Individual, contextual, and age-related acoustic variation in Simakobu (Simias concolor) loud calls.

Primate loud calls have the potential to encode information about the identity, arousal, age, or physical condition of the caller, even at long distances. In this study, we conducted an analysis of the acoustic features of the loud calls produced by a species of Asian colobine monkey (simakobu, Simias concolor). Adult male simakobu produce loud calls spontaneously and in response to loud sounds and other loud calls, which are audible more than 500 m. Individual differences in calling rates and durations exist, but it is unknown what these differences signal and which other acoustic features vary among individuals. We aimed to describe the structure and usage of calls and to examine acoustic features that vary within and among individuals. We determined the context of 318 loud calls and analyzed 170 loud calls recorded from 10 adult males at an undisturbed site, Pungut, Siberut Island, Indonesia. Most calls (53%) followed the loud call of another male, 31% were spontaneous, and the remaining 16% followed a loud environmental disturbance. The fundamental frequency (F0) decreased while inter-unit intervals (IUI) increased over the course of loud call bouts, possibly indicating caller fatigue. Discriminant function analysis indicated that calls were not well discriminated by context, but spontaneous calls had higher peak frequencies, suggesting a higher level of arousal. Individual calls were distinct and individuals were mainly discriminated by IUI, call duration, and F0. Loud calls of older males had shorter IUI and lower F0, while middle-aged males had the highest peak frequencies. Overall, we found that calls were individually distinct and may provide information about the age, stamina, and arousal of the calling male, and could thus be a way for males and females to assess competitors and mates from long distances.

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.

Mitochondrial phylogeny of leaf monkeys (genus Presbytis, Eschscholtz, 1821) with implications for taxonomy and conservation.

The langurs of the genus Presbytis inhabit tropical rainforests of Sundaland, and with more than 50 color variants grouped in up to eleven species, Presbytis is one of the most diverse Old World monkey genera. The number of taxa and their phylogenetic relationships however remain controversial. To address these issues, we analyzed a 1.8 kb long fragment of the mitochondrial genome, including the cytochrome b gene, the hypervariable region I of the D-loop and the intermediate tRNAs, from individuals representing nine species. Based on our data, we obtained various well-supported terminal clades, which refer mainly to described taxa. Relationships among these clades are not fully resolved, suggesting at least two radiations in the evolutionary history of the genus. According to divergence age estimates, radiations occurred in the late Miocene and the early to middle Pleistocene. Our findings support the revision of the current classification of the genus Presbytis and enable us to discuss implications for conservation. However, further studies including nuclear sequence data are necessary to completely understand the evolutionary history of the genus, and to address possible hybridization events among taxa.

Group structure and physical characteristics of Simakobu monkeys (Simias concolor) on the Mentawai Island of Siberut, Indonesia.

We present data on group structure and physical characteristics from free-ranging Simias concolor. Mean group size (n = 3) was 8.7 +/- 1.1 individuals with an average adult male:female sex ratio of 1:3. All individuals were sexed and allocated into three categories (infants, juveniles plus subadults and adults) on the basis of their physical development. Within age categories, head-body lengths ranged from 19.6 to 25, 34 to 44 and 42 to 53 cm. Corresponding body weights ranged from 0.5 to 0.9, 2.35 to 4.4 and 5.2 to 7.85 kg, respectively; on average adult males were 13% larger and 23% heavier than adult females. Results indicate that for S. concolor living in undisturbed habitat (i) group sizes are larger than previously reported and (ii) polygyny is the most likely mating system. Both results support an earlier proposal that group size and social organization in Simakobu monkey are related to the degree of habitat disturbance.

Signals of female reproductive quality and fertility in colony-living baboons (Papio h. anubis) in relation to ensuring paternal investment.

The fitness of a female's offspring depends cruicially on the traits, genetic and paternal, that the father contributes. As such, females may either have an interest in behaviorally choosing the highest-quality male, or in reliably signaling their fertility status to males. Combining hormonal data on a female's ovulatory fertile window with a behavioral context, we suggest that captive female olive baboons (Papio h. anubis) provide fathers with reliable signals of their fertile period. One signal, the maximum anogenital swelling (AGA), typically coincided with a 4-day fertile window of ovulation, which occurred 2-3 days prior to deturgescence. As expected from previous studies, AGA swelling indicated general attractiveness to males, and males attended to the relative attractiveness of females. Males approached and copulated with females significantly more often during the 4-day window around ovulation, irrespective of the absolute swelling stage. The two adult males present in the group were both able to copulate with consistent partners as at least two cycling females were available in most months; the dominant male was more selective about the timing of his copulations close to ovulation during the maximal swelling phase. Females with ovulatory but nonconceptive cycles were less attractive to males, especially during their maximal AGA swelling phase.

Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome.

