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International Journal of Primatology, Vol. 25, No. 5, October 2004 (
Male Masturbation in Free-Ranging
Japanese Macaques
Ruth Thomsen1,3 and Joseph Soltis2
Received November 5, 2003; revision February 5, 2004; accepted February 13, 2004
We studied masturbatory behavior of males over a 14-mo period in freeranging Japanese macaques (Macaca fuscata yakui) on Yakushima island,
Japan. We distinguished 2 types: (1) masturbation only and (2) masturbation
with final ejaculation. Both types occurred in all 15 adult troop males. We calculated masturbation only as an index (M/h). It occurred over the whole year;
however, it was more frequent during the mating than during the non-mating
periods. Masturbation with ejaculation was restricted to the mating period.
Male mating success correlated positively with social status. Both rate of masturbation only and masturbatory ejaculations increased as male social status
and male mating success declined. Lower-ranking males had higher rates
of masturbation only, i.e., they spent more time masturbating than higherranking males did. Lower-ranking males also had higher proportions of
ejaculates for masturbation, while higher-ranking males used most of their
ejaculates for mating.
KEY WORDS: masturbation; Japanese macaques; Yakushima.
INTRODUCTION
Male masturbation occurs in captive nonhuman primate species, including gibbons (Hylobates spp.), chacma baboons (Papio ursinus), mangabeys
(Cercocebus albigena), red spider monkeys (Ateles geoffroyi), chimpanzees
1 Institute
for Zoo and Wildlife Research, Department of Evolutionary Ecology, AlfredKowalke-Str. 17, 10315 Berlin, Germany.
2 Wildlife Tracking Center, Animal Programs Administration, Disney’s Animal Kingdom, P.O.
Box 10000, Lake Buena Vista, Florida 32830.
3 To whom correspondence should be addressed; e-mail: thomsen@izw-berlin.de.
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(Pan troglodytes), lowland gorillas (Gorilla gorilla gorilla) and some
macaque species (Bielert and van der Walt, 1982; Carpenter, 1942;
Linnankoski et al., 1993; Maple, 1977; Mootnick and Baker, 1994;
Nieuwenhuijsen et al., 1987). In a study on reproductive strategies in freeranging baboons (Papio cynocephalus anubis) Bercovitch (1989) noted that
masturbation to ejaculation did not correlate with testicular size.
Theory predicts that the amount of ejaculate is an important factor during sperm competition as a male should increase his chance to outcompete
the sperm of rival males by increasing the amount of sperm inseminated
into a female (Parker, 1970, 1982). This quantity model is supported by
comparative studies that show that testicular size and the level of female
promiscuity are highly and positively correlated within taxa (Gage, 1994;
Harcourt et al., 1981; Ridley, 1999). In short, the quantity model suggests
that males in species that face a high degree of sperm competition should
possess large testes, produce large amounts of sperm, store sperm in large
sperm storage organs, and finally inseminate large ejaculates into females.
Recently 34 out of a total of 52 nonhuman primate species masturbated
(65%). Masturbation only and masturbation to ejaculation, occurred more
often in species in a multimale multifemale social system than in species living
in other social systems (Thomsen et al., 2003). Masturbation to ejaculation
could be beneficial if it improves ejaculate quality in spite of the costs of
loosing sperm (Baker and Bellis, 1993). But it also could be costly if it reduces
a male’s chance for further copulations in the case they run out of sperm
because of previous masturbatory ejaculations.
Primate males of middle or low social status are often excluded from
mating due to successful mate guarding of females by males of higher social
status (Berard et al., 1994; Soltis et al., 2001). Since sperm production is continuous throughout the breeding season (Matsubayashi and Enomoto, 1983)
nonmating or less mating males of those species have 2 options regarding
their sperm: (A) store sperm inside capus, corpus and cauda epididymis and
vas deferens until an opportunity for copulation arises or (B) flush out sperm
by masturbation.
Our aim was (1) to get basic information of male masturbation in a
free-ranging primate species, (2) to detect patterns of male masturbation
during a whole year and (3) to test whether masturbation with and without ejaculation are related to male social status and male mating success.
We choose Japanese macaques (Macaca fuscata) as subject animals because
masturbation only occurs in captive males (Tokuda, 1961) and we saw masturbation to ejaculation ad libitum in a free-ranging population in 1993.
Furthermore, Japanese macaques are seasonally breeding primates, females
mate with multiple males, and degree of sperm competition is high (Soltis,
et al., 1999).
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METHODS
Definitions
Mating: Japanese macaques are series mounters. Mating refers to terminal, ejaculatory mounts that are characterized by a rigid posture of the
male and remaining ejaculate (white plug) on the female’s perineum (Soltis
et al., 2000).
