Dispersal Status Influences Hormones and Behavior in the Male Spotted Hyena

Male spotted hyenas (Crocuta crocuta) reach puberty at 24 months of age and then invariably emigrate from their natal clans 1 to 38 months later. Thus there are two classes of reproductively mature males in everyCrocutaclan: adult natal males born in the clan and adult immigrant males born elsewhere. In one free-living hyena population in Kenya, these two groups of males were compared with respect to measures of aggression, social dominance, sexual behavior, and circulating hormone levels. Adult natal males engaged in higher hourly rates of aggression than did immigrants, won all fights with immigrants, and were socially dominant to immigrants. In addition, adult natal males engaged in far lower hourly rates of sexual behavior with resident females than did immigrants, and natal males were never observed to copulate with natal females. Mean basal plasma cortisol values did not differ between the two groups of adult males, but cortisol concentrations in immigrants were positively correlated with tenure in the clan and with immigrant male social rank. Adult natal males had plasma testosterone levels significantly lower than those of immigrants. Social rank and plasma testosterone values were positively correlated among immigrant males. Thus two different relationships appear to exist between circulating testosterone and social rank in maleCrocuta:one apparent in immigrants and the other in natal adult males. Our results suggest that dispersal might disinhibit testosterone secretion in postpubertal male hyenas.     

A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas

Urinary steroid hormone levels were measured in wild male mountain gorillas (Gorilla gorilla beringei) to determine how levels of testosterone and cortisol corresponded with age and social rank. Urine samples were collected noninvasively from 18 males, ranging in age from 3–26 years, in three groups of wild mountain gorillas at the Karisoke Research Center, Rwanda, Africa, and samples were analyzed using radioimmunoassay procedures. Males were classified as being immature (<7 years), maturing (10–13 years), or adult (+13 years of age). Immature males had significantly lower levels of testosterone and higher levels of cortisol than both maturing and adult males. No differences in testosterone or cortisol levels were found between maturing and adult males. Dominant males exhibited a trend toward significantly higher levels of testosterone than subordinate males, but no difference was found between cortisol levels of dominant and subordinate males. These results suggest that the increase in testosterone associated with puberty occurs prior to any outward sign of development of secondary sexual characteristics. Within-group male–male competition may affect testosterone levels, but the lack of difference in cortisol levels between dominant and subordinate males suggests that subordinate males are not socially stressed, at least as measured by cortisol. Am. J. Primatol. 43:51–64, 1997. © 1997 Wiley-Liss, Inc.     

Breeding site fidelity in penduline tit Remiz pendulinus in Southern Hungary

Birds move between breeding locations to gain a better territory, avoid competition or reduce the deleterious effect of inbreeding. We investigated breeding site fidelity in a small European passerine, the penduline tit (Remiz pendulinus). This species has an exceptionally diverse breeding system, in which both males and females may have up to 5–7 mates in a single breeding season, and the eggs are incubated by a single parent: either the male or the female. We investigated the movements of males and females within three breeding seasons in Southern Hungary (2002–2004). Males moved for shorter distances between breeding sites (116 m, 63–333 m; median, lower quartile–upper quartile) than females (942 m, 415–2,382 m). Movements of males and females were consistent between years, and they were repeatable between subsequent nests of males, but not of females. Taken together, our results suggest that adult male penduline tits are more site-faithful than adult females. We suggest that this difference has an implication on their breeding ecology since male parental behaviour (desert/care) is expected to be influenced by local mating opportunities, whilst female parental behaviour is likely to depend on the mating opportunities in a large area around their breeding site.     

Effect of long-term simulated microgravity on some sexual traits of male Japanese quail

The aim of this study was to investigate the effects of long-term stay of Japanese quail in simulated microgravity on some sexual features of males. As a model for simulating microgravity exposure of birds in laboratory conditions was used hypodynamia. The mean left testis weight in males reared under hypodynamia from day 3 up to 180 days of age was lower than that of control (P<0.05), but the right testis weight differences between both groups were not significant. Also the area, volume and foam production of cloacal gland was not significantly decreased in hypodynamia birds at the end of experiment. By contrast, the plasma testosterone concentration of males living in hypodynamia was reduced about 50 % at 90 and 180 days of age in comparison to control (P<0.05) suggesting some negative effects on sexual development. Our results demonstrated that male quail kept under simulated microgravity conditions were sexually competent although their sexual efficiency was reduced especially in terms of plasma testosterone.     

