SEXUAL SWELLINGS OF FEMALE GIBBONS. Kalaweit Gibbon Rehabilitation Project, Kalaweit Care Centre, Jalan Punis No. 14,

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1 SEXUAL SWELLINGS OF FEMALE GIBBONS SUSAN M. CHEYNE 1 AND DAVID J. CHIVERS 2 1 Kalaweit Gibbon Rehabilitation Project, Kalaweit Care Centre, Jalan Punis No. 14, Panarung, Palangka Raya, Central Kalimantan, Indonesia. 2 Wildlife Research Group, Department of Anatomy, University of Cambridge. Word count 2206 KEYWORDS Gibbon, labial swelling, anogenital swelling, female. Address for correspondence: Susan M. Cheyne, CIMTROP, Kampus UNPAR Tanjung Nyaho, Palangka Raya, Central Kalimantan, Indonesia Tel: +62 (0) Fax Tel: +62 (0) susancheyne76@yahoo.com 1

2 ABSTRACT Female gibbons were observed for labial swellings from March 2002 August Data were collected on length of time each female was swollen, changes in swelling period as females matured and cycle length (number of days between onsets of consecutive swellings). Data were also collected on the behaviour of the males when the females were swollen. There was a significant relationship between age of the female gibbon and number of days she had labial swelling. There was no significant relationship between the age of the gibbon and the cycle length, nor between species (Hylobates. agilis. albibarbis and H. muelleri) and number of days swollen. Copulation was more common when females were swollen. Swelling in female gibbons, may be related to copulatory behaviour and serve to provide the male with some certainty of paternity through fertilisation insurance. INTRODUCTION Anogenital swellings are highly developed in several primate species (Short, 1977,, 1979,, 1981), where they are believed to be attractive to males (Bielert et al., 1989). (Clutton-Brock & Harvey, 1976) originally noted that species with exaggerated sexual skin swellings live in multi-male social systems. These exaggerated anogenital swellings are found only in Old World monkeys and apes and have been seen in many species (see (Struhsaker, 1976); (Nadler et al., 1979);(Dixon, 1983); Nunn, 1999). Several hypotheses have been proposed for the evolution and function of sexual swelling: best-male (Clutton-Brock and Harvey, 1976); many male (Hrdy, 1981) and the reliable indicator hypothesis (Pagel, 1994). Pagel (1994) did not acknowledge the presence of sexual swellings in gibbons and the results of the reliable-indicator hypotheses (Domb and Pagel, 2001; (Domb & Pagel, 2001; Pagel, 1994), have been questioned (Zinner et al., 2004) and disproved for several species (Emery & Whitten, 2003); (Setchell & Wickings, 2004). It is essential to develop a better understanding of sexual swellings in a wide array of species if we are to understand the evolution of exaggerated swellings, as well as other sexual traits, in primates. In that regard, we also need more quantitative and descriptive data of the sexual signals in different species to conduct these comparisons. Detailed 2

3 measurements of successive swelling cycles are necessary to investigate the behaviour of males in relation to sexual swelling. (Dahl & Nadler, 1989; Dahl & Nadler, 1992a; Dahl & Nadler, 1992b) noted that female gibbons also have conspicuous swelling of the outer labia during ovulation. (NUNN, 1999) noted that some features of exaggerated sexual swellings are correlated with features that may confuse or bias paternity among males. Nunn does not consider gibbons to have exaggerated sexual swellings, as only the labia is involved. In some species the swellings are much larger than in others and that they sometimes involve areas of skin beyond the immediate genital (labial) region. Gibbons, however, have small swellings, confined to labial tissues. While gibbons live in small monogamous family groups, they are not always exclusively monogamous in their mating behavior, as extrapair copulations have been recorded in some populations (H. lar: populations (Bartlett, 2001; Palombit, 1994; Reichard, 1995). This research suggests that gibbons are socially monogamous (vigorously defend a territory against other adult pairs) not sexually monogamous as they have been seen to engage in extra-pair copulations in fragmented/isolated populations (Bartlett, 2001; Palombit, 1994; Reichard, 1995). Dahl and Nadler (1989) propose that the sexual attractiveness associated with the obvious swelling may assist in maintaining the pair bond and could influence the ability of the female to retain and/or change mates. When gibbons are socially monogamous, the swelling may serve to increase certainty of paternity, while still allowing the female to attract other mates. Other primates that show anogenital swellings are sexually promiscuous, and frequently have multiple sexual partners e.g. chimpanzees and macaques. While gibbons have been seen to engage in extra-pair copulations, they are predominantly socially monogamous yet present sexual skin swellings smaller than those of more promiscuous species of primates. Thus the mating hypothesis could explain the presence of anogenital swellings in gibbons as a female adaptation to ensure the male remains to help raise the offspring, thereby ensuring his paternity. From March 2002 September 2003, a study was conducted on the behaviour of 101 gibbons housed at the Kalaweit Gibbon Rehabilitation Project, Central Kalimantan, Indonesia. During the course of this study, SMC noted that female gibbons exhibited cyclical swelling of the genital area. This paper is based on data collected systematically 3

