Neck-banded snakes (Genus Scaphiodontophis)

"Hi, I'm the bastard love-child of Lampropeltis triangulum and Storeria dekayi."

Also called Shovel-toothed Snakes or Skink-eaters, the members of the genus Scaphiodontophis are among the most unusually-patterned snakes. The one at the left should probably be called a neck-and-tail-banded snake, although I admit that's a little cumbersome.

As you can see, these snakes' patterns are just ridiculous. It looks like someone erased the middle third of a milksnake. But in fact this is how they evolved, for reasons we can only guess.

Well, we can do a bit more than guess. In an incredible 66 page paper in Biological Journal of the Linnean Society, Jay Savage and Joe Slowinski examined the morphology, taxonomy, variation, coloration, and behavior of Scaphiodontophis, and reached some very interesting conclusions.

Let's dispense with some basic biology first. These are non-venomous, diurnal, leaf-litter snakes found in humid evergreen forests. They are the only New World colubrines with hinged teeth, which are useful for eating skinks and other hard-bodied prey. The tail of adult Scaphiodontophis is an incredible 39 to 49% of the total length, disproportionately thick (*ladies*), fragile (d'oh!), and the autotomy of which probably acts as an antipredator device, much as it does in many lizard and salamander groups. Specifically, it reminds me of the glass lizards of the southeastern USA (genus Ophisaurus), whose tails can be a whopping 50-75% of their total length!

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Male Eastern Slender Glass Lizard (Ophisaurus attenuatus longicaudus) from Baker County, GA - Photo by E. Pierson Hill

So what is up with the coloration? At first glance it looks like just another coral-mimic, but a closer look reveals unparalleled pattern diversity in this genus. Individual snakes can have a pattern of tricolor monads (which are red bands separated by light-black-light), tricolor dyads (red separated by black-light-black), or even tricolor triads (red separated by black-light-black-light-black) or tetrads (red separated by...you get the idea). These sometimes extend along the entire body, are sometimes just on the anterior end, and are sometimes on the anterior and posterior but not the middle, as in the picture above. To make matters even worse, the black and yellow bands are sometimes offset so that they alternate with one another on the two sides of the body. Also, "as though the extreme variability of dorsal, head, nuchal, and subcaudal coloration were not sufficient to confound any attempt at systematic analysis," lament S&S, it all changes ontogenetically within an individual snake. Plus, many of the descriptions came from preserved specimens, whose coloration had changed due to the effects of preservative. Unsurprisingly, due to all of this variation, as many as seven different species of Scaphiodontophis were recognized at any one time.

Now in Technicolor!

In the 1950s and 1960s, discovery of co-occurrence and intergradation between these forms (sometimes on the same snake!) led herpetologists during the 70s and 80s to reclassify them based on nuchal pattern and coloration, resulting in a bizarre biogeographic pattern wherein two completely allopatric populations, one in central and eastern Panama and Colombia and the other in northern Central America, comprised S. annulatus, with S. venustissimus occupying the intervening geographic area. Anyone who knows anything about biogeography knows that this makes no sense, but it was the best we could do with the limited information we had. Specimens of many neotropical snakes are still hard to come by.

Anyhow, Savage and Slowinski sorted these descriptions out and synthesized all the known information on Scaphiodontophis, as well as a bunch of new information that they collected, and concluded that really there was just one highly variable species, whose dorsal color patterns could comprise an entire new semaphore alphabet.

It spells 'Suck it, herpetologists'

Towards the end of their section on variation, the authors conclude that "No two Scaphiodontophis have the same coloration when head, nuchal, body and tail patterns are considered in combination," which is pretty cool when you think about it. They developed a detailed system of notation for describing the color pattern of an individual Scaphiodontophis, which for one snake looks like: wZ/B-6D-22/2M-S/2M/u+. Seriously.

So what explains all this diversity of pattern? Well, your first question should probably be: why isn't the whole body banded? We have a partial answer to this question. This snake is an ambush predator, and it's typically found sitting motionless with the anterior third of its body exposed and the posterior remainder buried in the leaf litter. If that sounds like b-s (it did to me), check out this picture, apparently taken in captivity, of a Scaphiodontophis in "typical diurnal posture".

Photo from Henderson (1984)

This apparently unique juxtaposition of behavior and microhabitat might be responsible for differences in the type of pattern favored by selection on different parts of the snakes' bodies. That is to say, it is advantageous for the exposed part of the body to bear an aposematic banding pattern, for the same reason that favors the pattern in other Batesian mimics of venomous coral snakes -  the mimic (in this case, Scaphiodontophis) is parasitizing the honest warning signal of the venomous species (here, the coral snakes, genus Micrurus) and deterring predation, without having to go to the expense of developing venom or other defenses itself. However, this still doesn't explain what the disadvantage of having a banded posterior or middle body section would be - but clearly there is one, or else the entire snake should be banded (as a few populations in Nicaragua, Costa Rica, and Panama are). 

