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1.  Long-Term Oocyte-Like Cell Development in Cultures Derived from Neonatal Marmoset Monkey Ovary 
Stem Cells International  2015;2016:2480298.
We use the common marmoset monkey (Callithrix jacchus) as a preclinical nonhuman primate model to study reproductive and stem cell biology. The neonatal marmoset monkey ovary contains numerous primitive premeiotic germ cells (oogonia) expressing pluripotent stem cell markers including OCT4A (POU5F1). This is a peculiarity compared to neonatal human and rodent ovaries. Here, we aimed at culturing marmoset oogonia from neonatal ovaries. We established a culture system being stable for more than 20 passages and 5 months. Importantly, comparative transcriptome analysis of the cultured cells with neonatal ovary, embryonic stem cells, and fibroblasts revealed a lack of germ cell and pluripotency genes indicating the complete loss of oogonia upon initiation of the culture. From passage 4 onwards, however, the cultured cells produced large spherical, free-floating cells resembling oocyte-like cells (OLCs). OLCs strongly expressed several germ cell genes and may derive from the ovarian surface epithelium. In summary, our novel primate ovarian cell culture initially lacked detectable germ cells but then produced OLCs over a long period of time. This culture system may allow a deeper analysis of early phases of female primate germ cell development and—after significant refinement—possibly also the production of monkey oocytes.
doi:10.1155/2016/2480298
PMCID: PMC4655298  PMID: 26664406
2.  Urinary neopterin, a non-invasive marker of mammalian cellular immune activation, is highly stable under field conditions 
Scientific Reports  2015;5:16308.
Studying immunity and immune function in ecology and evolution requires field studies, but there has been a dearth of non-invasive markers of immune activation available for studying large wild mammals. Recently, we analytically and biologically validated the measurement of urinary neopterin (NEO), a biomarker of cellular immune activation, in captive macaques. However, applying this to free-ranging settings is complicated by issues involving sample collection, processing, storage, and transport. Here, we collected urine samples from captive macaques and undertook experiments simulating common field issues. We tested the effects on urinary NEO sample measurements following: dirt and faecal contamination; storage at room temperature; differences in processing and long-term storage methods (freezing, lyophilising, blotting onto filter paper); and freeze-thaw cycles. Our results show that concentrations of urinary NEO are highly stable – they are not affected by soil or faecal contamination, can be collected on filter paper and stored for many months frozen or lyophilised with minimal effect, and are resistant to multiple 24 hr freeze-thaws. With the addition of a biocidal preservative, concentrations are even stable at room temperature for long periods. Urinary NEO is remarkably resilient, and is highly suitable for non-invasive field studies of cellular immune responses in wild large mammals.
doi:10.1038/srep16308
PMCID: PMC4637859  PMID: 26549509
3.  Validation of a Novel Collection Device for Non-Invasive Urine Sampling from Free-Ranging Animals 
PLoS ONE  2015;10(11):e0142051.
Recent advances in non-invasively collected samples have opened up new and exciting opportunities for wildlife research. Different types of samples, however, involve different limitations and certain physiological markers (e.g., C-peptide, oxytocin) can only be reliably measured from urine. Common collection methods for urine to date work best for arboreal animals and large volumes of urine. Sufficient recovery of urine is thus still difficult for wildlife biologists, particularly for terrestrial and small bodied animals. We tested three collection devices (two commercially available saliva swabs, Salivette synthetic and cotton, and cotton First aid swabs) against a control to permit the collection of small volumes of urine from the ground. We collected urine samples from captive and wild macaques, and humans, measured volume recovery, and analyzed concentrates of selected physiological markers (creatinine, C-peptide, and neopterin). The Salivette synthetic device was superior to the two alternative devices. Concentrations of creatinine, absolute C-peptide, C-peptide per creatinine, absolute neopterin, and neopterin per creatinine measured in samples collected with this device did not differ significantly from the control and were also strongly correlated to it. Fluid recovery was also best for this device. The least suitable device is the First aid collection device; we found that while absolute C-peptide and C-peptide per creatinine concentrations did not differ significantly from the control, creatinine concentrations were significantly lower than the control. In addition, these concentrations were either not or weakly correlated to the control. The Salivette cotton device provided intermediate results, although these concentrations were strongly correlated to the control. Salivette synthetic swabs seem to be useful devices for the collection of small amounts of urine from the ground destined for the assessment of physiological parameters. They thus provide new opportunities for field studies to incorporate physiological markers, particularly on smaller bodied and terrestrial animals and where urine collection is difficult.
doi:10.1371/journal.pone.0142051
PMCID: PMC4633224  PMID: 26536024
4.  Physiological and behavioural responses to weaning conflict in free-ranging primate infants 
Animal behaviour  2014;97:241-247.