4 on the gibbons to look for patterns and causes of the swellings. The purpose in this study was to determine if there was any pattern to the anogenital swellings of female gibbons, if there was any relationship between age of female and number of days anogenital swelling was present, and if the presence of swelling affected copulatory behaviour between the female and her mate. Long-term observational data about the sexual swellings and ovulation period of the female gibbon is important in understanding the gibbon social system as it relates to the evolution of sexual swelling in Old World monkeys and apes. METHODS Study gibbons were 10 Hylobates agilis albibarbis and 7 H. muelleri spp (Table 1). All females were housed at the Kalaweit Gibbon Rehabilitation Centre in Central Kalimantan, Indonesia. The gibbons were all wild-born, captive raised individuals and all were housed in pairs with a male. Age estimates made from canine size taken during the medical given to all gibbons when they arrived at to the Kalaweit Project (canines increase with age of the gibbon, erupting about 3yrs and being fully emerged by 4yrs. Wear and tear can be used to estimate age of adults). Table 1 Study females: age, number of days swelling was present and average cycle length. Values presented are averaged across all females of the same age. Estimated age (years) Number of females in age group Average number of days swelling was observed Average cycle length (days) Total = 17 Overall average = 6.3 days Overall average = 23.8 days 4

5 All females were observed from March 2002 to August Data were collected on each individual s activity and behaviour for six days each month (during which all behaviours were noted using 10-min scan sampling: copulation data were collected during this time). Data on anogenital swellings were collected daily (by SMC and Kalaweit staff). All females were observed for the presence of swelling and a total of 17 females showed regular swellings and 17 separate swelling cycles were observed for each female (17 months data collection and 1 cycle/female/month). The total number of observation hours on all 17 females over 18 months was 2754 hours. All data were collected non-invasively and based only on visual observations (observers could approach to within 1m of all study animals). There was no bias in observation days i.e. each female was observed for equal periods of time while swollen and while not swollen (chi-squared: χ 2 = 25.98, d.f. = 16, p > 0.05). Prior to data collection, staff were shown photos of the various stages of gibbon labial swelling. The presence or absence of swelling was scored based on whether the vulva was open, pink and swollen or not. A level of swelling scale was developed as follows: 0) No swelling (Photo 1) 1) Small swelling (only a small area of pink was visible and labia partially swollen, Photo 2), 2) Large swelling (large pink-red area visible and whole labia swollen, Photo 3) 5

6 Photo 1 Subadult female H.muelleri (left) showing no swelling. Photo 2 Adult female H.agilis albibarbis with small swelling. 6

Photo 3 Adult female H. muelleri with large swelling. Inter-observer bias was tested using a paired t-test and no significance difference was found between the observers (5.

7 Photo 3 Adult female H. muelleri with large swelling. Inter-observer bias was tested using a paired t-test and no significance difference was found between the observers (5.8% of test observations were not in agreement, Table 2). Table 2 Inter-observer bias for scoring swelling size. Observer Number of paired Number of observations not in agreement observations Total Swelling period is described as the number of days from onset of swelling (whether small or large) to complete absence of swelling (detumescence). Menstrual cycle length was described as the number of days between onset of swelling the onset of the next swelling. RESULTS It was impossible to measure accurately the degree of swelling of all the female gibbons on a regular basis, hence the development of the scale, by which all data were 7

8 collected. For the purposes of this analysis the data were combined to give a dichotomous scoring of swollen or not swollen. Rarely was menstrual blood observed (1%, n = 100 observations). On average, each female was observed with swelling for 6.5 days (range 4-8 days). Swelling duration was averaged for each female for analysis. There was no relationship between the two species of gibbon and the number of cycle days, thus the data for both species were combined for further analysis. All females were observed initially to determine at what age menstruation began. There was a significant relationship between the age of the female gibbon and the length of swelling period (Spearman rank correlation R s = 0.701, n = 18, p = 0.002). No information is available on the relationship between age of female and size of swelling due to the difficulty of accurately photographing the swellings. There was no significant relationship between age and the cycle length as measured by the number of days between onset of swelling and the onset of another swelling (after detumescence: Spearman rank correlation R s = 0.177, n = 18, p > 0.05). There was a significant difference in the number of copulations that occurred when the female was swollen, compared to those when the female was not swollen (χ 2 = 8.154, d.f. = 3, p = 0.043). Of 108 copulations observed, 105 (97%) occurred when the female was swollen. Of 105 copulations, 89 (85%) occurred 1-2 days before detumescence (Figure 1). 8

