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Tuesday, September 29, 2015

Can snakes hear?

This post will soon be available in Spanish.

Last month I wrote about whether snakes sleep, a topic that is far more interesting than the minuscule amount of research devoted to it. Another common question is whether snakes can hear, since they don't have external ear openings. The short answer is yes, snakes can hear, but the long answer is (as usual) more complicated. Happily, there is a good deal of research on this question, including a recent review. In general, many popular sources and some scientific ones have incorrectly claimed snakes to be deaf, whereas a plethora of behavioral, neurological, and physiological experiments, particularly those performed by the eminent Princeton hearing researcher Ernest Glen Wever in the 1960s and 70s, by UC-San Diego neurologist Peter Hartline in the 1970s, and by herpetologist and anatomist Bruce Young from the 1990s to the present, have conclusively shown that snakes can detect and respond to sounds.

Anatomy of the human ear
Most tetrapods have a three-part ear (outer, middle, and inner) that is useful for detecting airborne sounds. The boundary between the outer and middle ear is called the tympanic membrane or "ear drum", and its function is to convert airborne sounds from the outer ear into fluid-borne ones in the inner ear1, by way of one or more middle ear bones. Sounds are ultimately converted by auditory hair cells called stereocilia into nerve impulses, which travel to and are interpreted by the brain. At many stages along the way, the sounds are amplified by the vibrations they produce in the different parts of the ear, including the middle ear bones (more on these in a minute). It's been suggested that this three-part system evolved (possibly multiple times) around the beginning of the Triassic Period, in concert with the evolution of sound production in insects, the probable prey of many early amniotes. Many modern animals, such as songbirds, bats, dolphins, humans, frogs, and crocodilians, have very sensitive hearing that can detect extremely quiet airborne signals in spite of the presence of other competing noises.

Micro-CT scan of a ball python's skull and ear.
Red: mandible; dark blue: quadrate;
green: columella; purple/light blue: inner ear chambers

From Christensen et al. 2012
You're probably familiar with the three bones of the middle ear in mammals, the malleus, incus, and stapes (also known as the hammer, anvil, and stirrup). Snakes and other reptiles have only a single middle ear bone, which is usually called the columella, although it is homologous with the mammalian stapes. The malleus and the incus evolved from the articular and quadrate bones in the lower jaw of early mammal-like reptiles, leaving modern mammals with a single lower jaw bone, the dentary. Modern reptiles still have three bones in their lower jaws, where they play a role in detecting vibrations, particularly those propagating through the ground. Most modern lizard ears are essentially like those of modern mammals, with a small external ear leading to a large ear drum close to the body's surface, which passes sound from the air (or the jawbones) to the columella and thence to the inner ear. In contrast, snakes lack all traces of an outer ear as well as an ear drum. Instead, a snake's columella is in direct contact with, and picks up vibrations from, its quadrate bone (the dark blue bone in the diagram above). You might suspect that this arrangement would only be useful for detecting ground-borne vibrations, and you'd be partially right: snakes are exquisitely sensitive to ground-borne vibrations. But, they can also detect airborne sounds.2

Diagram of the ear of a watersnake (Nerodia)
Modified from Wever 1978
Both older and several more recent experiments suggest that snakes can hear the vibrations produced by airborne sounds. Physiological data suggest that they are able to detect certain airborne frequencies directly using the inner ear, although the specific bioacoustic mechanisms remain poorly known. Instead, most airborne sounds are probably detected in using "somatic hearing". This happens when airborne sound waves strike a snake's body  and some of their energy is transferred to its bones, tissues, and organs, particularly the head and lung. The snake's vibration-sensitive hearing system can then pick up on and translate the vibrations from the rest of its body into fluid-borne vibrations and, ultimately, nerve impulses. So a snake probably can't hear, say, most music3 or human speech directly, but it can hear the sound of its own body vibrating in response to those sounds. So, instead of being deaf, snakes essentially have two auditory systems that are at least peripherally distinct. Whether signals from these two systems are integrated into a single neural pathway, as is the case for the eye and the pit organ, or whether they serve different functions, remains to be studied and determined.

The length and arrangement of the auditory hairs in the inner ears of snakes appears to be fairly uniform across species, at least relative to the variation seen in lizards, which can have very different auditory hair anatomy among families and often even among closely-related species. Snakes mostly have simple, tuatara-like papillae, which suggests that they have secondarily lost a more complex type of auditory organ. This might be due to the aquatic or burrowing lifestyle of their ancestors and/or to specializations of their lower jaws in response to their unusual eating habits. There is some variation in inner ear anatomy (and presumably in hearing capacity) among snakes: burrowing snakes have the longest papillae, arboreal snakes the shortest, and terrestrial snakes have papillae of intermediate length. Many mammals have over 10,000 auditory hair cells, whereas most snakes have only about 250 (although acrochordids have nearly 1,500). Supporting cells of unclear function are relatively more numerous in snakes and these cells have ultrastructural features that suggest that they are more specialized than those of other reptiles.

Hearing range of various animals, not including snakes
The louder and lower frequency airborne sounds are, the more easily a snake can detect them. This isn't entirely unlike our own hearing—although we do hear high-pitched airborne sounds directly more easily than snakes do, we also rely on amplification provided by our ear drums, inner ear hairs, and other parts of our bodies. Studies have shown that snakes can hear sounds in the 80-600 Hz range optimally, with some species hearing sounds up to 1000 Hz (for comparison, the range of human hearing is from 20-20,000 Hz). This means that a snake could hear middle C on a piano, as well as about one octave above and two below, but neither the lowest key (which is 27.5 Hz) nor the highest (which is 4186 Hz). The average human voice is around 250 Hz, which means that snakes can hear us talking as well. Of course, there is likely a lot of variation among snake species, and the hearing of most species has not been examined, so these are generalizations.

Use the player below to hear how the airborne parts of Led Zeppelin's classic "Good Times, Bad Times" would sound to a snake. Parts of the song below 80 Hz (some bass & drums) or above 600 Hz (almost all guitar, vocals, and cymbals) have been muted. This doesn't include their sensitivity to the groundborne vibration parts of the song, which you could simulate by turning the bass on your speakers all the way up.

Audibility curves for living reptiles, including birds (left). The lower
the curve, the quieter a sound can be detected at a given frequency.
You can see that snakes cannot hear very quiet sounds, but
otherwise are not that much worse than other reptiles
(although their hearing sucks compared to, say, owls).
Note the different y-axes. From Dooling et al. 2000.
What do snakes do with their hearing? Unlike frogs, birds, and insects, snakes don't seem to use sound for communication with each other. Although many snakes hiss and some use tail rattling, growling, scale rubbing, or cloacal popping to send messages to their would-be predators, these sounds are mostly above 2,500 Hz, so the snakes themselves cannot hear them. Some species are capable of producing sounds whose frequency overlaps with their hearing range, such as the loud, robust hisses of pinesnakes and gophersnakes (Pituophis), the bizarre and intimidating growling sounds of king cobras (Ophiophagus), and the famous rattles of some large rattlesnakes (Crotalus). Some people have suggested that rattlesnakes find their hibernacula by following the rattling sounds of other rattlesnakes, but this idea has been disproven because the power output of rattling is insufficient to serve as a long-distance signal, and playback experiments have not yielded a behavioral response to rattling.

