Convergent Evolution in Small Mammal Antisnake Defenses

This post is part of a Reptile and Amphibian Blogging Network (RAmBlN) online event called #CrawliesConverge. We are writing on convergent evolution in reptiles and amphibians. Find our event schedule here. Follow on Twitter or Facebook.

Northern Pacific rattlesnake consuming a California ground squirrel pup.
Photo: B.J. Putman

Fitness is determined by two things: survival and the propagation of one’s DNA. Individuals that survive longer than others have more chances to reproduce and thus pass on their genes. Their success will determine the genetic makeup of the next generation (the foundation of natural selection). Predators act as one of the strongest selective forces in nature because once eaten, an individual is neither able to survive nor reproduce. It’s no surprise then that animals evolve many unique ways to deter predation.

Rattlesnakes and some other venomous snakes hunt in a stereotyped manner called ambush hunting. They remain stationary at a hunting site, patiently waiting for unsuspecting prey to wander by. They employ a rapid strike, during which they embed their fangs into the prey’s body. They inject venom into the prey, then typically release it and let it succumb to the venom before ingesting it. Because most venomous ambush-hunting snakes around the world do not drastically deviate from this general strategy, their prey experience almost the same predation pressures. Thus, prey* have independently figured out similar ways to avoid being eaten by ambush-hunting snakes.  

*by prey, I’m talking about small mammals (squirrels, gerbils, chipmunks, etc.). Snakes also consume other types of prey, but as far as I know, these prey do not exhibit the same antisnake defenses as small mammals. 

Only a few research groups are studying the predator-prey relationship between small mammals and snakes. The most well-known study systems involve the Cape ground squirrel and cobras/puff adders in South Africa, the kangaroo rat and rattlesnakes in the southwestern US, and the California ground squirrel and rattlesnakes in California (my system!).  However, we know many other small mammals around the world exhibit similar defenses from anecdotal reports. 

Left: a Cape ground squirrel harassing a cobra.  Right: the squirrel leaps away from a strike.
Photo: shockmansion.com 

Small mammals across the globe deter snake predation in three main ways:

1) Sending Signals

Many small mammals are not scared by snakes. They boldly approach them, investigate, and sometimes attack the snake! Typically, they will also spend a considerable amount of time repeatedly moving a body appendage in front of the snake. Most animals like squirrels and chipmunks wave their tails at the snake (Kobayashi 1987, Hersek and Owings 1993, Clark 2005), while others, like kangaroo rats and desert gerbils, drum their feet against the ground (Randall and Matocq 1997, Randall et al. 2000). Upon first glance, this seems like a pretty dumb thing to do in front of an animal that could kill you. However, these repetitive movements serve as warning signals to the snake, and actually deter it from attacking. Research from our lab has shown that squirrel tail-flagging tells the snake that it has been discovered (it has lost the element of surprise), and that the squirrel is prepared for an attack (i.e. if the snake strikes, it will likely miss) (Barbour and Clark 2012, Putman and Clark 2015). These signals could also inform other small mammals in the area of the snake’s presence, further degrading the value of its hunting site (because if everyone knows where the snake is, everyone is going to avoid the area). Some suggest that small mammals wave their tails to make themselves look like a larger more formidable opponent to the snake, but no study has yet tested this hypothesis.

Video of a kangaroo rat footdrumming at a sidewinder rattlesnake in the Mojave Desert.
Snake in burrow. Rat starts drumming 0:53 sec into video.
Video from the Clark Lab YouTube Channel.

Video of a Cape ground squirrel and mongoose harassing a cobra. Both exhibit aerial leaps when startled. 

Video from Smithsonian Channel. 

2) Ninja Reactions

When small mammals signal to snakes that they are ready and able to evade a strike, they are not lying. Thanks to snake predation, small mammals around the world have become ninja warriors, able to rapidly escape sticky situations using aerial acrobatics. This is a serious adaptation because a snake can strike at a velocity of 4.5 m/sec, meaning it could take a snake less than 70 milliseconds to strike a prey 30 cm away!  Small mammals need to use a response pathway that bypasses cerebral processing in order to react fast enough. Hence, it has been suggested that their responses to strikes are a type of startle response induced by acoustic stimuli rather than visual (meaning they respond to the sound of a snake strike and not the sight of one). The visual system responds via G-protein-coupled receptors, which are too slow to induce the speed of response we observe. The mechanoreceptors of the acoustic startle response are much faster and bypass cerebral processing. One study supports this claim by showing that only kangaroo rats with intact auditory systems were able to avoid rattlesnake strikes, while experimentally deafened rats could not (Webster 1962).

A quick response is important in avoiding a snake strike, but so is the type of escape you use. Successfully outrunning a snake strike is unlikely (see velocity above) – you would literally need to be the Flash to survive.  So instead of running away from strikes, small mammals have evolved the ability to leap vertically or horizontally away. This type of escape quickly propels the body of the small mammal away from the vector of a snake strike. Once snakes initiate an attack, their ability to alter their strike trajectory is limited, and so prey benefit more from displacing their bodies vertically or horizontally than by trying to outdistance the strike by moving within the same plane as the strike trajectory. Videos of these aerial leaps show that small mammals use their tails to contort themselves, often rotating their bodies near 180 degrees while midair. Evasive leaping is known to occur in squirrels, mongoose, and kangaroo rats. Kangaroo rats are the masters though, propelling themselves several body lengths upward when threatened with a strike.

