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Are there any countries without snakes?

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Global distribution of all snake species combined
Public domain from Wikipedia
Terrestrial data from Ernst & Ernst (2011) and Cogger et al. (1998)
Sea snake data based on Campbell & Lamar (2004), Phillips (2002),
Ernst & Ernst (2011), and Spawls & Branch (1995)
Snakes are found in almost every country in the world, but there are a few places without wild1 snakes. Snake-free land generally falls into two categories: remote islands, mostly formed by volcanism or as atolls, that have never been part of a continental land mass and/or have been isolated from continents for a long time, and continental areas that are or were covered by ice within the last 26,000 years and haven't been recolonized since (for example, there are snake fossils from northern Canada, where no snakes live now, from a time when it was much warmer). There are also snake-free parts of the oceans, and probably there are some urban areas that are so disturbed that no snakes live there any more (e.g., downtown Manhattan), although they once did.

Iceland

Iceland is a volcanic archipelago just outside the Arctic Circle. Despite its high latitude, Iceland is warmed by the Gulf Stream and has a temperate climate, so snakes might actually do fairly well there, especially if they could take advantage of its plentiful geothermal features, as the high-altitude hot-spring snakes of Tibet (genus Thermophis) have done. However, Iceland has never been connected to any continent—instead, it was formed about 20 million years ago by a series of volcanic eruptions in the Mid-Atlantic Ridge, which separates the Eurasian and North American plates. It's been at about its current latitude the entire time, and, as far as anyone knows, has never been colonized by snakes. Today, the closest snakes are adders (Vipera berus) in both Scotland (470 mi away) and Norway (600 mi away), both of which are separated by a great deal of very cold ocean.

Ireland

Unlike Iceland, Ireland was once connected to other land masses. Parts of it are at least 1.7 billion years old. At the end of the Precambrian, two pieces of rock that would become Ireland could be found beneath the sea, one piece connected to the continent of Laurentia and the other piece to the smaller continent of Avalonia, both around 80° South. Over the next 50 million years, these two parts drifted northward, eventually uniting and breaking sea level near the equator about 440 million years ago, in the Silurian Period. Throughout the late Paleozoic Era, Ireland sank back under the sea and gained 65% of its modern mass as limestone deposits from huge coral reefs. At the beginning of the Mesozoic, Ireland was at the latitude of present-day Egypt and had a desert climate, and by the time snakes evolved (150 million years ago, in the late Jurassic-early Cretaceous) Ireland had separated from any other land mass, and has been connected on and off to this day. There is some debate over how recently a land bridge connected Ireland with Great Britain and, by extension, mainland Europe, with the consensus resting on the idea that Ireland was isolated by ocean by 16,000 years ago, at which time the climate was still quite cold and there was a lot more ice in Ireland than there is now. Although it's not insane to think that snakes might have colonized Ireland from Europe sometime during the 90 million years that preceded the Pleistocene Ice Ages, as they have since re-colonized Great Britain, so far no one has found any snake fossils in Ireland. But, viviparous lizards, natterjack toads, and common frogs have managed to make it to Ireland, and the slowworm has been introduced there, so it could happen one day. Likely successful colonists include adders (Vipera berus), grass snakes (Natrix natrix), or smooth snakes (Coronella austriaca) from Great Britain, France, or Scandinavia. The Irish climate is highly moderated by the gulf stream, with much milder winters than expected for such a northerly area, so snakes could do quite well there.

Cape Verde

Cape Verde is an island country consisting of 10 volcanic islands in the central Atlantic Ocean, 350 miles off the coast of the western African countries of Mauritania and Senegal. The Cape Verde Islands were all formed by the same volcanic hot spot, the oldest 26 million years ago and the youngest just 100,000 years ago. They have never been colonized by snakes from mainland Africa. There is a single reference to the Striped Sand Snake (Psammophis sibilans) on the island of Sal in a 1951 paper that, according to the authors, was an accidental introduction from Guinea-Bissau. Neither this snake nor any other has ever been recorded again from Cape Verde, although the archipelago is home to 31 endemic lizard species, more than any other island chain in the Macaronesian region.

New Zealand

New Zealand was part of Gondwana (aka Gondwanaland), the more southerly of the two supercontinents formed by the breakup of Pangaea 200-180 million years ago. Gondwana comprised the present-day continents of South America, Africa, Australia, India, and Antarctica as well as New Zealand. Today, New Zealand is the highest part of a mostly-submerged continent called Zealandia that broke away from Gondwana between 100 and 80 million years ago. Since that time, New Zealand has developed a unique flora and fauna that does not include any terrestrial snakes, which makes sense since it has been isolated since around the dawn of their evolution (and has been mostly submerged several times since). However, a steady trickle of reports of sea snakes, borne by oceanic currents beyond their normal range to New Zealand waters and beaches, was summarized in 1997, at which time an amazing 69 records of 2 species were known, dating back to 1837 (more records and a third species have been added since). About 90% are of pelagic sea snakes (Hydrophis platurus; formerly Pelamis platurus, also known as yellow-bellied sea snakes), a very widespread species that is infamous for vagrancy and recently made headlines when one washed ashore in Ventura County, California. The remaining 10% of records are of banded sea snakes (Laticauda colubrina), a species that normally sticks more closely to shores, and judging by their morphology most of these have likely come to New Zealand from Fiji or Tonga. In 1995, one specimen in the British Museum collected in New Zealand in 1925 and formerly classified as L. colubrina was re-identified as a new species from New Caledonia, L. saintgironsi, by herpetologists revising the widespread Laticauda colubrina complex.

Map of pelagic sea snake records from New Zealand
(1837-1997)
From Gill 1997
High sea surface temperatures in 1969-1975 and again in 1988-1990 coincided with major influxes of tropical and subtropical fishes, sea turtles, and sea snakes (up to 16 a year) carried to New Zealand waters by the East Australian Current. Most records are of single animals, but in March 1985 four H. platurus were found on Tokerau Beach in Northland. About three-quarters of sea snake records are from Austral autumn (March-May), and many are from the north coast of the north island, but H. platurus has been found all around the North Island, including in the Cook Strait, and once even on the north coast of the South Island (at Pakawau, Golden Bay, in March 1974)! All L. colubrina records are from the north-east coast of the North Island, except for one at Castlepoint, Wairarapa, in August 1977. All records are of adult snakes, and most (79%) were alive when found, usually washed ashore, but occasionally swimming freely. One even swam up a stream near the sea! Even more amazingly, several sea snakes have been found alive inland from the coast, including a May 1938 record of H. platurus "some distance" from the sea at Table Cape on the Mahia Peninsula, a January 1990 record of L. colubrina "well above" the high-tide line at Whangaruru Harbour, an April 1938 record of H. platurus 200 feet from the sea on a lawn at New Plymouth, and, most incredible, a September 1945 record of L. colubrina alive at Te Aroha, near Hamilton, which is over 12 miles from an estuary over a range of hills or over 27 miles from the ocean along the Waihou River. Unlike H. platurus, which is almost incapable of moving on land, L. colubrina is reasonably good at terrestrial locomotion, which could explain the inland presence of these snakes. Alternatively, the author of the review paper suggested that the snakes could have been carried inland by birds.2

New Zealand also owns the Chatham Islands 560 miles to the east, the Kermadec Islands 620 miles to the north, and Tokelau 2000 miles to the northeast3, but no sea snakes have been reported from these islands, probably because so few people live there. Like vagrant birds, even the records from mainland New Zealand surely represent just a small percentage of the total number of marine reptiles that have reached New Zealand over the years. However, New Zealand is still widely considered to have no native snakes, since H. platurus  stop feeding at sea temperatures below 18°C and die at temperatures between 14.5 and 17°C (the average sea temperature in the coldest month in northern New Zealand is 16°C).

Kiribati

Kiribati is a Pacific Island nation that straddles the region of the central Pacific Ocean where the Equator and the International Date Line cross, making it the only country that is in all four hemispheres. It consists of four island groups totaling 32 atolls and one coral island. Of these, approximately the eastern half (the Phoenix and Line Islands) are apparently devoid of snakes; at least, they are listed as having no snakes in the most up-to-date and authoritative guide to the reptiles of the Pacific Islands. This guide takes a conservative approach in listing only species that are confirmed by a museum specimen or literature record, so it's possible that at least pelagic sea snakes are found in the waters of eastern Kiribati. What is certain is that the western half of Kiribati (Banaba and the Gilbert Islands) is home to breeding populations of banded sea snakes (Laticauda colubrina), and possibly pelagic sea snakes as well. Additionally, there is a single record of an ornate reef seasnake (Hydrophis ornatus), a species that is normally found much farther west, from the Gilbert Islands. This might represent a vagrant, but more likely it is a misidentified or mislabeled specimen. So, Kiribati has no terrestrial snakes, unless you count banded sea snakes, which mate, lay eggs, and sometimes digest food on land, but hunt, catch prey, and spend much of their time in the ocean.

Tuvalu

Tuvalu is a Pacific Island nation south of Kiribati comprising three reef islands and six atolls and totaling 10 square miles, making it the fourth smallest country in the world. Like Kiribati, Tuvalu has no terrestrial snakes unless you count L. colubrina, but unlike Kiribati it has literature records of pelagic sea snakes off its shores. Happily, Tuvalu has decided to honor this species by putting it on one of its coins! It's a commemorative coin rather than a coin that's actually part of normal circulation, but still, it's pretty cool to have a snake on your money. Tuvalu is also home to at least 9 species of lizards and the introduced cane toad, so it's possible that snakes could show up there one day. In fact, it's even possible that a native, endemic blindsnake could have escaped detection on Tuvalu (or any other Pacific island) to this day. The only reason the Federated States of Micronesia aren't on this list is because of two unexpected species of endemic blindsnakes, Ramphotyphlops adocetus and R. hatmaliyeb, described in 2012 from two small islands, one in the eastern part of FSM and the other in the western part.

Nauru

Nauru is a relatively isolated Pacific Island nation and is one of the only countries smaller than Tuvalu (at 8.1 square miles, only Monaco and Vatican City, both in Europe, are smaller). Unlike many Pacific Island nations, Nauru is a single island. Nauru has no native terrestrial snakes, but it does have H. platurus off its shores, and it also has what is likely an introduced species, the ubiquitous Indotyphlops braminus or Brahminy Blindsnake, the only unisexual species of snake. It's actually amazing to me that we're on the seventh entry and haven't encountered this species yet, considering how widespread it is globally. The original native range of I. braminus is unknown, but it probably evolved in continental Asia. Because a single individual constitutes a reproductively-competent population, it has since spread all over the world, and it's unclear how long it has been established on Nauru or elsewhere in the Pacific. Many similarly-widespread species in the Pacific owe their distribution to human-assisted transport, the precise timeline of which is difficult to determine. Given the harm done to Nauru's environment by phosphate mining during the 20th century, it's unlikely that any native terrestrial snake would have survived.

Marshall Islands

The Marshall Islands (see above map) have close political ties with the USA, but they are self-governing. They are located north of Kiribati, west of the FSM, and south of Wake Island. The authoritative guide to the reptiles of the Pacific Islands lists only I. braminus from the Marshall Islands, but other sources suggest that at least a few brown treesnakes (Boiga irregularis), infamously introduced to Guam, have been found there as well, and it's possible that H. platurus and possibly other sea snakes are found off its shores. Both the Gilbert Islands in Kiribati to the south and Pohnpei and Kosrae in FSM to the west have L. colubrina, although an official page states that the Marshall Islands have no sea snakes. So, as far as we know the Marshall Islands have no snakes that are native and terrestrial (unless you count I. braminus as native, considering that we don't know how long it's been there).

Vatican City

The Vatican is a walled enclave within the city of Rome, Italy, with an area of 110 acres and a population of 842, making it the smallest internationally-recognized independent state in the world, both by area and population. I couldn't find any references confirming or denying the presence of wild snakes in the Vatican, but other wildlife seem to be pretty minimal, which makes sense considering that Rome has been a large city for thousands of years. But, snakes and other wildlife can hang on in some amazingly urbanized places, so I wouldn't completely rule out the presence of a few of the eight species of snakes that can surely be found in the surrounding Italian countryside. Monaco, another European microstate with a very dense population and a high degree of urbanization, is another possibility for a snake-less nation, although, given Monaco's reputation as a playground for the rich and famous (30% percent of its population are millionaires), there are certainly some who meet an alternate definition of the word "snake" within its walls.

Cover of a joke book that's blank inside
So there you have it: a maximum of ten countries out of 196 "without snakes", depending on where you want to draw the line. If we start expanding into territories or disjunct sections of larger countries, the list grows considerably, including places like Greenland, the Falkland Islands, Bermuda, Hawaii4, Wake Island, Johnston Atoll, Howland & Baker Islands, the Marquesas Islands, the Pitcairn Islands, Sala y Gomez, Isla Malpelo, St. Helena, the Faroe Islands, the Isle of Man, many Arctic and Antarctic islands, and Antarctica itself, which is owned by no country. And of course, as you can see from the map at the top, there are also large mainland areas of northern Europe, Asia, and North America, as well as the southern tip of Patagonia, that are too cold for snakes (although Vipera berus gets above the Arctic Circle in Scandinavia), not to mention the Atlantic, Arctic, and Antarctic Oceans5.