Snakes might eavesdrop on the alarm calls of other, more vocal animals, as some lizards do with bird alarm calls, but probably not since most of these calls are between 2,500 and 10,000 Hz, well above their optimal frequency range. Most likely, snakes use their hearing to monitor their environment for sounds produced by approaching predators or prey, many of which are ground-borne vibrations. Snakes can hear in stereo and can use their hearing to determine the directionality and thereby the sources of sounds. One genus of snakes that probably relies quite heavily on vibration to hunt are Saharan sand vipers (Cerastes). These snakes ambush lizards and rodents from a position partially or completely buried in sand. Experiments have shown that their reliance on chemosensing and thermal cues was minimal and that, although snakes with their eyes obscured had altered strike kinematics, they were still able to capture prey.

1 This is necessary because "hearing" evolved under water. Many fishes and fully aquatic amphibians (such as amphiumas) have a network of hair-like cells all over their body, which is called a lateral line system. The lateral line allows them to sense water-borne vibrations using their entire body like one big eardrum. When early amniotes emerged onto land, the inner ear was still adapted to detecting fluid-borne vibrations, and the eardrum and outer ear evolved to facilitate collection of airborne sounds and translation of them into fluid-borne ones. These adaptations were further refined as amniotes began to hold their bodies off the ground (lizards, mammals) or fly (birds), minimizing their ability to pick up ground-borne vibrations with their ears. Snakes probably have a better capacity to pick up ground-borne vibrations than most amniotes, since at least some part of their body is in contact with the ground (or a tree) most of the time. To date, no one has examined hearing in fully aquatic snakes.

2 Many burrowing and aquatic amniotes have lost their external ear opening, because their need to detect airborne sounds is minimal, they can rely mostly on ground-borne vibrations, and their middle/inner ear could be damaged during burrowing or swimming if it was exposed. 
Amphisbaeneans and other lizards lacking external ears hear mostly ground-borne vibrations, which makes sense considering that many of them are fossorial and spend most of their lives with most of their bodies in contact with the ground. Amphisbaeneans have lost more of their airborne sound detection capacity than most burrowing lizards, in that, like snakes, they have also lost their tympanum and have their columella connected directly to their lower jaw (some naked mole rats have a similar jaw-middle ear connection and rely heavily on vibrational communication). One leading hypothesis suggests that snakes evolved from burrowing ancestors, and another suggests that they evolved from aquatic ancestors, so perhaps snakes lost and then regained an ability to hear airborne sounds. Other limbless squamates, such as pygopod geckos, specialize in making high-frequency vocalizations and have sensitive hearing to match.

3 At least two studies have investigated whether cobras can hear the music played by snake charmers, and concluded that cobras are responding to tactile and visual stimuli, not auditory.


Christensen, C. B., J. Christensen-Dalsgaard, C. Brandt, and P. T. Madsen. 2012. Hearing with an atympanic ear: good vibration and poor sound-pressure detection in the royal python, Python regius. The Journal of Experimental Biology 215:331-342 <link>

Clack. J.A. 1997. The evolution of tetrapod ears and the fossil record. Brain, Behavior, and Evolution 50:198-212 <link>

Dooling, R.J., R.R. Fay, and A.N. Popper. 2000. Comparative Hearing in Birds and Reptiles. Springer, New York, NY, USA <link>

Dooling, R. J., Lohr, B., & Dent, M. L. 2000. Hearing in birds and reptiles. Pp. 308-359 in Comparative Hearing in Birds and Reptiles. Ed. by Robert J. Dooling, Richard R. Fay, and Arthur N. Popper. Springer New York <link>

Friedel, P., B. A. Young, and J. L. van Hemmen. 2008. Auditory localization of ground-borne vibrations in snakes. Physical Review Letters 100:48701 <link>

Fuong, H., Keeley, K. N., Bulut, Y., & Blumstein, D. T. 2014. Heterospecific alarm call eavesdropping in nonvocal, white-bellied copper-striped skinks, Emoia cyanura. Animal Behaviour, 95:129-135 <link>

Hartline, PH. 1971. Physiological basis for detection of sound and vibration in snakes. Journal of Experimental Biology 54:349-371 <link>

Ito, R., & Mori, A. 2010. Vigilance against predators induced by eavesdropping on heterospecific alarm calls in a non-vocal lizard Oplurus cuvieri cuvieri (Reptilia: Iguania). Proceedings of the Royal Society of London B: Biological Sciences, 277:1275-1280 <link>

Köppl, C., Manley, G. A., Popper, A. N., & Fay, R. R. 2014. Insights from Comparative Hearing Research. Springer New York <link>

Manley, G. A. 2012. Peripheral hearing mechanisms in reptiles and birds (Vol. 26). Springer Science & Business Media <link>

Manley, G. A., & Fay, R. R. (Eds.). 2013. Evolution of the Vertebrate Auditory System. Springer Science & Business Media <link>

Wever, E. G. 1978. The Reptile Ear: Its Structure and Function. Princeton: Princeton University Press <not available online>

Wever, EG and JA Vernon. 1960. The problem of hearing in snakes. Journal of Auditory Research 1:77-83 <not available online>

Young, B. A. 1997. A review of sound production and hearing in snakes, with a discussion of intraspecific acoustic communication in snakes. Journal of the Pennsylvania Academy of Science 71:39–46 <not available online>

Young, B. A. 2003. Snake bioacoustics: toward a richer understanding of the behavioral ecology of snakes. The Quarterly Review of Biology 78:303-325 <link>

Young, B. A., & Aguiar, A. 2002. Response of western diamondback rattlesnakes Crotalus atrox to airborne sounds. Journal of Experimental Biology 205:3087-3092 <link>

Young, B. A., & Morain, M. 2002. The use of ground-borne vibrations for prey localization in the Saharan sand vipers (Cerastes). Journal of Experimental Biology 205:661-665 <link>

Young, B. A., N. Mathevon, and Y. Tang. 2014. Reptile auditory neuroethology: What do reptiles do with their hearing? Pages 323-346 in C. Köppl, G. A. Manley, A. N. Popper, and R. R. Fay, editors. Insights from Comparative Hearing Research. Springer, New York <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Monday, August 31, 2015

Do snakes sleep?

This article will soon be available in Spanish.

