Non-reproductive sexual behavior in animals

Non-reproductive sexual behavior consists of sexual activities animals participate in that do not lead to the reproduction of the species. Although procreation continues to be the primary explanation for sexual behavior in animals, recent observations on animal behavior have given alternative reasons for the engagement in sexual activities by animals.[1] Animals have been observed to engage in sex for social interaction, demonstration of dominance, aggression relief, exchange for significant materials, and sexual stimulation. Observed non-procreative sexual activities include non-copulatory mounting (without penetration, or by the female), oral sex, genital stimulation, anal stimulation, interspecies mating, and acts of affection.[2] There have also been observations of animals engaging in homosexual behaviors, evincing it to be a natural part of life for many reptiles, insects, and animals, including lions. [3] [4][5]

Additionally mentioned, sex with dead animals[6] and sex involving juveniles.[7]

Social interaction and bonding

Lions are known to engage in sex to create bonds and interact with each other. Lions live in a social group known as a pride that consists of 2–18 females and 1–7 males. The females found in these prides were born into the pride. The males enter the pride from other prides. The success of reproduction for each individual lion is dependent on the number of male lions found in their social group. Male lions create coalitions and search for prides to take over. Successful coalitions have usually created a strong bond with each other and will take over prides. Once winning in a competition, all current males in the pride will be kicked out and left to find another pride. While in search for another pride these males will often engage in sexual behavior with each other; creating a strong bond in this new coalition created.[8][9]

Sex is a basic form of communication in bonobos’ life. It seems to infuse everything from simple expressions of affection to the establishment of dominance. Female bonobos have been observed to engage in sexual activities to create bonds with dominant bonobos. Having created this bond with the male, they will share food with each other and not compete with each other.[1] All members of the group are potential sex partners, males participate in sexual activity with other males, as do females with other females. These bonds made between females are for protection against male bonobos. If a male bonobo attempts to harass a female bonobo, the other females will help the female defend herself because of the strong bonds they have with each other.[10]

Aggression

Several species in the animal kingdom turn to sexual activity as a way to solve a disagreement. Bonobos are one species notoriously known for using sexual behavior to relieve their aggression with each other.[4] Sex is part of bonobo's daily routine and social life. Unlike other primates aggression is substituted with sex. Sexual activity in bonobos is very high, yet the rate of reproduction is the same as a chimpanzee.[1]

In a study concentrated on primate aggression, researchers wanted to observe primates in conflict. How primates coped and resolved conflicts was a main concern in this study. Researchers stated that after primates participated in a heated, physical fight; both primates involved in the fight would hug and have a mouth-to-mouth kiss. This action was considered as a demonstration of affection and reconciliation.[1]

Sexual interaction has also been witnessed in female bonobos to avoid aggression. When hungry, the female bonobo will approach a male bonobo and engage in sexual activity to avoid aggression. After their quick sexual activity, the female will take a portion of the male's food. The male will not demonstrate any form of aggression towards the female.[4]

Proximate causes

Awareness in species is difficult to determine. Learned behaviors that have been demonstrated in laboratories have provided good evidence that animals have instinct and a reward system. The behavior of laboratory animals demonstrates a mental experience wherein the animal's instincts tell it if it carries out a certain action, it will then receive what it needs.[11] For example, the lab rat will push the lever because it knows food will fall out of the hole in the wall. It does not need awareness, but it does seem to work on a reward system. The lab rat learned the action needed to be fed.

Studies of the brain have proven that pleasure and displeasure are an important component in the lives of animals.[12] It has been established that the limbic neural mechanism that generates reactions are very similar across all mammals. Many studies have concentrated on the brain reward system and how similar it is across mammals. Through extensive research, scientists have been able to conclude that the brain reward system in animals is extremely similar to that of humans. The mechanism of core pleasure reaction is significantly important for animals and humans.[12]

Case study

In a case study, female Japanese macaques were studied to find evidence of possible female copulatory orgasms. Through the study the frequency of orgasms did not correlate with the age of the Japanese macaques or the rank. Researchers observed that the longer and higher number of pelvic thrusts, the longer copulation lasted. There was an orgasmic response in 80 of the 240 Japanese macaques studied.[13]

Reward system

Evolutionary principles have predicted that the reward system is part of the proximate mechanism underlying the behavior. Because animals possess a brain reward system they are motivated to perform in different ways by desire and reinforced by pleasure.[11] Animals establish security of food, shelter, social contact, and mating because proximate mechanism, if they do not seek these necessities they will not survive.[14]

All vertebrates share similarities in body structure; they all have a skeleton, a nervous system, a circulatory system, a digestive system and excretory system. Similar to humans, non-human animals also have a sensory system. The sensory system is responsible for the basic five senses from touch to tasting. Most of the physiological and biochemical responses found in animals are found in humans. Neurophysiologists have not found any fundamental difference between the structure and function of neurons and synapse between humans and other animals.[11]

Case study

Recent studies using positron emission tomography (PET) and magnetic resonance imaging (MRI) has provided evidence proving that chemical changes that occur with emotions are similar between humans and non-human animals. In a study comparing guinea pigs and humans, it was determined that the distress experienced by offspring separation in a guinea pig and a human going through depression activates the same region of the brain. The opiate receptor was also examined, allowing observation of the pleasure stimuli. In the procedure both a human and a rat had their receptors blocked with a certain drug. Once receptors were blocked, both the rat and the human were exposed to pleasurable food, but both were disinclined to eat the food.[15]

Types of behavior

Engagements of sexual activities during non-breeding seasons have been observed in the animal kingdom. Dolphins and Japanese macaques are two of the many species that engage in sexual activities that do not lead to fertilization. Great varieties of non-copulatory mounting are expressed in several species. Male lions engage in mounting with other male lions, especially when in search for another pride.[8] The varieties of mounting include mounting without erections, mounting with erection but no penetration, and mounting from the side.

