Friday, November 7, 2014

Many Tales of the Snake Tail

Upon first glance, snakes’ bodies may appear to be one giant tail (or one long body depending on how you look at it). However, snakes actually have a defined tail region which is separate from their main body. The tail starts at the cloaca, the magic hole where defecation, fluid release, and reproduction take place. We have multiple holes for these functions, but snakes only have one.  

The snake's tail is just after the cloaca

So what’s so special about a snake’s tail? Well, because snakes are limbless, their tails fill many of the roles that limbs play in other animals. For instance, the tail is used to grasp onto things, in defense against predators, and as a communication device. Because snakes use their tails for a variety of functions, their tails often look different than the rest of their bodies.

Specialized tail movements are exhibited in more than 70 snake species (Greene 1973). Tail movements usually consist of conspicuous motions of waiving the tail back and forth. Although many species differ in the ways in which they move their tails (slow undulatory motions compared to fast jerky movements), all tail displays probably serve an adaptive function (they benefit the snakes in some way). Many proposed functions for this behavior exist. They are detailed below.  

Many juvenile vipers, including rattlesnakes, use their tails to attract prey in what’s called a caudal lure. Their tails are often brightly colored and mimic insect larvae. The movement of their tails attracts animals that eat insects such as lizards and amphibians. Usually these snakes abandon caudal luring behavior (and their tail coloration fades) once they reach adulthood because their diet switches to mammals which are not attracted to insect larvae (Rabatsky and Waterman 2005b, Reiserer and Schuett 2008). 

Can you tell the Yellow-Lipped Sea Krait's head apart from its tail (left)?  The Spider-Tailed 
Horned Viper from Iran has a lure that looks suspiciously like a spider (right). 

Other snakes use their tails in defense against predators. When attacked, many of these snakes will hide their heads under their bodies and waive their tails in the air. Some snakes, such as the Malaysian Pipe Snake (Cylindrophis rufus), do not just waive their tail at random, but violently strike it from side to side as if it were a head. The idea is that predators will aim for the tail thinking it is the snake’s head and this is beneficial to the snake because injuries to the tail are far less serious than injuries to the head. Many snake’s tails, such as those of the Indian Sand Boa (Eryx johnii.), actually resemble their heads in an effort to further confuse predators. Evidence of more scaring on some snakes’ tails compared to other parts of their bodies supports the notion that their tails deflect attacks away from the head (Greene 1973).

(Taken from Greene 1973)

What’s so fascinating about these tail displays is that they may hold the key to the evolution of the rattlesnake’s rattle. We know that today the rattle is used in defense and serves as a warning to predators. However, debate continues as to why the rattle evolved in the first place. There are two camps, those who believe the rattle first evolved to attract prey then switched to a defensive function and those who believe the rattle has always been for defense.  In support of the “prey -attractant-first hypothesis”, Schuett et al. (1984) state that the rattle pre-cursor must have started out small (1-2 segments) so it would have been incapable of making sufficient noise to warn others of the snake’s dangerousness. In support of the “function-has-never-changed hypothesis”, others point out that no other snake lineages that use their tails to attract prey have ever evolved anything similar to a rattle. 
The Dusky Pigmy Rattlesnake has a yellow tail and a small rattle. 
This tiny snake only has one rattle segment! Photo by Mark Herse.

The only rattlesnake we know of to use its tail (and not its rattle) for both prey capture and for defense in adulthood is the Dusky Pigmy Rattlesnake (Sistrurus miliarius barbouri). This species has the smallest rattle compared to its body size of all rattlesnakes (Cook et al. 1994), and 50% of adults in a typical population cannot produce sufficient rattling sounds because of the smallness of their rattles (Rabatsky and Waterman 2005a)! So these pigmy rattlesnakes may be similar to what rattlesnake ancestors may have looked and acted like. However, we don’t know for sure and debate continues on how and why the rattle evolved. 

