Now would be a good time to publish a massive and comprehensive overview of where we’re at in our understanding of colubrid snake diversity and phylogenetic history. But that’s not happening today. Instead…
Caption: a garter snake in the water, on show at The Deep in Hull, UK. The Deep is a big aquarium located on the edge of the Humber, and it’s home to tropical amphibians and reptiles as well as numerous marine species. Image: Darren Naish.
…. I here provide thoughts on a colubrid I recently got to see in captivity: the Lake Zacapu garter snake Thamnophis eques insperatus, several specimens of which are currently on show at The Deep, Hull, UK. They’ve been there since 2016, have bred there, and The Deep is the only collection in the UK – and indeed the whole of Europe – to house and exhibit this snake. Here’s an article announcing this news.
Caption: a baby Zacapu garter snake, as featured in news articles released by The Deep. Image: (c) The Deep.
On natricines and taxonomy. Garter snakes are a group of (mostly) North American colubrids, deeply embedded within the colubrid sub-group Natricinae. Here I have to mention that some experts argue that ‘Colubridae’ of tradition should be split up into various family-level sub-groups (e.g., Vidal et al. 2007, Zaher et al. 2009, 2019), in which case Natricinae becomes Natricidae. This is my personal preference (and.. yes, I can justify that. It’s to do with the divergence times of the respective lineages and how they compare to family-level groups in other tetrapod clades). Colubridae, in this classification, becomes restricted to that group that contains the Eastern racer Coluber constrictor and its numerous close relatives, and Colubridae sensu lato then becomes Colubroidea… which is a bit confusing as this name is (in the traditional taxonomic system) already in use for the clade that contains viperids and elapids in addition to colubrids sensu lato. My sense from recent publications is that workers mostly want to stick with a tweaked version of the traditional nomenclature (e.g., Pyron et al. 2011, Figueroa et al. 2016, Deepak et al. 2021), in which case we still recognize Natricinae within Colubridae.
Caption: substantially simplified colubrid phylogeny, based on the results of Figueroa et al. (2016), and using the taxonomy where the clades concerned are regarded as colubrid ‘subfamilies', not as ‘families’. Other articles – coming soon – will discuss various of these other groups. Images: Sibynophiinae: Thomas Brown, CC BY 2.0 (original here); Natricinae: Orchi, CC BY-SA 3.0 (original here); Pseudoxenodontinae: Umeshsrinivasan, CC BY-SA 3.0 (original here); Dipsadinae: Geoff Gallice, CC BY 2.0 (original here); Grayinae: Kate Jackson, used with permission; Calamariinae: in public domain; Ahaetuliinae: Rushenb, CC BY-SA 4.0 (original here); Colubrinae: Dawson, CC BY-SA 2.5 (original here).
Natricinae is a large group (containing about 40 extant genera) mostly associated with North America and Eurasia, though it does have representation in Africa and one outlier (the Common or Mair’s keelback Tropidonophis mairii) has made it to Australasia. Natricines are often associated with wetlands and some regularly eat fishes and amphibians. Crayfish, other crustaceans, and worms are eaten by some species.
Oviparity (egg-laying) is the norm for natricines outside of North America (just two Asian species are viviparous), but all American members of the clade are viviparous. Does this have any association with the aquatic proclivities of these snakes? That was tested in a recent study; read on. From the provincial west European perspective, natricines are among the most familiar snakes of all, since the species we encounter most frequently – as a British person I’m thinking of the Barred grass snake Natrix helvetica of western and central Europe – are members of this group. And if you haven’t heard the news, the ‘Grass snake Natrix natrix’ of tradition has proven to be three species, and the one present here in the west of Europe is N. helvetica (Kindler et al. 2017).
Caption: beautiful photo of a Barred grass snake. This species mostly occurs in the southern half of the UK, the Netherlands, France, Switzlerland and Italy, and is the most familiar snake species to those of us who live in western Europe. It’s diverse enough across this range that five subspecies are currently recognized. Image: Benny Trapp, CC BY-SA 4.0 (original here).
A brief rant on old Tetrapod Zoology material. One more thing on colubrids in general: I’ve published a fair amount about these snakes – their diversity, natural history, phylogeny and taxonomy – in past Tet Zoo articles. But those articles – the ones hosted at Scientific American (that’s ver 3) in particular – are now completely ruined. They no longer have their images (which were key), are paywalled, and I can’t find intact versions at wayback machine. That’s very dispiriting given that my intention in covering obscure material of this sort is, and always has been, to release it into the wild. There’s therefore no point in linking to it anymore.
Caption: the vast majority of old Tetrapod Zoology articles are ruined. I tried to access this (at left) 2012 Tet Zoo article on colubrid snakes, but all the images have been removed… aaaand you can only look at it for a second anyway before (at right) the note about subscription pops up and makes it invisible. Yes, I have archived versions of these articles (many thanks to those who obtained them and sent them on to me) and will republish them here in time. And I already have so much other stuff to do….
