The 9,999th Reptile

Click here to view this post in Spanish
Haga clic aquí para ver este mensaje en Español

Number of new snake species by decade, with highlights
Data from The Reptile Database

Linnaeus's 1758 Systema Naturae, the starting point of zoological nomenclature, described 118 species of reptiles, including 74 snakes (not counting the limbless lizards and amphibians he included in the same group). It took over 100 years for the number of described species of snakes to reach 1000, an event that probably passed without much notice amid the American Civil War. Since that time, new snake species descriptions have been added at the rate of about 15 a year, although molecular taxonomy has increased this pace over the last few decades. The trends for snakes and for reptiles as a whole have been similar, and on July 9th, 2014, a team of American, German, Lao, and Vietnamese scientists described a new species of gecko from Laos, which the journal Herpetological Review reported as the 10,000th reptile species. Needless to say, I was excited, but I was also extremely disappointed because I had been so hoping that it would be a snake! Rather than admit defeat and scrap this planned post, I emailed Peter Uetz at The Reptile Database, an incredible resource that I've praised before, to confirm that this gecko was indeed #10,000. As usual for taxonomy and as I should have suspected, the reality was a bit more complicated.

Although Cyrtodactylus vilaphongi was the 10,000th reptile species for a while, the order and position of entries in The Reptile Database is constantly changing. Although new species get added to the end of the list, it's common for two or more existing species to get synonymized or merged, which moves the position of all subsequent species up. Furthermore, sometimes species that were described long ago and subsequently synonymized are revalidated, leading to 'new' species that aren't really new in the sense that they have existed before. Finally, often existing species get split up, leading to additions that aren't as dramatic as legitimate new discoveries. This last complication is on the rise now that molecular systematics has enabled us to describe the cryptic diversity of some lineages, which are not all that morphologically distinct but may contain considerable genetic diversity.

At the time of my email to Peter last month, C. vilaphongi was the 9988th species, and (happily), a new snake, Siphlophis ayauma, was #10,000. Although this has probably changed again by now, I'm going to operate under the assumption that, since we can't really say with certainty that any particular species was #10,000, if it was a snake, it was probably one of the 11 brand new snake species that have been described so far this year. You can read about many of these on the blog 'Species New to Science', but I'm going to highlight them in a little more detail here.

Rhabdophis guangdongensis
From Zhu et al. 2014

The first new snake described this year, Rhabdophis guangdongensis, was collected by a team of Chinese herpetologists in Guangdong Province in 2008. The reason it wasn't described until the February 20th issue of the journal Zootaxa is because, as is often the case, it takes a couple of years to compare both the anatomy and the DNA of a suspected new species to reference specimens of known similar species and establish that the species really is new. In the past, particularly prior to the internet, the difficulty of doing this was a huge problem, resulting in close to half of all 'new' species later being invalidated as duplicates. The genus Rhabdophis  is distributed in southern and eastern Asia, and this is the 21st species. It's an extremely interesting genus from a chemical ecology perspective, because at least one species sequesters defensive chemicals from its prey and provisions them to its young (which I wrote about for Scientific American shortly after I started this blog). A recent paper by Yosuke Kojima and Akira Mori on the Japanese species R. tigrinus showed that females periodically leave wetlands for forest streams where they forage on toads, likely to obtain the necessary toxins for provisioning their offspring. The new species also has specialized structures, known as nuchal glands, on the back of its neck, so presumably it stores bufotoxins there as well, although this has yet to be verified.

Opisthotropis durandi
From Teynié et al. 2014

On March 3rd, a team of French, German, and Vietnamese scientists published a description of Opisthotropis durandi, a highly aquatic snake collected from the base of a waterfall in northern Laos. This is the seventh species of Opisthotropis described in the past 20 years, and the first from Laos (although other species are likely to occur there based on their occurrence in surrounding countries). Like the new Rhabdophis, it is also the 21st species in its genus. It is important to realize that, like most species new to science, this snake was already known by local people. It is called Ngou Koung or Ngou Kung, meaning “shrimp snake”, suggesting that it may eat shrimp. The pools at the base of the waterfall where the first specimen was found contained many small shrimp.