Weaning, characterized by maternal reduction of resources, is both psychologically and energetically stressful to mammalian offspring. Despite the importance of physiology in this process, previous studies have reported only indirect measures of weaning stress from infants, because of the difficulties of collecting physiological measures from free-ranging mammalian infants. Here we present some of the first data on the relationship between weaning and energetic and psychological stress in infant mammals. We collected data on 47 free-ranging rhesus macaque infants on Cayo Santiago, Puerto Rico, showing that faecal glucocorticoid metabolite (fGCM) concentrations were directly related to the frequency of maternal rejection, with fGCM concentrations increasing as rates of rejection increased. Infants with higher fGCM concentrations also engaged in higher rates of mother following, and mother following was associated with increased time on the nipple, suggesting that infants that experienced greater weaning-related stress increased their efforts to maintain proximity and contact with their mothers. Infants experiencing more frequent rejection uttered more distress vocalizations when being rejected; however, there was no relationship between rates of distress vocalizations and fGCM concentrations, suggesting a disassociation between behavioural and physiological stress responses to weaning. Elevated glucocorticoid concentrations during weaning may function to mobilize energy reserves and prepare the infant for continued maternal rejection and shortage of energetic resources.
doi:10.1016/j.anbehav.2014.09.016
PMCID: PMC4242433  PMID: 25431499
energetics; infant; primate; rhesus macaque; stress; weaning
5.  Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment 
American Journal of Primatology  2014;76(11):1049-1061.
Numerous animal species currently experience habitat loss and fragmentation. This might result in behavioral and dietary adjustments, especially because fruit availability is frequently reduced in fragments. Food scarcity can result in elevated physiological stress levels, and chronic stress often has detrimental effects on individuals. Some animal species exhibit a high degree of fission–fusion dynamics, and theory predicts that these species reduce intragroup feeding competition by modifying their subgroup size according to resource availability. Until now, however, there have been few studies on how species with such fission–fission dynamics adjust their grouping patterns and social behavior in small fragments or on how food availability influences their stress levels. We collected data on fruit availability, feeding behavior, stress hormone levels (measured through fecal glucocorticoid metabolites (FGCM)), subgroup size, and aggression for two groups of brown spider monkeys (Ateles hybridus) in a small forest fragment in Colombia and examined whether fruit availability influences these variables. Contrary to our predictions, spider monkeys ranged in smaller subgroups, had higher FGCM levels and higher aggression rates when fruit availability was high compared to when it was low. The atypical grouping pattern of the study groups seems to be less effective at mitigating contest competition over food resources than more typical fission–fusion patterns. Overall, our findings illustrate that the relationship between resource availability, grouping patterns, aggression rates, and stress levels can be more complex than assumed thus far. Additional studies are needed to investigate the long-term consequences on the health and persistence of spider monkeys in fragmented habitats.
doi:10.1002/ajp.22292
PMCID: PMC4229060  PMID: 24820229
habitat fragmentation; glucocorticoid metabolites; fission–fusion dynamics; spider monkeys; aggression
6.  Habitat Degradation and Seasonality Affect Physiological Stress Levels of Eulemur collaris in Littoral Forest Fragments 
PLoS ONE  2014;9(9):e107698.
The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.
doi:10.1371/journal.pone.0107698
PMCID: PMC4168001  PMID: 25229944
7.  Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior 
Behavioral ecology and sociobiology  2013;67(9):1457-1469.
The past decade has seen an increasing shift in animal communication towards more studies that incorporate aspects of signaling in multiple modalities. Although nonhuman primates are an excellent group for studying the extent to which different aspects of condition may be signaled in different modalities, and how such information may be integrated during mate choice, very few studies of primate species have incorporated such analyses. Here, we present data from free-ranging male rhesus macaques on sex skin coloration (modeled to receiver perception), bark vocal signals, androgen levels, morphometric variables, dominance status, and female mate choice. We show that, consistent with data on females, most intra- and interindividual variation in sex skin appearance occurs in luminance rather than color. Sex skin luminance was significantly correlated across different skin regions. Sex skin luminance did not correlate with the majority of bark parameters, suggesting the potential for the two signals to convey different information. Sex skin appearance was not related to androgen levels although we found some evidence for links between androgen levels and bark parameters, several of which were also related to morphometric variables. We found no evidence that either signal was related to male dominance rank or used in female mate choice, though more direct measures of female proceptive behavior are needed. Overall, the function of male sex skin coloration in this species remains unclear. Our study is among the first nonhuman primate studies to incorporate measurements of multiple signals in multiple modalities, and we encourage other authors to incorporate such analyses into their work.