Body development and puberty in spontaneously hypertensive rats

The body growth and the onset of puberty in spontaneously hypertensive rats (SHR) and in normotensive controls (WKY) have been studied. In female rats the onset of puberty was determined by both the age and the body weight at which the vaginal opening and first estrus appeared, as well as the ability of estradiol and progesterone to induce pituitary LH release. For this purpose females were injected with estradiol benzoate (0.1 mg/kg) and progesterone (1 mg/rat). Control animals received only oil vehicle. In male rats, puberty was assessed by studying the age and body weight at the time of balano-preputial separation. In another experiment, SH and WKY rats were decapitated on day 30 to determine FSH, LH, PRL, GH and testosterone plasma levels in males and FSH and LH in females. The results obtained show: a) A greater body weight, at all the ages studied (every 4 days between days 28 and 92) in SHR animals. b) A delay in vaginal opening and first estrus presentation in SHR females. c) Absence of spontaneous LH peaks in WKY females. d) Advancement in balano-preputial separation in SHR males and e) Higher plasma FSH levels in SHR males than in WKY males, without differences in other hormones.     

Seasonal and inter-individual variation in testosterone levels in badgers <Emphasis Type="Italic">Meles meles</Emphasis>: evidence for the existence of two endocrinological phenotypes

Elevated testosterone levels can lower condition and increase parasites. We analysed testosterone in 84 blood samples of wild European badgers Meles meles collected at regular intervals (winter = mating season; spring = end of mating season; summer = minor mating peak; autumn = reproductive quiescence), and related variation to body condition, subcaudal gland secretion, parasite burden, and bite wounding. All males showed elevated levels in winter and low levels in autumn. In neither season did testosterone correlate with fitness-related parameters. However, two different endocrinological phenotypes existed in spring and summer. Whilst some males lowered their testosterone to levels comparable to autumnal quiescence (Type 1), others maintained elevated levels comparable to those during winter (Type 2). In spring and summer high levels were correlated with lower body condition and increased parasite burden, and Type 2 males tended to suffer higher mortality rates than Type 1. No animals older than 6 years adopted phenotype 2, indicating that males either switch phenotypes with age or that Type 2 results in lower life expectancy, evidencing the costs of male reproduction in badgers.     

Age-dependent changes in calling effort in the bell cricket <Emphasis Type="Italic">Meloimorpha japonica</Emphasis>

We investigated how male age and body weight influence male mating effort in the bell cricket Meloimorpha japonica. We adopted a longitudinal approach to study resource allocation to male mating effort (calling duration during 24 h) in the bell cricket. Calling durations and body weight of each male were measured at 7–8 days (young age), 14–15 days (middle age), and 22–25 days (old age) after the final molt. Calling duration increased between young and middle age. During the period between middle and old age, the amount of change in the calling duration was positively correlated with the body weight. The results suggested that older (i.e., low residual reproductive value) and better quality males invested more resources in mating effort.     

Spermatogenesis parameters and testosterone production at puberty as predictors of testicular functional activity in mice (<Emphasis Type="Italic">Mus musculus</Emphasis>)

The aim of this study was to investigate fertility-associated parameters of spermatogenesis and androgenic status in male laboratory mice at puberty and to assess their prognostic significance in the realization of the definitive testicular function. In three inbred murine strains, BALB/cLac, CBA/Lac and PT, the serum testosterone level, its testicular concentration, epididymal sperm count (sperm reserve) and portion of sperm with abnormal head morphology were evaluated on days 45 (puberty) and 90 (adulthood) of postnatal development. CBA/Lac males were characterized by a lower epididymal sperm count vs. other strains at both ages indicative of poorer spermatogenesis. At the same time, CBA/Lac males had a lower portion of sperm with abnormal head morphology, and this could be considered as a compensatory reaction aimed at improving sperm fertility. Distinct inter-strain differences in the portion of sperm with morphologically abnormal heads were established at both ages, while the inter-strain ratio remained invariable (BALB/cLac > PT > CBA/Lac). Thus, the level of abnormal spermatogenesis in the pubertal period may have a predictive significance for the definitive testicular activity in adult mice. No inter-strain and age-dependent changes were found in serum and testicular testosterone levels except for the PT strain, in which both testosterone levels rose from puberty to adulthood, suggesting a shift of the pubertal testosterone peak towards later times. Our data show that in male laboratory mice the genetic peculiarities of the testicular function manifest themselves during puberty and persist until adulthood.     