Over the many years of remotely filming wild rattlesnakes, I have recorded three individuals exhibiting non-rattling tail displays (all adult Northern Pacific Rattlesnakes, one female and two males). This display consists of slowly flopping the raised tail from side-to-side (see video below).

Strimple (1992) emphasized the importance of collecting precise descriptions of the contextual stimuli that elicit tail displays to better understand their function. I have noticed some common themes among the three incidents I recorded. All snakes were in a loosely-coiled body position. This is different from an ambush coil which snakes employ when hunting prey. Snakes are typically loosely-coiled when shedding, digesting, or recovering from surgery (one snake was recovering from surgery, the other two could have been digesting but I am unsure). Snakes exhibited the display intermittently over several minutes (approximately 2-6 minutes), then left their sites almost immediately after. The cloaca of the snakes appeared swollen when they were displaying. Two snakes were alone when they displayed while the third was with another rattlesnake (both were males) and their tail displays can be viewed in the YouTube video above.

What could be the function of this non-rattling tail display? Although I lack enough evidence to definitively determine its function, I can speculate on the options.

Is it for prey capture?
  • This is unlikely because all snakes were not in hunting body positions when they exhibited this behavior (they were loosely-coiled).

Does it defend against predators? 
  • No predatory threat was visible on camera (although predators could have been close by) when this behavior was recorded. All defensive displays reported in other snake species are elicited by touching or severely harassing the snake (their first line of defense is camouflage). Thus, I remain skeptical that this is a defensive display given that the snakes were not physically disturbed.

Does it communicate with others of the same species?
  • This is possible. The cloaca appeared swollen and could have been discharging scented fluids (which have been shown to affect conspecifics). Perhaps the tail movements laid down the scent? Also in support of this, I recorded the tail display when two adult males were interacting with each other. The presence of one male appears to have caused the other to exhibit the display. Schuett (1997) found that tail writhing is displayed by defeated males after male-male combat in Copperheads (Agkistrodon contortrix), and is assumed to advertise the submission of the defeated male. However, it was not the breeding season and these males were never observed to behave aggressively toward each other. Thus, I remain doubtful that this display was to advertise submission.

I hope to converse with other naturalists and scientists who have seen similar tail behaviors in adult rattlesnakes. With enough anecdotal evidence we may be able to parse out the contexts in which this behavior occurs to generate hypotheses to test its function. 

Please contact me if you have observed this behavior! 



Cook, P. M., M. P. Rowe, and R. W. Van Devender. 1994. Allometric scaling and interspecific differences in the rattling sounds of rattlesnakes. Herpetologica 50:358–368.

Greene, H. W. 1973. Defensive tail display by snakes and amphisbaenians. Journal of Herpetology 7:143–161.

Rabatsky, A. M., and J. M. Waterman. 2005a. Non-rattling defensive tail display in the Dusky Pygmy Rattlesnake, Sistrurus miliarius barbouri: a previously undescribed behavior. Herpetological Review 36:236–238.

Rabatsky, A. M., and J. M. Waterman. 2005b. Ontogenetic shifts and sex differences in caudal luring in the dusky pigmy rattlesnake, Sistrurus miliarius barbouri. Herpetologica 61:87–91.

Reiserer, R. S., and G. W. Schuett. 2008. Aggressive mimicry in neonates of the sidewinder rattlesnake, Crotalus cerastes (Serpentes: Viperidae): stimulus control and visual perception of prey luring. Biological Journal of the Linnean Society 95:81–91.

Schuett, G. W. 1997. Body size and agonistic experience affect dominance and mating success in male copperheads. Animal Behaviour 54:213–24.

Schuett, G. W., D. L. Clark, and F. Kraus. 1982. Feeding mimicry in the rattlesnake Sistrurus catenatus, with comments on the evolution of the rattle. Animal Behaviour 32:625–626.

