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Sunday, November 27, 2016

Galápagos Racers: answers to your questions about the BBC Planet Earth II iguana chase scene

This post will soon become available in Spanish

Galápagos Racers (Pseudalsophis occidentalis)
on Fernandina Island, from the BBC's Planet Earth II footage
If you haven't seen the incredible footage of the "iguana chase scene" from the BBC's Planet Earth II Islands episode, I encourage you to watch it right away. In addition to being a highly dramatic cinematographic masterpiece, it raises a number of interesting questions about the biology of the snakes in the clip. For a few days after it aired, the Internet was buzzing with these questions, and I've cataloged the answers to some of the most popular ones below. If you have one that isn't listed, feel free to ask it in the comments! And, if you want to know more about the process I used to dig up some of this information, check out my tutorial for teaching oneself about obscure snakes.

What kind of snakes are they?

Throughout the clip, Attenborough calls them "racer snakes"1, but herpetologists would normally call the snakes on the screen Galápagos Racers. Although these snakes are called "racers", they're not closely related to North American racers (genus Coluber); it's been about 45 million years since these two snakes last shared a common ancestor.

Galápagos Racers belong to the genus Pseudalsophis. Depending on which sources you consult, there are between 4 and 7 species of Pseudalsophis in the Galápagos, as well as one in mainland South America.

Pseudalsophis slevini eating a gecko on Pinzón Island
Just like Galápagos tortoises, finches, and many other organisms, there are different species of Galápagos Racers on the different Galápagos Islands (one of the concepts that sparked Darwin's theory of evolution by natural selection). The film was made on Fernandina, the youngest, westernmost, and most volcanically-active island in the Galápagos. Fernandina has two species of snakes, Pseudalsophis slevini and Pseudalsophis occidentalis. The snakes in the film must be Pseudalsophis occidentalis, because they are too large and not boldly banded enough to be P. slevini. You can read the original descriptions of both species here.

None of the sources reporting which species is shown in the film are authoritative, but without exception when the species is given it is given as Pseudalsophis biserialis. This is not correct under any modern taxonomy, although there is also a good explanation for why it is mistakenly being used—P. occidentalis was briefly a subspecies of P. biserialis, but has mostly been and is now treated either as a subspecies of P. dorsalis or as its own species. See below for much more (probably too much) detail.

Why are there so many of them?

Galápagos Racer (P. dorsalis) among adult Marine Iguanas
on Santa Cruz, which are much too large for it to eat
Most snakes are not social, and because they must swallow their food whole they cannot share prey. These snakes are not found at such high densities year-round, but rather aggregate around consistent Marine Iguana nesting sites in May when the eggs are hatching.

Just as when baby sea turtles emerge from their nests, predators congregate at the temporary buffet, returning afterwards to their usual densities. Around the world, there are numerous examples of avian and snake predators exploiting emerging hatchling iguanas. Researchers working at other iguana nesting sites in the Bahamas, the West Indies, and Venezuela have hypothesized that snakes and other predators also converge on the nesting sites of these other iguanas to exploit the temporary food source.

The rest of the year, Galápagos Racers eat lava lizards, geckos, insects, marine fishes, and hatchling birds, as well as introduced rats and mice.

Are they really hunting in a pack?

Almost certainly not. Again, most snakes are not social, and because they must swallow their food whole they cannot share prey. Pack-hunting behavior is unknown in snakes.

Two P. occidentalis trying to eat the same iguana
Jaw-walking is a fixed action pattern in snakes and they
may eat things that only vaguely resemble their food
once they start jaw-walking them.
From Planet Earth II Behind the Scenes
Some species have surprisingly social behaviors. It would be really interesting to examine social behavior in these snakes. To my knowledge no one has done so. Although they obviously cannot share a single food item, but if they are foraging in the same time and place on a limited resource, there might be an opportunity for the evolution of social cues. At least one paper suggested that this might be the case with a pit viper. Even though the BBC videographers saw snakes actively fighting over the same prey items and in some cases eating one another, it's possible that more closely-related snakes are less likely to fight over food or eat one another, or that males are less likely to compete with or try to eat females. These are testable hypotheses.
However, these are not well-studied snakes. I don't think they are helping each other, but there's a lot that we don't know about snakes.

Few scientists are currently studying these snakes. It's a testament to the BBC that they are consistently able to film natural phenomena that are still unknown to science. Hopefully this tape will stimulate some research on this exact question, and on the ecology of Galápagos Racers. When I wrote about Galápagos Racers in 2013, not much was known about their ecology, and that's still the case. It's amazing that so little research has been done on these snakes, particularly in contrast to Galápagos tortoises and marine iguanas (not to mention finches and other non-avian reptiles).

Why don't the female Marine Iguanas just lay their eggs somewhere else, closer to the ocean maybe?

Fates of rock iguana hatchlings, over half of which were
eaten by Cubophis and Epicrates snake predators in their
first month of life. From Knapp et al. 2010
Marine Iguanas have to dig nests and lay their eggs in soft sand, away from the rocky, tidal foraging grounds of the adults. They choose protected lava reefs for this purpose, which are in short supply on most islands. One estimate suggested that the cost of  migrating to their nesting sites represented half the reproductive effort of female Galápagos land iguanas.

Many species of reptiles nest in areas where they otherwise do not spend much time, especially aquatic species (reptile eggs need to "breathe" air and cannot be laid underwater). Female Marine Iguanas may all use the same nesting sites because those are the only sites available, or they may choose to nest near one another because, just like with sea turtles, synchronous hatching of the young increases their probability of survival.

In a study of Bahamian rock iguanas (Cyclura cychlura), snake predation was the most likely cause of mortality for newborn iguanas dispersing away from their nests. They estimated that about 20-30% of hatchling iguanas survived their first month, and those that moved quickly and linearly away from their nests were the most likely to survive, perhaps because predators had learned to hang around the nesting area. Another study of Galápagos land iguanas showed that predation attempts by Galápagos hawks were more than three times as likely to be successful when the body temperature of the iguana hatchlings was below 90°F. And, baby Galápagos marine iguanas that hung around their hatching area had about a 10% lower survival rate than those that moved to the coast, which the researchers attribute mostly to higher risk of predation at the nesting area.

