Monday, April 20, 2015

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.

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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 :) :) :)






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Monday, March 30, 2015

In Search of the Coronado Island Rattlesnake

The famous arch of Cabo San Lucas
Baja California is my new obsession. The weather is perfect, the landscape is beautiful, and the ocean is always a stone’s throw away. I just got back from two trips past the border: (1) to Cabo for my honeymoon (where the screams of spring breakers soar through the air), and (2) to Southern Coronado Island in search of the elusive Coronado Island Rattlesnake.

Rattlesnakes live on several islands off the coast of Baja. Many of these snakes are the laid-back island counterparts of their mainland selves, and like other island inhabitants, many have drastically changed in body size from their mainland ancestors. For instance, Crotalus ruber lorenzoensis of San Lorenzo Island is a tiny descendent of the larger mainland Crotalus ruber. The Santa Catalina Island Rattlesnake (C. catalinensis) is one of the more famous species as it is the only known rattlesnake to “lose” its iconic rattle, although lorenzoensis and others seem to be on their way (Radcliffe and Maslin 1975). Poor thing only has one rattle segment to its name! Most of the Baja island rattlesnakes are endemic, which means they occur in one place and nowhere else (and this would be whichever island they inhabit). Although most of these snakes are not endangered, their endemic status is still a conservation concern because it means they have extremely restricted geographical ranges.  


The Catalina Island Rattlesnake (far left) is considered rattleless with only one small segment at the base of its tail. The two island
subspecies of ruber (middle and right) are on their way to becoming rattleless. Taken from Radcliffe and Maslin 1975.
  

The tiny island of Southern Coronado. Photo: B.J. Putman.

The Coronado Islands are about 15 miles South of San Diego and 8 miles from mainland Mexico. The largest of the four is Southern Coronado Island with just 1 square mile of land. The Coronado Island Rattlesnake (Crotalus oreganus caliginis) is the only snake species on the island*. Not much is known about this species and so my adviser at San Diego State University has collaborated with Dr. J. Jesus Sigala Rodriguez of Universidad Autonoma de Aguascalientes on a new project to learn more about its ecology. Last week, I went with him to the southernmost island to search for snakes that will become part of a long-term monitoring project. We drove from San Diego to Rosarito with minor hiccups other than being stopped by border patrol agents who could not comprehend the unusual amount of wooden cover boards in our trunk. From Rosarito, we took a panga boat to the island. In about 45 minutes we arrived to our destination. The island does not have a dock so our skilled boat driver slowly maneuvered the panga to the closest rocks, which we jumped onto from the boat.
Article correction: the night snake and gopher snake also live on Coronado Island

About to launch our boat in Rosarito, Mexico.


Although the island boasts 1 square mile of land, most of the land is inaccessible because it is so steep. We set off searching for snakes where we could and placed cover boards in areas that seemed promising. Alligator lizards (Elgaria multicarinata) were by far the most commonly encountered herp – we saw way too many to count! We also found a few skinks (Plestiodon skiltonianus). In all, our greatest find was a legless lizard (Anniella pulchra?).

We found 8 individuals of our target species, and not to brag, but this tiny girl found the most out of everyone in our group (brushes off shoulders). I found one of the rattlesnakes next to a dead alligator lizard. I assumed it was about to consume the lizard before I disturbed it. Interestingly though, the lizard’s eyes were missing which suggests it had been dead for some time (probably a day or two). We were thus unsure whether the snake had struck the lizard the day before and had just relocated it or whether the snake was scavenging it.

Left: The beautiful legless lizard.  Right: A rattlesnake found with an eyeless alligator lizard (sorry for my horrible photo editing skills)


Left: Processing a snake while enjoying the view.  Right: Drawing blood from a "tubed" individual.


We implanted a personal integrated transponder (PIT) tag into each snake we found. We also determined each snake’s sex, drew a blood sample, and recorded measurements on body size, rattle size, and mass. The Coronado Island Rattlesnake looks almost identical in pattern and coloration to the Southern Pacific Rattlesnake (C. oreganus helleri), its closest relative. In fact, the island snake is thought to have come from a mainland population of helleri. However, the island species dramatically differs from the mainland species in body size: it’s miniature in comparison. This may come as no surprise as island variants are often smaller than their mainland counterparts, a phenomenon known as Island Dwarfism.  