Expressions of affection are displayed in the animal kingdom as well. Affectionate behaviors do not include penetration or genital rubbing, but are still seen as a manner of sexual behavior. An affectionate activity can be as simple as licking.[4] Male lions are known for head rubbing, bats engage in licking, and mountain sheep rub horns and faces with each other.[16] Animals have also engaged in kissing, touching of noses, mouths and muzzles have been witnessed in African elephants, walruses, and mountain zebras.[5] Primates also engage in kissing that is incredibly similar to human display of kissing. Chimpanzees have full mouth-to-mouth contact, and bonobos kiss with their mouth open and mutual tongue stimulation.[4] There are a variety of acts to show affection such as African elephants intertwining their trunks, giraffes engaging in “necking”, and Hanuman langurs cuddling with each other in a front to back sitting position.

Non-penetrative genital stimulation is very common throughout the animal kingdom. Different forms of self and partner genital stimulation have been observed in the animal kingdom. Oral sex has been observed throughout the animal kingdom, from dolphins to primates. Bonobos have been observed to transition from a simple demonstration of affection to non-penetrative genital stimulation.[1][16] Animals perform oral sex by licking, sucking or nuzzling the genitals of their partner.[10][16] Another form of genital stimulation is masturbation. Masturbation is widespread throughout mammals for both males and females. It is less common in birds. There are several techniques, in which animals engage in masturbation from using paws, feet, flippers, tails, and sometimes using objects like sticks, pebbles, and leaves.[10] Masturbation occurs more often in primate species with large testes relative to their body size.[17]

Anal penetration

Anal penetration with the penis (both in heterosexual and male homosexual dyads) has been observed among some primate species. Male homosexual anal penetration has been recorded in Old World primate species, including gorillas, orangutans, and some members of the Macaca genus (namely, stumptail, rhesus, and Japanese macaques).[18][19][20][21] It has also been recorded in at least two New World primate species, the squirrel monkey and the spider monkey.[20][22] Morris (1970) also described one heterosexual orangutan dyad where all penetration was anal. However, the practice might have been a consequence of homosexual rearing, as the male orangutan in this dyad had had extensive same–sex experience.[23]

A case of male homosexual anal penetration with the finger has also reported among orangutans,[24] and Bruce Bagemihl mentions it as one of the homosexual practices recorded at least once among male chimpanzees.[10]

Autoeroticism or masturbation

Vervet monkey

It appears that many animals, both male and female, masturbate, both when partners are available and otherwise.[25][26] For example, it has been observed in cats,[27] dogs,[28][29] male deer,[30][31][32] rhinoceroses,[33] boars,[34] and male monkeys.[35][36]

A review from the University of Pennsylvania School of Veterinary Medicine says:[37]

[The] behavior known within the horse breeding industry as masturbation ... involves normal periodic erections and penile movements. This behavior, both from the descriptive field studies cited above and in extensive study of domestic horses, is now understood as normal, frequent behavior of male equids.[38] Attempting to inhibit or punish masturbation, for example by tying a brush to the area of the flank underside where the penis rubs into contact with the underside, which is still a common practice of horse managers regionally around the world, often leads to increased masturbation and disturbances of normal breeding behaviour.[39]

Castration does not prevent masturbation, as it is observed in geldings.[40] Masturbation is common in both mares and stallions, before and after puberty.

Sexologist Havelock Ellis in his 1927 Studies in the Psychology of Sex identified bulls, goats, sheep, camels and elephants as species known to practice autoeroticism, adding of some other species:

I am informed by a gentleman who is a recognized authority on goats, that they sometimes take the penis into the mouth and produce actual orgasm, thus practicing auto-fellatio. As regards ferrets ... "if the bitch, when in heat, cannot obtain a dog [ie, male ferret] she pines and becomes ill. If a smooth pebble is introduced into the hutch, she will masturbate upon it, thus preserving her normal health for one season. But if this artificial substitute is given to her a second season, she will not, as formerly, be content with it." ... Blumenbach observed a bear act somewhat similarly on seeing other bears coupling, and hyenas, according to Ploss and Bartels, have been seen practicing mutual masturbation by licking each other's genitals.