Studies on the population biology of Marine Iguanas have shown that most of their mortality is caused by "predation, starvation (sometimes as a result of being trapped by a rock), crushing by a rock, being beaten against rocks by the sea, and suffocation in collapsed nest burrows. Animals may also die after being swept out to sea by offshore currents". So, actually, predation may be the best way for them to go. Besides Galápagos Racers, their other predators include Galápagos Hawks, Short-eared Owls, crabs, and Giant Hawk-fish.

Are they venomous/dangerous to humans?

No. Like many snakes, Galápagos Racers are rear-fanged. This means that, although technically they are venomous, they don't pose a danger to humans. Rear-fanged snakes have grooved teeth (rather than hollow fangs) on the back of their upper jaw (as opposed to the front); they can use these teeth to get venom into their prey once they are biting it, but they cannot strike out and deliver venom the way a viper can. A small minority of rear-fanged snakes have delivered medically-significant bites to humans, but almost all of these take place in a captive setting. You can read more about the different types of snake fangs here.

I didn't know there were snakes in the Galápagos. How did they get there?

Map showing the estimated age of each of the
Galápagos Islands. From Ali & Aitchison 2014
Galápagos Racers colonized the Galápagos Islands from mainland South America, just like all of the other Galápagos fauna and flora. The modern Galápagos Islands formed from volcanoes over the past 4 to 5 million years, although some of them have been building beneath the ocean surface for up to 15 million years. It is thought that there have been islands in the Galápagos for at least 8 million years, but the oldest islands have eroded and are now back beneath the ocean surface.

Because the Galápagos Islands are located only six hundred miles off the coast of Ecuador, it is easier for them to be colonized by plants and animals from the mainland than for a more remote island chain such as Hawaii (which is >2,500 miles away from the nearest snake-inhabited landmass).

Molecular dating of the divergence time between Galápagos Racers and their closest mainland relative, Pseudalsophis elegans, suggests that it has been about 15 million years since they last shared a common ancestor. This suggests that the mainland ancestor of Galápagos Racers probably went extinct sometime over the last 15 million years, and that the ancestors of Galápagos Racers probably colonized the Galápagos Islands before any of the current islands existed (as is also the case for the Marine Iguanas). Until genetic work is done, we won't know how many times snakes colonized the Galápagos archipelago or how many distinct lineages there are.

Could the film have been staged?

Obviously the scenes are spliced together, but in my opinion there's no chance the Galápagos National Park would allow something like this to be staged. They are among the strictest places in the world for researchers to conduct scientific work. However, more recent episodes of Planet Earth II have been criticized for incorporating fake sound effects.


One of the few phylogenies to include Galápagos Racers
Broadly, Pseudalsophis is nested within a large clade of Caribbean, Central, and South American xenodontine snakes including, among numerous others, the genus Alsophis, which once contained Galápagos Racers and after which their current genus is named. They have been in a variety of genera since their description, especially Dromicus, which is no longer in use, from 1876 to 1997.

In 1973, herpetologist Charles Myers wrote: "The classification of colubrid snakes in general, and of South American colubrids in particular, is in a notoriously unsatisfactory state." Unfortunately, we are not that much better off today when it comes to Galápagos Racers. It seems pretty clear that the nearest relative of P. biserialis, P. dorsalis, and P. occidentalis is Pseudalsophis elegans, the only species in the genus found on the mainland (in Ecuador, Peru, and extreme northern Chile). Beyond that, there isn't a lot of clarity about their next-closest relatives. They are possibly most closely related to obscure South American "groundsnakes" in the genus Psomophis, or to the even more obscure genus Saphenophis, which was described by Myers as "quite lacking in peculiar or unique features" and so named "in allusion to one incontrovertible fact about these snakes...from the Greek saphenes (evident truth, clear) + ophis (a serpent), meaning 'clearly a snake'". We don't really have a great hypothesis about how the different lineages of Galápagos Racers are related to one another, or even if they are all descended from a single common ancestor, because we only have DNA from one of them so far.

Hypothesized scenario for the evolution of Pseudalsophis snakes
So far, we have no DNA evidence that would support or refute this model
From Ali & Aitchison 2014
Two reviews based on morphology addressed this question in the late 1990s. The first (Thomas 1997) focused exclusively on Galápagos Racers and suggested that P. biserialis, P. dorsalis, and P. occidentalis are descended from a shared common ancestor with P. elegans, but that P. hoodensis is more closely related to the mainland species Philodryas chammissonis, and that P. slevini and P. steindachneri are most closely related to Caribbean species. The other study (Zaher 1999), which looked at hemipene morphology over a much larger group of snakes, disagreed, finding a shared derived character—an inflated papillate ridge, placed far medially, on the medial surface of the lobes—linking the Galápagos Racers together with the mainland species P. elegans. Statements that Galápagos Racers have “very similar hemipenes” notwithstanding, Zaher was criticized for not describing the specific characters uniting the Galápagos species to the exclusion of others.

Maglio (1970) noted that the tooth counts and arrangement and the and shape of the premaxilla bone was most similar among the three Galápagos species that he examined (P. biserialisP. dorsalis, and P. slevini), and different from the West Indian species that Taylor later suggested are P. slevini's closest relatives. More recently, a study led by Grazziotin claimed that they "unequivocally support...Zaher's (1999) hypothesis based on morphology that continental Pseudalsophis elegans is closely related to the Galápagos Island species of Xenodontinae (herein represented by Pseudalsophis dorsalis), rather than to West Indian Alsophis and Antillophis, and mainland Philodryas (Thomas, 1997)." However, they obviously didn't read Thomas's paper very carefully, because he also hypothesizes that P. dorsalis is closely related to P. elegans, and the Grazziotin paper didn't sequence any DNA from P. slevini, P. steindachneri, or P. hoodensis, and therefore didn't test any hypotheses about them.

