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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.

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.






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>

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.

Monday, December 25, 2017

Life is Short but Snakes are Long 2017 Year in Review

Dear reader,

Life is Short but Snakes are Long turned 5 years old in April, and reached 1 million views on June 26th, 2017. I celebrated with a month-long recapitulation of the "best-of" on Twitter in the spring, and by taking a much-needed break from writing new content during the second half of the year.  I didn't make a formal announcement of this break because I honestly wasn't sure how long it would last (although I knew it wasn't permanent). During the past six months I've focused on settling in to my new job in Germany, traveling around Europe, publishing a key article from my dissertation, and applying to postdocs and "real" jobs. I'm currently waiting to hear whether I'll be starting something new in 2018—if I am, I plan to continue to write Life is Short but Snakes are Long as I have been. If I'm not, I plan to begin revising certain past articles, and writing new ones, for a book. In either case, I'm looking forward to a lot of new content in 2018.

As always, thank you for reading.

Andrew Durso

Vipera berus from Germany

Thursday, August 31, 2017

How many snakes are venomous and how many are constrictors?

This post will soon be available in Spanish

as of April 2017. I made the assumption that prey-killing behavior
didn't vary within genera, so if I found data for one species in a genus
I applied it to all others in the absence of specific data for those species.
Many people are aware that some snakes constrict their prey, and others use venom to kill their prey. Recently, somebody asked me what the breakdown was, and I had to admit that I didn't know exactly. My initial estimate was that 20% were venomous in a way that is medically-significant to humans, and that probably a similar number of species are opisthoglyphs that use venom that is not life-threatening to humans to subdue their prey (with a decent number of these pending discovery, confirmation, or further investigation). Estimating the percentage of constrictors was more difficult, but I suspected that it was no more than the percentage of snake species that use venom, and probably somewhat less. A lot of people don't realize that there is a huge third category of snakes that just seize their prey and swallow it alive, sometimes subduing it first by crushing it with strong jaws or pinning it to the ground with a coil (which hardly counts as constriction but could be an evolutionary precursor).

This inspired me to do some literature searching, and as I suspected nobody has ever attempted to estimate the exact percentages of snake species that use each kind of prey-killing behavior. As such, I have prepared a preliminary analysis, the full contents of which I intend to make publicly available after peer review. I hope that doing so will stimulate others to publish their observations of feeding behavior in poorly-known snakes (of which there are many), and add to the long history of discussion about the evolution of snake feeding modes, most of which took place before we had a solid grasp on the evolutionary relationships of extant snake families.

I found that the answer to this question is not as simple as it may seem. Many snakes unambiguously use venom or constriction, but many use neither, and some use both! Of course the data are not as detailed or abundant as we would like. What follows is a break-down of the categories I used, and some interesting exceptions that I uncovered.

Constrictors

Unambiguous constrictors make up just 11% of snake species, but include several well-known groups that are common in the popular consciousness, in zoos, and in the pet trade, including:
  • Boas: 61 species, including the eponymous Neotropical Boa constrictor, anacondas (Eunectes), and smaller tree and rainbow boas (Corallus, EpicratesChilabothrus) as well as several (sub)families of booid snakes from various and sundry locations around the world—Candoia from New Guinea and Melanesia, sand boas (Eryx) from northeast Africa, the Middle East, and southwestern Asia, Charina and Lichanura from North America, Ungaliophis and Exiliboa from Central America, Acrantophis and Sanzinia from Madagascar, and Calabaria from tropical west-central Africa.
  • Pythons: 40 species from Africa, Asia, and Australia
  • Ratsnakes, kingsnakes, and close relatives: 43 species of New World colubrine colubrids in the clade Lampropeltini and their Old World counterparts, including:
as well as some more obscure groups:
Anilius scytale constricting an amphisbaenian
From Marques & Sazima 1998
  • Tropidophiids or "dwarf boas", which are not closely related to boids and certainly evolved constriction independently (34 species)
  • Their close relative Anilius scytale (sort of; this snake has been observed to constrict large prey such as amphisbaenians)
  • Loxocemus bicolor, the Mexican burrowing snake, a close relative of pythons
  • Two speceis of Asian sunbeam snakes (genus Xenopeltis), which are also closely related to pythons
  • At least some (maybe all) Asian pipesnakes (family Cylindrophiidae)
  • Filesnakes (genus Acrochordus), which don't necessarily kill fish by constricting them but use their coils to hold them while they swallow
  • some lamprophiine colubrids (especially the well-known African house snakes Lamprophis and Boaedon)
  • the colubrine colubrid tribe Lycodontini (mostly wolf snakes, genus Lycodon)
  • some snail-eating snakes (Dipsas) coil around snails as they pry them out of their shells
  • even Wandering Gartersnakes (Thamnophis elegans)—sometimes! (more below)
These groups of snakes vary considerably in how often they employ constriction to kill their prey. Some probably use it almost all the time (although even ratsnakes eat prey that they don't constrict, such as bird eggs), whereas others use constriction only rarely, when encountering an unusually large or dangerous prey item relative to their size and strength (for example, one study showed that species of Python, Boa, Pantherophis, and Lampropeltis always constricted mice if they were at least 90% the diameter of the snake's head). Some, such as Regina alleni and Acrochordus filesnakes, may use constriction more so to immobilize the prey than to kill it/it probably doesn’t work that well under water (although Wandering Gartersnakes usually killed mice before eating them).