doi:10.1007/s00265-013-1521-x
PMCID: PMC4084859  PMID: 25013266
Coloration; Luminance; Vocal signals; Multimodal; Primate; Rhesus macaques
8.  Costs of and Investment in Mate-Guarding in Wild Long-Tailed Macaques (Macaca fascicularis): Influences of Female Characteristics and Male–Female Social Bonds 
International Journal of Primatology  2014;35(3-4):701-724.
Male primates living in multimale groups tend to direct mate and mate-guarding choices toward females of high reproductive value, i.e., high-ranking, parous females, or females with which they share strong bonds. Little is known, however, about the constraints that may limit male mate-guarding choices (the costs of this behavior) and the influence of the females’ quality on male investment in mate-guarding. We aimed to study the effects of female rank, parity status, and male–female social bond strength on the costs of and investment in mate-guarding by males. We carried out our study during two reproductive seasons on three groups of wild long-tailed macaques in Indonesia. We combined behavioral observations on male locomotion and activity with noninvasive measurements of fecal glucocorticoids (fGC). Males spent less time feeding when mate-guarding nulliparous females than when mate-guarding parous females and tended to have higher fGC levels when mate-guarding low-ranking nulliparous females than when mate-guarding high-ranking nulliparous ones. Evolution should thus favor male choice for high-ranking parous females because such a decision brings benefits at proximate (reduced costs of mate-guarding) and ultimate (higher reproductive value) levels. Further, male investment in mate-guarding was flexible and contingent on female reproductive and social value. Males were more vigilant and more aggressive toward other males when mate-guarding females to which they were strongly bonded and/or high-ranking ones than when mate-guarding other females. Our findings bring a new dimension to the study of mate choice by showing that males not only mate preferentially with high-quality females but may also aim to secure paternity with these females through optimized monopolization.
doi:10.1007/s10764-014-9775-3
PMCID: PMC4129240  PMID: 25152554
Feeding costs; Glucocorticoids; Macaca fascicularis; Mate choice; Reproductive effort; Vigilance
9.  The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses 
Social status primarily determines male mammalian reproductive success, and hypotheses on the endocrinology of dominance have stimulated unprecedented investigation of its costs and benefits. Under the challenge hypothesis, male testosterone levels rise according to competitive need, while the social stress hypothesis predicts glucocorticoid (GC) rises in high ranking individuals during social unrest. Periods of social instability in group-living primates, primarily in baboons, provide evidence for both hypotheses, but data on social instability in seasonally-breeding species with marked social despotism but lower reproductive skew are lacking. We tested these hypotheses in seasonally-breeding rhesus macaques on Cayo Santiago, Puerto Rico. We documented male fecal GC and androgen levels over a 10 month period in relation to rank, age, natal status and group tenure length, including during a socially unstable period in which coalitions of lower-ranked males attacked higher-ranked males. Androgen but not GC levels rose during the mating season; older males had lower birth season levels but underwent a greater inter-season rise than younger males. Neither endocrine measure was related to rank except during social instability, when higher ranked individuals had higher and more variable levels of both. High ranking male targets had the highest GC levels of all males when targeted, and also had high and variable GC and androgen levels across the instability period. Our results provide evidence for both the challenge and social stress hypotheses.
doi:10.1007/s00265-012-1420-6
PMCID: PMC3950204  PMID: 24634561
challenge hypothesis; social stress; male-male competition; social status; dominance
10.  Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis) 
Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males’ locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies.
doi:10.1007/s00265-013-1673-8
PMCID: PMC3950606  PMID: 24659851
Primates; Sexual selection; Mating costs; Field endocrinology; Feeding behaviour; Urinary C-peptide
11.  Cues to Androgens and Quality in Male Gibbon Songs 
PLoS ONE  2013;8(12):e82748.
