Smells like Mean Sprit

This post is written by BEACON’s own managing director Danielle Whittaker about her work that has been accepted pending minor revisions in a special issue of Journal of Comparative Physiology A. 

Dueling Juncos ~ Junco picture from Cortes Island Canada. Photo courtesy of Island Light Photography

Fighting is risky – at best, it uses up energy and time, and at worst, it results in injury and death. But the potential rewards can be major, like food, territory, maybe even a chance to mate with another female. How does an animal decide when to take that risk, and when to skip it? The answer may be found in their opponent’s smell.

Fighting ability and aggressive behavior are often linked to testosterone. In most animal species, males usually have higher levels of testosterone than females, though there is variation in both sexes. Testosterone alone doesn’t explain variation in behavior and other linked traits, however. Hormones like testosterone function as signaling molecules that tell receiving tissues to turn certain functions on or off, like building muscle or changing levels of stress hormones. Androgen receptors in the tissues receive that message, and the strength of the tissue’s response to the message depends on how many receptors it has. For example, Dr. Kim Rosvall and colleagues at Indiana University found that the density of androgen receptors in the brains of dark-eyed juncos, a common songbird, was related to aggressive behavior in response to an intruder.

Is there any way that birds can get information about their potential rivals’ hormones and hormone receptors, in order to predict their behavior and decide whether or not to attack? A likely mechanism is odor. For nearly a decade, I’ve been studying how dark-eyed juncos and other birds use odor from preen oil, secreted from the uropygial gland and spread on the feathers during preening, to assess and choose mates (see past blog posts here and here). I teamed up with Kim Rosvall to study the links between odor, aggression, testosterone, and uropygial gland androgen receptors of these same birds.

Danielle Whittaker picking up chicks. (Note: these are not juncos.)

At Mountain Lake Biological Station in Virginia, we located breeding juncos on their territories. Each subject was either a female incubating eggs, or a male mated to a female who was incubating. Incubation is a time when the birds are likely to aggressively defend their territories, to ensure they are able to care for the nestlings when they hatch. We presented each bird with a junco in a cage (we call this a “simulated territorial intrusion”). The bird typically responds with aggressive behavior, like swooping over or dive-bombing the cage (“flyovers”) or, if it’s a male, singing at the intruder. Spending time close to the cage is also considered aggressive. We measured all of these behaviors and then captured the bird to take samples. We measured the testosterone levels in their blood, the volatile compounds in their preen oil, and the levels of gene expression of androgen receptors in their uropygial glands.

The odor of a bird predicted how aggressively that bird would behave towards an intruder. These odors are complex, with 15 or more individual components, like a perfume. Different components correlated with different aggressive behaviors, such that different aspects of an individual’s odor related to how many songs they sang towards the intruder (in males), how much time they spent near the intruder’s cage (in females), and how many times they swooped over the cage (in both sexes). This level of detail suggests that an astute rival could detect not only how aggressive their opponent may be, but also what type of response they would be likely to face.

Gas chromatography-mass spectrometry chromatogram of junco preen oil, showing volatile compound peaks. By Helena Soini, modified from Whittaker et al 2013

Next we looked at whether this relationship was due to testosterone and androgen receptors affecting that odor. We found that in males only, both circulating testosterone and uropygial gland androgen receptors interacted to predict that male’s odor. This relationship was not found in females, which suggests that maybe a different hormone is responsible for communicating a female’s likelihood of attack.

This study shows us that individual odor in birds contains a wealth of information for potential rivals as well as potential mates. The links between hormones, behavior, and smell suggests that this signal is “honest” and can’t be bluffed. For many years, people believed that birds had little to no sense of smell (and some still do), but more and more studies are debunking this idea. Similarly, humans are believed to have a poor sense of smell compared to other mammals… but I often wonder just how much of our judgments of each other, and the decisions we make as a result, are based on smell, without us even knowing it.



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