In his 1999 book, Biological exuberance, Bruce Bagemihl documents that:

Autoeroticism also occurs widely among animals, both male and female. A variety of creative techniques are used, including genital stimulation using the hand or front paw (primates, Lions), foot (Vampire Bats, primates), flipper (Walruses), or tail (Savanna Baboons), sometimes accompanied by stimulation of the nipples (Rhesus Macaques, Bonobos); auto-fellating or licking, sucking and/or nuzzling by a male of his own penis (Common Chimpanzees, Savanna Bonobos, Vervet Monkeys, Squirrel Monkeys, Thinhorn Sheep, Bharal, Aovdad, Dwarf Cavies); stimulation of the penis by flipping or rubbing it against the belly or in its own sheath (White-tailed and Mule Deer, Zebras and Takhi); spontaneous ejaculations (Mountain Sheep, Warthogs, Spotted Hyenas); and stimulation of the genitals using inanimate objects (found in several primates and cetaceans).[41]

Many birds masturbate by mounting and copulating with tufts of grass, leaves or mounds of earth, and some mammals such as primates and dolphins also rub their genitals against the ground or other surfaces to stimulate themselves.[41]

Autoeroticism in female mammals, as well as heterosexual and homosexual intercourse (especially in primates), often involves direct or indirect stimulation of the clitoris ... This organ is present in the females of all mammalian species and several other animal groups.[41]

and that:

Apes and Monkeys use a variety of objects to masturbate with and even deliberately create implements for sexual stimulation ... often in highly creative ways.[41]

David Linden, professor of neuroscience at Johns Hopkins University, remarks that:

... perhaps the most creative form of animal masturbation is that of the male bottlenose dolphin, which has been observed to wrap a live, wriggling eel around its penis.[42]

Among elephants, female same-sex behaviours have been documented only in captivity where they are known to masturbate one another with their trunks.[43]

Oral sex

Animals of several species are documented as engaging in both autofellatio and oral sex. Although easily confused by laypeople, autofellatio and oral sex are separate, sexually oriented behaviors, distinct from non-sexual grooming or the investigation of scents.

Auto-fellatio or oral sex in animals is documented in spiders (Darwin's bark[44] and widow[45]), brown bears,[46] stump-tailed macaques,[47] Tibetan macaques,[48] wolves,[49] goats, primates, hyenas,[50] bats,[51] cape ground squirrels[52] and sheep (see section Masturbation for details).

In the greater short-nosed fruit bat, copulation by males is dorsoventral and the females lick the shaft or the base of the male's penis, but not the glans, which has already penetrated the vagina. While the females do this, the penis is not withdrawn and research has shown a positive relationship between length of the time that the penis is licked and the duration of copulation. Post copulation genital grooming has also been observed.[53]

Homosexual behaviour

Two male mallards, Anas platyrhynchos. Mallards have rates of male-male sexual activity that are unusually high for birds, in some cases, as high as 19% of all pairs in a population.[54]

The presence of same-sex sexual behaviour was not scientifically reported on a large scale until recent times. Homosexual behaviour does occur in the animal kingdom outside humans, especially in social species, particularly in marine birds and mammals, monkeys, and the great apes. As of 1999, the scientific literature contained reports of homosexual behavior in at least 471 wild species.[55] Organisers of the Against Nature? exhibit stated that "homosexuality has been observed among 1,500 species, and that in 500 of those it is well documented."[56]

To turn the approach on its head: No species has been found in which homosexual behaviour has not been shown to exist, with the exception of species that never have sex at all, such as sea urchins and aphis. Moreover, a part of the animal kingdom is hermaphroditic, truly bisexual. For them, homosexuality is not an issue.[57]

Homosexual behavior exists on a spectrum, and may or may not involve penetration. Apart from sexual activity, it can refer to homosexual pair-bonding, homosexual parenting and homosexual acts of affection. Engaging in homosexual behavior may allow species to obtain benefits such as gaining practice, relieving tension, and experiencing pleasure.[4][14][16] Georgetown University professor Janet Mann has specifically theorised that homosexual behaviour, at least in dolphins, is an evolutionary advantage that minimizes intraspecies aggression, especially among males.

"Humans have created the myth that sexuality can be justified only by reproduction, which by definition limits it to hetero sex," says Michael Bronski, author of The Pleasure Principle: Culture, Backlash, and the Struggle for Gay Freedom. "But here is an animal society that uses homosexuality to improve its social life."

After studying bonobos for his book Bonobo: The Forgotten Ape, primatologist Frans de Waal, a professor of psychology at Emory University in Atlanta, says that such expressions of intimacy are consistent with the homosexual behaviour of what he terms "the erotic champions of the world". "Same-sex, opposite-sex — bonobos just love sex play," de Waal said in an interview. "They have so much sex, it gets boring."

Homosexual behaviour is found in 6–10% of rams (sheep) and associated with variations in cerebral mass distribution and chemical activity.[58]

Approximately eight percent of [male] rams exhibit sexual preferences [that is, even when given a choice] for male partners (male-oriented rams) in contrast to most rams, which prefer female partners (female-oriented rams). We identified a cell group within the medial preoptic area/anterior hypothalamus of age-matched adult sheep that was significantly larger in adult rams than in ewes ...