Eutrachelophis bassleri and its weird penis
From Myers & McDowell 2014
A color photo of E. bassleri was published in Echevarría & Venegas 2015

Harvey Bassler, a petroleum geologist, explored many of the Amazon's upper tributaries for his work during the 1920s and 30s, during which time he collected over 4,200 snakes on the side. Bassler deposited his magnificent collection in the American Museum of Natural History in 1934, and on March 6th this year Charles Myers and Samuel McDowell published a monograph in the Bulletin of the American Museum of Natural History describing a species of snake collected by Bassler in 1927, for which they erected a new genus, Eutrachelophis (‘beautiful-necked snakes’’). They also placed in this genus a species originally described by Boulenger in 1905, Rhadinaea steinbachi, which they renamed Eutrachelophis steinbachi. Although the two species (and a third, yet undescribed) have very similar skeletons, muscles, glands, viscera, and markings, they probably would have been placed in separate genera had they been described in the 19th or early 20th century because their hemipenes are so different. E. steinbachi has long but relatively normal-looking hemipenes, whereas E. bassleri  has extremely unusual heimpenes tipped with a dome-like structure so strange (at least within the world of snake hemipenes) that the authors wrote "we have seen nothing quite like [it]." Hemipenes were traditionally considered one of the most taxonomically-important structures in snakes¹ because they were considered to be evolutionarily neutral (that is, unlikely to change in response to selection), but a growing awareness that evolution by both natural and especially sexual selection can influence the morphology of male genitalia led these authors to recognize that these two snakes were in fact close relatives. Although we await molecular confirmation, the authors propose a mechanism by which differential expression of Hox genes² could cause such a rapid divergence in hemipenal morphology between two sister species.

Siphlophis ayauma
From Sheehy et al. 2014

On January 12th, 2008, a group of American and Ecuadorian herpetologists stopped for lunch at a grilled-chicken restaurant in Paute, Azuay province, Ecuador. They noticed a peculiar sun-faded snake on display in a jar of alcohol that they couldn't quite put a name to. Following negotiation with the restaurant owner, the specimen was acquired and determined to belong to the genus Siphlophis, but could not be identified to any known species. A few months later, another specimen was found alive about 100 miles to the north, and two more were discovered in 2011 about the same distance to the south. A fifth individual is now recognized to have been hiding out unnoticed in the collection of the Museo de Zoología, Pontificia Universidad Católica del Ecuador. Because of its red-banded head and its occurrence in the mountains near cold (achachay) streams, the new species was named Siphlophis ayauma after the Kichwa spirit Aya Uma, a good spirit devil who derives strength from nature, particularly from cold mountain pacchas (cascades) and is represented in Kichwa folklore as having a colorful red-banded head. This is the seventh species in the genus, the third species known from Ecuador, and the first new species of Siphlophis since 1940. The results are published in the April 1st issue of the South American Journal of Herpetology.

Philodryas amaru
From Zaher et al. 2014

In a montane grassland high in the Andes Mountains of southern Ecuador, another genus gained its 21st species this year: Philodryas amaru. Known to the Ecuadorian and Brazilian authors since 2005, a small population of these striped racers was formally described in Zootaxa on April 4th this year. The new species resembles Philodryas simonsii in color pattern, but differs noticeably in its hemipenis morphology. "Amaru" means "snake" in Kichwa, and is also the name of a snake deity who influences water and the economy. This diurnal snake lays clutches of 9-13 eggs underground in galleries and under decaying logs, and probably eats frogs and lizards. It is a close relative of the Galapagos racers that I've written about before.

