Foraging energetics in patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus): implications for reproductive seasonality

The patas monkeys (Erythrocebus patas) in Kala Maloue, Cameroon, have their birth season in the mid-dry season, whereas closely related, sympatric tantalus monkeys (Cercopithecus aethiops tantalus) have their birth season in the wet season. To evaluate the optimality of a species-specific birth season, I estimated the daily intake of available energy and gross protein, and energy expenditure for one individual of each sex of each species between respective birth and mating seasons. The monkeys obtained a larger amount of available energy and gross protein in the birth season than in the mating season. No significant seasonal differences in energy expenditure between the birth and mating season were found. Thus, the birth season appears to be timed to the season when the monkeys can obtain more surplus energy and protein. Interspecific differences in the optimality of birth season were attributed to widely exploitative foraging, supported by the patas' high locomotive ability, which may enable them to obtain more energy from seeds of Acacia seyal and gums of A. sieberiana, and more protein from grasshoppers and seeds of A. seyal in the mid-dry season than the tantalus monkeys. A review of preceding studies suggests that the availability of seeds of Acacia fruiting during the dry season may exert the dominant influence on timing of birth not only in patas but also in savanna monkeys (Cercopithecus aethiops), which include the tantalus monkeys.     

Patterns of mating among male patas monkeys (Erythrocebus patas) in Kenya

An habituated group of wild patas monkeys was observed in Kenya for 550 h in 1984. Observations were made primarily during an interval that, as previous studies at the same site had demonstrated, coincided with the annual mating and conception periods. Earlier field studies of patas at other sites had reported that heterosexual patas groups had only a single resident adult male and that mating was harem-polygynous. At the Kenya site, by contrast, as many as six males were simultaneously resident and mated in the group during the conception period. Males adopted a variety of tactics to gain access to receptive females, ranging from opportunistic mating to attempts at sequestration that resembled consort behavior in other cercopithecoids such as savanna baboons and rhesus macaques. Aggressive competition for access to females took place among the males, although the number of completed copulations per male did not bear a positive relation to agonistic dominance rank. For patas monkeys, harem polygyny is only one available option within an overall mating system that is best described as a form of promiscuous polygyny, especially during periods when conception is most likely.     

Seasonal, sex, and interspecific differences in activity time budgets and diets of patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus), living sympatrically in northern Cameroon

I examined seasonal, sex, and interspecific differences in activity time budgest and diets of patas (Erythrocebus patas) and sympatric tantalus monkeys (Cercopithecus aethiops tantalus) on the basis of 5-day data sets collected in three and two different seasons, respectively, by the method of focal animal sampling. The seasons included species-specific mating and birth seasons. As compared with not only the birth season but also conspecific females, both patas resident male and tantalus male spent less time feeding and more time resting, day and night, in their respective mating seasons. Given that day-resting time includes time for vigilance for non-resident males and receptive females, this may reflect that males should minimize time spent feeding to allow maximum participation in other fitness-increasing activities such as mating-relating activities asSchoener (1971) predicted. In both species, the males consumed fruits containing less protein but more calories and showed a high feeding rate to compensate for the shorter time spent feeding in the mating season. In contrast, females consumed protein-rich food types (i.e. animals, protein-rich seeds, leaves, and flowers) in the birth season to meet the high demand for protein due to pregnancy and lactation. Given that the season for males was considered to be not a calendar but a reproductive “season” (i.e. mating or birth season), both sexes of patas spent more time moving and less time day- and night-resting than did the tantalus counterparts irrespective of the “season”. Patas subsisted on fruits, gums, and supplementarily lipid-rich seeds as an energy source and animal matters and protein-rich seeds as a protein source. In contrast, tantalus subsisted on fruits and lipid-rich seeds as energy and flowers and leaves as protein.     

Social and environmental determinants of reproductive cycles in patas monkeys

The menstrual cycles of a captive group of patas monkeys were followed for 15 months by taking vaginal smears and lavages three times a week. Without an adult male in the group, menstrual cycles still showed the expected qualitative changes previously associated with the onset and with the end of a mating period. The addition of an adult male to the female group, once mating season cycles were evident, did not result in further changes in erythrocytes or sediment levels in vaginal samples or cycle regularity. Menstrual-cycle onsets for related females were significantly more synchronized than onsets for unrelated females. Preliminary observations on adult male patas housed separately from the females indicate that they too undergo seasonal changes in physiology and behavior.     

