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Sunday, September 9, 2018

Venom resistance in kingsnakes

A kingsnake eating a western diamondback rattlesnake
Kingsnakes get their name because they eat other snakes, including venomous snakes like copperheads, cottonmouths, and rattlesnakes. They also eat lots of other kinds of prey, including non-venomous snakes, lizards, turtle eggs, and small mammals.

You often hear people say that kingsnakes are resistant or immune to the venom of copperheads, cottonmouths, and rattlesnakes. There is a subtle difference between the meaning of these two words.

Resistance is any physiological ability to tolerate or counteract the effects of a toxin or disease. Like many things in biology, resistance is not an all-or-nothing status, but a gradient. High enough resistance can result in immunity, where the toxin or disease has negligible or no effects.

A kingsnake eating a cottonmouth
Individuals can acquire resistance through repeated exposure to low doses of a toxin. The immune system recognizes the toxin as foreign and attacks it. It forms a memory of each attack and stores the pattern for later, which makes later responses to the same toxin quicker and more effective. If the toxin dose is later increased, the memory is reinforced & may become stronger. This is how antivenom is made, how people become resistant to snake venom, and also how vaccines against infectious diseases work.1

It is not how kingsnake resistance to viper venom works. Kingsnake resistance is evolved rather than acquired. This means that kingsnakes are born resistant to venom. As far as we know, their resistance levels are fixed for life & don’t change with age or exposure. This has happened over a long time through natural selection, over many generations of kingsnakes. We don't actually have a very exact  understanding of the physiological and molecular mechanisms behind how kingsnakes resist the toxic effects of viper venom. At least some of their resistance comes from antibodies—chemicals in their blood that interfere with the venom—because mice injected with kingsnake blood survive viper venom better than those that aren't, and the chemical composition of kingsnake blood changes after exposure to viper venom.

A kingsnake eating a western hognose snake
Any time a weapon appears, there is potential for counter-weapons (i.e. resistance and immunity) to appear in response. This happens through a process called a co-evolutionary arms race2. Just as the United States and the Soviet Union were involved in an arms race centered around nuclear weapons during the Cold War, so are venomous snakes and their prey & predators involved in arms races centered around their primary weapon—venom.

A major difference is that, unlike nations or humans, animals cannot plan for the future and decide to invest more energy in research & development of novel or better weapons technology for future generations. Instead, co-evolutionary arms races happen through natural selection. What start out as tiny variations in toxin resistance can be magnified over many generations. 

A kingsnake and a copperhead biting one another
When vipers were first evolving their front fangs, defensive bites became a new option for them. At first, their predators were probably not very good at resisting the effects of the venom, especially if the predator’s physiology was similar to that of their prey, and venom would have made a very good defense mechanism. Vipers would sometimes be killed and eaten, but many predators later died from their bites. Kingsnake predators that were slightly better able to tolerate the effects of the venom were more likely to survive. Eventually, all the kingsnakes without these venom resistance traits had been killed by vipers that they tried to eat, and only the resistant ones remained. On the other side, vipers that had venom with toxins that were, for example, slightly more painful or fast-acting, might have been more likely to survive a predatory attack. Thus, the arms race escalates. Vipers also exhibit flipping, jerking, “body bridging” and other escape behaviors as a defense against kingsnakes—suggesting, since they do not try to bite kingsnakes in defense, that their venom is essentially useless as an anti-kingsnake defense mechanism by now and that kingsnakes have “won” this arms race.

A mongoose eating a boomslang
This is why kingsnakes are immune to the venom of copperheads, cottonmouths, and North American rattlesnakes, but not to the venom of, for example, king cobras or black mambas. Because they live on different continents, there has never been an opportunity for kingsnakes and black mambas to enter into a co-evolutionary arms race (although both prey and predators of black mambas in Africa, such as honey badgers, and of king cobras in India, such as mongeese, have probably accomplished much the same thing).

Kingsnakes also eat coralsnakes, but amazingly they are not immune to the venom of Eastern Coralsnakes (Micrurus fulvius)—kingsnakes injected with coralsnake venom die quickly, and kingsnake blood is 0% effective at neutralizing venom proteins from coralsnakes. Presumably they are able to catch and consume coralsnakes without getting bitten. This could be because coralsnakes often eat other snakes, so perhaps their venom is more difficult for kingsnakes to evolve resistance against. Or, perhaps coralsnakes are rare or dangerous prey for kingsnakes, and it’s possible but not worth it for them to evolve resistance.

