Do cavity‐nesting primates reduce scent marking before retirement to avoid attracting predators to sleeping sites?

The largest population of endangered golden lion tamarins (Leontopithecus rosalia, GLTs) decreased from approximately 330 to 220 individuals between 1995 and 2000 due to a dramatic increase in predation at sleeping sites. We used behavioral data from eight social groups in this population to test two hypotheses: First, if GLTs attempt to mitigate the risk of predation at sleeping sites, they should reduce their rates of scent marking just prior to retirement. Second, if the benefits of scent marking prior to entering the sleeping site merit an increase in the rate of marking, then tamarins should increase their rate of pre-retirement scent marking during the breeding season, when such behavior would have its greatest impact on reproductive fitness. We used a generalized linear model (GLM) repeated-measures analysis to compare rates of daytime scent marking with rates of marking just prior to retirement for males and females. In addition, we compared scent marking prior to retiring in the nonbreeding season to marking rates before retirement in the breeding season for males and both sexes considered concurrently. Contrary to our expectations, GLTs significantly increased their rates of scent marking during the 30 min prior to entering their sleeping site-an observation driven by an increase in male (but not female) rates of marking. Rates of marking before entering the sleeping site were greater in the nonbreeding season compared to the breeding season, when both sexes were considered concomitantly and when males were evaluated alone. We conclude that GLTs do not attempt to minimize predation risk by decreasing scent marking in the period before they enter their sleeping site, and that tamarins do not scent mark at this time of day in order to transmit information about reproductive status or to control reproduction of subordinates. We speculate that scent marking in the 30 min prior to entering sleeping sites may serve to reduce predation risk by enabling tamarin groups to return quickly to favored sleeping sites in the evening when crepuscular predators are active.     

Sociosexual development,pair bond formation,and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus)

The effect of various social environments on sociosexual behavior was examined in six young female cotton-top tamarins (Saguinus oedipus oedipus) and in three established breeding females. Behavioral observations and hormonal samples were collected on young females while they were living with their families, when they were isolated from conspecifics, and after they were paired with an unrelated male. While living with the family, all females showed a suppression of fertility and low frequencies of sociosexual behavior. Following removal from the family, isolated females displayed an increase in rate of scent marking and an increase in hormonal levels. When young females were paired with males, they were exposed to scent secretions from their natal families, from an unfamilar family, and from a control for a total of 24 weeks. After pairing, hormonal levels increased dramatically, and ovarian cyclicity began. An increase in sociosexual behavior and elevated levels of scent marking accompanied this physiological change. Newly paired females had higher rates of affiliative behavior and scent marking than did established breeding females. However, both newly paired and established breeding males were more likely to initiate contact, grooming bouts, and social sniffing than were females. Time to first ovulation was later in females who were exposed to scent secretions from their natal families than it was in those females given a control for the first 8 weeks following pairing. No female conceived during exposure to scent secretions. However, once normal ovarian cycling had begun or a pregnancy was established, exposure to scent secretions had no effect. Thus, the social environment influences the fertility, sociosexual behavior, and pair bond formation of cotton-top tamarins. In addition, chemical stimuli found in the scent secretions produced by the natal family are most likely involved in reproductive suppression.     

The role of scent marking in the social communication of wild golden lion tamarins, Leontopithecus rosalia

The role of scent marking in the social communication of mammals is widely variable. One reason for this variation is that the function of scent marking may vary with different ecological and social conditions. The purpose of this study was to test four nonexclusive hypotheses explaining the role of scent-marking frequency in different ecological and social contexts for wild golden lion tamarins. Relative to ecological contexts, we compared scent-marking frequency during seasons of abundant and scarce food resources. Relative to social contexts, we compared scent-marking frequency when groups were isolated and when groups were in the presence of neighbouring groups. We found that the tamarins used scent marking to mark the location of food resources. Additionally, males used scent marking to communicate intrasexual dominance within their groups, while females did not. Our results also indicate that alpha females increased their scent-marking frequency to communicate to members of other groups, while the presence of members of other groups did not elicit a similar response by alpha males. We did not find evidence for a territorial function of scent marking in golden lion tamarins. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Sex Differences in Olfactory Communication in Saguinus labiatus

We assessed behaviors involved with depositing and receiving scent in three captive heterosexual pairs of red-bellied tamarins (Saguinus labiatus). The frequencies of scent deposition and scent investigatory behaviors differed between the sexes. Females scent marked exclusively by the anogenital gland. Males deposited 95.8% of scent marks via the anogenital gland and 4.2% via the sternal gland. Females scent marked at a significantly higher rate than that of males (0.9 ± 0.1 versus 0.3 ± 0.1 per 20 min, respectively). Males investigated the scent of their opposite-sex partners whereas females investigated no male scent. Mean ± SEM latency for males to investigate female scent was 208.7 ± 65.0 sec. Around 9% of all scent marks were overmarked within 8 min and there was a nonsignificant trend for males to overmark the scent of their female partners than vice versa. We discuss the sex differences in olfactory communication in red-bellied tamarins in terms of sexual selection theory.     

