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Males employ an anoxic kiss to reduce female struggle and increase compliance

The dam that forms Varsity Lake on the University of Colorado campus is solid, but nevertheless riddled with crevices that provide safe havens for western terrestrial garter snakes, Thamnophis elegans. Eager to witness the various fulminations of spring, I checked the walls on warm days in April to see the first crops of the snakes basking in the sun. On April 15, five snakes were basking at the top of the wall, but more snakes were below the dam, in the woods. I resolved to return the next day with a camera.

As a female emerges from the hibernaculum in spring, she is mobbed by eager males that form a mating ball. Photo by Jeff Mitton.

The next morning, a pair was mating beside the wall at the top of the dam, but they were partially hidden by dandelion foliage and flowers. However, the real action was happening beneath the dam in the woods, where a roiling, seething, slithering mass of snakes had formed a mating ball. This tangle was in constant motion, as the males wrestled and maneuvered to get into the mating position. The contest lasted 40 minutes before the snakes suddenly relaxed and dispersed.

Garter snakes spend the winter in brumation, the analog of mammalian hibernation for cold-blooded snakes, in communal hibernacula in rocks or below ground. In spring, males leave the hibernaculum first, for it takes them days to become active and coordinated in preparation for mating. About two weeks later, when a female emerges, emitting her sex pheromone, they rush to her to mate. But if several to many males converge on a single female, a mating ball is formed by the athletic competition to push other males aside and to maneuver into the appropriate position to mate.

In the accompanying photograph, the female’s head is at the lower-right side of the photo, larger and paler than the others. The six smaller heads are in the photo are all males. Two males have their heads appressed to her, just behind her head, and three other males are on their way, with a goal to get into the proper position.

In addition to the physical struggle, males may also employ an anoxic kiss to reduce her struggling and increase compliance. The kiss is an exhalation of deoxygenated air that deprives her of the oxygen she needs to keep struggling and in extreme cases can result in death.

Both males and females have a cloaca, or slit at the end of the abdomen and beginning of the tail that serves as an exit for intestinal and urinary functions and both entrance and exit for genital functions. A male everts his hemipenis, a structure that is two penises joined at the base, each adorned with tiny barbs and one major barb that is inserted into the female’s cloaca to serve as an anchor to assist penetration. Once penetration is achieved, the male releases sperm and then attempts to insert a mating plug, a gelatinous secretion that essentially glues the sides of her tract together. The glue only lasts a few days, but it will prevent competing males from adding their sperm. If, however, he is displaced before placing the mating plug, another male will add his sperm.

Once the female has mated, she stops emitting her pheromone and within minutes the males disperse.

What are the paternal consequences of the mating ball — one father, several, or many? The female holds fertilized eggs and after the young are developed she releases her live born, which are completely independent offspring. Brood sizes in garter snakes vary from three to around 80, and geneticists have analyzed genotypes of six western garter snake mothers and their broods. Three broods had a single father, two broods had two fathers and one brood had three fathers. For broods with multiple fathers, interpretation is complicated by the fact that garter snakes can store sperm. So a brood with two fathers may have been produced in a single mating ball, or a mixture of stored sperm and sperm received in a mating ball in the present year.

Although this mating ball contained only seven snakes, the constant squirming of entwined snakes was mesmerizing. Nevertheless, the visual impact of a truly large mating ball would be much greater. Narcisse Snake Dens, a wildlife area north of Winnipeg, Manitoba, has the greatest concentration of snakes in the world. A recent census estimated that the hibernacula in limestone caves contain 70,000 red-sided garter snakes, Thamnophis sirtalis. Imagine the mayhem of a female emerging from the hibernaculum to an area where hundreds or thousands of males wait.