Endocrine Correlates of Reproductive Status in Breeding and Nonbreeding Wild Female Moustached Tamarins

In callitrichid primates, reproduction is usually restricted to a single female per group. Reproductive rate is high and the occurrence of a postpartum estrus can lead to simultaneous lactation and pregnancy. In contrast, nonreproductive females often show ovarian inactivity. However, most studies on callitrichid reproductive physiology have been conducted in captivity, where conditions differ considerably from those in the wild, so that reproductive conditions may be strongly modified. Using fecal estrogen and progestogen measurements to monitor female reproductive status in 2 groups of wild moustached tamarins (Saguinus mystax), we examined 1) whether reproductive females in free-ranging groups also show postpartum estrus and 2) whether nonreproductive females demonstrate signs of ovarian activity. In both reproductive females, clear changes in the excretion pattern of progestogen and estrogen metabolites over time in combination with information on parturition dates allowed us to differentiate between pregnancy, a period of postpartum ovarian inactivity lasting for 54 and 64–82 days, and a period of ovarian activity before conception. Nonreproductive females demonstrated temporal fluctuations in hormone concentrations and absolute hormone levels that were similar to ones in the breeding females during the phase of ovarian activity. The results suggest that, in contrast to most captive female tamarins, reproductive females in wild groups of moustached tamarins do not have a postpartum estrus and that nonreproductive females show ovarian activity despite the presence of a breeding female. We therefore conclude that findings from captivity should be only carefully compared to the situation in the wild.     

A preliminary study of olfactory behavior of captiveLemur coronatus during the breeding season

The olfactory behavior of a captive population of crowned lemurs (Lemur coronatus)was studied during their annual breeding season in order to investigate its possible role in the fine-tuning of mating synchrony after photoperiodic initiation of reproductive activity. The frequencies of five stereotyped olfactory behavior patterns were recorded in four male-female groups during 315 1-hr observation sessions between October and March. The mean total scent-marking frequency of all males was positively correlated with their mean testicular size. Male anogenital-, head-, and allomarking frequencies decreased during the breeding season, whereas hand-marking frequencies remained constant. Male head-marking increased significantly in the 5 days preceding female vaginal estrus. Furthermore, males responded to many female scents by olfactory investigation and/or overmarking, whereas females never showed an observable behavioral response to male scent marks. The marking frequencies of two females did not change significantly during the breeding season, while those of two others decreased significantly. These results suggest qualitative changes of female scents during estrus and a less important role of male scents in intersexual communication in the context of reproduction than previously thought.     

Reproduction and larval development of the gastropodAlaba vladivostokensis in Vostok Bay, the Sea of Japan

The reproduction and development of the prosobranch gastropodAlaba vladivostokensis Bartsch were studied. In Vostok Bay,A. vladivostokensis reproduces in the warmest season at water temperatures of 19–23°C. The females lay egg masses in the shape of flat, coiled bands on eelgrass leaves and on sargosso thalluses. The total period of development from egg laying to larval settling takes 25–27 days. The reproduction and development patterns and larval morphology ofA. vladivostokensis are similar to that ofAustralaba picta (A. Adams), which inhabits the coast of Japan. It is suggested that the population ofA. vladivostokensis in Peter the Great Bay should considered as part of the wide geographical range ofA. picta.     

Metabolic cost of first reproduction in young female European roe deerCapreolus capreolus

In female roe deerCapreolus capreolus (Linnaeus, 1758), like in several deer species, first reproduction occurs before they have reached their full body size. This study quantifies, in young females, the energetic costs induced by the contemporaneously occurring events: growth and first reproduction. Resting metabolic rate and body mass were measured in young primiparous females from first mating to 4 months after parturition, and compared to values measured in fully-grown adult multiparous females. Throughout the 10-month period from mating to fawning, body mass increased in yearlings. Prior to the blastocyst implantation (month −5 before parturition) young females were lighter than adult females whereas after parturition they had the same body mass. Our results suggest that body growth was reinitiated during pregnancy in primiparous females. From mating to fawning, except in the first part of pregnancy, mass-specific metabolism was higher in primiparous females than in multiparous individuals indicating the occurrence of an additional cost due to growth in young females. The depressed level observed at the beginning of gestation could allow the resumption of growth at lower cost. Thus, the allocation of resources to both reproduction and growth was not detrimental to first reproduction in young female roe deer under experimental conditions withad lib feeding.     