A milksnake constricting a Dekay's brownsnake
Not every kingsnake species has been tested against every venom, but we do know that there is variation in which species are immune to which venoms. The only study to compare species in depth injected mice with mixtures of venom & snake blood and measured mouse symptoms and survival. They found that blood from Eastern Kingsnakes (Lampropeltis getula) had the widest spectrum of protection against the venoms tested and was the most effective at neutralizing many rattlesnake venoms, but the least effective against copperhead venom. Blood from kingsnakes from Florida & the Gulf Coast was the most effective at neutralizing the venom of copperheads & cottonmouths. Mole Kingsnake (Lampropeltis calligaster) blood is about 75% as effective at neutralizing Mojave Rattlesnake (Crotalus scutulatus) venom as the blood of Eastern Kingsnakes. Gray-banded Kingsnakes (L. alterna) have moderate neutralization potential against Western Diamondback (C. atrox) venom, but none against Eastern Diamondback (C. adamanteus) venom. Blood from milksnakes (formerly all called L. triangulum) from various locations had intermediate neutralization capacity, with blood from North American milksnakes being about 70% more effective against rattlesnake venom than blood from Central American milksnakes. Another study found that an eastern milksnake injected with copperhead venom died, and one injected with pigmy rattlesnake venom had "no noticeable ill effects", but a lack of replication prevents these results from being particularly meaningful. Somewhat surprisingly, blood from Long-nosed Snakes (Rhinocheilus lecontei), Cornsnakes (Pantherophis guttatus), Mussuranas (Clelia clelia), and Japanese Four-lined Ratsnakes (Elaphe quadrivirgata) was also effective at protecting mice from viper venoms, but blood from pinesnakes (Pituophis) and gartersnakes (Thamnophis) was not. Both vipers and elapids appear to have at least some level of resistance to their own venom, although detailed studies are lacking for most species.

Fight of the Mongoose and the Serpent Armies
An 1850 folio from the Mahabharata
Kingsnakes are just one of many species that have partial immunity or resistance to venom. Hedgehogs, skunks, opossums, and possibly snake-eagles also have resistance to viper venoms, and eels are resistant to sea krait venom. Unlike kingsnakes, we have actually figured out exactly which proteins in opossum blood are responsible for its snake venom neutralization capacity. We also know that mongeese have followed a different route, changing the shape of the toxin targets in their cells rather than putting molecules into their blood to combat the toxins (which means that their immunity cannot be transferred). Other predators of venomous snakes, such as indigo snakes (genus Drymarchon), appear to have gotten away with not evolving immunity, although I was unable to find any actual data on physiological responses of indigo snakes to venom, just statements saying they were not resistant, so it's possible that actual tests have not been carried out.

A mountain kingsnake constricting a skink
Opossum resistance to copperhead venom probably evolved in a similar way to kingsnake resistance, but vipers are also involved in co-evolutionary arms races with their prey. Many rodent prey of North American vipers are resistant, including wood rats, prairie voles, and ground squirrels. Think of how the U.S. during the Cold War had to balance foreign policy not just with the Soviet Union, but also with other nations. The emerging foreign policy is a compromise, just as the venom that evolves is a compromise of selection pressures from predators and prey. Resistant prey may select for venoms that are better at quickly incapacitating, whereas resistant predators may select for venoms that are less deadly and more painful; it’s difficult to predict exactly what will happen without knowing the exact mechanism of resistance. Sometimes selection from predators and prey may act in the same direction, other times in opposite directions. The details of these processes are what evolutionary biologists study on a day-to-day basis.



1 Creating a vaccine against snake venom is harder than creating one against an infectious disease that is caused by a virus or a bacterium. There are pit viper venom vaccines available for dogs and horses, made from the venom of Western Diamondback Rattlesnakes, but none are available for humans. Additionally, the canine vaccines must be given twice per year, immediate veterinary care is still required, & protection against other species of venomous snakes is poor, so the technology has a long way to go.



2 The most famous co-evolutionary arms race is between toxin-resistant gartersnakes & tetrodotoxin-defended newts in the Pacific Northwest of the US & Canada, although there are many others, such as that between most pathogens & the immune systems of their hosts, between brood parasites such as cuckoos & their hosts, and between bad-tasting plants and herbivores.


ACKNOWLEDGMENTS

If you want to know more, I'd suggest chapter 3 of Christie Wilcox's book Venomous, from which I drew while researching & writing this article. Thanks to Connie Wade, Pierson Hill, Alan Cressler, Joe McDonald, Elana Erasmus, and the Los Angeles County Museum of Art [public domain] via Wikimedia Commons for providing their images for this article. Thanks to Laura Connelly for reading a draft of this article.

REFERENCES

A kingsnake eating a ringneck snake
Barchan, D., S. Kachalsky, D. Neumann, Z. Vogel, M. Ovadia, E. Kochva, and S. Fuchs. 1992. How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. Proceedings of the National Academy of Sciences 89:7717-7721 <full-text>

Bdolah, A., E. Kochva, M. Ovadia, S. Kinamon and Z. Wollberg. 1997. Resistance of the egyptian mongoose to sarafotoxins. Toxicon 35:1251-1261 <abstract>

Bonnett, D. E. and S. I. Guttman. 1971. Inhibition of moccasin (Agkistrodon piscivoris) venom proteolytic activity by the serum of the Florida king snake (Lampropeltis getulus floridana). Toxicon 9:417-425 <abstract>

Carpenter, C. C. and J. C. Gillingham. 1975. Postural responses to kingsnakes by crotaline snakes. Herpetologica 31:293-302 <PDF>

Cates, C. C., E. V. Valore, M. A. Couto, G. W. Lawson, and J. G. McCabe. 2015. Comparison of the protective effect of a commercially available western diamondback rattlesnake toxoid vaccine for dogs against envenomation of mice with western diamondback rattlesnake (Crotalus atrox), northern Pacific rattlesnake (Crotalus oreganus oreganus), and southern Pacific rattlesnake (Crotalus oreganus helleri) venom. American Journal of Veterinary Research 76:272-279 <PDF>

