Male Masturbation in Nonhuman Primates 1 2 Thomsen et al. Masturbating male Japanese macaque (Macaca fuscata yakui) from Yakushima Island, Japan. (Photo by Ruth Thomsen.) Male Masturbation in Nonhuman Primates SPERM COMPETITION AND THE FUNCTION OF MALE MASTURBATION IN NONHUMAN PRIMATES Ruth Thomsen, Joseph Soltis, and Christian Teltscher Department Biology II, LM-University of Munich, Germany (R.T.); Laboratory of Comparative Ethology, National Institutes of Health, USA (J.S.); and Max-Planck-Institute for Behavioral Physiology, Seewiesen, Germany (C.T.) INTRODUCTION In humans, male masturbation is well documented by a large body of scientific literature. The most famous reports on human male sexuality that include masturbatory activity are Kinsey et al. [1948] and Hite [1981], in which men provided descriptions of their onanistic habits. At a proximate level of explanation, masturbation results from the coincidence of sexual desire and lack of sexual opportunity. At first glance, masturbation may appear non-adaptive in that ejaculates are produced only to be wasted. Andrologists have long considered male masturbation a natural part of human sexuality, however. Zimmerman et al. [1965], for example, argued that one function of male masturbation might be to flush out old or low quality sperm from the genital tract. In nonhuman primates, on the other hand, masturbation has either been ignored altogether, regarded merely as a compensatory act given a lack of mating opportunity during sexual arousal [e.g., Linnankoski et al., 1981; Bielert & van der Walt, 1982], or viewed as a pathology exacerbated by captivity [Dittrich, 1968; Savage & Malick, 1977; Beck & Power, 1988; Mootnick & Baker, 1994]. Can masturbation be integrated into an adaptive, evolutionary framework? Darwin [1859] originally proposed the theory of sexual selection, in contrast to natural selection, arguing that the former depends “not on a struggle for existence, but on a struggle between the males for possession of the female” (such that) “the result is not death to the unsuccessful competitor, but few or no offspring [p.136]”. Trivers [1972] expanded on Darwin’s ideas by showing how the non-investing sex (usually male) is the most likely to compete for access to the opposite sex, while the investing sex (usually female) is the more likely to mate with discrimination. One of the most obvious forms of sexual selection is direct contest competition that occurs between members of the same sex over access to opposite-sex mates, and can result in conspicuous sexual size dimorphism and weaponry [Andersson, 1994]. Much biologically meaningful sexual intrigue occurs after copulation, however. That is, competition also operates at the level of ejaculates from different males that compete to fertilize ova. 3 4 Thomsen et al. Although many scientists may have inherently recognized this fact, sperm competition was defined relatively late by Parker [1970] as: “...competition within a single female between the sperm from two or more males for the fertilization of the ova.” More recently, to incorporate the phenomenon of external fertilization, he has modified his definition to: “...competition between the sperm from two or more males for the fertilization of a given set of ova” [Parker, 1998]. Sperm competition is usually likened to a raffle, where the male with the largest amount of sperm is more likely to win fertilization of the ova [Parker, 1984; Parker et al., 1990; Parker, 1990]. If such is the case, why then do some animals paradoxically waste costly ejaculate by masturbating instead of conserving sperm for future mating opportunity, as observed in some bat species [Racey, 1979]? Masturbation may be viewed as an adaptation, however, provided sperm quality, in addition to sperm quantity, is taken into account. Baker and Bellis [1993, 1995] proposed that masturbation is a reproductive strategy whereby low quality sperm is flushed out of the system, thus increasing the quality of the next ejaculate, which then should outcompete older sperm from rivals during a sperm competition. Using the comparative approach, we investigated the distribution of masturbation across primate taxa in order to explore its adaptive significance. Unlike mammals generally [Ford & Beach, 1951; Beach, 1976], primate males seem to be unique in that they masturbate more or less regularly [e.g. Macaca arctoides: Linnankoski et al., 1981, 1993; Nieuwenhuijsen et al., 1986; Papio ursinus: Bielert & van der Walt, 1982; Pan troglodytes: Kollar et al., 1968] (Figure 1). Since humans exhibit a highly variable mating system and live