In a number of primate species, females utter loud and distinctive calls during mating. Here we aim to clarify the information content and function of Barbary macaque (Macaca sylvanus) copulation calls by testing (i) whether or not copulation calls advertise the female fertile phase and (ii) whether and how copulation calls influence male ejaculatory behaviour. In order to do this, we combined hormone measurements with acoustic analysis and behavioural observations. In contrast to a previous study implying that the structure of copulation calls indicates the timing of the fertile phase, our results, using objective endocrine criteria for assessing ovulation, provide evidence that the structure of copulation calls of female Barbary macaques does not reveal the timing of the fertile phase. More importantly, females seem to influence the likelihood of ejaculation by calling versus remaining silent and by adjusting the timing of call onset. Females make use of this ability to influence mating outcome to ensure ejaculatory matings with almost all males in the group. In addition, calls given during ejaculatory copulations differ from those during non-ejaculatory copulations, providing information about mating outcome for listeners. We conclude that in this species, copulation calls apparently serve to enhance sperm competition and maximize paternity confusion.

Molecular phylogeny and evolutionary history of Southeast Asian macaques forming the M. silenus group.

The 12 presently recognized taxa forming the Macaca silenus group represent the most diverse lineage within the genus Macaca. The present study was set up to clarify the phylogenetic relationships of the extant members of the M. silenus group and to explain their geographical distribution patterns seen today. A combined approach involving the analysis of one paternal (TSPY) and two maternal (cyt b and 12S-16S rRNA) molecular markers enabled us to resolve the phylogenetic relationships within this lineage. Our Y chromosomal marker is not informative enough to allow detailed conclusion. Based on our mitochondrial data, however, M. pagensis, endemic to the three southern Mentawai islands (Sipora, North- and South Pagai), split off early (2.4-2.6 mya) and represents a sister clade to the macaques from the northern Mentawai island of Siberut and from those of the Southeast Asian mainland, which diverged in a radiation-like splitting event about 1.5-1.7 mya. By combining our new results with available data on behavioural as well as climate and sea level changes in Southeast Asia during the Plio- and Pleistocene, we have developed two scenarios for the evolutionary history of this primate group, which may help explain the current geographical distribution of its members.

Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance.

In many anthropoid primates, mating activity is not restricted to the ovarian cycle but also occurs during pregnancy. Although it has been suggested that the main function of this post-conception mating is to confuse paternity, studies showing whether or not male primates can distinguish between the fertile phase of the conception cycle (FPCC) and the period of peak post-conception mating (peak PCM) are almost non-existent. Here, we examine whether the pattern of female sexual traits (specific sexual behaviors, sexual swelling) and female attractiveness to males differ between FPCC and peak PCM in 6 wild female long-tailed macaques. We also use fecal hormone analysis to investigate whether female traits during peak PCM are related to changes in female sex hormones. All females exhibited a distinct period of heightened mating activity around days 45-60 of gestation. During peak PCM, swelling size and frequency of female solicitations (but not reaching back) were significantly correlated with changes in the estrogen to progestogen ratio. Swelling size, frequency of female sexual behaviors and copulations and proportion of male-initiated copulations and ejaculations were not significantly different between FPCC and peak PCM. Although males spent significantly less time consorting females during peak PCM, all (particularly low-ranking and non-resident males) invested heavily in terms of reproductive costs associated with mate-guarding and mating during pregnancy. We conclude that post-conception mating in wild long-tailed macaques is not merely a by-product of endocrine changes and devoid of adaptive function. Our results more strongly support the hypothesis that it may form part of a female reproductive strategy to confuse paternity, which appears to apply particularly to low-ranking and extra-group males.

Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis).

The extent to which catharrine primate males are able to discern the fertile phase during the female ovarian cycle under natural conditions is still debated. In a recent study, we showed that wild male long-tailed macaques are able to detect the fertile phase, but the cues males used to assess female reproductive status remained unclear. In the present study, we tested female sex skin swelling and specific female behaviors for their reliability in signaling the fertile phase, as determined by measurement of fecal estrogens (E) and progestogens (P) during nine ovulatory cycles in seven free-ranging females. We found that changes in sex skin swellings showed a significant positive correlation to the E/P ratio, but swelling size did not significantly differ between cycle phases. In contrast, the frequency of two of the tested female behaviors, namely initiation of sexual interactions and reaching back for the male during copulation, was not only correlated with female reproductive hormones, but was significantly elevated during the fertile phase compared to nonfertile phases of the cycle. We thus conclude that female sex skin swelling does not reliably indicate the timing of the fertile phase in long-tailed macaques, whereas certain female behaviors do. Since cycles differed considerably in the number of males with which females had sexual interactions as well as in the number of sexual interactions with dominant males, the signaling character of these specific female behaviors appears to be robust against inconsistencies in these social variables. Female behavior might therefore play an important role in the recognition of the fertile phase by male macaques under natural conditions.

The sexually active states of free-ranging male African elephants (Loxodonta africana): defining musth and non-musth using endocrinology, physical signals, and behavior.