It's kind of like being a very inflexible chameleon.

It could also be that producing the bright red, yellow, and black pigments is energetically expensive, but coral snakes and many coral mimics (e.g., Lampropeltis, Erythrolamprus, Urotheca, Lystrophis) seem to do it just fine. I think it's more likely regional variation in predator response, but that idea requires rigorous testing.

What of the banding on the tail of some individuals of this species? I hinted at this already above when I mentioned that the tail is very fragile and can be urotomized like a lizard's. If the aposematic colors aren't sufficient to keep a predator from attacking (or if a predator is naïve or stupid and attacks anyway), Scaphiodontophis will thrash its head and tail about, presumably to emphasize the aposematic coloration ("are you *sure* you want to attack this?"). This behavior, combined with the bright tail coloration in some individuals, probably serves to direct predatory attacks toward the tail,. When physically restrained, the tail is easily broken between any two caudal vertebrae, allowing the snake to escape. This form of urotomy (tail breakage) is known as pseudautotomy, because the break is not under nervous control. Furthermore, the tail cannot be regrown, as it can in many lizards (which regrow their tails around cartilaginous rods) and salamanders (which can regrow their entire tail, bones and all). Instead, a calcified cap forms over the distal end of the broken tail. In museum collections, >70% of adult Scaphiodontophis have incomplete tails. S&S found no significant differences between differently-patterned Scaphiodontophis in the probability of having a broken tail, indicating that predation risk is approximately uniform across all patterns and populations. However, they did find indirect evidence that older (larger) individuals had shorter tails that had probably been broken more times than younger (smaller) snakes.

Residuals refers to the difference between the tail length of each snake specimen examined and the average tail length of snakes that size. SVL stands for snout-vent length, a common measure of snake size.

Savage and Slowinski point out that two other neotropical snake genera, Enulius and Urotheca, have convergently evolved thick, fraglie tails suited to urotomy. Two species of Urotheca are coral snake mimics, like Scaphiodontophis. So passive physical defenses, such as tail pseudautotomy. might serve as a secondary defense for Batesian mimics in the event that their mimicry is ineffective and elicits an attack. For example, other coral mimcs in Argentina, especially Lystrophis semicinctus, use thanatosis (death-feigning), another passive defense elicited by physical contact by a predator. 

South American Ringed Hog-nosed Snake - Lystrophis semicinctus

Studies have shown that coral snake mimics don't have to match the exact pattern of a coral snake very closely in order for motmots and kiskadees (predatory birds) to avoid them, and that they will direct attacks at the unbanded portion of a model if one end is banded and the other not. This could explain the partially-banded patterns. But if anything is to be learned from the history of research on Scaphiodontophis, it is that nothing about these incredibly interesting snakes is as simple as it seems.

ACKNOWLEDGMENTS 

Thanks to photographers Silviu Petrovan, Mauricio Rivera, Pierson Hill, Jaroslav Vogeltanz, and Jairo Maldonado for the use of their photos.

REFERENCES

Duméril, C., G. Bibron, and A. Duméril. 1854. Erpetologie Générale on Histoire Naturelle Compléte des Reptiles. Librairie Encyclopédique de Roret, Paris. 780 pages.
Dunn, E. R. 1954. The coral snake mimicry problem. Evolution 8:97-102.
Henderson, R. 1984. Scaphiodontophis (Serpentes: Colubridae): natural history and test of a mimicry-related hypothesis. Special Publication, University of Kansas Museum of Natural History 10:185-194.
Morgan E, 1973. Snakes of the subfamily Sibynophiinae [PhD dissertation]: University of Southwestern Louisiana.
Pyron, R. A., F. T. Burbrink, G. R. Colli, A. N. M. de Oca, L. J. Vitt, C. A. Kuczynski, and J. J. Wiens. 2010. The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Molecular Phylogenetics and Evolution 58:329-342.
Sasa, M. and S. Curtis. 2006. Field observations of mating behavior in the neck-banded snake Scaphiodontophis annulatus (Serpentes: Colubridae). Revista de Biologia Tropical 54:647-650.
Savage, J. M. and J. B. Slowinski. 1996. Evolution of coloration, urotomy and coral snake mimicry in the snake genus Scaphiodontophis (Serpentes: Colubridae). Biological Journal of the Linnean Society 57:129-194.
Savitzky, A. H. 1981. Hinged teeth in snakes: an adaptation for swallowing hard-bodied prey. Science 212:346-349.
Slowinski, J. B. and J. M. Savage. 1995. Urotomy in Scaphiodontophis: evidence for the multiple tail break hypothesis in snakes. Herpetologica 51:338-341.
Smith, S. 1975. Innate recognition of coral snake pattern by a possible avian predator. Science 187:759-760.
Smith, S. 1977. Coral snake pattern recognition and stimulus generalization by naïve greater kiskadee (Aves: Tyrannidae). Nature 265:535-536.
Taylor, E. and H. Smith. 1943. A review of American sibynophine snakes, with a proposal of a new genus. University of Kansas Science Bulletin 29:301-337.

