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Males associations with females (%)

Figure 6.2 Relationships between numbers of females with medium/large sexual skin swellings and percentages of males' associations with females throughout the mating season in two groups of talapoin monkeys (Miopithecus talapoin) in Cameroon. Source: From Dixson (1998a), after Rowell and Dixson (1975).

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Figure 6.3 Sexual behaviour during the menstrual cycle in captive groups of talapoin monkeys (Miopithecus talapoin). Data are for seven females.

Source: From Dixson et al. (1972); after Scruton and Herbert (1970).

face, rump, and genitalia. Mandrills occur in the rainforests of Gabon, Rio Muni, and Congo, and they form multi-male/multi-female social groups. So extensive are mandrill home ranges and so elusive are these animals that much remains to be learned about the details of their social organization under natural conditions. However, it is known that very large groups, sometimes called 'hordes' may occur; more than 1,000 monkeys have been counted in one such horde in Gabon. Hordes sometimes split into smaller sub-groups, and it used to be thought that these might represent single male units, indicative of a polygynous mating system (Stammbach 1987; Barton 2000). However, observations of semifree ranging and wild groups of mandrills in Gabon have shown that mandrills have a multi-male/ multi-female mating system (Dixson et al. 1993; Abernethy et al. 2002).

Abernethy et al. were able to attach radio collars to free-ranging male mandrills, and this produced some interesting findings. Adult males spent substantial periods outside of the social group, living a 'solitary' existence, but entering the group to compete for copulations during the annual mating season. Detailed studies of a semi-free ranging group, living in an enclosed area of natural rainforest in Gabon, have shown that the mating season corresponds to the long dry period of the year, typically peaking between May and July. Matings may continue beyond these months, however, so that the season is longer and more flexible in its timing than that described for the talapoin. Mandrills usually give birth from January to March (Figure 6.4). Social factors can also impact the timing of mating seasons, so that moving animals to set up a new group in a rainforested enclosure was associated with marked changes in the onset and timing of females' cycles (Setchell and Dixson 2001).

Although the mating season tends to last for longer in mandrills than in talapoins, female mandrills also develop sexual skin swellings and are receptive for extended periods of time, so that there is no circumscribed period of oestrus. Figure 6.5 shows data on sexual skin swellings and copulatory behaviour collected from mandrills in Gabon, early in the annual mating season when the first four of fourteen adult females in a semi-free ranging troop had entered a reproductive condition. The pattern of sexual skin

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Figure 6.4 Seasonal patterns of reproduction in a semi-free ranging group of mandrills (Mandrillus sphinx) in Gabon. Females develop their sexual skin swellings and conceive during the long dry season, with most of the subsequent births (X) occurring between November and January.

Source: After Setchell and Dixson (2001).

changes in these females was related to social rank. The three lowest ranking females (no. 17A: rank 12; no. 16: rank 13; no. 6: rank 14) had very long follicular phases, as indicated by the lengthy periods (32-39 days) it took for their sexual skin swellings to enlarge and then to begin to detumesce (initial detu-mescence or breakdown of the sexual skin is readily observable). Although menstrual cycles last for one month, on average, in female Old World monkeys, apes, and in women, these female mandrills had greatly extended the first half of the cycle, perhaps due to some problem in secreting sufficient ovarian oestradiol during follicular development, or to some reduction in sensitivity of the sexual skin to oestrogenic stimulation. In marked contrast was the situation observed in the most dominant female in the troop (no. 2 in Figure 6.5). She exhibited the expected 15 day follicular (swelling) phase and her sexual skin was maximally swollen for just 4 days before breakdown occurred.