Behavioral and reproductive responses of female opossums to volatile and nonvolatile components of male suprasternal gland secretion

Female gray short-tailed opossums (Monodelphis domestica) lack an estrous cycle and are induced into estrus by exposure to a pheromone in male scent marks. Behavioral and physiological responses of females to the volatile and nonvolatile components of scent marks were examined in two experiments. Young females (n = 9) were tested prior to and during their first estrus for behavioral responses to scent marks, collected on a 7-ml glass vial rubbed over the suprasternal gland of a mature male. The response to volatile components of the scent mark, recorded when marked and unmarked vials were covered with a perforated shield, was compared to the response to these vials when unshielded. Estrous females nuzzled the shields over marked vials (55.8 ± 8.5 nuzzles/10 min) more than the shielded clean vial (10.9 ± 2.4) (P < 0.05); a similar response was observed in anestrous females. Nuzzling of unshielded, scent-marked vials was higher (P < 0.05) during anestrus than in the same females when in estrus. The role of nonvolatile pheromones in reproductive activation was tested in adult females (n = 11) exposed for up to 14 days to a shielded, marked vial or to an unshielded, marked vial in a crossover design. All females exposed to unshielded vials expressed estrus, and 10 copulated. Only 2 females expressed estrus (significantly fewer, P < 0.05), when exposed to shielded marked vials, and neither copulated. These results demonstrate that females detect and respond behaviorally to both volatile and nonvolatile components of male suprasternal gland secretion, but the estrus-inducing pheromone in these secretions is nonvolatile.     

Age at first reproduction in philopatric female muriquis (<Emphasis Type="Italic">Brachyteles arachnoides hypoxanthus</Emphasis>)

Female northern muriquis (Brachyteles arachnoides hypoxanthus or B. hypoxanthus) at the Estação Biológica de Caratinga/RPPN-FMA, Minas Gerais, Brazil typically disperse from their natal groups at an average age of 6.1±0.6 years (median =6.0 years, range =5.3–7.8 years, n =22), prior to the onset of puberty and sexual activity. Immigrants do not conceive until at least their second mating season, and the minimum interval from immigration to first reproduction has been 2.0 years. Age at first reproduction in dispersing females, previously estimated at 8.9 years, has now been documented at 9.0 and 9.25 years for two females whose birth dates are known. This is older than the 7.5 years at which the only female previously known to have reproduced in her natal group gave birth. Here, we present new data from a second female that reproduced in her natal group. This female (BA) was first observed to copulate at 5.5 years, and gave birth to her first infant at 7.25 years of age. Her 1.75-year cycling-to-first conception delay was only slightly shorter than the minimum recorded for immigrant females, and thus was not responsible for her young age at first reproduction compared to dispersing females. Although our sample size is small, our findings suggest that early puberty may permit females to reproduce in their natal group, implying a possible link between life history trade-offs and dispersal patterns. Because the only two females that have reproduced in their natal group were maternal sisters, it is also possible that maternal effects on age at puberty can impact dispersal patterns, particularly in small populations of primates.     

Male pheromone stimulates ovarian follicular development and body growth in juvenile female opossums (Monodelphis domestica)

