The Snake Pit Organ
The snake pit organs
(sing. pit organ), or facial pits or labial pits, are unique sensory structures
found in crotaline and boid snakes that enable these animals to sense radiant
heat waves in the infrared (IR) region of the electromagnetic spectrum (Chen et al. 2012). Essentially, this sensory
system detects thermal radiation through infrared receptors located in the pit
organs and produces “heat images” of the surroundings that allows the snake to
detect and target endothermic (warm-blooded) prey (Krochmal et al. 2004). Until recently, prey
acquisition was established to be the only role of the pit organs and thus was
assumed to evolve for that purpose. However, recent studies suggest that the
pit organs are also utilized for behavioral thermoregulation (Krochmal et al. 2004).
Figure 1: Pit viper belonging to the Trimeresurus
genus (Left). Thermal image of a mouse; a common prey item of pit vipers
(Right).
Evolution
The pit organs is commonly considered to be an exclusive feature of a group
of snakes known as pit vipers, however similar structures (labial pits) have
also been discovered in some boid snakes (boas and pythons) (Krochmal et al. 2004). The pit vipers are members
of Crotalinae, a sub-family of Viperidae which include the venomous vipers, and
are distinguished from true vipers (Viperidae: Viperinae) by the presence of
the pit organs, hence pit vipers. Only some snakes from the Boidae
family, which include the nonvenomous boas and pythons, contain related pit
organ structures known as labial pits (Moon, 2011).
Figure 2: Phylogenetic relationships between members of the Viperidae
family. The asterix (*) indicates the origin of the pit organ.
According to a study conducted by Krochmal et al., the pit organs of pit vipers originated in Southeast Asia (Krochmal
et al. 2004). Although it is unclear
why these structures evolved, the pit vipers comprise approximately 75% of the
Viperidae family, suggesting that the evolution of the pit organs served a
vital purpose for survival (Greene, 1992). Molecular studies further describe a
series of mutations within proteins, which are responsible for the pit vipers’
acquired ability to sense infrared thermal radiation, that developed due to
Darwinian natural selection (Yokoyama et
al. 2011).
Several theories have been proposed for the evolution of the pit organ. One
theory suggests that these structures arose in response to large prey with
strong temperature contrasts, which would have conferred a detection advantage
to these snakes (Bakken & Krochmal, 2007). Another unsupported theory suggests
that these organs evolved as a defensive mechanism that would enable pit vipers
to act more efficiently during confrontations (Krochmal et al. 2004). A recent theory proposes that the organs not only
arose for prey detection, but also for behavioral thermoregulation that would
assist with measuring environmental temperatures and allow the snake to act
accordingly (i.e. find shelter during high temperatures) (Krochmal et al. 2004).
Anatomy
In pit vipers, a single large pit organ is located on each side of the
head between (and ventral to) the nostril and the eyes (Krochmal et al. 2004), whereas in boid snakes the
pit organs constitute several smaller pit structures that may line either the
upper lip, lower lip, or can be located in labial pits (Moon, 2011). It is
worth noting that pit organs may serve the same physiological function, however
their superficial appearance can differ according to the snake’s habitat
(Goris, 2011). The pit organ is located rostral (toward the rostrum or nose)
from the body in order to avoid detecting infrared heat waves coming from the
snake’s own body, thereby preventing the distortion of stimuli.
Figure 3: Red arrows indicate the superficial location of pit organs in
a python (boid snake) (top) and in a rattlesnake (pit viper) (bottom). Black
arrows indicate nostril openings.
The pit organ in pit vipers is comprised of several structures; the
outer and inner chambers, a thin membrane (or pit membrane), and a pore. The pit
membrane is suspended between the outer and inner chambers within the pit
cavity (Moon, 2011). The outer chamber is in direct contact with the exterior,
whereas the inner chamber interacts with the external air via the pore located
near the eye (Moon, 2011). Similar to the Eustachian tube in mammals, the pore
acts as an air pressure equalizer in the snake.
Figure 4: Pit organ structure of a crotaline snake. In the top image, N refers to the nostril, PO refers to the superficial pit organ,
and E refers to the eye.
Figure 6: Illustration of the
Crotaline pit organ.
