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.