In the course of the research I did for this post, I found many travel articles promoting the snakelessness of some of these places as overwhelmingly positive, as I'm sure it is for many ophidiophobic travelers. But, the risk that snakes pose is way, way smaller than the fear we have of them, and in my mind the real danger is that many people see eradication of snakes as a positive thing, despite the fact that many of them are in real danger of extinction. Mauritius barely made it off this list, with one of two native species extinct and the other hanging on thanks only to captive breeding and reintroduction efforts. St. Kitts & Nevis could lose its only native snake, the Saba or orange-bellied Racer (Alsophis rufiventris), and native snakes have gone extinct or become critically endangered on many other islands throughout the Pacific and Caribbean due to centuries of forest clearance, overgrazing, development, and the introduction of invasive species, not to mention the many continental snake species threatened by sprawling development and habitat fragmentation. So, please, let's keep this list from growing.



1 Given the growing popularity of herpetoculture, I'd be willing to bet that there are captive snakes in every country, although a few countries have stringent laws banning any captive snakes, including as pets as well as in zoos and research facilities.



2 Studies have shown that, although many Pacific birds avoid pelagic sea snakes, naive Atlantic birds will try eat them (only to throw them up, since they are apparently poisonous as well as venomous). New Zealand's birds might be sufficiently naive to try to eat one.



3 Zug's Reptiles and Amphibians of the Pacific Islands lists Tokelau as having no snakes, not even sea snakes, but does not cover the Chatham or Kermadec Islands.



4 Hawaii has introduced Brahminy Blindsnakes and, unlike many Pacific Islands, it is known that these colonized the island chain more recently, in 1930, when they were imported from the Philippines in potted palm trees. Hawaii also has pelagic sea snakes and there are a few records of introduced brown treesnakes and boa constrictors, but neither species has established a breeding population (yet).



5 A study evaluating the probability that pelagic sea snakes could enter the Caribbean and Atlantic through the Panama canal, as lionfish have, concluded that there were no real barriers to their colonization of the eastern side of the Americas, but so far this has not happened.


ACKNOWLEDGMENTS

Thanks to Kerry Nelson for doing some of the background research for this post as part of a discussion in the Wild Snakes: Education & Discussion Facebook group.

REFERENCES

Edwards, R. J., and A. J. Brooks. 2008. The Island of Ireland: Drowning the Myth of an Irish Land-bridge? Pages 19-34 in J. J. Davenport, D. P. Sleeman, and P. C. Woodman, editors. Mind the Gap: Postglacial Colonisation of Ireland. Special Supplement to The Irish Naturalists’ Journal <link>

Gill, B. J. 1997. Records of turtles and sea snakes in New Zealand, 1837-1996. New Zealand Journal of Marine and Freshwater Research 31:477-486 <link>

Heatwole, H., S. Busack, and H. Cogger. 2005. Geographic variation in sea kraits of the Laticauda colubrina complex (Serpentes: Elapidae: Hydrophiinae: Laticaudini). Herpetological Monographs 19:1-136 <link>

Hecht, M. K., C. Kropach, and B. M. Hecht. 1974. Distribution of the yellow-bellied sea snake, Pelamis platurus, and its significance in relation to the fossil record. Herpetologica 30:387-396 <link>

McKeown, S. 1996. A Field Guide to Reptiles and Amphibians in the Hawaiian Islands. Diamond Head Publishing.

Vasconcelos, R., J. C. Brito, S. Carranza, and D. J. Harris. 2013. Review of the distribution and conservation status of the terrestrial reptiles of the Cape Verde Islands. Oryx 47:77-87 <link>

Wynn, A. H., R. P. Reynolds, D. W. Buden, M. Falanruw, and B. Lynch. 2012. The unexpected discovery of blind snakes (Serpentes: Typhlopidae) in Micronesia: two new species of Ramphotyphlops from the Caroline Islands. Zootaxa 3172:39–54 <link>

Zug, G. R. 2013. Reptiles and Amphibians of the Pacific Islands: A Comprehensive Guide. University of California Press, Berkeley, California, USA <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.





Snakes that are Good Parents

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This article will soon be available in Spanish

Almost all mammals and birds care for their young to some extent, but most amphibians and reptiles do not. We tend to think of snakes as particularly asocial, and in many cases this is probably true. But, a growing body of evidence contradicts the generalization, made as recently as 1978, that "all reptiles produce precocial offspring without postnatal parental care", and shows that some snakes, in particular, are more caring parents than we typically think.

Vipers

A female Timber Rattlesnake (Crotalus horridus)
with her newly-born young
Probably the group of snakes most well-known for parental care are now the vipers, which is somewhat ironic considering the fierce but undeserved reputation of these venomous snakes. Although it was documented as early as 1850, parental care by vipers was not widely known or accepted by the scientific community until the 1990s; like crocodilians, it was assumed that these animals were too vicious to exhibit such caring behavior. When Laurence Klauber, at the time the world's foremost authority on rattlesnakes, wrote in 1956 that "Their propinquity [to aggregate]...does not result from any maternal solicitude; rather it is only because the refuge sought by the mother is also used as a hiding place by the young.", he was uncharacteristically incorrect; in hindsight, his words now seem almost willfully ignorant. In the 1990s, credible reports of parental care in wild pitvipers began to accumulate, corroborating the many older stories listed by Klauber, and in 2002, a seminal review paper based around two studies using radio-telemetry and DNA proved once and for all that mother rattlesnakes do stay with and care for their young. Today, you can read a whole blog about parental care in rattlesnakes, and we think that parental care is widespread (but not ubiquitous) among the ~230 species of pitvipers (aka crotalines or New World vipers). This is particularly remarkable because many of them give birth to live young, which they guard until the young's first shed, even though they may not have eaten for 9-10 months beforehand. It appears that the completion of the first shed cycle is the cue for them to separate, an event which is mediated by the same hormone in snakes as it is in birds and mammals. Because snakes swallow their food whole, the mother can't really feed her offspring, and they forage for themselves after they disperse. Pitvipers are the only snakes known to care for their living young; other snakes with parental care limit themselves to care of their eggs.

Pythons

A mother African Rock Python (Python sebae)
brooding her eggs
The next most well-known example of parental care in snakes is egg-brooding behavior in pythons, first documented in 1835. All 40 species of pythons lay eggs, and most of them coil tightly around them throughout incubation, forsaking food. As with vipers, early reports of this behavior were dismissed, but by the 1930s observations of pythons in zoos showed that they did indeed brood their eggs. Some species that live in cold climates, such as Indian Pythons (Python molurus) and Carpet Pythons (Morelia spilota), also generate heat using muscle contractions ("shivering"). Measurements taken of brooding Indian Pythons have shown that they can increase the temperature of their clutch by 7-10°F. Even though mother pythons may brood for up to 2 months, studies have found that, at normal temperatures, they rarely shiver and lose only about 6% of their body mass, suggesting that the costs of brooding are relatively small compared to the benefits, which also include reduced water loss by the eggs and hatchlings that develop faster and are larger and more active. The brooding instinct in mother pythons is very strong—lab experiments have shown that they will brood the eggs of other pythons just as readily as they will brood their own, and they will even brood rocks that are the same size as their eggs (a behavior reminiscent of the well-known fixed-action pattern of egg-retrieval behavior in graylag geese). Today, pythons are frequently used as models to study female reproductive behavior and life-history trade-offs.

King Cobras

Top: A female King Cobra guarding her nest
Bottom left: A diagram of a typical King Cobra nest
Bottom right: King Cobra eggs in an excavated nest chamber
From Hrima et al. 2014
That female King Cobras (Ophiophagus hannah) use their coils to build a nest of sticks and bamboo leaves and guard their eggs for two to three months has been known at least since 1892. Detailed observation of nest-building and attendance were made in captivity at the Bronx Zoo from 1953-1956, and wild King Cobra nests were surveyed and detailed observations made in 19691. King Cobra nests are the largest and most complex of any snake's, measuring up to four feet in diameter and rising to a similar height, with an internal chamber for the 20-50 eggs and sometimes a second one above for the snake, which abandons the nest just before the eggs hatch. The female must select her nesting material and bring it to the nest site, because the species of bamboo that are most commonly used in building the nest are not the most abundant species in the surrounding area. There are also some anecdotal reports that male King Cobras will guard the nest and/or the female. Some sources suggest that female King Cobras are more aggressive towards humans when they are guarding their nests, but most suggest that their behavior is no different than at any other time.

Other snakes

A female Mudsnake (Farancia abacura)
coils around her eggs in a subterranean nest
Maternal attendance or guarding of clutches of eggs is widespread in snakes, but observations in the wild are still fairly uncommon, mostly due to the difficulty of locating nesting sites. There are several excellent reviews of this topic, including those written by Rick Shine (1988), Carl Gans (1996), Louis Somma (2003), and Zach Stahlschmidt and Dale DeNardo (2011).

Other snakes that have been observed guarding their eggs in the wild include:
It's worth noting that, unlike the case with pythons, survival or physiological benefits to the eggs have not been documented in any of these cases. In addition, there are numerous anecdotal reports of egg attendance in other snakes, many of which are based on hearsay and are not backed up by data, photographs, or even descriptions. So, expect this list to grow, but keep in mind that parental care in snakes is still, and will probably always be, the exception rather than the rule.

Costs and benefits

Except for pythons and pitvipers, the costs and benefits of parental care in snakes have not been examined, and I've mentioned some of the evidence for both in pythons already. Why do rattlesnakes and other pitvipers care for their eggs or young? There are several non-mutually-exclusive theories, including:

A mother Pigmy Rattlesnake (Sistrurus miliarius) with
her brood. Because rattlesnake rattles are made of segments
that form each time the snake sheds its skin, newborn snakes
have only one segment and cannot yet make sound.
1. To protect them from predators. This might involve any or all of the following:

  • Physical concealment, especially of the eggs, which are less well-camouflaged than the adults.
  • Deterrence of predators, which may recognize an adult viper as a threat but not an egg or a juvenile.
  • Active defense from predators, using venom or the threat thereof. This may be especially important prior to the first shed of the young, since they would probably suffer their heaviest mortality during this stage because of their small size, inexperience, hampered eyesight and pit organ sensitivity, and, in rattlesnakes, their inability to use their rattle.
  • Socially-facilitated retreat from predators, in which the parent helps the young escape an attack by physically moving them, showing them what to do, or distracting the predator. These may seem like surprisingly sophisticated behaviors for snakes, but several observations of mother snakes and their young support this idea, and we are learning that many snakes have subtle but complex social lives and communication abilities that have long been underappreciated.

Antipredator benefits of parental care in snakes may vary geographically or in other ways, because some species of pitvipers do not seem to change their defensive behavior when they are guarding their young, but others are more defensive, and still others are less defensive but more distracting.
    Young Tiger Snakes (Notechis scutatus) snuggling
    and data showing that the more litter-mates
    they snuggle with, the more slowly they cool off
    From Aubret & Shine 2009
    2. Litters or clutches of several species of young snakes, including some rattlesnakes, aggregate together, without their mothers, in order to conserve water or heat—which, if they were mammals, we would call snuggling. Experiments have shown that they prefer to snuggle—sorry, I mean aggregate—inside shelters that contain their own scent cues, and that snuggling kept them warm, which helped them slither to shelter faster. No one has tested whether young pitvipers that snuggle with their mothers have higher body temperatures or lower rates of evaporative water loss than those snuggling with one another, but physics suggests that they would, since larger animals have a lower surface-area-to-volume ratio and thus lose heat and water more slowly. The presence of the mother may also offset the increased visibility or olfactory conspicuousness to predators of a bunch of aggregated young snakes. If this is the primary benefit, it is easy to see how maternal attendance of eggs could evolve into maternal attendance of the young, because we think that live birth has evolved many times in snakes, and parental care may have evolved and been lost as many as six and ten times, respectively, in vipers. It's probable that we will continue to fill in the gaps in our knowledge. For example, perhaps we're overlooking the behavior in some poorly-studied vipers, as we did in North American pitvipers for over a century.

    Viper family tree showing the evolution of parental care.
    A few details have changed but the basic shape of the tree
    is the same. Abbreviations: O=oviparous, V=viviparous;
    Tr=tropical, Te=temperate. From Greene et al. 2002
    3. The week or so of parental care may represent an imprinting period for the young snakes to learn the scent of their mother and of one another, similar to the time a young sea turtle spends imprinting on its natal beach or a young salmon on its natal stream. This would be especially important for snakes in cold climates because they use each others' scent trails to locate hibernation sites. Although there is no direct evidence for the third hypothesis, it is suggestive that, at least in the Americas, temperate pitvipers stay with their young, but live-bearing tropical pitvipers, which do not need to hibernate, do not2. Other explanations include that memories of their siblings' scents help young snakes avoid inbreeding later in life, or that they promote other social behaviors, such as communal basking. Some new data suggest that the adult behavior of pitvipers differs when they are deprived of a maternal attendance period. Tall tales about snakes abound, and initially social behavior ranked among them (there are still false tales about parental behavior in snakes, such as the idea that they swallow their young). Parental care in vipers may just be the tip of their social iceberg. Research over the last decade has shown that vipers make use of chemical information left behind by other vipers when they choose their foraging sites, like a dog sniffing a fire hydrant. This kind of cryptic sociality in snakes can lead to things like inheritance of birthing rookeriesnesting sites, and hibernation sites over many generations. Some research even suggests that pair-bonding might happen between male and female copperheads. Some lizards build multi-generational homes; might we one day discover snakes doing the same? If we do, my money is on vipers.