Figure 5: SEM images of the Crotaline pit organ. Image A shows a light
micrograph of a cross-section through the pit (Bar = 10 µm). Image B shows the
surface appearance of the outer epithelial covering of the pit membrane (5 µm).
Image C shows the surface appearance of the oberhauchten cells on the inner
lining of the pit organ (note the pores) (Bar = 2.5 µm).
Within the pit membrane are the infrared receptor terminal masses, which
are responsible for detecting the thermal signatures (Amemiya et al. 1995). Furthermore, the outer and
inner chambers are lined by oberhauchten cells which are covered by pores that serve
to reflect electromagnetic wavelengths that may be detected by the infrared
receptors and subsequently distort the thermal image (Amemiya et al. 1995).
Figure 7: Innervation of the Crotaline pit organ. Three branches of the
trigeminal nerve innervate the pit organ. C
- cerebellum, E - eyeball (blue), IC - inferior colliculus, MO - medulla oblongata, N = nostril (green), OB - olfactory bulb, OT - optic tectum, P - Pit organ (red), SC
- spinal cord, V - trigeminal
ganglion
The pit membrane is directly innervated by three branches of the trigeminal
nerve, which further branches into roughly 7,000 infrared-sensitive sensory
axon endings that are distributed throughout the membrane and excite the nerve
when warmed (Moon, 2011).
The membrane is also highly vascularized, and the capillary beds project
throughout the terminal nerve masses (TNMs) supplying these masses with blood
for cooling, as well as energy and oxygen (Moon, 2011). The TNMs are arranged
into a single layer, and lies beneath the outer epithelium of the pit membrane.
Myelinated fibers innervate the TNMs at the farthest point from the outer
epithelium, and gradually become unmyelinated as the fibers form a sensory
array (Moon 2011).
Physiology
The trigeminal nerve branches (from the opthalamic and maxillary
ganglia) which innervate the pit membrane connect ipsilaterally (on same side
as pit organ) to the lateral descending nucleus of the medulla oblongata (Moon,
2011). This essentially connects infrared sensation to the brain.
Neurons from the TNMs are spontaneously depolarized at irregular
intervals due to constant infrared radiation that is emitted by surrounding
objects. These stimuli travel from the pit organ to the brain, which “filters”
out extraneous background stimuli, and is adapted to focus only on objects in
motion (Goris et al. 2007). The
frequency of the neuron firing is determined by the infrared radiation of the
stimulus compared to the background stimuli (Goris et al. 2007). An object which emits higher infrared radiation (i.e.
has a higher temperature) than its surroundings will cause the neurons in TNMs
to fire more rapidly, allowing the snake to “see” the object. Lower
temperatures will decrease the rate of neuron firing (Goris et al. 2007).
Figure 8: SEM of a single terminal nerve mass (TNM), viewed from the
inner chamber. Upper arrow indicates the point where the nerve branches into a
mass (unmyelinated at this point). Lower arrow indicates the single nerve fiber
(myelinated). Bar = 10 µm
1. Infrared radiation
(mid-wavelength to far infrared range) stimulated the infrared receptors found
on the pit membrane.
2. Stimulus is passed from the
receptors through the trigeminal ganglia and on to the medulla oblongata for
initial processing.
3. Information is then sent to the
reticularis caloris, which refines the thermal “image”.
4. Information is then sent to the
contralateral optic tectum, where neurons (that respond to infrared and visual
stimuli) form a stereoscopic image.
5. This visual information is then
sent to the thalamus, where other aspects (colour, motion) are defined, and the
final image is formed.
* Information obtained from Goris,
2011
Blood flow through the TNMs refines the thermal profiles that are sent
to the brain. Infrared radiation on the infrared receptors causes the TNMs to
signal to the pericytes in the pit organ for an increase in blood flow to the
pit membrane, possibly by using nitric oxide (vasodilator) (Goris et al. 2007). The pericytes then
mechanically controls the amount of blood flow to the pit membrane.
Termination
of the infrared stimuli signals a decrease in blood flow, cooling the membrane
and preventing any “afterimages” from forming (Goris et al. 2007). It is the variations in blood flow to the pit
membrane which helps the snake to see precise thermal images.