As for whether or not the snakes in Planet Earth II should be called P. occidentalis or P. dorsalis occidentalis, that's really a lumper/splitter question. But, both the IUCN and the 2014 edition of Snakes of the World recognize P. occidentalis as a full species; it was originally described as such by Van Denburgh in 1912, sunk to a subspecies of P. dorsalis by Mertens in 1960, and re-elevated to a full species in a 1999 paper by Zaher that was not primarily concerned with taxonomy and appears to have subsequently been neglected. The Reptile Database is currently a holdout for the subspecies designation, which has not been disputed but which is also not explicitly supported by unambiguous data. Perhaps wisely, the official webpage of Galápagos National Park chooses not to use scientific names and refers to the Fernandina racers as the "western subspecies". The truth is that, until more research is done, we won't be able to settle on an accurate taxonomy for these snakes.



1 This sounds a bit redundant to a snake biologist, but it isn't incorrect. The one thing that I wish BBC programs would do is identify the species in them more precisely. I'm advocating for a "biologist mode" that can be activated which would show the location and identity of species in all clips, similar to the old MTV show Pop-up Video.


ACKNOWLEDGMENTS

Thanks to Andy Kraemer and Jim Moulton for the use of their photographs.

REFERENCES

Ali, J. R. and J. C. Aitchison. 2014. Exploring the combined role of eustasy and oceanic island thermal subsidence in shaping biodiversity on the Galápagos. Journal of Biogeography 41:1227-1241 <full-text>

Bisconti, M., W. Landini, G. Bianucci, G. Cantalamessa, G. Carnevale, L. Ragaini, and G. Valleri. 2001. Biogeographic relationships of the Galapagos terrestrial biota: parsimony analyses of endemicity based on reptiles, land birds and Scalesia land plants. Journal of Biogeography 28:495-510 <full-text>

Carpenter, C. C. 1966. The marine iguana of the Galapagos Islands, its behavior and ecology. Proceedings of the California Academy of Sciences (Series 4) 34:329-376 <full-text>

Christian, K. A. and C. R. Tracy. 1981. The effect of the thermal environment on the ability of hatchling Galapagos land iguanas to avoid predation during dispersal. Oecologia 49:218-223 <abstract>

Geist, D., H. Snell, H. Snell, C. Goddard, and M. Kurz. 2014. A paleogeographic model of the Galápagos Islands and biogeographical and evolutionary implications. The Galápagos: a natural laboratory for the Earth Sciences. American Geophysical Union, Washington DC, USA:145-166 <full-text>

Grazziotin, F. G., H. Zaher, R. W. Murphy, G. Scrocchi, M. A. Benavides, Y.-P. Zhang, and S. L. Bonattoh. 2012. Molecular phylogeny of the New World Dipsadidae (Serpentes: Colubroidea): a reappraisal. Cladistics 28:437-459 <full-text>

Grehan, J. 2001. Biogeography and evolution of the Galápagos: integration of the biological and geological evidence. Biological Journal of the Linnean Society 74:267-287 <full-text>

Günther, A. 1860. On a new snake from the Galápagos islands. The Annals and Magazine of Natural History 3:78-79 <full-text>

Hedges, S. B., A. Couloux, and N. Vidal. 2009. Molecular phylogeny, classification, and biogeography of West Indian racer snakes of the Tribe Alsophiini (Squamata, Dipsadidae, Xenodontinae). Zootaxa 2067:1-28 <full-text>

Knapp, C. R., S. Alvarez-Clare, and C. Perez-Heydrich. 2010. The influence of landscape heterogeneity and dispersal on survival of neonate insular iguanas. Copeia 2010:62-70 <full-text>

Laurie, W. and D. Brown. 1990. Population biology of marine iguanas (Amblyrhynchus cristatus). II. Changes in annual survival rates and the effects of size, sex, age and fecundity in a population crash. Journal of Animal Ecology 59:529-544 <full-text>

Maglio, V. J. 1970. West Indian xenodontine colubrid snakes: their probable origin, phylogeny, and zoogeography. Bulletin of the Museum of Comparative Zoology 141:1-54 <full-text>

Merlen, G. and R. A. Thomas. 2013. A Galapagos ectothermic terrestrial snake gambles a potential chilly bath for a protein-rich dish of fish. Herpetological Review 44:415-417 <full-text>

Mertens, R. 1960. Über die schlangen der Galápagos. Senckenbergiana Biologica 41:133-141 <not available online>

Myers, C. W. 1973. A new genus for Andean snakes related to Lygophis boursieri and a new species (Colubridae). American Museum Novitates 2522 <full-text>

Parent, C. E., A. Caccone, and K. Petren. 2008. Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B: Biological Sciences 363:3347-3361 <full-text>

Pyron, R. A., F. Burbrink, and J. J. Wiens. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13:93 <full-text>

Pyron, R. A., J. Guayasamin, N. Peñafiel, L. Bustamante, and A. Arteaga. 2015. Systematics of Nothopsini (Serpentes, Dipsadidae), with a new species of Synophis from the Pacific Andean slopes of southwestern Ecuador. ZooKeys 541:109-147 <full-text>

Radder, R. S. and R. Shine. 2007. Why do female lizards lay their eggs in communal nests? Journal of Animal Ecology 76:881-887 <full-text>

Rassmann, K. 1997. Evolutionary age of the Galápagos iguanas predates the age of the present Galápagos Islands. Molecular Phylogenetics and Evolution 7:158-172 <full-text>

Shine, R., L. X. Sun, M. Fitzgerald, and M. Kearney. 2002. Accidental altruism in insular pit-vipers (Gloydius shedaoensis, Viperidae). Evolutionary Ecology 16:541-548 <full-text>

Steindachner, F. 1876. Die schlangen und eidechsen der Galapagos-inseln. Zoologisch-botanischen Gesellschaft, Wien, Germany <Google book>

Swash, A. and R. Still. 2000. Birds, Mammals and Reptiles of the Galapagos Islands. Pica Press <Amazon>

Thomas, R. 1997. Galapagos terrestrial snakes: biogeography and systematics. Herpetological Natural History 5:19-40 <full-text>