Darawshi, S., U. Motro, and Y. Leshem. 2006. The ecology of the Short-toed Eagle (Circaetus gallicus) in the Judean Slopes Israel. The Rufford Foundation, RSG project, detailed final report <project>

de Wit, C. A. 1982. Resistance of the prairie vole (Microtus ochrogaster) and the woodrat (Neotoma floridana), in Kansas, to venom of the Osage copperhead (Agkistrodon contortrix phaeogaster). Toxicon 20:709-714 <abstract>

de Wit, C. A. and B. R. Weström. 1987. Venom resistance in the hedgehog, Erinaceus europaeus: purification and identification of macroglobulin inhibitors as plasma antihemorrhagic factors. Toxicon 25:315-323 <abstract>

Drabeck, D. H., A. M. Dean, and S. A. Jansa. 2015. Why the honey badger don't care: Convergent evolution of venom-targeted nicotinic acetylcholine receptors in mammals that survive venomous snake bites. Toxicon 99:68-72 <academia.edu>

Heatwole, H. and J. Powell. 1998. Resistance of eels (Gymnothorax) to the venom of sea kraits (Laticauda colubrina): a test of coevolution. Toxicon 36:619-625 <PDF>

Holding, M. L., D. H. Drabeck, S. A. Jansa, and H. L. Gibbs. 2016. Venom Resistance as a Model for Understanding the Molecular Basis of Complex Coevolutionary Adaptations. Integrative and Comparative Biology 10.1093/icb/icw082 <full-text>

Jansa, S. A. and R. S. Voss. 2011. Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PLoS ONE 6:e20997 <full-text>

Keegan, H. L. and T. F. Andrews. 1942. Effects of crotalid venom on North American snakes. Copeia 1942:251-254 <PDF>

Keegan, H. L. 1944. Indigo snakes feeding upon poisonous snakes. Copeia 1944:59 <PDF>

Lee, C.-Y., editor. 1979. Snake Venoms. Springer-Verlag, Berlin. <full-text>

Liu, Y.-B. and K. Xu. 1990. Lack of the blocking effect of cobrotoxin from Naja naja atra venom on neuromuscular transmission in isolated nerve muscle preparations from poisonous and non-poisonous snakes. Toxicon 28:1071-1076 <abstract>

Lomonte, B., L. Cerdas, J. Gené, and J. Gutierrez. 1982. Neutralization of local effects of the terciopelo (Bothrops asper) venom by blood serum of the colubrid snake Clelia clelia. Toxicon 20:571-579 <abstract>

Moussatché, H. and J. Perales. 1989. Factors underlying the natural resistance of animals against snake venoms. Memorias do Instituto Oswaldo Cruz 84:391-394 <PDF>

Neves-Ferreira, A. G., N. Cardinale, S. L. Rocha, J. Perales, and G. B. Domont. 2000. Isolation and characterization of DM40 and DM43, two snake venom metalloproteinase inhibitors from Didelphis marsupialis serum. Biochimica et Biophysica Acta (BBA)-General Subjects 1474:309-320 <abstract>

Nichol, A. A., V. Douglas, and L. Peck. 1933. On the immunity of rattlesnakes to their venom. Copeia 1933:211-213 <PDF>

Ovadia, M. and E. Kochva. 1977. Neutralization of Viperidae and Elapidae snake venoms by sera of different animals. Toxicon 15:541-547 <abstract>

Perez, J. C., W. C. Haws, V. E. Garcia, and B. M. Jennings III. 1978. Resistance of warm-blooded animals to snake venoms. Toxicon 16:375-383 <abstract>

Perez, J. C., W. C. Haws, and C. H. Hatch. 1978. Resistance of woodrats (Neotoma micropus) to Crotalus atrox venom. Toxicon 16:198-200 <abstract>

Perez, J. C., S. Pichyangkul, and V. E. Garcia. 1979. The resistance of three species of warm-blooded animals to western diamondback rattlesnake (Crotalus atrox) venom. Toxicon 17:601-607 <abstract>

Philpot, V. 1954. Neutralization of snake venom in vitro by serum from the nonvenomous Japanese snake Elaphe quadrivirgata. Herpetologica 10:158-160 <PDF>

Philpot, V. and R. G. Smith. 1950. Neutralization of pit viper venom by king snake serum. Experimental Biology and Medicine 74:521-523 <abstract>

Philpot, V. B., E. Ezekiel, Y. Laseter, R. G. Yaeger, and R. L. Stjernholm. 1978. Neutralization of crotalid venoms by fractions from snake sera. Toxicon 16:603-609 <abstract>

Poran, N. S., R. G. Coss, and E. Benjamini. 1987. Resistance of California ground squirrels (Spermophilus beecheyi) to the venom of the northern Pacific rattlesnake (Crotalus viridis oreganus): a study of adaptive variation. Toxicon 25:767-777 <abstract>

Swanson, P. L. 1946. Effects of snake venoms on snakes. Copeia 1946:242-249 <full-text>