Male bighorn sheep are divisible into two kinds: the typical males among whom homosexual behaviour, including intercourse, is common and "effeminate sheep", or "behavioural transvestites", which are not known to engage in homosexual behaviour.[59][60]

Male-male copulation has been observed in captive penguins[61] and homosexual behaviour has been observed among bats, in particular, the fruit bat.[62]

Homosexual pair-bonding and parenting

Homosexual pair-bonding can be established several ways; two of the main ways are pair bonding as partners or as companions.[10] As partners, both animals will engage in sexual activities with each other. In companion bonding, sexual engagement is not necessary in the relationship. This form of homosexuality is more of a partnership and friendship; they spend all their time together. More than 70 species of birds engage in one of these two bonding.[10]

Homosexual parenting (sometimes referred to as cooperative breeding) occurs in a wide variety of species in the animal kingdom.[10] Homosexual parenting can occur in different ways, one of the most common being two females (typically related) coming together to help one another raise their offspring. An example of this is in meadow vole populations. Summer is peak breeding season for meadow voles; however, going into winter and spring there is a division between the male and female meadow vole populations. They prefer communal nesting (because of the thermoregulatory benefits), and therefore, in the winter and spring female meadow voles will commonly not only nest with another female, but nurse their offspring together as well. This kind of communal nursing, and same-sex social bonds, among meadow voles is actually thought to benefit the young — increasing growth and survival rates.[63]

Homosexual parenting is especially present among certain species of birds,[10] one of the most famous examples being Laysan albatross. It is fairly uncommon among different species for unrelated individuals of the same sex to raise offspring together, but female-female pairings in Laysan albatross populations are one of the exceptions. This same-sex pairing and mutual cooperation in chick-rearing often occurs in the Laysan albatross populations which have uneven sex ratios (and an overall greater surplus of females). Also, Laysan albatross are known for being monogamous, and this tendency actually allows same-sex parenting to persist.[64]

Genital-genital rubbing

Genital-genital rubbing, or GG rubbing, among non-human animals is sexual activity in which one animal rubs his or her genitals against the genitals of another animal. The term GG rubbing is frequently used by primatologists to describe this type of sexual intimacy among female bonobos, and is stated to be the "bonobo's most typical sexual pattern, undocumented in any other primate".[65][66] The term is sometimes used in reference to GG rubbing among male bonobos, under the term "penis fencing", which is the non-human form of frot that human males engage in. Such rubbing between males is thought, according to varying evolutionary theorists, to have existed before the development of hominids into humans and bonobos, and may or may not have occurred in the homosexual activity of both of these genetically related species.[67]

Genital rubbing has been observed once among male orangutans[24] and several times in a small group of lar gibbons, where two males thrust their genitals together, sometimes resulting in ejaculation in one of the partners.[68] It has been observed among bull manatees, in conjunction with "kissing",[54] and is also common among homosexually active mammals.[54]

Inter-species sex

A dog mates with a coyote to produce a dog-coyote hybrid.

Some animals opportunistically mate with individuals of another species. This is more commonly observed in domesticated species and animals in captivity, possibly because captivity is associated with a decrease in aggression and an increase in sexual receptivity.[69] Nevertheless, animals in the wild have been observed to attempt sexual activity with other species.[70] It is mostly documented among species that belong to the same genus, but sometimes occurs between species of distant taxa.[71] Alfred Kinsey cites reports of sexual activity involving a female eland with an ostrich, a male dog with a chicken, a male monkey with a snake, and a female chimpanzee with a cat.[72]

A 2008 review of the literature found 44 species pairs that had been observed attempting interspecies mating, and 46 species pairs that had completed interspecies matings, not counting cases that had resulted in hybridization. Most were known from laboratory experiments, but field observations had also been made.[71] It may result in fitness loss because of the waste of time, energy, and nutrients.[71]

Male sea otters have been observed forcibly copulating with seals,[73][74] and male seals have been observed forcibly copulating with penguins.[75] Inter-species sexual behavior has also been observed in sea lions.[76] Male grasshoppers of the species Tetrix ceperoi often mount other species of either sex and even flies, but are normally repelled by the larger females.[71] Males of the spider mite species Panonychus citri copulate with female Panonychus mori mites almost as often as with their own species, even though it does not result in reproduction.[71]

The Japanese macaque has been observed attempting to mate with the sika deer.[77]

Sex involving juveniles

Male stoats (Mustela erminea) will sometimes mate with infant females of their species.[78] This is a natural part of their reproductive biology – they have a delayed gestation period, so these females give birth the following year when they are fully grown.

In one reported observation, a male spotted hyena attempted to mate with a female hyena, but she succeeded in driving him off. He eventually turned to her ten-month-old cub, repeatedly mounting and ejaculating on it. The cub sometimes ignored this and sometimes struggled "slightly as if in play". The mother did not intervene.[79][80]

It appears to be common in the Adélie penguin.[81]

Among insects, there have been reports of immature females being forcibly copulated with.[82]

Juvenile male chimpanzees have been recorded mounting and copulating with immature chimps. Infants in bonobo societies are often involved in sexual behaviour.[83] Immature male bonobos have been recorded initiating genital play with both adolescent and mature female bonobos. Copulation-like contact between immature bonobo males and mature female bonobos increases with age and continues until the male bonobo has reached juvenile age. In contrast, adult gorillas do not show any sexual interest in juvenile or infant members of their species. Primates regularly have sex in full view of infants, juveniles and younger members of their species.[84]

Necrophilia

A male black and white tegu mounts a female that has been dead for two days and attempts to mate. Photo by Ivan Sazima.[85]