Animal vocal signals may provide information about senders and mediate important social interactions like sexual competition, territory maintenance and mate selection. Hence, it is important to understand whether vocal signals provide accurate information about animal attributes or status. Gibbons are non-human primates that produce loud, distinctive and melodious vocalizations resembling more those of birds than of other non-human primates. Wild gibbons are characterized by flexibility in social organization (i.e., pairs and multimale units) as well as in mating system (i.e., monogamy and polyandry). Such features make them a suitable model to investigate whether the physiology (hormonal status) and socio-demographic features find their correspondence in the structure of their songs. By combining male solo song recordings, endocrine outputs using non-invasive fecal androgen measures and behavioral observations, we studied 14 groups (10 pair-living, 4 multimale) of wild white-handed gibbons (Hylobates lar) residing at Khao Yai National Park, Thailand. We collected a total of 322 fecal samples and recorded 48 songs from 18 adult animals. Our results confirmed inter-individuality in male gibbon songs, and showed a clear correlation between androgen levels and song structures. Gibbons with higher androgen levels produced calls having higher pitch, and similarly adult individuals produced longer calls than senior males. Thus, it is plausible that gibbon vocalizations provide receivers with information about singers' attributes.
doi:10.1371/journal.pone.0082748
PMCID: PMC3867390  PMID: 24367551
12.  Methodological Considerations in the Analysis of Fecal Glucocorticoid Metabolites in Tufted Capuchins (Cebus apella) 
Analysis of fecal glucocorticoid (GC) metabolites has recently become the standard method to monitor adrenocortical activity in primates noninvasively. However, given variation in the production, metabolism, and excretion of GCs across species and even between sexes, there are no standard methods that are universally applicable. In particular, it is important to validate assays intended to measure GC production, test extraction and storage procedures, and consider the time course of GC metabolite excretion relative to the production and circulation of the native hormones. This study examines these four methodological aspects of fecal GC metabolite analysis in tufted capuchins (Cebus apella). Specifically, we conducted an adrenocorticotrophic hormone (ACTH) challenge on one male and one female capuchin to test the validity of four GC enzyme immunoassays (EIAs) and document the time course characterizing GC metabolite excretion in this species. In addition, we compare a common field-friendly technique for extracting fecal GC metabolites to an established laboratory extraction methodology and test for effects of storing “field extracts” for up to 1 yr. Results suggest that a corticosterone EIA is most sensitive to changes in GC production, provides reliable measures when extracted according to the field method, and measures GC metabolites which remain highly stable after even 12 mo of storage. Further, the time course of GC metabolite excretion is shorter than that described yet for any primate taxa. These results provide guidelines for studies of GCs in tufted capuchins, and underscore the importance of validating methods for fecal hormone analysis for each species of interest.
doi:10.1007/s10764-013-9703-y
PMCID: PMC3789889  PMID: 24098064
ACTH challenge; Captive welfare; Cortisol; Sapajus; Storage effects; Stress
13.  Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques? 
Hormones and behavior  2012;61(5):696-705.
In contrast to most mammalian species, female sexual activity is not limited to the fertile phase of the ovarian cycle in anthropoid primates, which has long been proposed to conceal the timing of ovulation to males. It is now generally believed that females are still most attractive during the fertile phase, leading to high-ranking males successfully mate-guarding them specifically during this period. While studies conducted in species exhibiting exaggerated sexual swellings (probabilistic signal of the fertile phase) have generally supported this hypothesis, mixed support comes from others. Here, we investigated whether high-ranking males timed mate-guarding effort towards female fertile phases in rhesus macaques (Macaca mulatta). In this species, adult females do not exhibit sexual swellings, but undergo facial skin colour variation, an alternative oestrogens-dependent graded-signal of female reproductive status. We collected behavioural, hormonal and genetic paternity data during two mating seasons for one group of the free-ranging population of Cayo Santiago. Our results show that mate-guarding by top-ranking males did not completely cover the entire female fertile phase and that this tactic accounted for only 30-40% of all fertilisations observed. Males tended to prolong mate-guarding into the luteal phase (null probability of fertilisation), which mirrors the pattern of male attraction to female facial colour reported in an earlier study. These findings suggest that males may have limited knowledge regarding the exact timing of females’ fertile phase in rhesus macaques, which presumably allows females to gain more control over reproduction relative to other anthropoid primate species.
doi:10.1016/j.yhbeh.2012.03.003
PMCID: PMC3559102  PMID: 22449655
Prolonged sexual receptivity; concealed ovulation; mate-guarding; fecal steroids; reproductive strategies; fertile phase; genetic paternity analysis; primates; rhesus macaques
14.  Immune Function and HPA Axis Activity in Free-Ranging Rhesus Macaques 
Physiology & behavior  2011;104(3):507-514.
