A study of seasonally delayed puberty in the male hare, Lepus Europaeus.

The brown hare, Lepus europaeus, has a mating season which extends from January to September. Adult males exhibit pronounced seasonal changes in the reproductive tract which are associated with changes in LH secretion. Maximum plasma levels of immunoreactive LH occur between March and June and minimal levels in the autumn non-mating period from September to December; this seasonal cycle in gonadotrophin output is reflected by the appropriate changes in the secretion of testosterone from the testes and in the activity of the accessory sex glands. Juvenile animals reach puberty only during the adult mating season, and the age of puberty thus varies with the date of birth. Males born before May reach puberty and become fertile at 3 months of age, while those born from May to July grow to a mature body size during the autumn non-mating season but puberty is delayed for several months. Since some animals experiencing delayed puberty were found to have elevated plasma levels of LH and testosterone, it is concluded that puberty is not completely suppresed by the environmental effects of the autumn, but that the developmental process is prolonged, resulting in the juveniles being synchronized with the adults in their reproductive activity.     

Seasonal Changes in Plasma Levels of Sex Hormones in the Greater Rhea (Rhea americana), a South American Ratite with a Complex Mating System

Seasonal rhythm in sex hormones has been extensively studied in birds, as well as its relationship with the type of mating system. The Greater Rhea (Rhea americana), a South American ratite species, reproduces seasonally and has a complex mating system: female-defense polygyny and sequential polyandry. The present study aimed at analyzing the endocrine basis of reproduction in this species and its relationship with its mating system. We used HPLC and electrochemiluminescence techniques to identify and measure plasma testosterone and estradiol levels. Annual oscillations in sex hormones, testosterone and estradiol, in adult males and females were observed. Lower levels of these hormones were exhibited during the non reproductive season (February to July), whereas their maximum values were reached in September for males and November-December for females. These fluctuations reflect the seasonal changes in gonadal function. By contrast, no significant sex hormones oscillations were observed in juvenile males and females (negative control of seasonal changes). Greater rheas maintain high testosterone and estradiol levels throughout the reproductive period. The high testosterone levels during incubation and chick rearing did not inhibit parental behavior in males, which appears not to conform to the “Challenge Hypothesis”. In females, the high estradiol levels throughout the reproductive season would be needed to sustain their long egg-laying period.     

Sex differences in adrenal function in the lizard Cnemidophorus sexlineatus: I. Seasonal variation in the field.

In order to document sex differences in adrenal function and how this relates to gonadal function during the period of seasonal activity, blood samples from male and female six-lined racerunners, Cnemidophorus sexlineatus, were taken immediately after capture in the field for determination of plasma corticosterone and gonadal steroid concentrations. Plasma testosterone and dihydrotestosterone levels for males, and 17 beta-estradiol and progesterone levels for females, were measured. Trends in the concentration of plasma corticosterone differed significantly between males and females. In males the highest concentrations of corticosterone were measured in late spring and the lowest concentrations were measured in late summer. Whereas half of the variation in corticosterone levels among males could be explained as seasonal change, less than 1% of the variation among females could be explained as seasonal change. In males plasma corticosterone and androgens exhibited similar seasonal decreases. Corticosterone levels for females were not correlated with progesterone or 17 beta-estradiol levels. Sex differences in seasonal variation in plasma corticosterone concentrations suggest that corticosterone may be involved in the different reproductive strategies and energy requirements of males and females during the seasonal period of activity.     

Lack of pubertal influences on female dispersal in muriqui monkeys, Brachyteles arachnoides

The hormonal mediation of dispersal in female mammals is poorly understood, in part because of the difficulties of detecting the onset of ovarian cycling and puberty in dispersing individuals. We used noninvasive methods of faecal steroid assays to determine the timing of dispersal relative to puberty and ovarian cycling in wild female muriqui monkeys, a species in which males are philopatric and nearly all females transfer from their natal groups. Natal females had a mean+/-SE age of 73.4+/-7.2 months (N=18) at the time of their transfers. Intergroup transfers occurred when one or more sexually active adult females were present, but did not show any seasonal patterns. Faecal progesterone and oestradiol profiles from nine natal females prior to transfer and four non-natal females that transferred into our study group demonstrate unequivocally that dispersal occurs prior to puberty in this species. All females showed baseline oestradiol levels and low progesterone levels compared with cycling adult females. Immigrants were first observed to copulate at 11.2+/-2.2 months of age (N=4), prior to the onset of normal ovarian cycles, and gave birth to their first offspring at 33.8+/-7.3 months (N=4) after transferring. Mean cortisol levels did not differ between natal emigrants or recent immigrants, and were within the range of those of adult males during the nonbreeding season in 10 of the 11 prepubertal females sampled. These results indicate that female dispersal is not triggered by activational hormones associated with puberty or escape from reproductive suppression in this species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Annual changes in brain concentration of arginine vasotocin and isotocin correspond with phases of reproductive cycle in round goby,Neogobius melanostomus

