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Monday, August 27, 2012

Squirrel v. rattlesnake

This article is part of a series highlighting new research in snake biology presented by herpetologists at the World Congress of Herpetology VII in Vancouver, British Columbia. If you want to learn more about the WCH, check out the June 2012 issue of Herpetological Review, or follow the Twitter hashtag #wch2012, with which I will tag all posts in this series.

It might seem like a lopsided contest, but in the majority of interactions between Northern Pacific Rattlesnakes (Crotalus oreganus) and California ground squirrels (Spermophilus beecheyi), the squirrels walk away with their lives. This surprising result come from Rulon Clark, who in his talk during the venomous snake evolution session of the WCH7 last week filled us in on the latest work from his behavioral ecology lab at San Diego State University. Building on the work done by mammalogists Richard Coss and Don Owings at UC Davis, the Clark lab studies what ground squirrels are trying to say to their rattlesnake predators. You see, when a ground squirrel encounters a rattlesnake, it performs a behavior known as 'tail-flagging'. You can see an example of this behavior in the first half of this video:

and the potential consequence of not exhibiting it in the second half! It's been apparent for almost 35 years now that tail-flagging adult squirrels are safer from rattlesnakes than squirrels that don't perform this behavior, but why?

Dr. Clark enumerated several hypotheses that his lab has tested and falsified:
  • tail-flagging does not appear to be a form of quality advertisement, like stotting in ungulates, because its use is not correlated with the health or vigor of the squirrel
  • tail-flagging does not appear to result in predator confusion or misdirection, because the rattlesnakes that strike at tail-flagging squirrels are equally accurate in their strike direction as those that strike at squirrels that aren't tail-flagging
  • tail-flagging does not appear to be a form of harassment, like mobbing in birds & other animals, because the squirrels never attack rattlesnakes if the snakes are free-ranging (although they will if the snakes are caged, as they were in early experiments) and eventually leave the snakes alone after tail-flagging at them for a while.
Additionally, the tail-flag display is frequently given in the absence of a rattlesnake, as if to probe for potential predators nearby. So how is tail-flagging helpful? By videotaping countless hours of snake-squirrel interactions using stationary cameras - fortunately, rattlesnakes are fairly stationary themselves - Clark's group thinks they have the answer.

Crotalus oreganus from Utah
First, the squirrels are probably advertising their perception of the snakes, both to the snakes themselves and to each other. This is likely because tail-flagging by one squirrel increases the vigilance of other squirrels in the area. Furthermore, rattlesnakes that have been tail-flagged are actually more likely to abandon their ambush sites. Both these things only happen, however, when the tail-flagging squirrel is an adult. Similarly, we respond more seriously to cries of a fire by an adult than by a child. Juvenile squirrels also tail-flag, but presumably they are just practicing, so adults apparently do not take them seriously.

Second, the adult squirrels are probably also advertising their vigilance to the snakes. This is likely for two reasons: 1) the snakes are less likely to strike an adult tail-flagging squirrel than a non-tail-flagging one, and 2) if they do, squirrels that tail-flagged are more likely to successfully dodge the rattlesnake's strike. That's right - these ground squirrels can actually evade the snake's strikes. Don't believe it?

I hardly can either, but wow, that squirrel pulled a 180 and totally avoided what should have been a lethal strike. Although the squirrel in that video wasn't tail-flagging, Clark's group has shown that within about one foot of a rattlesnake, tail-flagging squirrels are more likely to dodge strikes successfully. As a result, rattlesnakes are less likely to strike at a tail-flagging squirrel - not because the energy cost is too high, but because a strike will surely cause the squirrel to run off, while waiting might result in the squirrel making a mistake by getting too close. After all, once a snake has been tail-flagged, it might as well move ambush sites, because the local squirrels are now aware of its presence.

In addition to employing highly effective perception and vigilance advertisement behaviors, those darn squirrels have also evolved to anoint their fur with rattlesnake scent! They get this odor from chewing up shed rattlesnake skins. Barbara Clucas showed that the snake scent application did not deter other squirrels or help reduce ectoparasites, bolstering the case that it is a form of olfactory camouflage that serves to reduce squirrel detectability to snake predators or to repel other rattlesnakes motivated to avoid hunting in the same area as a conspecific.

Figure from Clucas et al. 2008

By now, I imagine the snake biologists in the audience are itching to see a snake actually get one for once. Here you go:

If you want to see more videos and stay current on the Clark lab's research, subscribe to their Youtube channel or to Strike, Rattle, & Roll, a rattlesnake behavior blog published by Clark lab PhD student Bree Putman.


Thanks to Rulon Clark for his helpful review of this article.


Barbour, M. A. and R. W. Clark. 2012. Ground squirrel tail-flag displays alter both predatory strike and ambush site selection behaviours of rattlesnakes. Proceedings of the Royal Society B: Biological Sciences doi:10.1098/rspb.2012.1112. <link>

Clark, R. W., S. Tangco, and M. A. Barbour. 2012. Field video recordings reveal factors influencing predatory strike success of free-ranging rattlesnakes (Crotalus spp.). Animal Behaviour 84:183-190. <link>

Clucas, B., D. H. Owings, and M. P. Rowe. 2008. Donning your enemy's cloak: ground squirrels exploit rattlesnake scent to reduce predation risk. Proceedings of the Royal Society B: Biological Sciences 275:847-852. <link>

Coss, R. G. and D. H. Owings. 1978. Snake-directed behavior by snake naive and experienced California Ground Squirrels in a simulated burrow. Zeitschrift für Tierpsychologie 48:421-435. <link>

Owings, D. H. and R. G. Coss. 1977. Snake mobbing by California ground squirrels: adaptive variation and ontogeny. Behaviour 62:50-69. <link>

Rundus AS, Owings DH, Joshi SS, Chinn E, Giannini N (2007) Ground squirrels use an infrared signal to deter rattlesnake predation. Proceedings of the National Academy of Sciences 104:14372-14376 <link>

Creative Commons License

Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.


Unknown said...

Is the hypothesis that a snake won't strike a tail-wagging squirrel because the individual has learned it is not effective or is it that reluctance to strike a tail-wagging squirrel is a behavior with a genetic component and the trait has proliferated in the population?

Andrew Durso said...

Dave, great question. I had no idea, so I asked Rulon. He says: "It's a question I'd love to answer. We don't have any data on how these behaviors develop in snakes ontogenetically, so I can't say if it's learned or not. My gut feeling is that it's probably a bit of both--they may show some reluctance to strike animals that appear to know they are there (through orientation, posture, etc), and then on top of this they probably rapidly learn that squirrels that tail flag in particular are very hard to land a strike on." So look out for future research out of Rulon's lab addressing this question.

Andrew Durso said...

He adds: "We do see snakes occasionally try to strike adult squirrels that are tail flagging, but they've always missed (one snake hit a tail flagging pup once, though). Thus, there appears to be lots of opportunity for learning from experience for the snakes."

Unknown said...

Very cool...looking forward to reading more about this relationship. Thanks for tracking down an answer.