Lake Zacapu’s garter snakes, a brief history. Anyway…. as you might guess from its name, the Lake Zacapu garter snake is unique to Laguna de Zacapu, an upland lake (2000 m above sea level) in Michoacán, western Mexico. This is large for a lake (1 km wide and 400 m wide) but small as the entire geographical range of a subspecies, and it’s the only known place where this snake occurs, making it of conservation concern. So far as I can tell, I don’t think we can say more than that, since not enough is known to properly evaluate its conservation status. Lake Zacapu is spring-fed and feeds numerous irrigation canals that sustain crops. It was apparently not shown on maps until the mid-1960s (Conant 2003).
Caption: Conant’s 2003 map showing the location of Mexican lakes and drainage areas relevant to garter snake discovery, the caveat being that this depicts their appearance prior to European invasion, in c 1500. Image: Conant (2003).
I have to mention in passing that the lake is home to an endemic ambystomatid or mole salamander, Ambystoma andersoni, named in 1984. In fact, the history of the discovery and recognition* of this salamander – a neotenous species similar to the better known Axolotl A. mexicanum – is tied to that of the region’s garter snakes since the herpetologists who made these snake and salamander discoveries were co-operating and even on the same trips together (Conant 2003). I wrote about endemic Mexican mole salamanders in 2012, but it’s another article now rendered inaccessible.
* As ever, terms like ‘discovery’ and ‘recognition’ refer to the formal scientific canon, not to collective human knowledge. These animals were certainly known to the people who lived alongside them, as is usual.
Caption: Anderson’s salamander, one of several ambystomatid salamanders endemic to Mexico’s lakes. Most of these species are geologically young and among the most recently evolved of species known to science. Image: Arican, CC BY 3.0 (original here).
Also of interest is that T. e. insperatus is, like Anderson’s salamander, a recently discovered, recently described taxon, having been named in 2003 for a specimen collected as roadkill in 1961 (Conant 2003). This was found 6 km away from any suitable lake-side habitat, and this explains why Roger Conant gave it the subspecific name insperatus, meaning ‘unhoped for; unexpected’ (Conant 2003, p. 26). The specimen was an unsightly mess, and Conant didn’t figure the whole animal for that reason, instead only figuring the diagnostic scalation and pigmentation present on its body. Following this initial description, no further specimens were reported, leading to concern that the animal might not be extant.
It would appear, however, that this was due to insufficient knowledge of the location, since visits to the lake by garter snake specialist Steven Bol found the snakes relatively easy to find (Bol 2012). Bol reported that the Zacapu garter snake is variable in pigmentation, some individuals being light and prominently marked with yellow, others being darker and lacking yellow markings entirely.
Caption: I haven’t seen the published version of Bol’s 2012 article announcing the rediscovery of the Zacapu garter snake, but a well-illustrated online version is here; above is a screengrab. Image: (c) Steven Bol.
The Zacapu population is currently regarded as a subspecies of the Mexican garter snake, a large and heavy built garter snake (second in size only to the Giant garter snake T. gigas of California) that can reach 1.3 m in total length. I mostly think of garter snakes as slender animals less than 40 cm long, so the fact that there are hefty, thick-bodied species over a metre in length is surprising. Within natricines, garter snakes are especially close to the Nerodia water snakes, a wholly North American group (Figueroa et al. 2016).
Phylogenetic studies indicate that natricines originated in Asia around 40 million years ago (during the Late Eocene), and among the several dispersals that occurred within the history of the group was an eastwards one that involved the colonizing of North and Central America (Deepak et al. 2021). It appears that ancestral natricines were mostly terrestrial but there are indications that anuran-based diets and ‘aquatic generalist’ diets were important in the group’s early history. Vermivory – which is widespread in garter snakes and may be the main way they make a living in suburban environments – appears to be a specialized habit. Viviparity evolved independently at least three times, but not in correlation with aquatic habits (Deepak et al. 2021). Yes, viviparity is certainly useful for aquatic snakes (and other reptiles too), but you don’t need to be aquatic for viviparity to evolve, as is demonstrated by the numerous times it occurred in thoroughly terrestrial squamates.
Caption: a garter snake montage, depicting some of the variation in size and pigmentation present across the 35 or so species. Clockwise from left: Eastern garter snake T. sirtalis sirtalis, Coast garter snake T. elegans terrestris; Mexican garter snake T. eques. Images: Wilson44691, public domain (original here); Steve Jurvetson, CC BY 2.0 (original here); NS777, CC BY-SA 4.0 (original here).
A diversion on scale microornamentation. While looking at the captive Zacapu garter snake shown here, I noticed that the meniscus was bending around the snake to such a degree that the snake’s surface looked hydrophobic. Is this the case? Would a snake (or any squamate or reptile) benefit from having a hydrophobic surface? Animals known to be hydrophobic – like aquatic insects – are like this because they ‘want’ to remain on the water surface, not be immersed in or swim through it. However, a hydrophobic surface is also helpful because it prevents the attachment of air bubbles that otherwise interfere with buoyancy (e.g., Ishii et al. 2016).
Caption: the bending of the meniscus about the scales of a garter snake. This might not mean anything. It might just be normal for an object part-submerged in water. Buuut… does it also mean that this snake has water-repellent scales? Image: Darren Naish.