The role of endogenous gonadotropin-releasing hormone in the control of luteinizing hormone and testosterone secretion in the juvenile male monkey, Macaca fascicularis

To determine what changes occur in the activity of gonadotropin-releasing hormone (GnRH) neurons during pubertal development in primate species we tested the hypotheses that there are morphologic differences between GnRH-containing neurons in juvenile versus adult monkeys, and the low activity of the reproductive axis is governed by hypothalamic GnRH release in monkeys prior to puberty. We removed the brains from 5 juvenile and 5 adult male monkeys (Macaca fascicularis) and blocked, sectioned, and prepared each hypothalamus for light microscopic immunocytochemistry for GnRH-containing cells. The distribution and number of GnRH-containing neurons were similar in adult and juvenile brains; however, GnRH-containing perikarya in adult brains were significantly larger in total cross-sectional area (200 +/- 12 vs. 169 +/- 8 micron 2, P less than 0.05) and in cross-sectional area of the cytoplasm (139 +/- 2 vs. 88 +/- 6 micron 2, P less than 0.05) than in juvenile brains. In another group of 10 juvenile male macaques, we administered an antiserum to GnRH (Fraser #94; 2 ml/kg, i.v.) and monitored the effects on plasma luteinizing hormone (LH) and testosterone concentrations. The percentage of plasma samples with detectable LH levels decreased significantly (from 26.67 +/- 8.3% to 5.3 +/- 3.4%, P less than 0.05) after GnRH antiserum administration; however, plasma testosterone concentrations (0.08 +/- 0.02 ng/ml) remained unchanged. We conclude that during pubertal maturation in primate species there is increased synthesis and release of GnRH from a population of GnRH neurons that are active prior to puberty.     

Plasma testosterone concentrations during postnatal development in the male common marmoset

Repeated measurements of plasma testosterone (T) were made in 56 male marmosets from the day of birth until 300 days of age and in 44 adults (greater than 3 years). The resulting profile of plasma T during postnatal development shows higher levels during infancy (1-90 days) followed by a nadir between 100 and 170 days and then a progressive rise in T during puberty. Although T levels of up to 21 ng/ml were measured in infant males, mean levels (+/- SEM) were 5.4 +/- 0.6 ng/ml (days 1-10), declining gradually to 1.7 +/- 0.1 ng/ml (days 100-110). No increase in mean T levels between 15 and 100 days was identified, and the onset of puberty was earlier in some males than measured previously in this species.     

Androgens and male mating behavior in rough-skinned newts, Taricha granulosa

Cyproterone acetate was administered either orally or intraperitoneally to intact, adult male newts, Taricha granulosa. The number of males that exhibited the courtship behavior of clasping when tested with nuptial females was not altered by the antiandrogen treatments. In males which were unresponsive to nuptial females, the occurrence of clasping was not evoked by injections for 4 days of testosterone, dihydrotestosterone, or 11-ketotestosterone. Further, the incidence of clasping was not significantly elevated by injections of prolactin and/or testosterone for 30 days. The effect of sexual activity on testosterone and dihydrotestosterone levels in male newts was determined by radioimmunoassay of plasma collected from males which were: (1) isolated from females; (2) allowed to clasp a female for 2 min; or (3) allowed to clasp a female for 1 hr. The testosterone and dihydrotestosterone levels were unchanged during this period of clasping. In February and again in June, plasma androgen concentrations were measured in males which differed in their propensity to initiate courtship when paired with females. Androgen levels were similar for males that clasped a female and males that never attempted to clasp a female. Plasma androgen levels in the male newt are apparently not correlated with sexual responsiveness.     

Effects of accelerating growth on the onset of puberty in male mice

Sexual maturation was evaluated in male mice subjected to prenatal and preweaning overnutrition induced by reduction of litter size in embryonic and post-natal life. From birth to adulthood body weight was higher in overfed males than in controls. Plasma and testicular testosterone levels followed a similar pattern in normally fed and overfed males. Adult gonadotrophin levels were attained at 30 (FSH) and 40 (LH) days in controls and as soon as 20 days in overfed males. First fertile matings occurred at the same age in both groups. Overnourished males attained puberty when weighing considerably more than controls (34.7 +/- 0.4 vs. 29.4 +/- 0.3 g). The 30-day-old overfed males, which have attained the critical pubertal body weight of controls, were sexually immature. The data showed that in male mice puberty does not seem to be triggered by the attainment of a critical body weight.     

Reproduction in the male sub-Antarctic fur seal Arctocephalus tropicalis

The reproductive tracts of male sub-Antarctic fur seals Arctocephalus tropicalis ( n = 123), taken at Gough Island (40° 20'S, 9° 54'W) between November 1977 and October 1978, were examined. The presence of spermatozoa in the epididymal tubules showed that all males ≥4 years old had reached puberty, and the marked slower increase in mean testis weight and baculum length suggested that sexual (social) maturity was approached by 8-year-olds. Full adulthood was attained at 10–11 years of age based on the peak in mean testis and prostate weights, and mean baculum length. Secondary sexual characteristics were only fully developed in males ≥9 years old. A significant decline in mean testosterone concentration, and in testis, epididymis and prostate weights showed that adult males were reproductively quiescent during winter from May to July when seminiferous and epididymal tubules had lowest mean diameters with no spermatozoa present. Both the mean plasma testosterone concentration and mean testis weight peaked twice during the austral summer. The first peak coincided with the breeding season, and the second peak with the moulting period when adult males were impotent. Photoperiodic cueing might explain this seasonal trend.     