It seems that mammal-eating is a driver of the evolution of constriction in many cases: species that eat mammals are the only members of their genera/families that use constriction (Thamnophis elegans, Boiga irregularis, Lamprophis/Boaedon, some members of the Oxyrhopus/Clelia/Pseudoboa clade) and both these and species that are nested within mammal-eating clades but have shifted to other prey (Lampropeltis extenuatum, Elaphe quadrivirgata, Cemophora coccinea1) tend to have more variable, less efficient constricting behavior that is generally only used to immobilize rather than to kill prey, if it is used at all. As Alan de Queiroz and Rebecca Groen put it: “Thamnophis elegans are not finely tuned constricting machines” and “Numerous trials in which a garter snake, holding a mouse in its jaws, was chaotically thrown about by the prey's movements support our interpretation that long constriction latencies do not reflect adaptive plasticity in T. elegans.”. Constriction probably functions to reduce the cost of feeding in terms of time, energy, and/or the probability that the prey will harm the snake.

Conspicuously not in this category, we have the poorly-named and misleading North American Racer, Coluber constrictor, which is not a constrictor (thanks for nothing, Linnaeus).

Venom

Black Mamba (Dendroaspis polylepis) eating a bird
It's pretty clear which snakes use strong venom to subdue their prey; most of these are dangerously venomous to humans and so we're well aware of them. There are five major groups:
  • Viperids (341 species), including well-known pit vipers such as rattlesnakes, copperheads, and cottonmouths
  • Elapids (359 species), including coralsnakes, cobras, mambas, kraits, sea snakes, and diverse terrestrial Australian snakes ranging from death adders (genus Acanthophis) to bandy-bandys (genus Vermicella)
  • Genus Atractaspis (21 species), the stiletto snakes now known to be lamprophiids, which stab backwards with their fangs, mouth closed, to envenomate prey in subterranean burrows
  • Non-front-fanged colubrine colubrids, most notably boomslangs (Dispholidus typus), twigsnakes (genus Thelotornis), and probably their close relatives in the genus Thrasops, all of which have many functional characteristics of front-fanged snakes while their elongated teeth remain at the rear of the (albeit rather short) maxilla
  • some Asian natricine colubrids in the genera Rhabdophis, Macropisthodon, and Balanophis, which in addition to being (in a few cases lethally) venomous, also have the distinction of being among the only known poisonous snakes
Also, many snakes use venom to subdue their prey but are not dangerous to humans, either because they have fangs in the back of their mouth, have venom that is not adapted for causing physiological damage to mammals, or both. These include:
  • numerous dipsadine colubrids from the Caribbean and Central and South America, such as Xenodon, Thamnodynastes, Hydrodynastes, Coniophanes, Erythrolamprus, Rhadinaea, Leptoderia, and Apostolepis (and a few from North America, such as Heterodon and Hypsiglena)
  • some colubrine colubrids (genera such as Boiga, Leptophis, Tantilla, Toxicodryas, Platyceps, Oxybelis, Hierophis, Crotaphopeltis, Drymobius, Chilomeniscus, Ficimia, and Gyalopion) as well as the Asian genera Ahaetulla and Chrysopelea, sometimes split into a different subfamily (Ahaetullinae)
  • at least some natricine colubrids, such as Paratapinophis praemaxillaris and some North American gartersnakes (Thamnophis)
  • many species in the family Homalopsidae, 53 species of southeast Asian semi-aquatic snakes, some of which are also well-known for pulling apart large crabs and eating pieces of them
  • some (maybe most) lamprophiids, including aparallactines (Amblyodipsas, Aparallactus, Micrelaps, Polemon, Xenocalamus), lamprophiines (Gonionotophis), psamophiines (Mimophis, Psammophis), and the weird genus Psammodynastes ("mock viper")
and probably many more. It's actually possible that this is the largest group, because some of the "unknown" and "neither" species probably actually belong here. An interesting exception are Turtle-headed Seasnakes (Emydocephalus annulatus) and Beaded Seasnakes (Aipysurus eydouxii), which eat fish eggs and have mostly lost their venom, fangs, and venom glands. Another example of a reduction in fangs are some fossorial species of Tantilla, which have only slightly enlarged and faintly grooved rear maxillary teeth, in contrast to the more well-developed rear fangs of most other members of this large genus. These snakes appear to specialize on beetle larvae rather than on centipedes, although no one has looked to see if their venom is any different as a result.

