Above: A puma pausing in the wildlands of California (Photo courtesy of Jason Klassi/ExpeditionEarth.org)
Apex carnivores are well known for their effects on ecosystems, which include keeping prey populations balanced and limiting the spread of disease. Another important effect apex carnivores have is structuring their ecological communities. For example both prey and smaller carnivores avoid areas and habitats that are frequently used by apex carnivores, which directly affects their abundance and how they are spatially distributed. A major focus of my research is the scent communication of pumas and other felids, and over the past many years I have been curious about the effects that the scent of apex carnivores has on other species. Is it possible that apex carnivores also structure ecological communities through scent? Many carnivores use scent marks to advertise their territoriality for competitors and mates, and other species should easily be able to keep tabs on one another through the scent marks they leave behind.
A puma scent marking through scraping, their most frequent form of indirect communication (Video by Max Allen)
Pumas primarily use a form of scent marking called scraping, where they scrape in the ground with their hind feet and then leave scent on the mound of material they have created. Over the last five years I documented puma scent marking with motion-triggered video cameras, and I noticed something curious: gray foxes would arrive in the days following a puma visit, and rub their cheeks on the scrape the puma created. The first few times I saw the behavior I assumed it was just a strange behavior, but eventually I observed the behavior nearly 100 times, and there seemed to be a pattern: the fox would arrive within a few days of the puma and would always first investigate the scrape, then rub their cheek, before often urinating on top of it.
A video sequence where a puma exhibits scraping behavior, then a gray fox rubs its cheeks on the scrape (Video by Max Allen)
Because there was such a strong pattern I decided there must be a reason behind the behavior, and this piqued my curiosity about why the behavior was used. Considering the series of behaviors I observed, the first question I decided to test was whether gray foxes were attempting to deposit their scent or accumulate puma scent? To test this question I compared the objects that gray foxes rubbed their cheeks on to see if foxes were selecting for puma scrapes. If they were selecting for puma scrapes specifically, I hypothesized that at least half of the objects they rubbed their cheeks on would be puma scrapes, while if gray foxes rubbed their cheeks on more a diverse suite of objects then I reasoned that the foxes would not be selecting for puma scrapes. In running statistical analyses I found clear evidence that the gray foxes were selecting puma scrapes for cheek rubbing. 85% of the objects foxes rubbed their cheeks on were puma scrapes, with other objects being the ground (13%), a bobcat individual scrape (1%), and a shrub (1%). Since my evidence suggested that gray foxes appeared to be accumulating puma scent, my next step was to figure out why.
After much consideration, I came up with two possible explanations: mate attraction and predation avoidance, and I then set out to test these two competing hypotheses. I reasoned that if gray foxes were using puma scent for mate attraction, there should an increase in cheek rubbing on puma scrapes during the breeding season, and the exhibition of rubbing their cheek should be correlated with recent visitation by other foxes. After testing these hypotheses, I found no support for this hypothesis. Cheek rubbing did not vary among seasons, and it was negatively related to how recently a gray fox had visited (meaning foxes were more likely to rub their cheek the longer it had been since another visit by a fox, especially if it had been over two weeks since the last visit). Considering both of these findings, mate attraction does not appear to be the reason that gray foxes use cheek rubbing.
My other potential hypothesis was that gray foxes used cheek rubbing for predation avoidance. Gray foxes are small carnivores, and must avoid predators who want to exclude them from areas they use or in some cases kill them. Smaller carnivores have been shown to increase caution and alter their feeding behavior when exposed to the scent of larger carnivores, and coyotes and bobcats may exhibit caution when exposed to puma scent. In these situations gray foxes may be able to deter intraguild predation by applying puma scent to themselves, potentially causing a bobcat or coyote to hesitate in an attack and allowing the gray fox to escape. This may be a particular advantage for gray foxes as their main predation avoidance technique is tree climbing, and hesitation by a larger predator may give the gray fox time to escape into a tree.
Testing whether cheek rubbing behavior of gray foxes is for predation avoidance is more difficult, as we could not directly test the success of such a tactic. Therefore, we instead tested among possible explanations for the relative abundance (RA) of the four carnivores (fox, bobcat, coyote, puma) at community scrapes, in order to assess whether or not puma scent dissuaded bobcats and coyotes from using these areas. I tested three competing hypotheses: 1) if based on trophic abundance, there would be few pumas, some coyotes and bobcats, and many gray foxes; 2) if based on apex carnivore suppression, there would be many pumas, and few coyotes, bobcats, or gray foxes; 3) if based on mesocarnivores release, there would be many pumas, few coyotes and bobcats, and many gray foxes.
Another video sequence of a gray fox rubbing their cheek on a puma scrape (Video by Max Allen)
In testing for predation avoidance, we recorded 1,188 visits by pumas (RA = 19.97), 22 visits by coyotes (RA = 0.48), 446 visits by bobcats (RA = 9.51), and 903 visits by gray foxes (RA = 18.19). There was a clear difference in the relative abundance of the four species, with both coyotes and bobcats less abundant than pumas. Coyotes were also substantially less abundant than gray foxes, while bobcats were less so, and gray foxes and pumas were similar in abundance. This best supports my mesocarnivores release hypothesis, suggesting a cascading pattern in the abundance of carnivores at community scrapes. In this case, pumas suppress coyotes and bobcats, which releases gray foxes from suppression and increases their abundance. This best supports our predation avoidance hypothesis as the potential reason for cheek rubbing.
In summary, the evidence from our study suggests that cheek rubbing was apparently not used to advertise for mates, as the exhibition of cheek rubbing was not correlated seasonally with their breeding season or with how recently a gray fox had visited the site. Instead, the accumulation of puma scent may be used to deter predation, as there was a cascading pattern in the occurrence of pumas, coyotes (Canis latrans) and gray foxes at community scrapes. Gray foxes cheek rubbing on puma individual scrapes appears to be part of a complex behavioral cascade where a small carnivore acquires scent from a large carnivore to potentially dissuade competition and predation from dominant mesopredators. This behavior is likely to be most beneficial against larger predators that are smell-dominant, such as coyotes, and we found that gray foxes visited community scrapes 38 times more frequently than coyotes, suggesting that coyotes avoid community scrapes and puma scent, while gray foxes do not.
This is the first published study of a subordinate species using the scent of a dominant species to communicate with other species, and the observed behavioral cascade suggests that scent marking could also be a mechanism that impacts the distribution and abundance of species. The mechanisms and importance of scent marking for interspecific interactions are currently under represented in the literature. Scent marking is an integral part of the behavioral ecology of many mammals, but we have little functional knowledge of how interspecific interactions may occur via scent marking. The significance of our findings suggest that interspecific scent marking is a potentially rich area of research and an area in need of further research.
This study explores just one example of interspecific communication, and is just the beginning to understanding and interpreting these behaviors. More details on the entire study are available here. Keep up to date with my research as I explore these and other questions. Many thanks to my collaborators on this project: Chris Wilmers and Micaela Gunther; as well as Paul Houghtaling, Yasaman Shakeri, Anna Nisi, and the many field technicians and volunteers who contributed to the project.