Female opossums are induced into estrus by direct exposure to a non-volatile pheromone in male scentmarks. Juvenile females develop this responsiveness by 150 days of age (days), and earlier (130 days) if exposed to male pheromone beginning at 90 days. The goal of this study was to examine the effect of male pheromone on body growth and ovarian follicular development in young opossums. Females (n = 28) were weaned at 56 days and caged individually with ad libitum food and water from 84 days. Body mass was recorded 2–3 times weekly and the onset of estrus was monitored by urogenital sinus cytology. Exposed females were given continuous access to adult male scentmarks from 90 days and randomly selected for necropsy at 105 and 130 days. Unexposed females were isolated from direct contact with males and their scentmarks and randomly selected for necropsy at 90, 105, 130, and 150 days. Exposed females were larger (63.5 ± 1.1 g) than unexposed females (56.6 ± 1.1 g) at 130 days, and 4 of 5 had expressed estrus or proestrus. Uterine mass at 130 days was higher (P < 0.05) in exposed (129.8 ± 28.8 mg) than in unexposed (25.4 ± 6.7 mg) females, none of which expressed estrus by 150 days. The mean number of developing, antral follicles per female increased from 1.5 ± 1.5 at 90 days to 17.8 ± 5.2 at 130 days. Mean diameter of developing antral follicles at 130 days was larger in exposed (534 ± 54 μm) than in unexposed females (393 ± 4 μm). The results of this study demonstrate that pheromonal induction of first estrus in juvenile opossums is associated with an increased rate of body growth and follicular development.     

Initiation of early breeding in a population of Microtus townsendii (Rodentia) with the secondary plant compound 6-MBOA

Summary Feeding the secondary plant compound 6-Methoxybenzoxazolinone (6-MBOA) during winter to a free living population of Microtus townsendii accelerated breeding in females. Both the recruitment of young and sexual maturation of these young were advanced by four weeks in comparison with a control population. Overwintered females supplied with 6-MBOA matured at a lower body weight than control females. But there was no such weightat-maturity difference between the grids for males. During April and May 72% of all juveniles captured came from the experimental population. Winter reproduction and early recruitment of young stimulated by 6-MBOA could have important population consequences for these voles.     

Influence of exogenous gonadotropin-releasing hormone on seasonal reproductive behavior of the coyote (Canis latrans)

Wild Canis species such as the coyote (C. latrans) express a suite of reproductive traits unusual among mammals, including perennial pair-bonds and paternal care of the young. Coyotes also are monestrous, and both sexes are fertile only in winter; thus, they depend upon social and physiologic synchrony for successful reproduction. To investigate the mutability of seasonal reproduction in coyotes, we attempted to evoke an out-of-season estrus in October using one of two short-acting gonadotropin-releasing hormone (GnRH) agents: (1) a GnRH analogue, deslorelin (6-d-tryptophan-9-(N-ethyl-l-prolinamide)-10-deglycinamide), 2.1 mg pellet sc; or (2) gonadorelin, a GnRH (5-oxoPro-His-Trp-Ser-Tyr-Gly-Leu-Arg-Pro-GlyNH₂) porcine hypothalamic extract, 2.0 μg/kg im once daily for 3 consecutive days. A transient increase in serum concentrations of estradiol and progesterone (1 and 2 wk, respectively) was detected after treatment with deslorelin but not gonadorelin. Also, socio-sexual behaviors reminiscent of winter mating (including courtship, mate-guarding, precoital mounts, and copulatory ties) were observed among the deslorelin group. During the subsequent breeding season (January and February), however, preovulatory courtship behavior and olfactory sampling appeared suppressed; emergence of mounts and copulations were delayed in both deslorelin and gonadorelin treatment groups. Furthermore, whereas 8 of 12 females treated in October ovulated and produced healthy litters in the spring, 4 naïve coyotes failed to copulate or become pregnant. Thus, perturbation of hormones prior to ovulation in species with complex mating behaviors may disrupt critical intrapair relationships, even if fertility is not impaired physiologically.     

Studies on the relationship between the estrous cycle of BALB/c mice and their resistance to Paracoccidioides brasiliensis infection

A relationship between the estrous cycle and non-specific host resistance to Paracoccidioides brasiliensis yeast cells was examined by using both sexes of adult BALB/c mice. They were divided into 6 groups, including a male group and females at proestrus, estrus, metestrus-I, metestrus-II and diestrus. The mice received yeast cells through three different inoculation routes; intravenous, intraperitoneal and intratracheal. In all of the inoculation routes, the clearance of the yeast cells was influenced by the estrous cycle. The female mice at estrus, which might have high blood estrogen levels, showed a marked clearance of the yeast cells from the blood, peritoneal cavity and lungs. These results suggested that non-specific host resistance to the yeast cells was enhanced by estrogen. All female groups inoculated by the three routes showed higher clearance of the yeast cells than the male group.     