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.     

Male dominance and genetically determined reproductive success in the mandrill (Mandrillus sphinx)

Darwin referred to the adult male mandrill (Mandrillus sphinx) as the most brightly coloured of all mammals, citing the brilliant red and blue pigmentation of the face, rump, and genitalia as extreme examples of evolution by sexual selection. Considerable controversy exists concerning possible effects of sexually selected phenotypes via intermale competition on reproductive success. Behavioural and genetic studies of a large, semi-free ranging mandrill colony in Gabon have now demonstrated that clear-cut relationships exist between male secondary sexual development, social dominance, copulatory behaviour, and reproductive success in this primate species. Two morphological variants of adult male were identified; “fatted” males, with maximum secondary sexual coloration, which occupied dominant positions in the social group, and “non-fatted” males, with muted secondary sexual adornments, smaller testes and lower plasma testosterone levels, which lived as peripheral/solitary individuals. DNA fingerprinting analyses on infants born over five successive years showed that only the two most dominant, fatted males in the group had fathered offspring. Throughout the annual mating season these males attempted to mate-guard and copulate with females during periods of maximal sexual skin tumescence. Male rank and mating success were strongly positively related and the alpha male sired 80 – 100% of the resulting offspring during three consecutive years. Non-fatted adult males and group associated subadult males engaged in infrequent, opportunistic matings and did not guard females. Loss of alpha status resulted in a fall in reproductive success, but the effect was gradual; the deposed alpha male continued to father 67% and 25% of infants born during the next two years. Thus, whilst claims that male dominance determines mating success and paternity in primates have caused considerable debate, these results on mandrills provide unequivocal evidence for the existence of such effects.     

Prenatal androgens and the timing of seasonal reproductive transitions in sheep.

Both the onset of puberty in the lamb and the annual resumption of reproductive activity in adult male and female sheep are characterized by increased secretion of LH due to reduced responsiveness to steroid inhibition. However, the timing of puberty is sexually differentiated, for males undergo a reduction in sensitivity to steroid feedback at 10 wk of age, whereas females remain highly responsive to steroid inhibition until 30 wk. This sex difference is determined by androgens in utero. The present study was conducted to determine whether a sex difference exists in the timing of seasonal transitions in adult males and females. We compared serum LH in gonadectomized, estradiol-treated males (n = 7), females (n = 6), and androgenized females (n = 5) from blood samples collected twice weekly for one year. As determined by changes in the pattern of LH secretion, the onset and termination of the autumn breeding season were not different between males, females, and androgenized females (termination: 1 February +/- 4 days, mean +/- SE all groups; onset: males, 22 August +/- 4 days; females, 5 September +/- 18 days; androgenized females, 16 September +/- 10.5 days). However, there was a transient increase in LH (20 May to 23 June) in males, but not in females or androgenized females. Although no effects of prenatal testosterone were evident in the control of LH secretion in adult androgenized females, LH secretion in androgenized males was elevated throughout the nonbreeding season in 3 of 5 animals, indicating that exogenous testosterone may reduce seasonal increases in responsiveness to steroid inhibition.(ABSTRACT TRUNCATED AT 250 WORDS)     

Effects of mating rates on oviposition,sex ratio and longevity in a predatory mite <Emphasis Type="Italic">Neoseiulus cucumeris</Emphasis> (Acari: Phytoseiidae)

Two aspects of mating effects on the fecundity, sex ratio and longevity of Neoseiulus cucumeris (Acari: Phytoseiidae) were examined in laboratory experiments: (1) females mated by one, two or three different males (unmated and 3 days old) at 5-day intervals, and (2) females mated by males with different age/mating status (number of females mated previously by the male). Females allowed to mate with a second or third male at 5-day intervals produced 39 eggs on average, but those mated with a single male produced 28 eggs on average. Matings with additional males 5 or 10 days after the first male increased the duration of the oviposition period of these females by 5–7 days and at the same time reduced the post-oviposition period by about 10 days. Overall, females with additional matings by one or two different males at 5-day intervals survived a few days shorter than females without additional males. Mating with a different female each day, a male of N. cucumeris could mate with 5–8 females, which produced a total of 85–116 eggs: females mated with a male during days 1 and 2 in its adulthood and with a male of the last 2 days of life (days 7 and 8) produced about half as many eggs as females mated with a male during 3–6 days of its adulthood. Females mated with males that are too young or too old had a shorter oviposition period and a longer post-oviposition period and longevity than females mated with middle-aged males. In both experiments, rates of oviposition remained similar in females with high or low fecundity. This indicates that in both cases, the increased fecundity is due to the extension of the oviposition period through additional sperm supplied by the second male and or third male (in experiment 1) or more sperm by males not too young nor too old (experiment 2).     