Reproductive cycle of seasonally breeding fish is synchronized with changes of photoperiod and temperature in environment. We hypothesize that arginine vasotocin (AVT) and isotocin (IT) are involved in timing and synchronization of seasonal reproductive activity in the round goby (Neogobius melanostomus). To verify this hypothesis, we examined the annual profiles of brain AVT and IT in round goby males and females in relation to their reproductive cycle. Wild round gobies were exposed to annual environmental changes in their natural habitats from where they were sampled monthly over a year. AVT and IT were measured using HPLC with fluorescence detection preceded by solid-phase extraction. This study shows seasonal variations in brain AVT and IT levels. Profiles of changes were similar in males and females: the peak of AVT was observed before spawning in March-April, whereas that of IT during spawning in May–June. Furthermore, the lowest AVT level was noted out of breeding season from November to January, while the level of IT decreased immediately at the end of the spawning. The results show that high AVT levels correlate with pre-spawning period whereas the highest IT levels correspond to spawning. A significant decline in AVT and IT in non-spawning season coincided with the quiescent phase of gametogenesis in both sexes.     

Preweaning over- and underfeeding alters onset of puberty in the rat without affecting kisspeptin

The perinatal nutritional environment can permanently influence body weight, potentially leading to changes in puberty onset and reproductive function. We hypothesized that perinatal under- or overfeeding would alter puberty onset and influence concentrations of a neuropeptide crucial for successful puberty, kisspeptin. We manipulated Wistar rat litter sizes to derive small (SL), control (CL), and large (LL) litters containing 4, 12, and 20 rat pups respectively. This manipulation results in an overweight phenotype in SL rats and a lean phenotype in LL that persists throughout life. To investigate whether successful puberty onset is affected by neonatal under- or overfeeding, we examined indices of growth and development, including the onset of puberty, as well as the central expression of Kiss1 mRNA in these pups. Male LL rats reached puberty later than those from CL. These males also had reduced plasma testosterone and elevated 17beta-estradiol concentrations at puberty. The age at puberty onset was not affected in SL males despite accelerated growth. In females, puberty onset was not significantly delayed by having a lean phenotype, and steroid hormones were not affected. The age at onset was, however, younger in the SL females. Kiss1 mRNA in the hypothalamus was not affected by neonatal nutrition either at puberty or 7 days later. Our findings show early life underfeeding in males and overfeeding in females significantly affects puberty onset, altering steroid hormone concentrations in males, but this is not related to changes in hypothalamic kisspeptin.     

Parameters of Mating Effort and Success in Male European Ground Squirrels,Spermophilus citellus

Behavioural and physiological changes during the reproductive period were documented in male European ground squirrels including: initiated conflict, scent marking, locomotion and range size, as well as testis size, scrotal pigmentation, testosterone levels and changes in body mass. Spring emergence dates in adult males varied but preceded those of females. Gonadal maturation was complete in adult males at emergence. Most yearlings did not mature and emerged with females. After a quiescent premating phase, male range, range overlap, conflict rates and locomotion increased at female emergence. The synchrony of females, their small ranges and short latencies to ovulation produced a highly male-biased operational sex ratio (OSR) and potential for scramble competition polygyny. In contrast to other ground squirrel species, each female apparently mated with only a single male. Scramble competition did appear to occur, in that males tried to contact as many females as often as possible before copulation. Females placed high temporal prerequisites on males. Costs of scrambling were documented by body mass loss during mating, which covaried with the number of ‘acquired’ females. Testicular regression occurred earlier, and fattening, moult and onset of next hibernation were delayed in successful males. The determinant factor in these costs was found to be mass loss intensity during the main mating period. Surprisingly, this factor was best related to feeding changes and not to locomotion or aggression. Time budget constraints perhaps imposed by the female, with compounding influences of exercise and stress effects of conflict, then negatively affected ensuing seasonal activities. The individual changes may adversely affect individual survivability and/or future reproductive success.     

