Thong et al. Hystrix It. J. Mamm. (n.s.) 22(1) 2011: 139-147 meinschaft (SFB 550 and Schn 138/27-1), in Kerivoulinae and Murininae (Chi- the Conservation Leadership Programme roptera: Vespertilionidae) from Malay- SAME-SEX SEXUAL BEHAVIOUR IN BATS (UK and USA), the Darwin Initiative (DE- sia. J. Zool., Lond., 249: 359–374. FRA, UK, Project Nos: 14-001 and 18- Kruskop S.V., Eger J. 2008. A new species 002), and the Rufford Foundation (UK) for of tube-nosed bat Murina (Vespertili- MARCO RICCUCCI their various financial support. All methods onidae, Chiroptera) from Vietnam. applied comply with the national laws of Acta Chiropterol., 10(2): 213–220. GIRC (Gruppo Italiano Ricerca Chirotteri), via Maccatella 26/B, 56124 Pisa, Italy Vietnam and bat captures were carried out Schmieder D.A., Kingston T., Hashim R., E-mail: [email protected] under the license of competent authorities. Siemers B.M. 2010. Breaking the trade-off: rainforest bats maximize Received 25 August 2010; accepted 19 March 2011 REFERENCES bandwidth and repetition rate of echo- location calls as they approach prey. ABSTRACT - In recent years many studies have been published on animal homosexual- Borissenko A.V., Kruskop S.V. 2003. Bats Biol. Lett. Published online before ity. Here, we reviewed the available observations on bat homosexual behaviour, presenting of Vietnam and Adjacent Territories: print on 31 March 2010, some behavioural hypotheses. Same-sex sexual behaviours can be classified in 6 different an identification manual. Moscow, 212
139 Riccucci M.
1999; Judson 2003; Balcombe 2006; German pamphlets published by Karoly Sommer and Vasey 2006; Roughgar- Maria Kertbeny in 1869 (Kertbeny 2000). den 2009; Poiani 2010). Also at least In animal behaviour, there is no consensus one children's book, "And Tango on the terminology to be used for same sex sexual behaviours (Tab. 1). Makes Three", was produced, dealing “Same-sex sexual behaviour” is one with a homosexual couple, Roy and among several definitions: “actions be- Silo, two Chinstrap penguins in New tween members of the same sex that are York’s Central Park Zoo, that hatch also attributed to opposite-sex courtship or and raise a chick named Tango (Parnell mating interactions.” (Bailey and Zuk and Richardson 2005). 2009). According to Weinrich (1980) “ho- Recent zoological studies have pro- mosexual behaviour in animals” is “any vided abundant evidence for same-sex behaviour between two members of the sexual behaviour among animals, not same sex which uses the mechanisms of only in captivity but also in the wild sexual arousal. This definition is quite broad”. For Sommer and Vasey (2006) (reviews in: Bagemihl 1999; Rough- “homosexual behaviour refers to courtship garden 2004; Sommer and Vasey 2006; display, mounting and/or genital contact Bailey and Zuk, 2009). Currently, the and stimulation between same-sex indi- phenomenon has been reported in more viduals. […] this term does not imply some than 1500 animal species, including sort of life-long pattern of homosexual ac- most vertebrate groups and also insects, tivity or exclusivity, nor does it denote any spiders, crustaceans, octopi and para- particular form of enduring sexual relation- sitic worms, and it is well documented ship, monogamous or otherwise”. Bage- for 500 of them (Bagemihl 1999). Den- mihl (1999) used a broader approach: “het- niston (1980) concludes that "in the erosexuality is defined as courtship, affec- vertebrates, apparent homosexual be- tionate, sexual, pair-bonding, and/or par- enting behaviours between animals of the haviour increases as we ascend the opposite sex, while homosexuality is de- taxonomic tree toward mammals ...”. fined as these same activities when they Sexual behaviour in bats has been stud- occur between animals of the same sex.”