Voss, R. S. and S. A. Jansa. 2012. Snake-venom resistance as a mammalian trophic adaptation: lessons from didelphid marsupials. Biological Reviews 87:822-837 <PDF>

Weinstein, S. A., C. F. DeWitt, and L. A. Smith. 1992. Variability of venom-neutralizing properties of serum from snakes of the colubrid genus Lampropeltis. Journal of Herpetology 26:452-461 <PDF>

Weldon, P. J. 1982. Responses to ophiophagous snakes by snakes of the genus Thamnophis. Copeia 1982:788-794 <PDF>

Weldon, P. J. and G. M. Burghardt. 1979. The ophiophage defensive response in crotaline snakes: extension to new taxa. Journal of Chemical Ecology 5:141-151 <PDF>

Weldon, P. J. and F. M. Schell. 1984. Responses by king snakes (Lampropeltis getulus) to chemicals from colubrid and crotaline snakes. Journal of Chemical Ecology 10:1509-1520 <ResearchGate>

Werner, R. M. and J. A. Vick. 1977. Resistance of the opossum (Didelphis virginiana) to envenomation by snakes of the family Crotalidae. Toxicon 15:29-32 <PDF>

Wilcox, C. 2016. Venomous: How Earth's Deadliest Creatures Mastered Biochemistry. Scientific American. <official page>

Witsil, A. J., R. J. Wells, C. Woods, and S. Rao. 2015. 272 cases of rattlesnake envenomation in dogs: Demographics and treatment including safety of F(ab')2 antivenom use in 236 patients. Toxicon 105:19-26 <abstract>

Creative Commons License

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

Wednesday, March 7, 2018

The House Snake Mess for Dummies

This article will soon be available in Spanish

Inspired by Mike Van Valen's "The Ratsnake Mess for Dummies"
Please note that the information in this article is current as of March 2018 (no later)
Please contact me or leave a comment if you spot an error

Arguably House Snakes are much more of a mess than ratsnakes, which makes sense when you consider that they are they distributed over an area almost 7 times larger, including areas as diverse as the Sahara Desert, Congo Rainforest, Great Rift Valley, East African Savannah, Ethiopian Highlands, Okavango Delta, and Southern African Great Escarpment, and occur in a total of 46 countries, many of which have perennially turbulent political climates. It's no surprise that the number of herpetologists working in Africa is dwarfed by the number working in North America, and the vast majority of these people have not been of African descent (although that is beginning to slowly change).

African House Snake (Boaedon fuliginosus) from the
northernmost part of the range in Morocco.
Like everywhere in Africa, there are probably multiple
undescribed cryptic species within this lineage
What is surprising is that African House Snakes are popular in the pet trade and are important model organisms for studies of development, behavior, hormones and reproductive biology, yet we still know almost nothing about them in the wild, even though they are common and tolerant of anthropogenically-disturbed environments.

When most people think of African House Snakes, the scientific name that probably comes to mind is Lamprophis fuliginosus. In this article, I'll try to explain why this well-known species had to be moved into the genus Boaedon in 2011, and why it will probably be split up into multiple species sometime in the (hopefully-not-too-distant) future. The correct scientific name of many African House Snakes in captive breeding colonies may be difficult or impossible to determine, especially because most people don't know which part of Africa their House Snakes originally came from (and they may have since been bred with House Snakes from other parts of Africa).

Simplified phylogenetic tree of Lamprophiinae, with
focus on "house snakes" (genera Boaedon & Lamprophis).
There's enough uncertainty about the structure within Boaedon
that I didn't try to represent much of what's known.
For more detailed trees, see the KellyGreenbaum, & Trape papers.
Green are species lacking genetic data that can't be placed yet.
Red stars are multiple cryptic species (there could be more).

Click here for a larger version
To start, let's get a little taxonomic perspective. Pyron et al.'s 2011 article firmly established the family Lamprophiidae for a large group of mostly African snakes (321 species) formerly classified as colubrids but actually more closely-related to elapids (more detail here and here). They also found support for seven subfamilies of lamprophiids, of which only one, Lamprophiinae, concerns us today. There are currently 78 species placed in Lamprophiinae1, of which 25 are or have been at some point commonly called "House Snakes" and/or placed in the genus Lamprophis. Only one of these is Boaedon (formerly Lamprophis) fuliginosus, but in order to understand it, we'll need to take a closer look at the others.

A great deal of clarity was gained from the taxonomic actions of Chris Kelly & co-authors in 2011, who split the species in the genus Lamprophis up into several genera, depending on their relationships to other genera of lamprophiines. Even this study was only able to include data on ~40% of the species of lamprophiine snakes, so it's probable that surprises and new discoveries still await us.