Seasonality in Reproduction of <Emphasis Type="Italic">Lepilemur edwardsi</Emphasis>

Sportive lemurs are threatened species in the IUCN Red Data Book. However, quantitative information on their reproduction, urgently required for conservation, has been lacking. We collected first data on reproductive activity of Milne-Edwards’ sportive lemurs in a population inhabiting the dry deciduous forest of the Ankarafantsika National Park in northwestern Madagascar during 1998, 2001, and 2003. The species showed a seasonal reproduction. The main mating season extended from May to June, as indicated by the presence of males with high testes volumes and estrus females. In the mating and early postmating season and in the postparturition season, sexes did not differ in body mass. Females had a significantly higher body mass than males in August and November, indicating pregnancy, which together with the presence of small infants in October and November implies that gravidity in females lasted for about 4–5 mo. All litters consisted of singletons. Individuals with body mass at the lower limit of the population either did not develop measurable testes volumes (males) or were not in estrus (females). They were probably juveniles from the previous birth season that achieved sexual maturity not before their second year after birth. The first data on reproduction suggest a low reproduction rate for Lepilemur edwardsi and a request for a higher conservation status than previously attributed and the need for further management strategies.     

Environmental factors influencing the seasonality of estrus in chimpanzees

Although the energetics of the estrous cycle in primates is not well understood, evidence suggests that energy and nutrient acquisition influence ovulation and the timing of conception. Energy for estrus has to compete with energy allocated for cellular maintenance, thermoregulation, movement for food, and predation avoidance. While some chimpanzee (Pan troglodytes) populations do not have a seasonal birth period, evidence suggests that there is seasonality in the number of estrous females. Similarly, the onset of postpartum cycles has been reported to be seasonal. We used 33 months of data from the Taï National Park, Côte dIvoire, to examine how the number of estrous females in a given month was influenced by the abundance and distribution of food, diet, rainfall and temperature. In a second analysis, we examined if there was a seasonal effect on first estrous swellings in adolescent females and postpartum adult females. Results demonstrated that the number of females in estrous in a given month was positively related to food abundance and percent foraging time spent eating insects, and negatively related to mean rainfall in the two preceding months and the mean high temperature. The timing of first estrous swellings of postpartum females and prepartum young females was positively related to the food abundance, and negatively related to mean high temperature. These results showed that environmental conditions can seasonally limit the energetically demanding estrus cycle. The presence of estrous females increases gregariousness in chimpanzee communities, and this study identified environmental factors that affect estrus directly and hence social grouping indirectly.     

Estrus and estrogen changes in mated and unmated free-living European ground squirrels

The course of behavioral and vaginal estrus and patterns of circulating estrogens were followed in free-living European ground squirrels (Spermophilus citellus) after their emergence from hibernation. Normally mating females were compared to a second group in an area where males had been removed from the population before female emergence. Both groups showed vaginal estrus, but the patterns differed. Mating shortened vaginal estrus to a 3-day period compared to 8 days in unmated females. The extent (cell number) of cell cornification during estrus and the cellular components (percentage distribution) of metestrus did not differ between the two groups. Females in the area without males had significantly higher estrogen levels during estrus and metestrus compared to those in the control area. European ground squirrels were found to be monestrous, as none of the unmated females reentered estrus after metor diestrus was detected. The prolongation of vaginal estrus in unmated females can be viewed as either a physiological inevitability or an adaptation to low mate availability. The extension is still relatively short compared to other sciurid species and perhaps a product of constraints producing a strict time frame for reproduction.     