    1 The Kenyan herpetologist J.H.E. Leakey collected eggs from these nests and acknowledged in his paper the support of "the management of the International Hotel, who never once raised any objections to our housing live King Cobras in our rooms."



    2 Intriguingly, the only two Neotropical pitvipers known to have parental care are also the only two that lay eggs. One is the Colombian toad-headed pitviper (Bothrops colombianus), about which very little is known. The other, the Bushmaster (Lachesis muta), well-known by comparison, is nevertheless a secretive denizen of primary rain forests. In 1910, Inaugural Bronx Zoo herp curator Raymond Ditmars and his Trinidad correspondent, R. R. Mole, were the first to publish a photograph of a female Bushmaster guarding her eggs. They wrote of Bushmasters guarding their eggs in the wild, and numerous subsequent captive snakes have borne these observations out. Although Eyelash Pitvipers (Bothriechis schlegelii) have not been observed to guard their young, they may do so because their young shed several days after birth, like those of temperate pitvipers, rather than within 24 hours of birth, like most tropical live-bearing pitvipers. The pattern of parental care in Old World vipers, about which we have far less information, appears to be more complicated still.
    ACKNOWLEDGMENTS

    Thanks to my parents, for indulging my interest in snakes and encouraging me to pursue a career studying them, and to Jim Williams, Peter May, J. Lanki, and Matt Nordgren for the use of their photos.

    REFERENCES

    Aubret, F., X. Bonnet, R. Shine, and S. Maumelat. 2005. Energy expenditure for parental care may be trivial for brooding pythons, Python regius. Animal Behaviour 69:1043-1053 <link>

    Aubret, F., X. Bonnet, R. Shine, and S. Maumelat. 2005. Why do female ball pythons (Python regius) coil so tightly around their eggs? Evolutionary Ecology Research 7:743-758 <link>

    Aubret, F., and R. Shine. 2009. Causes and consequences of aggregation by neonatal tiger snakes (Notechis scutatus, Elapidae). Austral Ecology 34:210-217 <link>

    Bates, M. F. 1985. Notes on egg clutches in Lamprophis inornatus and Psammophylax rhombeatus rhombeatus. The Journal of the Herpetological Association of Africa 31:21-22.

    Benedict, F. G., E. L. Fox, and V. Coropatchinsky. 1932. The incubating python: a temperature study. Proceedings of the National Academy of Sciences 18:209-212 <link>

    Brashears, J., and D. F. DeNardo. 2012. Do brooding pythons recognize their clutches? Investigating external cues for offspring recognition in the Children's Python, Antaresia childreni. Ethology 118:793-798 <link>

    Brown, G. P., and R. Shine. 2007. Like mother, like daughter: inheritance of nest-site location in snakes. Biology Letters 3:131-133 <link>

    Brown, W. S., and F. M. MacLean. 1983. Conspecific scent-trailing by newborn timber rattlesnakes, Crotalus horridus. Herpetologica 39:430-436 <link>

    Butler, J.A., T.W. Hull, and R. Franz. 1995. Neonate aggregations and maternal attendance of young in the Eastern Diamondback Rattlesnake, Crotalus adamanteus. Copeia 1995:196–198 <link>

    Campbell, J. A., and W. W. Lamar. 1992. The taxonomic status of miscellaneous Neotropical viperids, with the description of a new genus. Occasional Papers of the Museum, Texas Tech University 153:1-31 <link>

    Case, T. J. 1978. Endothermy and parental care in the terrestrial vertebrates. American Naturalist 112:861-874 <link>

    Clark, R. W. 2007. Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites. Behavioral Ecology 18:487-490 <link>

    Clark, R. W., W. S. Brown, R. Stechert, and H. W. Greene. 2012. Cryptic sociality in rattlesnakes (Crotalus horridus) detected by kinship analysis. Biology Letters 8:523-525 <link>

    Cunningham, G. R., S. M. Hickey, and C. M. Gowen. 1996. Crotalus viridis viridis (Prairie Rattlesnake). Behavior. Herpetological Review 27:24 <link>

    DeNardo, D. F., O. Lourdais, and Z. R. Stahlschmidt. 2012. Are females maternal manipulators, selfish mothers, or both? Insight from pythons. Herpetologica 68:299-307 <link>

    Gans, C. 1996. An overview of parental care among the Reptilia. Pages 145-157 in J. S. Rosenblatt and C. T. Snowdon, editors. Parental Care: Evolution, Mechanisms, and Adaptive Significance. Academic Press, San Diego, California, USA <link>

    Graves, B. M. 1989. Defensive behavior of female prairie rattlesnakes (Crotalus viridis) changes after parturition. Copeia 1989:791-794 <link>

    Greene, H.W., P.G. May, D.L. Hardy, J.M. Sciturro, and T.M. Farrell. 2002. Parental behavior by vipers. Pp. 179-206 In Biology of the Vipers. Schuett, G.W., M. Höggren, M.E. Douglas, and H.W. Greene (Eds.).  Eagle Mountain Publishers, Eagle Mountain, UT <link>

    Hibbard, C. W. 1964. A brooding colony of the blind snake, Leptotyphlops dulcis dissecta. Copeia 1964:222 <link>

    Hoss, S.K. and R.W. Clark. 2014. Mother Cottonmouths (Agkistrodon piscivorus) alter their antipredator behavior in the presence of neonates. Ethology 120:933-941 <link>

    Hoss, S. K., D. H. Deutschman, W. Booth, and R. W. Clark. 2015. Post-birth separation affects the affiliative behaviour of kin in a pitviper with maternal attendance. Biological Journal of the Linnean Society 116:637-648 <link>

    Hoss, S.K., M.J. Garcia, R.L. Earley, and R.W. Clark. 2014. Fine-scale hormonal patterns associated with birth and maternal care in the cottonmouth (Agkistrodon piscivorus), a North American pitviper snake. General and Comparative Endocrinology 208:85-93 <link>

    Leakey, J. 1969. Observations made on king cobras in Thailand during May 1966. Journal of the National Research Council of Thailand 5:1-10.

    Mori, A., and T. M. Randriamboavonjy. 2010. Field observation of maternal attendance of eggs in a Madagascan snake, Leioheterodon madagascariensis. Current Herpetology 29:91-95 <link>

    Oliver, J. A. 1956. Reproduction in the king cobra, Ophiophagus hannah Cantor. Zoologica 41:145-152.

    Reiserer, R., G. Schuett, and R. Earley. 2008. Dynamic aggregations of newborn sibling rattlesnakes exhibit stable thermoregulatory properties. Journal of Zoology 274:277-283 <link>

    Savary, W. 1999. Crotalus molossus molossus (northern blacktail rattlesnake). Brood defense. Herpetological Review 30:45 <link>

    Schuett, G., R. Repp, M. Amarello, and C. Smith. 2013. Unlike most vipers, female rattlesnakes (Crotalus atrox) continue to hunt and feed throughout pregnancy. Journal of Zoology 289:101-110 <link>

    Shine, R. 1988. Parental care in reptiles. Pp. 275-330 In Biology of the Reptilia. Gans, C. and R.B. Huey (Eds.).  Alan Liss, New York <link>

    Smith, C. F., and G. W. Schuett. 2015. Putative pair-bonding in Agkistrodon contortrix (Copperhead). Northeastern Naturalist 22:N1-N5 <link>

    Somma, L. A. 2003a. Parental Behavior in Lepidosaurian and Testudinian Reptiles: A Literature Survey. Krieger Publishing Company, Malabar, Florida, USA.

    Somma, L. A. 2003b. Reptilian parental behaviour. The Linnean 19:42-44 <link>

    Stahlschmidt, Z.R. and D.F. DeNardo. 2011. Parental care in snakes. Pp. 673-702 In Reproductive Biology and Phylogeny of Snakes. Aldridge, R.D. and D.M. Sever (Eds.).  Science Publishers, Enfield, New Hampshire <link>

    van Mierop, L. H. S., and E. L. Bessette. 1981. Reproduction of the ball python, Python regius in captivity. Herpetological Review 12:20-22 <link>

    Wall, F. 1924. The Hamadryad or King Cobra, Naja hannah (Cantor). Journal of the Bombay Natural History Society 30:189-195 <link>

    Walters, A. C., and W. Card. 1996. Agkistrodon piscivorus conanti (Florida Cottonmouth). Brood defense. Herpetological Review 27:203 <link>

    Wasey, G. K. 1892. A nest of King Cobra's eggs. Journal of the Bombay Natural History Society 7:257 <link>

    Whitaker, N., P. G. Shankar, and R. Whitaker. 2013. Nesting ecology of the King Cobra (Ophiophagus hannah) in India. Hamadryad 36:101-107.


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    Life is Short but Snakes are Long 2015 Milestones

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    Dear reader,

    Instead of debuting my planned new content for this month, I wanted to take a moment to thank you for your readership, to review the several milestones reached by Life is Short but Snakes are Long in 2015, and to outline where it's headed in the future.

    The back cover of the paperback edition of Harry Greene's opus Snakes:
    The Evolution of Mystery in Nature
    , bearing the review by eminent
    nature writer David Quammen from which this blog takes its name
    Life is Short but Snakes are Long reached half a million unique views this year (by over 320,000 unique readers from nearly every country) on September 28th, 2015. When I began writing it on April 4, 2012, I would never have imagined that so many people would want to read about snakes. Since that time, the pace and intensity of my dissertation research has increased steadily, and my goal for this year was to publish one article a month, which I am proud to say I have achieved (unless you think that this one is cheating, which I kind of do). Even though I wrote fewer articles this year, many of them were more ambitious than my past articles, in that they synthesized large bodies of literature that I personally knew little about before I started writing.

    Countries and regions from which readers have accessed Life is Short
    From what I can see on this tiny map, we're missing only Svalbard,
    Western Sahara, Turkmenistan, and North Korea
    My other goals for this blog include: 1) to provide referenced, reputable information that is not available elsewhere, 2) to synthesize & translate information from the peer-reviewed literature, and 3) to indulge my own broad interests. I know I've been successful with #3, which was important to me because I was afraid of becoming too specialized in the process of getting my PhD. Whether or not I've succeeded at numbers 1 & 2 you'll have to tell me. Apparently at least a few people think so, because articles from Life is Short but Snakes are Long have been syndicated by HerpNation Media and linked to, covered, or republished (with permission) by:
    I also found out that one of my posts was nominated for a ‘Best Science Writing Online 2013’ contest (although it did not win). Because of the blog, I've also been asked to provide review services on snake biology to Bones on Fox TV, The Blacklist on NBC, and the children's book publisher Cherry Lake Publishing. Finally, I was invited to travel to San Antonio, Texas, in May for the International Herpetological Symposium to speak at their Science Café and also in their general program about Life is Short but Snakes are Long, which I really enjoyed. I want to thank the many editors, writers, scientists, publicists, and reporters who thought my writing was good enough to republish or pay attention to in some form.

    My Sonoran Coralsnake (Micruroides euryxanthus)
    I also reached a personal herping milestone this year: 100 snake species seen alive and in the wild, on July 30th, 2015, with a Sonoran Coralsnake (Micruroides euryxanthus) that I found on Portal Road in Cochise County, Arizona. This was an especially exciting snake for me because it was my first wild elapid and because I was there with the American Museum of Natural History Southwest Research Station's  Field Herpetology of the Southwest class, where the enthusiasm was nothing short of infectious. I also published several peer-reviewed journal articles and short notes this year, including one that I came across as a direct result of writing Life is Short but Snakes are Long. Because I'll be writing and (hopefully) completing my dissertation in 2016, I'll likely be relying more heavily on updating and re-posting existing material, since I'll have less time to research and write new material. But, I have some new articles planned that I've already begun working on, so there should be a mix of old and new in 2016.

    Life is Short but Snakes are Long would not be possible without support from volunteer translators Alvaro Pemartin& Estefania Carrillo, from Utah State University, particularly my advisor Susannah French and the Ecology Center, and from my loving girlfriend and editor Kendal Morris.

    Thank you, and happy 2016!

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    Bushmaster

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    This post will soon be available in Spanish

    Bushmaster (Lachesis muta) from Peru
    Lachesis is the name of one of the three Greek Moirai or Fates, sister-deities who determined the destiny of every human life by spinning each life as a thread on a loom. Her role in the process was to determine the length of a mortal's life, and so she is appropriately immortalized1 in modern biology in the genus name of Bushmasters, huge Latin American pitvipers that occasionally play the same role and are herpetologically mythical in their own right. Her sisters, Clotho (who spun the threads of life) and Atropos (who did the actual thread-cutting), are similarly honored in the Latin name of vipers of the genus Atropoides and in Clotho, an old synonym for some members of the African viper genus Bitis.