Gonadal development and plasma steroid levels during pubertal development in captive-reared striped bass, Morone saxatilis

Puberty is the period during which full sexual development occurs and the capacity to reproduce is acquired. Despite its importance, our understanding of the endocrine regulation of puberty in lower vertebrates is still limited. The objective of the present study was to describe the changes in gonadal development and plasma steroid levels in a relatively late maturing species, the striped bass, during the first four years of life. In about 65% of the females, puberty was initiated during the third year. Although gonadosomatic index (GSI) and oocyte diameter increased during this year, this first cycle was characterized by a heterogeneous population of developing oocytes, a relatively low mean maximum oocyte diameter, and an absence of yolk granules in the oocytes. Plasma 17beta-estradiol (E(2)) levels were low in all three-year-old fish, suggesting that an insufficient stimulation of vitellogenin production by E(2) may underlie the lack of vitellogenin incorporation into developing oocytes. All monitored parameters increased during the fourth year, but were still below the values attained by older females. In about 60% of the males, puberty was initiated during the first year and all males were mature by the third year. During the first two years, several immature males initiated spermatogenesis without reaching full maturity. In mature males, mean GSI, plasma testosterone, and 11-ketotestosterone levels increased simultaneously, reaching higher values each subsequent year. Our results indicate that, similar to the situation in mammals, more than one reproductive cycle is required in striped bass before complete adulthood is reached.     

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)     

Pinealectomy or superior cervical ganglionectomy do not alter reproduction in the wolf (Canis lupus)

Twelve wolves (6 male and 6 female) were used to study the role of the pineal in photoperiodic mediation of seasonal reproduction. Eight wolves were pinealectomized (PNX) or sham-pinealectomized (S-PNX) at 5 mo of age, and 4 were superior cervical ganglionectomized (SCGX) at 16 mo of age (2 males and 2 females per treatment). All attained puberty at the species-typical time, during their second breeding season, except 2 SCGX males that did not survive. Reproductive cycles of an additional male that was SCGX as an adult and the PNX and S-PNX wolves, followed for a minimum of 3 yr, did not differ from each other or from those of unoperated colony wolves on measures of serum testosterone and luteinizing hormone for males, or of serum estradiol and progesterone for females. Nor was the range of dates for ovulation different for treated vs. untreated females. Surgical transection of the olfactory tracts of 1 male and 1 female PNX wolf, inducing anosmia to control for the possibility of pheromonally synchronized cycles, also failed to alter the seasonality of these reproductive parameters. These results do not conform to the model of pineal mediation of sexual cycles for photoperiod-sensitive species. In spite of evidence for photoperiod influence, the wolf apparently relies on a system other than the pineal for seasonal control of reproduction.     

Passive transfer of maternal GnRH antibodies does not affect reproductive development in elk (Cervus elaphus nelsoni) calves

Gonadotropin-releasing hormone is intermittently released from the hypothalamus in consistent patterns from before birth to final maturation of the hypothalamic-pituitary-gonadal axis at puberty. Disruption of this signaling via GnRH vaccination during the neonatal period can alter reproduction at maturity. The objective of this study was to investigate the long-term effects of GnRH-antibody exposure on reproductive maturation and function in elk calves passively exposed to high concentrations of GnRH antibodies immediately after birth. Fifteen elk calves (eight males and seven females) born to females treated with GnRH vaccine or sham vaccine during midgestation were divided into two groups based on the concentration of serum GnRH antibodies measured during the neonatal period. Those with robust (>15 pmol ¹²⁵I-GnRH bound per mL of serum) titers (N = 10; four females and six males) were designated as the exposed group, whereas those with undetectable titers (N = 5; three females and two males) were the unexposed group. Onset of puberty, reproductive development, and endocrine function in antibody-exposed and unexposed male and female elk calves were compared. Neonatal exposure to high concentrations of GnRH antibodies had no effect on body weight (P = 0.968), endocrine profiles (P > 0.05), or gametogenesis in either sex. Likewise, there were no differences between groups in gross or histologic structure of the hypothalamus, pituitary, testes, or ovaries. Pituitary stimulation with a GnRH analog before the second potential reproductive season induced substantial LH secretion in all experimental elk. All females became pregnant during their second reproductive season and all males exhibited similar mature secondary sexual characteristics. There were no differences between exposure groups in hypothalamic GnRH content (P = 0.979), pituitary gonadotropin content (P > 0.05) or gonadal structure. We concluded that suppressing GnRH signaling through immunoneutralization during the neonatal period likely does not alter long-term reproductive function in this species.     

