Basics of snake skulls

This article will soon be available in Spanish!

Snakes have a lot more bones than we do, but they have a lot fewer types of bones. Aside from a few boas, pythons, pipesnakes, and blindsnakes with vestigial femurs, most snakes just have a few hundred vertebrae with one pair of ribs each (except in the neck & tail), and a skull.

The snake skull is a remarkable structure. Snake skulls are highly kinetic, with a lot more moving parts than our skulls. Human skulls have just one movable part: the temporomandibular joint, which opens and closes your mouth. Snake skulls have many joints and moving parts; they can move the left and right sides of their jaws independently, as well as the outer (maxilla) and inner (palatine+pterygoid) parts of their upper jaws. Many bones that are tightly knit together in the skulls of most animals are loosely connected by stretchy ligaments in snakes, allowing them to stretch their jaws over huge prey (pardon the goofy music in the linked video). Contrary to the popular phrase, snakes cannot actually "unhinge" their jaws (Harry Greene explains this very well in this video).

The right side of the skull of an alethinophidian snake (nose pointing to the right).
Bones with teeth are the maxilla (mx), palatine (pal), pterygoid (pt), and dentary (d).
From Cundall & Irish 2008. For a key to all abbreviations, click here.
The bones or parts of bones that are shaded are not present in all snake species.

Most snakes have teeth on four pairs of bones, two of which are the same as pairs of bones where humans do: the maxilla (most of our upper jaw) and the dentary (our lower jaw). In addition, almost all snakes have teeth on two bones that in humans form part of the roof of the mouth: the palatine and the pterygoid¹, which are connected one in front of the other. This means that snakes have two upper jaws on each side: an outer one (the maxilla) and an inner one (the palatine+pterygoid). If a snake has fangs, they are always on the maxilla². Some snakes, such as pythons, also have teeth on the premaxilla, where we humans have our incisors, although in most snakes the premaxilla is a part of the snout, has no teeth, and does not act as part of the jaws.

The right half of the skull of a snake, looking up from the bottom (nose pointing to the right).
Bones with teeth are the maxilla (mx), palatine (pal), pterygoid (pt), and dentary (d). The premaxilla (pmx) has no teeth.
From Cundall & Irish 2008. For a key to all abbreviations, click here.The bones or parts of bones that are shaded are not present in all snake species.

Tooth marks left by a
python bite (upper jaw
above, lower jaw below).

You can sometimes see this pattern of tooth marks left behind when a non-venomous snake lets go after biting something, and in fact many resources suggest that you can use the tooth pattern to determine³ whether or not a bite has come from a venomous snake (a viper at least, which are responsible for >99% of venomous snakebites in the USA), since most dangerously venomous snakes have different tooth patterns on account of their fangs, and most of their non-fang teeth don't usually come into contact with the target. I mentioned above that fangs are always on the maxilla, and that's because the maxilla is the primary prey-catching bone in the snake skull. As far as we know, fangs evolved only once, as enlarged teeth at the back of the maxilla in the ancestor of all living colubroid snakes about 75 million years ago. In many living species of snakes, this is still the situation, and the vast majority of these are not dangerous to humans (although some can inflict painful bites if allowed to chew for a few minutes, and a few can be deadly). In at least three cases (vipers, elapids, and atractaspidids), the fangs have moved up to the front of the maxilla, through the developmental suppression of the front part of the maxilla (and its teeth) in the snake embryo. I covered this and the evolution of grooved and hollow fangs in more detail in my article about snake fangs.

The right half of the skull of a snake, looking down from the top (nose pointing to the right).
No teeth are visible. From Cundall & Irish 2008. For a key to all abbreviations, click here.The bones or parts of bones that are shaded are not present in all snake species.

Although most people are most interested in the teeth and fangs, the rest of the snake skull is no less fascinating. The outer and inner upper jaw are connected by a toothless upper jaw bone called the ectopterygoid, which works like a lever to transfer muscular power from the muscles attached to the pterygoid out to the maxilla, which has no muscles of its own. When a snake is eating, the entire upper jaw (inner and outer parts) is raised and moved slightly backward, alternating the left and right sides and pulling the prey into the mouth: the characteristic "jaw-walking" or "pterygoid walk" motion of feeding snakes. So, the front of the pterygoid is attached to the back of the palatine, the ectopterygoid hangs off the outside of the pterygoid, and the maxilla hangs off of the other end of the ectopterygoid. In vipers, whose fangs fold, the maxilla and its fang are pushed forward by the ectopterygoid and pterygoid.