Swazi Rock Snakes, Inyoka swazicus, are endemic to rocky
outcrops in Swaziland and adjacent provinces of South Africa
There are currently 12 genera of lamprophiines. Two of these, Chamaelycus (4 species) and Dendrolycus (1 species), have not been included in any molecular phylogenetic trees, so we're going to ignore them for now. The general relationships of the other 10 genera have been sketched out, and they're divided into two groups of roughly equal diversity. The first includes the African Wolf Snakes (Lycophidion; 20 species) and the African File Snakes (Gonionotophis, including the former genus Mehelya; 15 species), as well as two monotypic genera: Hormonotus modestus (Uganda House Snake or Yellow Forest Snake) and Inyoka swazicus (Swaziland House Snake or Swazi Rock Snake). Both of these were originally described as species of LamprophisHormonotus left the genus in the 19th century, and Inyoka was created for swazicus by Kelly et al. 2011 (it means ‘snake’ in the Nguni language group, the main language group in Swaziland). When it was originally described in 1970, swazicus was thought to be intermediate between Lamprophis and Boaedon, both of which were in use at the time, but it turns out that the resemblance is superficial and it's closely related to neither. That takes care of the first two of our 25 House Snake species, which aren't really House Snakes at all.

The Olive Water Snake, Lycodonomorphus inornatus,
was formerly thought to be a Lamprophis
The second group of lamprophiines contains six genera. Three of these are rather small and pretty straightforward, if obscure: Ethiopian Mountain Snakes (Pseudoboodon; 4 species), Günther's Black Snake (Bothrolycus ater), and Red-Black Striped Snakes (Bothrophthalmus; 2 species). None of these have ever been called House Snakes or placed in Lamprophis2, and they are clearly morphologically distinct. A fourth genus, African Water Snakes (Lycodonomorphus; 9 species), includes two species that were formerly thought of as House Snakes: Ly. inornatus and Ly. rufulus (the second only briefly). Ly. inornatus is interesting because it's terrestrial, unlike the other species of Lycodonomorphus, which is part of why it was classified in Lamprophis for so long.

Fisk's House Snake, Lamprophis fiskii, is found in
rocky & sandy areas in the western part of South Africa
The really important finding of Kelly et al. 2011 was that Lycodonomorphus split up the remaining members of Lamprophis into two groups. The southern African group containing Lamprophis aurora got to keep the name Lamprophis, because L. aurora was the first species to be placed in Lamprophis (it is the "type species" of the genus). It got to bring along its close relatives L. fiskii, L. fuscus, and L. guttatus, all of which are small house snakes with attractive patterns, sometimes referred to as "dwarf house snakes", that are popular in the pet trade despite being relatively poorly known in the wild.

Olive House Snakes, Boaedon olivaceus
are found in forests rather than savannah
& grassland habitats
The other group needed a new name. Fortunately, Boaedon had already been used to refer to this group for a long time, from the 1850s to the 1980s. Four species in Kelly's study got "new" names: B. olivaceus, B. virgatusB. lineatus, and B. fuliginosus. Additionally, Kelly included B. maculatus in this group, because its morphology is similar to the other four species, but since we have no DNA evidence yet, this could change. These are sometimes informally called the "brown house snakes", in reference to their generally drabber patterns compared with the "dwarf house snakes". Morphological differences between these two genera include that Boaedon have enlarged anterior teeth on both the upper & lower jaw, and that the dorsal scales of Boaedon have apical pits, whereas those of Lamprophis do not.

Three other species get to stick around in Lamprophis for now: "L." abyssinicus and "L." erlangeri from the Ethiopian highlands, and "L." geometricus from the Seychelles. Probably once we get genetic data from these they will be moved into another genus, possibly Boaedon.

Most of the tree from Greenbaum et al. 2015, showing
the paraphyly of B. fuliginosus with respect to other
Boaedon species, and the geographic diversity of the samples.
Now, the problems aren't over. The thing is that, in Kelly's study, Boaedon "fuliginosus" was split up by B. olivaceus, which is clearly a good species and it makes no sense to sink it into fuliginosus, as well as by B. lineatus, which has a more complex relationship with B. "fuliginosus"3. There are at least seven lineages of Boaedon "fuliginosus" (probably more than 10), thus we can expect that at least 7-10 cryptic species are waiting to be described within this species complex. To quote Kelly et al.: "There have been several attempts to make sense of the intricate patterns of morphological variation in this complex, generally with only limited success."4. A handful of subspecies have been named based on morphology (e.g. mentalis in Namibia, angolensis from southeastern Angola to the southern DRC, arabicus in Yemen, bedriagae on the islands of São Tomé and Príncipe), some of which will probably eventually turn out to be used for full species.

Which, if any, of these future species will get to keep the name fuliginosus is not clear, because these decisions are made based on the location of the original specimen, called the "type locality". The type locality for L. fuliginosus was originally and incorrectly reported in 1827 as "Java". People were more careless back then. There is also no clear type specimen; at one point, one was designated, but it was lost by 1965. The type locality was subsequently corrected to the more accurate but still completely unhelpful "Africa" in 1962, and further restricted to either South Africa or Ghana, but which one isn't clear.