Reproductive synchronization in squirrel monkeys (Saimiri)

Groups of squirrel monkeys (Saimiri) that are exposed to certain seasonal environmental stimuli experience a yearly reproductive cycle with discrete mating and birth seasons. Seasonal rainfall or some rainfall induced seasonal changes (such as changes in vegetation or insect fauna) appear to be responsible for timing theSaimiri reproductive cycle. Animals of both sexes show significant physiological and behavioral changes during the yearly cycle. Whether the environmental timing factors affect both the males and the females equally, or affect only one sex directly and the other sex indirectly through social communication is not clear. Three mechanisms by which the reproductive activity of both males and females could be synchronized are presented, and data from a laboratory study and a field study relevant to each mechanism are presented. Several social interaction patterns frequently observed in the field study suggest that (1) male sexual activity may excite female sexual activity through male penile display and/or other stereotyped interactions and/or (2) female sexual activity may excite male sexual activity through pheromone and/or other communication channels.     

Some physiological and behavioural changes associated with oestrus and pregnancy in the squirrel monkey (Satmiri sciureus)

Peak values in the karyopyknotic index of vaginal smears from the squirrel monkey occurred at intervals of 10.9±0.1 days. The urinary excretory rate of a metabolite similar to preg-nanediol increased when ovulation was induced by exogenous gonadotropin therapy. Small amounts of this metabolite were excreted during lactation, periods of anoestrus and during the follicular phases of normal oestrous cycles. Significantly larger amounts were excreted during the 157 days gestation period and during the luteal phase which persisted for one week after a peak karyopyknotic index value was observed. Changes in the pattern of urinary electrolyte excretion were not correlated reliably with changes in ovarian differentiation. Sexual motivation was greatest at mid-cycle, became less after conception and persisted at a low level throughout gestation and lactation. The occurrence of oestrus was seasonal and independent of physical contact with males. The development of secondary sexual characteristics in the male was synchronized with the onset of seasonal oestrus in the females.     

Non-invasive assessment of reproductive status in Chinese water deer (Hydropotes inermis): Correlation with sexual behaviour

The annual reproductive cycle of Chinese water deer (Hydropotes inermis), a nearly threatened small cervid species, was studied by means of fecal steroid analysis coupled with behavioural observations. Data showed a clearly seasonal reproductive pattern. In adult males, the onset of androgen secretion, in October, was concomitant with the first manifestations of territoriality. Androgen metabolites concentrations reached significant peak values in December, when matings occurred. In mature females, there was a close synchrony in reproductive states: lactational/seasonal anoestrus from June to November, pregnancy from December to May. Fecal progesterone metabolites profiles suggested that silent ovulations occurred at the onset of breeding season and that females conceived at their first ovulation with behavioural estrus. The female sexual receptivity state might last only a few hours. High levels of sniffing, parades and pursuits, concomitant of the highest concentrations of androgen, could allow the males to detect the furtive estrus in the females present in their territory. We concluded that the non-invasive method applied for the first time in this species was useful for the evaluation of the endocrine status and its relation with behaviour.     

Reproductive biology and postnatal development in the tent-making bat Artibeus watsoni (Chiroptera: Phyllostomidae)

In this study we investigated the reproductive patterns and postnatal development in the tent-making bat Artibeus watsoni . We sampled two populations in the Golfito Wildlife Refuge and Corcovado National Park, south-western Costa Rica, from June 2003 to March 2005. Most females were pregnant during the months of January and June, and most were lactating in March and July, indicating that this species exhibits seasonal bimodal polyoestry, with the first parturition peak occurring in February–March and the second in June–July. Additionally, we observed a postpartum oestrus following the first parturition, but not after the second. Females entered oestrus again in November–December and had a gestation period of c . 3 months. A female-biased sex ratio of neonates was observed during the second parturition period, and young were born at 32 and 56% of their mothers' body mass and length of forearm, respectively. Adult proportions in length of forearm were attained faster than adult proportions in body mass, and sustained flight was only possible after 35 days of age, when pups had achieved 100 and 80% of adult length of forearm and body mass proportions, respectively. Weaning and roosting independence occurred when young were c . 30–40 days old, and young females appeared to remain close to their place of birth, at least for their first mating period, whereas adult males were never recaptured near their birth site. In addition, sexual maturity was reached in as little as 3 months in females born during the first parturition period, whereas females born during the second birth period in June–July seemed to reach maturity at 6 months of age. Our results show that A. watsoni belongs to the faster lane of the slow–fast continuum of life-history variation in bats, which may be attributed primarily to its roosting and feeding ecology.     