Demography and life history of free-rangingPropithecus diadema edwardsi in ranomafana national park,madagascar

I conducted the first long- term study of the life history patterns of Propithecus diadema edwardsi—Milne- Edward’s sifaka— in the rain forests of southeastern Madagascar, beginning in 1986. I report behavioral observations on a total of 33 individuals from three groups over a 9- year span. We captured,marked, and released 21 individuals. Individual group size ranged from three to nine sifakas. Two breeding females lived in groups I and II until 1993. A newly formed group (III) had one breeding female. Age at first reproduction is 4 years for females and 5 years for males. Gestation length is 179 days (n =2). Most births occurred in June (n = 17), but infants were also born in May (n = 2) and July (n =2). Nine of 21 (43%) infants born died before the age of 1 year, and 15 (67%) died before the age of reproduction. One female bred in her natal group after the death of the resident male and the immigration of an adult male. Another two females disappeared at 4 and 5 years of age;they could have emigrated or died. All 5- to- 6- year- old males (n = 4) have emigrated from their natal groups to adjacent groups. Two have committed infanticide. Five or more individuals were killed by Cryptoprocta ferox.Despite high mortality and offspring dispersal, the number of individuals in the two main groups remained nearly the same over the 9- year study.     

Evidence for spontaneous postlactational estrus in gray short-tailed opossums (Monodelphis domestica)

Previous studies of the gray short-tailed opossum have shown that ovarian activity and estrus are induced by male pheromones, but we recently documented urogenital sinus (UGS) estrus in postlactational females despite their isolation from the male stimuli known to be associated with induced estrus. Body weights and UGS smears were collected after removal of pups in midlactation (19-37 days postpartum), after weaning (55-61 days postpartum), or after pheromone exposure. Estradiol was measured by RIA in plasma samples collected from dams during lactation, after separation from pups, and at estrus. Average days to UGS estrus from pup removal or initial pheromone exposure differed (P<0.05) only between the midlactation and pheromone exposure groups. Postlactational females showed a decrease in body weight from the time of pup removal or weaning to estrus, which contrasts with the increase seen in pheromonally stimulated females. Plasma estradiol was elevated at estrus in all groups, and females that were paired with males at postlactational estrus mated and produced litters. This study demonstrates that gray short-tailed opossums consistently experience estrus within 2 wk of weaning their young and that postlactational estrus appears to be hormonally and behaviorally equivalent to estrus induced by direct exposure to male pheromones.     

Lipid stores, ovary development, and brain gene expression in Polistes metricus females

In order to gain insights into the mechanistic basis of caste and behavioral differences in Polistes paper wasps, we examined abdominal lipid stores and ovary development in Polistes metricus females in four groups: foundresses, queens, workers, and gynes. Queens had the largest ovaries, followed by foundresses, workers, and gynes. Gynes had 6x higher lipid stores than the other groups, and lipid stores were lower in foragers (foundresses, workers) than non-foragers (queens, gynes). Lipid levels and ovary development were negatively correlated across the four groups, but removing gynes from the analysis revealed a significant positive correlation for foundresses, workers, and queens, suggesting different energy allocation strategies for gynes vs. other groups. Expression levels of 9 genes (including three in the insulin pathway), examined in a previous study, correlated with either lipid stores or ovary development. These correlative results suggest important relationships between nutrition, reproduction, and division of labor in primitively social insects. We also show that it is possible to assign P. metricus females to one of the four female groups on the basis of wing wear (an indicator of foraging experience), lipid stores, and ovary development, which can facilitate caste-specific collections for future studies. Received 23 May 2008; revised 6 November 2008; accepted 20 November 2008.     

Introduction and integration of strangers into captive groups of tufted capuchins (Cebus apella)

We introduced two to four unfamiliar animals into three established groups (N = 6–9 per group) of tufted capuchins (Cebus apella).We present findings on the behavioral consequences of introductions as a function of age, sex, and residency status and long-term consequences for health and reproduction. No morbidity from aggression occurred at the time of introductions or during several months following, and reproduction was not compromised. Activity budgets and patterns of social spacing and interaction were little changed following the introductions except for increases in vigilance behavior, especially by newly introduced adult females. Adult females exhibited the strongest and longest-lasting response to changes in group composition. The results indicate that in this species (1) introductions of adult females can be carried out with acceptable risk to the newcomers provided that careful monitoring occurs, so that the onset of severe aggression instigated by resident females toward new females can be avoided, (2) juveniles can be introduced with minimal risk, and (3) adult males can be introduced into groups lacking resident adult males with minimal risk. Capuchins differ in important ways from the better-studied Old World monkeys in their response to introductions of strangers. The differences are instructive with regard to processes supporting species-typical social structure, which is less overtly hierarchical in capuchins than in macaques.     