Musth in male African elephants, Loxodonta africana, is associated with increased aggressive behavior, continuous discharge of urine, copious secretions from the swollen temporal glands, and elevated androgen levels. During musth, bulls actively seek out and are preferred by estrous females although sexual activity is not restricted to the musth condition. The present study combines recently established methods of fecal hormone analysis with long-term observations on male-female associations as well as the presence and intensity of physical signals to provide a more detailed picture about the physical, physiological, and behavioral characteristics of different states of sexual activity in free-ranging African elephants. Based on quantitative shifts in individual bull association patterns, the presence of different physical signals, and significant differences in androgen levels, a total of three potential sub-categories for sexually active bulls could be established. The results demonstrate that elevations in androgen levels are only observed in sexually active animals showing temporal gland secretion and/or urine dribbling, but are not related to the age of the individual. Further, none of the sexually active states showed elevated glucocorticoid output indicating that musth does not represent an HPA-mediated stress condition. On the basis of these results, we suggest that the term "musth" should be exclusively used for the competitive state in sexually active male elephants and that the presence of urine dribbling should be the physical signal used for defining this state.

Social parameters and urinary testosterone level in male chimpanzees (Pan troglodytes).

Studies investigating relationships between social parameters (such as dominance rank, rates of aggressive and sexual behaviors) and androgen (particularly, testosterone) levels in male primates have yielded inconsistent results. In the present study, we address the relationship between androgens, male dominance rank and rank-associated behaviors in two groups of captive chimpanzees, a species characterized by a pronounced dominance hierarchy between adult males. By combining behavioral observations with urinary testosterone (T) measurements, we found that the differences in T concentrations between males were small and not obviously related to their dominance rank. T levels were not related to the rates of initiated aggression and copulatory behavior, but a significant negative relationship between male T level and the rates of strong aggression received was apparent. Our findings, combined with those of others, suggest that any relationship between dominance rank and T depends upon the extent to which individual rank-associated behaviors (e.g. aggressive/sexual) are themselves related to T.

Molecular phylogeny of Mentawai macaques: taxonomic and biogeographic implications.

In order to elucidate the evolutionary history and taxonomy of the Mentawai macaques, we sequenced a 567 base pairs (bp) long fragment of the mitochondrial cytochrome b gene from 39 individuals representing pigtailed macaque populations from Siberut, Sipora, South Pagai, and Sumatra. Pairwise difference analyses carried out within and among populations have shown, that: (1) variation within populations is relative low, (2) variation among populations is increased, and (3) pairwise differences within and among the populations from Sipora and South Pagai are in the same range. From phylogenetic tree reconstructions including further macaque species, we detected a paraphyletic origin of Mentawai macaques with the Siberut population more closely related to Macaca nemestrina from Sumatra, than it is to populations from the Southern islands. Based on these results, we favour a scenario in that macaques entered the Mentawai islands by two independent colonisation events. Taking together the paraphyletic origin of Mentawai macaques and the genetic differences detected among pigtailed macaque populations, which are comparable with those observed among the seven Sulawesi macaque species, we propose to separate macaques from Siberut and Sipora, North and South Pagai into two distinct species, Macaca siberu and Macaca pagensis, respectively.

Organization of seminiferous epithelium in primates: relationship to spermatogenic efficiency, phylogeny, and mating system.

The succession in time and space of specific germ cell associations, denoted as spermatogenic stages, is a typical feature of mammalian spermatogenesis. The arrangement of these stages is either single stage (one spermatogenic stage per tubular cross-section) or multistage (more than one spermatogenic stage per tubular cross-section). It has been proposed that the single-stage versus multistage arrangement is related to spermatogenic efficiency and that the multistage arrangement is typical for hominids. In the present work, the arrangement of spermatogenic stages and the spermatogenic efficiency of 17 primate species, comprising Strepsirrhini (Prosimians: Lemuriformes, Lorisiformes), Platyrrhini (New World primates), Catarrhini (Old World primates), and Hominoidea (great apes and humans), were analyzed comparatively by quantitative histological and flow cytometric means. We found a predominant single-stage tubular organization in the Strepsirrhini, indicating that the single-stage form represents the ancestral state. The highest degree of multistage complexity was found in Hominoidea (except orangutan) and in Platyrrhini, but not in Catarrhini. Hence, no direct relationship between single-stage/multistage tubular topography and phylogeny could be established across primates. In fact, the tubule arrangement seen in Platyrrhini and Catarrhini primates is the reverse of what might be expected from phylogeny. Interestingly, spermatogenic efficiency was similar in all species. We found no correlation between single-stage/multistage arrangement and spermatogenic efficiency or mating system. We speculate that the presence of a single-stage/multistage organization might simply reflect germ cell clonal size. Our findings further indicate that sperm competition in primates is not reflected at the level of testicular function.