. ied since the XIX century (Rollinat and Perhaps this last definition is too wide and Trouessart 1895a, 1895b, 1895c; 1896; there is the risk of including social interac- 1897; Monticelli 1896). Recently, a tions under sexual behaviour (Sommer and particular copulatory behaviour has Vasey 2006). Another word, more in use in been investigated in the fruit bat the past, is “pederasty”; this word derives from the Greek paiderastia = "love of Cynopterus sphinx (Tan et al. 2009). th The aim of this review is to summarize boys", but in XIX century it indicated the current state of knowledge on homosexuality in general (“pédérastie” in Gadeau de Kerville, 1896; “päderastie” in same-sex sexual behaviour in bats, dis- Karsch, 1900). The term “tribadism” de- cussing recent reports in the historical notes a sort of female-female genital sex, context; existing controversies in the usually known now in animals as GG rub- field are also pointed out. bing (genito-genital) (Karsch 1900; Hoh- mann and Fruth 2000). Coercive sex (rape) A QUESTION OF TERMS is defined as “copulation resisted to the best of the victim’s ability unless such re- The term homoseksuäl (= homosexual) was sistance would probably result in death or used for the first time in two anonymous serious injury to the victim or in death or
140 Riccucci M. Homosexuality in bats
1999; Judson 2003; Balcombe 2006; German pamphlets published by Karoly injury to individuals the victim commonly been seen between mature females, Sommer and Vasey 2006; Roughgar- Maria Kertbeny in 1869 (Kertbeny 2000). protects” (Abele and Gilchrist 1977; mothers and daughters, pair of subordi- den 2009; Poiani 2010). Also at least In animal behaviour, there is no consensus Thornhill and Palmer 2000). Some authors nate males […]. One of two males en- one children's book, "And Tango on the terminology to be used for same sex prefer to use forced copulation (Hilton gaged in this activity was observed to sexual behaviours (Tab. 1). 1982; Brennan et al. 2007). More specifi- continue licking the genitals of the Makes Three", was produced, dealing “Same-sex sexual behaviour” is one cally here we define coercive sex (or rape with a homosexual couple, Roy and among several definitions: “actions be- or forced copulation) as sexual contact other [...] “ (Courts 1996). Silo, two Chinstrap penguins in New tween members of the same sex that are achieved: 1. without apparent consent; 2. “Copulation mount: The male grips the York’s Central Park Zoo, that hatch also attributed to opposite-sex courtship or by the use of physical force, coercion, de- female from behind, restraining her and raise a chick named Tango (Parnell mating interactions.” (Bailey and Zuk ception; and/or 3. when the victim is physi- forelimbs with his (his ventral surface and Richardson 2005). 2009). According to Weinrich (1980) “ho- cally impaired and/or asleep or uncon- against her dorsal) and holds the scruff Recent zoological studies have pro- mosexual behaviour in animals” is “any scious (in torpor or in hibernation). of her neck in his mouth. This has also vided abundant evidence for same-sex behaviour between two members of the It has long been observed that some ani- been observed between daughter and sexual behaviour among animals, not same sex which uses the mechanisms of mals appear to show behaviour resembling mother - the larger daughter relent- only in captivity but also in the wild sexual arousal. This definition is quite rape in humans, i.e. combining sexual in- broad”. For Sommer and Vasey (2006) tercourse with violent assault; these obser- lessly in pursuit for extended periods (reviews in: Bagemihl 1999; Rough- “homosexual behaviour refers to courtship vations of forced sex among animals are and fighting off approaching males. garden 2004; Sommer and Vasey 2006; display, mounting and/or genital contact not controversial but their interpretation is This was perhaps play behaviour incor- Bailey and Zuk, 2009). Currently, the and stimulation between same-sex indi- debated (Clutton-Brock and Parker 1995; porating male-female copulations. At- phenomenon has been reported in more viduals. […] this term does not imply some Thornhill and Palmer 2000; Travis 2003). tempted and actual mounts were also than 1500 animal species, including sort of life-long pattern of homosexual ac- As a general criterion, throughout the paper seen during “play” between pairs of most vertebrate groups and also insects, tivity or exclusivity, nor does it denote any it has been chosen to use the same terms mature females, pairs of males, by a spiders, crustaceans, octopi