Do snakes sleep? Do they dream? These may seem like obvious questions, especially since almost every species of mammal, bird, reptile, amphibian, fish, and invertebrate studied has been found to exhibit some kind of resting phase. But sleep is hard to study in snakes, at least in part because they seem never to close their eyes. Consequently, there is shockingly little research on sleep in snakes. A Google Scholar search for the terms "snake+sleep" returns papers about venomous snakebites to sleeping victims, sleepwalkers dreaming about snakes, and papers by Stanford geophysicist Norman H. Sleep on the geology of the Snake River in Idaho. But, despite the dearth of research, I promise this post won't be too much of a snooze...

Human EEG "brainwaves"
Sleep is a behavior that involves an immobile posture, decreased responsiveness to arousing stimuli such as noise and light, and rapid reversibility (the ability to quickly "wake up", as distinct from hibernation or a comatose state). The physiological criterion most frequently used to define sleep is the slowing down of "brain-waves" on an EEG. An EEG (electroencephalogram) measures electrical activity in your brain, which is caused by your brain cells talking to one another. Brain activity, which happens even during sleep, appears as wavy lines on an EEG recording, hence brain 'waves'. When mammals and birds are sleeping, they exhibit two alternating patterns of EEG activity: 1) slow-wave sleep (SWS, also called synchronized, quiet, or non-REM sleep), which is characterized by high amplitude (75-400 μV), low frequency (0.5-4 Hz) EEG waves, and 2) "paradoxical" sleep (PS, also called desynchronized, active, or REM sleep), which is characterized by low voltage (5-10 μV), high frequency (13-30 Hz) EEG waves that are physiologically more like those in awake animals (hence the name "paradoxical"). In humans and cats, paradoxical sleep is associated with rapid-eye movement (REM, measured by electro-oculography or EOG), complete muscle relaxation (measured by electromyography or EMG), muscle twitching, irregular breathing/heartbeat, and, in humans at least, with dreaming.

Lizards wearing EEG-recording equipment while awake and asleep
From Flanigan 1973
Although sleeping patterns are enormously variable across the animal kingdom, most mammals and birds tested exhibit both SWS and PS, or variations on that theme. In some basal mammals and birds (echidnas, platypus, ostriches), eye movement and relaxed muscle tone are associated with both quiet and active sleep. Periods of rest or quiescence associated with EEG changes similar to those seen in mammalian sleep are clearly present in turtles and in crocodilians, but EEG data suggest that these animals do not exhibit REM sleep. Some experiments have found REM-like sleep in lizards, whereas others have not. Experiments in which lizards, turtles, and crocs were subjected to continuous arousal for 24-48 hours showed that they spent more time sleeping afterwards and that their brains produced more high-voltage spikes. Tortoises given the drug atropine, derived from the mandrake plant and used to produce deep sleep in humans since at least the fourth century B.C.E., also produced more spikes, suggesting that EEG spikes are in fact analogous signs of quite sleep in reptiles and mammals. Interpreting EEG data is complicated because SWS waves differ between mammals and reptiles, perhaps because reptile and mammal brains differ in structure, particularly with respect to the neocortex, the source of these waves in mammals. Furthermore, some reptiles sometimes seem to exhibit sleep-like brain activity when they are awake, perhaps because ectotherms basically fall asleep when they get cold.

Waking (top) and sleeping (bottom) python EEG
and EMG waves. From Peyrethon & Dusan-Peyrethon 1969
The single study of a snake was done by French comparative sleep researchers J. Peyrethon and D. Dusan-Peyrethon, who also studied sleep in fish, caimans, cats, and mice in the 1960s at the Laboratoire de Médecine Expérimentale in Lyon. They used EEG to monitor the brainwaves of a four-foot African Rock Python (Python sebae) over two days. They reported that sleep-like brain waves were produced almost 16 hours a day, increasing to over 20 hours following feeding, and that these brainwaves corresponded with slower breathing and heart rate, some muscle relaxation, and perhaps a lowered behavioral response threshold. They did not see any evidence for active sleep in the EEG. As far as I can tell, this is the only study ever conducted on sleep in a snake.

Snakes do have circadian rhythms, and many snakes are active only at particular times of day. Racers (Coluber), hog-nosed snakes (Heterodon), patch-nosed snakes (Salvadora), and sipos (Chironius) are strictly diurnal, whereas aptly-named nightsnakes (Hypsiglena), broad-headed snakes (Hoplocephalus), and kraits (Bungarus) are strictly nocturnal. But many snakes do not fit nicely into these categories. Good examples include ratsnakes (Pantherophis) and many vipers, but many other snakes may be active at any time of the day or night, depending on the time of year, so it's hard to predict when or for how long they might be expected to sleep. You often observe snakes exhibiting sleep-like behavior, sitting in one spot for hours, days, or even weeks at a time, like the Puff Adder (Bitis arietans) in the video at left. But the thing is, that snake is actually foraging. A viper might sit motionless for many days, such a long time that if a mammal exhibited that same behavior, we might think it was sick or dead! But in fact this is how many snakes forage for prey, hyper-alert to their immediate surroundings, ready to ambush, strike, and envenomate small animals that stray too close. Do they sleep when they are waiting, or are they awake the entire time? Radio-telemetry studies of bushmasters (Lachesis muta) in the wild suggest that they might have strict cycles of attentiveness, "awesomely alert during darkness and almost as if drugged by day", with relatively abrupt transitions each way. On the other hand, many marine mammals and migratory birds do not seem to sleep for long periods of time without suffering any obvious consequences. When engaged in constant activity, these animals close one eye and sleep one half of their brain at a time. Other animals, including perhaps some lizards, sleep one hemisphere at a time in contexts of high predation risk. Might snakes that use sit-and-wait foraging strategies do something similar?

I photographed this Sonoran Lyresnake (Trimorphodon lambda)
during the day, but it was found at night. Their skinny slit-like
pupils enhance their night vision, making distant
objects sharper by increasing the depth of field,
like using a small aperture on a camera lens.
If lyresnakes sleep, it's probably during the day.
How would a researcher tell if a snake was sleeping? Snakes never close their eyes. Or, more accurately, their eyelids are always closed, but they are covered by clear scales. Either in the wild or in captivity, observations of snakes seeming to "wake up" (implying that they were sleeping) are rare: motionless snakes rarely twitch, and other signs of PS are either normal for snakes (such as irregular breathing/heartbeat) or anatomically impossible (REM). You could imagine a series of experiments where an experimenter used EEG and high-speed infrared videography to record the brainwaves and behavioral responses of snakes to arousing stimuli. What stimuli to use is an open question, since snakes don't necessarily respond to bright lights or loud noises even when they're awake. Because snakes inhabit a primarily chemosensory world, it might be possible to wake one up using a smell. The human experience would suggest that the onset of chemosensory signals is inherently too gradual to really be surprising, but this might or might not be true for snakes. What about the infrared sense of some snakes? Could a bright infrared light wake them up? Can snakes see when they're asleep? What would that even be like? Only further studies will tell for sure.