Roughly the same fang movements are made during striking and swallowing. Supratemporal (st), quadrate (q), mandible (ma), pterygoid (pt), ectopterygoid (ec), palatine (pa), prefrontal (pf), maxilla (mx). From Kardong 1977

The independent left and right movement
of the upper jaws of a viper.
Abbreviations as above. From Kardong 1977.

Amazingly, in most snakes there is no direct connection between the upper jaws and the braincase⁴. Instead, the palatine and maxilla are connected to the braincase by long ligaments, which give them great freedom of motion. The front end of the palatine is connected more firmly to the snout, albeit still with some freedom to move. The rear end of the maxilla is also connected by a ligament to the lower jaw. It's really the movements of the palatine and pterygoid that swallow the prey. The lower jaws mainly press the prey against the upper jaws, and the teeth on the dentary and maxilla rarely contact the prey and play little active role in swallowing.

The lower jaws or mandible participate in the process of feeding as well, and unlike in humans they have a loose attachment of the lower jaws to each other at the front of the dentary bones. The dentary bones are connected firmly at the back to the articular bones, which are connected to the quadrate bones at a flexible joint, which are connected to the back of the braincase by the supratemporal bones, also at a somewhat moveable joint. Together with the flexible palato-maxillary apparatus ("upper jaws"), this three-part lower jaw allows snakes to open their mouths very wide, walk their heads over, and consume things that are as big as they are without breaking them into smaller pieces or using their non-existent hands. The quadrate also attaches to the columella, which is the sole inner ear bone in reptiles; thus, the lower jaw also conducts sound to the ear.

So there you have it. The snake skull is divided into four functional units: the braincase, the snout, the palato-maxillary apparatus ("upper jaws") and the mandibular apparatus ("lower jaws"), each of which can move independently (well, except for the braincase, which is relatively stationary). The upper jaws are divided into two partially separated structural-functional units, a medial swallowing unit and a lateral prey capture unit, both of which work with the lower jaws to accomplish their tasks.

From Frazzetta 1970. Click for larger size.

A quick note about a special case: one of my favorite snakes, and one of the first I wrote about on this blog, Casarea dussumeri, are often called Round Island boas, although I chose to use the more apt "splitjaw snakes" in my article. As if the usual kinesis of the snake skull isn't enough, these snakes have a maxilla that is uniquely subdivided into two movable parts, called the anterior and posterior maxilla. The anterior maxilla has 10 teeth and the posterior maxilla has 12. It is thought that the divided maxilla evolved through incomplete development, because the maxilla of other snakes forms in two parts before fusing together in the embryo, and the function is thought to be to help Casarea encircle hard, cylindrical prey such as skinks.

We still have a lot left to learn about snake skulls. We didn't even cover half of the bones in this article. You don't actually so much find snake skulls as you do carefully prepare them. The individual bones are so small and light and fragile that they tend not to fossilize well, nor can they easily be found among the other bones of a snake's skeleton. Even normal cleaning and preparation methods can damage the fragile bones of tiny snake skulls. Thus, there is much left to discover about how they work!

Skull of Natrix natrix from Andjelković et al. 2017. Mobile connections marked with red dashed arrows and circles.Paired bones are shown in yellow (pa – palatine, pt – pterygoid, ec – ectopterygoid, mx – maxilla, st – supratemporal,q – quadrate, cp – compound bone, d – dentary, pf – prefrontal), unpaired bones are shown in green or grey (pmx – premaxilla, na – nasal, b – braincase, smx – septomaxillae & vomers).

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1 Although the pterygoids are stand-alone bones in the roof of the mouth of many vertebrates, in humans they are called the pterygoid processes of the sphenoid bone because they are fused to the sphenoid bone.^↩

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2 There is one very strange snake, Pythonodipsas carinata from Africa, that has an ungrooved fang on the palatine bone. They aren't any studies of their functional morphology so we don't really know exactly how they use their palatine fangs, but they use constriction to subdue their prey.^↩

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3 I don't necessarily recommend this, partly because if you've been bitten then it's too late, and partly because it's better just to learn the few venomous snake species that live in your area than it is to try to follow some "rule" that inevitably has exceptions.^↩

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4 Atractaspidids have a ball-and-socket joint between the prefrontal (part of the braincase) and the maxilla, which along with a gap, bridged by a ligament, between the pterygoid and palatine, allows them to "strike" with their fang backwards, with a closed mouth, using just the fang on one side, a useful if terrifying adaptation for envenomating prey in underground burrows. A hook-like ridge on the fang increases the size of the wound, presumably enhancing the absorption of venom.^↩

ACKNOWLEDGMENTS

Thanks to gibby for the use of their photograph.