Van Denburgh, J. 1912. Expedition of the California Academy of Sciences to the Galápagos Islands, 1905-1906. IV. The snakes of the Galapagos Islands. Proceedings of the California Academy of Sciences (Series 4) 1:323-374 <full-text>

Wallach, V. W., Kenneth J. and J. Boundy. 2014. Snakes of the World: A Catalogue of Living and Extinct Species. CRC Press, Boca Raton, Florida, USA <Google book>

Weinstein, S. A., D. A. Warrell, J. White, and D. E. Keyler. 2011. "Venomous" Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of "Colubrid" Snake Bites. Elsevier, Amsterdam <Google book>

Werner, D. I. 1983. Reproduction in the iguana Conolophus subcristatus on Fernandina Island, Galapagos: clutch size and migration costs. American Naturalist 121:757-775 <abstract>

Zaher, H. 1999. Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bulletin of the American Museum of Natural History 240:1-168 <full-text>

Zaher, H., F. G. Grazziotin, J. E. Cadle, R. W. Murphy, J. C. Moura-Leite, and S. L. Bonatto. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: A revised classification and descriptions of new taxa. Papeis Avulsos de Zoologia (Sao Paulo) 49:115-153 <full-text>

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.

Friday, October 28, 2016

Snakes with feet, anti-goo saliva, and more recent updates

This post will soon be available in Spanish


More of the latest snake news and research (for other recent updates, see posts from March, June, and August)—and, perhaps the most exciting news of all is that I have defended my dissertation and will be returning to writing more in-depth content in the next few months!

Rattlesnake Roundups (I and II)
A Texas conservation licence plate ironically depicting
a Western Diamond-backed Rattlesnake (Crotalus atrox).
Funds from these plates support a variety of valuable
conservation projects in Texas
 under the Texas
Wildlife Action Plan
, although none are specific to snakes.
Advocates for increasing state oversight of rattlesnake roundups in Texas received disappointing news this week when the Texas Parks and Wildlife Commission decided that they would not support a proposed ban on using gasoline fumes to collect rattlesnakes. Rather than reviewing and voting on the issue at their bi-annual meeting next month, the TPW Commission decided to remove it from their agenda entirely, citing "insufficient support from legislative oversight or the potentially regulated community". This decision marks the second time reviewing the ban has been put off, and unfortunately it is likely to be the last until the effort to reform roundups is re-initiated. The announcement included the statement that "TPWD [Texas Parts and Wildlife Department] staff still believe that there are better options for collecting snakes that do not adversely impact non-target species, and we will continue to work with the snake collecting community to develop and implement best practices that reduce potential impacts to these species", although in the absence of specific details it is hard to believe that this issue will remain at the fore of wildlife management in Texas without continued pressure from advocates of scientific rattlesnake management. However, Representative Susan King of Sweetwater's 2015 house bill 763 requires that petitions to state agencies (including TPWD) that are signed by <51% Texas residents are not valid, which means that the ability of non-Texans to influence policy on this issue is now greatly diminished.

If you're not familiar with the issues surrounding the gassing ban, I encourage you to read the 2016 Snake Harvest Working Group report, the same document that was available to the TPW Commission prior to their decision this week. Among other topics, it contains data on the adverse impacts of gassing on non-target endangered species, which is the primary impetus for the ban. It hints at human health impacts of consuming meat from gassed rattlesnakes. The SHWG report also summarizes previously unavailable data on roundup economics, showing that profits are not related to the number of rattlesnakes at an event and did not decline after gassing was banned in Alabama and Oklahoma. Stakeholder survey responses and the vast majority (>90%) of public comments from Texans were in favor of the gassing ban, as are many TWPD employees.

The TPW Commission is solely responsible for this decision. You can let the TPW Commission and Texas State Representative Susan King of Sweetwater (or your own state representative, if you live in Texas) know whether you think they are acting in the best interest of the majority of the public and in accordance with game management principles at the links provided (if you no longer have a fax machine, you can send a fax over the Internet here).

Goo-eating Snakes and the Eggs that Evade Them and Basics of Snake Fangs
Mandibular glands of Dipsas alternans
From Zaher et al. 2014
This discovery is from 2014, but it's newer than either of the past posts to which it's germane and I just found out about it. Perhaps you've seen the incredible rapid hatching behavior that treefrog eggs have evolved to escape from snake predators, including cat-eyed snakes (genus Leptodeira), blunt-headed tree snakes (genus Imantodes), and snail-sucking snakes (genera Sibon and Dipsas). These snakes also eat a variety of other gooey prey, such as earthworms, leeches, snails, slugs, adult frogs, caecilians, and, more rarely, non-gooey prey like lizards and reptile eggs. They have a number of adaptations that help them consume their sticky, viscous prey, including long, slender teeth, skull bones and muscles modified for extreme lower jaw extrusion, and a short-snouted, large-eyed look that resembles a snake embryo. Recently, a team of scientists from Brazil discovered a new one: a protein-secretion delivery system in the lower jaw.

Are the secretions venom? No. Dipsas and its relatives always extract snails using a sudden strike, followed by fast, alternating probing motions of the mandible inside the shell; this behavior could hardly depend on a chemical reaction of any kind. Instead, the gland secretions probably play a role in mucus control and prey transport rather than immobilization or killing of the prey. Although the glands in some species are associated with muscles, they are not connected to any teeth, but rather open onto the floor of the mouth, which in some species is covered with extensively loose, folded skin. Hypertrophied infralabial glands have been known from some dipsadine species since the 1960s, but the new paper describes the muscles and other soft tissues surrounding them and documents their variation among several dozen species of this very speciose group of snakes. On the other side of the world, pareatid snail-eating snakes have independently evolved a similar lifestyle, complete with upper jaw glands of perhaps similar function.

Why snakes are long and Why do snakes have two penises?