So here's what we know: snakes probably do sleep, perhaps most of the time, but we don't really know when, for how long, how deeply, or whether or not they have paradoxical sleep, including dreaming. Sleep patterns are probably quite diverse across the >3500 species, of which only one has been examined. Many snakes do yawn, but this has been interpreted either as a means to gather chemical cues or to reposition musculoskeletal elements, in contrast with the hypothesized functions of yawning in humans (possibly regulating brain temperature, causing increases in blood pressure, blood oxygen, and/or heart rate in order to improve motor function and alertness, or as a social cue). Sleep is such a basic element of human biology, so if you ask me, the subject of sleep in snakes, and broader questions about the diversity, evolution, and function of sleep across the animal kingdom, should be keeping researchers awake at night.


Thanks to Kendal Morris for suggesting this question, and to Harry Greene, David Cundall, and Gordon Burghardt for sharing their observations.


Ayala-Guerrero, F., & Huitrón-Reséndiz, S. 1991. Sleep patterns in the lizard Ctenosaura pectinata. Physiology & Behavior 49:1305-1307 <link>

Bauchot, R. 1984. The phylogeny of sleep in vertebrates [birds, reptiles, amphibians, fish]. Annee Biologique (France) 23:367-392 <link>

Brischoux, F., Pizzatto, L., & Shine, R. 2010. Insights into the adaptive significance of vertical pupil shape in snakes. Journal of Evolutionary Biology 23:1878-1885 <link>

Campbell, S. S., & Tobler, I. 1984. Animal sleep: a review of sleep duration across phylogeny. Neuroscience & Biobehavioral Reviews 8:269-300 <link>

De Vera, L., González, J., & Rial, R. V. 1994. Reptilian waking EEG: slow waves, spindles and evoked potentials. Electroencephalography and Clinical Neurophysiology 90:298-303 <link>

Flanigan, W. F. 1973. Sleep and wakefulness in iguanid lizards, Ctenosaura pectinata and Iguana iguana. Brain, Behavior, and Evolution 8:417-436 <link>
Greene, H. W., & Santana, M. 1983. Field studies of hunting behavior by bushmasters. Estudios de campo del comportamiento de caza por parte de las cascabelas mudas. American Zoologist 23:897 <link>.

Hartse, K.M. and A. Rechtschaffen. 1974. Effect of atropine sulfate on the sleep-related EEG spike activity of the tortoise, Geochelone carbonaria. Brain, Behavior, and Evolution 9:81-94 <link>

Libourel, P. A., & Herrel, A. 2015. Sleep in amphibians and reptiles: a review and a preliminary analysis of evolutionary patterns. Biological Reviews <link>

Peyrethon, J., & Dusan-Peyrethon, D. 1969. Etude polygraphique du cycle veille-sommeil chez trois genres de reptiles. CR Soc Biol (Paris) 163:181-186 <not available online>

Rattenborg, N. C. 2006. Do birds sleep in flight? Naturwissenschaften 93: 413-425 <link>

Roe, J. H., Hopkins, W. A., Snodgrass, J. W., & Congdon, J. D. 2004. The influence of circadian rhythms on pre-and post-prandial metabolism in the snake Lamprophis fuliginosus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 139:159-168 <link>

Siegel, J. M. 2008. Do all animals sleep? Trends in Neurosciences 31: 208-213 <link>

Siegel, J. M., Manger, P. R., Nienhuis, R., Fahringer, H. M., Shalita, T., & Pettigrew, J. D. 1999. Sleep in the platypus. Neuroscience 91: 391-400 <link>

Tauber, E.S., J. Rojas-Ramirez, and R. Hernandez-Peon. 1968. Electrophysiological and behavioral correlates of wakefulness and sleep in the lizard (Ctenosaura pectinata). Electroencephalography and Clinical Neurophysiology 24:424–443 <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Tuesday, July 7, 2015

Snakes that decapitate their food

This article will soon become available in both Spanish!
Este artículo se convertirá pronto disponible en español!

Click here to read this article in Japanese

Crab-eating Snake (Fordonia leucobalia) eating a crab
A few years ago I wrote an article about southeast Asian crab-eating snakes, the only snakes (at the time) known to break apart their food instead of swallowing it whole. Although I ended that article by wondering how many more strange snake dietary adaptations we might discover, I didn't actually anticipate writing a sequel to that article—it was so unique that the BBC filmed it for their series Life in Cold Blood, and I doubted that anyone would discover another snake that tore apart its prey. You can imagine my surprise when recently I was asked to review a paper about another snake that breaks its food apart! I was also delighted that this snake was a scolecophidian, because I feel that they are underrepresented both on this blog and in snake biology in general. It is a bit unsatisfying that it is the Brahminy Blindsnake (Indotyphlops braminus, formerly known as Ramphotyphlops braminus), the best studied scolecophidian by far by virtue of its enormous range and unusual breeding habits, but I think this exciting discovery could become extended to some or most of the other >400 species of blindsnakes.

A blindsnake with decapitated termite heads
stuck to the back of its head
Late last year, herpetologist Yosuke Kojima, a postdoctoral researcher at Kyoto University, and entomologist Takafumi Mizuno, a graduate student at Kyoto Institute of Technology, made a chance finding. They had been close friends since elementary school and shared an interest in behavioral and chemical ecology. Together, they planned some experiments to learn more about interactions between blindsnakes and their primary prey, ants. Mizuno's lab also kept colonies of termites (in this case, Reticulitermes speratus), which are also eaten by blindsnakes. Blindsnakes are unusual in that they eat many small prey at a time rather than a few large prey infrequently. Blindsnakes often eat 20 or more prey items at a time, and the maximum number of prey items ingested by a single individual is 1,431 for Anilios (Ramphotyphlops) nigrescens from Australia. Because blindsnakes often gorge themselves when feeding in an ant or termite nest, they often eat very quickly, using a raking technique of the mandibles (in leptotyphlopids) or of the maxillae (in typhlopids). Nate Kley's lab at Stony Brook University has taken some fantastic videos of blindsnake feeding techniques.