Necrophilia describes when an animal engages in a sexual act with a dead animal. It has been observed in mammals, birds, reptiles and frogs.[6] It sometimes occurs in the Adélie penguin.[81] Homosexual necrophilia has been reported between two male mallard ducks. One duck was believed to be pursuing another duck with the goal of rape (a common aspect of duck sexual behaviour) when the second duck collided with a window and died immediately. The observer, Kees Moeliker, suggested that "when one died the other one just went for it and didn't get any negative feedback—well, didn't get any feedback."[86] The case study earned Moeliker an Ig Nobel Prize in biology, awarded for research that cannot or should not be reproduced.[87]

References

1. Waal, F (1995). "Bonobo sex and society". Scientific American. 272 (3): 82–8. Bibcode:1995SciAm.272c..82W. doi:10.1038/scientificamerican0395-82. PMID 7871411.
2. Balcombe, J. (2006). Pleasurable Kingdom: Animals and the Nature of Feeling Good. Palgrave Macmillan. pp. 109, 115.
3. https://en.wikipedia.org/wiki/List_of_animals_displaying_homosexual_behavior. Missing or empty |title= (help)
4. Dubuc, C; Alan F. Dixson (2012). "Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Humans". International Journal of Primatology. 34: 216–218. doi:10.1007/s10764-012-9648-6. S2CID 41078495.
5. Bailey, W; Zuk, M. (2009). "Same-sex sexual behavior and evolution". Trends in Ecology & Evolution. 24 (8): 439–460. CiteSeerX 10.1.1.461.6046. doi:10.1016/j.tree.2009.03.014. PMID 19539396.
6. de Mattos Brito, L. B., Joventino, I. R., Ribeiro, S. C., & Cascon, P. (2012). "Necrophiliac behavior in the "cururu" toad, Rhinella jimi Steuvax, 2002, (Anura, Bufonidae) from Northeastern Brazil" (PDF). North-Western Journal of Zoology. 8 (2): 365.CS1 maint: multiple names: authors list (link)
7. Dukas, R (2010). "Causes and consequences of male–male courtship in fruit flies". Animal Behaviour. 80 (5): 913–919. doi:10.1016/j.anbehav.2010.08.017. S2CID 54253398.
8. Pusey, Anne E (2013). "The Evolution of Sex-Biased Dispersal in Lions". Behaviour. 101 (4): 275–310. JSTOR 4534604.
9. Cooperation, I; Anne E. Pusey (2013). "Competition": 636–642. Cite journal requires |journal= (help)
10. Bagemihl, B (1999). Biological exuberance: Animal homosexuality and natural diversity. New York: Profile Books Limited. ISBN 978-0-312-19239-6.
11. Griffin, D (1981). Question of animal awareness: Evolutionary continuity of mental experience. New York: William Kaufmann Inc.
12. Balcombe, J (2006). Pleasurable kingdom:animals and the nature of feeling good. New York: Macmillan.
13. Troisi, A; M. Carosi (1998). "Female orgasm rate increases with male dominance in Japanese macaques". Animal Behaviour. 56 (5): 1261–1266. doi:10.1006/anbe.1998.0898. PMID 9819343. S2CID 35187116.
14. Hedricks, A (1989). "The evolution of sexual dimorphism in animals: Hypotheses and tests" (PDF). Trends in Ecology & Evolution. 4 (5): 136–138. doi:10.1016/0169-5347(89)90212-7. PMID 21227335.
15. Berridge, K; M. Kringelbach (2008). "Affective neuroscience of pleasure: reward in humans and animals". Psychopharmacology. 199 (3): 457–80. doi:10.1007/s00213-008-1099-6. PMC 3004012. PMID 18311558.
16. Balcombe, J (2009). "Animal pleasure and its moral significance". Applied Animal Behaviour Science. 118 (3–4): 208–216. doi:10.1016/j.applanim.2009.02.012.
17. Dixson, Alan F.; Anderson, Matthew J. (2004). "Sexual behavior, reproductive physiology and sperm competition in male mammals" (PDF). Physiology & Behavior. 83 (2): 361–371. doi:10.1016/s0031-9384(04)00362-2. PMID 15488551.
18. Solanki GS; Zothansiama (2012). "Male homosexual behavior among different age groups in captive stump-tailed macaque (Macaca arctoides): socio-sexual or sexually motivated?". International Multidisciplinary Research Journal. 2 (2): 22–27. ISSN 2231-6302.
19. Erwin J.; Maple T (1976). "Ambisexual behavior with male-male anal penetration in male rhesus monkeys". Archives of Sexual Behavior. 5 (1): 9–14. doi:10.1007/bf01542236. PMID 816329. S2CID 46074855.
20. Werner, Dennis (January 1, 2001). "Chapter 13: The evolution of male homosexuality and its implications for human psychological and cultural variations". In Sommer, Volker; Vasey, Paul (eds.). Homosexual Behaviour in Animals. Cambridge University press. pp. 316–346. ISBN 9780521864466.