On top of a hill on the island. About to place down some cover boards.


Island dwarfism is an interesting phenomenon because it goes against Cope’s Rule, the prevailing trend in nature that organisms evolve toward larger body sizes. But islands provide special circumstances whereby they limit animals to a restricted area and also limit the amount of available resources. Hence, compared to giants, dwarfs are able to utilize limited resources more completely and are less likely to succumb to population crashes (Wassersug et al. 1979).


Left: A snake found coiled under a rock.  Right: Same snake tubed and ready for processing.


Island Gigantism also occurs, whereby animals grow in body size when isolated on islands. Gigantism is thought to result from many islands’ lack of large mammalian predators. Without these predators, animals are free to grow and exploit niches that were unavailable to them on the mainland. This is a phenomenon known as Predator Release.

Changes in available prey resources can also influence island dwellers’ body sizes. Across all island snake species, populations that are dwarfed tend to prey on lizards and populations that are giant tend to prey on colonies of nesting seabirds (Case 1978). For rattlesnakes that specialize on small mammal prey, islands lacking small mammals should lead to dwarfism and islands with prey equivalent to or larger than small mammals should lead to gigantism. Another interesting benefit larger-bodied viperid snakes have is their enhanced ability to fast compared to smaller snakes (Meik et al. 2010). Thus, gigantism benefits viperid snakes on islands where prey population sizes frequently fluctuate and/or where prey have relatively high extinction rates. 

Left: A specimen of the giant speckled rattlesnake of Angel de la Guarda.
Right: a specimen of the dwarf speckled rattlesnake of El Muerto Island.
Taken from Meik et al. 2010.
  
Almost all Baja California island rattlesnake populations are dwarfs. Only one, the Angel de la Guarda Island speckled rattlesnake (C. mitchelli angelensis), has undergone island gigantism. The Speckled Rattlesnake (Crotalus mitchelli) seems to love the island life boasting three descendants (C. m. angelensis, C. m. mitchelli, and C. m. muertensis) on 14 different islands. A study done by Meik et al. (2010) found that the body sizes of island populations of speckled rattlesnakes were best explained by island size (Meik et al. 2010). Smaller islands house smaller snakes and larger islands house larger snakes. The authors found that rattlesnakes typically tend toward dwarfism on islands that are smaller than about 20 square kilometers. In addition, rattlesnakes tended to dwarf on islands where the relative abundance of small lizards was greater than rodents. The authors then suggest that shifts to consuming larger prey (chuckwallas), fluctuating prey densities, and predator release likely resulted in gigantism for the speckled rattlesnakes on Angel de la Guarda Island.

Larger islands tend to house bigger snakes (SVL = snout-vent-length, a measure
of body size). Taken from Meik et al. 2010.

Dwarfism of the Coronado Island Rattlesnake is likely the result of small island size (less than 2 square kilometers!), and a greater reliance on lizard prey (pocket mice are the only known rodent inhabitant of the island). Research from the long-term monitoring program should provide quantitative data to support these theories. In all, islands are awesome (and beautiful) places that can act as “closed” ecosystems providing scientists the means to conduct unique experiments and find new discoveries.




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Saturday, February 7, 2015

What do the Grammys and The Fear of Snakes Have in Common?

The Grammys are this Sunday and one of my favorite artists, St. Vincent, is nominated for Best Alternative Music Album. The first track on her album is entitled "Rattlesnake" (which is awesome), but its lyrics may not represent snakes in a good way. This song is about the fear and intensity of being isolated in the wilderness for the first time. She wrote the song after an experience in the American Southwest where she wandered alone through the desert one night and thought she heard a rattlesnake’s rattle. Based on the song’s lyrics and music composition, this was a frightening experience for her. Would this song have a different title if rattlesnakes were not feared by people?



Here are the lyrics to the song Rattlesnake by St. Vincent:

Follow the power lines back from the road
No one around so I take off my clothes
Am I the only one in the only world?

I see the snake holes dotted in the sand
As if the Seurat painted the Rio Grande
Am I the only the one in the only world?

Sweating, sweating no one is behind me
Sweating, sweating no one will ever find me

The only sound out here is my own breath
And my feet stuttering to make a path
Am I the only one in the only world?