REFERENCES

Albright, R. G. and E. M. Nelson. 1959. Cranial kinetics of the generalized colubrid snake Elaphe obsoleta quadrivittata. I. Descriptive morphology. Journal of Morphology 105:193-239.

Albright, R. G. and E. M. Nelson. 1959. Cranial kinetics of the generalized colubrid snake Elaphe obsoleta quadrivittata. II. Functional morphology. Journal of Morphology 105:241-291.

Andjelković, M., Tomović, L., & Ivanović, A. 2017. Morphological integration of the kinetic skull in Natrix snakes. Journal of Zoology, 303:188-198 <link>

Cundall, D. 1983. Activity of head muscles during feeding by snakes: a comparative study. American Zoologist 23:383-396.

Cundall, D. and H. W. Greene. 2000. Feeding in snakes. Pages 293–333 in K. Schwenk, editor. Feeding: Form, Function, and Evolution in Tetrapod Vertebrates. Academic Press, San Diego, CA.

Cundall, D. and F. Irish. 2008. The snake skull. Pages 349-692 in C. Gans, A. S. Gaunt, and K. Adler, editors. Biology of the Reptilia. Volume 20, Morphology H. The Skull of Lepidosauria. The University Of Chicago Press, Chicago, Illinois, USA <link>

Frazzetta. T. 1970. From hopeful monsters to bolyerine snakes? The American Naturalist 104:55-72 <link>

Frazzetta, T. 1971. Notes upon the jaw musculature of the Bolyerine snake, Casarea dussumieri. Journal of Herpetology 5:61-63

Irish, F. and P. Alberch. 1989. Heterochrony in the evolution of bolyeriid snakes. Fortschritte der Zoolologie 35:205.

Juckett, G. and J. G. Hancox. 2002. Venomous snakebites in the United States: management review and update. American Family Physician 65:1367-1375 <link>

Kardong, K. 1974. Kinesis of the jaw apparatus during the strike in the cottonmouth snake, Agkistrodon piscivorus. Forma et functio 7:327-354.

Kardong, K. V. 1977. Kinesis of the jaw apparatus during swallowing in the cottonmouth snake, Agkistrodon piscivorus. Copeia 1977:338-348 <link>

Lombard, R. E., H. Marx, and G. B. Rabb. 1986. Morphometrics of the ectopterygoid in advanced snakes (Colubroidea): a concordance of shape and phylogeny. Biological Journal of the Linnean Society 27:133-164 <link>

Maisano, J. A. and O. Rieppel. 2007. The skull of the Round Island boa, Casarea dussumieri Schlegel, based on high-resolution X-ray computed tomography. Journal of Morphology 268:371-384 <abstract>

Raynaud, A. 1985. Development of Limbs and Embryonic Limb Reduction. Pages 59-148 in C. Gans and F. Billett, editors. Biology of the Reptilia. Volume 15. Development B. John Wiley & Sons, New York <link>

Rieppel, O. 2012. “Regressed” Macrostomatan Snakes. Fieldiana Life and Earth Sciences 5:99-103 <link>

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

Basics of Snake Fangs

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Solenoglyphous fangs of a Gaboon Viper

Snake fangs are specialized, elegantly modified teeth. Some are like hypodermic needles, others are more like water slides. But all serve essentially the same purpose: to inject venom into the snake's prey. Occasionally, the fangs are also used in defense, but studies show that snakes striking in defense are far less likely to inject venom than when they're striking at a prey item, a fact that has assuaged the fears of many an ophidiophobic. I wanted to write a brief review of snake fang types, because their anatomy is very interesting and also because of their important role in classifying snakes and understanding how different groups of snakes are related to each other.