    Ditmars filming the Bushmaster "Lecky" at the Bronx Zoo in 1934
    ©WCS. Courtesy of the WCS Archives
    If you're interested in Bushmasters and herpetological history, check out Dan Eatherley's new book, "Bushmaster: Raymond Ditmars and the Hunt for the World's Largest Viper", which chronicles the life and times of the Bronx Zoo's first reptile curator and one of America's first and most successful popular herpetological writers. Ditmars authored 24 books, >200 articles, and pioneered nature films in an era when video technology was still in its infancy. Eighty years ago, he was a household name in New York, enjoying a celebrity attained by few herpetologists. President Theodore Roosevelt praised Ditmars's The Reptile Book and invited him to the White House. One of the reasons for his popularity was his "obsession" with keeping large, exotic, sexy, venomous snakes—such as Bushmasters—in captivity, an endeavor on which the press regularly reported. Ditmars was reporter for New York Times when he was young, and the paper published 12-15 stories a year on his exploits between 1899 and 1942. Such was the popularity drummed up for snakes that, when a short-lived Bushmaster named "Lecky" was exhibited at the Bronx Zoo in 1934, it was credited with attracting an estimated 100,000 additional guests at the zoo and a 60% increase in visitors at the nearby American Museum of Natural History’s reptile hall.

    The first photograph of a female Bushmaster guarding her eggs,
    taken by C.S. Rogers in Trinidad, was published in Ditmars (1910),
    and subsequently as a postcard sold at the Bronx Zoo.
    The snake was a captive in the possession of R.R. Mole.
    Bushmasters are unique among New World vipers, with the possible exception of the rare Bothrops colombianus, in laying eggs rather than giving birth to live young. Because they guard their eggs, a phenomenon that Ditmars and his correspondent R.R. Mole first described, they may offer insight into the complex evolution of parental care in pitvipers. In Ditmars's time, there was a single, widespread species of bushmaster, with four subspecies separated by tropical mountain ranges; we now recognize those four subspecies as species on the basis of morphological, behavioral, and molecular differences. Bushmasters are also the only pitvipers where the venom of juveniles appears to lack the chemical potency of adults, at least towards mammals. Many vipers feed on amphibians or other reptiles when they are young and switch to mammals as they grow up2, which might explain this observation. Bushmasters are the world's longest vipers3 (Gaboon Vipers exceed them in weight) and the longest venomous snakes in the Americas (King Cobras exceed them in length).

    Ditmars wears a snake fang tie pin
    on the book's cover
    Eatherley's book is well-researched and accurate. I found it to be an exciting read with an excellent historical perspective. My biggest criticism was that it was a little sensational at times, as are most popular accounts dealing with venomous snakes. I particularly enjoyed the author's description of his experiences meeting up with some New York City herpers to seek Gartersnakes (Thamnophis sirtalis), Brownsnakes (Storeria dekayi), and other snakes that could still be found in the northern part of Central Park in the 1880s, when Ditmars was cutting his herpetological teeth. I was also interested to learn that Ditmars supplied snake venom to early antivenom producers and set a precedent, still in place today, of zoos stocking exotic snake antivenoms for the dual purpose of protecting their keepers and providing them to the medical community when bites from exotic species occur elsewhere.

    In his writing, Ditmars often portrayed Bushmasters as aggressive, in contrast to many other herpetologists who have described their manner as relatively gentle, even timid. In reality, they are, like most venomous snakes, cowards first, then bluffers, and lastly warriors, and their large size has earned them a reputation as formidable warriors as well as a prominent position in folklore throughout Latin America4. Their mystique and biology effectively drive Eatherley's book, only the second biography of Ditmars ever written (the first, by Laura Newbold Wood, was written for children and published in 1944, just two years after Ditmars's death). Throughout the book, Eatherley goes from stating that negative responses towards reptiles are “of course, the norm for most of us” (p. 11) to tracing a rapid path from ecstasy to palpable disappointment, familiar to any snake enthusiast, when informed during his search for a wild Bushmaster in Trinidad that a nearby farmer has found one, but killed it (p. 255). I think that Ditmars would be pleased with his abiding influence, nearly 75 years after his death, in inspiring passion for and love of snakes.

    You can read two other reviews of Eatherley's book, published last month in Copeia and Herpetological Review.



    1 I suppose she was already immortal, since she's a Greek Goddess.




    2 Strangely, bushmasters seem to be one of the only vipers where this shift is not well-documented. Collecting data on young snakes is hard, and the venom study found that venom chemistry became more adult-like after just one year, so perhaps we've just missed the shift. Another hypothesis is that bushmasters tend to hold onto their prey after striking it, unlike other vipers which strike, release, and relocate, so perhaps the rapid immobilizing venom components have been replaced by a mechanical means of immobilization.



    3 Regarding their maximum length, Campbell & Lamar's authoritative reference on venomous reptiles of the western hemisphere says: "Documented reports of measured specimens are scarce, however, and the maximum length has been the subject of some hyperbole. Hoge and Lancini (1962) claimed 4.5 m, Abalos (1977) claimed 3.5 m, Ditmars (1937) mentioned specimens of 11 feet (3.35 m) but apparently never saw one exceeding 3m, Bellairs (1969) gave the maximum length as between 3.05 and 3.36m, Dunn (1951) gave the maximum length as 14 feet (4.27 m), and Mertens (1960) listed 13 feet (3.96 m) as the maximum size. Sandner-Montilla (1994) claimed a record of 5.28 m for a Venezuelan specimen of L. muta (with 6-cm fangs!), but such records must be placed in the same realm as 20-m anacondas and other legendary monsters.", and concludes "The great 
    majority of adult specimens of all species of Lachesis measure less than 2.5 m, and 3.5 m is likely near the maximum size."



    4 Bushmasters play other roles in human culture as well—as food. 
    Bora and Yagua Indians in eastern Peru consider them a delicacy. They are certainly one of the few snakes large enough to make a filling meal for a family.


    ACKNOWLEDGMENTS

    Thanks to Dan Eatherley and Arcade Publishing for producing such a wonderful book, of which they kindly provided me a copy, to Drew Foster for sharing an advance copy of his review of this book for Copeia, to Marisa Ishimatsu and the Wildlife Conservation Society for the use of their photographs, and to Harry Greene for shedding a little more light on the diets of juvenile bushmasters.

    REFERENCES

    Adler, K. 1989. Contributions to the History of Herpetology. Volume 1. Society for the Study of Amphibians and Reptiles, Oxford, Ohio <link>

    Campbell, J. A., and W. W. Lamar. 2004. The Venomous Reptiles of the Western Hemisphere (2 Vol.). Cornell University Press, Ithaca, New York <link>

    Ditmars, R. L. 1910. Reptiles of the World : Tortoises and Turtles, Crocodilians, Lizards, and Snakes of the Eastern and Western Hemispheres. Macmillan Co., New York <link>

    Gutiérrez, J., C. Avila, Z. Camacho, and B. Lomonte. 1990. Ontogenetic changes in the venom of the snake Lachesis muta stenophrys (bushmaster) from Costa Rica. Toxicon 28:419-426 <link>

    Eatherley, D. 2015. Bushmaster: Raymond Ditmars and the Hunt for the World's Largest Viper. Arcade Publishing, New York, New York <link>

    Foster, C. D. 2015. Bushmaster: Raymond Ditmars and the Hunt for the World’s Largest Viper [book review]. Copeia 103:1107-1109 <link>

    Novotny, R. J. 2015. Bushmaster: Raymond Ditmars and the Hunt for the World's Largest Viper [book review]. Herpetological Review 46:657-659 <link>

    Wood, L. N. 1944. Raymond L. Ditmars: His Exciting Career With Reptiles, Animals and Insects. The Junior Literary Guild and Julian Messner, Inc., New York <link>

    Zamudio, K. R., and H. W. Greene. 1997. Phylogeography of the bushmaster (Lachesis muta: Viperidae): implications for neotropical biogeography, systematics, and conservation. Biological Journal of the Linnean Society 62:421-442 <link>

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    Dragonsnakes and Filesnakes Revisited

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    I've written about both filesnakes (family Acrochordidae) and dragonsnakes (part of the family Xenodermidae1) before. Traditional snake taxonomy suggests that, although they branch off from the main stem of the snake family tree at about the same time, they're not very closely related. But, new evidence emphasizes the uniqueness of dragonsnakes and thickens the plot in the unfolding story of the evolution of snakes.

    Two hypotheses about the relationships of the major groups of snakes.
    Left: tree based on nuclear genes, showing Acrochordidae and Xenodermidae
    as successive outgroups to core Colubroidea
    Right: tree based on mitochondrial genes, showing a sister relationship
    between Acrochordidae and Xenodermidae
    From Oguiura et al. 2009
    Most phylogenetic analyses are pretty consistent in classifying both filesnakes and dragonsnakes as caenophidians, or "advanced" snakes. But, they differ in their placement of dragonsnakes and other xenodermids, including the truly strange and obscure odd-scaled snakes (Achalinus), bearded snakes (Fimbrios), stream, earth, or red snakes (Stoliczkia2), wood, mountain, or narrow-headed snakes (Xylophis), and a new genus, just described in 2015 and still without a common name, Parafimbrios. Most analyses group xenodermids with the colubroids (pareids1, vipers, homalopsids, colubrids, lamprophiids, and elapids), albeit as the most basal branch. Many textbooks actually define Caenophidia as Colubroidea + Acrochordidae (aka Acrochordoidea), distinctly separating the colubroids from the filesnakes on the basis of shared, derived characteristics such as wide ventral scales, as well as features of the skull, hemipenes, and the muscles, cartilages, and arteries between the ribs. However, several recent trees based on DNA sequences suggest instead that filesnakes and dragonsnakes might be one another's closest living relatives.

    Study
    Acrochordid-Xenodermid Relationship
    Support
    How many species?
    What data were used?
    X&A
    -
    -
    Morphology
    X+A
    8%
    37
    ND4
    X+A
    98%
    98
    4 mitochondrial genes
    A,X
    not reported
    25
    7 nuclear genes
    A,X
    >95%
    50
    20 nuclear genes
    A,X*
    100%
    30
    12 nuclear genes
    A,X
    94%
    131
    2 mitochondrial genes + 1 nuclear gene
    A,X
    97-100%
    761
    3 mitochondrial genes + 2 nuclear genes
    X,A
    95-100%
    141 extant +
    51 extinct
    610 morphological characters
    A,X
    100%
    161
    44 nuclear genes
    X+A
    95%
    4,161
    5 mitochondrial genes + 7 nuclear genes
    A,X*
    99%
    32
    333 nuclear loci
    with 100% coverage
    A,X
    91%
    4,162
    5 mitochondrial genes + 47 nuclear genes
    A selection of studies that have examined the relationship between acrochordids and xenodermids.
    X+A means that the two are each other's closest relatives; A,X means that acrochordids are more distantly
    related to colubroids than xenodermids; X,A means that xenodermids are more distant
    *Relationships differed depending on which methods were used


    Arafura Filesnake (Acrochordus arafurae)
    For example, the first study to use DNA to examine the relationships of these two groups of snakes found some support for each hypothesis, concluding that the "potential sister-taxon relationship of acrochordids and xenodermines [is] a reasonable hypothesis requiring future testing." In 2003, data from three more mitochondrial genes resulted in the same relationship, causing the authors to suggest that xenodermids should be excluded from Colubroidea. However, since that time, numerous studies have not repeated this result. In 2009, one research group predicted that "these differences...are due to taxonomic sampling issues", predicting that as DNA was collected from more species of snakes, the basal position of Acrochordus would be confirmed.

    Dragonsnake (Xenodermus javanicus)
    So, it was a real surprise when a 2013 analysis, the largest yet, including samples from 80% of all snake genera, placed Acrochordidae and Xenodermidae as sister groups. Neither a follow-up analysis combining that dataset with one containing data from many more genes nor an analysis using only the most complete data have settled the issue. The latter study compared several methods for generating phylogenetic trees and found that the relationship between acrochordids and xenodermids depended a lot on which methods were used. Part of the problem is that, even if they are each others' closest relatives, they still diverged between 70 and 80 million years ago, making them susceptible to a problem in phylogenetics known as long-branch attraction, which happens when the amount of evolutionary change within a lineage causes that lineage to appear similar (and thus closely related) to another long-branched lineage, solely because they have both undergone a lot of change, rather than because they are actually related.

    Bearded Snake (Fimbrios klossi)
    The truth is that both acrochordids and xenodermids are obscure snakes, and we don't have that much data on either one of them. They are both found in areas of the world that are hard to get to. Morphologically, they appear superficially similar, and an association between them was first hypothesized in 1893But, even the most comprehensive morphological trait database for snakes is missing crucial data on their anatomy, such as whether or not their hemipenial spines are mineralized. This would be helpful to know because  the hemipenial spines of basal snakes such as boas and pythons are not mineralized, whereas those of definitive colubroids are heavily mineralized.