APPENDIX

Like a lot of species, Scaphiodontophis annulatus has a complex nomenclatural history. Now, I'm not trying to say that 19th century taxonomists sucked at their jobs, especially not considering the variation they had to work work (above) and the difficulty of getting specimens and literature, but man did Scaphiodontophis get mis-named a lot. It was first called Ablabes annulatus by Constant Duméril in 1853, but this name is invalid because he didn't include a full description of the species along with it, anticipating that such a description would be published the following year. The reason he anticipated this was because he himself was planning to do so, and he did, along with his son Auguste and assistant Gabriel Bibron, at which time they placed it in a subgenus of Ablabes, which they called Enicognathus (Greek for 'single jaw'). Unfortunately for  Duméril & colleagues, Enicognathus was already in use for a species of Chilean parakeet. When E. D. Cope realized this in 1875, he changed the subgenus to Henicognathus, presumably with instructions to anyone who owned a copy of  Duméril's book to "just add an H to the beginning" in order to save everyone a lot of work. This plan backfired, however, because Henicognathus was also already in use (Louis Agassiz had used the same 'add an H' trick in 1846 for the bird genus). Fortunately, the Belgian zoologist George Albert Boulenger, in ignorance of Cope's invalid change (but rightfully for the same reason as Cope), specified another replacement subgenus for Duméril's invalid one: Polydontophis, which means 'many toothed snake' in Greek, sometimes spelled  Polyodontophis.

Bear with me, because here is where it gets complicated. Subgenera are not often used these days, although there has been a push to bring them back, but they can be moved between genera just as genera can be moved between families. In 1910, Leonhard Stejneger moved the three synonymous subgenera (Enicognathus, Henicognathus, and Polydontophis) from Ablabes to Herpetodryas. The genus Herpetodryas had been in existence since 1837, when it was created by Hermann Schlegel to house what he called "les formes élancées elles habitudes des serpens d'arbre" - the slender tree snakes, many of which have very long tails. Howeber, in order to understand Stejneger's placement of the neck-banded snake in Herpetodryas, we have to backtrack to before Duméril's description of Ablabes annulatus. In 1826, Friedrich Boie described a new species of snake, collected by his brother Heinrich on a lethal trip to Java, that he called Coluber geminatus. Antedated by Linnaeus' Systema Naturae by only 68 years, Boie chose to place his new snake in the genus Coluber because it was one of the very few snake genera in existence at the time. It was not uncommon for later authors to split up genera that were becoming large, and the herpetologist Hermann Schlegel did just this in 1837, moving C. geminatus into a new genus, Herpetodryas. Shortly thereafter, Austrian zoologist Leopold Fitzinger moved the species again, into a new genus he called Sibynophis (Duméril was ignorant of this name but aware of Schlegel's, or else we can presume he might have used  Sibynophis instead of Ablabes in 1853, because he placed Herpetodryas geminatus in Ablabes at that time without recognizing Sibynophis geminatus as a synonym). This meant that, in 1910 when Stejneger moved Ablabes  (Polydontophis) annulatus back into Herpetodryas, he was really moving it to Fitzinger's  Sibynophis (he noted this). This actually made sense, because we now know that Sibynophis and Scaphiodontophis are each others' closest relatives - together, they made up the subfamily Sibynophiinae, according to Dunn (1928). However, because one is found in the Old World and the other in the New, Taylor and Smith split the genus in 1943, assigning the species (seven of Scaphiodontophis, nine of Sibynophis)  their modern names. Another similar genus of snakes from Madagascar, Liophidium, was initially included in the genus Sibynophis by some authors, morphological and biogeographic clues has led herpetologists to place them in the subfamily Pseudoxyrhophiinae instead.

Recently, Pyron et al. (2010) erected a new subfamily of Colubridae for Scaphiodontophis, on the basis of molecular differences from the other colubrids, which they called Scaphiodontophiinae. This serves to emphasize the differences between this genus and its relatives, which are certainly many. However, Pyron et al.'s tree did not include genetic data from Sibynophis, a genus of Asian colubrids and the putative closest relatives of Scaphiodontophis. At the very least, the inclusion or exclusion of Sibynophis from Scaphiodontophiinae needs clarification, and at most, the effect of these sequences on the overall tree structure should be assessed, because it may be that the degree of difference between Scaphiodontophis and other colubrids is not sufficient to warrant a separate subfamily. If Sibynophis and Scaphiodontophis together form a subfamily, then Pyron et al.'s name for that taxon is preoccupied by the name Sibynophiinae.