Monday, March 31, 2014

Seeking Field Assistants

Field assistants needed for my research - starting mid-May

Study on the antisnake behavior in California ground squirrels and its implications for hunting rattlesnakes

Location: Blue Oak Ranch Reserve, California (

Dates:  Middle of May through July (approx. May 15th-July 20th 2014)

Job description:  The Clark lab at San Diego State University is seeking motivated individuals to assist in a behavioral study on predator-prey interactions between northern Pacific rattlesnakes (Crotalus oreganus oreganus) and California ground squirrels (Otosperomphilus beecheyi).  Individuals will live and work with other field assistants at the Blue Oak Ranch Reserve in the foothills east of San Jose, California.  Assistants will help with capture and radio telemetry of rattlesnakes, implementation of fixed videography in the field, and behavioral experiments on wild animals. This a great opportunity to gain experience with trapping, marking and handling of animals, radio telemetry, GPS, videography, and other basic behavior and ecology field techniques.

Qualifications:  No experience necessary, but applicants with lab or field research experience will be given priority. On-the-job training will be provided.  Must be able to hike long distances over rough terrain carrying heavy equipment, conduct patient observations for long periods of time (up to 10 hours/day), and live in a remote wilderness area with primitive facilities. Must be able to work and live comfortably in variable environmental conditions including both cold/hot weather and in tick/mosquito habitats. Must be passionate about science, hardworking, independent, good-natured, love working in the outdoors, and able to share close living quarters with other researchers. Room and board (research facility fees and food) are provided, but interns will be required to sleep in tents for the entirety of the field season.

Application:  Please apply by April 15th. To apply, please send a cover letter and resume (including contact information for three references) detailing your experience with field biology, outdoor skills, and animal behavior to Bree Putman at: 

Tuesday, March 25, 2014

A Snake's Scavenger Hunt

The way you eat probably doesn't change much daily. Sure, you have to make a few decisions like whether you should go out, get delivery, or make food at home. You also must decide whether to eat with your hands or silverware, at the dining room table or on the go. But overall, your mode of eating generally consists of preparing a meal which you take approximately 10 minutes to consume while sitting down, and as with most things in life, there are exceptions to this rule (like Adam Richman of Man Vs. Food). 

This man is an exception to the "human foraging mode"

Unlike humans, snakes have two main foraging modes called ACTIVE and AMBUSH (or sit-and-wait). Active foraging consists of actively searching for and pursuing relatively immobile prey (e.g. sleeping or resting prey, or prey such as newborn animals). Ambush foraging consists of remaining at a hunting site for several hours to days to opportunistically attack prey that passes by. Active foragers generally have high endurance, but also high energy demands, while ambush foragers are low energy specialists, but have low endurance. 

Characteristics of the two main foraging modes in snakes

Browsing is also recognized as an alternative hunting mode in some snakes. For instance, Turtle-Headed Sea Snakes (Emydocephalus annulatus) in New Caledonia swim slowly searching for fish nest eggs in crevices along the ocean bottom (Shine et al 2004). A fourth foraging mode in snakes is less understood: SCAVENGING! Many people have described scavenging in snakes, but few have conducted formal studies on this interesting behavior (I could only find one during a quick literature search). Snakes are thought to employ scavenging opportunistically, eating carrion (dead decaying animals) only when chance allows. The one study I found showed that Western Diamondbacks (Crotalus atrox) were willing to consume mice that had been dead for 48 hours, but Black Rat Snakes (Elaphe obsolete) were not. The Diamondback rattlesnakes could even locate dead mice hidden within gravel (probably using their sense of smell).   


A review in 2002 by Devault and Krochmal found 39 published accounts of scavenging in snakes, which in total yielded 50 observations of this behavior. I’m sure that more than 10 years later, this number has increased. They found that pit vipers (snakes in the family Crotalinae) and piscivoruous snakes (those that eat fish) were most commonly reported as scavenging. Scavenging was also not limited to one prey type. What still remains unclear is what percentage of snakes’ total diet consists of scavenged carrion. This question is nearly impossible to answer with traditional snake diet studies that examine gut contents. As you can imagine, it is extremely hard to determine whether digested material in the gut came from freshly killed prey or carrion. One would need to literally observe a snake’s foraging behaviors 24/7 to answer this question.

The research we conduct in the Clark Lab attempts to expand our knowledge on rattlesnake (Crotalus oreganus) foraging behavior and diet with the use of fixed videography. Cameras overlooking snakes record their behaviors for prolonged periods of time, sometimes capturing rarely observed events. I am pleased to announce that this past summer (2013), we finally found a scavenging rattlesnake! Ironically, we did not discover this snake with our fixed video cameras, but by chance. Watch Iggy scavenging on my YouTube channel!