and para- particular form of enduring sexual relation- used by the author(s) of the paper where mature female to a male, who also ship, monogamous or otherwise”. Bage- the behaviour is mentioned. sitic worms, and it is well documented groomed his genitals, and by a mother mihl (1999) used a broader approach: “het- for 500 of them (Bagemihl 1999). Den- to her daughter”. “Male-male mounting erosexuality is defined as courtship, affec- RESULTS niston (1980) concludes that "in the behaviour in P. rodricensis is thought vertebrates, apparent homosexual be- tionate, sexual, pair-bonding, and/or par- enting behaviours between animals of the to be a way of asserting dominance. haviour increases as we ascend the opposite sex, while homosexuality is de- Observations of P. livingstonii would taxonomic tree toward mammals ...”. Same-sex sexual behaviours can be fined as these same activities when they appear to confirm this, as male-male Sexual behaviour in bats has been stud- classified in 6 different groups and till occur between animals of the same sex.”. mounting apparently did not have a ied since the XIX century (Rollinat and now have been documented in 22 spe- Perhaps this last definition is too wide and sexual function, as the mounting male Trouessart 1895a, 1895b, 1895c; 1896; there is the risk of including social interac- cies of megabats and microbats. was never observed to have an erect 1897; Monticelli 1896). Recently, a tions under sexual behaviour (Sommer and particular copulatory behaviour has Vasey 2006). Another word, more in use in 1. In captivity penis” (Courts 1996). been investigated in the fruit bat the past, is “pederasty”; this word derives Greenhall (1965) describes homosexual from the Greek paiderastia = "love of behaviour in Desmodus rotundus Cynopterus sphinx (Tan et al. 2009). th Studying the social behaviour of Ptero- The aim of this review is to summarize boys", but in XIX century it indicated pus livingstonii in captivity, several (vampire bat) as an “aberrant behav- the current state of knowledge on homosexuality in general (“pédérastie” in observations were collected on male- iour”; the captive males were seen in- Gadeau de Kerville, 1896; “päderastie” in same-sex sexual behaviour in bats, dis- male and female-female sexual behav- volved in licking and rubbing one an- Karsch, 1900). The term “tribadism” de- other bodies and genitals; masturbation cussing recent reports in the historical notes a sort of female-female genital sex, iour (Tab. 2). context; existing controversies in the usually known now in animals as GG rub- “Play: involves prolonged gentle wres- among young males has also been ob- field are also pointed out. bing (genito-genital) (Karsch 1900; Hoh- tling, holding, mounting, biting and served. mann and Fruth 2000). Coercive sex (rape) genital interest […] May lead to one Pre-copulatory behaviour in captivity A QUESTION OF TERMS is defined as “copulation resisted to the bat being mounted by the other […] but was observed in Corynorhinus rafines- best of the victim’s ability unless such re- for males, without an erect penis. So- quii: four hibernating males had been The term homoseksuäl (= homosexual) was sistance would probably result in death or cial play (or perhaps in some cases, confined with an unmated female. A used for the first time in two anonymous serious injury to the victim or in death or homosexual behaviour) of this kind has male used to rub his snout over the face,
141 Riccucci M.
Table 1 - Same-sex sexual behaviour in bats.
Mutual homosexual grooming and licking Nelson 1964, 1965; Greenhall 1965; Courts 1996 Homosexual masturbation Greenhall 1965 Homosexual play Neuweiler 1969; Courts 1996 Homosexual mounting Rollinat and Trouessart 1895, 1896; Reed 1946; Vesey-Fitzgerald 1949; Neuweiler 1969; Barclay and Thomas 1979; Thomas et al. 1979; Crucitti 1981; Gebhard 1995; Courts 1996; Crucitti in litteris) Coercive sex – Rape – Forced copulation Pearson et al. 1952; Barclay and Thomas 1979; Thomas et al. 1979; Gebhard 1995; Judson 2003 Cross species homosexual sex (Myotis Vesey-Fitzgerald 1949 daubentoni and M. nattereri)
Table 2 - Bat species observed while engaging in homosexual activities.