Causus rasmusseni
From Broadley 2014; photo by Paul L. Lloyd

Night adders (genus Causus) are a small and unusual group of vipers found in sub-Saharan Africa. They were once thought to be the most primitive vipers and were placed in their own subfamily, but they are now grouped with the viperines even though they have a plethora of unusual features: platelike head scales, round pupils, a different hinge mechanism for their erectile fangs, incomplete fang canal closure, and elongate venom glands in most species. On April 25th of this year, Don Broadley³ described the first new species of Causus since 1905. He named it Causus rasmusseni after the late Jens Rasmussen, a Dutch expert on African snakes who died in 2005. This species is found only in the watershed between the Congo and Zambezi basins, where it co-occurs with three other species of Causus. Broadley first became aware that there might be a new species of night adder in this region in 1991, when he noticed pale gray C. rhombetaus from northwestern Zambia with black markings and low ventral scale counts. In 2013, someone sent him a picture of one eating a toad (another unusual adaptation that night adders share with several other snakes), which prompted him to look again at the unusual specimens and describe them as a new species. Few molecular data are available for Causus, so this diagnosis is based on morphology alone.

Micrurus potyguaraFrom Pires et al. 2014

Brazil is graced with nearly 400 species of snakes, including 30 of the world's ~80 species of coralsnakes. The morphology of coralsnakes is highly variable, and there are many misidentified specimens in museum collections, so it is often difficult to recognize new species. A group of Brazilian herpetologists working on the tri-colored coralsnakes from the endangered northeastern coastal forests discovered a new species, which they described in the June 5th issue of Zootaxa (if any of these dates are your birthday, then you share a birthday with that of a new species of snake!).

Top: Jaw of Lycodon aulicus
From Jackson & Fritts 2004
Middle: Lycodon zoosvictoriae
From Neang et al. 2014
Bottom: Lycodon cavernicolus
From Grismer et al. 2014

Wolfsnakes (genus Lycodon) are named for their fearsome-looking fang-like anterior maxillary teeth. Unlike the true fangs of vipers, elapids, and atractaspidids, wolfsnake teeth are not grooved or hollow and they have no venom. Instead, their strongly arched upper jaw helps them feed on skinks, whose hard, cylindrical bodies fit snugly into their diastema, or the gap between their anterior and posterior teeth. The wolf-like anterior teeth keep the skink from being squeezed out of the mouth, while the posterior teeth slice through the skink's cycloid scales. At least 16 of the nearly 60 species of Lycodon have been described since the 1990s, including two this June: Lycodon zoosvictoriae from the Cardamom Mountains of southwestern Cambodia, and L. cavernicolus from a limestone cave in peninsular Malaysia. The latter is a cave-adapted species, both specimens of which were found climbing several feet above the cave floor, in total darkness. It's likely that they eat a cave-adapted gecko. Many of the caves in this region are in immediate danger of being quarried for cement before their endemic fauna and flora can be fully documented. Both of these species were also described in Zootaxa, which is a relatively new journal dedicated almost exclusively to rapid publication of new species descriptions, with the stated goal of aiding conservation efforts by circumventing the lengthy delays normally associated with publication of new science. Since its inception in 2001, Zootaxa has become a daily journal that has published nearly one quarter of all new animal taxa and nomenclatural acts in the last five years, including over 400 new species of reptiles and the 7000th species of amphibian.

"Cloudogram" of Crotalus triseriatus species group
showing the new nine-species arrangement
From Bryson et al. 2014

Just three days before the new gecko, a team of scientists from Mexico, the USA, and Canada published a genetic analysis of the Crotalus triseriatus species group, which contains small montane rattlesnakes found in Mexico and the southwestern USA. Although five species were historically recognized within the group, an analysis of seven nuclear genes revealed that there are at least nine species, including two that were previously recognized as subspecies and two more that have not heretofore been formally recognized. The paper described the two new species: Crotalus tlaloci, named for Tláloc, the Aztec god of rain, and Crotalus campbelli, named for herpetologist Jonathan Campbell. The authors of this paper suggest that these rattlesnakes speciated rapidly from a single common ancestor during the uplifting of the Trans-Mexican Volcanic Belt near the end of the Neogene period 2.6 million years ago, which makes sense because they are not very mobile and populations of their common ancestor likely would have become isolated from one another  on various "Sky Islands" of suitable habitat during the genesis of this new mountain range. Many species are endemic to the high-altitude pine-oak forests and grasslands of this region, which has become famous as the overwintering grounds of the Monarch Butterfly.