Pelvic girdles (dark blue) and hind limbs (red) of lizards,
living snakes, and extinct snakes with fully-developed limbs.
ZRS is the name of the SHH enhancer gene
that has been partially deleted in snakes.
From Leal & Cohn 2016
Many people are familiar with the tiny vestigial legs or "spurs" of boas, pythons, and other henophidian snakes. These structures are sexually dimorphic and are used by male boas and pythons in male-male combat and also to titillate females before and during matingNew data from the University of Florida describes how the spurs are formed: a weak flicker of activity by a gene called Sonic hedgehog (SHH) during the first few hours of embryonic development, in contrast to strong, sustained activity of this gene in lizard embryos throughout their development, forming legs. In snakes, unique genetic deletions from an enhancer of SHH explain its weak activity; transgenic mouse embryos with the same deletions showed similarly SHH weak activity, whereas mouse embryos grown with a lizard enhancer developed normally. Caenophidian snakes, such as vipers, gartersnakes, and cobras, had more extreme deletions and mutations, with the cobra barely retaining any of the SHH enhancer gene.

Amazingly, the researchers also found that HOXD13, the part of the limb-building gene that's responsible for building hands and feet, was unaltered in python embryos, and that python embryos develop not just a pelvic girdle and femur, which form the spur in adulthood, but cartilaginous templates of a tibia, fibula, and foot, which are reabsorbed prior to hatching. Although living snakes appear to follow a gradual pattern of limb shrinkage and loss, some extinct snakes that are thought to have been more similar to boas and pythons than they were to blindsnakes also had fully-developed, albeit small, limbs, complete with feet, as adults. This new discovery helps explain the apparent evolutionary "re-appearance" of these structures; they were never completely lost in the first place. As for the reason why not, snake HOXD genes and their regulators appear to be equally important to the development of their paired hemipenes, structures of obvious importance.

REFERENCES

Oliveira, L., A. L. Costa Prudente, and H. Zaher. 2014. Unusual labial glands in snakes of the genus Geophis Wagler, 1830 (Serpentes: Dipsadinae). Journal of Morphology 275:87-99 <link>

Leal, F. & Cohn, M.J. 2016. Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and HOXD enhancers. Current Biology DOI:10.1016/j.cub.2016.09.020 <link>

Leal, F. & Cohn, M.J. 2014. Development of hemipenes in the ball python snake Python regius. Sexual Development, 9, 6-20 <link>

Savitzky, A.H. 1983. Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. American Zoologist, 23, 397-409 <link>

Texas Parks and Wildlife Department. 2016. Snake Harvest Working Group Final Report <link> <references> <summary>

Zaher, H., de Oliveira, L., Grazziotin, F.G., Campagner, M., Jared, C., Antoniazzi, M.M. & Prudente, A.L. 2014. Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evolutionary Biology, 14, 1-28 <link>

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

Wednesday, September 28, 2016

Xenophidion: The Snake with the Mystery Penis

This post will soon be available in Spanish

Xenophidion schaeferi
From Das 2010, painted by Szabolcs Kókay
For a combination of phylogenetically distinct, taxonomically confusing, and poorly known, you simply cannot beat the spinejaw snakes, genus Xenophidion. Described in 1995, there are two species, each known from a single specimen1. That makes even dwarf pipesnakes (family Anomochilidae), of which we've obtained several new color photos recently, seem relatively well-represented. Putting together this article strained my research powers—xenophidiids don't even have an English language Wikipedia page (yet). Google the name of the family and it asks whether you meant Xenophilius, the first name of a minor character from Harry Potter, who has more than twice as many results. Xenophidion means "small strange snakes" in Greek, and indeed we have barely scratched the surface of how strange these snakes probably are. And, to top it all off, no one has ever seen its penis. Read on to find out why.

Collection locations of the only specimens of
Xenophidion acanthognathus (red)
and Xenophidion schaeferi (green)
The story of Xenophidion begins on the morning of November 20th, 1987. It was 8:15 AM when Chicago Field Museum Herpetologist Robert F. Inger found a snake beneath some moss on rock during field work in a selectively-logged forest near Mendolong, in Sabah's Sipitang District on the island of Borneo. Inger, an expert in the herpetology of southeast Asia who by that time in his life had "made thorough searches of thousands of square meters of forest floor litter with the help of very sharp-sighted local men", had never seen a snake like this before, and he brought it back to Chicago and placed it in the Field Museum collection.

Almost a year later, at 10:00 PM on November 5th, 1988, German amateur herpetologist Christian Schäfer collected and photographed a snake at the edge of a trail near Templer Park, about 12 miles north of Kuala Lumpur in peninsular Malaysia. Schäfer donated his specimen to the Zoological Museum in Berlin in the spring of 1993. Curators Rainer Günther and Ulrich Manthey recognized it as unique and asked esteemed herpetologists Van Wallach and Bob Inger to compare it to specimens at Harvard and Chicago. Inger recognized similarity between Schäfer's specimen and his own, and sent both specimens back to Berlin to be described as new species. The dissimilarity between the two new specimens and all other known snakes was so great that they chose to establish a new genus, which they tentatively placed into the family Colubridae (which at the time was much more inclusive). The genus was elevated into a new family after the dissection of the X. acanthognathus specimen by Wallach and Günther in 1998 failed to reveal an obvious affinity with any existing family.

Drawing and photograph of the jaw spine of X. schaeferi (labeled 'Pp')
From Günther & Manthey 1995
The two specimens share a number of unique features that distinguish them from all other living snakes. Their head scales, especially those along their lips, bear numerous sensory papillae. Their prefrontal scales are much larger than those of other snakes, taking up most of the top of the head in front of the eyes, and the space between their eyes is slightly concave. Their upper jaw bears a long, spiny palatine process, after which X. acanthognathus ("spine jaw" in Greek) is named. Their small eyes, short tail, and wedge-shaped head all suggest a mostly fossorial lifestyle. Like many "henophidian" snakes, their ventral scales are only slightly wider than their dorsal scales. But, unlike so many henophidians, both species of Xenophidion lack any vestiges of a pelvic girdle, left lung, or coronoid bone, suggesting that they are more closely related to caenophidian snakes. Wallach and Günther noted several similarities among the visceral characteristics of Xenophidion and tropidophiids, including a tracheal lung and unlobed kidneys., although we now know that tropidophiids are most closely related to aniliids. They also suggested that Xenophidion and another enigmatic snake family, bolyeriids, might be related.