under a variety of influences associated with civilization that can fundamentally alter patterns of reproduction, we limited our investigation to nonhuman primates. We present the results of a survey of 91 biologists, who returned 131 questionnaires concerning masturbation in 52 nonhuman primate species. The information gained from the questionnaires is on the whole less anecdotal and more detailed and reliable than information in the literature on this topic. First, we investigated the distribution of masturbation across primate taxa, and compared its frequency in captive to wild-living primates. If masturbation occurs only (or mainly) in captivity, then it may not warrant detailed study from an evolutionary viewpoint. Masturbation in captive species still may be of interest to animal caretakers, however. Second, we examined the relationship between masturbation and the level of sperm competition. If masturbation is related to sperm competition and functions to flush out low quality sperm [Zimmerman et al., 1965; Baker & Bellis, 1993, 1995], then it should be observed most often in species forming multimale-multifemale (MM-MF) breeding systems. This is because females mate regularly with multiple males in such groups, as evidenced from copious behavioral observations [e.g. Tutin, 1979; Dunbar, 1984; Small, 1990; Ohsawa et al., 1993; Berard et al., 1994; Manson, 1996; Dixson, 1998; Soltis et al., 1999]. On the other hand, a growing body of DNA-paternity analyses conducted in a variety of animals reveals that females living in monogamous social groups do not mate exclusively with the resident male [e.g., birds: Poldmaa et al., 1995; Dixon et al., 1994; prairie dogs: Travis et al., 1996]. Despite these findings, however, sperm competition is Male Masturbation in Nonhuman Primates Figure 1. A captive, group-living male baboon (Papio anubis) sits masturbating in the Fort Reno Science Park, University of Oklahoma. (Photo by Janette Wallis) probably still lower in such species than in species forming MM-MF groups, in which females not only mate with many males (sources above) but often do so within several hours [Macaca fuscata: personal observation; M. mulatta: Lindburg, 1983]. In contrast, the degree of promiscuity in monogamously living female gibbons (Hylobates lar) is much less extensive [Reichard, 1995]. If masturbation is observed to occur independently of the breeding system, however, then explanations other than sperm competition might be sought. MATERIALS AND METHODS Questionnaires The questionnaire concerning the observation of nonhuman primate male masturbation was sent to biologists between 1996 and 2000. Since contributors were free to pass the questionnaire on to colleagues, the exact number of recipients is unknown. The questionnaire requested information concerning the species (common and scientific name), study site (wild, semi-free, captive), breeding system (MM-MF, monoga- 5 6 Thomsen et al. mous, dispersed, family group, or one-male unit) and the approximate amount of observation time the researcher had spent observing that particular species. The scientific name of the species was verified using Rowe [1996]. If a researcher did not mention the scientific name, we used the common name to locate it in Rowe [1996]. Where the scientific names used by contributors differed from those of Rowe, we used Rowe’s classification to maintain consistency. “Wild” refers to animals living under natural conditions in their native habitat, “semi-free” refers to animals living in large outdoor cages or monkey parks, and “captive” refers to animals living in cages, zoological gardens or laboratories. Although more than one breeding system can occur within a single species [e.g., Semnopithecus entellus: Sommer & Ragpurohit, 1989; Borries et al., 1991], we used the designation from the questionnaire, ignoring other available information from the literature or from researchers who did not participate in the survey. If a respondent offered two possible breeding systems for one species, we used the system mentioned in Rowe [1996]. As it may be difficult to observe masturbation in the wild, especially in small sized animals or in those occupying the higher strata of a tropical rainforest, “masturbation” was divided into three types: (1) rhythmic masturbation only (M), i.e., rhythmic rubbing of the penis (excluding simply holding the penis), (2) masturbation culminating in ejaculation (ME), and no observation of masturbation (N). Responses had to be noted as either “yes” or “no”, excluding such possibilities as “perhaps” or “probably.” Questionnaires that contained