Chironius diamantina
From Fernandes & Hamdan 2014

Surprise! Just when you thought we were through, at press time the description of four more new species of snake had just been published, all from relatively recent issues of Zootaxa. One is a Brazilian species of Chironius, one of my favorite genera. Chironius diamantina is the 16th species in the genus, which is unusual is having a very low, even number of dorsal scale rows (10 or 12), the central pair of which are strongly keeled, giving the snake a distinctly flat-backed appearance. This species is found in riparian forests along rocky streams in coastal Brazil, not too far south of the new coralsnake (above). Chironius are diurnal and generally eat birds and mammals. Another is a new Asian keelback, Herpetoreas burbrinki, from near the border of China, India, and Burma. which is relatively closely related to the Rhabdophis above. Finally, two new species from the large ground-dwelling Latin American genus Atractus, both small and described from single specimens collected decades ago in Colombia (perhaps they will one day be rediscovered). More new species from both of these groups will likely follow, given the taxonomic untidiness of their genera. [Update: shortly after publication David Salazar-Valenzuela alerted me to the fact that I had missed his description, with colleagues, of a third new Atractus from the cloud forests of northern Ecuador earlier this year, in the journal Herpetologica. They mention that some of the specimens were collected from under logs alongside an undescribed species of slender blindsnake of the genus Trilepida, so it seems we are at 3,500 this year without a doubt!] [[Update II: It seems I missed more than I thought - a new species of Trimeresurus from Sumatra was described in September from specimens collected in 1899, and a new Ninia from Trinidad was described in August from a 1988 specimen.]]

In addition to these 15 species, there are a couple of species of snake which were described long ago but that were revalidated recently, including several scolecophidians (Typhlops silus, first described in 1959; Afrotyphlops angeli, first described in 1952; and Letheobia acutirostrata, first described in 1916) and a rattlesnake (Crotalus armstrongi, originally described as a subspecies in 1979 and elevated by the same group that described C. tlaloci and C. campbelli). These are typically announced with less fanfare than the truly new descriptions that I've highlighted above.

Although it's actually been the slowest year for new snakes since 1997⁴, we have 15 new snakes this year, bringing snakes to a total of 3,499 (and 2014 isn't over yet!). We could make it to 3,500 snakes in the same year that we hit 10,000 reptiles. I think these milestones in taxonomy emphasize the importance of reptiles and how much we have left to learn about them. I doubt that the pace of new species descriptions will slow down anytime soon, as experts estimate that less than 15% of the species on Earth have yet been described. Increasingly, reptiles, and snakes in particular, are becoming poster-children for biodiversity and conservation, a welcome change from their history of being overlooked and maligned. Soon, we will have high-quality global range maps for all species of reptiles, an achievement reached some time ago by amphibians, mammals, and birds, which will enable their incorporation into global assessments of vertebrate diversity and conservation planning. It's an exciting time.

For a complete list of all 24 snake species eventually described in 2014, click here.

ACKNOWLEDGMENTS

Thanks to Peter Uetz at The Reptile Database for sharing with me some inside information, and to the authors of these papers for their photos.

REFERENCES

Newspaper clipping from 10 January 1960
showing Broadley with his amputated finger.
You can see more at the finger's Facebook page
or listen to Broadley describe the experience here.

Angarita-Sierra, T. 2014. Hemipenial Morphology in the Semifossorial Snakes of the Genus Ninia and a New Species from Trinidad, West Indies (Serpentes: Dipsadidae). South American Journal of Herpetology 9:114-130 <link>

Broadley, D. G. 2014. A new species of Causus Lichtenstein from the Congo/Zambezi watershed in north-western Zambia (Reptilia: Squamata: Viperidae). Arnoldia Zimbabwe 10:341-350 <link>

Bryson, R. J., C. W. Linkem, M. E. Dorcas, A. Lathrop, J. M. Jones, J. Alvarado-Diaz, C. I. Grunwald, and R. W. Murphy. 2014. Multilocus species delimitation in the Crotalus triseriatus species group (Serpentes: Viperidae: Crotalinae), with the description of two new species. Zootaxa 3826:475-496 <link>

Cope, E. D. 1895. The classification of the Ophidia. Transactions of the American Philosophical Society 18:186-219 <link>