Cross-sections of fangs:
F is an aglyphous tooth.
G is an opisthoglyphous fang.
H is a proteroglyphous fang.
I is a hollow solenoglyphous fang.
From Bauchot (2006)

Many snakes produce venom, which is essentially very strong saliva, in glands in their heads (which is where you produce your saliva, too). We call these glands venom glands if they are well-developed, complete with an interior cavity, a duct connecting to a hollow fang, and compressor muscles that generate high pressures when the jaws are rapidly closed. If they lack these features, we usually call them Duvernoy's glands instead. Because there is a lot of variation among snake species in the structure of these glands and their associated teeth, there is some debate about whether or not venom glands and Duvernoy's glands are really two forms of the same thing. Either way, three groups of snakes (atractaspidines, elapids, and viperids) have independently evolved an advanced apparatus to deliver large quantities of venom during a brief strike, and many other snakes (and a few lizards) have evolved less sophisticated, but still relatively effective, modifications to their teeth in order to deliver venom after they have grabbed their prey and are "chewing" on it. The teeth of modern snakes are classically divided into four types, three of which are typically called fangs. The four tooth types have fancy names, all of which involve the Greek word glyph, one of the meanings of which is "groove". They are as follows:

Solenoglyphous

Folding of solenoglyphous fangs.
Fang is in red, maxilla green,
prefrontal orange, pterygoid yellow,
ectopterygoid purple. Vipers lack
premaxillary and palatine teeth.
From Bauchot (2006)

This most sophisticated fang type evolved once, in the ancestor to all modern vipers, which lived in Asia about 40 million years ago. Fossils suggest that solenoglyphous fangs have changed little since that time, even though vipers have undergone an incredibly successful radiation into 320 extant species found on all continents except for Australia and Antarctica. Solenoglyphous fangs are long and tubular and are attached to the snake's maxillary bone. Most snakes have several tooth-bearing bones, including four (the premaxilla, maxilla, pterygoid, and palatine) in the upper jaw, and one (the dentary) in the lower. In humans, three of these bones (the premaxilla, maxilla, and dentary) also bear teeth - your premaxilla holds your top incisors, while your maxilla holds your upper canines and molars and your dentary all your lower teeth - while the others form part of the roof of the mouth. In vipers, the maxilla bears only a single tooth (the fang) and is hinged so that the fangs can be folded back parallel to the jaws when the mouth is closed, or erected perpendicular to the jaws, the position when striking. The teeth in the pterygoids and dentaries work together to manipulate food once it gets into the mouth. Solenoglyphous fangs are strikingly similar to hypodermic needles. They have a hollow core that receives venom from the venom gland at the entrance orifice near the base and injects it from a slit-like exit orifice on the front of the fang near the tip. If the opening were at the very tip of the fang, its strength would be compromised and it would lack the sharp point needed to penetrate the target. Even under normal use, vipers shed their fangs every two months.

Modified solenoglyphous fang of
African Burrowing Asp (Atractaspis engaddensis)

A similar fang type evolved a second time about 29 million years ago in a group of African snakes, currently placed in the family Lamprophiidae, subfamily Atractaspidinae. Two genera, Atractaspis (mole vipers, burrowing asps, or stiletto snakes) and Homoroselaps (African dwarf garter or harlequin snakes), possess elongate anterior fangs, although only those of the stiletto snakes are movable. Stiletto snake fangs pivot on a socket-like joint that is more flexible than those of vipers, allowing these snakes to strike beside and behind them with their mouth closed. This is an adaptation to living underground and envenomating small mammals and other reptiles in narrow subterranean burrows. The fang morphology of atractaspidines and viperids is remarkably similar, considering that these two snake lineages last shared a common ancestor over 40 million years ago.

Proteroglyphous

Proteroglyphous fangs of an Eastern Green Mamba
(Dendroaspis angusticeps). Don't try this.
From Bauchot (2006)

This fang type also evolved only once, in the ancestor to all modern elapids, which lived 25-40 mya in Asia or Africa. Proteroglyphous fangs are in the front of the mouth and are about three times shorter than solenoglyphous fangs. This is because they are not hinged. Snakes with proteroglyphous fangs typically strike their prey and hang on until the venom has taken effect, as opposed to releasing they prey and then tracking it down. Some elapids constrict their prey at the same time as envenomating it. Over 350 species of elapids exist today, including well-known groups such as cobras, mambas, death adders, taipans, coralsnakes, and sea snakes, and less-well-known species, mainly found in Australia, of which a good number are small, secretive, and not considered dangerous to humans.