21. Gordon, TP; Bernstein, IS (1973). "Seasonal variation in sexual behavior of all-male rhesus troops". American Journal of Physical Anthropology. 38 (2): 221–226. doi:10.1002/ajpa.1330380214. PMID 4632071.
22. Busia, L; Denice, AR; Aureli, F; Schaffner, CM (May 2018). "Homosexual behavior between male spider monkeys (Ateles geoffroyi)" (PDF). Archives of Sexual Behavior. 47 (4): 857–861. doi:10.1007/s10508-018-1177-8. PMID 29536259. S2CID 3855790.
23. Morris, Desmond (January 1, 1970). "The response of animals to a restricted environment". In Morris, Desmond (ed.). Patterns of Reproductive Behavior. McGraw-Hill. pp. 490–511. ISBN 978-0224617956.
24. Fox, Elizabeth A. (2001). "Homosexual Behavior in Wild Sumatran Orangutans (Pongo pygmaeus abelii)". American Journal of Primatology. 55 (3): 177–181. doi:10.1002/ajp.1051. PMID 11746281. S2CID 21561581.
25. Watson, P. F. (1978). Artificial breeding of non-domestic animals: (the proceedings of a symposium held at the Zoological Society of London on 7 and 8 September 1977). Academic Press for the Zoological Society of London. ISBN 978-0-12-613343-1. Retrieved 9 February 2013.
26. Balcombe, Jonathan P. (2011). The Exultant Ark: A Pictorial Tour of Animal Pleasure. University of California Press. pp. 89–. ISBN 978-0-520-26024-5.
27. Schwartz, S (1999). "Use of cyproheptadine to control urine spraying and masturbation in a cat". Journal of the American Veterinary Medical Association. 214 (3): 369–71. PMID 10023399.
28. Journal of the American Veterinary Medical Association. American Veterinary Medical Association. 1931.
29. Müller, Georg Alfred (1897). Diseases of the dog and their treatment. W.H. Hoskins. pp. 183–.
30. Marchinton, R. Larry; Moore, W. Gerald (1971). "Auto-Erotic Behavior in Male White-Tailed Deer". Journal of Mammalogy. 52 (3): 616–617. doi:10.2307/1378600. JSTOR 1378600.
31. Leonard Lee Rue III (2004). The Deer of North America. Globe Pequot Press. ISBN 978-1-59228-465-8. Retrieved 8 September 2013.
32. Leonard Lee Rue, III (2001). The Deer Hunter's Illustrated Dictionary: Full Explanations of More Than 600 Terms and Phrases Used by Deer Hunters Past and Present. Globe Pequot Press. ISBN 978-1-58574-349-0.
33. R. Eric Miller; Murray E. Fowler (31 July 2014). Fowler's Zoo and Wild Animal Medicine. Elsevier Health Sciences. ISBN 978-1-4557-7399-2.
34. Shipley, Clifford F (1999). "Breeding soundness examination of the boar". Journal of Swine Health and Production. 7 (3): 117–120. Archived from the original on 2018-02-16. Retrieved 2018-02-15.
35. A. F. Dixson (26 January 2012). Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Humans. Oxford University Press. ISBN 978-0-19-954464-6.
36. Jean-Baptiste Leca; Michael A. Huffman; Paul L. Vasey (19 January 2012). The Monkeys of Stormy Mountain: 60 Years of Primatological Research on the Japanese Macaques of Arashiyama. Cambridge University Press. ISBN 978-0-521-76185-7. Retrieved 8 September 2013.
37. McDonnell, S. M. "Specific Normal Behaviors of Domestic Horses That Are Misunderstood as Abnormal". Equine Behavior Laboratory, University of Pennsylvania School of Veterinary Medicine. Retrieved 4 June 2010.
38. McDonnell, S.M.; Henry, M.; Bristol, F. (1991). "Spontaneous erection and masturbation in equids" (PDF). J Reprod Fertil Suppl. 44: 664–665.
39. McDonnell, S. M.; A. L., AL (2005). Squires, E. (ed.). "Aversive conditioning of periodic spontaneous erection adversely affects sexual behavior and semen in stallions" (PDF). Animal Reproduction Science. 89 (1–4): 77–92. doi:10.1016/j.anireprosci.2005.06.016. PMID 16112531. Periodic spontaneous erection and penile movements known as masturbation (SEAM) occur normally at approximately 90 min intervals in awake equids. ... The effects of aversive conditioning] are consistent with suppressed sexual arousal and reduced breeding efficiency. Semen volume and total number of sperm per ejaculate were significantly less
40. McDonnell, S. M.; Diehl, N. K.; Garcia, M. C.; Kenney, R. M. (1989). "Gonadotropin Releasing Hormone (GnRH) Affects Precopulatory Behavior in Testosterone-Treated Geldings" (PDF). Physiology & Behavior. 45 (1): 145–148. doi:10.1016/0031-9384(89)90177-7. PMID 2657816. S2CID 18061735.
41. Bagemihl, pp. 71, 209–210
42. Linden, David J. (2011). Pleasure: How Our Brains Make Junk Food, Exercise, Marijuana, Generosity, and Gambling Feel So Good. p. 98. ISBN 978-1-85168-824-1.
43. Bagemihl, B. (1999). Biological Exuberance: Animal Homosexuality and Natural Diversity. St. Martin's Press. pp. 427–30. ISBN 978-1-4668-0927-7.