Level of neuroactive steroids in the brain and sex-related peculiarities of formation and extinction of conditioned reflex in rats

Sex-related peculiarities of dynamics of brain sex steroids in the process of learning and extinction of the conditioned reflex of passive avoidance have been studied in model experiment. Prior to learning of the conditioned reflex, female rats were found to be distinguished by manifestation of anxiety and fear as compared with male rats. At formation of the conditioned reflex, no significant sex-related differences were detected between males and females, whereas extinction of the conditioned reaction of passive avoidance in males occurred by 2–3 days faster than in females. At learning of conditioned reaction of passive avoidance, in sexually mature male rats there was revealed an increase of the testosterone content in various brain structures, especially in hippocampus and frontal cortex, while its level in blood plasma remained unchanged. Also shown was an elevation of estradiol concentration in female amygdale, whereas at extinction of the conditioned reaction of passive avoidance, a rise of estradiol values was noted in hippocampus and cingular cortex. At the same time, the testosterone level in blood plasma did not change, whereas after extinction of the conditioned reflex the estradiol concentration decreased statistically significantly. Different dynamics of changes of the sex steroid levels in brain and blood plasma can indicate a possibility of their formation in the nervous tissue. The performed correlation analysis confirms the concept of selective involvement of testosterone and estradiol of individual brain structures in realization of processes of learning and memory in sexually mature male and female rats.     

Plasma androgens in spotted hyaenas (Crocuta crocuta): influence of social and reproductive development

Differences in plasma testosterone and androstenedione concentrations in male spotted hyaenas belonging to various reproductive and social categories 4 clans resident in South Africa and Botswana suggest that central-immigrant males have the highest concentrations of androgens, reflecting their roles as mating males. Social inhibition of reproductive function may occur in other males. A reversal in the ratio of testosterone: androstenedione occurs at puberty in most individuals, testosterone becoming the dominant hormone, especially in males that have procured mating rites. Cubs of either sex had low testosterone concentrations, except for a 4-day-old male that displayed adult concentrations, which were accompanied by a temporary testicular descent. Plasma testosterone concentrations in females largely reflected ovarian activity and showed no correlation with androstenedione concentrations. Female cubs had androstenedione concentrations significantly higher than those in all other social categories except for the central-immigrant males. The androgen profiles presented here suggest that the key to the behavioural dominance of female spotted hyaenas over males may lie with the neonatal developmental stages, rather than with the androgen patterns of adult animals.     

Continuous light after a long-day treatment is equivalent to melatonin implants to stimulate testosterone secretion in Alpine male goats

In rams, artificial long days followed by continuous light stimulate testosterone secretion during the non-breeding season. The objective of this study was to determine whether artificial long days followed by continuous light could stimulate testosterone secretion in Alpine bucks as well as in those exposed to long days followed by a melatonin treatment. All bucks were kept in shaded open pens. Control males were exposed to natural photoperiod conditions (n=5). Males of the two experimental groups were exposed to 2.5 months of long days from 1 December (n=5 each). On 16 February, one group of males was exposed to 24 h of light per day until 30 June; the other group was exposed to natural variations of photoperiod and received two s.c. melatonin implants. Testicular weight was determined every 2 weeks, and the plasma testosterone concentrations once a week. In the control and the two photoperiodic-treated groups, a treatment×time interaction was detected for testicular weight and plasma testosterone concentrations (P<0.001). In control bucks, testicular weight increased from January and peaked in June, whereas in both photoperiodic-treated groups, this variable increased from January, but peaked in April, when the values were higher than in controls (P<0.05). In the control group, plasma testosterone concentrations remained low from January to June, whereas in both photoperiodic-treated groups, this variable remained low from January to March; thereafter, these levels increased in both photoperiodic-treated groups, and were higher than controls in April and May (P<0.05). We conclude that continuous light after a long-day treatment stimulate testosterone secretion in Alpine male goats during the non-breeding season as well as the long days followed by a melatonin treatment. Therefore, continuous light could replace the implants of melatonin.