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Male Homosexual Behaviour Accompanied by Ejaculation in a Free-Ranging Troop of Japanese Macaques (Macaca fuscata)

Yuji Takenoshita
Department of Zoology, Graduate School of Science, Kyoto University, Kyoto, Japan 

Folia Primatol 1998; 69: 364-367

Key Words
I. Homosexual behaviour, Mounting, Arashiyama, Macacafuscata

Introduction
Study Troop and Method
Results
Discussion
Acknowledgments
References

Introduction

Homosexual behaviour among males in free-ranging Japanese macaques (Macacafuscata) has not been reported, whereas that among females has frequently been reported under both free-ranging and captive conditions [1],[ 2]. Mountings between males, commonly seen in Japanese macaques, have not been regarded as 'sexual behaviour'. In most cases, such interactions consist of a single mount and are not accompanied by ejaculation [3]

In this paper, I analyse observed cases of male-male mountings with ejaculation among a free-ranging troop of Japanese macaques and examine whether this behaviour can be classified as 'sexual behaviour'. The causal factors and effects of such behaviour are discussed.

Study Troop and Method

The study was conducted in the Arashiyama Monkey Park, Kyoto prefecture, Japan, and involved members of the Arashiyama E and F troops. All the monkeys have been individually identified since 1954, and birth dates and matrilineal kin relations are known except for those individuals which came from outside Arashiyama [4]. Soybeans and wheat grains were given to the monkeys by the park staff 4 times a day.

Observation periods encompassed two mating seasons, from September 1993 to February 1994 (period 1) and September 1994 to February 1995 (period 2). Total observation days were 162. The number of individuals in each period was 172 and 181 for the E troop, and 134 and 129 for the F troop, respectively. The adult sex ratio (number of males over 7 years old/number of females over 5 years old) was 0.36 in period I and 0.32 in period 2 for the E troop. and 0.35 and 0.33 for the F troop, respectively. 

 Table 1. List of males who engaged in mounting events with ejaculation

Name

Age at period 1 years

Testicles

Natal troop

 Troopl 

Unit1

Momo - 677584

10.5

d

F

F-E

P

Mino - 6369748389

5.5

nd

E

E

C

Mino - 637590

4.5

nd

E

E

C

Glance - 647188

6.5

d

F

F

P

Opress - 7581872

7.5

d

E

E

P

Meme - 6280882

6.5

nd

E

E

C-P

d = Testicles descended; 
nd=testicles not descended; 
C=central unit; 
P=peripheral unit; 
C-P=basically central unit though sometimes seen in the peripheral unit.
1 When the mounting events with ejaculation were observed.
2 Confirmed by indirect evidence (see text).

                                 
The Arashiyama troops consisted of two social subunits. The central unit was composed of high-ranking adult males, adult females and their immature offspring. The peripheral unit consisted of low-ranking adult males and young males. Association between the units was not frequent [5].
Data were collected by the ad libitum method. In this paper, the term 'mounting event' refers to an interaction between two monkeys that involved one or more mountings. The termination of a mounting event was defined by separation of the two participants by at least 15 m, by a cessation of mounting for at least 5 min, or by ejaculation [3].

                                      
Results

Four males were observed to engage in male-male mounting events with ejaculation (table 1). Two of them (Mino-6369748389 and Mino-637590) were prepubescent (i.e. just before testicular descent). They were born in the E troop and usually foraged near their mothers in the central unit of the E troop. Momo-677584 was born in the F troop and transferred to the E troop during period I. Glance-647188 was a peripheral male of the F troop. Momo-677584 and Glance-647188 were sexually mature but had not yet reached their full adult body size.

Eleven mounting events with 152 mountings were observed in three pairs: Momo-677584 and Mino-6369748389 (pair 1); Glance-647188 and Mino-637590 (pair 2); Momo-677584 and Mino-637590 (pair 3). All these pairs were combinations of a young adult male and a prepubescent male. No member of a pair had shared maternal kinship. In the cases of pair 1 and pair 3, both participants mounted each other, while in the cases of pair 2 only Glance-647188 mounted Mino-637590.