    Parafimbrios lao
    From Teynié et al. 2015
    Within the past year, two new studies on the chromosomes of dragonsnakes (Xenodermus javanicus) have been published. In the first, the karyotype (the number of chromosomes and their shape) of dragonsnakes was reported for the first time. In humans, each cell normally contains 23 pairs of chromosomes, for a total of 46. In most snakes, each cell normally contains 18 pairs of chromosomes, for a total of 36. Usually, eight of these pairs are relatively large (called macrochromosomes), and the other ten are somewhat small (called microchromosomes). Dragonsnakes have 16 pairs of chromosomes, for a total of 32, of which seven are large and nine are small. The dragonsnake karyotype probably evolved by two fusion events, one of two macrochromosomes and the other between a macrochromosome with a microchromosome. There are some other exceptions to the 18-pair pattern; some snakes have as few as 12 or as many as 25 pairs, including the only other xenodermid to have been karyotyped, the Sichuan Odd-scaled Snake (Achalinus meiguensis), which has just 12 pairs of chromosomes.

    Amami Odd-scaled Snake (Achalinus werneri)
    From the 1960s to the 1980s, before DNA sequencing became cheap and easy, scientists invested heavily in collecting karyotypes from a diversity of species for comparative purposes, so we can say with pretty good certainty that the ancestral state for all snakes is 36 (18 pairs). That's the number in filesnakes, pareids, most vipers, homalopsids, and many "crown colubroids" (colubrids, lamprophiids, and elapids, although there are lots of exceptions in these three groups).  The fusions in xenodermids emphasize their uniqueness, but unfortunately don't shed any new light on their phylogenetic placement.

    Stoliczkia borneensis
    The other study focused on the sex chromosomes. In humans, sex is determined by which combination of sex chromosomes a baby receives from its parents: two X chromosomes make a female, whereas an X and a Y chromosome make a male. It's pretty similar in snakes, with a twist: the sex chromosomes are called Z and W instead of X any Y, and females are the heterogametic sex (meaning that a Z and a W chromosome make a female, and two Z chromosomes make a male). Birds and many other reptiles also have ZW sex determination. In many colubroid snakes, the W chromosome is about twice the size of the Z,  and it is often unusual in other ways as well, such as having sections of highly condensed chromatin or a different centromere position. In contrast, filesnakes, boids, and other more basal snakes have morphologically indistinguishable Z and W chromosomes, although they still contain different genes and perform different functions.

    Perrotet's Narrow-headed Snake (Xylophis perroteti)
    Are members of this genus really xenodermids? Or, like the
    former xenodermids Oxyrhabdium and Nothopsis, will they
    prove to be more closely related to something else?
    One reason the W chromosome looks so different from the Z in colubroids is that it contains repetitive elements called Bkm ('banded krait minorsatellite') repeats, which consist of the sequence "GATA" (sometimes "GACA") repeated thousands of times. Mammalian X chromosomes and avian W chromosomes also have these repeats. Cell biologists think that these repeats function to inactivate all the genes on the W chromosome except for those that determine sex3. Both mammalian X chromosomes and snake W chromosomes become very dense in body cells, so that none of the genes on them can be expressed. They only decondense and plays their brief, female-determining roles, in maturing eggs that are destined to become females. Unlike in mammals, the sex chromosomes of snakes span the gamut from completely identical to markedly differentiated, allowing biologists to study the evolution of chromosomal sex determination. The new study showed that female dragonsnakes have two different-looking sex chromosomes, with many Bkm repeats in the W, whereas the two Z sex chromosomes of male dragonsnakes look similar and lacked Bkm repeats, bolstering the relationship between xenodermids and other colubroids and diminishing the relationship between xenodermids and filesnakes.

    The other major finding of the new study is the documentation that at least part of the sex chromosomes are homologous across all families of caenophidian snakes, suggesting that snake sex chromosomes emerged in the common ancestor of Caenophidia some 60-80 million years ago. One gene that is only on the Z chromosome in all caenophidians, including dragonsnakes, is also found on the W chromosome in filesnakes. The Z-chromosome-specific genes in caenophidians were on both the Z and W chromosomes in boas, pythons, and sunbeam snakes (Xenopeltidae), as well as in bearded dragons and anoles. Other toxicoferan lizards with ZW sex chromosomes, including chameleons and monitor lizards, seem to have evolved them independently.



    1 A recent article in the journal Herpetological Review pointed out that the grammatical rules for structuring family and subfamily names from genus names have recently been incorrectly applied in two cases involving snakes which concern this article: 1) Xenodermatidae/inae for the family/subfamily containing Xenodermus, the root of which is "dermus", a masculine noun with which the masculine specific epithet javanicus is correctly coupled (not the neuter javanicum; in contrast think of the neuter Heloderma horridum in family Helodermatidae). The correct family or subfamily name is thus Xenodermidae/inae. 2) Pareatidae or Pareatinae for the family containing Pareas, which is also masculine, making the correct family/subfamily name Pareidae/inae.



    2 Don't confuse this snake genus (Stoliczkia) with a genus of extinct ammonite (Stoliczkaia), both named for Czech biologist Ferdinand Stoliczka. The extra "a" was added to the original spelling of the snake genus by Boulenger in 1899, probably by accident, and this genus is still widely misspelled today (e.g., on GenBank and on Wikipedia before I fixed it while writing this article).



    3 It's also thought that "GATA" is a particularly potent regulatory sequence, with the power to turn nearby genes on and off. In a way, the sex genes have essentially 'hijacked' the W chromosome, turning off all its other genes, and simultaneously creating a concentrated source of mutation-causing elements. Chromosomal sex determination may therefore constitute a unique and potentially very powerful genotypic mechanism for abruptly enhancing evolutionary rates, which might have contributed to the explosive radiations of species in clades with chromosomal sex determination, such as mammals, birds, squamates, and certain groups of insects.

    ACKNOWLEDGMENTS

    Thanks to Thomas CalameSam HowardKonrad MebertZeeshan MirzaTakehito Sato, and Stephen Zozaya for the use of their photos.

    REFERENCES

    Boulenger, G. A. 1893. Catalogue of the Snakes in the British Museum (Natural History). Volume I., containing the families Typhlopidae, Glauconiidae, Boidae, Ilysiidae, Uropeltidae, Xenopeltidae, and Colubridae Aglyphae, Part. Trustees of the British Museum, London. <link>

    Boulenger, G. A. 1899. Description of three new reptiles and a new batrachian from Mt. Kina Balu, North Borneo. Annals and Magazine of Natural History 7:451-453 <link>

    Gauthier, J. A., M. Kearney, J. A. Maisano, O. Rieppel, and A. D. B. Behlke. 2012. Assembling the squamate Tree of Life: perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History 53:3-308 <link>

    Jerdon, T. C. 1870. Notes on Indian Herpetology. Proceedings of the Asiatic Society of Bengal 1870:66-85 <link>

    Jones, K., and L. Singh. 1985. Snakes and the evolution of sex chromosomes. Trends in Genetics 1:55-61 <link>

    Lawson, R., J. B. Slowinski, B. I. Crother, and F. T. Burbrink. 2005. Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 37:581-601 <link>

    Kelly, C. M. R., N. P. Barker, and M. H. Villet. 2003. Phylogenetics of advanced snakes (Caenophidia) based on four mitochondrial genes. Systematic Biology 52:439-459 <link>

    Kraus, F., and W. M. Brown. 1998. Phylogenetic relationships of colubroid snakes based on mitochondrial DNA sequences. Zoological Journal of the Linnean Society 122:455-487 <link>

    Oguiura, N., H. Ferrarezzi, and R. Batistic. 2009. Cytogenetics and molecular data in snakes: a phylogenetic approach. Cytogenetic and Genome Research 127:128-142 <link>

    O’Meally, D., H. R. Patel, R. Stiglec, S. D. Sarre, A. Georges, J. A. M. Graves, and T. Ezaz. 2010. Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Research 18:787-800 <link>

    Pokorna, M., and L. Kratochvíl. 2009. Phylogeny of sex‐determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zoological Journal of the Linnean Society 156:168-183 <link>

    Pyron, R. A., F. T. Burbrink, G. R. Colli, A. N. M. de Oca, L. J. Vitt, C. A. Kuczynski, and J. J. Wiens. 2011. The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Molecular Phylogenetics and Evolution 58:329-342 <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 Biology 13:53 <link>

    Pyron, R. A., C. R. Hendry, V. M. Chou, E. M. Lemmon, A. R. Lemmon, and F. T. Burbrink. 2014. Effectiveness of phylogenomic data and coalescent species-tree methods for resolving difficult nodes in the phylogeny of advanced snakes (Serpentes: Caenophidia). Molecular Phylogenetics and Evolution 81:221-231 <link>

    Rovatsos, M., M. Johnson Pokorná, and L. Kratochvíl. 2015. Differentiation of sex chromosomes and karyotype characterisation in the Dragonsnake Xenodermus javanicus (Squamata: Xenodermatidae). Cytogenetic and Genome Research 147:48-54 <link>

    Rovatsos, M., J. Vukić, P. Lymberakis, and L. Kratochvíl. 2015. Evolutionary stability of sex chromosomes in snakes. Proceedings of the Royal Society B: Biological Sciences 282:20151992 <link>

    Savage, J. M. 2015. What are the correct family names for the taxa that include the snake genera Xenodermus, Pareas, and Calamaria? Herpetological Review 46:664-665 <link>

    Sharma, G., and U. Nakhasi. 1980. Karyological studies on six species of Indian snakes (Colubridae: Reptilia). Cytobios 27:177-192 link>

    Teynié, A., P. David, A. Lottier, M. D. Le, N. Visal, and T. Q. Nguyan. 2015. A new genus and species of xenodermatid snake (Squamata: Caenophidia: Xenodermatidae) from northern Lao People’s Democratic Republic. Zootaxa 3926:523-540 <link>

    Vicoso, B., J. Emerson, Y. Zektser, S. Mahajan, and D. Bachtrog. 2013. Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biology 11:e1001643 <link>

    Vidal, N., A. S. Delmas, P. David, C. Cruaud, A. Couloux, and S. B. Hedges. 2007. The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. Comptes Rendus Biologies 330:182-187 <link>

    Wang, G., S. He, S. Huang, M. He, and E. Zhao. 2009. The complete mitochondrial DNA sequence and the phylogenetic position of Achalinus meiguensis (Reptilia: Squamata). Chinese Science Bulletin 54:1713-1724 <link>

    Wiens, J. J., C. A. Kuczynski, S. A. Smith, D. G. Mulcahy, J. W. Sites, T. M. Townsend, and T. W. Reeder. 2008. Branch lengths, support, and congruence: testing the phylogenomic approach with 20 nuclear loci in snakes. Systematic Biology 57:420-431 <link>

    Wiens, J. J., C. R. Hutter, D. G. Mulcahy, B. P. Noonan, T. M. Townsend, J. W. Sites, and T. W. Reeder. 2012. Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species. Biology Letters 8:1043-1046 <link>

    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 <link>

    Zheng, Y., and J. J. Wiens. 2016. Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Molecular Phylogenetics and Evolution 94:537-547 <link>

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    State Snakes, Linnaean Names, and Other Recent Updates

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    As I wrote in December, the demands of completing my dissertation (and my new position as a science reporter with Utah Public Radio) haven't left me enough time to write the more in-depth long-form content that I (and readers, it seems) like so much. If all goes according to plan, I should return to those more elaborate articles towards the end of 2016, but in the meantime I wanted to highlight some recent and exciting updates to some of my older articles.

    What the State Snakes Should Be

    A Common Gartersnake (Thamnophis sirtalis)
    eats a Woodhouse's Toad (Anaxyrus woodhousei)
    In February the state of Virginia became the first state to officially designate a state snake. They chose the Common Gartersnake (Thamnophis sirtalis), despite being literally one of only two states in the nation to share their name with a genus of snake! If they had read my 2013 article, they might have gone with my pick of Virginia valeriae, the widespread Smooth Earthsnake, instead. But, perhaps there was already enough controversy: the gartersnake was proposed by 11-year-old Aiden Coleman of Williamsburg, but was put down by senators for being too wimpy. A couple of senators preferred the Timber Rattlesnake (Crotalus horridus), but the gartersnake was reinstated after Coleman asked one of them "just how much like West Virginia do you want us to be?"—unlike the legislators, Coleman already knew that the Timber Rattlesnake is the (very well-chosen) state reptile of West Virginia. The bill is now with the governor, whom some have suggested is the real snake.

    The Linnaean Snakes

    An Eastern Ribbonsnake from the panhandle of Florida
    Heads up, taxonomy buffs—the scientific name of the Eastern Ribbonsnake (currently Thamnophis sauritus) is probably about to change to Thamnophis saurita, for some fairly technical linguistic reasons. Linnaeus named both this species and Thamnophis sirtalis, but because Linnaeus's description for sirtalis better matched sauritus, the two names were for decades confusingly interchanged. All seemed to be settled by a 1956 ICZN ruling, but in March a new paper in the journal Herpetological Review pointed out that Saurita, the original spelling used by Linnaeus, was capitalized and that its –a ending did not match the masculine gender of his genus Coluber. According to the grammatical rules of species naming that Linnaeus followed and which we still follow, this means that he meant "Saurita" to be a noun, rather than an adjective, and so the ending should not change to match the gender of the genus. The common assertion that "The specific name sauritus is New Latin, meaning lizardlike" is incorrect: sauros is Greek, not Latin, and the suffix –ita does not mean "like", but "little" (in Spanish). An obscure 5th-Century Greek dictionary by the lexicographer Hesychius, which is famous for being the only remaining source for a lot of ancient Greek words and would have been available to Linnaeus, lists "Saurita" as "a kind of serpent", settling the issue.