Masturbation: Rhythmic manual rubbing of the erect penis for ≥5 sec.
Masturbation with ejaculation: Rhythmic manual rubbing of the erect
penis terminating in ejaculation.
Study Animals and Sites
We conducted observations on NINA-A-troop in the Hanyama study
site on the Northwestern coast of Yakushima Island (Maruhashi, 1980).
The troop has been continuously habituated to human observers since 1994
(Yakushima Research Group). During the study period it comprised ca. 50
individuals, including juveniles and infants. Troop composition changed between 2 mating periods (MP) due to natural demographic processes such
as deaths, births, immigration and emigration. It consisted of 15 adult males
and 15 adult females during MP 1997 (October–February) and 12 males and
13 females during MP 1998 (October-November). All adults could be recognized individually. We calculated social status (rank 1–15) via a dominance
matrix. The age of each male (4–15 years) was known (Soltis et al., 2000).
Behavioral Data Collection
From October 1997 until November 1998 we collected data on both
types of masturbation and on male mating success via focal animal sampling (Thomsen) and ad libitum observations (Thomsen and Soltis, Altmann,
1974). Total time of focal sampling (males and females) comprised 1204 h
by Thomsen (Soltis et al., 2000). Total time of focal sampling of the 15 males
by Thomsen is 435 h 30 min (mean ± s.d. = 30.1 ± 22.5 h/male, range: 6 h
10 min – 12 h).
From time of detection of the troop in the morning the selected male
was located and followed during the daytime over a 2-day period, if possible.
If the focal male could not be detected within a 30-min period of initially
finding the troop, we followed the male with the closest lower social status
instead for the rest of the day. If a male was lost in the dense and steep forest,
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we followed him again when he could be located. We included focal samples in the analysis if he was followed successfully for ≥6 h per observation
day without interruptions for >5 min (N = 12 males in MP 1997, N = 13
males in MP 1998). To calculate amount of time a male spent masturbating
per hour observation (independently of final ejaculation) we used one-zero
sampling. Within 1-min-periods on the instance of the sample point it was
recorded whether or not the focal male had masturbated during the preceding sample interval (Martin and Bateson, 2002). We calculated an individual
masturbatory index by dividing the total number of observed masturbations
by duration of total focal sampling time in h per male (M/h). Whenever we
saw a male mating or masturbating with ejaculation we recorded exact time
and social circumstances.
Statistics
We calculated nonparametrical statistics via SPSS version 9.0 for Windows. All tests are two-tailed and two-tailed alpha is 0.05 (Conover, 1980).
RESULTS
Seasonal Differences in Masturbation
We could follow 13 of 15 males for ≥6 h during observation days. Time
that males spent with masturbating reached a maximum from October until
February when at least one troop female was in estrus (M/h: mean ± s.d. =
4.1 ± 1.9, N = 13 males). It was significantly reduced during the nonmating
period between March and August 1998, i.e. when no female was in estrus
(M/h: mean ± s.d. = 1.2 ± 0.9; Wilcoxon, z = −3.19, p < 0.001).
Masturbation Only and Male Social Status
Incidence of masturbation increased as male social status declined
(Fig. 1). The lower a male’s social status the higher his masturbatory index (accuracy 0.1), i.e. the more time he spent with masturbation during
the 14-mo period (rs = 0.75, N = 13, p < 0.05). This correlation applied to
both mating (rs = 0.75, N = 13, p < 0.01) and nonmating periods (rs = 0.71,
N = 13, p < 0.01). The smaller correlation coefficient of the nonmating period might be a result of fewer males present regularly in the troop during
this period of the year.
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Fig. 1. Masturbatory index of free-ranging Japanese macaque males on Yakushima island,
Japan, in relation to their social status. The lower a male’s social status the more time he
spent masturbating.
Masturbation to Ejaculation and Male Mating Success
We observed a total of N = 213 ejaculations: 105 during mating and
108 finished a masturbatory event. We observed all 15 troop males to masturbate to ejaculation at least once. Masturbation with ejaculation occurred
during different social circumstances. Males masturbated in the presence
of a mating pair (N = 19, 17.6%). Males masturbated in the presence of
an estrous female (N = 40, 37.0%). In 7 out of the 40 cases (17.5%), they
mated successfully on the same day after they had masturbated with ejaculation. Males started masturbating after an estrous female had passed them
(N = 14, 13.0%). Males masturbated in the presence of other masturbating
males (N = 10, 9.3%). Males masturbated when staying solitarily in the forest (N = 20, 18.5%). We could not clearly assign 5 cases (4.6%) to any of
these situations.