Dowling, H. G. 1967. Hemipenes and other characters in colubrid classification. Herpetologica 23:138–142 <link>

Grismer, L. L., E. S. H. Quah, S. Anuar, M. A. Muin, P. L. Wood Jr, and S. A. M. Nor. 2014. A diminutive new species of cave-dwelling Wolf Snake (Colubridae: Lycodon Boie, 1826) from Peninsular Malaysia. Zootaxa 3815:51-67 <link>

Guo, P., Q. Liu, L. Zhang, J. X. Li, Y. Huang, and R. A. Pyron. 2014. A taxonomic revision of the Asian keelback snakes, genus Amphiesma (Serpentes: Colubridae: Natricinae), with description of a new species. Zootaxa 3873:425-440 <link>

Fernandes, D. and B. Hamdan. 2014. A new species of Chironius Fitzinger, 1826 from the state of Bahia, Northeastern Brazil (Serpentes: Colubridae). Zootaxa 3881:563-575 <link>

Trimeresurus gunaleni
From Vogel et al 2014

Jackson, K. and T. H. Fritts. 2004. Dentitional specialisations for durophagy in the Common Wolf snake, Lycodon aulicus capucinus. Amphibia-Reptilia 25:247-254 <link>

Köhler, G. and M. Kieckbusch. 2014. Two new species of Atractus from Colombia (Reptilia, Squamata, Dipsadidae). Zootaxa 3872:291-300 <link>

Linnaeus, C. 1758. Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. [10th ed.]. Laurentii Salvii, Holmiae, Stockholm, Sweden <link>

Myers, C. W. and S. B. McDowell. 2014. New Taxa and Cryptic Species of Neotropical Snakes (Xenodontinae), with Commentary on Hemipenes as Generic and Specific Characters. Bulletin of the American Museum of Natural History 385:1-112 <link>

Neang, T., T. Hartmann, S. Hun, N. J. Souter, and N. M. Furey. 2014. A new species of wolf snake (Colubridae: Lycodon Fitzinger, 1826) from Phnom Samkos Wildlife Sanctuary, Cardamom Mountains, southwest Cambodia. Zootaxa 3814:68-80 <link>

Pires, M. G., N. J. da Silva Jr., D. T. Feitosa, A. L. d. C. Prudente, G. A. P. Filho, and H. Zaher. 2014. A new species of triadal coral snake of the genus Micrurus Wagler, 1824 (Serpentes: Elapidae) from northeastern Brazil. Zootaxa 3811:569-585 <link>

Atractus savagei
From Salazar-Valenzuela et al. 2014

Salazar-Valenzuela, D., O. Torres-Carvajal, and P. Passos. 2014. A New Species of Atractus (Serpentes: Dipsadidae) from the Andes of Ecuador. Herpetologica 70:350-363 <link>

Schneider, N., T. Q. Nguyen, M. D. Le, L. Nophaseud, M. Bonkowski, and T. Ziegler. 2014. A new species of Cyrtodactylus (Squamata: Gekkonidae) from the karst forest of northern Laos. Zootaxa 3835:80-97 <link>

Sheehy, C. M., M. H. Yánez-Muñoz, J. H. Valencia, and E. N. Smith. 2014. A new species of Siphlophis (Serpentes: Dipsadidae: Xenodontinae) from the eastern Andean slopes of Ecuador. South American Journal of Herpetology 9:30-45 <link>

Teynié, A., A. Lottier, P. David, T. Q. Nguyen, and G. Vogel. 2014. A new species of the genus Opisthotropis Günther, 1872 from northern Laos (Squamata: Natricidae). Zootaxa 3774:165-183 <link>

Uetz, P. 2010. The original descriptions of reptiles. Zootaxa 2334:59-68 <link>

Vogel, G., P. David, and I. Sidik. 2014. On Trimeresurus sumatranus (Raffles, 1822), with the designation of a neotype and the description of a new species of pitviper from Sumatra (Squamata: Viperidae: Crotalinae). Amphibian and Reptile Conservation 8:1–29 <link>