Reproduction of Calanus glacialis in the Laptev Sea, Arctic Ocean

Abundance and reproductive biology (gonad maturation and egg production) of the Arctic copepod Calanus glacialis were studied in the Laptev Sea and adjacent Arctic Ocean in September 1993 and from July to September 1995. Both abundance and reproductive activity were subject to strong spatial and seasonal variability, which was related to the ice cover, feeding conditions and circulation pattern. Maximum abundance of the C. glacialis population was generally confined to the outer shelf and slope with depths between 50 and 1000 m. During both cruises, highest egg production rates and largest number of young copepodite stages were observed in the eastern Laptev Sea, where the development of the C. glacialis population seems to follow the opening of the “Siberian Polynya”. In the western part, which is usually covered by pack ice, females were all immature, and no young stages were found. However, females responded quickly to a temporary opening of the ice there in 1995 and spawned. Starvation experiments showed that food-independent reproduction fuelled by internal energy resources was at least partly responsible for relatively high egg production rates at low ambient food concentrations. Egg production rates in starved females were considerably higher than those previously reported. Accepted: 14 June 2000     

Breeding biology of Tenagomysis tasmaniae Fenton,Anisomysis mixta australis (Zimmer) and Paramesopodopsis rufa Fenton from south-eastern Tasmania (Crustacea: Mysidacea)

The number, size and developmental stage of young in the brood pouch of female Tenagomysis tasmaniae, Anisomysis mixta australis and Paramesopodopsis rufa was recorded throughout the year. Breeding was intensive from spring till the end of autumn for the three species. Calculation of the egg ratio for each species showed that their major reproductive peaks occurred during spring and summer. A winter depression in the breeding cycle was observed for T. tasmaniae and P. rufa, but A. mixta australis ceased breeding during winter. Seasonal variation in the length of gravid females and number of young carried was evident for these three species. Females were longer in spring and summer and carried more young than in autumn and winter. A linear relationship between female length and brood size was demonstrated for each species; annual and seasonal equations were calculated for females carrying each developmental stage. The seasonal equations showed that for a female of given length fecundity was greater during spring than any other season. Natality was estimated to be highest during late spring, summer and early autumn for the three species. No seasonal variation in the size of eggs was evident for the three species. The reproduction pattern of T. tasmaniae, A. mixta australis and P. rufa appears to be very similar to that reported for the majority of iteroparous coastal temperate mysids throughout the world.     

Early reproduction and increased reproductive allocation in metal-adapted populations of the terrestrial isopod Porcellio scaber

Organisms inhabiting metal-contaminated areas can be stressed by metal exposure and are possibly subject to selection, resulting in increased metal tolerance and changes in growth and/or reproduction characteristics. In a previous study it was found that in the terrestrial isopod Porcellio scaber, sampled from the vicinity of a zine smelter, the body size was small and the brood size was large compared to isopods from a reference area. To assess whether these differences were due to genetic differentiation between strains, isopods collected from a reference wood, a zinc smelter area and a lead mine were cultured on non-polluted food, while growth, reproduction and metal concentrations were studied in first and second laboratory generations. The isopods from the three populations differed in age and weight at first reproduction, although there were hardly any differences in growth. The females of the mine and the smelter population started to reproduce earlier, at a lower weight, which resulted in fewer young per female. However, reproductive allocation (=wight of young relative to the weight of the mother) was higher in mine and smelter isopods. We conclude that the isopods at the metal-contaminated sites have been selected for early reproduction and increased reproductive allocation. The results indicate that populations inhabiting metal-polluted sites have probably undergone evolutionary changes. This study showed that growth and reproduction characteristics of different populations under laboratory conditions may provide information on selection processes in the field.