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax)

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.     

Neonatal and pubertal development in males of a cooperatively breeding primate, the cotton-top tamarin (Saguinus oedipus oedipus).

In cooperatively breeding groups of mammals, reproduction is usually restricted to a small number of individuals within the social group. Sexual development of mammals can be affected by social environment, but we know little regarding effects of the cooperative-breeding system on males. Cotton-top tamarin (Saguinus oedipus oedipus) offspring typically do not reproduce in their natal group, even though they may be physically mature. We examined neonatal and pubertal development in captive male cotton-top tamarins as an example of reproductive development within a cooperative-breeding system and to compare cotton-top tamarins with the general primate model. Puberty was characterized using both hormonal and physical measures. Data were collected on urinary levels of LH, testosterone (T), dihydrotestosterone (DHT), cortisol, and the ratio of DHT to T; testicular development; body weight; and breeding age. We determined that 1) pubertal LH secretion began at Week 37, 2) a surge of T secretion followed at Weeks 41-44, and 3) an increase in the metabolism of T to DHT may have occurred at an average age of 48.6 wk. Most of the rapid weight gain was completed by Week 24, before hormonal increases and rapid scrotal growth. We concluded that rapid pubertal testicular growth in captive cotton-top males was completed by an average 76 wk, but that completion of the individual pubertal spurt can occur between 56 and 122 wk. In a cooperative-breeding system, the opportunity for successful reproduction is dictated by the social environment, but we found no evidence that male offspring were developmentally suppressed in their natal social groups. Our findings suggest that puberty in male New World callitrichid primates occurs more quickly than puberty in Old World primates, even though both have similar patterns of development.     

Effects of age, sex, and reproductive status on scent marking frequencies in the golden lion tamarin, Leontopithecus rosalia

This study reports on the longitudinal changes in scent marking frequencies of male and female lion tamarins in relation to age, reproductive status, and group composition. Juvenile males and females in family groups and subordinate males in trios (2 males, 1 female) scent marked infrequently. Juvenile females scent marked less than juvenile males and began scent marking later. Adult pair-bonded males and females scent marked with similar frequencies. Females showed scent marking increases during mid-pregnancy, but their scent marking decreased both before and again after parturition. Both males and females exhibited decreases in scent marking while transporting dependent infants.     

Social and developmental influences on urinary androgen levels in young male white-faced marmosets (Callithrix geoffroyi)

Callitrichine primates (marmosets and tamarins) often remain in their natal groups beyond the time of sexual maturity. Although studies have characterized the development of female reproductive function in callitrichine offspring, less is known about the male reproductive development. To document reproductive development in male marmosets, we monitored urinary androgen (uA) excretion in males housed in a captive colony of white-faced marmosets (Callithrix geoffroyi). Young male marmosets showed relatively low and stable rates of uA excretion early in life, with elevated production at the end of the juvenile period (9-10 months) and again at the onset of adulthood (16 months). uA levels of adult breeding males were also measured to compare to adult-aged sons. Although breeding males did have higher uA levels than their adult-aged sons, these differences did not reach conventional levels of significance. Evidence from some other reports has suggested that androgen levels of males in other species are influenced by social factors, such as the presence of a sexually receptive female or of dependent offspring. In this study, however, uA levels did not vary, based on their mothers' pregnancy status or the presence of younger siblings in the natal group. Patterns of androgen excretion in the white-faced marmoset roughly reflect those of other callitrichine species. Furthermore, unlike callitrichine daughters, gonadal activity in sons does not seem to be sensitive to within-group social cues.     