IN CAPTIVITY Pteropus livingstonii Courts 1996 Pteropus rodricensis Courts 1996 Desmodus rotundus Greenhall 1965 IN THE WILD Pteropus poliocephalus Nelson 1964, 1965 Pteropus giganteus Neuweiler 1969 Corynorhinus rafinesquii Pearson et al. 1952 Miniopterus schreibersii Crucitti in litteris Eptesicus serotinus Rollinat and Trouessart 1895;Vesey-Fitzgerald 1949 Myotis bechsteinii Vesey-Fitzgerald 1949 Myotis capaccinii Crucitti 1981 Myotis daubentonii Vesey-Fitzgerald 1949 Myotis lucifugus Barclay and Thomas 1979; Thomas et al. 1979 Myotis myotis Rollinat and Trouessart 1896 Myotis mystacinus Vesey-Fitzgerald 1949 Myotis nattereri Nyctalus noctula Vesey-Fitzgerald 1949; Gebhard 1995 Nyctalus leisleri Pipistrellus pipistrellus Plecotus auritus Vesey-Fitzgerald 1949 Barbastella barbastellus Rhinolophus ferrumequinum Rhinolophus hipposideros
142 Riccucci M. Homosexuality in bats
Table 1 - Same-sex sexual behaviour in bats. neck, forearms and ventral surface of (from early September until early De- the female; in one occasion he mounted cember). In some way it is seasonally Mutual homosexual grooming and licking Nelson 1964, 1965; Greenhall 1965; Courts on the female’s back; several time the bisexual and both sexes show this form 1996 female flew off and “he would embrace of mutual homosexual grooming, more Homosexual masturbation Greenhall 1965 and nose the first bat that he encoun- common in males. Pteropus giganteus Homosexual play Neuweiler 1969; Courts 1996 tered regardless of sex. Even torpid males often mount one another (with males would receive from him as much erections and thrusting) while play- Homosexual mounting Rollinat and Trouessart 1895, 1896; Reed 1946; Vesey-Fitzgerald 1949; Neuweiler as a minute of nosing before he contin- wrestling (Neuweiler 1969). In Myotis 1969; Barclay and Thomas 1979; Thomas et ued his search.” (Pearson et al. 1952). lucifugus males often mount other al. 1979; Crucitti 1981; Gebhard 1995; Courts Following the previously mentioned males (as well as females) during the 1996; Crucitti in litteris) definitions, this behaviour can be re- late fall and winter, when many of the Coercive sex – Rape – Forced copulation Pearson et al. 1952; Barclay and Thomas garded as “coercive sex or rape or mounted individuals are torpid. These 1979; Thomas et al. 1979; Gebhard 1995; forced copulation”. coercive copulations usually include Judson 2003 A male Eptesicus serotinus was ob- ejaculation and the mounted animal Cross species homosexual sex (Myotis Vesey-Fitzgerald 1949 served while trying to mount other often makes a typical “copulation call”, daubentoni and M. nattereri) males in captivity; one male ap- consisting of a long squawk (Barclay proached another with his penis erect and Thomas 1979; Thomas et al. 1979). Table 2 - Bat species observed while engaging in homosexual activities. and mounted him from behind, grasp- A similar behaviour was seen in hiber- ing him above the neck and thrusting nacula of Nyctalus noctula; sexual ac- his penis between the other male's legs tive males, woken up from lethargy on IN CAPTIVITY (Rollinat and Trouessart 1895c). This a warm day, were involved in mating Pteropus livingstonii Courts 1996 mating attempt occurred during hiber- with active and lethargic females. Pteropus rodricensis Courts 1996 nation (February), when the males were “Several times attempts were made to Desmodus rotundus Greenhall 1965 put in a warm room. The same behav- copulate with lethargic males. These IN THE WILD iour was seen in Myotis myotis, again then behaved like females, calling out Pteropus poliocephalus Nelson 1964, 1965 during the arousal from hibernation and loudly and presenting their buccal Pteropus giganteus Neuweiler 1969 following location in a warm room glands with opened mouth” (Gebhard Corynorhinus rafinesquii Pearson et al. 1952 (Rollinat and Trouessart 1896). 