Neither

Dipsas indica coiling around a snail, from Sazima 1989
Most snakes (38% of species) seize their prey and swallow them alive. Generally these snakes are eating prey that are much smaller than they are, which lack serious physical defenses (although many of them may have chemical defenses that the snakes circumvent in other ways, such as through toxin resistance). These include:
Some of the aforementioned goo-eaters do use their coils to support the shells of snails while they pry out the soft innards. Dipsas coils around the snail’s shell and Sibynomorphus use as s-shaped loop of their body to support the shell, whereas some Sibon crawl backward through crevices to wedge snails into them, providing an anchor against which they use their body muscles to pull out the soft parts.

Both

Finally, there are some really interesting examples of snakes that use both venom and constriction to subdue their prey, although not always at the same time. Perhaps most impressive but least well-documented in the scientific literature are two viper species that sometimes use constriction in conjunction with venom: Ovophis monticola and O. okinavensis2.

Pseudonaja textilis constricting a mouse
From Mirtschin et al. 2006
A review by Rick Shine & Terry Schwaner brought together data on numerous Australian elapids that, although they clearly have and use venom, also use their coils to subdue and hold prey while envenoming it. In many of these species, including tiger snakes (Notechis), brown snakes (Pseudonaja), curl/myall snakes (Suta), whip snakes (Demansia), Australian coral snakes (Simoselaps), crowned snakes (Cacophis), and olive seasnakes (Aipysurus laevis), the coils are not used alone as the primary method of prey subjugation, and one recent paper suggested that we think of them as "part of a 'combined arsenal' of prey subjugation strategies".

To explain the "apparent paradox of why a species should use both venom and constriction to subdue its prey", Shine & Schwaner offered three possible non-mutually-exclusive explanations:
  1. The venom may be of low toxicity and thus slow to act, so holding onto the prey with either jaws or coils might allow more venom to be injected
  2. Species with short fangs, such as Pseudonaja, and/or that feed on on heavily armored prey , such as skinks, may use constriction to give themselves additional time to find a "chink in the armor" and envenomate their prey
  3. Using constriction in addition to venom may prevent snakes from losing track of bitten and envenomated prey that escape, or from being harmed by retaliating prey that are held onto
The Australian elapids recorded to use constriction feed mainly on lizards and frogs, although mammals are common prey items of Pseudonaja and Notechis. Puff Adders (Bitis arietans) choose to release large rodents and rabbits, but hold onto smaller prey, although they have not been reported to use constriction (and given their specialized body shape, they probably do not, nor do they need to since they are equipped with long fangs, strong venom, and strike-induced chemosensory searching). However, immobilizing prey with coils probably plays a larger role in prey subjugation for many rear-fanged species with slower-acting venom, such as:
  • colubrine colubrids Boiga irregularisMacroprotodon, Platyceps gracilis, Stegonotus, Telescopus, Trimorphodon
  • dipsadine colubrids from the Caribbean (Alsophis, Cubophis), Central & South America (Clelia, Helicops, ImantodesOxyrhopusPhilodryasTropidodryasSiphlophisPhimophis, and Pseudoboa), and North America (DiadophisFarancia)
  • the sibynophiine colubrid Sibynophis collaris
  • some homalopsids, like Fordonia, Hypsiscopus, and Myron
  • a few lamprophiine lamprophiids, such as Lycophidion
  • pseudaspine lamprophiids Pseudaspis and Pythonodipsas
  • some pseudoxyrhophiine lamprophiids Leioheterodon and Madagascarophis
  • some psammophiine lamprophiids (e.g., the Montpellier Snake and its relatives in the genus Malpolon, Hemirhagerrhis, Psammophis, and Rhamphiophis)
  • even Wandering Gartersnakes (Thamnophis elegans)—sometimes!
Elaphe quadrivirgata not constricting a frog (Rana ornativentris)
Mori (1991) showed that these snakes constrict large mice,
pin small mice with a single coil, and swallow frogs alive
In many cases, only large endothermic prey (usually mammals) are constricted, whereas snakes will swallow small, easily subdued prey alive. Even some specialized constrictors will consume small prey whole, suggesting that almost all snakes can change strategies depending on what type of prey they are subduing. The bottom line is that, if you're a snake that's eating mammals, you need to have either constriction or venom, and maybe both, because:
  1. Mammals are big, or at least a lot of snakes like to eat mammals that are relatively large compared to their body size
  2. They are endotherms with the metabolic capacity for sustained struggling
  3. They can fight back with sharp teeth and strong jaws capable of seriously injuring or killing a snake, in a way that a frog or a lizard cannot
This generalization is supported by observations showing that mammals tend to be killed by constriction prior to being swallowed more often than prey such as frogs, and that larger prey tend to be killed by constriction first, then swallowed. Evidently the amount of struggling is one cue used by Thamnophis elegans to decide whether or not to constrict prey. Experiments carried out by Akira Mori and others have shown that "the degree of such behavioral flexibility is, to some extent, species-specific, and it has been suggested that dietary specialists change their behavior more efficiently than dietary generalists, especially when they are young".

