The influence of social cues on the reproductive endocrinology of male brown-headed cowbirds: field and laboratory studies

Captive male brown-headed cowbirds exposed to long days exhibit gonadal growth and have elevated plasma testosterone (T) levels. This photoperiodic response is enhanced if males are housed with female cowbirds: Photostimulated males with females increase plasma testosterone levels sooner than do individually housed photostimulated males. Peak plasma T levels are similar in both groups, although peak levels are maintained longer in males housed with females. The gonadal cycle is similarly affected; males in the presence of females have earlier gonadal recrudescence and maintain mature gonads longer than do photostimulated males without females. Plasma corticosterone levels increase in the unpaired males, suggesting that removal of social cues is stressful for these birds. Free-living paired males have significantly higher plasma testosterone levels than do unpaired/unknown males early in the season, when social relationships are being established; the levels are similar thereafter. There is no difference between the two groups in testicular maturation rates; nor do they differ in plasma corticosterone levels at any time of the season. These results suggest that social stimuli are important in modulating the secretion of testosterone in males early in the season when pairing occurs, and possibly late in the season as well, probably to prevent termination of breeding prior to that of females.     

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.     

Predictors of social status in cynomolgus monkeys (Macaca fascicularis) after group formation

The purpose of the present study was to determine whether various behavioral and hormonal markers obtained in individually housed monkeys would be predictive of social rank following group housing. Body weight, serum cortisol and testosterone levels, and locomotor activity in an open-field apparatus were examined in 20 experimentally naive male cynomolgus monkeys (Macaca fascicularis) while they were individually housed. It was hypothesized that eventual subordinate monkeys would have higher cortisol levels and increased locomotor activity scores. These monkeys were then placed in social groups of four (five pens of four monkeys), and social rank was determined based on outcomes of dyadic agonistic encounters. Body weight correlated significantly with eventual social rank. In general, the heavier the monkey the higher the social rank. Locomotor activity in an open-field apparatus following administration of a low dose of cocaine (0.01 mg/kg, i.v.), which has been shown to increase CNS dopamine, correlated with eventual social rank such that individually housed monkeys with high levels of locomotion were more likely to become subordinate. Serum cortisol and testosterone levels failed to correlate with eventual social rank. Hypothalamic-pituitary feedback sensitivity and adrenal responsiveness were examined by measuring cortisol levels after administration of dexamethasone and following ACTH challenge. Cortisol responses in these tests were not associated with eventual social rank. These results suggest that, in addition to body weight, the level of reactivity in a novel environment after administration of a low dose of cocaine is a potential trait marker for social rank. This trait is apparently not associated with hormone levels, but may involve other CNS mechanisms.     

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.     

Subspecies differences in hormonal and behavioral responses after group formation in squirrel monkeys

The behavioral and hormonal responses of squirrel monkeys of the Bolivian and Guyanese subspecies were compared after a group formation procedure. Two groups of each subspecies, consisting of five females and three males (later reduced to two) were observed daily during the week of group formation and for nine weeks following removal of a single male from each group. Measures of plasma cortisol were examined in the females after the initial group formation and after the groups were reduced by one male. The levels of plasma testosterone were assessed in all the males during the initial week of group formation. Linear dominance hierarchies were determined both within and across the sexes in both subspecies. The frequency and directionality of low-level aggressive interactions indicated that females of the Bolivian subspecies were dominant to the males, while the males of the Guyanese subspecies ranked over all the females. Additionally, the Bolivian squirrel monkey females showed an elevation of plasma cortisol on the day of group formation, which declined 48 hr later, then reelevated after the groups were reduced by one male and declined gradually over a nine-week period. Guyanese females showed little change in cortisol levels during both periods. This suggests fundamental hormonal, as well as behavioral, differences between the two subspecies. The change in plasma testosterone levels in the males during the initial week of group formation was positively correlated with social status. Furthermore, differences in the dynamics within individual groups for each subspecies were reflected by the levels of plasma cortisol of the female members.     

Seasonal weight changes in male rhesus monkeys (Macaca mulatta)

Adult male rhesus monkeys lose weight during the breeding season and regain it during the nonbreeding season. The annual pattern of maximum weight gain just prior to the onset of breeding resembles the seasonal “fattening” seen in squirrel monkeys, but the period of weight gain is less discrete. The magnitude of weight change is less in younger males, in that sexually immature males gain weight in both seasons, but significantly less during the breeding season. Females do not lose weight during the breeding season. Post hoc analyses revealed no significant correlations between male testosterone levels, dominance ranks, weights, or weight changes. The heaviest animals as juveniles were predictably the heaviest as adolescents. The timing of seasonal changes in testosterone did not correlate with the timing of changes in weight; weight losses followed the rise in testosterone, and weight gains continued until early in the breeding season after testosterone levels had already begun to rise. It is suggested that seasonal hormonal changes may influence activities in individuals and that changes in the activities of particular group members may alter the activity patterns of other group members. This alteration of activity patterns due to group influences on individuals as well as individual influences on the group may explain why hormonal regulation of seasonal weight appears to be indirect and why individuals (juveniles) experiencing no seasonal hormonal changes nonetheless show differences in activity patterns and seasonal weight changes.     