44. Gregorič, Matjaž; Šuen, Klavdija; Cheng, Ren-Chung; Kralj-Fišer, Simona; Kuntner, Matjaž (2016). "Spider behaviors include oral sexual encounters". Scientific Reports. 6: 25128. Bibcode:2016NatSR...625128G. doi:10.1038/srep25128. ISSN 2045-2322. PMC 4850386. PMID 27126507.
45. Gruber, Karl (6 May 2016). "These male spiders perform oral sex – and lots of it". Washington Post. Every time males engage in sex, they salivate on their mate’s genitals. “In this spider species, the male first hooks his fang to female genitals, and then salivates into them. He repeats this behavior before, between and after copulation, up to 100 times in one mating,” says Matjaž Gregorič of the Slovenian Academy of Sciences and Arts, who led the new study. Gregorič isn’t sure what motivates the behavior, which has only been recorded in two other invertebrates: fruit flies and widow spiders. The practice hasn’t been well-documented in widow spiders, so their bedroom habits don’t make the darwini's proclivity for oral activities any less mysterious.
46. These Bears Are Having Lots Of Oral Sex, And Scientists Think They Know Why (The Huffington Post) By: Grenoble, Ryan.
47. Suzanne Chevalier-Skolnikoff (1976). "Homosexual behavior in a laboratory group of stumptail monkeys (Macaca arctoides): Forms, contexts, and possible social functions". Archives of Sexual Behavior. 5 (6): 511–527. doi:10.1007/BF01541216. PMID 827276. S2CID 59447.
48. Hideshi Ogawa (2006). Wily Monkeys: Social Intelligence of Tibetan Macaques. Kyoto University Press. pp. 4–. ISBN 978-1-920901-97-4.
49. Fox, M. W. (1972). "The Social Significance of Genital Licking in the Wolf, Canis lupus". Journal of Mammalogy. 53 (3): 637–640. doi:10.2307/1379064. JSTOR 1379064.
50. G. R. Pafumi (15 January 2010). Is Our Vision of God Obsolete?. Xlibris Corporation. ISBN 978-1-4500-0396-4.
51. Tan, M.; Jones, G.; Zhu, G.; Ye, J.; Hong, T.; Zhou, S.; Zhang, S.; Zhang, L. (2009). Hosken, David (ed.). "Fellatio by Fruit Bats Prolongs Copulation Time". PLOS ONE. 4 (10): e7595. Bibcode:2009PLoSO...4.7595T. doi:10.1371/journal.pone.0007595. PMC 2762080. PMID 19862320.
52. Waterman, J. M. (2010). Briffa, Mark (ed.). "The Adaptive Function of Masturbation in a Promiscuous African Ground Squirrel". PLOS ONE. 5 (9): e13060. Bibcode:2010PLoSO...513060W. doi:10.1371/journal.pone.0013060. PMC 2946931. PMID 20927404.
53. Tan, Min; Gareth Jones; Guangjian Zhu; Jianping Ye; Tiyu Hong; Shanyi Zhou; Shuyi Zhang; Libiao Zhang (28 October 2009). Hosken, David (ed.). "Fellatio by Fruit Bats Prolongs Copulation Time". PLOS ONE. 4 (10): e7595. Bibcode:2009PLoSO...4.7595T. doi:10.1371/journal.pone.0007595. PMC 2762080. PMID 19862320.
54. Bagemihl
55. Bagemihl, Bruce (1999). Biological Exuberance: Animal Homosexuality and Natural Diversity. St. Martin's Press. p. 673.
56. "Oslo gay animal show draws crowds". BBC News. 19 October 2006. Archived from the original on 29 October 2006. Retrieved 19 October 2006.
57. "1,500 animal species practice homosexuality". News-medical.net. 23 October 2006. Retrieved 19 February 2007.
58. Roselli, C. E.; Larkin, K.; Resko, J. A.; Stellflug, J. N.; Stormshak, F. (2003). "The Volume of a Sexually Dimorphic Nucleus in the Ovine Medial Preoptic Area/Anterior Hypothalamus Varies with Sexual Partner Preference". Endocrinology. 145 (2): 478–483. doi:10.1210/en.2003-1098. PMID 14525915.
59. In Brief: Rams Will Be Rams. washingtonpost.com (4 July 2004). Retrieved on 15 February 2011. Archived 23 September 2018 at the Wayback Machine
60. STANFORD Magazine: May/June 2004 > Feature Story > On the Originality of Species Archived 2012-02-12 at the Wayback Machine. Stanfordalumni.org (2 July 2003). Retrieved on 15 February 2011.
61. "Central Park Zoo's gay penguins ignite debate" by Dinitia Smith, San Francisco Chronicle, 7 February 2004
62. Riccucci, Marco (2011). "Same-sex sexual behaviour in bats". Hystrix It. J. Mammal. (N.s.). 22 (1): 139–147. doi:10.4404/hystrix-22.1-4478.
63. Parker, Karen; Lee, Theresa (2003). "Female Meadow Voles (Microtus pennsylvanicus) Demonstrate Same-Sex Partner Preferences". Journal of Comparative Psychology. 117, No.3: 283–289 – via PubMed.
64. Young, Lindsay; Zaun, Brenda; VanderWerf, Eric (27 May 2008). "Successful same-sex pairing in Laysan albatross". Biology Letters. 4: 323–325 – via PubMed.