In mammals, the hypothalamic-pituitary-adrenal (HPA) axis and immune system play an important role in the maintenance of homeostasis. Dysregulation of either system resulting, for example, from psychosocial or reproductive stress increases susceptibility to disease and mortality risk, especially in aging individuals. In a study of free-ranging rhesus macaques, we examined how female age, reproductive state, social rank, and body condition influence (i) aspects of cytokine biology (plasma concentrations of interleukin-1 receptor antagonist (IL-1ra), IL-6 and IL-8), and (ii) HPA axis activity (plasma and fecal glucocorticoid levels). We also assessed individual differences in cytokine and hormone concentrations over time to determine their consistency and to investigate relations between these two indicators of physiological regulation and demand. Female monkeys showed marked increases in HPA axis activity during pregnancy and lactation, and increased circulating levels of IL-1ra with advancing age. Inter-individual differences in IL-1ra and IL-8 were consistent over successive years, suggesting that both are stable, trait-like characteristics. Furthermore, the concentrations of fecal glucocorticoid hormones in non-pregnant, non-lactating females were correlated with their plasma cortisol and IL-8 concentrations. Some individuals showed permanently elevated cytokine levels or HPA axis activity, or a combination of the two, suggesting chronic stress or disease. Our results enhance our understanding of within- and between-individual variation in cytokine levels and their relationship with glucocorticoid hormones in free-ranging primates. These findings can provide the basis for future research on stress and allostatic load in primates.
doi:10.1016/j.physbeh.2011.05.021
PMCID: PMC3133459  PMID: 21635909
rhesus macaque; cytokines; cortisol; aging; reproduction; allostatic load
15.  Sexual signalling in female crested macaques and the evolution of primate fertility signals 
Background
Female signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females’ interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour.
Results
We show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this.
Conclusion
Though probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.
doi:10.1186/1471-2148-12-89
PMCID: PMC3483276  PMID: 22708622
Fertility signals; Sexual selection; Sexual swellings; Primate
16.  You Mate, I Mate: Macaque Females Synchronize Sex not Cycles 
PLoS ONE  2011;6(10):e26144.
Extended female sexuality in species living in multimale-multifemale groups appears to enhance benefits from multiple males. Mating with many males, however, requires a low female monopolizability, which is affected by the spatiotemporal distribution of receptive females. Ovarian cycle synchrony potentially promotes overlapping receptivity if fertile and receptive periods are tightly linked. In primates, however, mating is often decoupled from hormonal control, hence reducing the need for synchronizing ovarian events. Here, we test the alternative hypothesis that females behaviorally coordinate their receptivity while simultaneously investigating ovarian cycle synchrony in wild, seasonal Assamese macaques (Macaca assamensis), a promiscuous species with extremely extended female sexuality. Using fecal hormone analysis to assess ovarian activity we show that fertile phases are randomly distributed, and that dyadic spatial proximity does not affect their distribution. We present evidence for mating synchrony, i.e., the occurrence of the females' receptivity was significantly associated with the proportion of other females mating on a given day. Our results suggest social facilitation of mating synchrony, which explains (i) the high number of simultaneously receptive females, and (ii) the low male mating skew in this species. Active mating synchronization may serve to enhance the benefits of extended female sexuality, and may proximately explain its patterning and maintenance.
doi:10.1371/journal.pone.0026144
PMCID: PMC3192140  PMID: 22022541
17.  Information content of female copulation calls in wild long-tailed macaques (Macaca fascicularis) 
Primates are unusual in that many females display sexual signals, such as sex skin swellings/colorations and copulation calls, without any sex role reversal. The adaptive function of these signals remains largely unclear, although it has been suggested that they provide males with information on female reproductive status. For sex skin swellings, there is increasing evidence that they represent a graded signal indicating the probability of ovulation. Data on the functional significance of copulation calls are much scarcer. To clarify the information content of such calls, we recorded copulation calls in wild long-tailed macaques (Macaca fascicularis) and analysed the structure of these calls during the ovarian cycle. Specifically, we correlated selected call parameters with the female oestrogen to progestogen ratio (obtained from faecal samples), which are known to be elevated during the female's fertile phase. In addition, we ran a general linear mixed model for these call parameters, testing factors (cycle phase, occurrence/absence of ejaculation, male dominance status, occurrence/absence of mate guarding) which potentially influence female copulation calls in primates. Our results show that copulation calls of female long-tailed macaques signal mating outcome and rank of the mating partner, but not female reproductive status. They also show for the first time on primates that copulation calls can convey information on whether a female is mate guarded or not. We suspect that the function of these calls is manipulation of male mating and mate-guarding behaviour and that in this way the degree of sperm competition and ultimately male reproductive success is influenced.