The only photograph of a living Xenophidion schaeferi (FMNH 235170),
taken by W. Grossmann. From Günther & Manthey 1995


In 2004, the sequence of the cytochrome b gene of X. schaeferi was sequenced. This is still the only gene we have from either species of Xenophidion, and it has suggested a sister relationship between Xenophidion and Bolyeriidae and a distant relationship between Xenophidion and Tropidophiidae in several studies. Evidently, unpublished CT scans of the skull of Xenophidion show that these snakes also have a joint in the maxilla, a characteristic unique to bolyeriids. We know almost nothing about the diet of Xenophidion, but thankfully the stomach of the X. acanthognathus specimen contains a Sphenomorphus skink. Skinks are also eaten by bolyeriids, which use their hinged upper jaws to grasp their hard-bodied,  relatively non-deformable prey. It's not inconceivable that Xenophidion might do this as well. The current geographic distribution of Bolyeriidae is limited to Round Island in the Indian Ocean, which suggests that the common ancestor of these two families was probably ancient and widespread across Gondwanaland.

Ventral view of the sole specimen of
Xenophidion acanthognathus (ZMB 50534)
From Günther & Manthey 1995
There are numerous differences between the two species of Xenophidion. Both have 23 dorsal scale rows at midbody, but the dorsal scales of X. acanthognathus are more heavily keeled than those of X. schaeferi. They have a similar number of ventral scales (181 vs, 178), but X. acanthognathus has 51 subcaudals, 8 more than X. schaeferiXenophidion schaeferi also has more teeth on the palatine (10 vs. 8), pterygoid (16 vs. 13), and especially the dentary bone (19 vs. 12) than X. acanthognathus. Finally, X. acanthognathus has a large yellow-white patch on its neck. Because both of the specimens are females, the hemipenes, which contain many taxonomically useful characters, have not been described. But, conveniently, the oviduct of the X. acanthognathus specimen contains two eggs, so at least we know the reproductive mode of these snakes.

Snake family tree from Figueroa et al. 2016showing
Xenophidiidae + Bolyeriidae as sister to Caenophidia
Click for a larger version
Some phylogenetic studies suggest that Xenophidiidae and Bolyeriidae might be sister to Caenophidia, leading some to call these two families "proto-colubroids". However, other genetic analyses group them with boas, pythons, and other "henophidian" snakes instead. Hopefully further gene sequencing will sort this out, and of course fresh Xenophidion specimens wouldn't hurt. The forestry station where Inger collected X. acanthognathus is still operational and researchers continue to work there—I hope they know to keep their eyes open for small, strange snakes. Unfortunately, the primary forest where X. schaeferi was collected was cleared two years later and is now a banana plantation. Both peninsular Malaysia and Borneo are losing their forests to timber harvesting and oil palm plantations at an alarming rate. People get upset when they learn that deforestation endangers charismatic species such as orangutans, leading to efforts to make palm oil production more sustainable. This is really challenging because palm oil is used in all kinds of delicious things, such as Girl Scout Cookies, and high-profile controversy over its sustainability has been fueled by people's love for orangutans. I'm here to suggest that the many mysteries of Xenophidion—including what its penis looks like—may never be solved if the rain forests of southeast Asia are lost, and that Xenophidion is at least as valuable and interesting as orangutans.



1 The IUCN page for Xenophidion acanthognathus mentions a second specimen from Kinabalu, but I couldn't find any other references to this specimen. Instead, the IUCN references page pointed me, through a couple of intermediates, to a paper (published before the discovery of Xenophidion) that included a reference to the type specimen of Stoliczkia borneensis, which was collected on Mount Kinabalu. Since Stoliczkia borneensis is in the family Xenodermidae, I suspect there may have been some confusion around the somewhat similar family names. VertNet lists only the single Sipitang specimen of X. acanthognathus, as does Wallach et al.'s 2014 edition of Snakes of the World
. Both species of Xenophidion are listed as Data Deficient by the IUCN.


ACKNOWLEDGMENTS

Thanks to Szabolcs Kókay, who painted the only color image of Xenophidion for A Field Guide to the Reptiles of South-east Asia.

REFERENCES

Chan-ard, T., Grossmann, W., Gumprecht, A. & Schulz, K.D. 1999. Amphibians and reptiles of Peninsular Malaysia and Thailand: an illustrated checklist. Bushmaster Publishing, Wuerselen, 240 pp. <link>

Das, I. 2010. A field guide to the reptiles of South-East Asia. New Holland Publishers, London, 376 pp. <link>

Das, I. 2012. A naturalist’s guide to the snakes of South-East Asia. John Beaufoy Publishing, Oxford, 176 pp. <excerpt/link>

Figueroa, A., A. D. McKelvy, L. L. Grismer, C. D. Bell, and S. P. Lailvaux. 2016. A species-level phylogeny of extant snakes with description of a new colubrid subfamily and genus. PLoS ONE 11:e0161070 <link>

Günther, R. & U. Manthey. 1995. Xenophidion, a new genus with two new species of snakes from Malaysia (Serpentes, Colubridae). Amphibia-Reptilia 16:229-240 <link>

Lawson, R., J. B. Slowinski & F. T. Burbrink. 2004. A molecular approach to discerning the phylogenetic placement of the enigmatic snake Xenophidion schaeferi among the Alethinophidia. Journal of Zoology 263:285-294 <link>

Pyron, R. A., F. Burbrink, and J. J. Wiens. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13:93 <link>

Wallach, V. & R. Günther. 1998. Visceral anatomy of the Malaysian snake genus Xenophidion, including a cladistic analysis and allocation to a new family (Serpentes: Xenophidiidae). Amphibia-Reptilia 19:385-405 <link>

Wallach, V. W., Kenneth J. and J. Boundy. 2014. Snakes of the World: A Catalogue of Living and Extinct Species. CRC Press, Boca Raton, Florida, USA <link/sample>

Creative Commons License

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

Wednesday, August 17, 2016

Why snakes are long (and other recent updates)

This post will soon be available in Spanish 

A Western Hog-nosed Snake (Heterodon nasicus)
depredating a turtle nest in Nebraska
As I did in March and June, I wanted to highlight some recent and exciting updates to some of my earlier articles. There is so much recent snake news this month, which is lucky for me because I've been writing my dissertation, which I'll be defending next month, so I haven't had much time to write. anything else! I hope to return to longer-form content in October.