    The Truth About Snakebite

    Close-up of part of Liz Nixon's infographic
    Fear of snakes made the New York Times op-ed section this week in an insightful article about the way humans assess the relative risks of terrorism and climate change. Although I completely agree with the article's point, in my opinion the author missed an opportunity to emphasize how our fear of snakes, like our fear of terrorism, is way beyond the risk posed by either (especially in the USA). It was a bit frustrating for me to read an article that came so close to making the analogy that we fear snakes even though they are unlikely to do us harm, but instead used fear of snakes as an example of an urgent fear distracting us from more gradual, but ultimately more dangerous threats. It's a tricky subject, but I did like the comparison between the number of deaths in the USA from falling in the bathtub (464/year) vs. from a terrorist attack (17/year)—both more likely than death from venomous snakebite (5/year). Also, if you haven't seen it, check out the awesome infographic that scientific illustrator Liz Nixon made using some of the data in my snakebite post.

    Tetrodotoxin-resistant Snakes

    An Eastern Hog-nosed Snake eats a toad
    I rarely reference my own research on this blog, but last year I collaborated with Dr. Butch Brodie and members of his lab to publish some data on tetrodotoxin resistance in hog-nosed snakes (genus Heterodon). These snakes are well-known toad-eaters, but the few records of them eating newts were scattered until I brought them together in our new paper. Combined with molecular and whole-body resistance data, we showed that Eastern Hog-nosed Snakes from parts of upstate New York are more resistant to tetrodotoxin (TTX) than even the most resistant gartersnakes. But, Eastern Hog-nosed Snakes elsewhere are not as TTX-resistant, and Western Hog-nosed Snakes do not appear to be TTX-resistant at all. Most interesting, the mechanism of resistance appears to be something quite distinct from the conserved mutations in gartersnakes and other newt-eating snakes, and so far unknown.

    ACKNOWLEDGMENTS

    Thanks to David HerasimtschukPatti and Jack Sandow, and Pierson Hill for the use of their photos.

    REFERENCES

    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>

    Feldman, C. R., A. M. Durso, C. T. Hanifin, M. E. Pfrender, P. K. Ducey, A. N. Stokes, K. E. Barnett, E. Brodie III, and E. Brodie Jr. 2016. Is there more than one way to skin a newt? North American snakes with convergent feeding adaptations do not share a common genetic mechanism. Heredity 116:84-91 <link>

    Kraus, F. and H. D. Cameron. 2016. A note on the proper nomenclature for the snake currently known as Thamnophis sauritus. Herpetological Review 47:74-75

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    Even snakes have their charismatic megafauna

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    Bitis harenna
    From Gower et al. 2016
    Last year, I wrote about the 10,000th reptile and the 3,500th snake species to be described by scientists. The pace has not slowed down—as of its most recent update last week, The Reptile Database currently lists 3,596 species of snakes out of a total of 10,391 species of (non-avian) reptiles. A few weeks ago, the March 21st issue of the frequently-published journal Zootaxa (volume 4093, issue 1) included descriptions of three of these new snake species. What's interesting is that I initially looked this issue up because I saw one of them being shared a lot on social media—a new large species of viper. The other two, a pipesnake and a blindsnake, hadn't received as much attention. Zootaxa tweets all of their new species, and an examination of their feed shows that the viper tweet received 4 retweets and 2 likes, whereas the pipesnake and the blindsnake received 2 retweets and one like each (even though the pipesnake had a photo1 and was on the cover). Even though that's a small sample size, I think it's telling that even snakes have their charismatic megafauna.

    A bongo (Tragelaphus eurycerus, top)
    and a tiger (Panthera tigris, bottom).
    You only needed a caption for one
    It seems backwards, in a way, that the dangerously venomous viper should be more popular than the innocuous pipesnake. One conservation blogger, Corey Bradshaw, put it nicely by saying that "the only thing worse than being labelled deadly is not being called anything at all". Bradshaw pointed out that drawing attention to the potential for a species to cause harm to humans is not necessarily bad for the species in question. Even though snake biologists often decry these claims as exaggerated (usually because they are), Bradshaw wondered whether they are really very harmful. He suggested that people are generally more fascinated with animals that could kill us (even if they rarely do) than they are with entire groups of benign species, such as skinks or plethodontid salamanders, which are often considered boring (if a person is even aware of their existence). Compare tigers with, say, bongos. Both are critically endangered, inarguably gorgeous animals from exotic places. Tigers sometimes kill and eat people. Everyone knows a tiger. Most people think a bongo is a drum. Or, if you want a snake example, take rattlesnakes. Rattlesnakes are the Bald Eagles of snakes. They are distinctly North American. Everybody in North America knows them. One was on our flag. In contrast, the USA has never had a Smooth Greensnake (Opheodrys vernalis) on its flag, even though they are beautiful and North American and eat spiders. Perhaps the idea that any publicity is good publicity applies to conservation as well. Then again, perhaps not—many residents of Massachusetts are needlessly worried about a Timber Rattlesnake reintroduction plan on an island in the Quabbin Reservoir, probably in part because of the bad PR that rattlesnakes get on a regular basis. If the Massachusetts Division of Fisheries & Wildlife were reintroducing Smooth Greensnakes, I doubt that most people would care (and it certainly wouldn't have been the subject of such venomous debate in the media). Indeed, Illinois's Lincoln Park Zoo is reintroducing Smooth Greensnakes in Chicago, and nobody is writing letters to the editor about it (and, in a way, that's a shame, because it's an interesting and worthwhile effort).

    Letheobia mbeerensis
    From Malonza et al. 2016
    Anyway, I wanted to give some well-deserved press to the two less-publicized new snakes. The blindsnake, Letheobia mbeerensis, is pink with tiny, barely visible eyes. It was described from a single specimen collected southeast of Mt. Kenya in April of 2014 by a local farmer, who found it while tilling his fields. This person, whose name was not known to the scientists who wrote the article, made a considerable effort to get the snake identified—he traveled 125 miles from Siakago to Nairobi, where he gave the specimen to the Nairobi Snake Park, who forwarded it to herpetologists at the National Museums of Kenya. It is unique in having a relatively long tail (for a blindsnake), and in being found in a moist inland savanna. The other two Kenyan species of Letheobia, one of which was just described in 2007, are found in coastal lowlands with sandy soils. It is the 24th species of blindsnake known from Kenya, but I can guarantee that it won't be the last.

    Historical drawings of Cylindrophis ruffus
    Illustrations A-C from Scheuchzer 1735
    D-E from 
    Seba 1735
    From Kieckbusch et al. 2016
    The story of the new pipesnake is even more interesting, and I suspect the paper in which it is described will ultimately be the most read and most cited of the three snake papers in this issue. This is because, in addition to describing the new species, it contains "an overview of the tangled taxonomic history of C[ylindrophis] ruffus", a widespread species commonly known as the Red-tailed or Common Pipe or Cylinder Snake. The fourteen species of Asian Pipesnakes (family Cylindrophiidae) are secretive and semifossorial snakes with small eyes, bodies that barely taper at all, and ventral scales only slightly larger than or equal in size to their dorsal scales. Many have contrasting light and dark ventral blotching with conspicuous bright coloration on the underside of their short tail, which they expose when threatened. Scientific knowledge of these snakes predates modern biological nomenclature. One is pictured in Albertus Seba's Thesaurus, which was one of Linnaeus's main sources, although Linnaeus didn't include C. ruffus in either the 1758 or the 1766 edition of his Systema Naturae—instead, its first post-Linnaean description was written by Laurenti in 1768. Compared with other CylindrophisC. ruffus has a much larger distribution than any other species of Asian pipesnake. It's one of those species that is really a species complex—a group of closely related species that are very similar in appearance, to the point that the boundaries between them are often unclear. Other well-known examples include African House Snakes (Boaedon fuliginosus, formerly Lamprophis fuliginosus) and American Milksnakes (Lampropeltis triangulum). Often unusual populations of these species are described as separate species, but without extensive rangewide sampling it's easy to miss more subtle, clinal variation, especially when that variation is genetic rather than morphological. A recent revision of milksnakes split this wide-ranging species into several, and researchers have been working on African House Snakes as well. But no one has really examined Red-tailed Pipesnakes. Last year, a group of European and Indonesian researchers examined a large number of Cylindrophis museum specimens and discovered several specimens which did not fit any recognized species. But many of these specimens are old and some of their locations are uncertain. We don't have a lot of molecular data, and we have no specimens at all from many areas. And, no one has yet carried out a totally comprehensive review of the species complex (which really should encompass the entire genus, since the milksnake researchers found that some "milksnakes" were actually more closely related to mountain kingsnakes than they were to other milksnakes).

    Cylindrophis ruffus raising its tail "flag"
    Despite its re-description in 2015, Cylindrophis ruffus is still a species complex that suffers from a lot of complexity. Its morphology is highly variable. Its geographic range limits are unsettled. There is no type specimen. The original type locality (“Surinami”) is a hemisphere away, obviously an error, which complicates decisions about which populations of C. ruffus should get to keep that name and which should change. The 2015 paper, as the authors of this month's paper delicately put it, "contain[s] some inaccuracies, including descriptive errors, which unfortunately increase the complexity of an already intricate taxonomic situation". The researchers state that they are currently undertaking the kind of comprehensive review that I called for above, but that in the process they discovered a morphologically distinct population from central Java, which they describe as Cylindrophis subocularis in this paper. But the real value of this paper, in my mind, is the step-by-step description of the history of this snake, starting with its first depiction in 1735 and continuing to present day. I'll leave the gory details for those who are really interested (the full-text is available here), but suffice it to say that the story of Cylindrophis ruffus is much more interesting than I ever knew (it took almost 100 years to get the geography right), and far from over.



    1 Granted, it was a photo of a preserved specimen.


    ACKNOWLEDGMENTS

    Thanks to M. A. MuinNigel Swales and Marcus Meissner for the use of their photos.

    REFERENCES

    Amarasinghe, A. A. T., P. D. Campbell, J. Hallermann, I. Sidik, J. Supriatna, and I. Ineich. 2015. Two new species of the genus Cylindrophis Wagler, 1828 (Squamata: Cylindrophiidae) from Southeast Asia. Amphibian and Reptile Conservation 9:34-51 <link>

    Gower, D. J., E. O. Z. Wade, S. Spawls, W. Böhme, E. R. Buechley, D. Sykes, and T. J. Colston. 2016. A new large species of Bitis Gray, 1842 (Serpentes: Viperidae) from the Bale Mountains of Ethiopia. Zootaxa 4093:41-63 <link>

    Kieckbusch, M., S. Mecke, L. Hartmann, L. Ehrmantraut, M. O’Shea, and H. Kaiser. 2016. An inconspicuous, conspicuous new species of Asian pipesnake, genus Cylindrophis (Reptilia: Squamata: Cylindrophiidae), from the south coast of Jawa Tengah, Java, Indonesia, and an overview of the tangled taxonomic history of C. ruffus (Laurenti, 1768). Zootaxa 4093:1-25 <link>

    Malonza, P. K., A. M. Bauer, and J. M. Ngwava. 2016. A new species of Letheobia (Serpentes: Typhlopidae) from central Kenya. Zootaxa 4093:143-150 <link>

    Scheuchzer, J. J. 1735. Physica Sacra Iconibus Anaeis Illustrata, Procurante & Sumtus Suppeditante. Tomus IV. Augustae Vindelicorum et Ulmae, Ulm <link>

    Seba, A. 1734-1765. Locupletissimi rerum naturalium thesauri accurata descriptio, et iconibus artificiosissimis expressio, per universam physices historiam :opus, cui, in hoc rerum genere, nullum par exstitit. Apud Janssonio-Waesbergios & J. Wetstenium & Gul. Smith, Amstelaedami <link>

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    Rattlesnake Roundups Revisited

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    A chalkboard at the 2016 Sweetwater Rattlesnake Roundup,
    showing that a record number of pounds of snake had
    already been bought and sold by the second day, and that
    commerce was suspended on the third and fourth days of the
    event due to the massive surplus.
    Photo source unknown.
    At the 58th annual Sweetwater Rattlesnake Roundup this March, a record 24,481 pounds of rattlesnakes (about 25,000 individuals), primarily Western Diamond-backed Rattlesnakes (Crotalus atrox), were slaughtered. That's over four times the all-time average and about five times the recent average, breaking from a trajectory of slow decline at the few remaining rattlesnake roundups. The Sweetwater Jaycees attribute this year’s record catch to heavy rains, an explanation which might hold some water, but another probable contributing factor is the possibility of an impending Texas Parks & Wildlife ban on using gasoline fumes to collect rattlesnakes, which was discussed this week at a meeting in Austin on May 25th, 2016. The Texas Parks and Wildlife Commission decided to begin developing language for a new rule either prohibiting or further regulating this practice in the state. The rule is still far from going into effect, and would include a two-year delay on the effective date. It won't be reviewed again until November 2016 (at which time, watch this space for a link to an opportunity for a public comment, if available). TPWD's Snake Harvest Working Group recommended earlier this year that Texas join 29 other states in banning this environmentally-harmful practice, which has been shown to kill numerous non-target species and has been compared with other unsportsmanlike methods of hunting, such as shooting at an out-of-range bird or fishing with dynamite. The state wildlife agency has been moving slowly but steadily to regulate rattlesnake collection in Texas because of the economic importance of rattlesnake roundups to towns like Sweetwater (e.g., over 25,000 people contributed over $8 million to the local economy in 2015, although the TPWD report found that the weather and the diversity of other events had stronger associations with profits than the number of rattlesnakes at an event).

