Snakes Deceive to Get a Little Snuggle

A lone red-sided garter snake.
Photo by Tracy Langkilde.

The red-sided garter snake is a small snake species with the largest and most northern distribution of all reptiles in North America. These northern ranges can get quite cold for any animal, let alone a reptile. Like most reptiles, they are ectotherms, meaning they regulate their body temperature largely by exchanging heat with their environment. If an animal gets almost all of its body heat from a cold environment, its body is also going to be cold… So what is a poor red-sided garter snake to do?

Red-sided garter snakes that live in the northern end of their range in Manitoba, Canada spend their cold-season (6-8 months of it) hibernating in underground dens called hibernacula. Tens of thousands of snakes may share a winter den and every spring, they emerge to mate and eat and do all the other fun things that snakes do when they’re awake. (If you would like to witness the spectacular sight that is the emergence of the garter snakes, it is occurring this month in the world-famous snake-watching Interlake region of Manitoba).

A whole lotta red-sided garter snakes in a spring-mating
frenzy. Photo by Tracy Langkilde.

When a snake first emerges from its groggy hibernation state its body is cold and movements are sluggish, which puts it at a high risk of predation from animals like crows and weasels. Females are generally at less risk of predation at this time because emergence-time is also sexy-time for this species and females generally find themselves in the middle of a writhing ball of already-warmed-up male suitors (appropriately called a mating ball). For the female, this both increases her body temperature faster (which will allow her to move faster sooner) and provides any would-be predators with many other snakes to choose from.

Female red-sided garter snakes produce a male-attracting pheromone (a chemical released by an animal that affects the physiology and/or behavior of other individuals of the same species). Researchers Rocky Parker and Robert Mason at Oregon State University found that the amount of pheromone females produce increases as the females hibernate from fall to spring. This pheromone is a blend of saturated and unsaturated methyl ketones (molecules responsible for many natural odors and flavors) and males are more strongly attracted to the unsaturated components. The chemical composition of the female pheromone also changes from fall to spring, such that female spring pheromones are dominated by these highly attractive unsaturated pheromone components. Presumably, the sexier the pheromone, the more suitors are attracted and the more benefits a recently-emerged female can acquire.

It seems that this smell-sexy-and-create-mating-ball strategy is a useful solution for recently-emerged females, but what about recently-emerged males? Parker and Mason collected courting male red-sided garter snakes and brought them into the lab. Then they either implanted them with estrogen (a sex hormone strongly involved in female sexual physiology and behavior) or did not (as a control group). Males with estrogen implants produced more pheromones, had higher ratios of unsaturated pheromone components to saturated pheromone components, and were more attractive to courting males. When the researchers removed the estrogen implants from some of the males, they became less attractive again. So in the lab, estrogen treatment of males makes them produce more female-like pheromones that other courting males respond to. This shows that males are capable of using this smell-sexy-and-create-mating-ball strategy, but do they use it in nature?

This graph shows the amount of courtship
received by females, "she-males", and "he-males"
when either cold or hot. Figure from Shine,
Langkilde and Mason's Behavioral Ecology
and Sociobiology Paper (2012).

Robert Mason at Oregon State University and Rick Shine and Tracy Langkilde at the University of Sydney, Australia collaborated to explore this relationship between temperature and male production of female-like pheromones. It turns out, male red-sided garter snakes in nature can and do produce female-like pheromones when they emerge from their den. Shine, Langkilde and Mason collected some of these males that were being courted by other males (the researchers refer to them as “she-males”). They also collected some males that were courting females (they called them “he-males”) and some females. They then exposed the snakes to different temperatures for 15-minute intervals and tested their attractiveness to other courting males. 

This graph shows the amount of courtship received
by "she-males" when cooled (open circles) and
heated (filled circles) for 15-minute intervals.
Figure from Shine, Langkilde and Mason's Behavioral
Ecology and Sociobiology Paper (2012).

 The researchers found that females were courted the most, “he-males” the least, and “she-males” were courted an intermediate amount. Interestingly, “she-males” only attracted courtship when they were cold (and their chances of survival could be improved by a mating ball) and their attractiveness shifted with every 15-minute shift in temperatures. How did they do this? 15 minutes is probably not enough time for a hormonal change to alter the pheromone composition enough to change attractiveness so drastically.

An important clue comes from the composition of the pheromones themselves. Remember that red-sided garter snake pheromones are a blend of saturated and unsaturated methyl ketones and males are more strongly attracted to pheromones that have a high ratio of unsaturated components to saturated components. Well, saturated and unsaturated fats respond differently to cold: Unsaturated fats (like cooking oil) remain a liquid at cooler temperatures, whereas saturated fats (like margarine) become solid. Solids are less volatile than liquids, which makes them not smell as much. Shine, Langkilde and Mason hypothesize that the ratio of unsaturated to saturated ketones is lower in “she-males” than in females. In the cold, the high amount of saturated components of the “she-male” pheromone is turned off, which raises the ratio of unsaturated to saturated ketones, making them attractive. As the snake warms up, the saturated components of the “she-male” pheromone is turned on, which lowers the ratio of unsaturated to saturated ketones, making them unattractive.

Remarkably, male red-sided garter snakes can change their pheromones to mimic or not mimic females in response to brief changes in temperature. How cool is that?

Want to know more? Check these out:

1. Shine, R., Langkilde, T., & Mason, R. (2012). Facultative pheromonal mimicry in snakes: “she-males” attract courtship only when it is useful Behavioral Ecology and Sociobiology, 66 (5), 691-695 DOI: 10.1007/s00265-012-1317-4

2. Parker, M., & Mason, R. (2012). How to make a sexy snake: estrogen activation of female sex pheromone in male red-sided garter snakes Journal of Experimental Biology, 215 (5), 723-730 DOI: 10.1242/jeb.064923

3. Parker, M., & Mason, R. (2009). Low Temperature Dormancy Affects the Quantity and Quality of the Female Sexual Attractiveness Pheromone in Red-sided Garter Snakes Journal of Chemical Ecology, 35 (10), 1234-1241 DOI: 10.1007/s10886-009-9699-0

4. For an awesome blog about social snakes from a researcher’s perspective, go to http://blog.socialsnakes.org/ (or http://www.public.asu.edu/~mamarell/ for more information)