Chemical communication of reproductive status in female cotton-top tamarins (Saguinus oedipusoedipus)

Among Callitrichids, scent secretions have been identified as carrying information regarding species, subspecies, gender, social status, individuality, hormonal status, and timing of ovulation. We propose that information regarding familiarity and reproductive status is also communicated. Seven male–female pairs of cotton-top tamarins (Saguinus oedipus oedipus) were presented with several drops of distilled water, a scent secretion from the female of that pair, scent secretions from unfamiliar, reproductively mature but noncycling females, and scent secretions from unfamiliar, reproductively cycling females. Behavioral responses from both males and females were recorded over a 10 min period. Differences in behavioral response for both males and females were significant across all four conditions. This indicates that cotton-top tamarins are capable of discriminating a familiar scent from an unfamiliar scent as well as the reproductive status of an unfamiliar female. The communication of this information may play an important role in regulating mate selection, reducing reproductive competition, and stabilizing transfers in and out of groups in the wild. Am. J. Primatol. 45:337–349, 1998. © 1998 Wiley-Liss, Inc.     

Characterization and Social Correlates of Fecal Testosterone and Cortisol Excretion in Wild Male <Emphasis Type="Italic">Saguinus mystax</Emphasis>

Reproductive success in male primates can be influenced by testosterone (T) and cortisol (C). We examined them in wild Saguinus mystax via fecal hormone analysis. Firstly, we wanted to characterize male hormonal status over the course of the year. Further we tested the influence of the reproductive status of the breeding female, social instability, and intergroup encounter rates on T levels, comparing the results with predictions of the challenge hypothesis (Wingfield et al., 1990). We also tested for interindividual differences in hormonal levels, possibly related to social or breeding status. We collected data during a 12-mo study on 2 groups of moustached tamarins at the Estación Biológica Quebrada Blanco in northeastern Peru. We found fairly similar T and C levels over the course of the year for all males. Yet an elevation of T shortly after the birth of infants, during the phase of ovarian inactivity of the groups breeding female, was evident. Hormonal levels were not significantly elevated during a phase of social instability, did not correlate with intergroup encounter rates, and did not differ between breeding and nonbreeding males. Our results confirm the challenge hypothesis (Wingfield et al., 1990). The data suggest that reproductive competition in moustached tamarins is not based on endocrinological, but instead on behavioral mechanisms, possibly combined with sperm competition.     

Social Polyandry and Multiple Paternity in the Omei Treefrog in the Southwest China

Group spawning,polyandry reproductive behaviors,and multiple paternity are increasingly reported in anuran species.The Omei treefrog(Rhacophorus omeimontis),endemic to subtropical and mountainous forests of central and southwestern China,is a polyandrous lek-patterned breeder commonly showing multiple males-one female matings during the breeding season.To detect the traits of social and genetic polyandry in this species and explore the relationships between these traits,we investigated the breeding behaviors of a population of R.omeimontis in the Fengtongzhai National Nature Reserve,Baoxing County,Sichuan,China.We conducted paternity analyses using six microsatellite genetic markers.A total of 30 matings were recorded in the field(four monogamous pairs and 26 spawning groups).Our results revealed high proportions of social polyandry(86.7%) and multiple paternity(70.0%) and the numbers of joining males and genetic fathers among matings ranged from 1 to 8 and from 1 to 4,respectively.There was a significantly positive correlation between the intensities of social and genetic polyandry,indicating that multiple males-one female breeding behaviors could be an important promoter of multiple paternity.We considered the intense social polyandry and multiple paternity as consequences of intense male-male competition under a male-biased sex ratio and genetic benefits pursuing of the females.However,the proportion of genetic fathers in a spawning decreased with the increase of joining male number and most of their offspring belonged to a few males.This might be caused by a "making the best of a bad lot" reproductive strategy of the inferior male individuals.     

同时而非先后一雌多雄交配增加不同温度下食蚜瓢虫的适合度（英文）

【目的】尽管一雌多雄在瓢虫科中常见,但各研究中获得的数据不足以解释雌虫多次交配和一雌多雄的一般适应性意义或适合度后果。本研究以温度为胁迫因子,旨在评价一雌多雄的某些益处（如增加的适合度）是否可传递给后代。【方法】本研究检测了黄斑盘瓢虫Coelophora saucia (Mulsant) 3种交配处理中的适合度：一雌一雄（与同一雄虫交配5次,1次/d）,先后一雌多雄（与5头不同的雄虫依次交配5次,即每天与新的雄虫交配1次）,以及同时一雌多雄（放进5头雄虫,任由雌虫选择雄虫,交配5次,1次/d）。观察了各交配处理不同温度下（25, 27和 30℃）繁殖力、卵的育性、后代发育和存活。【结果】结果表明,经历一雌多雄然后进行交配选择或竞争的雌性的繁殖能力最强,后代能在更广温度范围内最好地适应发育和存活。但先后一雌多雄交配的雌性与一雌一雄交配的雌性的繁殖能力相似。【结论】结果说明,在无交配选择或雄性竞争的条件下,一雌多雄的益处不明显。这可能是由于在依次射精的雄性间存在精子竞争,或由于雌性的隐性选择。据我们所知,本研究中观察发现的无交配选择时不表现一雌多雄的益处的现象,之前在昆虫中未观察到过。     

Fitness benefits of polyandry for experienced females

Females often mate with several different males, which may promote sperm competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in birds where recent reviews have suggested that females gain few genetic benefits from extra‐pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of sexual conflict.     