We found Iggy, a pregnant female northern Pacific rattlesnake on May 23rd at 11:46 am. She was scavenging a decapitated ground squirrel pup lying on the edge of a dirt road. She attempted to eat it several times over 7 minutes. She also dragged its body 16 meters from its initial location. Iggy had a hard time consuming the dead pup probably because it was missing its head, and snakes mostly consume their prey head-first. From our video recordings of her attempting to consume the pup, it seems that she was able to locate the anterior (front) region of the body, but could not get a good enough grip to start the consumption process. Eventually she gave up on it and slithered into the shade of a burrow.  

Devault TL, Krochmal AR (2002) Scavenging by snakes: an examination of the literature. Herpetologica 58:429–436.

Gillingham C, Baker E (1981) Evidence for Scavenging Behavior in the Western Diamondback Rattlesnake (Crotalus atrox). Zeitschrift fuer Tierpsychologie 55:217–227.

Lillywhite HB, Sheehy CM, Zaidan F (2008) Pitviper Scavenging at the Intertidal Zone: An Evolutionary Scenario for Invasion of the Sea. Bioscience 58:947–955.

Shine R, Bonnet X, Elphick MJ, Barrott EG (2004) A novel foraging mode in snakes: browsing by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae). Funct Ecol 18:16–24.

Wednesday, February 12, 2014

Rattlesnakes' Superpower: Seeing in the Dark

HAPPY DARWIN DAY! This post is a part of the Reptile and Amphibian Blogging Network’s (@RAmBlNetwork) Herps Adapt! event. 

RAmBlN is showcasing the remarkable evolutionary abilities of reptiles and amphibians by posting 1-2 blog posts per day starting Feb. 12th and ending on Feb. 16th.

My Feb. 12th counterpart is Bryan Hughes on rattlesnake crypsis.

Visit our webpage for more info! 

Your ability to see is a marvelous adaptation. In fact, your eyes are so amazingly complex that they are often used as an argument against Darwin’s theory of natural selection (just Google ‘eye against evolution’). However, saying a biological structure is too complex to have evolved is like saying God is too absurd to be real (both arguments are dumb, but let’s not start this debate here). In fact, the natural world is full of complex structures, including sensory systems even more amazing than the human eye (in my opinion). In honor of Charles Darwin, I write about a rattlesnake sensory superpower formed through thousands of years of evolution.

As you may have guessed from the title, this post will be about rattlesnakes' ability to detect electromagnetic wavelengths in the infrared (IR) range. Although some other animals can detect IR radiation – for instance, vampire bats use it to locate blood hotpots on mammals, and the beetle, Melanophila acuminata, uses it to locate forest fires where it lays its eggs in freshly charred conifer trees (Campbell et al. 2002) - snakes are the only known animals to form ‘visual’ images using the IR wavelength spectrum. Thus, they once again win in the animal kingdom badassness contest.

Sorry vampire bat and black fire beetle, your IR sensing capabilities are nothing compared to rattlesnakes 

*Disclaimer* - This entire post is a summary of the brilliant and easy-to-read review by Richard Goris. He has been working on this system for several years and I highly recommend reading the entire review.

Pathetic humans can only see light from 380-780 nm. Infrared light occurs at much longer wavelengths. 

Let us consider the selective pressures that led rattlesnakes to seeing IR radiation. What ecological problems led to this type of complexity? What is the adaptive value of this sense? How does it enhance overall fitness? These are the questions evolutionary biologists ask to understand the function of biological structures.

What are snakes’ ecological problems?
  1. Their regular vision is extremely limited at night, dawn, and dusk  
  2. Their field of vision is probably often obstructed by vegetation because they have a ground-view of the world

Rattlesnakes view the world from the ground up. Seems like it might be hard to see through all that thick grass!

Rattlesnakes hunt in ambush usually within some sort of cover, and usually at night, (or dawn and dusk) when the temperature is not too hot for them (remember they can’t regulate their own body temp). The ability to precisely target prey is critical for survival because the cost of losing a meal is great. Hence, seeing in the IR range could greatly improve snakes’ ability to detect prey under these 2 problematic conditions, and we get the evolution of a sensory structure unique to the animal kingdom: heat-sensing facial pits!

Squirrels normally blend into their surroundings (left image), but not when you can see in the IR range (right image)!

Not all snakes sense heat. Only some boas and pythons and all pit vipers have this superpower. Pit vipers are aptly named after their heat-sensing pits and include the rattlesnakes, cottonmouths, copperheads, and many Asian vipers (in the sub-family Crotalinae). I will only go into detail on the pit organ structure of pit vipers; boas and pythons are a bit different (they usually have multiple pits located on their labial scales, their 'lips').

