J. Keith Hodges

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.

Field and Laboratory Methods in Primatology: Field endocrinology: monitoring hormonal changes in free-ranging primates

Field endocrinology can be considered as the application of non-invasive methodologies to examine behavioural endocrine interactions in primates living in natural conditions and social settings. In bringing together laboratory and field-based research methods, the discipline provides new and exciting opportunities for developing a more integrated approach to studies of primate behavioural ecology. Traditionally, field studies have relied mainly on visual measures, such as behaviour and/or morphology. Although this has generated a great deal of essential information, its limitation is that interpretation of the observations is often based on assumptions concerning the physiological context inwhich theyweremade. The availability of non-invasive methodologies based on measurement of hormones in either urine or faeces now provides us with quantitative measures of physiological status by which the significance of observational data can be gauged. This greatly facilitates the testing of hypotheses concerning the adaptive significance of behavioural and morphological traits and mating systems and is helping to provide new insights into reproductive processes in an evolutionary context. Field endocrinology also facilitates a better understanding of the impact of anthropogenic activities on primate physiology. In combination with studies of the health status of wild primates (Chapter 8), this can help to elucidate the link between environmental stress, health and reproductive parameters and thus to estimate the viability of threatenedpopulations (Pride, 2005;Chapman et al., 2007). In this chapter, we review the most important aspects fieldworkers need to be aware of when planning and carrying out

Organization of Seminiferous Epithelium in Primates: Relationship to Spermatogenic Efficiency, Phylogeny, and Mating System

Abstract 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.

Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis) : male monopolisation, female mate choice or post-copulatory mechanisms?

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.

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 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.

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.

Acoustic Niches of Siberut Primates

The loud calls nonhuman primates use in long-distance communication have supposedly been selected for efficient information transfer in the habitat. The differential effects of scattering and reverberation and the masking effects of background noise predict that loud calls produced in rain forest habitats should be low-pitched and whistle-like with low-frequency modulation. Callers may also use particular calling posts or times of day with reduced background noise to increase the efficacy of sound transmission. We studied the loud calls of the 4 sympatric primate species on Siberut Island. Only Kloss gibbons (Hylobates klossii) fulfilled the predictions regarding both the structure and use of calls. Though the other 3 species —Mentawai macaques (Macaca siberu), pig-tailed langurs (Simias concolor), and Mentawai leaf monkeys (Presbytis potenziani)— also concentrated their main energies in the spectral window with the lowest background noise, their calls were not adapted to long-range transmission. All 4 species produced loud calls exclusively no lower than 18 m above ground, but food abundance and shelter in the canopy may also be factors. Though all 4 species produced the majority of loud calls in the morning, it was not the only time of day with reduced background noise. We suggest that phylogenetic inheritance may better explain the structure of calls than adaptation to the habitat. In sum, the observed usage of spectral and temporal niches is not solely an adaptation to the sound profile of the habitat, though it clearly improves their transmission.

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.

Male Dominance Rank, Female Mate Choice and Male Mating and Reproductive Success in Captive Chimpanzees

Mating and consequently reproductive success in male vertebrates are predominantly determined by intermale competition and female mate choice. Their relative importance however, is still poorly understood. We investigated the interrelationship between male dominance rank — a formal indicator of male competitive ability — female mate choice, and male mating success in a multimale-multifemale group of captive chimpanzees. In addition, we examined the relationship between male dominance rank and reproductive success determined by genetic paternity analysis over a 13-yr period in the same captive population. We related the frequencies of sociosexual behaviors to the female anogenital swelling stage and female fertile phase as determined by urinary and fecal progestogen analysis. Rates of behaviors in both sexes increased with increasing intensity of female swelling, but they were not influenced by the timing of the fertile phase. Male mating success was clearly related to male dominance rank, with high-ranking males performing the overwhelming majority of copulations. This was mainly due to both rank-related rates of male soliciting behavior and intermale aggressiveness during the period of well-developed female anogenital swelling. Although females solicited copulations mainly from the high-ranking males and thus expressed a mate choice based on rank, their overall contribution in initiating copulations and thus influencing male mating success was low. The data on paternity from the population, which always contained 4 adult males, revealed that α-males sired the majority (65%) of offspring. We conclude, that male dominance rank is an important determinant of male mating and reproductive success in captive (and presumably wild) chimpanzees and that female mate choice is of minor importance in modulating male reproductive outcome.