Maxilla of a proteroglyphous snake showing the almost
completely closed groove along the anterior edge connecting
the two orifices, as well as the aglyphous tooth at the
rear of the maxilla. This line may be obscured in longer fangs.
From Shea et al. 1993

Unlike solenoglyphs, some proteroglyphs have other teeth on the maxilla behind the fang. However, the fang is always separated from the other teeth by a gap, called a diastema. Some elapids have more than one functional fang on each side. In both vipers and elapids, there are usually at least two fangs on each maxilla at any one time, one that is in use and one that is a reserve fang. Both fangs are draped in a layer of connective tissue and skin called the fang sheath. Some proteroglyphs have partially movable fangs, including many of the most dangerous species such as mambas, taipans, and death adders. A few, such as spitting cobras, have modified exit orifices to their fangs that are smaller and rounder than in other cobras, a modification that increases the velocity with which venom is ejected. Modifications to the muscles and the fang sheath also facilitate spitting in these cobras. A few elapids, such as sea snakes that eat only fish eggs, have lost their fangs and their venom glands, which suggests that the primary role of venom, at least among elapids, is in feeding rather than in defense.

Opisthoglyphous

Opisthoglyphous fang of Eastern Hog-nosed Snake

These are commonly known as "rear-fanged" snakes. Opisthoglyphous fangs are grooved rather than hollow and are found near the back of the maxilla, behind the normal teeth. Typically, snakes with rear fangs must chew on their prey to bring their fangs into a biting position. There is considerable variation in the size, shape, and number of opisthoglyphous fangs from species to species, and sometimes even within a species. Most opisthoglyphous fangs are connected to Duvernoy's glands, which differ from true venom glands in several important ways, most notably in that they lack associated muscles to generate the pressure needed to evacuate venom, as in solenoglyphous and proteroglyphous snakes. The pressure on the venom glands of biting solenoglyphs and proteroglyphs can exceed 30 psi, the pressure of a car tire, whereas the pressure inside the Duvernoy's glands of opisthoglyphs is generally less than 5 psi. Because Duvernoy's glands also lack a chamber for storing venom, the idea is emerging that opisthoglyphous snakes probably secrete their venom only during chewing, which explains why prolonged bites by opisthoglyphs generally have more severe effects.

Opisthoglyphous fangs of Boomslang (Dispholidus typus)
Don't do this either.

Most of these snakes are not harmful to humans, with a few notable exceptions. Boomslangs and Twigsnakes are arboreal, diurnal African colubrines that prey on lizards and birds. They have short heads, rear fangs situated comparatively close to the front of the mouth, and partially muscled Duvernoy's glands. They also have potent venoms and their bites have killed several people, including two prominent snake biologists, Karl Schmidt and Robert Mertens. Bites from other rear-fanged snakes are known to cause relatively mild, transient, and local symptoms, but clinical documentation of these bites and their effects is scattered, incomplete, and frequently anecdotal. Many are written by the victim themselves! The above notwithstanding, bites from opisthoglyphs are generally less medically important than those from proteroglyphs and solenoglyphs. As a result, snake venom research has not focused on them, so there is still much that we do not know about this group of snakes, some of which are becoming increasingly common in the pet trade. Based on what little we do know, the composition of opisthoglyph venom/Duvernoy's secretion is fairly similar to that of viperids, elapids and atractaspidines, which makes sense given that each of these groups is more closely related to certain opisthoglyphs than they are to one another.

A: python, B: viper, C: rear-fanged colubroid, D: cobra
The f  marks the portion of the maxilla where the fang develops.
E shows the elongation of the posterior part of the
maxilla pushing forward the developing fang of a
night adder (d.a.o. = days after oviposition)
From Vonk et al. 2008

Unlike the first two groups, opisthoglyphous fangs appear to have evolved more than once, in snakes as diverse as Quill-snouted Snakes, Neck-banded Snakes, and Boomslangs. At least, that's what we used to think. Actually, it is likely that both solenoglyphous and proteroglyphous fangs evolved from opisthoglyphous fangs, as revealed by an ingenious study that used evidence from embryology and genetics to reveal the evolutionary origins of the three types of snake fangs. In a snake embryo, tubular fangs are formed by the infolding of ridges on the front and back sides of the fang, such as those that form the groove of opisthoglyphous fangs. Furthermore, front fangs develop from the rear part of the upper jaw, and are strikingly similar in their formation to rear fangs. They are pushed into the front of the mouth by disproportionate growth of the initially small part of the maxilla that is behind them. Finally, in the anterior part of the maxilla of front-fanged snakes, expression of a gene called sonic hedgehog, which is responsible among other things for the formation of teeth, is suppressed.