ambiguous answers were excluded from the analysis. In cases where a species was represented more than once in the questionnaire replies, information from the researcher with the longest period of observation was used in the analysis. If, however, two different answers concerning the same species were received, such as one questionnaire recording “yes” for masturbation with ejaculation and another “no”, the positive answer was used and the negative answer ignored, without respect to the length of time spent observing the species. Of the 131 returned questionnaires, 52 were analyzed - each representing a separate species or subspecies. The 79 questionnaires not included in the analysis were rejected based on redundant, conflicting or missing information, as outlined above. Thirty-three (63.5%) of the 52 species exhibited a MM-MF breeding system. The remaining 19 (36.5%) species exhibited breeding systems other than MM-MF. Seventeen species lived in captivity, five under semi-free conditions, and 30 in the wild (Table I). Statistical analysis The data collected from questionnaires were subject to phylogenetic regression analysis to examine the association between the occurrence of masturbation and breeding system, while controlling for phylogenetic propinquity [Felsenstein, 1985; Harvey & Pagel, 1991]. We performed phylogenetic “independent contrast” regression analysis after Grafen [1989], and the primate phylogeny adopted was that of Purvis [1995]. We used the Glim-4-program (Royal Statistical Society, 12 Errol Street, London, EC1Y8LX, Great Britain) to calculate regression coefficients (ß), F-values, and 1-tailed p-values. Table I. Returned questionnaires referring to the observation of masturbation in 52 primate species in alphabetical order. BS = breeding system, MM-MF = multi-male multi-female, other = one-male-unit, family group, solitary, monogamous or dispersed breeding system. ME = masturbation with ejaculation, M = rhythmic masturbation, N = no observation of masturbation. Male Masturbation in Nonhuman Primates 7 8 Thomsen et al. Male Masturbation in Nonhuman Primates 9 10 Thomsen et al. Table II. Masturbation in 52 wild and captive primate species and masturbation in relation to the breeding system. *The 5 semi-free living species were incorporated into the total number of species. Wild Captive Total* Number of species 30 (100%) 17 (100%) 52 (100%) Masturbation with ejaculation (ME) 15 (50%) 3 (17.6%) 21 (40.4%) Masturbation only (M) 7 (23.3%) 6 (35.3%) 13 (25%) Masturbation total 22 (73.3%) 9 (52.9%) 34 (65.4%) No masturbation (N) 8 (26.7%) 8 (47.1%) 18 (34.6%) Multimale-multifemale (MM-MF) 19 (63.3%) 9 (52.9%) 33 (63.5%) Other 11 (36.6%) 8 (47.1%) 19 (36.5%) Breeding system Two degrees of freedom (df) were assigned to each F-value. The first df results from the number of independent variables used in the analysis, and the second from the number of contrasts. Significance was set at alpha=0.05. Each species was designated as “MM-MF” or “Other” (monogamous, dispersed, family group, solitary, or one-male unit). We performed nine separate phylogenetic regression analyses. First, we conducted regressions for (1) wild animals only (N=30), (2) captive animals only (N=17), and (3) for all combined (N=52). Semi-free animals (N=5) were not analyzed separately, and one species had undefined living conditions. For each of the above categories (1-3), three types of comparisons were made among masturbation types. In (A), species in which rhythmic masturbation or masturbation with ejaculation was observed were compared to species in which masturbation was not observed (M or ME versus N). In (B), species in which masturbation with ejaculation was observed were compared to species in which only rhythmic masturbation was observed or masturbation was not observed (ME versus M or N). Finally, in (C), Male Masturbation in Nonhuman Primates Figure 2. Occurence of masturbation in 52 primate species in relation to their breeding system. MM-MF = multimale-multifemale, other = one-male unit, family group, monogamous, solitary or dispersed breeding system. species in which masturbation with ejaculation was observed were compared to species in which masturbation was not observed (ME versus N). RESULTS Masturbation in wild and captive nonhuman primates Rhythmic masturbation or masturbation with ejaculation was observed in 34 of 52 species (65.4%). Masturbation with ejaculation was observed in 21 of 52 species (40.4%), and only masturbation was observed in an additional 13 of the 52 species (25.0%). Eighteen species (34.6%) were not observed to masturbate (Table