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.     

Presence of mother and unfamiliar female alters levels of testosterone,progesterone, cortisol,adrenocorticotropin, and behavior in maturing Guinea pigs

Although the guinea pig is characterized by precocial physical development and minimal active maternal care, studies suggest the presence of the mother can influence neuroendocrine and behavioral activity of offspring even well beyond weaning. Previous results may have been influenced by the procedure of housing weaned subjects with the mother to within 2 days of testing. The present study examined approximately 40-day-old guinea pigs housed apart from the mother for 0 (not rehoused), 2, or 10 days. Rehousing without the mother led to elevations in plasma testosterone (measured in males), progesterone (measured in females), cortisol, and adrenocorticotropin (ACTH) (both measured in males and females). Offspring housed without the mother for 10 days had the highest progesterone, cortisol, and ACTH levels. Testosterone elevations were observed in 2-day-, but not 10-day-, rehoused animals. Regardless of rehousing condition, 60 min isolation in a novel test cage elevated progesterone, cortisol, and ACTH, and reduced testosterone. These effects were all moderated if the subject was tested with the mother or another female. Sexual behavior toward the mother was observed frequently, but only in males housed apart from her prior to testing. Overall, males and females that had been housed apart from the mother interacted with her as they would an unfamiliar female. Our results corroborate previous findings, suggest the effect of housing apart from the mother on male testosterone is transitory, and indicate that continuous housing with the mother past weaning suppresses circulating progesterone in females and cortisol and ACTH in both sexes.     

Old,socially housed rhesus monkeys manipulate objects

Recent research has indicated that old, individually housed monkeys show little interest in novel objects. Yet unanswered is whether this effect is caused primarily by age or housing condition. The purpose of this study was to assess the role of social living in promoting responsiveness to objects. We measured the rates of object manipulation in older animals, assessed responsiveness over time to particular objects as a measure of habituation, and examined social influences on object use. Several social groups of rhesus monkeys that contained older adults were studied. These groups were housed in indoor pens or in an outdoor enclosure, and all monkeys had continuous access to a variety of objects in their home environment. In contrast to previous studies of individually housed monkeys, our group-housed monkeys showed sustained interest in objects. Old monkeys manipulated objects extensively, and this response was all the more significant, given that the objects were not novel. Monkeys housed in an outdoor enclosure showed object manipulation patterns that were not different from monkeys housed in indoor pens. However, females exhibited much higher object-related responses than males. Social facilitation played a role in the reactions of some monkeys to objects. Patterns of social facilitation as well as avoidance were present in two of the three indoor groups that were observed. Failure to manipulate objects in rhesus macaques appears to be more a function of individual housing than of old age. Factors such as environmental complexity, social needs, and early experience should be considered in order to understand why individually housed rhesus monkeys are unresponsive to objects. © 1993 Wiley-Liss, Inc.     

The development of seasonal variation in gonadal hormones and body weight in the maturing squirrel monkey

Captive-born squirrel monkeys of three different subtypes (Colombian, Bolivian, Peruvian), ranging in age from 1 to 4.5 years for males and 1 to 3.5 years for females, were examined at 3-month intervals throughout the year for seasonal changes in levels of plasma testosterone and progesterone and in body weight. Cyclical activity of testosterone in males began between 2 and 3 years of age but became more defined by the time the animals were 3–4 years old. Peak values occurred in February and May and corresponded to the the time of year in which adults normally mate. Elevations of progesterone occurred initially at approximately 2.5 years of age in February and May, and mainly infernales of the Colombian subtype. However,unlike levels of testosterone in males of this age, which declined in August and November (following the typical breeding season), levels of progesterone in females continued to increase during these months. Seasonal changes in body weight were also found in males but these changes were less evident than, and did not correlate with, hormonal changes.     

