percentage of birds using lower perches increased as the number of vultures present increased, suggesting that top‐level perches were occupied first. AHY birds used top‐level perches more often than expected and HY birds used top‐level perches less often than expected, implying that age‐related dominance affected perch selection. On 61 of 82 d (74%), top‐level perches of both towers were occupied and, on 8 d (10%), only top perches on one tower were occupied. However, on 13 d (16%), both top‐level and lower‐level perches were occupied on one tower while no vultures perched on the other tower, suggesting that social attraction to other vultures can override a general preference for top‐level perches. Thus, our results provide evidence that social attraction, age‐related dominance, and preference for higher perches are proximate factors influencing perch selection in communally roosting Turkey Vultures. Ultimate factors that may be responsible for Turkey Vultures preferring higher roosting perches are reduced risk of predation, less exposure to fecal droppings that might reduce their plumage quality, and better visual information for locating food sources.     

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.     

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.     

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.     

Effects of reproductive state on vocalizations in squirrel monkeys (Saimiri sciureus)

Vocalizations and behavior of a group of 6 squirrel monkeys, 2 males and 4 females, were recorded during the nonbreeding and breeding seasons. Behavioral and physical criteria were used to determine the presence of estrus. During the breeding season the types of vocalizations uttered by estrous females changed, and the adult male increased his rate of vocalizing. Err vocalizations by estrous females were associated with increased following and initiation of affiliative behavior with the adult male, and may have functioned to facilitate these interactions. Errs appeared to be related to changes in female reproductive state rather than to the behavior of others. The adult male increased vocalizations associated with sexual and aggressive behavior (squeals and cackles), primarily in response to the estrous females' persistent initiation of interactions with him. We concluded that certain vocalizations in Saimiri reflected changes in the reproductive state of males and females, and functioned to mediate changes in social bonding during the breeding season.     

Sleep quantitation in common marmoset, cotton top tamarin and squirrel monkey by non-invasive actigraphy

Sleep quantitation data on the Neotropical primate species, apart from the squirrel monkey, are still sparse. As such, we have quantitated sleep in the common marmosets (Callithrix jacchus), cotton top tamarins (Saguinus oedipus) and squirrel monkeys (Saimiri sciureus) reared in one primate facility simultaneously, by non-invasive actigraphy. The range in total sleep time/24h measured for male adult common marmosets, cotton top tamarins and squirrel monkeys were 713-793 min (n=4), 707-889 min (n=4) and 459-475 min (n=2) respectively. The range in sleep episode length /12h dark phase for marmosets, tamarins and squirrel monkeys were 21-52 min (n=3), 10-28 min (n=4) and 9-15 min (n=2) respectively. Since vigilance is a critical evolutionary adaptive feature of predator avoidance among Callitrichid monkeys and squirrel monkeys, the shorter ranges in sleep episode length recorded, even under captivity, in this study could be interpreted as probable indicators of such vigilance behavior during the rest phase. We hypothesize that the vigilance behavior when it exists during a primate's active phase should also prevail when it is at rest (sleep). This hypothesis deserves additional testing in female Callitrichid monkeys.     

Behavioral research in breeding colonies of Old World monkeys.

The existence of an active behavioral research program using animals in primate breeding colonies was considered to be not only a compatable multiple use of animals, but a way of materially improving the management and efficiency of the breeding colonies. In colonies of monkeys specifically established for behavioral research programs directed at the examination of social relationships, incidental breeding resulted in levels of reproductive success equivalent to or greater than that normally experienced in colonies devoted entirely to breeding. Behavioral research revealed patterns of seasonality, fostering, kidnapping, and infant care which would otherwise have escaped notice and which would significantly influence culling and management choices in a breeding colony. Many young males and certain low ranking adult males actively contributed to reproduction. Females born and reared in the colonies were the most productive, exceeding wild born or other introduced females in reproductive efficiency. Specific recommendations for establishing, expanding and culling of nonhuman primate breeding colonies were derived from the behavioral research.     

Annual physiological changes in individually housed squirrel monkeys (Saimiri sciureus)

This study investigated whether annual changes in physiology occur in individually housed squirrel monkeys (Saimiri sciureus). Physiological measures were monitored for 20 months. Over the course of the study, all individually housed males and females exhibited clear annual changes in gonadal and adrenal hormone levels, and males exhibited species‐typical changes in body weight. Females exhibited a typical pattern of hormonal changes, with elevations in gonadal steroids occurring during the same months as elevations in cortisol. Males, however, exhibited an atypical pattern, as elevations in hormone levels were not synchronized with each other; rather, elevations in testosterone occurred out of phase with changes in cortisol and body weight. The timing of annual events in individually housed subjects was compared to that in nearby social groups, in which the timing of the breeding season from year to year was determined by social group formations and was outside the naturally occurring breeding season. Elevations of ovarian and adrenocortical hormones in individually housed females were synchronized with indices of breeding in heterosexual social groups. Similarly, weight gain in males was associated with elevations in cortisol and, as with socially housed males, tended to precede seasonal breeding in the social groups. In contrast, annual testosterone elevations for individually housed males were not synchronized with breeding in nearby social groups. We conclude that direct physical interaction is not required for the annual expression of breeding readiness. Synchrony of seasonality among squirrel monkeys may be accomplished by distant social cues in females, but males may require physical interaction for complete synchrony of annual physiological changes. Am. J. Primatol. 47:93–103, 1999. © 1999 Wiley‐Liss, Inc.