Time-sequence of a blindsnake ingesting and decapitating
a termite worker. From Mizuno & Kojima 2015
Supplementary video here
As Mizuno fed termites to the blindsnakes, he observed something very unusual. The blindsnakes typically grabbed and swallowed the termites backwards. Most snakes usually swallow their prey head-first, so this was weird enough. But, it gets weirder. Often, when the snake had maneuvered a termite so that only its head stuck out of the snake's mouth, it would rub its face on the bottom of the tank, decapitating the termite. All of the termite soldiers and about half of the termite workers offered to the blindsnakes were decapitated. Occasionally, a snake would regurgitate a termite that it had consumed whole, decapitate it, and re-consume the body. Decapitated termite heads became attached to the back of the snake’s head or were scattered around the bottom of the cage. The snakes never ate the decapitated heads. There did not appear to be a cost to decapitation—whether a snake decapitated a termite or not, the time required to completely ingest it was about 3 seconds. However, twice blindsnakes were observed swallowing termites head-first, which took only about 1-1.5 seconds. This may not seem like a big difference, but when you're eating hundreds or thousands of prey items in one sitting, it can add up!

Intact termite heads in the feces of a blindsnake
From Mizuno & Kojima 2015
Why do blindsnakes remove the heads of their prey? One reason might be that termite heads contain glands full of toxic chemicals called terpenes. But, unlike predators that remove the skin of various amphibians to avoid the toxins in their skin glands, blindsnakes don't always remove the heads of their prey, suggesting that they aren't that susceptible to terpene poisoning. It's even been suggested that some blindsnakes might be sequestering defensive chemicals from the ants and termites that they eat, just as gartersnakes sequester tetrodotoxin from newts, in which case they might actually prefer the part of the termite with more chemicals. A more likely hypothesis is that the heads are less digestible than the termites' bodies. Between 26 and 100% of the termite heads consumed by blindsnakes in Mizuno & Kojima's experiment remained undigested in the snakes' feces. Additionally, the snakes preferred to eat the worker termites rather than the more heavily-armored soldier termites, and the few soldier termites they did eat were newly-molted. Removing the termites' scleritized heads might allow blindsnakes to pack more soft, squishy bodies into their stomachs, maximizing the nutrition they get out of their meals. It's a bit like you or me peeling a banana or an orange, or removing the husk from a coconut. Since soldier termites have pinching mandibles, removing their heads might also prevent the blindsnakes from being bitten from the inside, which is a bit like you or me...removing the horns of a cow before eating it, if we ate cows alive and whole, I guess?

Evidently the raking maxillae of typhlopids
are sufficiently dexterous to manipulate
prey inside the mouth to position them
for decapitation.
From Kley 2001
Since snakes don't have hands, they've got to remove any indigestible parts using the only maneuverable part they do have—their jaws. Unlike other blindsnakes (which use bilaterally synchronous jaw movements similar to those of all other vertebrates) but like alethinophidians, typhlopid blindsnakes can move the left and right sides of their highly mobile upper jaws independently and asynchronously. Despite its sophistication, the ratcheting movements of their maxillary raking mechanism are insufficient, by themselves, to allow them to decapitate their prey. We must await further functional-morphological studies to assess the role of the toothless lower jaw, which could act as a wedge or blade, in this process. Since snakes cannot really "bite", arthropods, with their jointed limbs and bodies, might be the only type of prey that a snake could pull apart. There are a fair number of snakes that eat arthropods, but most of them are relatively obscure. Besides the crab-eating snakes, one might look for prey-dismembering behavior in sonorines, a tribe of desert-dwelling snakes from southwestern North America, other North American snakes such as the colubrines Tantilla and Opheodrys and the natricine Regina, the dwarf racers of Africa and the Middle East (genus Eirenis), the centipede-snakes of Africa (genus Aparallactus), or certain kukrisnakes (genus Oligodon). In addition to the typhlopid blindsnake in this study, two short notes from the 1950s and 60s document similar decapitation behaviors in two different species of leptotyphlopids (Epictia goudotii [formerly Leptotyphlops phenops] from Central America and Rena dulcis [formerly L. dulcis] from Texas), despite their radically different jaw morphology. I won't be surprised if it turns up in other scolecophidian families as well, since this most-basal group of living snakes probably co-evolved with the early radiation of ants and termites, their favorite prey.


Thanks to Brendan Schembri for the use of his photo, and to Takafumi Mizuno and Yosuke Kojima for giving me the opportunity to write about their discovery in advance of its publication and for translating it into Japanese.


Kley, N.J. 2001. Prey transport mechanisms in blindsnakes and the evolution of unilateral feeding systems in snakes. American Zoologist 41:1321-1337 <link>

Mizuno, T. and Y. Kojima. In press. A blindsnake that decapitates its termite prey. Journal of Zoology 10.1111/jzo.12268 <link>

Prestwich, G.D., B. Bierl, E. Devilbiss, and M. Chaudhury. 1977. Soldier frontal glands of the termite Macrotermes subhyalinus: Morphology, chemical composition, and use in defense. Journal of Chemical Ecology 3:579-590 <link>

Reid, J.R. and T.E. Lott. 1963. Feeding of Leptotyphlops dulcis dulcis (Baird and Girard). Herpetologica 19:141-142  <link>

Savitzky, A.H., A. Mori, D.A. Hutchinson, R.A. Saporito, G.M. Burghardt, H.B. Lillywhite, and J. Meinwald. 2012. Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies. Chemoecology 22:141-158 <link>

Shine, R. and J.K. Webb. 1990. Natural history of Australian typhlopid snakes. Journal of Herpetology 24:357-363 <link>

Smith, H.M. 1957. Curious feeding habit of a blind snake, Leptotyphlops. Herpetologica 13:102 <link>

Stokes, A.N., A.M. Ray, M.W. Buktenica, B.G. Gall, E. Paulson, D. Paulson, S.S. French, E.D.B. III, and J. E.D. Brodie. 2015. Otter predation on Taricha granulosa and variation in tetrodotoxin levels with elevation. Northwestern Naturalist 96:13-21 <link>

Vidal, N., J. Marin, M. Morini, S. Donnellan, W.R. Branch, R. Thomas, M. Vences, A. Wynn, C. Cruaud, and S.B. Hedges. 2010. Blindsnake evolutionary tree reveals long history on Gondwana. Biology Letters 6:558-561 <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Tuesday, June 30, 2015

The Linnaean Snakes: Part II

This post will soon be available in Spanish!

Click here to read Part I.

Last month I wrote about "serpentine royalty": the first species of snakes to be formally described using the Linnaean system—those described by Linnaeus himself in the 1758 10th edition of Systema Naturae. Out of 100 snake species in that tome, let's take a closer look at the four that still bear their original names.

Infographic showing the "tenure" of 807 snake genera used by more than one taxonomist.
An additional 387 genera used only once are not shown, for a total of 1,194. Of these, about 500 are currently in use.
The three longest lines at the top are the original three genera coined by Linnaeus in 1758 and still in use today.
Data span 1758-2010, from The Reptile Database.
Click for full version.

Coluber constrictor

In the immortal words of Jeffrey C. Beane: "Linnaeus first gave me my scientific name, but reflecting upon it, I think: “What’s his game?” Perhaps he was drunk on that day (or smoked pot), for a snake I am, yes, but constrictor I’m not."