II). Twentytwo of 30 wild species (73.4%) and 9 of 17 (52.9%) captive species masturbated either rhythmically or with ejaculation. There was no significant difference in the occurrence of masturbation between wild living versus semi-free and captive living species (Fisher’s exact test, N=51, p > 0.05). Masturbation and breeding system Figure 2 shows the occurrence of masturbation with ejaculation and rhythmic masturbation with regard to the breeding system of the 52 named species. Twentyseven of 33 (81.8%) species living in a MM-MF breeding system and 7 of 18 (38.8%) species living in other breeding systems were observed to masturbate. Nineteen of 33 (57.6%) “MM-MF species” masturbated with ejaculation and 2 of 18 (11.1%) “other species” did so. 11 12 Thomsen et al. Table III. Phylogenetic regression analysis of the occurrence of masturbation in 52 nonhuman primate species. ME = masturbation with ejaculation, M = masturbation only, N = no masturbation was observed. For variables, see text. 1. Wild 2. Captive 3. All Combined A. Number of species: ME and M vs N 30 17 52 ß 0.44 0.22 52 F 9.86 0.3 9.62 df 1 and 9 1 and 8 1 and 28 p < 0.025 NS NS B. Number of species: ME vs M and N 30 17 52 ß 0.57 0.05 0.49 F 12.86 0.02 16.36 df 1 and 16 1 and 4 1 and 23 p < 0.005 NS < 0.001 C. Number of species: ME vs N 23 11 39 ß 0.66 0.05 0.51 F 176.68 0.02 16.41 df 1 and 7 1 and 3 1 and 15 p < 0.001 NS < 0.005 When analyzing only the 17 captive species, no association between breeding system and the occurrence of masturbation could be found (Table III, column 2). When analyzing only wild groups or all groups combined, however, all tests yielded a positive and significant association between the occurrence of masturbation and a MM-MF breeding system (Table III, columns 1 and 3). The strictest test from an evolutionary standpoint is that comparing masturbation with ejaculation to no masturbation in wild living species only (p < 0.001, Table III, column 1, row C). Male Masturbation in Nonhuman Primates DISCUSSION Masturbation is a common behavior in nonhuman primates We obtained results for 52 of 243 primate species [22.2%, Rowe, 1996]. Based on this sample, masturbation appears to be a common behavior in nonhuman primates, as it is in humans. Males in 73.3% of wild living species were observed masturbating and in 40.4% masturbation until ejaculation was observed. Furthermore, we found no statistical difference in the incidence of masturbation between wild and captive groups. In fact, the incidence was higher in wild than in captive contexts (wild: 73.3%, captive: 52.9%). This result indicates that masturbation is not merely a byproduct of captivity. Masturbation in captive versus wild species Although masturbation is common in both wild and captive contexts, cases of pathological masturbation due to captivity are likely to exist. For example, haremgroup mountain gorillas (Gorilla gorilla beringei) and monogamous gibbons (Hylobates spp.) both exhibit breeding systems usually unassociated with masturbation, yet reports of masturbation for captive members of these species are available [Mootnick & Baker, 1994; Table I]. In the case of captive gibbons, masturbation was directed towards humans or humans providing food, and as such may be considered artifacts of captivity. In many cases, however, the proximate cause of masturbation may be similar in captivity and the wild, in particular, when sexual motivation is combined with a lack of sexual opportunity. In captivity, this may occur when males are housed without females [e.g., Macaca arctoides: Nieuwenhuijsen et al., 1986, 1987], especially when there is visual contact with unattainable females in a neighboring cage [e.g., M. arctoides: Linnankoski et al., 1993; M. fuscata: personal observation]. In the wild essentially the same phenomenon occurs, for example, when low ranking males are excluded from mating with receptive females who are nevertheless in plain visual contact [e.g., M. fuscata: personal observation; M. silenus: A. Kumar, questionnaire]. Masturbation is dependent on the level of sperm competition Our results confirm that nonhuman primate species exhibiting MM-MF breeding systems have a higher probability of male masturbation than species exhibiting other breeding systems, independent of phylogenetic relationship. Furthermore, the degree of sperm competition is highest in MM-MF groups. Our results show that males of species facing a high risk of sperm competition are more likely to masturbate than males of species in which there is considerably less risk of sperm competition. This contrasts with previous theories of sperm competition in mammals, which emphasize the importance of sperm volume and sperm number [testis size: Harcourt et al., 1981; Hosken, 1998; sperm number: Møller, 1988]. Consistent with the latter reasoning is the fact that larger testes produce more sperm [e.g., Amann et al., 1976]. Furthermore, testis size and the number of males with whom a female copulates are highly correlated within many orders, from insects to mammals [Ridley, 1999]. These facts, however, give the impression that only ejaculate quantity is important in sperm competition. 