Relative size of the venom gland (VG) in
A: rear-fanged colubrid (Helicops leopardinus),
B: boomslang, C: homalopsid,
D: cornsnake, E: African egg-eater
SG = supralabial salivary gland
From Fry et al. 2008

Although developmental similarity is not conclusive proof of structural homology (similarity due to inheritance rather than due to other factors), these findings are consistent with the hypothesis that solenoglyphous, proteroglyphous, and at least some opisthoglyphous fangs are homologous structures. The hypothetical evolutionary trajectory was thus: some snakes evolved grooved fangs in the rear of their mouth. In a few cases (viperids, elapids, and atractaspidines), they subsequently lost the preceding teeth as what was formerly a rear fang became a tubular front fang. Other snakes retained their anterior teeth (at least some non-front-fanged colubroids), and still others developed fangs but then lost them (aglyphs such as ratsnakes). Evidence for this surprising final part comes from the formation of the maxilla and its teeth, which takes place in a single piece in pythons, but from two pieces in all fanged snakes as well as in ratsnakes, a pattern which supports a single evolutionary origin and subsequent loss of fangs. Additionally, vestigial Duvernoy's glands have been found in ratsnakes, egg-eaters, pareatid slug-eaters, and other nonvenomous aglyphs, a discovery that has led to the misleading generalization that all snakes are venomous and much subsequent misunderstanding among the non-scientific community. Toxic saliva does not a venomous animal make, as evidenced by the fact that even human saliva injected subcutaneously will produce pain and swelling.

Aglyphous

Both boas and pythons have only
aglyphous teeth, which is about
the only thing this film got right.

This word is used to describe unmodified teeth, essentially non-fangs. All snakes, even those that possess fangs of the first three types, have aglyphous teeth which they use for gripping their prey as they manipulate it during swallowing. As I just mentioned, many advanced snakes that today have only aglyphous teeth probably evolved from fanged ancestors. Several of these snakes, such as North American kingsnakes, ratsnakes, and bullsnakes, have atrophied Duvernoy's glands that lack toxin-producing serous cells. These snakes employ other sophisticated techniques, such as constriction, which is also used by more primitive snakes like boas and pythons (which did not evolve from fanged ancestors).

There are very few dangerous species of aglyphs, but one, Rhabdophis tigrinus, is becoming well-known as one of the only snakes capable of sequestering toxins from its prey for use in its own defense. This species has enlarged posterior maxillary teeth that lack grooves, so they are by definition aglyphous. However, it has relatively potent venom and has caused the deaths of several people. Among colubroids, the distinction between opisthoglyphs and aglyphs has never been entirely clear, but I'm distinguishing between them here because they are two of the four traditionally recognized types of snake teeth. Although the four types of snake teeth in this article are commonly discussed, a more accurate classification for snake teeth might be to divide them into tubular (the fangs of viperids, elapids, and atractaspidines), grooved (the rear fangs of non-front-fanged colubroids), and ungrooved (all other snake teeth).

Aglyphous (ungrooved) teeth and rear fangs of
Rhabdophis tigrinus
From Mittleman & Goris 1974

Happily for snake biologists like myself, the evolution of fangs opened the door for a massive evolutionary radiation of advanced snakes (>2800 species, or >80% of all living snake species). Although sophisticated venom delivery systems, of which fangs are just one of many integral parts, were clearly evolutionary advantageous, they have obviously also been costly at times, leading to their loss in ratsnakes, egg-eaters, and other lineages of advanced snakes. Also worth noting is that many lineages of basal snakes have got along just fine without venom, so there is not an inherent superiority of being venomous as the word "advanced" seems to imply. Rather, some have suggested that during periods of transition from forest to grassland, such as that which took place simultaneous to the dramatic colubroid radiation during the Miocene, snake taxa that were characterized by slow locomotion and constriction (boas & pythons) were supplanted by those characterized by rapid locomotion (many aglyphous colubrids) or passive immobilization (tubular- and grooved-fanged vipers, elapids, and atractaspidines that could use venom to catch their prey). Of course, both slow locomotion and constriction have subsequently been re-evolved among the colubroids, but there has been a lot of time since the Miocene.

ACKNOWLEDGMENTS

Thanks to Daniel Rosenberg (boomslang fang) and Nick Kiriazis (hognose fang) for use of their photographs.