Map of the species currently in Boaedon Lamprophis
Question marks indicate areas where the species range
is uncertain (pink=lineatus complex, green=olivaceus,
brown="fuliginosus"/"capensis" complex)
Click here for larger version
Finally, there is the issue of Boaedon "capensis", a putative species described in 1997 by Hughes and occurring east of a hazy and ill-defined zone angling northeast-southwest from the Gulf of Aden along the Great Rift Valley, then turning east and extending to the Atlantic Ocean possibly near the Angola-Namibia border, but potentially as far north as the mouth of the Congo River and thus also including three of the largest and most poorly-surveyed countries in Africa: Angola, the Democratic Republic of the Congo, and Sudan (including the still relatively new country of South Sudan). This name effectively replaces fuliginosus in eastern and southern Africa, but the exact boundaries are not remotely known, and it will probably turn out that both species are non-mutually-exclusive complexes of cryptic species. Because of the type locality confusion of fuliginosus, it could even turn out that both names (fuliginosus and capensis) are the same southern African species5, and that the western and central African species will need new names.

Boaedon radfordi, a new species from the Uganda-DRC
border region. From Greenbaum et al. 2015
Recent discoveries have begun the process of adding to the number of species of Boaedon: in 2015, Eli Greenbaum and colleagues named a new species, B. radfordi, from the Albertine Rift in the eastern DRC and Uganda (which was formerly confused with B. olivaceus), and also unexpectedly found that a subspecies of Lycodonomorphus subtaeniatus was actually an undescribed species of Boaedon from a lake in south-central DRC, named B. upembae, that is most closely related to B. virgatus. They wisely refrained from making premature splits to the fuliginosus/capensis complex, stating that "Given the complicated taxonomic history and nebulous type locality for B. fuliginosus, substantial additional sampling and morphometric analyses are needed to assign...B. fuliginosus lineages to available names and to describe new species." They did, however, show that divergence among the various lineages currently referred to as B. fuliginosus could have happened as long as 21 million years ago.

Boaedon longilineatus, a new species from Chad
From Trape & Mediannikov 2016
In 2016, Trape & Mediannikov examined 1,370 specimens from eight countries and described 5 new species of Boaedon from central Africa, bringing the total number of species to 13 (including capensis and the certainly paraphyletic "fuliginosus"). Together, two of these, B. perisilvestris and B. subflavus, seem to effectively separate fuliginosus (western Cameroon and west) and capensis (Angola-DRC-S.Sudan and east), having been split from the middle of the species complex's geographic range; but many sources still use fuliginosus for populations east of the distribution of perisilvestris and subflavus. Trape & Mediannikov seem comfortable with the idea of restricting B. fuliginosus to West Africa, and suggest that a blackish color without clear lines on the head could distinguish the species there, despite the absence of any consistent scale characteristics6. Right now, it's impossible to say how the 5 species described by Trape & Mediannikov fit with those described by Greenbaum or with the clades outlines in Kelly, because they used the 16S RNA gene, whereas the other two studies used three different genes (cyt-b, ND4, and c-mos).

Boaedon capensis from South Africa
So, we seem to be approaching stability, but the most problematic one remaining is the one everybody's heard of, knows and loves. Trape's latest definition notwithstanding, between fuliginosus and capensis, African House Snakes in the strictest sense occur in every country in Africa except for Algeria, Tunisia, Libya, Egypt, Sudan, and offshore countries like Madagascar, the Comoros, and the Seychelles7. At the moment, the L. "fuliginosus" complex is still one of the most widespread snake species in the world.

In case you lost count, a quick recap of species that are or have been in Lamprophis:
  1. Hormonotus modestus (Yellow Forest Snake or "Uganda House Snake"; moved in 1850s)
  2. Inyoka swazicus (Swazi Rock Snake or "Swaziland House Snake"; moved in 2011)
  3. Pseudoboodon lemniscatus (briefly in Lamprophis in 1904, barely counts, see footnote2)
  4. Lycodonomorphus inornatus (originally described as a Lamprophis because it was terrestrial, but always a little weird; moved in 2011)
  5. Lycodonomorphus rufulus (briefly in Lamprophis 1840s-1860s, barely counts)
  6. Lamprophis aurora (type species for the genus, will always be a Lamprophis by definition)
  7. Lamprophis fiskii (gets to stick with aurora)
  8. Lamprophis fuscus (gets to stick with aurora)
  9. Lamprophis guttatus (gets to stick with aurora)
  10. "Lamprophis" abyssinicus (awaiting DNA data; Ethioipian highlands)
  11. "Lamprophis" erlangeri (awaiting DNA data; Ethioipian highlands)
  12. "Lamprophis" geometricus (awaiting DNA data; Seychelles)
  13. Boaedon lineatus (type species for the genus, will always be a Boaedon by definition, although as defined it too is likely a cryptic species complex)
  14. Boaedon virgatus (gets to stick with lineatus)
  15. Boaedon olivaceus (gets to stick with lineatus)
  16. Boaedon maculatus (awaiting DNA data; got to stick with the above 3 because of morphology; Horn of Africa)
  17. Boaedon radfordi (described by Greenbaum et al. 2015, split from olivaceus)
  18. Boaedon upembae (formerly Lycodonomorphus subtaeniatus upembae; moved by Greenbaum et al. 2015; in the B. virgatus group)
  19. Boaedon littoralis (split from B. lineatus by Trape & Mediannikov 2016, but lacks DNA data)
  20. Boaedon longilineatus (split from B. lineatus by Trape & Mediannikov 2016)
  21. Boaedon paralineatus (split from B. lineatus by Trape & Mediannikov 2016)
  22. Boaedon perisilvestris (the first of many cryptic species to be split from B. fuliginosus; by Trape & Mediannikov 2016)
  23. Boaedon subflavus (the 2nd split from B. fuliginosus by Trape & Mediannikov 2016)
  24. Boaedon capensis (replaces fuliginosus in east Africa, could be multiple cryptic species)
  25. Boaedon fuliginosus (definitely at least 7 cryptic species, probably many more, no guarantee that any will be called fuliginosus)
The Aurora House Snake, Lamprophis aurora, is the
type species of the genus Lamprophis, meaning it will always
be in Lamprophis unless that genus goes away completely
Whether fuliginosus goes away completely or remains, it won't be going back to Lamprophis unless Lycodonomorphus does too, or unless new genomic data overwhelm the signals found in the genes used by Kelly's, Greenbaum's, & Trape's studies. There's a recurring debate in taxonomy about whether we should attempt to preserve widely-used and well-known names like fuliginosus, since people are probably going to continue using them anyway, or do away with "the burden of heritage" and adhere strictly to a system that discards 150-year-old names if they prove inconvenient or impossible to keep, at the risk of creating confusion & resentment. Proponents of the second argue that eventually people won't remember the old names, and I think they're right: I was born in the 1980s and didn't realize that Lamprophis fuliginosus was called Boaedon for 130 years beforehand; when I learned its name in ~1999, it was as Lamprophis fuliginosus and that was that. These changes might seem radical, but whenever possible they reinstate older names, like Boaedon, the disuse of which might seem radical to an older generation.