Importance of the signals provided by the buck for the success of the male effect in goats

Under temperate and subtropical latitudes, ewes and goats display a reproductive seasonal pattern and their sexual activity during the anestrous period can be stimulated and synchronized by the introduction of males in the group, which is called the "male effect". The response of females to the male effect in the middle of the anestrous season is weak or absent. This failure may be due to the inability of the female to respond to males, as a result of a refractoriness of the female to the male stimulus. But, it may also be due to a low quality stimulus provided by the male which is, as the females, in seasonal rest. We tested this latter hypothesis in seasonally inactive goats kept under subtropical conditions by comparing the use of males with their sexual behavior stimulated or not by photoperiodic treatments. Treated males were able to induce estrous activity of females during the whole anestrus season. We have also determined that previous separation of the males and continuous contact during teasing are not absolute requisites when active bucks are used. While odor from the male and its sexual behavior play a primary role in inducing ovulation, vocalizations appear to facilitate the display of the does' estrous. It remains to be determined to which extent these conclusions apply under temperate latitudes and with more seasonal breeds.     

Effects of fasting and exogenous melatonin on annual rhythms in the blue fox (Alopex lagopus)

The arctic fox (Alopex lagopus) is a winter-active inhabitant of the high arctic with extreme fluctuations in photoperiod and food availability. The blue fox is a semi-domesticated variant of the wild arctic fox reared for the fur industry. In this study, 48 blue foxes were followed for a year in order to determine the effects of exogenous melatonin and wintertime food deprivation on their reproductive and thyroid axes. Half of the animals were treated with continuous-release melatonin capsules in July 2002, and in November-January, the animals were divided into three groups and either fed continuously or fasted for one or two 22-day periods. Food deprivation decreased the plasma triiodothyronine and thyroxine concentrations probably in order to preserve energy due to a decreased metabolic rate. The same was observed in the plasma testosterone levels of the males but not in the plasma estradiol concentrations of the females. Exogenous melatonin advanced the autumn moult and seasonal changes in the voluntary food intake. It also advanced the onset of the testosterone peak in the males. The plasma estradiol levels of the females were unaffected, but the progesterone levels peaked more steeply in the sham-operated females. Melatonin exerted a strong influence not only on the reproductive axis of the males but also on the seasonal food intake. The species seemed quite resistant to periodic involuntary food deprivation.     

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.     

Seasonal plasticity of brain aromatase mRNA expression in glia: divergence across sex and vocal phenotypes

Although teleost fishes have the highest levels of brain aromatase (estrogen synthase) compared to other vertebrates, little is known of its regulation and function in specific brain areas. Previously, we characterized the distribution of aromatase in the brain of midshipman fish, a model system for identifying the neural and endocrine basis of vocal-acoustic communication and alternative male reproductive tactics. Here, we quantified seasonal changes in brain aromatase mRNA expression in the inter- and intrasexually dimorphic sonic motor nucleus (SMN) and in the preoptic area (POA) in males and females in relation to seasonal changes in circulating steroid hormone levels and reproductive behaviors. Aromatase mRNA expression was compared within each sex throughout non-reproductive, pre-nesting, and nesting periods as well as between sexes within each season. Intrasexual (male) differences were also compared within the nesting period. Females had higher mRNA levels in the pre-nesting period when their steroid levels peaked, while acoustically courting (type I) males had highest expression during the nesting period when their steroid levels peaked. Females had significantly higher levels of expression than type I males in all brain areas, but only during the pre-nesting period. During the nesting period, non-courting type II males had significantly higher levels of aromatase mRNA in the SMN but equivalent levels in the POA compared to type I males and females. These results demonstrate seasonal and sex differences in brain aromatase mRNA expression in a teleost fish and suggest a role for aromatase in the expression of vocal-acoustic and alternative male reproductive phenotypes.