Is that the wind finally picking up?
Is that a rattle sounding from the brush?
I'm not the only one in the only world

Running, running, running rattle behind me
Running, running, no one will ever find me
Running, running, running rattle behind me
Running, running, no one will ever find me
Sweating, sweating, sweating, rattle behind me
Running, running, no one will ever find me
Sweating, sweating, sweating, rattle behind me
Running, running, no one will ever find me


A broad theme of the song centers on a fear of snakes. Is this fear justified? Long long ago, snakes were in fact a predator of early man (and still prey on some hunter-gatherers today!) and so we hold an evolutionary reason for why we would be afraid of snakes. In the song, she becomes frightened after hearing the rattling sound of a rattlesnake. A lot of studies have focused on fear responses related to seeing to snake, but not hearing the sound of a snake. Is our response to hearing a snake different from when we see one? 

Rattlesnakes are good at hiding in the grass. Our ability to quickly detect 
snakes is important. Photo by B.J. Putman 


Past studies have shown that humans possess the keen ability to quickly detect hidden snakes, and this has led to the Snake Detection Theory which states that our strong need to detect snakes in the past has led to human’s crazy snake-finding skills which are no longer necessary for our current survival (Soares and Esteves 2014; Van Strien et al. 2014). However, our ability to find snakes quickly does not explain the psychological fear many people have towards snakes (Tierney and Connolly 2013). Some scientists believe that the fear of snakes is transmitted from mother (or father) to the child – it is a learned response. In support of this, both human and primate infants show greater fear of snake-like objects only after observing fearful reactions to the objects by their mothers (Mineka et al. 1984, Gerull and Rapee 2002)


Our fear of snakes stems largely from cultural learning.
The Snakes In Hats Tumblr is trying to change people's perception of snakes,
cause how can you NOT love animals wearing tiny hats? Adorable.


As past studies have shown, the fear that occurs after seeing a snake is likely culturally learned (unjustified), but the fear that occurs after hearing rattling may be justified. Little to no studies have been done on human responses to rattlesnake rattling, but research on other animals suggests that hearing a snake can indeed be startling, but differs from seeing a snake.  

As an example (and plug for my own study system), ground squirrels respond fearfully to rattlesnake rattling. They can even discriminate between more and less dangerous rattlesnakes just based on sound. Larger more dangerous snakes produce rattling with higher amplitudes and lower frequencies – louder and lower in pitch – than smaller snakes. In addition, warmer more dangerous rattlesnakes produce louder rattling with faster click rates than colder less dangerous rattlesnakes (Rowe and Owings 1996). In one study, squirrels tail flagged and stood alert more following playbacks of recorded rattling sounds from more dangerous snakes (Swaisgood et al. 2003). 


Both warmer snakes and larger snakes have higher amplitude rattling - they are very loud! 
Taken from Rowe and Owings 1996.


Dan Blumstein, researcher at UCLA, has been studying what he calls – The Sound of Fear (dun dun duuuun). He’s looked into the acoustic qualities of sounds associated with fear from the alarm calls and screams of mammals to the soundtracks of Hollywood films (like the music during the classic shower scene in Psycho). His team has found that sounds that make us aroused/jumpy/uneasy contain more noise than neutral sounds. What does that mean exactly? Well, noise doesn’t sound nice because it contains non-linearities, or sound wave distortions. Noise is more complex and more atonal than sounds we consider soothing. We may find noise so disturbing because its acoustic characteristics are more variable and somewhat unpredictable, making us less likely to habituate to them (Blesdoe and Blumstein 2014). Marmots (Blumstein and Récapet 2009), Great-tailed Grackles, (Slaughter et al. 2013), and White-crowned Sparrows (Blesdoe and Blumstein 2014) respond “fearfully” to noise.





The rattle is currently used by rattlesnakes for defense – warning potential predators of the snake’s dangerousness (see previous blog post). It makes sense that the sound of rattling be associated with fear to deter other animals from harming the threatened rattlesnake. Indeed, the rattling of a rattlesnake is noisy and atonal like screams and alarm calls. Its distinct acoustic qualities may justly explain our fear after hearing but not seeing a rattlesnake. The Rattlesnake song itself is jarring because of its use of dissonant and atonal sounds. In the end, we see that St. Vincent was likely expressing a true emotional response to a scary sound, which is also a conserved evolutionary response across distantly related species. 


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