The reproductive status of nonbreeding group members in captive golden lion tamarin social groups

Reproductive activity is limited to only one female in many species of callitrichid primates (marmosets and tamarins): daughters and subordinate females do not produce offspring. A suppression of ovulatory cyclicity is responsible for the lack of reproductive activity in three species of callitrichids studied to date. This study evaluated the endocrine status of golden lion tamarins (Leontopithecus rosalia) housed as daughters or sons in family groups and of individuals housed in isosexual peer groups. Daughters 17 months of age and older and a subordinate female had high levels of estrogen excretion. Mean levels of estrogen excretion in these females were similar to those of nonpregnant, breeding adult females (17.14 ± 6.82 versus 11.93 ± 6.33 μg/mg creatinine, respectively). Estrogen profiles were similar to those of breeding adult females, with sinusoidal cycles in estrogen excretion. Younger daughters in family groups (10 and 12 months old) showed markedly lower levels of estrogen excretion (0.84 ± 0.58 μg/mg creatinine). Estrogen profiles lacked the sinusoidal nature of cycles in older daughters and breeding females, and elevations in estrogen excretion occurred frequently and remained elevated for 1 or 2 days. Plasma testosterone levels in males varied widely, but mean concentrations did not differ among males housed in different social conditions. These results suggest that older daughters and subordinate females may be capable of expressing normal ovarian function in the presence of a breeding adult female. This finding may account for two unusual observations in the lion tamarin: the high level of female-female aggression and the presence of groups in the wild with more than one actively breeding female.     

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.     

Testosterone production and spermatogenesis in free-ranging Eurasian lynx (Lynx lynx) throughout the year

Seasonal variation in reproduction is common in mammals as an adaptation to annual changes in the habitat. In lynx, male reproduction activity is of special interest because female lynxes are monoestric with an unusual narrow (about 1 month) breeding season. In Eurasian lynx, mating occurs between January and April depending on the latitude. To characterize the seasonal pattern of sperm and testosterone production in free-ranging Eurasian lynxes, long-term frozen-stored testis material obtained postmortem from 74 hunted or road-killed lynxes in Sweden was used to analyze annual changes in testis mass, testicular testosterone content, and spermatogenetic activity. Values of most gonadal parameters obtained in subadult lynxes were significantly different from the values observed in adult males. In adult lynxes, a moderate annual fluctuation of gonadal parameters was found which was most profound for testis weight and testicular testosterone concentration reaching highest values in March (median of 2.18 g and 2.67 μg/g tissue respectively). Grouping the data of pre-/breeding (January–April) and postbreeding season (May–September) revealed significant changes in testis weight and testosterone concentration. The relative spermatogenetic activity remained high in postbreeding testes. However, net sperm production decreased according to reduction of testis mass and a tendency to lower cauda epididymal sperm numbers in the postbreeding period was observed. Our results demonstrate that it is possible to analyze the gonadal activity of frozen testis/epididymis tissue postmortem and that male Eurasian lynxes show—opposite to the females—only moderate seasonal changes in their reproductive capacity.     

Diurnal and annual variation of adrenocortical activity in the squirrel monkey

Diurnal changes in basal cortisol levels and stress reactivity were assessed in male and female squirrel monkeys. Blood samples were collected at four-hour intervals throughout the day and night in the mating and nonmating seasons. Basal cortisol levels in females were similar in both seasons, but males tended to have higher cortisol levels during the mating season, especially at night. For both sexes, cortisol secretion was highest between 0400 and 0800 preceding the onset of the diurnal activity period. Assessment of cortisol responses following brief handling and anesthesia indicated that stress responses were relatively stable across the year, but cortisol increments were slightly higher in the nonmating season. Cortisol levels post-stress were generally related to prior baseline values. Thus, a knowledge of biorhythmic changes in basal hormone levels was important for predicting hormone levels after acute stressors. Males also underwent marked seasonal variation in their basal testosterone levels, which markedly altered the nature of their testosterone responses 30-minutes poststress. © 1995 Wiley-Liss, Inc.     

Hormonal correlates of dominance in meerkats (Suricata suricatta)

In cooperatively breeding meerkats (Suricata suricatta), individuals typically live in extended family groups in which the dominant male and female are the primary reproductives, while their offspring delay dispersal, seldom breed, and contribute to the care of subsequent litters. Here we investigate hormonal differences between dominants and subordinates by comparing plasma levels of luteinizing hormone (LH), estradiol and cortisol in females, and testosterone and cortisol in males, while controlling for potential confounding factors. In both sexes, hormone levels are correlated with age. In females, levels of sex hormone also vary with body weight and access to unrelated breeding partners in the same group: subordinates in groups containing unrelated males have higher levels of LH and estradiol than those in groups containing related males only. When these effects are controlled, there are no rank-related differences in circulating levels of LH among females or testosterone among males. However, dominant females show higher levels of circulating estradiol than subordinates. Dominant males and females also have significantly higher cortisol levels than subordinates. Hence, we found no evidence that the lower levels of plasma estradiol in subordinate females were associated with high levels of glucocorticoids. These results indicate that future studies need to control for the potentially confounding effects of age, body weight, and access to unrelated breeding partners before concluding that there are fundamental physiological differences between dominant and subordinate group members.     