Strimple P. D. 1992. Caudal-luring: a discussion on definition and application of the term. In: Strimple PD, Strimple JL, eds. Contributions in herpetology. Cincinnati, OH: Greater Cincinnati Herpetological Society, 49–54.

Tuesday, October 14, 2014

My Second Publication Has Video of Ninja Squirrels

So…it’s been a while since I blogged mainly because there hasn’t been much to write about. My summer field season was suuuppper slow and filled with many road bumps. Snakes, unfortunately, are not very active during drought times (just ask Mike Cardwell). However, I have been working on a post about an extraordinary rattlesnake behavior that I recorded in three individuals; cannot give you any details at the moment, but I plan to write a Herpetological Review article about it once I gather more insight from other snake researchers. Stay tuned. Anyway, this post is not about that, but about the first publication to stem from my dissertation research (and my second publication overall). Woohoo!

When they encounter a rattlesnake, squirrels approach it and waive
their tails back and forth (a behavior aptly called tail flagging)

Squirrels tail flag (a vertical side-to-side motion of the tail) to deter snake predators (both rattlesnakes and gopher snakes). Tail flagging deters snakes because it signals to them that they have been discovered, and because snakes rely on surprise to attack prey, their likelihood of hunting success drops significantly. So after receiving tail flagging displays from squirrels, snakes relocate to a new hunting site where prey are unaware of its hidden location (Barbour and Clark 2012). There’s just one problem with tail flagging: squirrels use it most often when no snake is present. Are squirrels dishonestly advertising their discovery of a snake? This was the question I sought to answer.

Is tail flagging a dishonest signal?

Many animals use signals similar to tail flagging to advertise their awareness of predators. However, these animals also exhibit their signals when predators are absent. This is a common phenomenon!
Just like ground squirrels, these two bird species, the moorhen 
(left) and motmot (right), flick their tails in the absence of predators.

Why would animals signal to predators when no predator is around? The idea is that they are not signaling their awareness of a predator, but their readiness for a surprise attack from hidden predators (this is also called vigilance). Vigilant animals that are prepared for an attack should be harder to catch than non-vigilant animals. But in order to test the hypothesis that animals signal vigilance in the absence of predators, we need to simulate predator attacks on signaling and non-signaling prey and then record their responses. We predict that signaling prey will escape more effectively than non-signaling prey. 

Unaware individuals should not respond effectively to surprise attacks.

And so this is exactly what I did! I simulated rattlesnake strikes on tail-flagging and non-tail-flagging squirrels and filmed their responses using a high speed video camera. You may be wondering how I simulated a snake strike. Well, I didn’t have to do too much work because a strike-simulator already exists on the market and it’s called the “Snake in a Can Prank.”

Inspiration for the strike-simulating device

I modified these prank toys and shot them at unsuspecting squirrels. I tested squirrel responses to the strike-simulator under three treatments that affected their tail-flagging: 1) No Snake Present, 2) Snake Present, and 3) Recent Snake Encounter. Most squirrels did not tail flag when no snake was present (No Snake), squirrels actively interacted with a present rattlesnake (Snake Present), and squirrels maintained tail flagging behaviors after recently encountering a snake that was no longer present (Recent Snake). The Recent Snake treatment is unique because it decouples the effect of predator presence from tail flagging.  

And now…the Results. Squirrels in the Recent Snake treatment (tail flagging in the absence of predators) were more effective at evading surprise attacks than squirrels in the other two treatments. This was just what I expected. Tail flagging in the absence of snakes associated with faster reaction times and escape speeds. 