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Figure 6.5 Details of sexual interactions during sexual skin swelling cycles in four female mandrills (Mandrillus sphinx), during the annual mating season in Gabon. Swelling sizes are rated on a four-point scale (0 = flat; 1 = small; 2 = medium; 3 = fully swollen). The day of initial sex skin breakdown, at the end of the follicular phase of the menstrual cycle, is indicated by a vertical arrow. Mate-guarding episodes by males are shown as horizontal bars (□ = male no. 14; ■ = male no. 7). Ejaculatory mounts are indicated by symbols for each adult male (o= no. 14; • = no. 7; X = no. 15; * = no. 13) and subadult male( + = no. 2B). Author's data.

Figure 6.5 Details of sexual interactions during sexual skin swelling cycles in four female mandrills (Mandrillus sphinx), during the annual mating season in Gabon. Swelling sizes are rated on a four-point scale (0 = flat; 1 = small; 2 = medium; 3 = fully swollen). The day of initial sex skin breakdown, at the end of the follicular phase of the menstrual cycle, is indicated by a vertical arrow. Mate-guarding episodes by males are shown as horizontal bars (□ = male no. 14; ■ = male no. 7). Ejaculatory mounts are indicated by symbols for each adult male (o= no. 14; • = no. 7; X = no. 15; * = no. 13) and subadult male( + = no. 2B). Author's data.

Patterns of sexual behaviour involving these females and the various adult and sub-adult males are also shown diagrammatically in Figure 6.5. There were three troop-associated adult males (alpha male 14; beta male 7; and theta male 15), three peripheral/solitary adults, and three troop associated sub-adult males. The two most dominant troop males (no. 14 and no. 7) engaged in mate-guarding episodes with individual females at the height of sexual skin swelling. Mate guarding thus focused upon 'single' females (males did not guard or herd units of females as hamadryas or gelada males do). Guarding must be energetically very costly for such males as they follow each female closely, often giving deep 'two phase grunts'.

Activities such as feeding take second place to the defence of their mating opportunities. Male no. 14 (the most dominant male) showed guarding behaviour on 126 (82 per cent) days during the 156 day annual mating period. Such strategies are highly effective, as DNA typing studies show that dominant males have greater reproductive success (Dix-son et al. 1993). It may be for this reason that such males develop large reserves of subcutaneous fat in the rump and flanks to sustain them in the mating season (Wickings and Dixson 1992a). The observation that male mandrills may leave troops after the mating season and forage alone (Abernethy et al. 2002) may be connected to the conflicting demands of reproduction and feeding ecology.

In female baboons, ovulation occurs at the end of the maximum phase of sexual skin swelling, in a time window of 2-5 days before sexual skin detumescence, or on the day of initial sexual skin breakdown (Wildt et al. 1977). This is likely to be the case in mandrills as well, although the necessary endocrine and laparoscopic studies have not been carried out on this species. It is clear, however, that dominant males terminate guarding abruptly once a female's sexual skin begins to detumesce. Up until then, copulations occur throughout the phase of maximal swelling. For example, it can be seen in Figure 6.5 that male no. 14 began to guard female no. 17A and to copulate with her as soon as she had developed a full swelling; he continued to do so for a 20 day period, until sexual skin breakdown brought an end to sexual interactions. Thus it seems likely that the female's sexual skin acts as a graded signal of female reproductive quality in mandrills, as has been proposed for other monkeys and chimpanzees which possess such swellings (Nunn 1999). Male mandrills are under considerable selection pressure to limit guarding and copulation to the ovulatory period; in reality female swellings provide only approximate information concerning likelihood of ovulation, and females are attractive and receptive sexually for extended time periods (especially so in the case of lower-ranking troop members). Thus there is no restricted period of female sexual receptivity or oestrus in mandrills.

These findings on the sexual behaviour of mandrills and talapoins are consistent with the results of field and laboratory studies on a wide range of Old World monkeys and the great apes. Copulations are not distributed randomly throughout the menstrual cycle; mounts and ejaculations are more frequent during the follicular phase or at mid-cycle than during the luteal phase in macaques, baboons, mangabeys, chimpanzees, gorillas, and orangutans (Dixson 1998a). Students of primate sexuality have long been aware that ovarian hormones have powerful effects upon female sexual attractiveness in some species, so that increases in male sexual activity may be due, in part, to enhanced female attractiveness during the follicular phase or at mid-cycle (Herbert 1970). Females may also actively invite males to copulate; Beach (1976b) coined the term proceptivity to define this aspect of female sexuality.