Function
The primary function of the pit organ is to aid in prey acquisition. Pit
vipers generally hunt at night (when visibility is low), and it is the use of
these facial pits that enable these snakes to detect, localize, and capture
their prey (Chen et al. 2012). They
hunt in cool foraging sites where infrared radiation is low, which causes any
endothermic animals in the area to contrast with their surroundings, allowing
the snake easily detect their prey (Bakken & Krochmal, 2007). Localization
of the prey is provided by both infrared input and visual input. It is the ability
of thermal images, provided by the pit organ, that allow the snake to strike
accurately and effectively (Van Dyke & Grace, 2010). Venom injected into
the prey will cause the animal to eventually die, and any bleeding will leave a
trail of infrared “bread crumbs” to the dead animal.
Figure 9: Thermal image of a
bird, in contrast with a cool background.
Another recently verified role of the pit organs is behavioral
thermoregulation (Krochmal et al.
2004). Snakes are cold-blooded animals, thus their body temperature are
dependent on the surrounding environmental temperature. Pit organs are capable
of detecting modest fluctuations in emitted thermal radiation, which enables
the snake to “sense” the surrounding surface temperatures (Krochmal et al. 2004). This allows the snake to
make a thermoregulatory decision, and seek shelter with the appropriate ambient
temperature (Krochmal et al. 2004).
For example, if the surrounding temperature is high, the snake would seek
refuge in a cooler region (Bakken & Krochmal, 2007).
Figure 10: Rattlesnake in the
shade.
Finally, these pit organs were also thought to play a defensive role against
predators, as they involved in conjunction with several defensive displays
(Greene, 1992). It is possible that the additional thermal information provided
by the pit organ would aid the snake in precise striking (Krochmal et al. 2004). It further suggests that
these snakes would rely on direct confrontation rather than escape. However, no
direct evidence has yet shown that the pit organs also serve an antipredator
role (Krochmal et al. 2004).
References
- Amemiya, F., Goris,
R., Masuda, Y., Kishida, R., Atobe, Y., Ishii, N., & Kusunoki, T. (1995).
The surface architecture of snake infrared receptor organs. Biomedical Research -Tokyo. 16(6):
411-421
- Bakken, G. S., & Krochmal, A. R. (2007). The
imaging properties and sensitivity of the facial pits of pitvipers as
determined by optical and heat-transfer analysis. Journal of Experimental Biology. 210(16):
2801-2810
- Chen, Q., Deng, H., Brauth, S. E., Ding,
L., & Tang, Y. (2012). Reduced Performance of Prey Targeting in Pit Vipers with Contralaterally
Occluded Infrared and Visual Senses. PLoS
ONE. 7(5)
- Goris, R. C. (2011). Infrared
Organs of Snakes: An Integral Part of Vision. Journal
of Herpetology. 45(1): 2-14
- Goris, R. C., Atobe, Y.,
Nakano, M., Funakoshi, K., & Terada, K. (2007). Blood flow in snake
infrared organs: Response-induced changes in individual vessels.
Microcirculation (New York). 14(2), 99-110
- Greene, H. W. (1992). The behavioral and ecological
context of pitviper evolution. In J. Campbell & E. Brodie, Jr. (Eds.), Biology of Pitvipers (pp.
107-117). Tyler, Texas: Selva.
- Krochmal, A. R., Bakken, G. S., & LaDuc, T. J.
(2004). Heat in evolution's kitchen: Evolutionary perspectives on the functions
and origin of the facial pit of pitvipers (Viperidae: Crotalinae). Journal of Experimental Biology. 207(24):
4231-4238
- Moon, C. (2011).
Infrared-sensitive pit organ and trigeminal ganglion in the crotaline snakes. Anatomy & Cell Biology. 44(1):
8-13
- Van Dyke, J. U., &
Grace, M. S. (2010). The role of thermal contrast in infrared-based defensive
targeting by the copperhead, Agkistrodon
contortrix. Animal Behaviour.
79(5): 993-999
- Yokoyama, S., Altun, A.,
& DeNardo, D. F. (2011). Molecular convergence of infrared vision in
snakes. Molecular Biology
and Evolution. 28(1): 45-48
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