1995). Miniopterus schreibersii Crucitti in litteris According to Vesey-Fitzgerald (1949) Eptesicus serotinus Rollinat and Trouessart 1895;Vesey-Fitzgerald 1949 2. In the wild homosexual behaviours were observed Myotis bechsteinii Vesey-Fitzgerald 1949 in all British bat species (twelve in Myotis capaccinii Crucitti 1981 Among the reproductive calls of Ptero- 1949): “Homosexuality is common in Myotis daubentonii Vesey-Fitzgerald 1949 pus poliocephalus Nelson (1964) iden- the spring in all species, and, since the Myotis lucifugus Barclay and Thomas 1979; Thomas et al. 1979 tified a “precopulation call”: “This males are in full possession of their Myotis myotis Rollinat and Trouessart 1896 pulsed grating call is continuously ut- powers, I suspect throughout the sum- Myotis mystacinus Vesey-Fitzgerald 1949 tered by the partners of hetero- or ho- mer... I have even seen homosexuality Myotis nattereri mosexual grooming, in which the wing between Natterer's and Daubenton's Nyctalus noctula Vesey-Fitzgerald 1949; Gebhard 1995 membranes are wrapped around the bats (Myotis nattereri and M. dauben- Nyctalus leisleri partners, and the chest, neck, and wing tonii)". Pipistrellus pipistrellus membranes of the other are bitten and In two different situations Crucitti Plecotus auritus Vesey-Fitzgerald 1949 licked” ; males may have an erection (1981) saw Myotis capaccinii males in Barbastella barbastellus (Nelson 1965). This species lives in the same position of male-female het- Rhinolophus ferrumequinum Rhinolophus hipposideros sex-segregated camps during the non- erosexual mounting, one gripping the breeding period, before conception back of the other’s fur. A similar be-
143 Riccucci M. haviour was also observed in Miniop- male insect has the imperious need to terus schreibersii (Crucitti, in litteris). copulate but no females are available; the latter refers to coupling between DISCUSSION males in the presence of available fe- males. Captivity probably caused the In general, it is difficult to collect in- number of cases of homosexuality to formation on same-sex sexual behav- increase but "il n'en est pas moins abso- iour (Dagg 1984), because being rather lument certain" (nevertheless it is abso- rare, it can be easily overlooked by re- lutely certain) that couplings between searchers. Moreover, some authors may male insects also occur in a state of be either reluctant to refer to or not complete freedom; such occurrence concerned with homosexual events. also takes place among vertebrates Referring to bats, their nocturnal activ- (Gadeau de Kerville 1896). Homosex- ity and the difficulty to distinguish the ual behaviour is usually observed in sex of mating individuals make this solitary mammals under two condi- task even harder. Denniston (1980) re- tions: 1) reproductive fitness is main- ported that “frequent homosexual activ- tained through homosexual behaviour ity has been described for all species of when the availability of one sex, usu- mammals of which careful observa- ally females, is limited; 2) animals kept tions have been made". As most ani- in intensive housing conditions perform mals have only been observed in the homosexual behaviour to dissipate wild for a limited amount of time, more stress and wield dominance (Feige et field studies will consequently increase al. 2007). our knowledge of homosexuality in the c) What causes same-sex sexual behav- animal kingdom and the number of iour? Several explications have been species reported with homosexual be- proposed: social play; physical contact haviours. (non-play); dominance-assertion; ag- Some general questions are: gression and intrasexual conflict; social a) “Captivity and domestication” vs. tension regulation; sexual excitement; “natural conditions”: same-sex sexual social relationship; alloparental care; behaviour is more frequent in captive practice for adult heterosexual copula- than in wild populations, maybe be- tion; poor discrimination (Bagemihl cause males and females are grouped 1999; Sommer and Vasey 2006). together by sex or in