Two figures from my study. Squirrels in the Recent Snake treatment reacted
faster and displaced their bodies more quickly (quicker escape speed) than
squirrels in the other two treatments.Letters indicate differences between
groups (no difference between 
Snake Present and No Snake
Furthermore, these squirrels used unique ninja-like maneuvers to flee from the attack (unlike squirrels in the other two treatments which mostly ran away from the attack). Vigilant squirrels leapt either vertically or horizontally, contorting their bodies, and using their tails to propel them through the air. This type of flee maneuver makes sense if one is trying to escape a rattlesnake strike. Strikes are extremely fast, but once a snake strikes, it cannot alter its strike trajectory. Thus, it’s better to move outside of the plane of the strike than the try to outdistance it (which is probably ineffective considering the speed at which a rattlesnake can strike). 

Squirrels in "ninja-mode" use evasive leaps to escape simulated snake strikes. This occurs most often when squirrels have
 encountered a snake, but then no longer know where it is (because it has been removed). 


My study called, The fear of unseen predators: ground squirrel tail flagging in the absence of snakes signals vigilancecan be found in a future issue of the journal, Behavioral Ecology. Advanced access to this publication can be found here

Tuesday, May 20, 2014

Daredevil Gopher Snake Gets Rescued!

I arrived at my field site (Blue Oak Ranch Reserve) a little over a week ago. Work has been pretty slow as we are trying to capture rattlesnakes to implant radio transmitters into. Three days ago, we ended work early and were hanging out at the field station (a large barn). I noticed snake-like slithering near the roof of the barn so I looked up. Lo and behold a gopher snake (Pituophis catenifer) had weaseled its way (or shall I say “snaked” its way) about thirty feet up the barn wall! At first, I thought this sight of the wall-climbing snake was strange, but then I realized that it was heading straight towards a bird’s nest. I became extremely excited as I had never seen a snake ambush birds before. I got out my camera and started to record the snake.

Although I mainly think of gopher snakes as ambushing squirrel pups inside their burrows, these snakes are common bird nest predators, and will go for both cavity-nesting and open-nesting bird species. A study performed by Eichholz and Koenig In central California (1992) found that approximately 21% of bluebird nests and 36% of nest failures are caused by snakes, making snakes the primary cause of nest mortality. They also found that gopher snakes do not randomly search tress for nests, but only climb those with active nests. This suggests that they have the ability to detect bird nests from the ground (probably by picking up chemical cues). These snakes seem to prefer eating baby birds instead of eggs, and their preference increases as the babies grow older. Another report by Czaplewski et al. (2012) describes a gopher snake making a dangerous climb to ambush cliff swallow nests in Utah. The authors’ note the appearance of several small food items in the snake’s belly.

 Gopher snake browsing on cliff swallow morsels (taken from Czaplewski et al. 2012)

Back to my story, the snake appeared to be entering the bird nest when it suddenly became very still. I waited for it to continue its movement into the nest, however it started to twist and squirm. It had become tangled in plastic mesh netting on which the nest was built. Unable to reach the snake, I thought for sure it would die.

If only snakes could use ladders, then bad things wouldn't happen...

As it remained motionless stuck within the netting, a wren approached the snake and made loud calling sounds. This could have been the mother bird defending her eggs. Many birds will make specific alarm calls in response to snake predators. A recent study shows that Japanese great tits (Parus major minor) produce alarm calls that encode information about the type of predator (Suzuki 2014). These birds use a “jar” call for snake predators and a “chicka” call for crows and martens (a type of weasel). These calls are thought to warn offspring and other birds, but they may also deter the snake from further pursuit of the nest (something called pursuit-deterrent signaling). My current research examines the use of pursuit-deterrent signaling in California ground squirrels against rattlesnake predators.

View the whole gopher snake story on the Youtube video above!

The gopher snake remained stuck in the mesh netting near the roof of the barn, and I thought for sure it would die. However, Erik, the reserve steward came to the rescue! He found a tall ladder that he used to reach the snake and remove it from the barn wall. The snake remained tangled in the mesh and we had to cut it out. Poor snake had ripped some of its skin open trying to free itself. I applied anti-septic liquid bandage to its cuts, and am now keeping it in captivity so that its skin can heal. I will release it soon so it may resume its daredevil climbs.

