Serpentine Cross-Dressers

Natural History, Feb, 2001 by Richard Shine, Robert Mason

Some male Manitoban garter snakes wear the alluring scent of females.

Garter snakes may be the most common snakes in North America, but the subspecies known as the red-sided garter snake provides an uncommon annual spectacle. During the severe, six- to eight-month winters in Manitoba, Canada, these small, nonvenomous snakes sequester themselves in deep crevices to avoid freezing. Since such sites are rare in the barren, rocky region between Lake Manitoba and Lake Winnipeg, snakes that have dispersed across many miles in the summer gather by the thousands to spend the winter at the few suitable spots. Some of their major dens are located about seventy-five miles north of the city of Winnipeg and are surrounded by swampland that during the warmer months provides an abundance of frogs, the snake's favorite prey. When dens near swampland empty out in early spring, some of them disgorge more than 10,000 snakes from rocky depressions as small as sixteen feet long and six feet wide.

Over the past fifteen years, one of us (Bob Mason) has been visiting these dens in an attempt to understand the snakes' behavior. Males and females mass together in the same dens, emerging from hibernation between late April and the end of May. (In dens that receive more sunlight, the exodus can take place somewhat earlier.) Males emerge first. Having reached the surface, they stay close to the den for the better part of May. It's now mating season, and they're waiting to intercept the tardy females. As soon as a female appears, a seething ball of dozens (often hundreds) of amorous suitors forms around her. This rippling clot of snakes may move en masse over rocks and vegetation until the female has mated. Some "mating balls" however, contain no females. In 1985 Bob Mason, working with David Crews, of the University of Texas, reported that frenetic males frequently attempt to mate with certain other males that they evidently mistake for females. These "she-males," they observed, are indistinguishable in size and markings from ordinary males, and they also seek female mates--yet they attract other males by the score.

Female mimicry by males, although not common, occurs throughout the animal world. Among some anole lizards, for instance, males that are too small to defend a territory of their own may manage to live within a dominant male's territory if they can avoid conflicts by passing as females. Common sunfish produce two kinds of males--a large? dominant male that builds and defends a nest and tries to attract females to it, and a smaller male that resembles, and behaves like, a female. This female mimic swims between a mating pair just as the dominant male is about to fertilize the female's eggs and fertilizes some of them himself.

Manitoba's red-sided garter snakes, however, are the only snakes known to have males that mimic females. How does an amorous male garter snake tell a male from a female in the horde of snakes emerging in early spring from a large den? By sensing the pheromones that emanate from the animals' skin. When snakes flick their tongues in and out, they pick up chemical cues from the air, which they transfer to a sensory organ in the roof of the mouth. When a male tongue-flicks another snake, he instantly determines his neighbor's apparent gender by the scent of the lipids on its skin. Bob and David discovered the pheromone differences during their first year of collaboration, and a few years later they were able to synthesize the signaling chemical in the lab.

Why do some males smell like females? At first the researchers hypothesized that a male's release of female chemicals might benefit him by confusing his rivals: the she-male would be the only male snake within a mating ball that knows who the real females are. At this stage of the game, Bob and David also thought that individual snakes remained either she-males or he-males throughout an entire mating season, if not an entire lifetime. There the story remained until Rick Shine came from Australia in 1997 to visit Bob at the garter snake dens. Rick became so intrigued with the abundance of female mimics he saw there that he returned the following year with two research assistants from the University of Sydney, specifically to study the she-males, and our collaborative attack on this puzzle got under way.

First we attempted to quantify the attractiveness of individual snakes. Holding various "target" snakes by the tail, we crouched in the grass near a den and placed them in front of mate-searching males. We then recorded the mate-searchers' level of interest. Responses ranged from ignoring the target or rapidly flicking the tongue to aligning the body with that of the presented snake and trying to mate. With this simple method, we were able to confirm that she-males (which we had extracted from the center of mating balls) were indeed very attractive to ordinary males, though a bit less so than real females. Indeed, the she-males proved to be attractive to one another and sometimes even to themselves. (If a she-male accidentally encountered part of his own body, he might spend quite a bit of time busily courting himself!)