The Racer (Coluber constrictor) is one of only four snakes
that have gone by the same scientific name since 1758.
Today Coluber contains only 14 species, 11 of which
were recently reallocated to it from Masticophis
In 1758 Linnaeus placed 61 species into Coluber,
of which only C. constrictor remains.
Many contemporary naturalists have been puzzled by the scientific name of the North American Racer, which normally crams its live prey into its mouth rather than constricting it. Linnaeus's descriptions ("Inhabits Canada. Triangular head1. It approaches men, twisting itself around their feet, but it is harmless."[10th ed.]/"Inhabits North America. Runs swiftly and bites very hard, but is not poisonous. Twists itself around the legs of such as approach it. Very smooth and slender. Black, pale blue beneath, white throat."[12th ed.]) glibly paraphrase that of his student Pehr Kalm2, who gave a several-page account of racers in his 1753 book Travels in North America. Among other myths, Kalm recounts tales told by "numbers of credible people" that racers, especially males interrupted during mating in the spring, will chase and trip people, but he was unable to reproduce the behavior despite his best efforts, saying "I know not for what reason they shunned me, unless they took me for an artful seducer". He was also doubtful of the claim that racers and other snakes enchant or hypnotize their prey, but he was reluctant to discount the possibility entirely because "many of the worthiest and most reputable people have related [the story], and...it is so universally believed here that to doubt it would be to expose one's self to general laughter." Given their willingness to accept these and other myths, it's not unlikely that Kalm and some of his informants, including the naturalists John Bartram and Cadwallader Colden, also confused racers with ratsnakes, both species being black along the east coast, which accounts for Kalm's descriptions of racers constricting and climbing large trees to eat birds' eggs, and might explain their perpetual misnomer.

Racer plate from Catesby's Natural History.
Catesby also described cornsnakes but not ratsnakes,
suggesting that perhaps he too confused ratsnakes and racers.
The English naturalist Mark Catesby3 had previously described racers, which he called Anguis niger, and other snakes in his 1731 Natural History of Carolina, Florida and the Bahama Islands, the first published account of the flora and fauna of North America. Apparently Linnaeus didn't think much of this book, because he dismissed it in his introduction to the reptiles by writing "Catesby sketched a few serpents more beautifully than he made notes about them". He must have had some respect for Catesby, though, for he named both the lily-thorn Catesbaea and the bullfrog Rana catesbeiana after him. It is a bit of a mystery where the racer specimen that Linnaeus saw originated, or if he even saw one. If he did, it must have been collected and sent to him by Kalm, but the whereabouts of Kalm's specimens of North American snakes, if they exist, are unknown. There is a specimen of a racer in the Royal Museum in Stockholm which is marked with a Linnaean label. An 1802 catalogue states that the specimen came from the King, but of all the snakes with these labels it is the only one Linnaeus does not describe in his 1764 manuscript on the King's collection, Museum Adolphi Friderici (where the binomial system is used for the first time), so this information is probably erroneous. Also described by Linnaeus but subsequently lost are Kalm's specimens of Northern Watersnakes (today, Nerodia sipedon) and Common Gartersnakes (today, Thamnophis sirtalis), as well as two more mysterious specimens which Linnaeus named Coluber leberis and Coluber ovivorus4.

Boa constrictor

Top: Boa constrictor
Bottom: Boa constrictor plate from Linnaeus & Sundius's
1748 Surinamensa Grilliana, drawn by P. A. Petersson
and engraved by C. Bergquist
Unlike racers, this snake is the eponymous constrictor. The name boa comes from the Latin boa for ‘large snake,’ after an animal mentioned in the Natural History of Pliny the Elder, which ate cows ('bos' in Latin). Linnaeus, whose descriptions were written in a kind of telegram style, without verbs, in a deliberate effort to be as brief as possible and save space, was particularly laconic if descriptions had already been published by himself or others. Of this species he said only that it "inhabits the [West] Indies and warm parts of the Americas", because boa constrictors had already been described by two of his primary sources on snakes, the Dutch naturalists Albertus Seba and Laurens Gronovius. Additionally, a specimen collected in Surinam by Claes Grill reached Linnaeus in the 1740s, and is described and illustrated in a dissertation defended by Peter Sundius, one of Linnaeus's early students. The catalogue of the King of Sweden's natural history collection also contains a description of one. However, Linnaeus could have been even more succinct had he recognized that a dark-colored specimen from the collection of Charles de Geer, a Swedish entomologist, was also a Boa constrictor. This collection was also the source of his anaconda, Burmese Python, and a handful of other snakes he had seen nowhere else, all of which are now in the Royal Museum in Stockholm, but he did not recognize that the boa in de Geer's collection was the same species that he had already called Boa constrictor.

Image of an African Python (Python sebae) from Charles Challié Long's
1876 book Central Africa: Naked Truths of Naked People
The caption reads "Capture of a Boa-Constrictor"
The confusion may have arisen because de Geer's specimen had many more ventral scales than other boas Linnaeus had examined. Linnaeus preferred to use the number of ventral and subcaudal scales to distinguish species of snakes over their color or pattern (like his quantitative sexual system for classifying plants, Linnaeus's methods were a predecessor to modern ones), but he recognized that even these scale counts varied considerably within species. Kalm stated that his teacher thought "it was better to make use of an imperfect character than none at all" and he was hopeful that "time, and greater acquaintance with this class of animals may perhaps clear up their natural characters". Linnaeus named Boa constrictor earlier on the page than Boa orophias, which is why we use the former name rather than the latter, which is now used for a subspecies from St. Lucia. In his defense, Linnaeus did write of B. orophias: "Face of the constrictor, but dark", suggesting that he thought they might be the same snake. To Linnaeus's terse description, Gmelin, writing in the 13th edition of Systema Naturae, added: "beautifully variegated with rhombic spots, belly whitish" and noted that it is "of vast strength and size, measuring sometimes 12 yards long, and by twisting itself round the bodies of deer, leopards, and other larger quadrupeds, breaks the bones, and after covering them over with a slimy mucus gradually swallows them". Certainly these descriptions helped popularize these large and impressive snakes, specimens of which were curios of the highest value. This popularization led to many explorers and travel writers calling any large snake a boa constrictor (including pythons) for centuries to come.