Erik was this snake's "knight in shining armor" 

 The gophie really did a number on itself. Luckily, we were able to cut away the mesh.


Czaplewski, N. J., K. S. Smith, J. Johnson, C. Dockery, B. Mason, and I. D. Browne. 2012. Gopher Snake Searching Cliff Swallow Nests in East Central Utah. Western North American Naturalist 72:96–99.

Eichholz, M. W., and W. D. Koenig. 1992. Gopher Snake Attraction to Birds’ Nests. The Southwestern Naturalist 37:293–298.

Suzuki, T. N. 2014. Communication about predator type by a bird using discrete, graded and combinatorial variation in alarm calls. Animal Behaviour 87:59–65.

Monday, May 12, 2014

To Detect a Predator: A Multimodal Approach

This is another guest post from undergraduate scientist, Jenny Schefski. She previously wrote a post on this blog last summer when she was conducting research for her independent project (read the post here). Now, she elaborates more on the concept behind her research and why it is important. 

As humans, we rarely need to rely on all of our senses to find food, shelter, or mates. Indeed, these necessities are often advertised and/or delivered to us with little effort. With virtually no predators, we aren’t even likely to need our senses to avoid becoming prey. 

Unlike wild animals, most people have little trouble finding food, shelter, or even mates.

Unless you’re unlucky enough to encounter Hannibal, you probably aren’t too concerned about becoming a predator’s next meal.

However, most animals heavily rely on their senses to avoid predators, and to find food, shelter, and mates. By utilizing multiple senses, animals increase their likelihood of success in a variety of conditions. Sharks, for example, are capable of using a wide array of senses to locate prey.1 This is especially important in the ocean since prey can be sparse and visibility can be poor. By utilizing multiple senses to find their prey, sharks maximize their likelihood of foraging success.

Sharks maximize their hunting efficiency by using multiple senses to track down prey.

The use of multiple senses to gather information about one’s environment is called multimodality.2 Multimodality is important to the study of animal interactions because multiple sensory inputs can lead to complex behaviors. In simpler terms, a noise from Animal 1 might result in a specific behavior from Animal 2. However, the scent of Animal 1 might lead to a different behavior from Animal 2. 

Let’s say a= a snake’s pattern, and b= a snake’s scent. The shapes that follow the arrows represent all of the possible response behaviors from a hypothetical squirrel. (Partan & Marler 2005).

Predator-prey interactions often involve complex behaviors. In order to avoid becoming a predator’s next meal, prey must be able to identify and detect their predators.  Over millions of years, prey have fine-tuned many of their senses to the detection of specific predators. For example, wolf spiders can detect the specific frequency of vibrations from their bird-predator’s pecking on a tree.3  Spiders that were experimentally exposed to the pecking frequency stopped all courtship behaviors and movement. Even more, wolf spiders also respond to the shadow of a bird predator; except, in this case, they increased locomotion and escape behaviors. This study is not only a prime example of how prey can detect sneaky predators, but also how multimodal interactions can lead to complex outcomes.

Wolf spiders can identify and respond to the pecking, calling, and even shadow of a bird-predator. Of course, there are always prey that miss the memo(s). This unfortunate wolf-spider probably should have paid more attention to his senses.  

Not only is multimodality important for predator detection, but it is also key for species discrimination. For example, brown anoles can detect their bird-predator, the grackle, by sight and by sound.4  Throughout the day, brown anoles see and hear multiple birds. So how can they know when to hide or when it’s safe to do important things like forage or look for a mate?  Since the anole can identify the grackle’s specific appearance and call, it can discriminate between the grackle and other non-threatening birds. By having the ability to cue-in on the grackle using multiple senses, the anole can maximize its time to forage and search for a mate, and minimize its likelihood of becoming a grackle’s next meal.

Brown anoles can identify the appearance and call of their predator, the great tailed grackle. This ability allows anoles to distinguish the grackle from non-threatening birds so they don’t have to hide all day.