Zaher, H., J. C. Arredondo, J. H. Valencia, E. Arbeláez, M. T. Rodrigues, and M. Altamirano-Benavides. 2014. A new Andean species of Philodryas (Dipsadidae, Xenodontinae) from Ecuador. Zootaxa 3785:469–480 <link>

Zhu, G.-X., Y.-Y. Wang, H. Takeuchi, and E.-M. Zhao. 2014. A new species of the genus Rhabdophis Fitzinger, 1843 (Squamata: Colubridae) from Guangdong Province, southern China. Zootaxa 3765:469-481 <link>

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

Tetrodotoxin-resistant snakes

Click here to read this post in Spanish
Haga clic aquí para leer este blog en español

An adult male Taricha granulosa in breeding condition.
There is enough tetrodotoxin in this newt to kill you
and about 29 other people.

Gartersnakes eat newts. I mentioned this remarkable fact in my article on the Scientific American Guest Blog, but it's interesting enough to warrant a more detailed treatment. In 1990, Edmund D. Brodie III and his father, Edmund D. Brodie Jr, published a paper in the journal Evolution that provided the first evidence of a pair of species in a highly coupled arms race. Previously, the concept of an arms race had been criticized because the potential cost to the prey (loss of life) was perceived as more dire than the potential cost to the predator (merely the loss of dinner). This imbalance, known as the life-dinner principle, led scientists to suggest that tightly co-evolving arms races between predators and prey could not exist, because selection pressure on the predator would always be less than that on the prey. However, reasoned Brodie & son, if the prey's defenses are lethal, then selection might be equally strong on both predator and prey, because only highly resistant predators could survive a predation event. This is the case in the predator-prey dynamic between the Rough-skinned Newt (Taricha granulosa) and the Common Gartersnake (Thamnophis sirtalis), which is centered around a toxin called tetrodotoxin.

Chemical structure of tetrodotoxin

Tetrodotoxin is a very interesting chemical. James Bond was poisoned with it at the end of From Russia with Love (and saved by an antidote, which does not exist in real life). It's responsible for the tingling sensation caused by eating properly prepared fugu (and woe betide those who consume this Japanese pufferfish dish improperly prepared). Named after the pufferfish family, it is found in a wide variety of organisms, from flatworms to the blue-ringed octopus, its biological origins are enigmatic. Many species are thought to sequester it from symbiotic bacteria, although some, including newts, are believed to be capable of synthesizing it themselves. In the lab, tetrodotoxin is created under conditions of extreme heat and pressure, and how this molecule is generated inside of living cells is a mystery. Furthermore, it is an extremely potent poison: tetrodotoxin binds to and occludes the extracellular pore of voltage-gated ion channels embedded in muscle cell membranes, preventing the flow of sodium ions into the cell and interrupting the action potentials necessary for muscle contraction. This is not unlike the effect produced by local anesthetics, which also block sodium channels, but with two important differences: they do so from the inside of the cell and their effects are reversible.

Map of gartersnake resistance to tetrodotoxin
Outside of the range of the Rough-skinned Newt,
gartersnakes have essentially no resistance.
Figure from Brodie Jr. et al 2002

The elder Brodie showed in 1968 that many predators died if they were forced to eat newt, including bobcats, herons, kingfishers, moles, weasels, bass, catfish, and most snakes, including racers, rattlesnakes, gophersnakes, whipsnakes, rubber boas, and sharp-tailed snakes. Notably, Common Gartersnakes survived, although they were temporarily incapacitated. Brodie realized that he could measure snake toxin resistance by timing how long a snake was incapacitated for or how much its crawling speed slowed down when it was given a standardized dose of tetrodotoxin. Using this method for measuring resistance, the Brodies demonstrated that newt toxicity and gartersnake toxin resistance co-vary predictably across most of the Pacific Northwest; for example, on Vancouver Island, newts have very low levels of TTX and gartersnakes have almost no resistance to the toxin, whereas in central Oregon and in California's San Francisco Bay area, newts are tens of thousands of times more toxic and gartersnakes have correspondingly high resistance (for the most part, but read on!).