I’m not sure that anyone imagines squamate scales to simply be flat sheets of featureless keratin, but they’re anything but once you learn about them at the microscopic level. Indeed, anatomists have known since at least the 1870s that squamate scales possess microornamentation or nanotexture (take your pick) that perhaps has a function in epidermal integrity, in the frictional properties of the skin, or in anti-fouling and self-cleaning. Does this microornamentation also provide water-repellent properties and thus make life easier for species that swim? Exploring this topic properly would require an article all its own and I might have to come back to it. Some particularly fascinating research concerns the hydrophobic properties of rattlesnake scales (where the scales are used to harvest rainwater and even sleet and snow; the snakes then drink the collected water from their own skin; Phadnis et al. 2019) and those of Gaboon vipers Bitis rhinoceros (Spinner et al. 2014). In the latter, nanoridges and other nanostructures make the scales superhydrophobic, this being most prominent on the black scales. These have a velvety texture.
Caption: rainwater droplets clinging to rattlesnake scales (at left), with a close-up image of a scale at right. As discussed by Phadnis et al. (2019), the scale microornamentation appears adapted for this role.
Caption: at left, Bitis has an extremely complex scale surface microornamentation, which is hierarchical on some scales (like the black ones shown in B): there are leaf-shaped protrusions marked with micro-ridges. As the diagram shows, microornamentation varies according to which region of the body the scales come from. At right, we see how the black, velvety scales have superb water-shedding qualities. Images: Spinner et al. (2014).
More recent work has also shown that lipid coatings on snake scales provide lubrication and wear protection (Baio et al. 2015). It also appears that these lipids make the scales hydrophobic, and work done on the microornamentation of natricine scales – including that of garter snakes – indicates that these snakes have a surface pore pattern where cup-like chambers may “assist in the retention of the exudate on the surface of the scale. Such a coating of fatty material on the surface might form a water barrier on the skin especially advantageous to aquatic taxa” (Chiasson & Lowe 1989, p. 109). So… are garter snake scales water-repellent and, if they are, is this an adaptation for amphibious life? Yes, it would appear so.
Finally… yeah, I’m so angry about the situation with the old colubrid-themed articles from Tet Zoo ver 3 that I’ll be republishing them here, with updates.
For previous Tet Zoo articles on squamates, see… [UPDATE: as per the comments above, it now seems that at least some of these articles have been made inaccessible by Sci Am]
Tale of the Takydromus, September 2013
Racerunner Lizards of the World Unite, October 2014
What's With All These New Chameleon Names?, Part 1, February 2016
By the Horns of Trioceros, the Casque of Calumma, the Brood of Bradypodion--Chameleons, Part 2, February 2016
Palleon, Archaius, Kinyongia, Nadzikambia--The Last Chameleons, Part 3, March 2016
The Tropidurine Treerunners, December 2017
The Tet Zoo Guide to Mastigures, August 2018
The Remarkable Basilisks, May 2023
Do Lizards Really Have ‘Mite Pockets’?, March 2024
Refs - -
Chiasson, R. B. & Lowe, C. H. 1989. Ultrastructural scale patterns in Nerodia and Thamnophis. Journal of Herpetolology 23, 109-118.
Conant, R. 2003. Observations on Garter Snakes of the Thamnophis eques complex in the Lakes of Mexico’s Transvolcanic Belt, with descriptions of new taxa. American Museum Novitates 3406: 1-64.
Deepak, V., Cooper, N., Poyarkov, N. A., Kraus, F., Burin, G., Das, A., Narayanan, S., Streicher, J. W., Smith, S.-J. & Gower, D. J. 2021. Multilocus phylogeny, natural history traits and classification of natricine snakes (Serpentes: Natricinae). Zoological Journal of the Linnean Society 195, 279-298.
Figueroa, A., McKelvy, A. D., Grismer, L. L., Bell, C. D. & Lailvaux, S. P. 2016. A species-level phylogeny of extant snakes with description of a new colubrid subfamily and genus. PLoS ONE 11, e0161070.
Ishii, D., Yamasaki, H., Uozumi, R. & Hirose, E. 2016. Does the kinorhynch have a hydrophobic body surface? Measurement of the wettability of a meiobenthic metazoan. Royal Society Open Science 3, 160512.
Kindler, C., Chèvre, M., Ursenbacher, S., Böhme, W., Hille, A., Jablonski, D., Vamberger, M. & Fritz, U. 2017. Hybridization patterns in two contact zones of grass snakes reveal a new Central European snake species. Scientific Reports 7, 7378.
Pyron, R. A., Burbrink, F. T., Colli, G. R., Montes de Oca, A. N., Vitt, L. J., Kuczynski, C. A. & Wiens, J. J. 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.
Vidal, N., Delmas, A.-S., David, P. Cruaud, C., Couloux, A. & Hedges, S. B. 2007. The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. C. R. Biologies 330, 182-187.
Zaher, H., Grazziotin, F. G., Cadle, J. E., Murphy, R. W., Cesar de Moura-Leite, J. & Bonatto, S. L. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia, Museu de Zoologia da Universidade de São Paulo 49, 115-153.