Another predator-prey system that is ideal for the study of multimodal predator detection and discrimination is that of the California ground squirrel. California ground squirrels have two snake-predators: the Pacific gopher snake and the northern Pacific rattlesnake. Gopher snakes are non-venomous and rely on their stealth to invade squirrel burrows in search of pups. Conversely, rattlesnakes are venomous and can quickly kill both pup and adult squirrels. Since each snake poses a different level of immediate risk, it would behoove ground squirrels to not only identify a snake predator, but also discriminate between a venomous and non-venomous one. 

California ground squirrels have two snake-predators: the northern Pacific rattlesnake (top) and the Pacific gopher snake (bottom). Rattlesnakes are more threatening to squirrels because of their ability to quickly inject squirrels with deadly venom. (Photos: Joseph Chase)

Previous studies show that ground squirrels do indeed discriminate between gopher snakes and rattlesnakes.5 This is evidenced by squirrels’ behavior toward each snake species. Ground squirrels tend to be more aggressive toward gopher snakes and will approach them more closely. When presented with a rattlesnake, ground squirrels are likely to monitor it more often, but maintain more distance from it.

Exactly how California ground squirrels discriminate between each snake-predator remains unclear. We do know that squirrels can identify each snake by its visual appearance.5 However, there are a variety of reasons why vision is not always a reliable mode of detection for ground squirrels. Not only do squirrels often encounter snakes in their very own, dimly lit burrows, but they also encounter them often in dense vegetation. Furthermore, both rattlesnakes and gopher snakes blend into their surroundings very well. All of these factors suggest that squirrels might use another sense to detect each snake and discriminate between the two species.

Can you find the snakes in these photos? California ground squirrels often encounter snakes moving through the grasses that they feed on. Spoiler: a gopher snake (left) and a rattlesnake (right). (Photos: Joseph Chase)

My research focuses on how California ground squirrels use multiple senses to detect and discriminate between gopher snakes and rattlesnakes. One previous lab study suggested that California ground squirrels can identify the scent of each snake-predator.6 My work takes this study to the field, a more realistic setting. By manipulating the scent of rattlesnake and gopher snake models, I can tease apart the role of each cue in squirrel response behavior. My ongoing analysis has led me to many questions: Does the smell of a snake make squirrels more wary of their environment or does it elicit anti-snake behavior? What will squirrels do when presented with a rattlesnake model that smells like a gopher snake? Do squirrels trust visual or olfactory input more when deciding how to react to a snake predator?

I am still in the process of analyzing seemingly endless field footage, but I hope to have some answers soon!


1.  Hueter, R.E., D.A. Mann, K.P. Maruska, J.A. Sisneros, and L.S. Demski. 2004. Sensory Biology of Elasmobranchs. Biology of Sharks and Their Relatives 1: 326-358.

2. Partan, S.R. and P. Marler. 2005. Issues in the classification of multimodal communication signals. The American Naturalist 166:231-245.

3.  Lohrey, A.K., D.L. Clark, S.D. Gordon, and G.W. Uetz. 2009. Antipredator responses of wolf spiders (Araneae: Lycosidae) to sensory cues representing an avian predator. Animal Behaviour 77:813-821.

4.  Elmasri, O.L., M.S. Moreno, C.A. Neumann, and D.T. Blumstein. 2012. Response of brown anoles Anolis sagrei to multimodal signals from a native and novel predator. Current Zoology 58:791-796.

5.  Towers, S.R. and R.G. Coss. 1990. Confronting snakes in the burrow: snake-species discrimination and antisnake tactics of two California ground squirrel populations. Ethology. 84:177-192. 

6.  Hennessy, D.F. and D.H. Owings. 1977. Snake species discrimination and the role of olfactory cues in the snake-directed behavior of the California ground squirrel. Behaviour. 65:115-123.