The finding of an inverse relationship between social dominance and feeding priority among pairs of unfamiliar adult male vervet monkeys (Cercopithecus aethiops sabaeus)

Dominance is often presumed to confer priority of access to resources. This study evaluated the relationship between two assessments of dominance: (1) social dominance, based on agonistic interactions and (2) feeding priority among pairs of unfamiliar adult vervet monkeys (Cercopithecus aethiops sabaeus) differing in scrotal colour, but matched for height, weight and testicular volume, during paired introduction experiments. Results of this investigation showed that neither size differences nor scrotal colour were predictive of feeding priority, and social dominance was inversely related to feeding priority. This finding demonstrates that different assessments of dominance can yield different outcomes even within the same primate taxon. I propose that male dominance rank may best predict access to resources when there is direct contest competition over a resource, which is not immediately exhaustible, whereas highly impulsive low ranking males may gain a competitive edge in scramble competitions for ephemeral and small resources.     

Male Competition,Mating Success and Female Choice in a Seasonally Breeding Primate (Erythrocebus patas)

Mammals with restricted breeding seasons often show brief but intense bouts of male competition for mates and male reproductive success has been attributed to male competitive abilities, with the most aggressively successful males able to control access to fertile females, or with females choosing to mate with such males. We studied male competition, mating behaviour and female mate selection in patas monkeys, a primate with a restricted breeding period. We observed two habituated patas groups in Laikipia District, Kenya, during Jun.-Aug. 1983. During the study, one group had a single resident male while the other group had multiple adult males. Within the multimale group, experienced adult males were no more successful than the subadult male. The sole resident male had a significantly higher rate of fights won (p < 0.02) although he did not differ from the multimale group males in rate of aggression or initiation of fights. We found no significant differences in either mating success or female preference based on males' experience or residency. The rates at which males copulated with and were solicited by females were not significantly correlated. We found no evidence of stable dominance ranks among males in the multimale group and aggressive success was not significantly correlated with copulation rate for males in the multimale group. Subadult males were responsible for the majority of copulations observed during the final third of the breeding season. Our observations of this patas population showed a fluid number of males in groups, with the same groups able to shift rapidly from single to multimale structure. This fluidity may result from the large fluctuations in numbers of breeding-age males and females observed over 4 yr of studying this population.     

Male Demography,Female Mating Behavior,and Infanticide in Wild Patas Monkeys (Erythrocebus patas)

Infanticide by males has been hypothesized to be a naturally selected behavioral strategy that increases the infanticidal male's reproductive success. The sexual selection hypothesis has been challenged via alternative, nonadaptive hypotheses that dispute its empirical and theoretical bases. Two of the most widely recognized alternatives are the social pathology hypothesis, in which infanticide results from overcrowding or recent human disturbance, and the generalized aggression hypothesis, in which infanticide is an epiphenomenon of increased male aggression. We report the first case of infanticide in wild, seasonally breeding patas monkeys (Erythrocebus patas) living at a low population density in a stable habitat, conditions which do not support the social pathology hypothesis. Its exceptional occurrence is consistent with the sexual selection hypothesis: over a 7-year period the infanticidal male was the only one of 13 resident males that was not present during the actual conception season but was present during the following birth season. Also consistent with this hypothesis, mothers were differentially targeted for male aggression, which increased sevenfold during the days surrounding the infanticide and then decreased to baseline levels after the infanticide. Aggression targeted at mothers does not support the generalized aggression hypothesis. As predicted by the sexual selection hypothesis, females began soliciting mating immediately after the infanticide, despite its occurrence in the nonconceptive season.     

Mating strategy and reproductive success of male patas monkeys (Erythrocebus patas)

Mating behavior and paternity of offspring of wild patas monkeys were studied at Kala Maloue National Park, Cameroon. Observation of patas groups over three years revealed that multi-male situations occurred after takeover of the position of a resident male. Direct observation of behavior showed that resident males (harem males) occupied only 31% of mating in multi-male situations and 100% in one-male situations. DNA-typing revealed that resident males sired two of four of infants in the one-male situation and four of five in the multi-male situation. Under the two years cycle of the one-male situation and the multi-male situation, calculation shows that resident males sired more offspring than sneakers both in observation and paternity testing. Sneak mating occurred during both one-male and multi-male situations, and resident males performed compensatory mating, with dilution of sneaker sperm; these activities explain the discrepancy found between observation of mating and results of paternity discrimination.     