Three species of TTX-resistant snakes:
top: Amphiesma pryori
middle: Erythrolamprus epinephelus
bottom: Rhabdophis tigrinus

It's now known that a number of different snake species are resistant to tetrodotoxin and are capable of eating newts and other TTX-laden prey with impunity. These include two other species of gartersnake, the Santa Cruz gartersnake (Thamnophis atratus), which also eats Rough-skinned Newts, and the aquatic garter snake (Thamnophis couchii), which preys on California Newts (Taricha torosa). A Japanese newt, Cynops ensicauda, is eaten by Pryer's Keelback (Amphiesma pryeri). Some frogs also have tetrodotoxin, and two species, an Atelopus toad in Central American and a Polypedates treefrog in eastern Asia, are respectively eaten by the dipsadine Erythrolamprus [Liophis] epinephelus and the natricine Rhabdophis tigrinus. Not only has tetrodotoxin resistance also arisen in these other species of snakes around the world, but the mechanism, which involves changing the shape of the sodium channel pore so that the toxin binds less tightly, has evolved the exact same way in each lineage of snakes, via functionally identical mutations to the gene sequences. This is remarkable because these snakes are moderately but not very closely related to one another, and even more so because pufferfish also have many of the same mutations. These mutations are not found in humans, rats, most snakes, or other non-resistant vertebrates. All this suggests that there are a limited number of ways that evolution can change a sodium channel to make it more resistant to TTX and still maintain its function. In most cases, these and other natricine and dipsadine snakes are probably resistant to multiple prey toxins, as they are known to regularly consume other toxic amphibians and invertebrates.

Common Gartersnake (Thamnophis sirtalis)
from Oregon's Willamette Valley, where newt toxicity and
snake resistance are both at their peak

Although all newts and some other amphibians possess TTX, T. granulosa is many times more toxic than any other species, and its primary predator is many times more resistant than any other snake. Common Gartersnakes themselves actually retain sufficient quantities of newt-derived TTX in their liver for one to two months after eating newts to severely incapacitate or kill their predators, which was the general subject of my original article. Whether or not any of the other TTX-resistant species sequester the toxin remains unknown, although it seems likely. In a few places, Common Gartersnakes have evolved such high resistance to TTX that they have effectively "won" their arms race with their newts. Because snake TTX resistance apparently evolves in a stepwise fashion, with each new mutation to the snake sodium channel pore structure rapidly making it much tougher for TTX to bind tightly, gartersnakes are capable of making quicker leaps in the arms race than are newts, which presumably must evolve higher toxicity by increasing the amount of TTX they produce. Eventually, some gartersnakes seem to have reached a point where no amount of TTX could incapacitate them, so their newt populations (which were already pretty toxic) stopped being selected to produce more toxin. Since we don't really know how they get their toxin in the first place, they might be limited in their ability to produce or sequester it or its precursors.

There's much left to discover about this system, which is perhaps one of the most interesting in snake biology. Where are newts getting tetrodotoxin from? How many other times has TTX resistance evolved in snakes, and has it happened the same way every time [Update: the answer is no!]? To what extent are gartersnakes using newt-derived TTX to protect against their own predators? Someday, we will find out.

ACKNOWLEDGMENTS

Thanks to current and former members of the Brodie lab, especially Dr. Edmund D. "Doc" Brodie Jr., for discussing this system with me over the last three years.

REFERENCES

Brodie Jr, E. D. 1968. Investigations on the skin toxin of the adult rough-skinned newt, Taricha granulosa. Copeia 1968:307-313 <link>

Brodie III, E. and E. Brodie Jr. 1999. Costs of exploiting poisonous prey: evolutionary trade-offs in a predator-prey arms race. Evolution 53:626-631 <link>

Brodie III, E., C. Feldman, C. Hanifin, J. Motychak, D. Mulcahy, B. Williams, and E. Brodie Jr. 2005. Parallel arms races between garter snakes and newts involving tetrodotoxin as the phenotypic interface of coevolution. Journal of Chemical Ecology 31:343-356 <link>

Geffeney, S., E. Brodie Jr, P. Ruben, and E. Brodie III. 2002. Mechanisms of adaptation in a predator-prey arms race: TTX-resistant sodium channels. Science 297:1336-1339 <link>