(a) the pit organ of pit vipers is located in between the eye and nostril. (b) the pit functions similar to a pinhole camera - light (peach color) enters the outer chamber and stimulates membrane receptors.

Pit vipers have two pit organs, each in between an eye and a nostril on either side of the face (in what’s called the loreal region). The pit organ has three parts: an inner chamber and an outer chamber separated by a thin membrane. The membrane functions as a ‘retina’, detecting IR radiation that enters the pit. The pit receptors respond extremely rapidly to tiny changes in temperature thanks to their large number of mitochondria, more than that of any known sensory organ. Neurons in the pit fire rapidly when an object of higher temperature than the background enters the ‘field of view’, and the same neurons reduce their firing frequency when an object of lower temperature than the background enters the ‘field of view’. Thus, pit vipers can distinguish between warmer and cooler objects. Thanks to the work of Krochmal and Bakken, we now believe that heat-sensing snakes can not only see endothermic prey, but also ectothermic prey, such as amphibians and reptiles, using their infrared sense. The shape of the pit can be circular, triangular, rectangular, or slitlike depending on the species, and is usually oriented slightly downward in arboreal (tree-dwelling) species.

The morphology and size of the pits vary depending on the species' habitat, daily activity times, and diet. Some species have 
more angular pit organs while others have more circular organs.

The pit organs maximize the detection of wavelengths between 8,000 - 12,000 nm. These wavelengths correspond to the average temperature of mammal body heat (their prey). However, the pits are capable of detecting most of the electromagnetic spectrum, from the near ultraviolet to the microwave range. Thus, to maximize efficiency, they must fend off, weaken, or dissipate all unnecessary wavelengths. One solution to this problem is the presence of several depressions on the pit membrane. These disperse short wavelengths, while allowing free passage of longer IR wavelengths.  

Several pitlike depressions about a half micrometer in depth disperse short wavelengths of light and contribute to the efficient functioning of the pits. The surface of the pit membrane is covered with depressions, while the inner chamber is covered with domes that also have their surface covered with these depressions. Domes prevent back-scatter of IR rays. (taken from Goris 2011)

IR information is sent from the pit organ to the optic tectum of the brain. Visual information from the snakes’ eyes is also sent to this region. These two sets of information are mapped onto the surface of the optic tectum creating a composite image of the color ‘infrared’ in addition to the three primary colors (red, greenish-yellow, blue-violet) detected by the regular eyes. Thus, the pits essentially act as eyes except they have different sensory cells than the photoreceptor cells that pick up wavelengths in the visual spectrum.

In essence, pit vipers have four eyes (i.e. they create four information codes, two from the pits and two from the eyes) that are integrated in the brain to produce one single image of their environment. It is wrong to consider snakes’ pit organs as an independent sixth sense. Pits do everything eyes do, just a little differently, providing these snakes with enhanced vision.

"I see warm people" The pit organs are NOT a sixth sense.

The superpower of seeing in the dark makes rattlesnakes impressive predators, and could act as a strong selective pressure leading to antisnake adaptations in their prey. In fact, California ground squirrels have been shown to discriminate between heat-sensing rattlesnakes and heat-insensitive gopher snakes by increasing heat in their tails only when interacting (i.e. tail flagging) with rattlesnakes. The infrared illuminated tail of tail-flagging squirrels could either (1) provide the deceptive illusion of a larger, more formidable opponent, and/or (2) be a part of a multimodal signal that advertises information about the squirrel to the snake indicating a decreased likelihood of a successful attack. Both would deter snakes from striking. Hence, the infrared sensory system of rattlesnakes may have also shaped the evolution of a signal used by their prey, and the last chapter of my dissertation will test this assumption. 

In a laboratory arena, squirrels interacting with captive rattlesnakes heated their 
tails while squirrels interacting with gopher snakes did not. (taken from Rundus et al. 2007).

I am currently evaluating the function of squirrel tail heat by testing wild squirrel responses to staged gopher snake and rattlesnake encounters, and by testing wild rattlesnake responses to biorobotic ground squirrel presentations. I will resolve how snakes integrate this type of thermal information by decoupling tail heat from flagging using the biorobotic squirrel. I am extremely excited about this study because it will shed light on how prey use unique forms of communication to manage their predators’ hunting behavior. Check back regularly for updates on this work!

A biorobotic squirrel that I can control the tail flagging and heating of is used to understand whether snakes alter their 
hunting behaviors in response to squirrel tail heat. Biorobot with cool tail (middle) vs biorobot with hot tail (far right).