Sexual harassment among captive patas monkeys (Erythrocebus patas)

Observations of the sexual harassment occurring within a captive group of patas monkeys are reported. Immature males performed most harassing attacks, while immature and adult females were infrequent harassers. The adult male of the group appeared to be the object of the majority of attacks, and on occasion the male’s copulatory behavior was modified by harassment. It is hypothesized that the harassing attacks performed by immature patas monkeys may be based upon (a) the excitatory effect of witnessing adult sexual interactions, and (b) the approach/withdraw conflict experienced during close approach to the adult male. The preservation of the one-male group structure is suggested as a possible function of sexual harassment.     

Differential habitat utilization by patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) living sympatrically in northern Cameroon.

In order to obtain reliable evidence for differences in habitat preferences between two closely related savanna-dwelling primate species, namely, patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus), I collected data on vegetation and patterns of range use concurrently at a single study site, Kala Maloue, Cameroon, in a similar manner for a group of each species. Kala Maloue consisted of 64% grassland mostly dominated by Gramineae spp. and the rest was woodland. Tantalus monkeys showed preference for woodland, especially gallery forest, much more than did the patas irrespective of the season. Moreover, patas preferentially established their home range in grassland in the wet season. Interspecific and seasonal differences in habitat preferences could be interpreted on the basis of interspecific and seasonal differences in preferences for main food. In dry season, tantalus utilized water-containing areas at a frequency closely in proportion to the availability of such areas while the patas utilized water-containing areas more frequently than expected. This is because tantalus established a smaller home range along the river where water was never completely depleted throughout the dry season. Both the patas and the tantalus preferred woodland to grassland as sleeping sites possibly owing to predation avoidance. Both the daily travel distance per group weight and the home range size per group weight were greater for patas than for tantalus partly because of higher preference for grassland with low habitat quality in the case of patas. It is suggested, however, that high locomotive ability enabled patas to effectively utilize small and widely dispersed items of food such as grasshoppers and to explore areas with high availability of food and water and with preferable sleeping sites.     

Seasonal changes in plasma concentrations of immunoreactive inhibin and testicular activity in male Japanese monkeys

Seasonal changes in plasma immunoreactive (ir-) inhibin, testosterone, LH, and FSH concentrations were examined in five sexually mature male Japanese monkeys (Macaca fuscata fuscata) housed indoors individually, to explore the reproductive cyclicity in the male. Blood samples were collected monthly throughout one year, and testicular size, semen volume, and number of sperm in the semen were ascertained at the same time in the same animals. Semen samples were obtained by penile electrostimulation. The results showed a clear seasonal increase in all parameters: plasma ir-inhibin, testosterone, testicular size, semen volume, and total number of sperm in the liquid portion of the semen during the autumn and winter months in synchrony with the natural breeding season. In contrast, plasma LH and FSH remained unchanged throughout the year, although plasma FSH tended to increase during the breeding season concomitant with an increase in plasma ir-inhibin. A significant positive correlation between FSH and ir-inhibin was observed in two of five monkeys. The positive correlations between plasma ir-inhibin and testicular activities during both the developing and regressing phases of the testicular cycle indicate that plasma ir-inhibin is a useful indicator of testicular activity as well as an indicator of Sertoli cell function in the Japanese monkey.     

Despotic wild patas monkeys (Erythrocebus patas) in Kala Maloue, Cameroon

The socio-ecological model predicts that the quality, distribution, and patch size of food resources determines the dominance hierarchy of female monkeys based on the type of food competition they experience. Comparative studies of closely related species have evaluated the socio-ecological model and confirmed its validity. For example, female patas monkeys in Laikipia, Kenya, form a nonlinear and unstable dominance hierarchy (i.e., egalitarian), whereas females of sympatric, closely related savannah monkeys form a linear and stable dominance hierarchy (i.e., despotic), in accordance with the model's predictions of the characteristics of food resources. I compared agonistic interactions involving food between patas monkeys (Erythrocebus patas) and sympatric savannah monkeys (Cercopithecus aethiops) in Kala Maloue, Cameroon. I found linear dominance hierarchies not only in savannah monkeys, but also in patas monkeys in Kala Maloue. The rates of agonistic interactions during feeding between patas monkeys were equivalent to those between savannah monkeys in Kala Maloue; further, these rates were significantly higher than those of both Laikipia patas and savannah monkeys. The results imply that patas monkeys in Kala Maloue are not egalitarian, but are despotic, similar to savannah monkeys. Disparity in the dominance hierarchies of patas monkeys between Kala Maloue and Laikipia were attributable to the differences in the characteristics of food resources. Although patas monkeys in Laikipia subsist on small and dispersed food resources within a high-density area, those in Kala Maloue subsisted on food resources that were clumped in intermediate-sized patches within a low-density area. This study shows that the socio-ecological model is applicable not only for interspecific comparisons but also for intraspecific comparisons.     