Crotalus durissus

Global distribution of 35 species of the genus Crotalus
Data from IUCN; click for a larger version
Rattlesnakes have captured the attention of Europeans ever since they first started settling the New World. Using their Nahuatl (Aztec) name, Teuhtlacocauhqui, Francisco Hernández described them in his 1615 Quatro Libros de la Naturaleza"When they strike, the bite is fatal unless treated promptly...It has a tail with rattles, one for each year of its life...It has two curved fangs in its upper jaw to inject its venom...It moves in a slithering fashion. Indians hunt and capture them and hang them around their necks...Those who raise them at home say they can live for up to a year without eating anything...When wounded and angry, it whips around, shaking its rattles, and raises its neck to frighten those nearby. However, it does not bite unless provoked." Hernández's book also contains the earliest illustration of a rattlesnake, which is certainly Crotalus durissus. Many other 16th and 17th century authors also wrote about rattlesnakes, dating back to their earliest mention in print, by Cieça de Leon in 1554. Many of these writings contain both accurate information and the first printed iterations of several still-current myths. Clearly, native Americans had known of rattlesnakes since ancient times; the Aztecs and Mayans had a rattlesnake constellation which may have been part of their zodiac.

Top: Neotropical Rattlesnake (Crotalus durissus)
Bottom: The earliest illustration of a rattlesnake
in a book, from Hernández 1628
Because of their tails, Linnaeus thought that rattlesnakes were so unusual that he placed them in their own genus, Crotalus, separating them from other vipers (which he placed in the genus Coluber despite their solenoglyphous fangs). Linnaeus described three species of rattlesnakes: Crotalus horridus (see below), C. durissus, and C. dryinas. Like Boa constrictor and B. orophias, we now consider the latter two species to be the same, but unlike the boa names we use the name durissus for the species even though dryinas precedes it on the page5. Although most rattlesnakes are North American, Linnaeus's C. durissus specimen was collected by Claes Grill in Surinam and originally described in detail in 1748 in the same dissertation that contained the boa constrictor description. In contrast, the "C. dryinas" specimen was from the king of Sweden's collection and lacked geographic data. It is clear that King Adolf Frederick was not the most attentive curator—his curatorial record is incomplete, and over time many of his specimens have been lost and their labels mixed up or deliberately modified. He wasn't the most assertive head of state either, described as "little more than a state decoration"—although apparently he did like snakes. Both rattlesnake specimens from his collection that Linnaeus examined have apparently been lost for over 100 years, and the Grill specimen is lost as well. As a result, and because Linnaeus's descriptions are so terse, the names of the three rattlesnakes (horridus, durissus, and dryinas) were for many years confusingly and inconsistently applied. For example, both Holbrook and Duméril referred to the timber rattlesnake as C. durissus in their respective classic works, Duméril additionally called the neotropical rattlesnake C. horridus, and Boulenger refers to the eastern diamondback as C. durissus in his catalogue of snakes in the British Museum.

Crotalus horridus

Crotalus horridus is the type species of the genus Crotalus,
which today contains 39 species.
Of this snake which would come to symbolize America, Linnaeus wrote (appropriately) "Lives in America. Very venomous; its antidote is Senega (snakeroot). It is eaten by pigs, and calls down birds and squirrels from the trees into its jaws." This is a lengthy description for him, especially considering that timber rattlesnakes had already been described in 1683 (by Edward Tyson, who dissected one), 1721 (by Richard Bradley), 1734 (by Albertus Seba), and in 1745 and 1754 by Linnaeus himself (the first time in a dissertation defended by Barthold Rudolph Hast describing specimens from Count Carl Gyllenborg's collection of rare herps, insects, corals, and minerals, and the second time in his description of the collection of the Swedish king, Museum Adolphi Friderici). C. horridus is the only North American snake Linnaeus described that was not sent to him by Kalm or by his other primary North American informant, Alexander Garden. The specimen that he described had 7 rattle segments, and he was able to give a count of the ventral scales (167), which indicates that he examined a complete specimen, but the specimen that is now in the Royal Museum in Stockholm is represented only by a severed tail, which has 12 rattle segments, and a head, which is actually from a bushmaster (Lachesis muta). Like the specimens of the neotropical rattlesnakes, apparently the original specimen has been missing since at least 1899, and possibly much earlier.6

Catesby's Timber Rattlesnake (which he called Vipera
, but which Linnaeus and we call Crotalus horridus).
Kalm considered this "an incomparable illustration".
Although Kalm did not collect a rattlesnake for Linnaeus, he gave a lengthy, detailed, and incredibly accurate description of rattlesnakes and their relationship with humans, which is as much an account of snake biology as it is of the cultural history of colonial America. His words suggest that rattlesnakes were already on their way out in eastern North America in the mid-1700s: "In all my travels, I saw only 3 living specimens. I frequently heard them in the nearby thicket, but it seemed inadvisable to pursue them." It is a testament to Kalm's scientific training that he surpassed many modern observers in accurately stating that "The snake is usually 3 to 4 feet long. The largest one I saw was 6 feet long and as thick as the calf of a man's leg. Usually they are as thick as the wrist" and "They travel slowly, thus one need not fear being overtaken" and "The rattler is peculiar in that he usually does not injure a person unless forced to defend himself."  Despite these honest observations, Kalm had no special love of snakes, including them in a list of reasons that he preferred Sweden to America: "The rattlesnakes, horned-snakes, red-bellied, green, and other poisonous snakes, against whose bite there is frequently no remedy, are in great plenty here".

Timber Rattlesnake from Bradley (1721)
Catesby also described the Timber Rattlesnake, which he called Vipera caudisona, at length. Gmelin, writing in the 13th edition of Systema Naturae, expanded Linnaeus's description in both inaccurate ("The most venomous of the serpent tribe") and accurate ("They seldom bite unless when irritated, or for the purpose of securing their prey, and the fascinating power which has been attributed to them is probably nothing more than that they first bite the animal and patiently watch till it dies to devour it") ways. In 1754 in Museum Adolfi Frederici Linnaeus wrote: "...nor can he escape with life who is bitten by the Rattle-snake (Crotalus horridus) in any part near a great vein. But the merciful God has distinguished these pests by peculiar signs, and has created them most inveterate enemies; for as he has appointed cats to destroy mice, so has he provided the Ichneumon [mongoose] (Viverra Ichneumon) against the [cobra], and the Hog to persecute the latter. He has moreover given the Crotalus a very slow motion, and has annexed a kind of rattle to its tail, by the motion of which it gives notice of its approach; but, lest this slowness should be too great a disadvantage to the animal itself, he has favoured it with a certain power of fascinating squirrels from high trees, and birds from the air into its throat, in the same manner as flies are precipitated into the jaws of the lazy toad."