Also, although I rarely promote my own research on this blog, I'm very excited to have just published the second chapter of my masters thesis, documenting the diet of Western Hog-nosed Snakes (Heterodon nasicus) in Illinois using stable isotopes to quadruple our sample size. We showed that the diet of juveniles was composed mostly of Six-lined Racerunners (Aspidoscelis sexlineata) and their eggs, whereas adults mostly feed on aquatic turtle eggs! Surprisingly, we found very little evidence that these snakes were eating amphibians, which are considered to be staples of their diet elsewhere.

Snake Genomes, Lizards of Glass, and Why Snakes are Long

Variation in the length of different vertebrate bodies,
including a Rosy Boa (Lichanura)
From Head & Polly 2015
Researchers from the Gulbenkian Institute of Science in Portugal used data from the king cobra and Burmese python genomes as part of new research that's too meta for me not to write about. The developmental biology of snakes deserves a whole article (and, indeed, is the subject of an entire book chapter), but snake development is uniquely interesting from the perspective of understanding the evolution of both limblessness and body elongation. A very recent article in the journal Developmental Cell shed light on the genetic regulation of body length in vertebrates, which varies from a dozen or fewer in humans and most vertebrates to over 200 in many snakes and caecilians and exceeds 400 in some snake species.

For a long time, scientists thought that Hox genes, which control many aspects of body layout and development, probably controlled body length too. But, so far experiments modifying Hox genes have failed to produce differences in body length, and most snake Hox genes are not substantially different from those of other vertebrates. Instead, the new study showed that the "junk DNA" surrounding a different gene, called Oct4, apparently influences body length in developing vertebrate embryos. Although the Oct4 gene itself was already known to play a role in regulating stem cell flexibility, the surrounding DNA was formerly considered to be "junk DNA" because it was not translated into RNA and seemed to have no purpose. Measurements showed that Oct4 is active for longer in developing snake embryos than in mouse embryos, which is probably what causes their bodies to grow so long. And, just by copying snake "junk DNA" into mouse embryos, the researchers were able to artificially increase both the level of expression of Oct4 in mouse embryos as well as the length of their bodies. Comparing the genomes of snakes, lizards, and mammals showed that the Oct4 "junk DNA" of snakes differed from that of lizards and mammals. Interestingly, glass lizard (Ophisaurus) Oct4 "junk DNA" was similar to that of geckos and anoles, even though these limbless lizards share an elongated snake-like body form with snakes.

Conservation Successes with Indigo Snakes

Seasonal variation in the probability of moving of female (top)
& male (bottom) Eastern Indigo Snakes (Drymarchon couperi)
in Florida. From Bauder et al. 2016
Many snakes make seasonal movements to and from hibernacula, in search of food or mates, or for other reasons. Often, we think of these movements as driven by the changing of seasons, either the wet and dry seasons in the tropics or the four well-defined temperate seasons. But, we don't know much about the seasonal movements of snakes that live in tropical and sub-tropical zones. For a species with such a small range, Eastern Indigo Snakes have fairly different requirements in the northern part of their range, where frosty Georgia winter nights force them to rely on deep, warm Gopher Tortoise (Gopherus polyphemus) burrows, and in sub-tropical peninsular Florida, where they are less reliant on such particular shelters. A recent study by a group of Florida scientists, including Orianne Society staff, used radio-telemetry to document a seasonal pattern of movement in Florida Indigo Snakes that differs from their pattern in Georgia. In particular, male Florida Indigos are most likely to move in the late fall and early winter, when they are searching for mates, whereas both males and females stay put during the spring, for reasons yet unknown. In contrast, Indigos in the rest of their range maintain small winter home ranges on xeric sandhills but use much larger home ranges and a greater diversity of habitats during the rest of the year.

Malagasy Leaf-nosed Snakes

A female Langaha pseudoalluaudi
Photo from iNaturalist
Global all-taxa citizen science portal iNaturalist's observation of the week this week was a very rare snake indeed, a photograph of Langaha pseudoalluaudi. Less than two dozen other individuals of this species have ever been found by scientists. The first was collected in 1966 and described in 1988, and the second individual was photographed in 2003 by a Durrell Wildlife Conservation Trust biologist. Since that time, a handful of other records have trickled in from the field in Madagascar, including a few photos on Flickr and the only known photo of a male, published in a field guide in 2007. This individual was found by group of Operation Wallacea volunteers on a conservation research expedition, one of whom, Victoria Jackson, a student of Biological Sciences at the University of Exeter, posted it on iNaturalist. Of the three species of Langaha, none of which are particularly well-known, L. pseudoalluaudi is by far the rarest and most poorly-known. Perhaps the most fascinating aspect of Langaha biology is their obvious anatomical sexual dimorphism, a feature that is very rare among snakes. Females of all three Langaha species have a serrated snout that resembles a small flower that has not fully bloomed. Female L. pseudoalluaudi also have protruding horn-like scales above their eyes. Males have smooth, pointed snouts instead that resemble the seed pods of a Madagascan legume. We have very little idea why these snakes might be sexually dimorphic—the nose ornaments could be shaped by sexual selection, or they might function to make the snakes more cryptic to predators or prey, if the sexes forage or hide in different environments or on different foods.

Do Snakes Sleep?