13 14 Thomsen et al. We emphasize not the quantity of sperm alone but the quantity and quality of sperm, which jointly determine the competitiveness of an ejaculate. Parameters of ejaculate which measure quality include sperm velocity, sperm morphology and the percentage of motile sperm per ejaculate (motility), all of which are known to be important factors for fertilization [Mann & Lutwak-Mann, 1981; Mortimer & Templeton, 1982; Barrat & Cooke, 1991]. Moreover, we now know from work on Japanese macaques (Macaca fuscata) that sperm quantity increases, but that sperm quality decreases, with increased storage time in the cauda epididymis [Thomsen, 2000]. Thus, a clear trade-off exists between the absolute quantity and the overall quality of an ejaculate. A high volume but low quality ejaculate may indeed lose in sperm competition with a low volume but high quality ejaculate. If this is so, then the adaptive consequence of well-timed masturbation would be to flush out low quality sperm, ensuring that the next ejaculate will be of higher quality, although it may at the same time be of smaller volume. In short, masturbation may be part of the primate males’ reproductive strategy, by which ejaculates are optimized with respect to their ability to fertilize ova in a sperm competition game with rival males. Methodological limitations One problem of the “questionnaire” method may be that the breeding system itself influences observers’ ability to observe masturbation. For example, masturbation may be more difficult to detect in harem groups than in MM-MF living groups since those who observe harem groups may concentrate on the resident male and may rarely observe all-male groups, in which masturbation may be more likely to occur. This argument, however, does not apply to captive species, since the chance to observe masturbation in, for example, a single-caged Hamadryas baboon (one-male unit) or in a Japanese macaque (MM-MF) is the same. Also, in the wild, all-male groups or solitary males may be around the female group and observable at least sometimes, especially when females are in estrus. Finally, some researchers [e.g., Yamagiwa, mountain gorillas] have focused exclusively on all male groups or on solitary males. In any case, according to our questionnaires, 6 of 9 species forming one-male groups actually were observed to masturbate. Another difficulty was that some primates are seasonal breeders (species with clear mating and birth periods), others are non-seasonal breeders (mating all year round) and still other species cannot be assigned to a category due to different opinions of researchers or to existing transitional stages. In some seasonal breeding species, testicular size increases in the breeding season and decreases in the non-breeding season [e.g., Macaca fuscata: Matsubayashi et al., 1991]. Ejaculate production and, therefore, masturbation with ejaculation is restricted to the breeding season and thus cannot be detected in the non-breeding season. However, the behavior of masturbation itself (without ejaculation) also occurs frequently in the non-breeding season at least in one well studied species [Macaca fuscata, Yakushima Island, Thomsen, 2000]. Some of the contributors to the questionnaire were able to remember whether they observed masturbation during the breeding or non-breeding season, while others could not. Species without mating seasons also were observed to masturbate with ejacula- Male Masturbation in Nonhuman Primates tion (e.g., Macaca nigra, Pan troglodytes) so that we know that this behavior is not completely restricted to seasonal breeders. CONCLUSIONS AND PROSPECTS Using phylogenetic regression analysis in a comparison of 52 nonhuman primate species, male masturbation was found to be strongly associated with species that exhibit a MM-MF breeding system. Put another way, masturbation occurs most in species that experience the most intense sperm competition. Based on the physiological data on ejaculate quantity and quality from previous studies and the results of the phylogenetic regression analysis presented in this paper, we conclude that masturbation is an adaptation to sperm competition whereby old ejaculate is discarded. These results support the masturbation hypothesis put forward by Baker & Bellis [1993, 1995] and suggest that both sperm quantity and sperm quality are important factors in sperm competition games. Finally, the knowledge of masturbation in nonhuman primates is not only interesting from an evolutionary viewpoint, but can be used also in research surrounding nonhuman primates’ ejaculate. First, ejaculate can be collected soon after masturbation (e.g., from a clean ground floor under a hanging cage) in the laboratory so that electro-ejaculation is not necessary. Also, chimpanzees can be trained to masturbate with ejaculation into an artificial vagina [Gould & Young, 1996]. Second, the ejaculate collected after masturbation from wild living primate species can be used for DNAanalysis [Soltis et al., 2001], endocrinological (or other type of physiological) studies, virological (or other medicinal) studies, and to investigate male fertility in the wild [Thomsen, 2000]. In summary, the knowledge of masturbating species and the collection of masturbatory ejaculates may become a promising non-invasive method for future studies in primatology. ACKNOWLEDGMENTS Above all, we are extremely grateful to all the respondents to the questionnaire. Prof. Volker Sommer gave critical suggestions and advice during an early stage of the study and special thanks belong to him for providing unpublished data on male masturbation. R.T. thanks Prof. Gerhard Neuweiler, Dr. Barbara Fruth, and Dr. Gottfried Hohmann for continuous support of her work in a variety of ways and Prof. Heribert Hofer for his help. R.T. was financed by a grant (HSP III, No. D/97/16290) from the German Academic Exchange Service (DAAD). J.S. received support from the USA National Science Foundation and the Japan Society for the Promotion of Science. Thanks also to the contributors to the questionnaire, who were not named in Table I: G. Anzensberger, R. Boouratna, A. Boug, F. Colmenares, H. Donkin, B. Fruth, S. Fujita, G. Hanya, S. Harcourt, S. Hayakawa, V. Hayes, S. Heiduck, D. Hill, C. Knogge, I. Küderling, N. Kutsukake, M. Libet, A. Meder, B. Moorman, R. Noe, H. Ohsawa, A. Paul, P. Peibrot, S. Perry, S. Preuschofft, U. Radespiel, S. Rumenap, A. Schaefers, J. Seier, J. Silk, K. Stewart, H. Sugiura, T. Tanaka, K. Watanabe, D. Wrogemann, G. Yamakoshi and D. Zumpe. 15 16 Thomsen et al. 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Female mating strategy in an enclosed group of Japanese macaques. Am J Primatol 47:263-278. Soltis J, Thomsen R, Takenaka O. 2001. The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. Anim Behav 62: 485-494. Sommer V, Ragpurohit LS. 1989. Male reproductive success in harem groups of Hanuman langurs (Presbytis entellus). Int J Primatol 10:293-317. Thomsen R. 2000. Sperm competition and the function of male masturbation in Japanese macaques (Macaca fuscata). [Dissertation]. Munich: University of Munich. 89 p. CD-ROM. Travis SE, Slobodchikoff CN, Keim P. 1996. Social assemblages and mating relationships in prairie dogs: a DNA fingerprint analysis. Behav Ecol 7:95-100. Trivers R. 1972. Parental investment and sexual selection. In: Sexual selection and the descent of man. Campbell B, editor. Chicago: Aldine Press. p 52-97. Tutin CEG. 1979. Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29-38. Zimmerman SJ, Maude MB, Moldawer M. 1965. Frequent ejaculation and total sperm count, motility, and form in humans. Fertil Steril 16:342-345. Dr. Ruth Thomsen is a post-doctoral fellow at the Institute of Zoo & Wildlife Research (IZW) at Berlin, Germany. Her doctoral research concerned the costs and benefits of male masturbation and the quality of ejaculates in wild Japanese macaques on Yakushima Island, Japan. She currently works with a project on female mate choice and ejaculate quality of domestic cats. Male Masturbation in Nonhuman Primates Dr. Joseph Soltis is a post-doctoral fellow at the National Institutes of Health. He has conducted research on the conflict between the sexes in wild Japanese macaques on Yakushima Island, Japan, and currently examines the endocrinology of affiliative relationships in squirrel monkeys at the NIH. Dr. Christian Teltscher completed his Ph.D. at the Max-Planck Institute for Behavioral Physiology, Seewiesen, Germany. His research topics were virilization in primates and the endocrinology of wild hyenas in the Serengeti National Park, Tanzania. He currently works in the molecular biology industry. 19