Mating and Residence Patterns of Male Patas Monkeys

A longterm study of a population of patas monkeys (Erythrocebus patas) in Kenya indicated fluid male residence patterns. While a single adult male was present in each of the two main study groups for most of each year, several males were present and mating in groups during some conception periods. Tenures of males in heterosexual groups were generally short; some males were resident in both groups and some had more than one tenure in the same group. When not in heterosexual groups, males lived as solitaries or in all-male associations.     

Effects of season and social interaction on fecal testosterone metabolites in wild male giant pandas: implications for energetics and mating strategies

In the first-ever study of reproductive endocrinology in wild male giant pandas (Ailuropoda melanoleuca), we provide new insights into the reproductive ecology of the species. We tracked and observed pandas in Foping Nature Reserve of the Qinling Mountains for 3 years, collecting fecal samples for testosterone metabolite analysis and data on reproductive activity. Males encountered multiple potential mates and competed for reproductive access to females. Male testosterone metabolites increased in February, peaked in March and April, and fell back to baseline after the mating season. However, males did not maintain a high testosterone level throughout the mating season. Male testosterone instead peaked during encounters with potential mates and declined between encounters. These results indicate that testicular activity is typically dormant until mobilized by interactions with females and potentially by interactions with male competitors. This suggests that male pandas may be energetically constrained, elevating testosterone levels only when necessary to meet the demands of intrasexual competition and courtship and fertilization of females. Maintaining a high testosterone level is metabolically expensive and male pandas enter the mating season during a period of low food availability. If this hypothesis is correct, male panda body condition may be an important determinant of reproductive outcome, and anthropogenic activities that diminish foraging resources may have significant impacts on the mating ecology of the species, affecting its conservation.     

黄山短尾猴繁殖的季节性和雌性性活动方式

1987年开始,我们对中国黄山的短尾猴(Macaca thibetana)的性和繁殖行为进行了研究。本文根据1992年全年野外观察,对黄山短尾猴的繁殖季节性和雌性性活动方式进行深入研究,以揭示短尾猴繁殖方式和雌性性行为如何影响雄性性行为。研究采用全事件取样和目标动物取样法。结果表明,短尾猴黄山种群的交配和产仔是季节性的：交配季节发生在7月至12月,其特征是交配频率高并伴有射精;产仔季节为1月至4月。交配季节之外的交配虽有少量发生．但交配频率很低且几乎不射精。成年雌性的会阴部有轻微肿胀的性皮,但性皮的大小和颜色既不随猴群繁殖季节变化,也不随雌性个体生理周期变化。同时,雌性缺乏典型的性要求的行为——发情。因此,我们认为雌性短尾猴倾向于隐蔽自己的排卵。对46个连续观察日中成年雄性对雌性的性行为分析还表明：雄性能够区别潜在繁殖和不繁殖的雌性但不能对同一雌性的生理状况做出准确判断。隐蔽排卵是雌性在性接受期间接受大量交配的主要原因。本研究否定了短尾猴的交配是非季节性的假设(Wadaand Xicmg,1996)[动物学报51(3)：365—375,2005]。     

白马雪山自然保护区响古箐滇金丝猴（Rhinopithecus bieti）的交配行为

灵长类交配模式是灵长类社群结构和婚配制度的重要表征之一,其研究有助于了解灵长类社群结构和两性交配策略。2013年11月至2014年10月,我们对云南白马雪山国家级自然保护区一人工辅助投食滇金丝猴群进行了观察研究,采用焦点动物取样法和全事件记录法收集了雌雄个体的交配相关的行为数据,主要包括邀配对象、交配过程、持续时间和回合数,以及参与交配的雌雄对在交配结束后的相互理毛的持续时间和回合数。研究结果表明：研究群滇金丝猴全年均有交配行为,交配高峰期在7-9月,两性参与交配的积极性和对季节变化的响应不同;交配主要由雌性通过邀配发动（76%）,交配高峰期也是雌性邀配的高峰期;雄性爬跨频次（年均0.43次/月,n=5）和射精爬跨比（年均19%,n=5）则在全年无显著变化。交配行为发生的典型表现为：雌性通过小跑或跳跃进入雄性视线范围内,爬伏呈臀向雄性邀配;雌猴爬伏时离雄猴的远近距离不同（<1m vs. 2-5m ： 69% vs. 31%）会影响其邀配成功率（<1 m vs. 2-5 m ：68% vs. 40%）;若一次邀配失败,雌猴可能会连续爬伏邀配（最多4次）,连续多次邀配的成功率显著高于单次邀配（79% vs. 52%）。交配结束后雌性会主动为雄性理毛,但雌性主动理毛与交配是否射精无关。     