REFERENCES

Bauchot R, editor. 2006. Snakes: A Natural History. New York, New York: Sterling Publishers. <link>

Cundall, D., (2002) Envenomation strategies, head form, and feeding ecology in vipers. In: Biology of the Vipers: 149-162. G. W. Schuett, M. Höggren, M. E. Douglas & H. W. Greene (Eds.). Eagle Mountain Publishers, Eagle Mountain, UT <link>

Greene, H. W. (1997) Snakes: The Evolution of Mystery in Nature. Berkeley: University of California Press <link>

Fry BG, Scheib H, van der Weerd L, Young B, McNaughtan J, Ramjan SR, Vidal N, Poelmann RE, Norman JA, 2008. Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Mol Cell Proteomics 7:215-246 <link>

Hayes, W. K., S. S. Herbert, G. C. Rehling & J. F. Gennaro, (2002) Factors that influence venom expenditure in viperids and other snake species during predator and defensive contexts. In: Biology of the Vipers: 207-234. G. W. Schuett, M. Höggren, M. E. Douglas & H. W. Greene (Eds.). Eagle Mountain Publishers, Eagle Mountain, UT <link>

Jackson K, 2002. How tubular venom‐conducting fangs are formed. J Morphol 252:291-297 <link>

Kardong, K. V. & T. L. Smith, (2002) Proximate factors involved in rattlesnake predatory behavior: a review. In: Biology of the Vipers: 253-266. G. W. Schuett, M. Höggren, M. E. Douglas & H. W. Greene (Eds.). Eagle Mountain Publishers, Eagle Mountain, UT <link>

Kardong KV, 1996. Snake toxins and venoms: an evolutionary perspective. Herpetologica 52:36-46 <link>

Kuch, U., J. Müller, C. Mödden & D. Mebs (2006). Snake fangs from the Lower Miocene of Germany: evolutionary stability of perfect weapons. Naturwissenschaften 93, 84-87

LaDuc, T. J., (2002) Does a quick offense equal a quick defense? Kinematic comparisons of predatory and defensive strikes in the Western Diamond-backed Rattlesnake (Crotalus atrox). In: Biology of the Vipers: 267-278. G. W. Schuett, M. Höggren, M. E. Douglas & H. W. Greene (Eds.). Eagle Mountain Publishers, Eagle Mountain, UT <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.

Stiletto snakes

Click here to view this article in Spanish!

Haga clic aquí para ver este artículo en español!

Atractaspis duerdeni

I've always thought that the atractaspids were a highly interesting group of snakes, deserving of an article or two. During the early stages of my cursory research, however, I found that palaeozoologist Darren Naish, author of the excellent blog Tetrapod Zoology, has already written an article containing what one commenter called "the most comprehensive information on Atractaspids anywhere on the web." Since I didn't think I could top that, I decided to focus on what we've learned about atractaspids since Darren's article came out in 2008. If you want to learn more about the many fascinating adaptations atractaspids have evolved for burrowing and closed-mouth fang-stabbing, including why they're known as والد من سواد ('father of blackness'), among other such macabre names, in Arabic-speaking countries in their native range, you'll want to read that article in addition to this one.

The correct placement of the atractaspids within the snake tree of life has been elusive since their initial description in 1843, when they were placed in the Elapidae alongside cobras and coralsnakes. In later classifications, they have been placed in the Viperidae, the Colubridae, the Lamprophiidae, or in their own family, to which various names have been applied, including Atractaspidae (atractaspids), Atractaspididae (atractaspidids, because why not add in an extra 'id'?), and Atractaspidinae (atractaspidines; this last name referring to a subfamily rather than a family). Once considered to include a wider diversity of snakes, the Atractaspidinae is now comprised of just two genera, the proteroglyphous Homoroselaps (2 species, known as Harlequin Snakes) and the eponymous, solenoglyphous Atractaspis (21 species). Aglyphous and opisthoglyphous snakes formerly included in this group are now assigned to a closely related subfamily, the Aparallactinae, which includes 50 species in nine genera, several of which are deserving of their own articles. This taxonomy is based on part of a larger analysis of advanced snakes undertaken by Alex Pyron and colleagues and published in 2010, and hinted at in earlier analyses such as this one by Kraus & Brown.

Part of the tree presented in Pyron et al. 2010, showing the relationships of atractaspids to other African snakes now placed in the Lamprophiidae. A surprising finding of this paper was that lamprophiids share a common ancestor with the front-fanged elapids, including cobras, sea snakes, and coral snakes, about 44 million years ago.