Bimorphism in Male Verreaux’s Sifaka in the Kirindy Forest of Madagascar

Male primates in species with pronounced secondary sexual adornments can exhibit reversible or irreversible bimorphism, i.e., striking variation in the degree to which males express the adornments. Verreaux’s sifaka (Propithecus verreauxi verreauxi) use scent marking as a form of communication and exhibit sex differences in scent glands. Some males exhibit a pronounced brown staining around their sternal gland, whereas others do not. We studied morphological and behavioral characteristics of males in 6 social groups in Kirindy Forest, Madagascar, from November 2000 to March 2002 to evaluate the hypotheses that the bimorphism in male sifaka chest status represents alternative mating tactics and is a badge of status. Males are clearly divided into 2 categories: clean and stained chests, with rare, but informative, intermediate males. The chest staining probably results from the males scent marking with their sternal glands, because stained-chested males scent marked significantly more often than clean-chested males. Though sample sizes are small, chest status did not appear to depend on body size. Chest status is reversible and related to dominance rank. In each group, only 1 male, the dominant, was stained-chested, whereas all other (subordinate) males were clean-chested. These findings suggest that stained chests are visual and olfactory signals of dominance rank and that clean chests signal lack of competitive intent. Thus, this bimorphism may reflect alternative mating tactics used by males to maximize their reproductive success based upon their social environment.     

Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis)

The effects of different social living conditions on estrogen excretion and on the ovarian cycle of saddle back tamarins were investigated. Urinary estrogens were monitored as indices of ovarian cyclicity in groups of adult females living under the following experimental conditions: (1) five parous females, each living with an adult castrated male (in one of the females plasma estradiol and progesterone were also measured); (2) five adult daughters living with their families. Each daughter was then removed from her family and paired with a vasectomized male. After pairing, scent marks collected from the family were introduced daily to one of the daughters and her mate. Scent exposure was then discontinued and hormone excretion measured for several weeks. The remaining four daughters were not exposed to family scent. The females living with castrated males showed urinary estrogen cycles of an average length of 17.5 ± 1.0 days. The plasma estrogen cycle was of the same length. The females studied under condition 2 showed low, noncycling estrogen levels while living in their families. They responded to pairing with an increase in the level of urinary estrogens, and four out of five showed regular estrogen cyclicity. The fifth female exposed to family scent marks after pairing also showed an increase in urinary estrogens. However, as long as scent transfer was maintained, no cycle was observed. Estrogen excretion increased again, and cyclicity commenced when scent transfer was discontinued. It is concluded that ovarian estrogen production is suppressed and cyclicity does not occur as long as daughters live in their families. Release from suppression and perhaps stimulation by the male cause a rapid increase in estrogen levels and the onset of cyclicity. Chemical stimuli produced by the family, perhaps particularly by the mother, may be involved in reproductive suppression.     

Endocrine Monitoring of Wild Dominant and Subordinate Female Leontopithecus rosalia

In captive callitrichid primates, female reproductive function tends to vary with social status. However, little is known about the interplay between these factors in wild groups. We report observations on normative ovarian function in dominant and subordinate female golden lion tamarins (Leontopithecus rosalia) living in wild groups. We monitored ovarian status by measuring, via enzyme immunoassay, concentrations of excreted pregnanediol glucuronide (PdG) and estrone conjugates (E₁C) in fecal samples collected noninvasively from individuals in social groups in the Poço das Antas Biological Reserve, Rio de Janeiro State, Brazil. Dominant breeding females demonstrated steroid levels similar to those previously reported for wild cotton-top tamarin females, with statistically significant rises during pregnancy. The duration of elevation of fecal steroids in breeding females was ca. 4 mo, which corresponds with estimates of gestation from captive studies. Low steroid concentrations from December to June suggest a seasonally-related period of infertility in female golden lion tamarins. Dominant and subordinate females demonstrated several differences in endocrine function. In general, younger females living in intact natal family groups showed no evidence of ovarian cyclicity. We noted endocrine profiles consistent with ovulation and subsequent pregnancy for behaviorally subordinate females living in groups with unrelated males or in which a reversal in female dominance status occurred. Results suggest that in addition to changes in female reproductive endocrinology associated with puberty, the regulation of reproduction in females in wild callitrichid groups can be sensitive to status and relatedness to breeding males.     