9 % of matings Day of cycle Number of matings Swelling size Figure 1 Swelling size against average number of matings throughout the swollen period. There was also a significant difference in the number of times the female presented her rump to the male (sexual solicitation/pre-copulatory behaviour) while she was swollen compared to when she was not (χ 2 = 7.264, d.f. = 3, p = 0.039). Prior to copulation, the female would groom the male and present her rump. This presentation is often accompanied by the female reaching out and pulling the male towards her (pers. obs.) Mating lasted an average of 34 seconds (range seconds, n = 108). If the male achieves successful intromission, the female will often emit soft hoo sounds. It was not possible to determine if ejaculation occurred on all mating attempts however successful intromission is believed to be accompanied by ejaculation. Males do appear to inspect the swelling when females present but it is unclear whether they are responding to swelling size or to the sexual presentation alone. DISCUSSION There is an urgent need in gaining more information on the relation of gibbon swelling patterns to behavioral and endocrinological correlates. From the observations in this study we noted a significant relationship between the age of the female gibbon and the number of days labial swelling was exhibited. Older females ( 7 years) were swollen 9

10 for longer (in days) than younger females. Juvenile females were seen to have swellings. Despite many gibbons living in captivity in zoos and research centres around the world, there appears to be very little information available regarding their ovulation cycle and of the accompanying swelling of the vulvae. (Geissmann, 1991) suggests that the onset of menstruation may not be an accurate predictor of the onset of sexual maturity. Gibbons may undergo a period in which they are sexually active, but not reproducing, explaining the observed delays between the onset of menarche and the time of first reproduction. Thus the focus was on the observable cycle length indicated by the swelling of the vulva and not on whether the gibbons were sexually mature. The most interesting result is the relationship between copulation behaviour, swelling and solicitation rates. If the purpose of the conspicuous swelling is to retain the presence of the male, we would expect that the female would allow him more mating rights or the male would attempt more mountings during the swelling period, as he associates the swelling with sexual activity. From the data, this does appear to be the case, though there was insufficient information to determine whether the increased number of copulations was due to an increase in presenting from the female or from an increase in mounting attempts by the male due to the visual stimulus of the female swelling. This swelling has a predictable cycle length, which increases as the female ages, increasing her sexual attractiveness to the male, thereby ensuring that he remains with the female to defend joint territory and offspring. An alternative to the paternity theory is that the swelling functions as fertilisation insurance, i.e. indicates when the male should mate to ensure maximum likelihood of conception. One suggestion is that the swelling serves to attract multiple males during the initial pair-formation (Dahl and Nadler, 1992a) and/or there is a relationship between the swelling (possibly indicating female availability) and inter-male competition. The sexual swelling may also mediate pair maintenance (Dahl and Nadler, 1989). Concealed ovulation in the female gibbon would not give the male any certainty of paternity, so there would be no incentive for the male to stay and invest time and energy in the female, her offspring and protecting the territory. Thus, to ensure that the male has some certainly of paternity (ensuring that he remains to defend the female, offspring and the territory), the female has a small, but obvious indicator of when she is sexually receptive. 10

11 No significant relationship was found between the age of the gibbon and the cycle length. The two species showed no significant difference between the numbers of days the females showed swelling. Additionally, males copulated with females more frequently when sexual swelling was present, and most frequently in the 1-2 days preceding detumescence. Most females were observed to cycle, as identified by the presence of a pronounced sexual swelling of the outer labia, which waxed and waned each month within the period of their menstrual cycle. Although blood was observed infrequently, it was not seen when the females were swollen. Data on the duration over which ovulation occurred matched that noted by Nadler et al. (1993), though they collected data on only four Hylobates lar females over a total of 6 cycles. The sexual skin swellings of gibbons cannot be explained by any of the previously proposed hypotheses: Best male gibbons are monogamous and there is no competition among males for access to females Many males while gibbons do appear to have extra-pair copulations, this is not a common social strategy and EPC s are rare, thus it is unlikely that this hypothesis is the main reason for sexual swelling in gibbons. Reliable indicator there was no obvious difference in the size of swellings of the gibbons in this study. More information is needed to accurately measure the size of swellings, but this hypothesis has been proposed for multi-male species and has received criticism. Following on from the work of Dahl and Nadler (1989) regarding the relationship between sexual swelling and mate-retention, we propose a different hypothesis for the evolution of sexual skin swellings in gibbons: certainty of paternity where the female uses the swelling to advertise to the pair-male when she is most receptive, thus ensuring his paternity and ensuring he will remain with the female to assist with territorial defence. The sexual swellings may have a role in extra-pair copulations as females could use these swellings to advertise to non-pair males when they are receptive. More data are needed on the relationship between sexual swellings and EPC s in the wild. 11