With the exception of the lowest-ranking male (rank 15) all other 14
troop males mateed at least once with ejaculation (range: 1–28; mean ± s.d. =
7.0 ± 8.9). Total number of ejaculates inseminated by NINA-A-troop males
into females increased with social status (rs = 0.934, N = 15, p < 0.01).
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Proportion of Ejaculates Used to Mate and to Masturbate
Proportion of all ejaculations occurring during mating increased with
male social status (rs = 0.68, N = 15, p < 0.01). In contrast, proportion used
for masturbation decreased with social status (rs = −0.67, N = 15, p < 0.01).
For instance, 7 (21.2%) of the alpha-male ejaculations were masturbatory,
whereas at least half (50%–100%) of ejaculations of males of rank ≥6 were
masturbatory (Fig. 2). The 2nd-ranking male, which masturbated disproportionately often given his rank (57.5%) was displaced from the alpha position 3 days before data collection started in October 1997 (Soltis, personal
observation).
DISCUSSION
We focused on male masturbation because female masturbation has not
been observed in the population. All 15 males of NINA-A-troop, males of
3 surrounding troops (Miki Matsubara, Hideki Sugiura, Sachiko Hayakawa,
personal communication) and 4 non-troop males (own observations) masturbated during the study period. Masturbation also occurs in Japanese
macaques in a provisioned troop at Arashiyama, Japan (Michael Huffman,
unpublished data) and in males in solitar cages (own observations).
The male masturbatory index was higher during the mating (mean
M/hour = 4.2) than during the nonmating periods (mean M/hour = 1.2).
Fig. 2. Proportion of ejaculates which NINA-A-troop males (N = 15)
used for mating and for masturbation in relation to their social status. Higher-ranking males used a higher proportion of ejaculates for
mating while mid- and low-ranking males used higher proportions for
masturbation.
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During the mating period, NINA-A-troop males masturbated 4.2 times
within 60 min independently from ejaculations. This would be 50.4 times
within one 12-h day. There is no comparative datum from other free-ranging
primate species available yet, however, the value seems to be high. Macaques
in general may masturbate more frequently than chimpanzees or other nonseasonal or less promiscuous species do. Seasonality might be important for
the amount of masturbation due to the presence of visible cues, i.e. estrous
females or mating pairs.
The masturbatory index in our subjects is related to male social status.
Males of low social status spent more time masturbating than males of high
social status did. In rhesus macaques (Macaca mulatta) male social status
correlated positively with median mount series duration (Manson, 1996).
Brief and hidden copulations of sneaker males are perhaps an adaptive
response to the threat of mount series disruption by higher-ranking males
(Dunbar, 1984; Manson, 1996; Ohsawa et al., 1993). In humans, there is a
linear relationship between motile sperm concentration and motile sperm
number and the time taken to produce a masturbatory ejaculate within 5–
30 min (Pound et al., 2002). In macaques masturbation only could function
to increase precopulatory sexual arousal of lower-ranking males that might
increase sperm number in the cauda epididymis and vas deferens before
mounting.
Proportion of all ejaculations used for mating increased with social status, while in low- and middle-ranking males ejaculations were largely masturbatory. Although masturbation to ejaculation occurred during differing
social circumstances, the majority of 67.6% of cases occured in the presence of an estrous female, which may reflect the same pattern of masturbation stimulated by visual cues in captives (Bielert and van der Walt, 1982;
Linnankoski et al., 1993). Furthermore, in 7 cases, sneaker males masturbated only a few times (2–17 min) before mating. The behavior also occurs
in rhesus macaques (Carpenter, 1942) and savanna baboons (Bercovitch,
1989; Ransom, 1981). Masturbation to ejaculation before mating could also
be accidental, i.e. The quantity model to improve number of motile sperm
by masturbating proximate to mating might fail and males simply lost their
ejaculates. Or it could lead to lower ejaculate volume and reduced sperm
number, but to a better ejaculate quality because the next ejaculate that is
used for mating may contain fewer but quicker moving sperm. This interpretation of the observed pattern would support the quality model of Baker
and Bellis (1993).
Finally, describing patterns of masturbation in wild populations might
inform future models of sperm competition in primates, which should incorporate observations of mating behaviors in addition to data on quantity and
quality of sperm.
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ACKNOWLEDGMENTS
We thank all members of the Yakushima Research Group in Japan
for their interest and active discussion during this study. Special thanks
go to Juichi Yamagiwa, Kiyoaki Matsubayashi and Hideyuki Ohsawa from
Primate Research Institute of the Kyoto-University for their support. RT
is grateful to Gerhard Neuweiler, Department Biology II, University of
Munich and to Heribert Hofer, Institute for Zoo and Wildlife Research,
Berlin, who enriched this work with critical comments. The study was financed
by the German Academic Exchange Service (HSP III, D/97/16290).
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