The distinction between proceptivity (female sexual initiation) and receptivity (the female's willingness to accept the male) is an important one, because the neuroendocrine mechanisms underlying the two kinds of behaviour differ in significant ways. At the hypothalamic level, for example, lesions which cause marked deficits in proceptivity in female common marmosets (a New World monkey species) have little or no effect on sexual receptivity (Kendrick and Dixson 1986; Dixson and Hastings 1992). The temporal patterning of female proceptivity and receptivity may also differ markedly during the menstrual cycle. Thus, in the chacma baboon, females present the rump as a sexual invitation to males, but they may also seek to make eye-contact at the same time (Figure 6.6). Such eye-contact proceptivity increases in frequency during the follicular phase, peaks during the peri-ovulatory period, and then declines markedly during the luteal phase of the cycle. Yet, as Figure 6.6 also shows, female chacma baboons continue to accept males' mounting attempts and remain sexually receptive throughout the menstrual cycle. The decline in copulatory frequencies during the luteal phase is due, in large measure, to decreased female attractiveness and loss of sexual skin swelling at this time.

Alternatives to the use of simplistic oestrous terminology to define female sexuality have thus been available for more than 30 years; the definitions of female attractiveness, proceptivity, and receptivity (Beach 1976b) are broadly applicable in studies of sexual behaviour, and are especially useful in research on primate (including human) sexuality. The propensity for female monkeys and apes to display sexual receptivity at times other than when ovulation is likely is widespread, and should not be dismissed as an artefact of studying behaviour under captive conditions. In freeranging rhesus monkeys, for example, Loy (1970) observed that females showed 'dual estrus periods', at mid-cycle and peri-menstrually. When male and female rhesus monkeys are pair tested in the laboratory, some pairings show this same pattern, so that frequencies of mounts and ejaculations peak at mid-cycle and prior to menstruation (Figure 6.7A). However, other pairings show either an increase in copulations throughout the follicular phase (Figure 6.7B) or they may mate only infrequently and without any obvious cyclical changes in behaviour (Figure 6.7C).

Detailed studies of rhesus monkey sexual behaviour have shown that these patterns result, in part, from variations in female sexual attractiveness, as well as from differences in the relationships between partners during free-access pair tests (Goy 1979; 1992). Robert Goy noted that mutual attractiveness is an important determinant of copulatory frequency and its cyclical patterning during pair tests. The fact that copulation is situation dependent, and not simply dependent upon female hormonal status, has been amply demonstrated by studies of monkeys and apes. In many species males are larger and physically more powerful than females. Males may attempt to initiate sexual interactions more frequently than females under laboratory conditions where space is restricted, just as in the wild males sometimes attempt to coerce females into mating with them. Within the confines of a laboratory cage, or a small enclosure, it is often difficult for females to refuse males when they attempt to mate, and females are also less likely to exhibit their normal cyclical patterns of proceptivity. However, when testing conditions are manipulated so as to provide females with greater control over mating interactions, then mid-cycle increases in proceptivity are better defined and copulations are more frequent at that time (e.g. in the rhesus monkey: Wallen 1982; Wallen and Winston 1984).