doi:10.1007/s00265-011-1260-9
PMCID: PMC3249197  PMID: 22247587
Macaca fascicularis; Copulation calls; Sexual signal; Female reproductive status; Male dominance status; Ejaculation; Consortships; Estrogens; Progestogens; Faecal hormones
18.  Do Women's Voices Provide Cues of the Likelihood of Ovulation? The Importance of Sampling Regime 
PLoS ONE  2011;6(9):e24490.
The human voice provides a rich source of information about individual attributes such as body size, developmental stability and emotional state. Moreover, there is evidence that female voice characteristics change across the menstrual cycle. A previous study reported that women speak with higher fundamental frequency (F0) in the high-fertility compared to the low-fertility phase. To gain further insights into the mechanisms underlying this variation in perceived attractiveness and the relationship between vocal quality and the timing of ovulation, we combined hormone measurements and acoustic analyses, to characterize voice changes on a day-to-day basis throughout the menstrual cycle. Voice characteristics were measured from free speech as well as sustained vowels. In addition, we asked men to rate vocal attractiveness from selected samples. The free speech samples revealed marginally significant variation in F0 with an increase prior to and a distinct drop during ovulation. Overall variation throughout the cycle, however, precluded unequivocal identification of the period with the highest conception risk. The analysis of vowel samples revealed a significant increase in degree of unvoiceness and noise-to-harmonic ratio during menstruation, possibly related to an increase in tissue water content. Neither estrogen nor progestogen levels predicted the observed changes in acoustic characteristics. The perceptual experiments revealed a preference by males for voice samples recorded during the pre-ovulatory period compared to other periods in the cycle. While overall we confirm earlier findings in that women speak with a higher and more variable fundamental frequency just prior to ovulation, the present study highlights the importance of taking the full range of variation into account before drawing conclusions about the value of these cues for the detection of ovulation.
doi:10.1371/journal.pone.0024490
PMCID: PMC3177841  PMID: 21957453
19.  Concealed Fertility and Extended Female Sexuality in a Non-Human Primate (Macaca assamensis) 
PLoS ONE  2011;6(8):e23105.
In numerous primates living in mixed-sex groups, females display probabilistic cues of fertility to simultaneously concentrate paternity to dominant males while diluting it amongst others as a means to reduce the risk of infanticide and to increase male care for offspring. A few species, however, lack these cues and potentially conceal fertility from males; yet, to date, little is known about mating patterns and their underlying proximate mechanisms in such species. Here, we investigated mating activity and sexual consortships relative to female reproductive state in wild Assamese macaques (Macaca assamensis), a species where females lack prominent anogenital swellings and copulation calls. During two mating seasons (2837 contact hours) we recorded sexual and social behaviors, sexual consortships, and collected 1178 fecal samples (n = 15 females) which were analyzed for progestogen concentrations to assess female reproductive state and to determine the timing of ovulation and conception. Although mostly conceiving in their first ovarian cycle, females were sexually receptive throughout the entire 4-month mating season, and within-cycle mating frequencies were not increased during fertile phases. Dominant males did not monopolize fertile matings, and consortships by high-ranking males lasted for long periods, which were not exclusively linked to female fertile phases. Furthermore, females copulated promiscuously but not randomly, i.e. for almost every female, matings were concentrated to a certain male, irrespective of male rank. Collectively, we demonstrate that fertility is undisclosed to males. The extreme extended female sexuality facilitated by concealed fertility may allow females to create differentiated mating relationships within a promiscuous mating system. Our study provides important new insight into the plasticity of female sexuality in non-human primates.
doi:10.1371/journal.pone.0023105
PMCID: PMC3154278  PMID: 21853074
20.  Urinary C-Peptide of Insulin as a Non-Invasive Marker of Nutritional Status: Some Practicalities 
PLoS ONE  2011;6(7):e22398.