Video showing the difference between squirrels running and leaping away from a 

simulated rattlesnake strike (spring-loaded cork). 

Video from Clark Lab YouTube Channel.

Video of a kangaroo rat leaping tremendously high in response to a strike.

Video from Clark Lab YouTube Channel.

3) Venom Resistance

Venom resistance levels of California ground squirrel 
blood paired with venom from different species of 
rattlesnake. Squirrels effectively inhibit the venom of
 C. oreganus and also  C. v. viridis, a close relative of 
C. oreganus (gray bars). Resistance against C. atrox 
venom is low (red bar) because California squirrels are 
not generally preyed upon by this snake species. 
Taken from Biardi et al. 2011.

Innate resistance to venom is what allows small mammals to closely approach and harass venomous snakes. Many small mammals are born with blood plasma factors that allow them to neutralize the effects of venom. Selection to minimize these effects is strong because even if an animal survives an attack, it must also minimize hemorrhage, tissue destruction, and disruptions to other bodily functions that follow envenomation because these could mess up the day-to-day activities of the animal. Thus, snakes and small mammals are often caught in an evolutionary arms race: snakes up their venom toxicity when the prey evolves a stronger defense, and this causes the adaptation cycle to repeat itself.
  

Several species of small mammal are known to harbor particularly high levels of venom resistance including the mongoose, opossum, woodrat, woodchuck, and some species of ground squirrel (see Ovadia and Kochva 1977, Perez et al. 1978, Poran andCoss 1990, Biardi and Coss 2011, Jansa and Voss 2011). Interestingly, the Cape ground squirrel which behaves similarly toward venomous snakes as the California ground squirrel is not resistant to either of its snake predators, the snouted cobra and the puff adder (Phillips et al. 2012). Findings like these help us understand the constraints associated with evolving such defenses.  

Many studies that have quantified venom resistance are flawed because they do not compare snakes and small mammals from the same area. For example, a study might examine how well squirrel blood inhibits venom by mixing it with venom pooled from snake species across the country, not just the species that only prey on the squirrels. Furthermore, if each population is in its own evolutionary arms race, even using venom of the appropriate snake species may provide us with an inaccurate measure of resistance – we have to use snakes and small mammals from the exact same population because prey evolve specific blood plasma properties to combat their local snakes, while snakes evolve specific venom properties to overcome the local prey’s resistance. Matt Holding at Ohio State University is doing exactly this with the California ground squirrel-Pacific
rattlesnake system, and others are on their way to improving our knowledge on this topic.

***

Snakes not only remove prey individuals from a population (rodent control), but impact their behaviors and physiology. The unique but similar defenses small mammals have evolved against snake predation demonstrate snakes’ importance as top level predators in ecosystems worldwide.  

The infographic below summarizes this blog post - distribute at will :) :) :)

References:

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 279:3827–3833.

Biardi,J. E., and R. G. Coss. 2011. Rock squirrel (Spermophilus variegatus) blood sera affects proteolytic and hemolytic activities of rattlesnake venoms. Toxicon 57:323–331.

Clark,R. W. 2005. Pursuit-deterrent communication between prey animals and timber rattlesnakes (Crotalus horridus): the response of snakes to harassment displays. Behavioral Ecology and Sociobiology 59:258–261.

Hersek, M. J., and D. H. Owings. 1993. Tail flagging by adult California ground squirrels: a tonic signal that serves different functions for males and females. Animal Behaviour 46:129–138.

Jansa, S.A., and R. S. Voss. 2011. Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PloS one 6:e20997.

Kobayashi,T. 1987. Does the Siberian chipmunk respond to the snake by identifying it? Journal of Ethology 5:137–144.

Ovadia, M., and E. Kochva. 1977. Neutralization of Viperidae and Elapidae snake venoms by sera of different animals. Toxicon 15:541–547.

Perez, J. C., W. C. Haws, V. E. Garcia, and B. M. Jennings. 1978. Resistance of warm-blooded animals to snake venoms. Toxicon 16:375–383.

Phillips, M.A., J. M. Waterman, P. Du Plessis, M. Smit, and N. C. Bennett. 2012. Noevidence for proteolytic venom resistance in southern African ground squirrels. Toxicon 60:760–763.

Poran, N. S., and R. G. Coss. 1990. Development of antisnake defenses in California ground squirrels (Spermopilus beecheyi): I. behavioral and immunological relationships. Behaviour 112:222–224.

Putman, B. J., and R. W. Clark. 2015. The fear of unseen predators: ground squirrel tail flagging in the absence of snakes signals vigilance. Behavioral Ecology 26:185–193.

Randall, J. A., and M. D. Matocq. 1997. Why do kangaroo rats (Dipodomys spectabilis) footdrum at snakes? Behavioral Ecology 8:404–413.

Randall, J. A., K. A. Rogovin, and D. M. Shier. 2000. Antipredator behavior of a social desert rodent: Footdrumming and alarm calling in the great gerbil, Rhombomys opiums. Behavioral Ecology and Sociobiology 48:110–118.

Webster,D. B. 1962. A function of the enlarged middle-ear cavities of the kangaroo rat, Dipodomys. Physiological Zoology 35:248–255.