    Locations of the remaining rattlesnake roundups,
    including non-lethal festivals.
    From TPWD Report Reference Document (p. 22)
    Ironically, this year's surplus of snakes drove the price of rattlesnake down so much (historically as high as $10.00 per pound, this year the price fell below $0.50/lb. despite efforts to maintain higher prices) that only about a quarter of the rattlesnakes collected were purchased for their meat, rattles, and skins before all demand had been exhausted. Rattlesnakes collected using gassing are no longer purchased by the antivenom industry, because of their short lifespan and poor health (as well as a more nuanced understanding of the importance of geographic variation in venom composition, emphasizing the necessity of knowing the geographic origin of each snake used in venom research). The fate of the rattlesnakes left unsold after Sweetwater (which some have speculated as being up to 75,000) has not been made public, although reports suggest that prices are also down at other roundups in Texas and Oklahoma, possibly as a result of vendors trying to sell their snakes there. Anyone who has gone to great expense to collect snakes in this manner and now cannot find a buyer is at risk of losing their investment. Claims about the impacts on snakebites to humans and livestock if these snakes were to be released are unsubstantiatable and untrue, considering that the survival of wild snakes captured and released elsewhere is greatly reduced (not to mention the dubiousness of the link between rattlesnake abundance and snakebite frequency in the first place).

    Trajectory of profit (red, blue), number of snakes (purple), and
    weather conditions (green) at the Sweetwater Roundup over the last decade.
    Chart prepared by Rob Denkhaus, TPWD Wildlife Diversity Advisory Committee
    and presented in TPWD Report Reference Document (p. 64)
    I am hopeful that eventually all stakeholders can overcome the cognitive dissonance between the flawed concept of predator population control (which was the original impetus behind rattlesnake roundups) and the implicit economic reasons behind their persistence. Although rattlesnake roundups are inarguably sensational and exploitative, claims about the sustainability of the wild rattlesnake harvest cannot currently be independently evaluated (I encourage anyone interested in the subject to read my previous article and check out this well-researched book). But, increasing oversight by Texas wildlife agencies could allow them or others to monitor the effect of the harvest on rattlesnakes, which could lead to valuable insights into snake biology and help prevent economic and environmental disasters like this year's Sweetwater roundup. This week's decision inches us towards the hopeful possibility of a sustainable snake harvest that could, over time, change the relationship between humans and western diamondbacks into a positive one, similar to our view of white-tailed deer, bobwhite quail, or largemouth bass. It's a non-traditional model for snake conservation, to be sure, but the efforts of the TPWD Snake Harvest Working Group combined with actions being taken by some unlikely allies, such as roundup organizer Jackie Bibby, will hopefully continue to move us towards a common goal of respectfully managing rattlesnakes as either game or non-game wildlife and not as pests. The best part: we can help people in the process (e.g., by providing healthier products with stable prices, such as rattlesnake meat untainted with gasoline).


    Percentage of time radio-tracked Burmese Pythons spent
    fully concealed (black), partly visible (gray), and mostly visible (white).
    In nineteen 30-minute searches of a 30 x 25 m enclosure containing
    ten pythons, only two pythons were detected out of
    190 possible detection opportunities.
    From Dorcas & Willson 2013
    And—as if the irony weren't already thick enough—compare the above totals with the ~2000 lbs. of Burmese Python (106 snakes) collected in Florida this year as part of an Florida Fish and Wildlife Conservation Commission-sponsored contest to control a snake whose populations actually do need to be "controlled" (despite the near-total impossibility of doing so). Among the several reasons for the difference include the lack of cultural inertia promoting snake hunting in Florida, the challenging habitat of the Everglades, and the snakes' biology—pythons don't aggregate the way rattlesnakes do. If gassing is banned in Texas, flushing rattlesnakes out of their hibernacula en masse will no longer be a legal hunting strategy. Does this mean that rattlesnake roundup totals will become more like those of the Python Challenge? Not necessarily—the TPWD report references alternative strategies already in use in other parts of the country that can still yield hundreds of pounds of rattlesnakes. Would a change in the hunting methods allowed have positive effects on snakes and other wildlife? Almost certainly. What would be the impacts on the roundup? I think it's worth pointing out that many former roundups, such as the Claxton Rattlesnake Festival in Claxton, Georgia, hosted by the Evans County Wildlife Club, and the Fitzgerald Wild Chicken Festival in Fitzgerald, Georgia, still generate economic opportunity for their towns without collecting and killing wild snakes. I think it's quite likely that events like the Sweetwater Rattlesnake Roundup could continue to bring benefits to their communities without using gas to extract rattlesnakes from their dens.

    ACKNOWLEDGMENTS

    Thanks to Ray Autry and Dale Burton from the Rise Against Rattlesnake Roundups Facebook group for pointing me to some resources about the 2016 Sweetwater Roundup.

    REFERENCES

    Adams, C.E. and J.K. Thomas. 2008. Texas Rattlesnake Roundups. Texas A&M University Press, College Station, Texas <link>

    Arena, P. C., C. Warwick, and D. Duvall. 1995. Rattlesnake Round-ups. Pages 313-324 in R. L. Knight and K. Gutzwiller, editors. Wildlife and Recreationists. Island Press, Washington, DC <link>

    Campbell, J. A., D. R. Formanowicz Jr, and E. D. Brodie Jr. 1989. Potential impact of rattlesnake roundups on natural populations. Texas Journal of Science 41:301-317.

    Dorcas, M. E., and J. D. Willson. 2013. Hidden giants: problems associated with studying secretive invasive pythons. Pages 367-385 in W. I. Lutterschmidt, editor. Reptiles in Research. Nova Biomedical, New York, New York <link>

    Elliott, W. R. 2000. Conservation of the North American cave and karst biota. Pages 665-689 in H. Wilkens, D. Culver, and W. Humphreys, editors. Subterranean Ecosystems. Elsevier, Amsterdam.

    Jackley, A. M. 1939. Rattlesnake Control and Conservation. South Dakota Conservation Digest 6:11.

    Margres, M. J., J. J. McGivern, M. Seavy, K. P. Wray, J. Facente, and D. R. Rokyta. 2015. Contrasting modes and tempos of venom expression evolution in two snake species. Genetics 199:165-176 <link>

    Reinert, H., and R. Rupert. 1999. Impacts of translocation on behavior and survival of Timber Rattlesnakes, Crotalus horridus. Journal of Herpetology 33:45-61 <link>

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

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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.

    Virgin Birth, the Color of Fossil Snakes, and More Recent Updates

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    This post will soon be available in Spanish

    As I did in March, I wanted to highlight some recent and exciting updates to some of my older articles.

    Snakes That Give Virgin Birth

    Phylogenetic pattern of parthenogenesis in snakes
    Molecular tree on left, morphological tree on right
    From Booth & Schuett 2016
    When I wrote about asexual reproduction in snakes in February 2014, new records of this phenomenon were rapidly accumulating, from snakes as distantly related as cottonmouths and boa constrictors. In a new paperWarren Booth and Gordon Schuett review the knowns and unknowns of "virgin birth" in snakes, a subject which has become their specialty (it even has its own Facebook group). Although obligate parthenogenesis is still known only from Brahminy Blindsnakes (Indotyphlops braminus), the new summary reports that facultative parthenogenesis has now been documented in 20 species of alethinophidian1 snakes, and this list is anticipated to grow, although so far confirmed cases are limited to five lineages: boids, pythonids, Acrochordus, Crotalinae, and Natricinae. This new synthesis formalizes one of the trends that I wrote about in 2014, namely distinguishing between "Type A" facultative parthenogenesis, in which the offspring produced are large clutches of viable females that seem to have a strange "WW" sex chromosome arrangement (apparently typical of boas and pythons), and "Type B" facultative parthenogenesis, which is where all the offspring are male and few are born alive, many with extreme developmental abnormalities (apparently typical of colubroids).

    Most intriguing is the hypothesis laid out for explaining this dichotomy: that boas and pythons (and possibly other basal alethinophidian snakes) might have an XY sex determination system rather than a ZW one like most snakes. Changes from ZW to XY or vice versa (and between genetic and temperature-dependent sex determination) have been documented in geckos and turtles, and could have been overlooked in boas and pythons due to their similar-looking sex chromosomes (tests are currently underway to falsify or verify this hypothesis). If true, this would explain the production of all-female offspring by facultative parthenogenesis; instead of WW, those females would be XX, just like humans!

    Identifying Snake Sheds

    True-color representation of the fossil snake
    (MNCN 66503) in McNamara et al. 2016.
    The dentition looks too solenoglyphous for a
    colubrid, although the 10-million year old specimen,
    which is missing its head, has not and
    probably can not be identified to species.
    Ever since the first reports of color from the skin and feathers of dinosaur fossils were published in Science in 2010, I've been fascinated by the ability of paleontologists to see in color when they look into the past. A new paper in the journal Current Biology reveals the color of a fossil snake, determined from using scanning electron microscopy (SEM) to examine microfossils of certain types of skin cells, called chromatophores. So far, only melanin-based chromatophores (melanosomes, which are responsible for brown and black color) have been detected in fossilized skin and feathers, probably because they are the most resistant to the decomposition process. But, this study was also able to detect and measure other types of chromatophores from fossilized skin, including xanthophores (responsible for yellow, orange, or red color, derived from carotenoids or pteridines) and iridophores (responsible for iridescence). By comparing the fossil's chromatophore abundance and position to that of living reptiles, they were able to reconstruct the original color and pattern of the fossil snake's skin. For example, in the skin of living snakes, xanthophores with many more pteridine granules than carotenoid granules produce a red hue, whereas xanthophores with equal amounts of carotenoid granules and pteridine granules—as in the fossil—produce yellowish hues. Skin regions with abundant iridophores and xanthophores, but relatively few melanophores, are associated with green hues in some living skinks, whereas skin regions with many melanophores, a few xanthophores, and no iridophores suggest correspond to dark brown or black tones. As you can see in the depiction, this snake seems to have had a pale, creamy venter and a green back and sides, with areas of brown/black and yellow/green, perhaps not unlike modern Green Watersnakes (Nerodia floridana) or Boomslangs (Dispholidus typus).

    Snakes Flying Without Planes

    Photo and diagram of courtship behavior of Chrysopelea paradisi
    Taken at the Sepilok Jungle Resort in Sabah, Malaysia
    Female shown in gray, males in blue, green, and orange
    From Kaiser et al. 2016
    A new report on the mating behavior of Paradise Flying Snakes (Chrysopelea paradisi) showed that their courtship can involve multiple males. Although several experiments have been performed on the gliding behavior of these snakes, almost nothing is known about their natural history in the wild. Males of many species of snakes court females en masse by rubbing their chins along their bodies, a behavior which allows them to sense her sex pheromones and jockey for position. The role played by the female in choosing a male is unclear in most snake species; although conventional biological wisdom suggests that females should be the choosy sex, male-male competition seems to dominate courtship behavior in several species of snakes. Multi-male courtship behavior precedes mating in some well-studied temperate snakes (e.g., gartersnakes emerging from hibernation), as well as in some tropical species (e.g., anacondas, some other southeast Asian colubrids, such as Boiga irregularis and Dryophiops rubescens). Of course, it seems that most female snakes can store sperm for long periods of time, and they may have some control over which male's sperm to use to fertilize their eggs, so the genetic contribution of a female snake's male partners may not follow from their courtship or mating success. Unlike the terrestrial or aquatic mating balls documented for other snakes, the flyingsnakes in this observation were able to move as a unit for almost 50 feet through complex habitat—under a porch, up a tree—an adaptation that seems to fit their active, arboreal lifestyle and might help reduce the likelihood of a predatory attack during what must otherwise be a vulnerable time.



    1 In a few places, the authors use "alethinophidian" to refer to boas, pythons, and their relatives but not caenophidians, when instead they should have either used "henophidian" or "basal alethinophidian" (they mostly use the latter term throughout). Many people don't like the term "henophidian" because it is a paraphyletic group, but it is a convenient way to refer to non-scolecophidian, non-caenophidian snakes. In my mind it's essentially synonymous with "basal/stem alethinophidian". Alethinophidians are all snakes except for blindsnakes (scolecophidians), and Caenophidia is a subset of Alethinophidia. There are also at least three references to "Caenophidia + Colubroidea", which is confusing because Colubroidea is a subgroup of Caenophidia, and Caenophidia = Colubroidea + Acrochordus, which is perhaps what they meant.

    ACKNOWLEDGMENTS

    Thanks to Gordon Schuett for clearing up some of the details of his recent paper.