P.S. - Andrew Durso also wrote a blog post in 2012 on the IR sensing capabilities of snakes. Check out his version here.

Monday, December 9, 2013

Snakes and the Ecology of Fear

Fear is a common word and feeling associated with snakes. Ophidiophobia is one of the most shared fears of people worldwide. Although this post will not discuss the many proposed hypotheses for people’s fear of snakes, it will cover how fear can influence ecosystem processes. This post will mainly focus on rattlesnakes as predators – all statistics/facts I report are based on studies of North American rattlesnake populations.

Most people are afraid of snakes because of their nasty reputation which is propagated by the popular media. Snakes are deemed aggressive killers, and although many studies have demonstrated the docility of snake temperament, they are in fact killers. However, snakes are not killers of humans (less than 0.001% of all snake bites in the U.S. result in death), but killers of their small mammal prey. This makes our fear of snakes irrational, but small mammals have much to fear. This fear dictates how small mammals live their lives, often impacting whole ecosystems.

When predators chase and kill their prey they exert consumptive effects on the prey population

When people think of predators, they usually think of a predator chasing down and eating its prey. Direct killing events are important in maintaining prey population numbers, but a predator’s consumptive effects (those due to the direct killing and consumption of prey) on the ecosystem are usually nothing compared to its non-consumptive effects (those that do not result in the direct death of prey). For instance, a lioness can chase and take down one wildebeest, but the stampede of the wildebeest herd created by this chase may kill other wildebeest and other species (remember the Lion King stampede?), destroy vegetation, and induce a stress response in all animals involved that will persist long after the initial predation event.  

Involvement in a life-threatening predatory attack has been shown to enable rapid and enduring learning in prey species, to induce physiological stress significant enough to impair the day-to-day activities of prey, and to drastically affect the functioning of food chains in the ecosystem. Such non-consumptive predatory effects are collectively called the Ecology of Fear. Here, I will discuss how the stress responses of prey to their predators affect many aspects of their lives, and how rattlesnakes can be used as model predators to study stress in wild small mammal populations. 

First, let’s define what a stressor is. A stressor is any stimulus that either directly threatens an animal’s survival or is perceived to do so. Fear-induced stress is psychological and occurs when a stimulus is perceived by an animal as threatening through evaluation by the cognitive regions of the brain. Cues that indicate predator presence can invoke fear-induced stress.

The stress response pathway starts in the brain at the hypothalamus which releases CRH (corticotropin-releasing hormone) into the pituitary. This stimulates the pituitary to release ACTH (adrenocorticotropic hormone) into the blood stream. ACTH stimulates the adrenal glands to produce stress hormones (corticosteroids). Corticosteroids create the physiological responses we feel to stress and influence our behaviors. The is normally called the HPA-axis. 

We also must keep in mind that not all stress is bad. In fact, the stress response pathway evolved to help animals cope with fluctuations in their environment. Most people believe that stress starts to have negative health effects only when it persists for too long. However, whether prolonged exposure to predators causes long-term negative impacts on prey populations is still debatable. It is proposed that although the stress response of prey to predators alters the prey’s immediate health, the long-term response is adaptive.   

When exposed to predators, prey alter their day-to-day activities. For example, they may forgo feeding in food patches where they usually consume high energy food, and instead feed in low energy food patches. Predator presence not only limits where prey can feed, but can also cause fear-induced stress that increases prey metabolic rate (breathing rate) which accelerates the rate at which prey use energy. So prey burn a lot of energy, but cannot access the food to replace this lost energy because they are afraid of predators. If this cycle persists long enough, prey body condition can drastically decrease and could result in death by starvation.   

Prey may also forgo mating or have lower reproductive success when predators are perceived to be present. Several studies have shown that females of different species of animals exhibit lower birth rates or litter sizes when in a state of fear-induced stress. Forgoing mating is considered adaptive if it is better for prey to wait to have babies after the amount of predators in the area has declined. This is called predator-induced breeding suppression.

Older yellow-belled marmot mothers that exhibit high levels of stress hormones produce significantly smaller litters than mothers with low levels of stress hormones (as seen by the graph). Taken from Monclus et al. (2011).