Sleep in Bearded Dragons
From Shine-Idelson et al. 2016
There has only ever been one study of sleep in snakes. It was conducted in France in 1969 on an African Rock Python (Python sebae), which produced sleep-like brain waves almost 16 hours a day, increasing to over 20 hours following feeding. The data suggest that these brainwaves corresponded with slower breathing and heart rate, some muscle relaxation, and perhaps a lowered behavioral response threshold. There was no evidence for REM sleep in this snake. Evidence for REM sleep in other reptiles is mixed. The April 29th issue of Science contained new data from the Max Planck Institute for Brain Research documenting slow-wave and rapid eye movement (REM) sleep in Bearded Dragons (Pogona vitticeps). This is pretty cool because Bearded Dragons and snakes might be pretty close relatives (if phylogenetic trees using molecular data are to be believed) and it suggests that not only do reptiles definitely sleep, they may also dream. Previously, scientists had hypothesized that slow-wave and REM sleep evolved independently in birds and mammals and, like parental care, could be linked to endothermy. The unequivocal evidence for these sleep phases in reptiles suggest that REM sleep evolved much earlier and probably only once. The senior author on the study, neuroscientist Gilles Laurent was quoted as saying "If you forced me to speculate and to use a loose definition of dreaming, I'd speculate that [Bearded Dragon] dreams are about recent notable events: insects, maybe a place where there are good insects, an aggressive male in the next terrarium, et cetera. If I were an Australian dragon living in Frankfurt, I'd be dreaming of a warm day in the sun."

The 9,999th Reptile

Geophis lorcana
From Canseco-Márquez et al. 2016
Snake species number over 3,600 this month, in part because of the description of a new species of Geophis from Mexico. The beautiful Geophis lorcana is the 50th species in the genus Geophis and the 8th new species in that genus since the turn of the century. It was discovered in the cloud forests of the Sierra Zongolica and Sierra de Quimixtlán mountains by biologist Miguel Ángel de la Torre Loranca, in whose honor the new species is named. Like other Geophis, this snake is fossorial and secretive, and has a small geographic range. Further exploration of this region combined with molecular and anatomical data is likely to yield additional new species, although the habitats in which they are likely to be found are vulnerable to a variety of threats. Other new snake species from the past year include 10 new blindsnakes in the genus Epictia from Central and South America, a new boa from the Bahamas that sheds light on the island biogeography of the Caribbean, and a new species of Neotropical watersnake (genus Helicops) whose specific epithet is taken from one of Tolkien's Elvish languages.

Identifying Snake Sheds

Antaresia stimsoni inside its shed skin
Video still from Alice Springs Reptile Centre
It's not peer-reviewed research, but a recent video from the Alice Springs Reptile Centre in Alice Springs, Australia showed an unusual occurrence—a shedding Stimson's Python (Antaresia stimsoni) that seemed to have gotten stuck inside of an endless loop of its own shed skin. The snake must have crawled into the mouth orifice of the shed skin before it finished shedding the skin from the posterior part of its body. According to a Facebook post, the Alice Springs Reptile Centre staff reported that they had not observed this phenomenon before and that the python was able to free itself after about three hours of crawling in a circle by making a small, tidy exit hole in the shed. The video was featured on the popular IFLS science fan site.

ACKNOWLEDGMENTS

Thanks to John Iverson for the use of his photo.

REFERENCES

Female Langaha pseudoalluaudi
From its original description
in Domergue 1988
Aires, R., Jurberg, Arnon D., Leal, F., Nóvoa, A., Cohn, Martin J. & Mallo, M. (2016) Oct4 is a key regulator of vertebrate trunk length diversity. Developmental Cell, 38, 262-274 <link>

Bauder, J.M., Breininger, D.R., Bolt, M.R., Legare, M.L., Jenkins, C.L., Rothermel, B.B. & McGarigal, K. (2016) Seasonal variation in Eastern Indigo Snake (Drymarchon couperi) movement patterns and space use in peninsular Florida at multiple temporal scales. Herpetologica, 72, 214-226 <link>

Canseco-Márquez, L., C. J. Pavón-Vázquez, M. A. Lòpez-Luna, and A. Nieto-Montes de Oca. 2016. A new species of earth snake (Dipsadidae, Geophis) from Mexico. ZooKeys 610:131-145 <link>

Costa, H. C., D. J. Santana, F. Leal, R. Koroiva, and P. C. A. Garcia. 2016. A New Species of Helicops (Serpentes: Dipsadidae: Hydropsini) from Southeastern Brazil. Herpetologica 72:157-166 <link>

Domergue, C. A. 1988. Notes sur les serpents de la région malgache. VIII: Colubridae nouveaux. Bulletin du Muséum national d'histoire naturelle. Section A, Zoologie, biologie et écologie animales 10:135-146 <link>

Durso, A. M. and S. J. Mullin. 2016. Ontogenetic shifts in the diets of Plains Hog-nosed Snakes (Colubridae: Heterodon) revealed by stable isotope analysis. Zoology DOI:10.1016/j.zool.2016.07.004 <link>

Head, J. J. and P. D. Polly. 2015. Evolution of the snake body form reveals homoplasy in amniote Hox gene function. Nature 520:86-89 <link>

Held Jr., L. I. 2014. The snake. Pages 75-94 in L. I. Held Jr., editor. How the Snake Lost its Legs. Cambridge University Press, Cambridge <link>

Kuchling, G. (2003) New record, range extension, and colouration in life of Langaha pseudoalluaudi (Reptilia: Colubridae) in north-western Madagascar. Salamandra, 39, 235-240 <link>

Reynolds, R. G., A. R. Puente-Rolón, A. J. Geneva, K. J. Aviles-Rodriguez, and N. C. Herrmann. 2016. Discovery of a Remarkable New Boa from the Conception Island Bank, Bahamas. Breviora 549:1-19 <link>

Shein-Idelson, M., Ondracek, J.M., Liaw, H.-P., Reiter, S. & Laurent, G. (2016) Slow waves, sharp waves, ripples, and REM in sleeping dragons. Science, 352, 590-595 <link>

Wallach, V. 2016. Morphological review and taxonomic status of the Epictia phenops species group of Mesoamerica, with description of six new species and discussion of South American Epictia albifrons, E. goudotii, and E. tenella (Serpentes: Leptotyphlopidae: Epictinae). Mesoamerican Herpetology 3:216-374 <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.