Morphological work on atractaspids has continued to be carried out by Dave Cundall and his students and colleagues at Lehigh University. I had the opportunity to hang out with Dave a bit recently, and he shared some of his recent findings with me. For instance, he said, the long-held idea that Atractaspis fed predominantly on litters of baby mammals might be only party true. The stomach of some atractaspids, he told me, is almost as long as the entire body, an adaptation that could be construed as functioning to accommodate multiple prey items (pups in a litter) but also large, elongate ones (such as amphisbaenians or caecilians), which also frequently occupy underground spaces where hunting by fang-stabbing is effective. Dave also mentioned that digestion in these snakes takes place, as one might expect, only in the stomach, not in the esophagus, although ingested prey may extend forward into the esophagus if they are too large to fit in the stomach. Differences in the tissue lining these two parts of the digestive system account for a pH change of up to 4 units between the esophagus and the stomach, one of the few clues that these two organs in snakes are derived from separate structures in other vertebrates (since their morphological separation in many snakes is subtle at best). Other discoveries made by Dave and his student Alex Deufel, including how atractaspids, perhaps uniquely among advanced snakes, have traded-off prey transport for maximum fang-stabbing ability, have been described in excellent detail by Darren at TetZoo.

No one is quite sure why, but some Atractaspis also possess extremely elongate venom glands, such as those seen here in a dissected A. fallax.

Other recent work on atractaspids includes advances in understanding their unusual venom chemistry and in treating its effects, including the discovery and production of the first atractaspid antivenom in 2007. In a test of this antivenom conducted at the National Antivenom and Vaccine Production Center in Riyadh, Saudi Arabia, rabbits injected with a lethal dose of Atractaspis venom were saved from death by a pre-injection treatment of any one of three drugs: nitroglycerin, atractaspid antivenom, or bosentan, a drug for the treatment of pulmonary hypertension. However, when the drugs were administered after the venom, as would be the case in an actual snakebite, all rabbits treated with nitroglycerin and half the rabbits treated with atractaspid antivenom died. Only the hypertension drug bosentan protected rabbits from the venom in the realistic scenario, leading the author to conclude that bosentan might have a higher affinity to the venom receptors than either the antivenom or the venom compounds themselves.

Atractaspis engaddensis

Finally, a 2011 study by Katie Moyer and Kate Jackson of Whitman College helped initiate our understanding of how the 21 species of Atractaspis are related to one another. Remarkably, this is the first time someone has investigated this question, and because Moyer & Jackson used morphological data, there are likely to be some changes once DNA sequences for these species become available. Using characteristics of the scale arrangements, they prepared an evolutionary tree that differed from all previous hypotheses about how the species of Atractaspis are related. Although their analysis is limited by the paucity of available data, it represents a starting point for understanding the evolution of this highly unique group of snakes.

ACKNOWLEDGMENTS

Thanks to Michael & Patricia Fogden and Donald Schultz for photographs.

REFERENCES

Abd-Elsalam M, 2011. Bosentan, a selective and more potent antagonist for Atractaspis envenomation than the specific antivenom. Toxicon 57:861-870.

Bourgeois M, 1961. Atractaspis – a misfit among the Viperidae? News Bulletin of the Zoological Society of South Africa 3:29.

Deufel A, Cundall D, 2003. Feeding in Atractaspis (Serpentes: Atractaspididae): a study in conflicting functional constraints. Zoology 106:43-61.

Greene HW, 1997. Snakes: The Evolution of Mystery in Nature. Berkeley: University of California Press.

Ismail M, Al-Ahaidib M, Abdoon N, Abd-Elsalam M, 2007. Preparation of a novel antivenom against Atractaspis and Walterinnesia venoms. Toxicon 49:8-18.

Moyer K, Jackson K, 2011. Phylogenetic relationships among the Stiletto Snakes (genus Atractaspis) based on external morphology. African Journal of Herpetology 60:30-46.

Naish D, 2008. Side-stabbing stiletto snakes. Tetrapod Zoology.
<http://scienceblogs.com/tetrapodzoology/2008/05/26/sidestabbing-stiletto-snakes/>

Pyron RA, Burbrink FT, Colli GR, de Oca ANM, Vitt LJ, Kuczynski CA, Wiens JJ, 2010. The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol Phylogenet Evol 58:329-342.

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