There's further debate about the utility of splitting up cryptic species complexes, especially if it makes it almost impossible to identify which species you're looking at by morphology alone. These same issues are recapitulated in the North American ratsnake taxonomic "mess", North American slimy salamanders, egg-eating snakes, and in countless other species groups around the world. When I was writing this article, I thought more than once that I should just wait for a better time when it's all stabilized, but actually there's never a good time; we're always learning more. Ultimately, fleshing out and revising phylogenies and taxonomies will teach us a lot about biodiversity, evolution, and human nature. My advice is to try to be open-minded rather than bitter and ugly when discussing them. There is no "right" or "wrong", there are just rules we've (mostly) agreed to follow. It's an exciting time.

If this group of snakes interests you, watch the labs of Christopher Kelly, Jakob Hallermann, Aaron Bauer, and Jean-François Trape for future research that should make much of this article obsolete.



1 Note the difference between the endings of the family ("-idae") and subfamily ("-inae") names.



2 Except for Pseudoboodon lemniscatus, but that was only once, in 1904. It counts, but only in the same way as stuff you did once in college. This is complicated enough already.



3 Sources differ on whether B. lineatus is distinct from B. fuliginosis, but it seems to be in western Africa (though both could be multiple cryptic species). Some resources use B. lineatus for house snakes with head stripes in e.g. Uganda, Ethiopia, and Sudan, but increasingly these are referred to as B. capensis. Characteristics used to distinguish B. virgatus & B. olivaceus from B. fuliginosus/capensis/lineatus include undivided subcaudal scales in B. olivaceus and only 23 dorsal scale rows in B. virgatus, as well as the fact that B. virgatus B. olivaceus are found in forests whereas the others are savannah species.



4 The presence or absence of head stripes has been used as a highly visible character, but ultimately this probably won't prove to be closely correlated with genetic variation (and it's complicated by the fact that some Boaedon populations have head stripes as juveniles but lose them as adults). This is also the case in North American ratsnakes, where former subspecies with radically different adult color patterns, like E. o. rossalleni and E. o. quadrivittata turned out to be so genetically similar to the more widespread black phenotype that they are now not recognized. This is part of a move away from the subspecies concept in general, wherein many authors either synonymize subspecies with existing species as "mere variants" or elevate them to full species status using genetic data. I think we can expect this trend to continue with House Snakes.



5 This could happen if South Africa is chosen as the type locality of fuliginosus, because the type locality of capensis is also in South Africa—if South Africa ultimately contains just one species from the fuliginosus complex, then it will get to keep the older name (fuliginosus), and other former members elsewhere should not use the name capensis in order to avoid further confusion. If the type locality of fuliginosus is chosen to be in Ghana instead, then the name will probably continue to be used in western Africa. Let us hope for the 2nd option.



6 This isn't an identification guide, but if you want to see the scale characters for the different species, you can refer to the tables and descriptions in the Kelly, Greenbaum, and Trape papers.



7 "B. fuliginosus" are also found on the Arabian peninsula in Yemen; this could be the most obvious future split if these are shown to be their own lineage, and several sources have already used the name arabicus for them, although just a few individuals are known and additional biological specimens from Yemen are hard to come by. A recent paper used bedriagae as the name of a full species on the islands of São Tomé, with a new species being described from the neighboring island of Príncipe.


ACKNOWLEDGMENTS

Thanks to Peter Uetz for his advice on literature, and to Konrad Mebert, Cliff & Suretha Dorse, and Dan Rosenberg for the use of their photos.