I have just mentioned only two of a myriad of ways that predators affect prey other than direct consumption. The non-lethal effects of predators make up a major field of research right now, and studies on these effects have been influential in understanding stress-related diseases in humans, like PTSD (post traumatic stress disorder). However, there are several problems with many of these predator-prey studies. First, most studies are conducted in a controlled laboratory environment and as several papers have pointed out, results found in the lab don’t always translate well to wild animal populations. Second, the few studies on wild animal populations that do exist do not actually know the exact locations of their predators, or how predators behave in response to their prey. An index of predator density is usually estimated through monitoring surveys (traps and wildlife cameras), and this index is correlated to the stress levels of wild prey populations. Wild prey responses to actual predators are almost never examined. Studies that use rattlesnakes as model predators may provide answers on whether prey exhibit fear-induced stress when actively confronting a real predator.   

Why are rattlesnakes model predators for predator-prey studies? Let me tell you.
  1. These snakes are large-bodied and amenable to implantation of radio transmitters. Radio transmitters emit a radio wave that can be picked up by a receiver, allowing researchers to track the exact location of individual snakes. Thus, we can know where snakes implanted with transmitters are at all times.
  2. Rattlesnakes are sit-and-wait ambush hunters that remain at a hunting site for hours to days waiting for unsuspecting prey to pass them by. This is great because once we know where a snake is, we know it’s going to be there for a while. We can monitor a snake’s location and see how prey respond to it. Since rattlesnakes have low endurance and do not chase their prey, their prey are also more willing to inspect them.
  3. Rattlesnakes are not easily disturbed by human observers, usually relying on camouflage to blend into their surroundings. Thus, researchers including myself have figured out that one can easily set up fixed video cameras overlooking snakes to record when they interact with prey.
  4. Researchers can easily restrain rattlesnakes in the field when they want to present a live predator to specific individuals of wild prey. Most studies are only able to use predator cues such a scent, or models/replicas of predators to elicit prey responses.


Photos of the typical ambush posture of hunting rattlesnakes (which consists of a tightly coiled body), and the wireless network security cameras we use to record natural rattlesnake behaviors.

Because of the abovementioned qualities of rattlesnakes, we can use them to more easily study fear-induced stress in wild prey. For instance, we can present a restrained rattlesnake to focal prey individuals, and examine how long each individual's stress response persists after discovering the snake. If prey experience prolonged stress after encountering a snake, they may reduce time spent on other important activities such as feeding or mating, as mentioned previously. This could have ecosystem level consequences. For example, ground squirrels create burrow systems that are widely used by many different animals in their ecosystem. If squirrels are greatly concerned with avoiding snake predators, they may reduce time spent on burrow construction, limiting the amount of available burrows to others in the area. We are currently conducting these types of studies on wild ground squirrel populations in California. 

As in previous studies, we can examine how the density of rattlesnakes in an area affects their prey’s stress response. Most studies have examined how mammalian or avian predators affect prey populations. An important distinction between these two predators and rattlesnakes is that rattlesnakes are ectothermic, or ‘cold-blooded’, while mammals and birds are endothermic, or ‘warm-blooded’. Cold-blooded animals are often found at much higher densities in an ecosystem than warm-blooded animals. Because rattlesnakes occur at higher densities than large mammalian carnivores, their effects on shared prey are likely different. For instance, theory suggests that prey should not mount strong defensive responses to predators when they encounter predators too often. Thus, prey may not respond to rattlesnake populations as strongly as mammalian carnivore populations. 

Finally, rattlesnakes also exhibit distinct activity seasons as a consequence of being ‘cold-blooded’. When the climate becomes either too hot or too cold they ‘hunker down’ in a refuge, patiently waiting for the bad weather to pass. Their prey may acknowledge times when snakes are inactive and exhibit changes in their activities and stress response pathway. For instance, prey may take advantage of cold days (when snakes are incapable of a lot of activity) by feeding/mating more. An increase in prey behaviors may be correlated with changes in stress hormone levels.      

The Ecology of Fear is an exciting field of research from which we can not only learn a lot about wild animal responses to predators, but also our own responses to traumatic events. Few studies have examined the fear-induced effects of snake predation even though rattlesnakes are model predators for such studies. I hope that my research along with research from others will advance our knowledge on this topic. 

This post was inspired by a special feature on the ecology of stress in the journal, Functional Ecology, published this year. I took several of my examples from two particular papers in this special feature and am grateful for these authors' review of the literature:

Other resources used in this post:

This post is also a part of the first herpetology blog carnival organized by a network of students, naturalists, and professionals whose goal is to use social media to communicate information about amphibian and reptile natural history, science, and conservation. Our inaugural event is inspired by the Year of the Snake, and so we are writing blog posts about the diversity of ecosystem services provided by snakes. We encourage everyone to follow us on Twitter using #SnakesAtYourService. We hope this social media event will be the first of many that touch on different themes related to the importance of amphibians and reptiles.

'Snakes At Your Service'  participating blogs and authors: