Male Masturbation in Nonhuman Primates
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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.
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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-
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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
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Male Masturbation in Nonhuman Primates
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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.
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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
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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.
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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.
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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.
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