12 ACKNOWLEDGEMENTS SMC would like to thank Chanee (Aurelién Brulé), the director of the Kalaweit Project, and all Kalaweit staff who helped with data collection: Pak Didi, Amud, Setia, Nanto, Sinar, and Penyang. Also thanks to LIPI, the Indonesian Institute of Science for permission to work in Kalimantan. Many thanks to Raffaella Commitante for comments on earlier versions of this manuscript. Funding was provided by The Gibbon Foundation, the C.K. Marr Educational Trust and Downing College, Cambridge. REFERENCES Bartlett, T. Q. (2001). Extra-group copulations by sub-adult gibbons: implications for understanding gibbon social organisation. American Journal of Physical Anthropology. 32 (supplement):36. Bielert, C., L. Grirolama, and S. Jowell. (1989). An experimental examination of the colour component in visually mediated sexual arousal of the mala chacma baboon (Papio ursinus). Journal of Zoology 219: Clutton-Brock, T. H., and P. H. Harvey. (1976). Evolutionary rules and primate societies. Pages in P. P. G. Bateson, and R. A. Hinde, editors. Growing Points in Ethology. Cambridge University Press, Cambridge. Dahl, J. F., and R. D. Nadler. (1989). The external genitalia of female gibbons. American Journal of Primatology 18: Dahl, J. F., and R. D. Nadler. (1992a). The external genitalia of female gibbons (Hylobates lar). The Anatomical Record 232: Dahl, J. F., and R. D. Nadler. (1992b). Genital Swelling in Females of the Monogamous Gibbon, Hylobates (H) lar. American Journal of Physical Anthropology 89: Dixon, A. F. (1983). Observations on the evolution and behavioural significance of "sexual skin" in female primates. Advances in the Study of Behaviour 13: Domb, L. G., and M. Pagel. (2001). Sexual swellings advertise female quality in wild baboons. Nature 410:

13 Emery, M. A., and P. L. Whitten. (2003). Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behavioural Ecology and Sociobiology 54: Geissmann, T. (1991). Reassessment of the age of sexual maturity in gibbons (H. lar). American Journal of Primatology 23: Hrdy, S. B. (1981). The Woman that Never Evolved. Harvard University Press, Cambridge, Mass. Nadler, R. D., C. E. Graham, D. C. Collins, and K. G. Gould. (1979). Plasma gonadotrophins, prolactin, gonadal steriods and genital swelling during the menstrual cycle of lowland gorillas. Endocrinology 105: Nunn, C., L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Animal Behaviour 58: Pagel, M. (1994). The evolution of conspicuous oestrus advertisement in Old World monkeys. Animal Behaviour 47: Palombit, R. A. (1994). Extra pair copulations in a monogamous ape. Animal Behaviour 47: Reichard, U. (1995). Extra Pair Copulation in a monogamous gibbon (H. lar). Ethology 100: Setchell, J. M., and E. J. Wickings. (2004). Sexual swelling in mandrills (Mandrillus sphinx):a test of the reliable indicator hypothesis. Behavioural Ecology 15: Short, R. V. (1977). Sexual selection and the descent of man. Pages 3-19 in J. H. Calaby, and C. H. Tyndale-Biscoe, editors. Reproduction and Evolution. Australian Academy of Science, Canberra. Short, R. V. (1979). Sexual selection and its component parts, somatic and genital selection, as illustrated by man and the great apes. Advanced Study of Behaviour 9: Short, R. V. (1981). Sexual selection in man and the great apes. Pages in C. E. Graham, editor. Reproductive Biology of the Great Apes: Comparative and Biomedical Perspectives. Academic Press, New York. Struhsaker, T. T. (1976). The red colobus monkey. Chicago University Press, Chicago. 13

14 Zinner, D., C. L. Nunn, C. P. van Schaik, and P. M. Kappeler. (2004). Sexual selection and exaggerated sexual swellings of female primates.. Pages in P. M. Kappeler, and C. P. van Schaik, editors. Sexual Selection in Primates: New and Comparative Perspectives.. Cambridge University Press, Cambridge. 14

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