Psychosocial and hormonal aspects of hierarchy formation in groups of male squirrel monkeys

Accounts of primate social dominance hierarchies often imply that the achievement of superior status is a “goal”, akin to a valued resource or commodity, and that hierarchies emerge in multimale groups from prolonged competitive conflicts over social status. This possibility is not consistent with our observations of five newly formed triads of adult male squirrel monkeys (Saimiri sciureus). Stable linear hierarchies based on clear asymmetries in the direction of intermale agonism and genital displays were established quickly, with virtually no reciprocal fighting, and in the absence of rank-related differences in plasma cortisol or testosterone. Although affiliative social overtures were initiated more often by high-ranking and middle-ranking males, affiliative overtures were directed equally often toward all members of each group. From the outset of the study all males, regardless of rank, spent an average of 33% of their time huddling in affiliative contact with male cagemates. These results suggest that in newly formed groups of adult male squirrel monkeys, social hierarchies reflect an expedient convention that reduces conflict and facilitates the formation of small cohesive groups. © 1994 Wiley-Liss, Inc.     

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)     

Squirrel monkey dominance and social behavior as related to group size and group structure

Adult male and female squirrel monkeys were tested in nonsocial adaptation and pairwise and triad social situations differing in sex composition. Social behaviors, nonsocial behaviors, and dominance hierarchies were observed during social testing. Dominance hierarchies were similar in groups differing in size and social structure. Nonsocial behaviors decreased in females and submissive animals paired with males or dominant monkeys. Aggressiveness between females decreased and the beginnings of coalitions between females were observed in the presence of a male. The social behavior patterns, but not dominance hierarchies, are consistent with behaviors observed in larger groups of squirrel monkeys.     

Social cues and hormone levels in male Octodon degus (Rodentia): a field test of the Challenge Hypothesis

Social interactions are important factors determining and regulating individual behaviors. Testosterone has been related to agonistic interactions, while glucocorticoids have been related to social stress, especially during interactions of dominance. We compared testosterone and cortisol concentrations in male degus (Octodon degus, Rodentia) under laboratory conditions without male social interactions, with data from wild males in nature. Under natural conditions, males should present higher levels of testosterone during the breeding season due to social interactions (Challenge Hypothesis). Alternatively, intense social instability could act as a stressing environment, raising glucocorticoids, which inhibit testosterone concentrations. Our results show a significant increase in agonistic interactions between males during the breeding season, and disappearance of non-agonistic male interactions during this period. Hormone levels in breeding season show nonsignificant differences between laboratory groups, but testosterone concentrations in field males were significantly higher than in laboratory males. Testosterone levels were similar among pre-breeding and breeding periods, but in field animals the concentration was approximately 30% higher than in laboratory degus. In field animals, we found two different mating strategies: resident males, with territorial behavior, and transient males, displayed an opportunistic approach to females. Finally, cortisol presents a similar pattern in both laboratory and field animals; pre-breeding values of cortisol are higher than during the breeding season. This suggests that social interactions in O. degus activate a rise in testosterone, supporting the Challenge Hypothesis, and could be considered as partial support of the Social Stress Hypothesis.     

The hormonal and behavioral response to group formation, seasonal changes, and restraint stress in the highly social Malayan Flying Fox (Pteropus vampyrus) and the less social Little Golden-mantled Flying Fox (Pteropus pumilus) (Chiroptera: Pteropodidae)

This study examined behavioral and physiological responses (changes in inter-animal spacing, total glucocorticoids, testosterone, and body mass) to the formation of breeding and same-sex groups in two bat species, the socially gregarious Malayan Flying Fox (Pteropus vampyrus) and the less social Little Golden-mantled Flying Fox (Pteropus pumilus). We hypothesized that social instability, especially in the breeding groups and especially in P. vampyrus, would result in elevated glucocorticoids and that social facilitation of breeding and/or male-male competition would result in persistently higher levels of testosterone in breeding males. Seasonal rhythms in all measures were also predicted, and the glucocorticoid stress response was expected to vary by sex, season, and group type. Nearly all animals responded to group formation with elevated glucocorticoids, but, for breeding animals (especially aggressive male P. vampyrus), these responses persisted over time. In both species, breeding group formation resulted in elevated testosterone in males. Glucocorticoids, testosterone, testes volume, and body mass generally peaked in the breeding season in males (late summer and early autumn), but the seasonal glucocorticoid peak in females occurred in late winter and early spring. All animals responded to restraint stress with elevations in glucocorticoids that largely did not differ by sex, time of year, reproductive condition, group type, or, in lactating females, the presence of her pup. Changes in both behavior and physiology were more evident in P. vampyrus than in P. pumilus, and we believe that their underlying social differences influenced their responses to group formation and to the changing seasonal environment.