Nutritional status is a critical element of many aspects of animal ecology, but has proven difficult to measure non-invasively in studies of free-ranging animals. Urinary C-peptide of insulin (UCP), a small polypeptide cleaved in an equimolar ratio from proinsulin when the body converts it to insulin, offers great promise in this regard, and recent studies of several non-human primate species have utilized it with encouraging results. Despite this, there are a number of unresolved issues related to the collection, processing, storage and transport of samples. These include: contamination of samples on collection (most commonly by dirt or faeces), short-term storage before returning to a field station, differences in processing and long-term storage methods (blotting onto filter paper, freezing, lyophilizing), and for frozen samples, transportation while keeping samples frozen. Such issues have been investigated for urine samples in particular with respect to their effects on steroid hormone metabolites, but there has been little investigation of their effects on UCP measurement. We collected samples from captive macaques, and undertook a series of experiments where we systematically manipulated samples and tested the effects on subsequent UCP measurements. We show that contamination of urine samples by faeces led to a decrease in UCP levels by >90%, but that contamination with dirt did not have substantial effects. Short-term storage (up to 12 hours) of samples on ice did not affect UCP levels significantly, but medium-term storage (up to 78 hours) did. Freezing and lyophilization for long-term storage did not affect UCP levels, but blotting onto filter paper did. A transportation simulation showed that transporting frozen samples packed in ice and insulated should be acceptable, but only if it can be completed within a period of a few days and if freeze-thaw can be avoided. We use our data to make practical recommendations for fieldworkers.
doi:10.1371/journal.pone.0022398
PMCID: PMC3142156  PMID: 21799844
21.  Color signal information content and the eye of the beholder: a case study in the rhesus macaque 
Behavioral Ecology  2010;21(4):739-746.
Animal coloration has provided many classical examples of both natural and sexual selection. Methods to study color signals range from human assessment to models of receiver vision, with objective measurements commonly involving spectrometry or digital photography. However, signal assessment by a receiver is not objective but linked to receiver perception. Here, we use standardized digital photographs of female rhesus macaque (Macaca mulatta) face and hindquarter regions, combined with estimates of the timing of the female fertile phase, to assess how color varies with respect to this timing. We compare objective color measures (camera sensor responses) with models of rhesus vision (retinal receptor stimulation and visual discriminability). Due to differences in spectral separation between camera sensors and rhesus receptors, camera measures overestimated color variation and underestimated luminance variation compared with rhesus macaques. Consequently, objective digital camera measurements can produce statistically significant relationships that are probably undetectable to rhesus macaques, and hence biologically irrelevant, while missing variation in the measure that may be relevant. Discrimination modeling provided results that were most meaningful (as they were directly related to receiver perception) and were easiest to relate to underlying physiology. Further, this gave new insight into the function of such signals, revealing perceptually salient signal luminance changes outside of the fertile phase that could potentially enhance paternity confusion. Our study demonstrates how, even for species with similar visual systems to humans, models of vision may provide more accurate and meaningful information on the form and function of visual signals than objective color measures do.
doi:10.1093/beheco/arq047
PMCID: PMC2892627  PMID: 22475874
color signaling; communication; receiver perception; visual discrimination threshold modeling
22.  Estrogen and Progestogen Correlates of the Structure of Female Copulation Calls in Semi-Free-Ranging Barbary Macaques (Macaca sylvanus) 
Females of many Old World primates produce conspicuous vocalizations in combination with copulations. Indirect evidence exists that in Barbary macaques (Macaca sylvanus), the structure of these copulation calls is related to changes in reproductive hormone levels. However, the structure of these calls does not vary significantly around the timing of ovulation when estrogen and progestogen levels show marked changes. We here aimed to clarify this paradox by investigating how the steroid hormones estrogen and progesterone are related to changes in the acoustic structure of copulation calls. We collected data on semi-free-ranging Barbary macaques in Gibraltar and at La Forêt des Singes in Rocamadour, France. We determined estrogen and progestogen concentrations from fecal samples and combined them with a fine-grained structural analysis of female copulation calls (N = 775 calls of 11 females). Our analysis indicates a time lag of 3 d between changes in fecal hormone levels, adjusted for the excretion lag time, and in the acoustic structure of copulation calls. Specifically, we found that estrogen increased the duration and frequency of the calls, whereas progestogen had an antagonistic effect. Importantly, however, variation in acoustic variables did not track short-term changes such as the peak in estrogen occurring around the timing of ovulation. Taken together, our results help to explain why female Barbary macaque copulation calls are related to changes in hormone levels but fail to indicate the fertile phase.