Geffeney, S., E. Fujimoto, E. Brodie, and P. Ruben. 2005. Evolutionary diversification of TTX-resistant sodium channels in a predator–prey interaction. Nature 434:759-763 <link>

Hanifin, C. T. and E. D. Brodie Jr. 2008. Phenotypic mismatches reveal escape from arms-race coevolution. PLoS Biology 6:e60 <link>

Feldman, C. R., E. D. Brodie, and M. E. Pfrender. 2012. Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes. Proceedings of the National Academy of Sciences 106:13415-13420 <link>

Stokes, A. N., P. K. Ducey, L. Neuman-Lee, C. T. Hanifin, S. S. French, M. E. Pfrender, E. D. Brodie, III, and E. D. Brodie Jr. 2014. Confirmation and distribution of tetrodotoxin for the first time in terrestrial invertebrates: two terrestrial flatworm species (Bipalium adventitium and Bipalium kewense). PLoS ONE 9:e100718 <link>

Williams, B. L. and R. L. Caldwell. 2009. Intra-organismal distribution of tetrodotoxin in two species of blue-ringed octopuses (Hapalochlaena fasciata and H. lunulata). Toxicon 54:345-353 <link>

Williams, B. L., E. D. Brodie Jr., and E. D. Brodie III. 2004. A resistant predator and its toxic prey: persistence of newt toxin leads to poisonous (not venomous) snakes. Journal of Chemical Ecology 30:1901-1919 <link>

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

Basics of Snake Fangs

Click here to read this post in Spanish!
Haga clic aquí para leer este blog en español!

Solenoglyphous fangs of a Gaboon Viper

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

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

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

Solenoglyphous

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

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

Modified solenoglyphous fang of
African Burrowing Asp (Atractaspis engaddensis)

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

Proteroglyphous

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

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

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

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

Opisthoglyphous

Opisthoglyphous fang of Eastern Hog-nosed Snake

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

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

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

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

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

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

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

Aglyphous

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

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

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

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

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

ACKNOWLEDGMENTS

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

REFERENCES

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

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

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

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

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

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

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

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

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

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

Mittleman M, Goris R, 1974. Envenomation from the bite of the Japanese colubrid snake Rhabdophis tigrinus (Boie). Herpetologica 30:113-119 <link>

Pyron, R. A., F. T. Burbrink, G. R. Colli, A. N. M. de Oca, L. J. Vitt, C. A. Kuczynski & J. J. Wiens (2011). The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol. Phylogenet. Evol. 58, 329-342 <link>

Savitzky AH, 1980. The role of venom delivery strategies in snake evolution. Evolution 34:1194-1204 <link>

Shea G, Shine R, Covacevich JC, 1993. Elapidae. In: Glasby C, Ross G, Beesley P, editors. Fauna of Australia. Canberra: AGPS <link>

Vonk FJ, Admiraal JF, Jackson K, Reshef R, de Bakker MA, Vanderschoot K, van den Berge I, van Atten M, Burgerhout E, Beck A, 2008. Evolutionary origin and development of snake fangs. Nature 454:630-633 <link>

Weinstein SA, Warrell DA, White J, Keyler DE, 2011. "Venomous" Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of "Colubrid" Snake Bites. Amsterdam: Elsevier <link>

Weinstein SA, White J, Keyler DE, Warrell DA, 2013. Non-front-fanged colubroid snakes: A current evidence-based analysis of medical significance. Toxicon. 69, 103-113 <link>

Weinstein S, White J, Westerström A, Warrell DA, 2013. Anecdote vs. substantiated fact: the problem of unverified reports in the toxinological and herpetological literature describing non-front-fanged colubroid (“colubrid”) snakebites. Herpetological Review 44:23-29.

Wüster, W., L. Peppin, C. Pook & D. Walker (2008). A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes). Mol. Phylogenet. Evol. 49, 445-459 <link>

Young BA, Dunlap K, Koenig K, Singer M, 2004. The buccal buckle: the functional morphology of venom spitting in cobras. J Exp Biol 207:3483-3494 <link>

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