Behavioural observations on captive pairs of wild caught tamarins (Saguinus mystax)

Quantitative data are given on 12 categories of behaviour, including scent marking, allogrooming, huddling, and proximity for individual tamarins within 14 male, female pairs and the mated pair of one family group of four animlals. Time sample data were recorded at 30 sec intervals to a total of 260 hr. In addition, some data were collected from within time sample intervals. Individual and intergroup variation in behaviour was a main finding of the study. It was found, however, that females scent marked significantly more than males, at least on the basis of their total marking frequencies, that females tended to groom males more than vice versa, and that although the general proportions of activities were similar in two conditions of housing, their spatial distribution was different under the two conditions. There was very little overt aggression among the pairs.     

Saddle-back tamarin (Saguinus fuscicollis) reproductive strategies: Evidence from a thirteen-year study of a marked population

We monitored a population of four to seven groups of individually marked saddle-back tamarins (Saguinus fuscicollis; Callitrichidae) at the Cocha Cashu Biological Station in Peru's Manu National Park every year from 1979 through 1992. In this paper we use data on life histories, group compositions, group formations, and dispersal patterns collected during these 13 years to examine the reproductive strategies of males and females. Group compositions and mating patterns were quite variable in this population, with both monogamy and cooperative polyandry common. In polyandrous groups, two males shared a female's copulations and cooperatively cared for her young. Although most groups contained a single breeding female, we recorded four cases in which secondary females successfully reared young. Most young females appeared to wait in their natal groups for the first opportunity to fill a primary breeding position in their own or a neighboring group. Females that acquired primary breeding positions maintained those positions for a mean of 3 years. No female was observed to transfer between groups a second time. Variation in female lifetime reproductive success was high. Half of the females marked as juveniles never bred; the other half produced an average of 3.5 young. A paucity of female breeding opportunities may explain the high mortality of females between 2.5 and 4.5 years of age and the resulting male-biased adult sex ratio. The majority of groups contained more than one probable male breeder. Polyandrous groups included both related and unrelated males. Behavioral differences between Cocha Cashu tamarins and other studied populations may result from the pressures of living in an environment inhabited by nine other primate species and numerous predators. © 1996 Wiley-Liss, Inc.     

Evolution of polyandry in a communal breeding system

The evolution of polyandry requires an asymmetrical factor thatfavors more matings per breeding female than per breeding male,thus reversing Bateman's principle. Here a model is presentedfor the evolution of avian cooperative polyandry. The modelshows that polyandry can evolve if communal breeding is initiallyadvantageous and if increasing clutch size beyond an optimumis detrimental. The advantage of communal breeding favors theaddition of more breeders (either males or females) and thusselects against breeding as single pairs (monogamy). The optimaldutch size creates the asymmetry that favors adding male breeders(polyandry) over adding female breeders (polygyny). Adding femalesis detrimental because females must lay eggs to reproduce andcan therefore increase the clutch size of the group. On theother hand, males can reproduce by sharing paternity withoutincreasing dutch size. It is shown that cooperative polyandryevolves either because it maximizes both male and female fitnessor because polygyny and monogamy are behaviorally unstable.Data from acorn woodpeckers support the assumptions of the modeland suggest that cooperative polyandry evolved because it isbehaviorally more stable. The persistence of monogamy and polygynyin acorn woodpeckers (at a lower incidence than polyandry) isalso examined. Polygyny in these birds represents a case ofthe Prisoner's Dilemma     

Extra-pair paternity in the Skylark Alauda arvensis

We present the first quantitative data on the genetic breeding system of a lark (Alaudidae), the Skylark Alauda arvensis . Using a set of eight microsatellite loci isolated in a variety of passerine species, we genotyped 171 offspring from 52 broods of Skylark and detected 35 extra-pair offspring (20%), in 14 different broods (27%). All offspring matched their putative mother, so there was no evidence of intraspecific brood parasitism. Previous non-genetic studies had suggested that the species was predominantly socially monogamous, with only rare occurrences of social polygyny and polyandry, although some behaviours, such as mate guarding, did suggest the possibility of extra-pair copulations. The relatively high level of extra-pair paternity in this species is likely to affect the variation in male reproductive success because extra-pair paternity was non-randomly distributed amongst males, with those with shorter wings more likely to be cuckolded.