doi:10.1007/s10764-011-9517-8
PMCID: PMC3139882  PMID: 21892238
Acoustic structure; Copulation call; Estrogen; Progesterone; Steroid hormone
23.  Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques 
Animals signal their reproductive status in a range of sensory modalities. Highly social animals, such as primates, have access not only to such signals, but also to prior experience of other group members. Whether this experience affects how animals interpret reproductive signals is unknown. Here, we explore whether familiarity with a specific female affects a male's ability to assess that female's reproductive signals. We used a preferential looking procedure to assess signal discrimination in free-ranging rhesus macaques, a species in which female facial luminance covaries with reproductive status. We collected images of female faces throughout the reproductive cycle, and using faecal hormone analysis to determine ovulation, categorized images as coming from a female's pre-fertile, ovulating, or post-fertile period. We printed colour-calibrated stimuli of these faces, reproducing stimuli perceptually the same in colour and luminance to the original appearance of females. These images were presented to males who were either unfamiliar or familiar with stimuli females. Overall, males distinguished ovulatory from pre-ovulatory faces. However, a significant proportion of males did so only among males familiar with stimuli females. These experiments demonstrate that familiarity may increase a receiver's ability to use a social partner's signals to discern their reproductive status.
doi:10.1098/rspb.2011.0052
PMCID: PMC3177625  PMID: 21471112
familiarity; experience; cognition; reproductive signals; ovulation; discrimination
24.  Urinary C-Peptide Measurement as a Marker of Nutritional Status in Macaques 
PLoS ONE  2011;6(3):e18042.
Studies of the nutritional status of wild animals are important in a wide range of research areas such as ecology, behavioural ecology and reproductive biology. However, they have so far been strongly limited by the indirect nature of the available non-invasive tools for the measurement of individual energetic status. The measurement of urinary C-peptide (UCP), which in humans and great apes shows a close link to individual nutritional status, may be a more direct, non-invasive tool for such studies in other primates as well and possibly even in non-primate mammals. Here, we test the suitability of UCPs as markers of nutritional status in non-hominid primates, investigating relationships between UCPs and body-mass-index (BMI), skinfold fatness, and plasma C-peptide levels in captive and free-ranging macaques. We also conducted a food reduction experiment, with daily monitoring of body weight and UCP levels. UCP levels showed significant positive correlations with BMI and skinfold fatness in both captive and free-ranging animals and with plasma C-peptide levels in captive ones. In the feeding experiment, UCP levels were positively correlated with changes in body mass and were significantly lower during food reduction than during re-feeding and the pre-experimental control condition. We conclude that UCPs may be used as reliable biomarkers of body condition and nutritional status in studies of free-ranging catarrhines. Our results open exciting opportunities for energetic studies on free-ranging primates and possibly also other mammals.
doi:10.1371/journal.pone.0018042
PMCID: PMC3068145  PMID: 21479215
25.  Testing the priority-of-access model in a seasonally breeding primate species 
Behavioral Ecology and Sociobiology  2011;65(8):1615-1627.
In mammals, when females are clumped in space, male access to receptive females is usually determined by a dominance hierarchy based on fighting ability. In polygynandrous primates, as opposed to most mammalian species, the strength of the relationship between male social status and reproductive success varies greatly. It has been proposed that the degree to which paternity is determined by male rank decreases with increasing female reproductive synchrony. The priority-of-access model (PoA) predicts male reproductive success based on female synchrony and male dominance rank. To date, most tests of the PoA using paternity data involved nonseasonally breeding species. Here, we examine whether the PoA explains the relatively low reproductive skew in relation to dominance rank reported in the rhesus macaque, a strictly seasonal species. We collected behavioral, genetic, and hormonal data on one group of the free-ranging population on Cayo Santiago (Puerto Rico) for 2 years. The PoA correctly predicted the steepness of male reproductive skew, but not its relationship to male dominance: the most successful sire, fathering one third of the infants, was high but not top ranking. In contrast, mating success was not significantly skewed, suggesting that other mechanisms than social status contributed to male reproductive success. Dominance may be less important for paternity in rhesus macaques than in other primate species because it is reached through queuing rather than contest, leading to alpha males not necessarily being the strongest or most attractive male. More work is needed to fully elucidate the mechanisms determining paternity in rhesus macaques.
doi:10.1007/s00265-011-1172-8
PMCID: PMC3134767  PMID: 21874084
Dominance; Reproductive skew; Mating skew; Priority-of-access model; Genetic paternity analysis; Primates; Rhesus macaques

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