Other notable snake species described by Linnaeus

Linnaeus described 83 other snake species between his 10th and 12th editions that are still considered valid today, plus 31 that are not (including Crotalus dryinas and Boa orophias). These include many familiar, widespread, and notable species, including 2 scolecophidians, Anilius scytale, and an Asian pipesnake from Sri Lanka (all of which he placed in the genus Anguis, which we today use for legless lizards), several huge constrictors including the Indian Python, Boa Constrictor, and Green Anaconda (but also three smaller tree boas and two sand boas, the latter also in Angius), 13 vipers including the fer-de-lance, copperhead, European adder, bushmaster, and pygmy rattlesnake, a pair of homalopsids, 46 colubrids (including many familiar European and American species but also an African egg-eater and an Asian flying snake), 5 lamprophiids, and 9 elapids (including 3 cobras, 2 coralsnakes, and 2 sea snakes). He also made a few brief comments about snake anatomy and biology as footnotes or in his introductory material, including his method for counting ventral and subcaudal scales (first used in Amphibia Gyllenborgiana and still in use today) as well as the correct observations that "Serpents of our country hibernate and in the early spring shed their skin, that is to say, their old age" and "Serpentes often swallow down prey twice as thick as their neck, on account of their expandable, unarticulated jaws". In other works, he presents a great deal of information on snakebite and, the consummate botanist, its treatment using various medicinal plants. Although Linnaeus bore no special love for snakes, he treated them as he did other biodiversity, and I encourage all modern biologists to do the same—to view snakes as wildlife rather than pests, as a beautiful and diverse part of our natural heritage, to see them as what they are rather than what we imagine them to be.

It is tempting to imagine Linnaeus as a brilliant solitary taxonomist, aided and sent specimens by his correspondents, colleagues, and students but intellectually working alone. But, as today, Linnaeus relied heavily on his network both to obtain specimens and to describe them with reference to those who had gone before. Of the 74 species in the 10th edition, only four were brand new original descriptions (these were Vipera aspis from southern Europe, Epicrates cenchria from South America, Erythrolamprus triscalis from Curaçao, and Duberria lutrix from Africa), and the 12th contained scarcely more, mostly southeastern North American species sent to Linnaeus by Alexander Garden. Almost ten times that many new snakes were described last year alone.

Coronella austriaca from Laurenti 1768
It's probably safe to assume that Linnaeus described every snake he ever saw, since this is what he did with everything else. And, considering he lived in Sweden most of his life and never traveled further south than Germany, he did pretty well, nailing numerous tropical species of snake collected by others and sent either to him, or that he examined in the collections of zoologists in Germany, England, and Holland. Systema Naturae contains snakes from every continent except for Australia, which was only just becoming known in Europe at the time of Linnaeus's death (his correspondant Joseph Banks and two of his apostles, Daniel Solander and Anders Sparrman, sailed around the world with James Cook and visited Australia and Oceania in the 1760s and 1770s; Linnaeus's health was poor throughout the 1770s and he died in 1778). But, there is one glaring oversight in Linnaeus's snake work: he described only two of the three native Swedish snakes (Natrix natrix and Vipera berus). Both of these he initially described in his 1746 Fauna Svecica, an account of the animals of Sweden containing 1,357 species in its original edition (upated 1761 with 2,266 species), in which he used cumbersome pre-binomial names such as Coluber natrix scutis abdominalibus CLXX squamis caudae LX ("Water snake with 170 ventral scales and 60 subcaudal scales"), which later became the much simpler yet no less unequivocal Coluber natrix in Systema Naturae. But he missed one: the smooth snake, Coronella austriaca, which was described by J.N. Laurenti7 and named for his native Austria (where it is also found) ten years after the 10th edition of Systema Naturae. Did Linnaeus ever see a Coronella in all the years he lived, worked, and botanized in Sweden? Smooth snakes are active during the day in dry, sunny clearings where they bask in bushes, and although they are not found as far north as Uppsala, they do occur in Småland, where Linnaeus grew up. It seems likely that Linnaeus would have seen them—did he think they were the same species as another kind of snake? If not, why did he leave them out of Fauna Svecica and Systema Naturae, which were intended to be as comprehensive as possible?

1 In the 10th edition Linnaeus confused specimens of racers with those of the black form of the Eastern Hognose Snake (Heterodon platirhinos), but by the 12th edition these had been separated and the phrase "triangular head" removed from the description of the racer.

2 After whom the mountain laurel genus Kalmia is named.

3 Like Maria Sibylla Merian before him, Catesby was among the first naturalists to draw his plants and animals interacting in their natural habitats, a style of representation that would later be used by Alexander Wilson and John James Audubon. He was also the first to abandon the Native American names for his subjects, instead establishing scientific binomials based on relationships a la Linnaeus. Had his work been published three decades later, he might have been immortalized as the father of North American herp taxonomy, and many of the scientific names that we use today could have been very different. Catesby's book, richly illustrated, was much more popular than Linnaeus's.

4 The specimen named Coluber leberis was likely a Storeria, the only genus found in the area traversed by Kalm (Pennsylvania, New York, New Jersey, and southern Ontario) with matching scale counts. Although the scale counts and pattern description match S. occipitomaculata better and this species is more common than S. dekayi in northeastern North America, the specimen could have been either, and since we cannot examine it, the name is not used. Coluber ovivorus is even more enigmatic, because the description does not match any northeastern snake well.

5 This is because, by the time it was all sorted out, the name C. durissus had ended up being in more widespread use, so the "proper" name dryinas was suppressed by the International Commission on Zoological Nomenclature.

6 There is a reasonable chance that the specimen that Linnaeus first named C. horridus was actually from South America, and thus was really C. durissus as well, but since we cannot prove this beyond a shadow of a doubt, in 1926 the International Commission on Zoological Nomenclature decided to continue to use it for the timber rattlesnake.

7 Little is known about Laurenti. No picture of him exists, and his 1768 thesis, 
Specimen medicum, was his only publication. In it, he elevated Linnaeus's order Reptilia to a class, distinguishing it from class Amphibia, into which Linnaeus lumped both amphibians and reptiles. Laurenti also tripled the number of reptile genera, coining some of today's most familiar genus names, including Vipera, Natrix, Laticauda, Dipsas, and Naja.


Thanks to Todd PiersonPatrick Jean, and JD Willson for the use of their photos, and to my mom for getting me William Blunt's Linnaeus for Christmas this year, which inspired this article.


Andersson, L.G. 1899. Catalogue of the Linnaean type-specimens of snakes in The Royal Museum in Stockholm. Bihang till Kongl. Svenska Vetenskaps-Akademiens Handlingar 24:1-35 <link>

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Linnaeus C. 1746. Fauna Svecica Sistens Animalia Sveciæ Regni: Quadrupedia, Aves, Amphibia, Pisces, Insecta, Vermes, Distributa per Classes & Ordines, Genera & Species. Differentiis Specierum, Synonymis Autorum, Nominibus Incolarum, Locis Habitationum, Descriptionibus Insectorum. Stockholmiæ [Stockholm] (Sweden): Sumtu & literis Laurentii Salvii <link>

Linnaeus, C. 1746. Museum Adolpho Feidericianum. Uppsala University, Uppsala <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.