REFERENCES

For map references, see map inset

Bates, M. F., W. Branch, A. Bauer, M. Burger, J. Marais, G. Alexander, and M. De Villiers. 2014. Atlas and red list of the reptiles of South Africa, Lesotho and Swaziland. South African National Biodiversity Institute <full-text>

Bogert, C. M. 1940. Herpetological results of the Vernay Angola Expedition. Part 1. Snakes, including an arrangement of African Colubridae. Bulletin of the American Museum of Natural History 77:1-107 <link>

Branch, W. R. 1984. The House Snakes of southern Africa (genus Lamprophis). Litteratura Serpentium 204:106-120 <link>

Brassine, M. C., C. M. R. Kelly, N. P. Barker, and M. H. Villet. 2008. The phylogenetics of the Lamprophis fuliginosus/capensis species complex in southern Africa. Page 13  Proceedings of the 9th Conference of the Herpetological Association of Africa, Sterkfontein Dam, South Africa.

Broadley, D. G. 1969. The African house snakes—How many genera? The Journal of the Herpetological Association of Africa 5:6-8 <preview>

Ceríaco, L. M., M. P. Marques, and A. M. Bauer. 2018. Miscellanea Herpetologica Sanctithomae, with a provisional checklist of the terrestrial herpetofauna of São Tomé, Príncipe and Annobon islands. Zootaxa 4387:91-108.

Conradie, W., R. Bills, and W. Branch. 2016. The herpetofauna of the Cubango, Cuito, and lower Cuando river catchments of south-eastern Angola. Amphibian and Reptile Conservation 10:6-36 <full-text>

de Witte, G. F. 1963. The colubrid snake genera Chamaelycus Boulenger and Oophilositum Parker. Copeia 1963:634-636 <full-text>

Greenbaum, E., F. Portillo, K. Jackson, and C. Kusamba. 2015. A phylogeny of Central African Boaedon (Serpentes: Lamprophiidae), with the description of a new cryptic species from the Albertine Rift. African Journal of Herpetology 64:18-38 <abstract>

Hallermann, J. and A. Schmitz. 2007. First results on the taxonomy of the Lamprophis fuliginosus complex in Africa. 14th European Congress of Herpetology and SEH Ordinary General Meeting <abstract book>

Hughes, B. 1997. Dasypeltis scabra and Lamprophis fuliginosus - two pan-African snakes in the Horn of Africa: a tribute to Don Broadley. African Journal of Herpetology 46:68-77 <abstract>

Kelly, C. M. R., W. R. Branch, D. G. Broadley, N. P. Barker, and M. H. Villet. 2011. Molecular systematics of the African snake family Lamprophiidae Fitzinger, 1843 (Serpentes: Elapoidea), with particular focus on the genera Lamprophis Fitzinger 1843 and Mehelya Csiki 1903. Molecular Phylogenetics and Evolution 58:415-426 <academia.edu>

Pyron, R. A., F. T. Burbrink, G. R. Colli, A. N. M. de Oca, L. J. Vitt, C. A. Kuczynski, and J. J. Wiens. 2011. 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 <full-text>

Roux-Estève, R. and J. Guibé. 1965. Contribution a l’étude du genre Boaedon (Serpentes, Colubridae). Bulletin du Muséum National d’Histoire Naturelle, Paris 36:761-774.

Roux-Estève, R. and J. Guibé. 1965. Étude comparée de Boaedon fuliginosus (Boié) et B. lineatus D. et B. (Ophidiens). Bulletin de l’Institut Fondamental d’Afrique Noire, Dakar 27A:397-409.

Schaefer, N. 1970. A new species of house snake from Swaziland, with notes on the status of the two genera Lamprophis and Boaedon. Annals of the Cape provincial Museums 8:205-208 <full-text from BHL>

Schätti, B. 1989. Amphibians and reptiles from the Yemen Arab Republic and Djibouti. Revue Suisse de Zoologie 96:905-937 <full-text from BHL>

Thorpe, R. and C. McCarthy. 1978. A preliminary study, using multivariate analysis, of a species complex of African house snakes (Boaedon fuliginosus). Journal of Zoology 184:489-506 <abstract>

Trape, J.-F. o. and O. Mediannikov. 2016. Cinq serpents nouveaux du genre Boaedon Duméril, Bibron & Duméril, 1854 (Serpentes : Lamprophiidae) en Afrique centrale. Bulletin de la Societe Herpetologique de France 159:61-111 <abstract>

Vidal, N., W. R. Branch, O. S. G. Pauwels, S. B. Hedges, D. Broadley, M. Wink, C. Cruaud, U. Joger, and Z. Nagy. 2008. Dissecting the major African snake radiation: a molecular phylogeny of the Lamprophiidae Fitzinger (Serpentes, Caenophidia). Zootaxa 1945:51-66 <full-text>

Visser, J. 1979. Notes on two rare house snakes – Part 1. Lamprophis fiskii Boulenger (1887) and L. swazicus Schaefer (1970). Journal of the Herpetological Association of Africa 19:10-13.

Visser, J. 1979. Notes on two rare house snakes – Part 2: The generic status of Lamprophis fiskii Boulenger (1887) and Lamprophis swazicus Schaefer (1970). Journal of the Herpetological Association of Africa 21:31-37.

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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, February 12, 2018

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 1970Click 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).



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.



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.



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.



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>

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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.