Garter Snake Mating Ball

Come spring-time, these piles of snakes emerge from their den. Males are ready to mate after their second hibernation, while females mate after three years. The males swarm when the females awaken, beginning the mating ball. In these balls, dozens of males compete amongst themselves to woo one female. During these few weeks after waking, males will not eat nor display acts of aggression. They are solely focused on courting and mating. In this odd mix of pseudo-polyandry (while up to hundreds of males court one female, the first few males to successfully copulate often prevents subsequent copulations from competitors via a mating plug (Shine et al 2003), and the females’ pheromone titrates plummet (Uhrig et al 2012)), both species have developed a host of strategies, not only to increase their reproductive fitness, but also just to survive this violent onslaught.

Image of Mating Ball

There's a female in there, somewhere.

She-Males

Some males adopt a strategy of trickery, confusing their competition by posing as a female snake through secretion of female scents. While this is a well-known occurrence (Shine and Philips 2001), there is debate as to what advantage she-males garner over male-males. One long-standing hypothesis held that she-males posed as females to deceive their male-male competition (Crews 1985). Males tend to wake from hibernation before the females, giving them time to prepare their bodies before swarming the drowsy females. This hypothesis states that the she-males take advantage of this by luring the early rising males away from the den. After drawing the male-males away from the den, the she-male stops secreting his feminine scent, and darts back to the untended females. However, a few more recent studies have proposed an alternative reason for the existence of she-males. Again, upon arising from hibernation, the snakes need time to restart their bodies’ mechanisms. This is a difficult process for the snakes, as they don’t produce their own heat and the hibernaculums are often in well protected, shaded areas. This second hypothesis would have she-males attracting the male-males to initiate a warming cuddle puddle. A snake playing the role of the female in a mating ball is much more covered, allowing greater protection from predators and the chance to steal heat from other males. Rather than conferring a direct sexual advantage, then, female mimicry might have developed more to increase individual fitness.

Doing away with trickery

Upon emerging from the den, females slither away from the imminent crushing piles of males, seemingly reluctant to be courted. There are a few advantages gained by moving away from the den: small females avoid being crushed (Shine and LeMaster 2001), the females are more well distributed when they give birth, and retention of stored sperm (a female can store the sperm from multiple males in her spermatheca, and research suggests that she may actually have a mechanism for choosing the healthiest ejaculate). One study looked at whether this reluctance might actually be a kind of sexual selection—allowing time for the males to compete against each other for the chance to copulate—or whether the females were actually just attempting to avoid the males all together. Shine et al’s study (2003) suggested the latter, that females were attempting to avoid harassment. Examples of this harassment include giant males overpowering females or the anoxic kiss (puffs of deoxygenated air) delivered by males known to induce an oxygen deprived intoxication and sometimes death. Shine and Mason (2005) looked at this question from the males’ perspective, asking whether larger males tended to be more successful due to male/male competition or male/female coercion. Again, their study suggests the latter.

Costly Mating

Since a male can copulate many times, it is to their reproductive advantage to stick around the den for as long as possible, searching for unmated females. However, more time spent at the den means less time feeding. Thus, only the largest males, those that accumulated the most resources from the previous year, can afford to wait for extra copulations (Gregory 2011). During this time, females must expend massive amounts of energy, and expose themselves to greater levels of predation, by the induced pregnancy. It would be advantageous for females to grow their young quickly are able to return to feeding sooner. Indeed, it has been shown that the larger females give birth quicker, furthering a causal loop whereby they are then allowed more time to feed (Gregory 2006).

Evidence for Behavioral Plasticity

Interestingly, it has been shown that, dissociated from potential chemical cues, simply having acquired more courting males makes a female more attractive; simply having more suitors directly increases attractiveness (Joy and Crews 1985). Yet, as more males enter into a mating ball, the males demonstrate a degree of behavioral plasticity. Vigorously competing against dozens of males during courtship would be costly. Instead, the males make greater attempts to increase female receptivity (Shine and Langklide 2003). Research around this finding also noted that smaller males invested more in similarly increasing female receptivity, leaving the more vigorous courting displays to the heaviest males.