different ways Current knowledge about same-sex than in the wild; captive animals can sexual behaviour in bats does not allow form bonds atypical of natural situa- to answer any of the previous ques- tions. tions. b) Why does homosexual behaviour Even less known is the meaning of occur? Referring to insects, Gadeau de cross species sex; sometimes animals Kerville (1896) distinguished two cate- harass other animals (from the same or gories: “pédéderastie par nécessité” closely-related species) for sex. As an (pederasty by necessity) and example, an Antarctic fur seal was ob- “pédérastie par goût” (pederasty by served while attempting to have sex taste/choice); the former occurs when a with a king penguin on Marion Island
144 Riccucci M. Homosexuality in bats haviour was also observed in Miniop- male insect has the imperious need to (De Bruyn 2008). Either the seal’s ACKNOWLEDGMENTS terus schreibersii (Crucitti, in litteris). copulate but no females are available; predatory impulse had been redirected the latter refers to coupling between into sexual arousal or it was a sexual I would like to thank Jiří Gaisler (Depart- DISCUSSION males in the presence of available fe- manifestation of the play instinct of ment of Botany and Zoology, Masaryk males. Captivity probably caused the seals. Unfortunately, it is not possible University, Brno), Gareth Jones (School of In general, it is difficult to collect in- number of cases of homosexuality to to extrapolate these hypotheses to ex- Biological Sciences, University of Bristol) and Sébastien Puechmaille (School of Bi- formation on same-sex sexual behav- increase but "il n'en est pas moins abso- plain the inter-specific same-sex events ology and Environmental Science, Univer- iour (Dagg 1984), because being rather lument certain" (nevertheless it is abso- recorded by Vesey-Fitzgerald (1949). sity College Dublin) for their valuable rare, it can be easily overlooked by re- lutely certain) that couplings between More observations are needed to better comments, and Pierangelo Crucitti (Società searchers. Moreover, some authors may male insects also occur in a state of classify and understand these different Romana di Scienze Naturali - SRSN) for be either reluctant to refer to or not complete freedom; such occurrence behavioural patterns, keeping in mind providing useful information. I am also concerned with homosexual events. also takes place among vertebrates that any account of homosexuality in grateful to Mrs. Rosanna Bertozzi, librar- Referring to bats, their nocturnal activ- (Gadeau de Kerville 1896). Homosex- animal is in some way the account of ian, Faculty of Agriculture, University of Pisa and to Bibliothèque mondiale des ity and the difficulty to distinguish the ual behaviour is usually observed in human interpretations of these phe- chauves-souris (Genève). sex of mating individuals make this solitary mammals under two condi- nomena (Bagemihl 1999). tions: 1) reproductive fitness is main- task even harder. Denniston (1980) re- Reviewing the available records on ported that “frequent homosexual activ- tained through homosexual behaviour REFERENCES homosexual behaviour among non- ity has been described for all species of when the availability of one sex, usu- human animals, it appears that this be- mammals of which careful observa- ally females, is limited; 2) animals kept Abele L., Gilchrist S. 1977. Homosexual tions have been made". As most ani- in intensive housing conditions perform haviour is not exclusive over their rape and sexual selection in Acantho- whole lifespan (Cvorovic 2006; Som- cephalan worms. Science 197: 81-83. mals have only been observed in the homosexual behaviour to dissipate Bailey N.W, Zuk M. 2009. Same-sex sexual wild for a limited amount of time, more stress and wield dominance (Feige et mer and Vasey 2006; contra Poiani 2010). Accordingly, at first sight this behavior and evolution. 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