65. de Waal FB (1995). "Bonobo sex and society". Sci. Am. 272 (3): 82–8. Bibcode:1995SciAm.272c..82W. doi:10.1038/scientificamerican0395-82. PMID 7871411. Perhaps the bonobo's most typical sexual pattern, undocumented in any other primate, is genito-genital rubbing (or GG rubbing) between adult females. One female facing another clings with arms and legs to a partner that, standing on both hands and feet, lifts her off the ground
66. Paoli, T.; Palagi, E.; Tacconi, G.; Tarli, S. B. (2006). "Perineal swelling, intermenstrual cycle, and female sexual behavior in bonobos (Pan paniscus)". American Journal of Primatology. 68 (4): 333–347. doi:10.1002/ajp.20228. PMID 16534808. S2CID 25823290.
67. Kirkpatrick, RC; Lévi-Strauss, C (2000). "The Evolution of Human Homosexual Behavior" (PDF). Current Anthropology. 41 (3): 385–413. doi:10.1086/300145. PMID 10768881. Archived from the original (PDF) on 2015-05-13.
68. ANNA-MARIE A. R. EDWARDS (1991). "Homosexual Behaviour in Wild White-handed Gibbons (Hylobates lar)". Primates. 32 (3): 231–236. doi:10.1007/BF02381180. S2CID 26662075.
69. DelBarco‐Trillo, J., Gulewicz, K., Segal, A., McPhee, M. E., & Johnston, R. E. (2009). "Can captivity lead to inter‐species mating in two Mesocricetus hamster species?". Journal of Zoology. 278 (4): 308–312. doi:10.1111/j.1469-7998.2009.00577.x.CS1 maint: multiple names: authors list (link)
70. Miletski, Hani (2002). Understanding Bestiality and Zoophilia. Bethesda, Maryland: East-West Publishing. p. 51.
71. Gröning, J., & Hochkirch, A. (2008). "Reproductive interference between animal species" (PDF). The Quarterly Review of Biology. 83 (3): 257–282. CiteSeerX 10.1.1.522.2234. doi:10.1086/590510. PMID 18792662. Archived from the original (PDF) on 2015-02-23. Retrieved 2015-02-23.CS1 maint: multiple names: authors list (link)
72. Kinsey, Alfred (1953). Sexual Behavior in the Human Female. W.B. Saunders Company. p. 503.
73. Harris, Heather S.; et al. (2010). "Lesions and behavior associated with forced copulation of juvenile Pacific harbor seals (Phoca vitulina richardsi) by southern sea otters (Enhydra lutris nereis)". Aquatic Mammals. 36 (4): 331–341. doi:10.1578/am.36.4.2010.331.
74. Mulvaney, Kieran (11 March 2011). "The Other Side of Otters". Discovery News.
75. Alford, Justine (17 November 2014). "Seals Caught Having Sex With Penguins". IFLScience.
76. Miller, Edward H., Alberto Ponce de León, and Robert L. Delong. "Violent interspecific sexual behavior by male sea lions (Otariidae): evolutionary and phylogenetic implications." Marine mammal science 12.3 (1996): 468-476.
77. Pelé, Marie; Bonnefoy, Alexandre; Shimada, Masaki; Sueur, Cédric (10 January 2017). "Interspecies sexual behaviour between a male Japanese macaque and female sika deer". Primates. 58 (2): 275–278. doi:10.1007/s10329-016-0593-4. PMID 28074343. S2CID 10630464.
78. Doncarlos, Michael W., Petersen, Jay S., Tilson, Ronald L.; Petersen; Tilson (1986). "Captive biology of an asocial mustelid; Mustela erminea". Zoo Biology. 5 (4): 363–370. doi:10.1002/zoo.1430050407.CS1 maint: multiple names: authors list (link)
79. Jeffrey Moussaieff Masson (21 October 2009). When Elephants Weep: The Emotional Lives of Animals. Random House Publishing Group. ISBN 978-0-307-57420-6. Retrieved 28 May 2013.
80. Kruuk, H. (1972) The Spotted Hyena, University of Chicago Press, ISBN 0-226-45508-4, p. 232
81. https://www.theguardian.com/world/2012/jun/09/sex-depravity-penguins-scott-antarctic
82. Bloom, Richard W. & Dess, Nancy Kimberly (2003). Evolutionary psychology and violence: a primer for policymakers and public policy advocates. Greenwood Publishing Group. pp. 87–. ISBN 978-0-275-97467-1.
83. Dawkins, Richard (2004). "Chimpanzees". The Ancestor's Tale. Houghton Mifflin. ISBN 978-1-155-16265-2.
84. Sommer, Volker & Vasey, Paul L. (2006). Homosexual behaviour in animals: an evolutionary perspective. Cambridge University Press. pp. 290–. ISBN 978-0-521-86446-6.
85. Sazima, I. (2015). "Corpse bride irresistible: a dead female tegu lizard (Salvator merianae) courted by males for two days at an urban park in South-eastern Brazil". Herpetology Notes. 8: 15–18.
86. Moeliker, C.W. (2001). "The first case of homosexual necrophilia in the mallard Anas platyrhynchos (Aves: Anatidae)". Deinsea. 8: 243–247. ISSN 0923-9308. Archived from the original (PDF) on 2011-07-24.
87. MacLeod, Donald (8 March 2005). "Necrophilia among ducks ruffles research feathers". The Guardian. London. Archived from the original on 10 April 2006. Retrieved 5 April 2006.