Unknown

After my initial pass at collecting these data (during which I made several sweeping assumptions, some of which later turned out to be oversimplifications), I was left with 36% of species unknown. Following a more thorough literature search, I managed to get this down to 10%, which is still 363 species of snakes. In many cases I made assumptions based on generalizations about the biology of groups of snakes—for instance, I assumed that all scolecophidians use neither constriction nor venom, that all vipers use venom, and so forth. But many dipsadine and colubrine colubrids, and many lamprophiids have not been directly studied, and I could find no reports in the literature about their feeding habits. In some cases we don't even know what they eat, and ecological diversity in these groups is very high, such that there are few consistent patterns that I could use to infer prey subjugation mode for these 370 species. Teach yourself about obscure snakes and help fill in the blanks!

A few examples:
Evolution of prey subjugation strategies in snakes

Phylogenetic tree from Greene 1994
For an overview of some of the updates, click here
The most recent similar review was done by Harry Greene in 1994, in which he revised earlier hypotheses he put forth with Gordon Burghardt in the journal Science 16 years before. We now know a lot more about the snake family tree than we did in 1994, particularly the fine details of relationships within the Caenophidia. Overall, the basic pattern has held up rather well—constriction evolved first in basal alethinophidians during the late Cretaceous, accompanying or preceding most other evolutionary innovations that permit snakes to consume large prey, such as kinetic skulls. Greene pointed out that this was before the origin of rodents, often mentioned as potentially relevant to the evolution of snake prey-killing behaviors. Constriction was then lost at least twice—once in uropeltids (which feed underground on earthworms, although I'm not actually aware of any detailed observations of uropeltid feeding behavior) and at least once in basal colubroids, where it might have been  at first replaced by venom. Venom was then subsequently lost in numerous caenophidian lineages, replaced by re-evolution of constriction in some or by other specializations (tooth diastemata for holding skinks, egg-eating) in others, and in some caenophidian lineages snakes use both as appropriate, sometimes together (or they may elect to use neither even if both are available).

Both constriction and venom reduce the cost of feeding in terms of time, energy, and/or the probability of the prey harming the snake, but in constricting snakes, everyday locomotion and large prey neutralization are coupled, whereas in venomous snakes they are independent (snakes don't use their fangs to get around). This could be one reason why venom as an evolutionary innovation led to a more speciose radiation of snakes; it's also more susceptible to evolutionary arms races, because prey can evolve resistance to certain venom compounds, but not to constriction. Specialization for constriction is more than just behavior—constricting species also have more vertebrae per unit length than non-constricting species. And there are costs to both, which must be outweighed by the benefits of that defining snake trait: being able to consume prey almost as large, and sometimes much larger, than yourself!



1 An interesting exception are Scarletsnakes, Cemophora coccinea, the closest relatives of kingsnakes, which feed mostly on reptile eggs but also use their coils to hold lizard prey in the rare instances when they eat them. It is certain that Scarletsnakes evolved from constricting ancestors but because they almost never eat prey that need to be killed beforehand, evidently they rarely constrict.



2 okinavensis has been shown not to be closely related to other Ovophis, but no new genus has yet been created for it because more data are needed.


ACKNOWLEDGMENTS

Thanks to Karen Morris for asking me this question, and to Alpsdake and Danny Davies for the use of their photos.

SELECTED REFERENCES

For a full list of all the references I consulted in preparing this post, click here

Andrade, R. d. O. and R. A. M. Silvano. 1996. Comportamento alimentar e dieta da "Falsa-coral" Oxyrhopus guibei Hoge & Romano (Serpentes, Colubridae). Revista Brasileira de Zoologia 13:143-150 <full-text>

Auffenberg, W. 1961. Additional remarks on the evolution of trunk musculature in snakes. The American Midland Naturalist 65:1-16 <full-text>

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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.