When the males mounted they showed penile erection and thrusting and young adult males ejaculated in 3 cases (1 case for each dyad). The mountee's penis also erected while he was mounted. Momo-677584 sometimes reached back and stimulated the mounter's penis manually. No anal penetration was confirmed.

Prepubescent males showed several characteristics which are typical of ovulating females; they had bright red faces and emitted vocalizations similar to 'ovulating calls'. Additionally, the prepubescent male tended to sit in front of the young male with ventrodorsal contact during the mounting events as is seen in male-female mounting events. In fact, when a prepubescent male exhibited the above behavioural and physiological characteristics, he and his partner strongly resembled the mating pair of a young male and ovulating female. 

The pairs formed consort relationships which lasted several days. They foraged together, groomed each other, attacked other monkeys together and engaged in mounting events. None of the adult males and females seemed to pay any attention to these consort pairs. It was once observed that Momo-677584 chased the consort pair of Glance-647188 and Mino-637590 and consequently forced them to terminate the mounting event. 

In addition to the above observation, 2 other males were noted to have congealed semen on their lower back on one occasion in the study period (table 1). It is obvious that they had been mounted and ejaculated on by other males. Mino-6369748389 and Mino-637590 were observed to engage in sexual behaviour with troop E females.

                                                                                 
Discussion

Mounting events observed in this study included most of the behavioural elements typical of heterosexual interactions of Japanese macaques (multiple mountings, pelvic thrust, ejaculation, consortship), and shown by physical and behavioural characteristics of one of the participants mimicking characteristics during ovulation. Also these interactions occurred during the mating season. These interactions might be classified as sexual behaviour.

It is difficult to examine the causal factor (i.e. abnormal hormonal state [6], [7]) of these behaviours since there is no physiological information available. All the pairs were combinations of a male from troop E and a male from troop F, so it is unlikely that the participants had formed abnormally affiliative relations as juveniles as reported by Erwin and Maple [8].

There are two hypotheses about homosexual behaviour: 

(1) it is a training for mature heterosexual behaviour [9], and 

(2) it serves to regulate one's tension [6], [10], [11].

 

First, were the homosexual behaviours training for heterosexual intercourse? The interactions observed in this study included several behavioural elements which are rarely seen in heterosexual intercourse, i.e. mutual mounting, thrusting without intromission and emission of female-like calls by males. If these behavioural elements were seen in heterosexual intercourse, the interaction would become less harmonious and would disturb fertilization. Thus, it is not valid to regard these behaviours as training for heterosexual intercourse.

Second, did the homosexual behaviours reduce social tension between the males? In this study, mounting events did not occur after a fight or at feeding time. Thus, this hypothesis is not applicable to these cases.
                                                          

Although the sex ratio of adults of the Arashiyama troops during the study period was not biased towards males compared to other troops [12], it is difficult for peripheral males to gain access to ovulating females, since the central adult males would attack the peripheral males if they tried to do so. Females did not tend to prefer prepubescent males. In group-living rhesus macaques, the males engaged in homosexual behaviour when their access to females was physically limited [13]. Thus in these cases, it is possible that the males engaged in homosexual behaviour as an alternative to heterosexual intercourse, because their access to ovulating females was socially limited.

                                                     Acknowledgments 

I wish to thank Prof. T. Nishida for his guidance and encouragement. Drs. J. Yamagiwa, Y. Takahata. H. Ihobe and D.S. Sprague for stimulating discussion and valuable advice, Dr. S. Suzuki. Ms. L.A. Turner and other members of the Laboratory of Human Evolution Studies of Kyoto University for discussion and helpful criticism and Mr. N. Asaba and other staff of the Iwatayama Monkey Park for their support during the field study. 

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References 

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