When orangutans are pair tested to observe sexual behaviour in captivity, the huge males may force their female partners to mate on almost every test. However, if a vertical dropgate divides the testing area, so that only the (much smaller) female has room to slide underneath and reach the male, then she is more pro-ceptive at mid-cycle and copulations are more frequent at this time (Nadler 1977; 1988). Such observations indicate that cyclical changes in the effects of ovarian hormones upon the brain and sexual behaviour certainly occur in anthropoids, but they are subtle, situation dependent, and more influenced by variations in mutual attractiveness between the sexes than is the case

Figure 6.6 Sexual behaviour during laboratory pair tests in chacma baboons (Papio ursinus). Data (collected during four cycles in eight females) are aligned to the day of sexual skin breakdown (BD). Female proceptivity (presentations and presentations accompanied by eye-contact) is shown in the lower graph. Acceptance ratios to invitations made by the opposite sex are shown in the upper graph. Note that females accept males' attempts to mount throughout the cycle, whereas males accept far more of the females' invitations when the latter have large swellings and are sexually attractive.

Figure 6.6 Sexual behaviour during laboratory pair tests in chacma baboons (Papio ursinus). Data (collected during four cycles in eight females) are aligned to the day of sexual skin breakdown (BD). Female proceptivity (presentations and presentations accompanied by eye-contact) is shown in the lower graph. Acceptance ratios to invitations made by the opposite sex are shown in the upper graph. Note that females accept males' attempts to mount throughout the cycle, whereas males accept far more of the females' invitations when the latter have large swellings and are sexually attractive.

Source: From Dixson (1998a); after Bielert (1986).

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Figure 6.6 continued for many mammals. Hence the term 'oestrus' is no more appropriate when applied to descriptions of sexual behaviour in female monkeys or apes, than it would be in descriptions of human sexuality.

Given that female Old World monkeys and apes do not exhibit oestrus, is the same true for other non-human primates? Prosimians such as the lemurs, galagos, and lorises exhibit circumscribed periods of sexual receptivity, which are tightly controlled by ovarian hormones (Dixson 1995a; 1998a).

It is more acceptable to retain the term 'oestrus' in relation to studies of sexual behaviour in prosimian primates. However, among the New World monkeys, females have been observed to permit copulation outside of the peri-ovulatory period and during pregnancy in a number of species. In the common marmoset (Callithrix jacchus), for example, females remain sexually receptive and procep-tive after removal of the ovaries and adrenal glands (Dixson 1987c). The adrenal cortex represents a significant secondary source of sex steroids, but it

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Figure 6.7 Variable patterns of copulatory behaviour in pairs of rhesus monkeys (Macaca mulatta) during the female partner's menstrual cycle. (A) In these pairs, mounts peak in frequency at mid-cycle and pre-menstrually (the black bars = menstruations). (B) Mounts are most frequent during the follicular phase, and decrease during the luteal phase of the cycle. (C) Sexual activity is at low levels in these pairs, and there is little evidence of cyclical changes.

Source: From Dixson (1998a); after Everitt and Herbert (1972).

plays no essential role in the maintenance of sexual behaviour, at least in marmosets (Figure 6.8). Thus, although female marmosets certainly display cyclical changes in their sexual activity (Kendrick and Dixson 1983; Dixson and Lunn 1987), they are not dependent upon oestrogen, progesterone, or other steroid hormones for the expression of proceptivity or receptivity.

In evolutionary terms, it appears that a relaxation of rigid hormonal control of female sexual behaviour is a trait shared by the anthropoids in general, and would have been present in the common ancestors of the New World and Old World representatives of the sub-order (Figure 6.9). Loss of oestrus, if that is the appropriate term, is an ancient phenomenon, and represents part of our evolutionary inheritance from non-human ancestors. Precursors of Homo sapiens, among the australopithecines, would not have exhibited oestrus, nor is it necessary to postulate that they possessed external signals of reproductive status, such as sexual skin swellings. The evolution of sexual skin swellings in the chimpanzee and bonobo (Genus Pan) may have occurred after the common ancestors of these apes diverged from the line which ultimately gave rise to Homo. This possibility should not surprise us, as sexual skin swellings have arisen and have been lost a number of times during anthropoid evolution (Dixson 1983b; 1998a; Sillen-Tulberg and M0ller 1993).

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