Differences among isolates of simian hemorrhagic fever (SHF) virus

Simian hemorrhagic fever (SHF) virus is a member of the Togaviridae family which currently is unclassified to genus. We have studied the relatedness of four different SHF virus isolates obtained from infected macaque or patas monkeys. Differences were found among isolates in type and severity of disease produced in patas monkeys, cell sensitivity to infection, viral antigens, and levels of specific antibody induced in patas monkeys. Based on these criteria, the four isolates have been grouped in two categories: those producing acute infections in patas monkeys (LVR, P-180) and those producing persistent infections (P-248, P-741). The P-180 isolate induced the most severe disease in experimentally infected patas monkeys, but only occasionally were their infections fatal. Persistently infected patas monkeys were viremic over a period of years, but showed no signs or symptoms of infection. All four isolates were found to be antigenically related by use of enzyme-linked immunosorbent assay (ELISA); the P-248 isolate showing the weakest antigenic relationship. However, none of the four isolates induced cross-neutralizing antibodies in infected patas monkeys. High titers of specific IgG antibody (up to 31,250 as determined by ELISA) were induced in acutely infected patas monkeys (LVR, P-180), but antibody was barely detectable (less than or equal to 50) in persistently infected patas monkeys (P-248, P-741). LVR lytically infected USU-104 cells, patas monkey peritoneal macrophages (PMAC), and rhesus monkey PMAC. The P-180 isolate lytically infected both patas monkey PMAC and rhesus monkey PMAC, but not USU-104 cells. The isolates producing persistent infections (P-248, P-741) lytically infected only rhesus monkey PMAC. These results show that marked differences exist among isolates of SHF virus from naturally infected animals. These differences should be useful in categorizing new isolates.     

Male aggression and the sexual behavior of Japanese monkeys

The factors that regulate male aggressive behavior towards females during the mating season and their relationship to the sexual behavior of Japanese monkeys were investigated. Observations were made on the Shiga A troop in Nagano Prefecture for 132 days during both the non-mating and mating seasons in three successive years. As a result, chasing towards females was observed in males older than 4 years. The frequencies of this type of behavior increased in the mating season. The chasing rank of the individual males did not correlate with the male dominance rank but with the tree-shaking rank. Chasing was directed not only at estrous females but also at non-estrous females. Pairs of both sexes in which chasing was observed, tended to have sexual interactions. Both hormonal and social factors should be considered in the regulation of chasing. The role of aggression in the formation of new male-female bonds in discussed.     

Age at sexual maturity of males and timing of the mating season of polar bears (Ursus maritimus) in Greenland

Age at sexual maturity among male polar bears (Ursus maritimus) and timing of the mating season were studied by microscopic and macroscopic analysis of the reproductive organs from 165 male and 92 female Greenland polar bears. Males became sexually mature in the spring following their fifth birthday. Testes sampled during the spring reached 95% of their asymptotic length at 5.8 years. Some spermatozoa were found in 2- to 4-year-old bears during the spring, but only in low concentrations in a mixture of other cell types. The first corpus luteum was found on 1 April and most ovulations were estimated to occur before mid-May which indicate that the peak of the mating season begins in late March and ends in May. These findings are somewhat different from a similar study from Svalbard, where the mating season is estimated to peak later and male polar bears are found to become mature earlier. We hypothesize that these differences occur because adolescent males have their peak testicular activity after the main breeding period and therefore appear to be fully sexually mature during summer and not during spring.     

Long-term study of the social dynamics of patas monkeys (<Emphasis Type="Italic">Erythrocebus patas</Emphasis>): group male supplanting and changes to the multi-male situation

Data on social changes in patas monkey (Erythrocebus patas) groups were collected to clarify the general characteristics of male supplantation and to evaluate the overall role of supplanting in patas society. Seven patas groups were observed in Kala Maloue National Park, Northern Cameroon for 11 years. Analysis of this data revealed that social change, such as male supplanting, was restricted to the mating season. Male supplanting occurred in the course of outsider males seeking to gain access to estrous females within the heterosexual group and supplanting was inevitably followed by a multi-male situation arising in the group. Many cases of multi-male invasion were preceded by the supplanting of resident males and the multi-male situation arose due to a temporary absence of serious aggression towards invader males by the new resident males. Notably, an all-male group was found only once and it did not contribute to the supplanting of resident males in the one-male group. Electronic Publication