    REFERENCES

    Booth W, Schuett GW (2016) The emerging phylogenetic pattern of parthenogenesis in snakes. Biological Journal of the Linnaean Society 118:172-186 <link>

    Gamble, T., J. Coryell, T. Ezaz, J. Lynch, D. Scantlebury, and D. Zarkower. 2015. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Molecular Biology and Evolution 32:1296-1309 <link>

    Kaiser H, Lim J, Worth H, O’Shea M (2016) Tangled skeins: a first report of non-captive mating behavior in the Southeast Asian Paradise Flying Snake (Reptilia: Squamata: Colubridae: Chrysopelea paradisi). Journal of Threatened Taxa 8:8488–8494 <link>

    Kuriyama, T., K. Miyaji, M. Sugimoto, and M. Hasegawa. 2006. Ultrastructure of the Dermal Chromatophores in a Lizard (Scincidae: Plestiodon latiscutatus) with Conspicuous Body and Tail Coloration. Zoological Science 23:793-799 <link>

    Li, Q., K. Q. Gao, J. Vinther, M. D. Shawkey, J. A. Clarke, L. D’Alba, Q. Meng, D. E. G. Briggs, and R. O. Prum. 2010. Plumage color patterns of an extinct dinosaur. Science 327:1369 <link>

    McNamara, Maria E., Patrick J. Orr, Stuart L. Kearns, L. Alcalá, P. Anadón, and E. Peñalver. 2016. Reconstructing Carotenoid-Based and Structural Coloration in Fossil Skin. Current Biology <link>

    McNamara, M. E., D. E. G. Briggs, P. J. Orr, D. J. Field, and Z. Wang. 2013. Experimental maturation of feathers: implications for reconstructions of fossil feather colour. Biology Letters 9 <link>

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    What the Provincial Snakes of Canada Should Be

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    In case, like many Americans, you need a map
    Happy Canada Day! And indeed there is a lot to celebrate, in particular Canada's new liberal government and the positive effects it has had on science and the environment. Three summers ago, I wrote in two parts (I and II) about what the symbolic snakes of each of the US states should be, inspired by the witty and spot-on post 'The State Birds: What They SHOULD Be' from thebirdist.com. In response to a tweet from Canadian Field Naturalist, a journal that publishes ecology, behaviour, taxonomy, conservation, and other topics relevant to Canadian natural history, and because Canadian provinces also have various representative symbols (none reptilian, except for the feathered kind, which I might add are somewhat better chosen than those of the US states), this summer I decided to cover the US's northern neighbor as well. Does Canada even have any snakes, you might ask? In fact, Canada is home to 27 species of snake, which might surprise those of us who have grown up in regions farther south. That's enough for every province and territory to have two provincial snakes, with one left over, although the uneven geographic distribution of species precludes that, as we'll see. I followed the same "no duplication" rule as I did for the State Snakes, but I allowed snakes that had been used as U.S. State Snakes to be used again, because almost all of the species found in Canada had also been used for a U.S. state. Feel free to chime in with your opinion about what your favorite province's snake should be, if it differs from my choice.

    1. Alberta. Prairie Rattlesnake (Crotalus viridis)


    Prairie Rattlesnake (Crotalus viridis)
    Alberta, well-known for its dinosaurs, also harbors a fairly substantial diversity of modern reptiles for a place with such long winters. Seven species of snake can be found in the province, but perhaps the most quintessential are Prairie Rattlesnakes. Prairie Rattlesnakes in Alberta occur in shortgrass prairies, dry grasslands, and sagebrush in the southeastern part of the province. At the northwestern edge of their range, Prairie Rattlesnakes in Alberta take 5-8 years to reach sexual maturity, and give birth to 4-12 live young, which are quite large (~11" long; compared to ~9" in the more southerly parts of their range). Females may remain with their young for up to 10 days after giving birth. Historically, Prairie Rattlesnakes were found as far west as Calgary and almost as far north as Red Deer, but the species has declined in many areas due to persecution and habitat loss. Venomous snakes are rarely very popular, but provincial symbol-hood might help establish rattlesnakes as wildlife to be valued rather than pests to be exterminated (and Alberta is already quite progressive about protecting its snakes).

    2. British Columbia. Sharp-tailed Snake (Contia tenuis)


    Sharp-tailed Snake (Contia tenuis)
    BC might be my favorite province, principally because of the Nanaimo Bar, a three-layer no-bake dessert created in the eponymous coastal city of Nanaimo. I chose the Sharp-tailed Snake to represent BC because in some ways it resembles a reversed Nanaimo Bar—the dorsal coloration is similar to the graham-cracker-and-almond base, the color of the sides to the vanilla custard center (sort of), and the belly to the delectable chocolate-and-coconut topping. These snakes are found on Vancouver Island, the nearby Gulf Islands, and possibly on the adjacent mainland. These cute little snakes eat slugs, including the infamous banana slugs, which I bet don't taste anywhere near as good as Nanaimo Bars. Descriptions of Sharp-tailed Snakes were first published in 1852 (by herpetologists Spencer Fullerton Baird & Charles Frédéric Girard, who received collections made the decade before in the Puget Sound area), exactly 100 years before the first printed recipes featuring Nanaimo bar ingredients were published in the Women's Auxiliary to the Nanaimo Hospital Cookbook (although I'll admit that's a pretty tenuis connection).

    3. Manitoba. Western Hog-nosed Snake (Heterodon nasicus)


    Western Hog-nosed Snake (Heterodon nasicus)
    Even though Manitoba is very well-known for its Narcisse Gartersnake Dens, it has greater snake diversity than several of the other provinces, for which the gartersnake must be reserved. Some of Manitoba's most interesting snakes are Western Hog-nosed Snakes, which are found in sandy areas in the southwestern part of the province. As with other snakes at the northern limits of their range, they have a short activity season—they mate in May and lay 5-12 eggs in late June or early July, which then hatch by August. A study of Western Hog-nosed Snakes in Spruce Woods Provincial Heritage Park, Manitoba, found that they emerge from their burrows on any day when they could achieve a body temperature of at least 29°C (84°F). Like gartersnakes (though not quite to the same extent), these snakes can achieve fairly high densities in certain areas, so I think they could be good candidates for expanding our knowledge of snake ecology and behavior in the wild into phylogenetically-uncharted territory, challengingthe statement made by Rick Shine in 1987 that "It's a good thing you Yanks have garter snakes, or you wouldn't have anything to study."

    4. Newfoundland & Labrador. Maritime Gartersnake (Thamnophis sirtalis pallidulus)


    Maritime Gartersnake (Thamnophis sirtalis pallidulus)
    Newfoundland and Labrador is the only Canadian province without any native snakes. However, in recent years southwestern Newfoundland in the vicinity of St. David's has apparently been colonized by Maritime Gartersnakes, a beautiful subspecies of Common Gartersnake. Although no genetic analyses have been performed, it's likely that this population was founded by individuals shipped across the Gulf of St. Lawrence in hay bales or other cargo from Québec, New Brunswick, Nova Scotia, or Prince Edward Island. A poll by the CBC revealed that 12% of respondents thought that the recent colonization was "actually kind of cool", whereas a discouraging 49% of respondents were "not happy about it at all". It's rumored that gartersnakes were purposefully but unsuccessfully released in the St. John's area in eastern Newfoundland decades ago, either by farmers hoping to control rat populations or by someone who brought them back from the mainland hoping to sell them as pets (though both scenarios are likely more urban legend than fact). A string of recent mild winters may have allowed the gartersnakes in western Newfoundland to persist, but the extent to which climate change will enable a Florida-pythons scenario writ-small in Newfoundland remains to be seen. At the very least, this could be a golden opportunity for snake biologists to study what happens when snakes enter an ecosystem from which they have been absent for thousands of years, a rare event even in an age of snake invasions.

    5. New Brunswick. Smooth Greensnake (Opheodrys vernalis)


    Smooth Greensnake (Opheodrys vernalis)
    Soctsman Andrew Leith Adams was an army physician who served in India, Egypt, and Canada during the 1800s. He spent his spare time studying the natural history of these countries, about which he later wrote several books, including his 1873 Field and forest rambles, with notes and observations on the natural history of eastern Canada. In it, he wrote "The Reptiles of New Brunswick are neither numerous nor formidable.", which, compared with the snake fauna he doubtless experienced in Egypt and India, was certainly true. He mentioned several snake species, in particular noting that "One of our most common fangless snakes is the active little green species (C. vernalis)", using the C. to abbreviate the genus Coluber, which Linnaeus had used for practically all snakes except boas and rattlesnakes. This handsome species has also frequently gone by the binomial Liochlorophis vernalis, among a half-dozen other genera into which it has been placed over the years.

    6. Northwest Territories. Red-sided Gartersnake (Thamnophis sirtalis parietalis)


    Mating ball of Thamnophis sirtalis parietalis
    Red-sided Gartersnakes are the only snakes found in the Northwest Territories, where they achieve high densities near Fort Smith between the southern shore of the Great Slave Lake and Wood Buffalo National Park. Because there are few suitable hibernacula, thousands of individuals share the same den. Long winters and short, cool summers have resulted in a mating system that is unusual among snakes, although it is also possibly the most well-known because it is easily studied. Upon emergence from the in mid-April, snakes spend 2-3 weeks hanging around the entrance, during which time males compete fiercely to mate with females, forming colossal "mating balls". They then migrate over 2.3 miles (3.75 km) to their summer marshland habitat, where they remain until late August, giving birth to litters of young that are relatively small in number (~12 vs. ~19 in Manitboa) and large in body size (191 mm SVL vs. 154 mm in Manitoba). Females in the NWT rarely give birth in two successive years, instead saving up energy from one year in order to reproduce the next. They also mature at larger body sizes (570 mm SVL vs. 527 mm in Manitboa) than snakes further south. I bent the rules a little here since both Newfoundland and the NWT have only T. sirtalis (they have different subspecies, and this species might be split up fairly soon). 

    7. Nova Scotia. Ring-necked Snake (Diadophis punctatus)


    Brown-morph and normal Diadophis punctatus from Nova Scotia
    From Gilhen 2011
    Ring-necked Snakes are cute little snakes that mostly eat invertebrates, although they have been known to snack on the occasional salamander. In Nova Scotia, they can be found almost throughout the province, and an unusual brown morph occurs, particularly on Big Tancook Island in Mahone Bay along the east coast. According to the notebooks of Harry Piers, an early 20th century naturalist, museum curator, and historian, ringnecks were known to the native Mi'kmaq People as “the worst snake, Um-taa-kum (k)”, although it's not clear why. One communal nest found under a boulder near McCabe Lake in Halifax County contained 117 eggs, which must have been laid by at last 15, and probably many more, females (clutch size ranges from one to eight).

    8. Nunavut. Ellesmere Island erycine (Eocene boa)

    Drawing of Ellesmere Island erycine vertebra
    Dotted lines show best-guesses at broken-off parts
    A. Dorsal and B. right lateral view
    From Estes & Hutchison 1980
    Unfortunately, there are no living wild snakes in Nunavut. Initially I was going to get around this by writing only about the true provinces, but then I found evidence that a 50-million-year-old fossil snake vertebrae was found on Ellesmere Island, above the Arctic Circle at about 78.5° north (find it here at the awesome new Paleobiology Database Navigator). This vertebra belonged to an undescribed species of boid snake probably related to rubber boas, and it was found in an Eocene fossil deposit that used to be a lush river delta and floodplain, with abundant swamps, alongside pike, bowfin, and gar, mud & softshell turtles, alligators, monitor lizards, giant salamanders, and even primates. The single bone is part of the collection of the Canadian Museum of Nature (specimen number 32403) and hasn't been assigned to a species or even a genus because it's broken. Paleontologists are fairly confident that it is an erycine boid based on comparisons made with a half-dozen other extinct genera that probably belong in this group. Recent phylogenies of booids elevate Erycinae to a family, but do not include extinct taxa, so it's difficult to say for sure how these snakes were related to each other and to living species.

    9. Ontario. Eastern Foxsnake (Pantherophis vulpinus)

    Eastern Foxsnake (Pantherophis vulpinus)
    Ontario has more snake species to choose from than any other province, including seven that are found nowhere else in Canada. At the JMIH meeting in Reno last summer, I posed the question of which one best represented Ontario to herpetologist Jacqueline Litzgus, a native of Ontario and a professor at Laurentian University. She was unhesitant in recommending the Eastern Foxsnake, the only species of snake whose range is mostly in Canada (which perhaps makes it sort of a national snake as well, although the common gartersnake is found in more provinces). Foxsnakes are large constrictors that are closely related to cornsnakes and (slightly less closely) to ratsnakes. They probably recolonized northern North America more quickly after the retreat of the glaciers than most snakes because of their mobility and the flat terrain left behind in the midwest. We once thought that the two species had a disjunct range, with the western foxsnake (formerly P. vulpinus) being found in the USA between the Missouri River and Lake Michigan, separated by a foxsnake-less area in northeastern Indiana and the lower peninsula of Michigan from the eastern foxsnake (formerly P. gloydi), which was found south and east of Lake Huron in Ontario, Michigan, and Ohio. However, a 2011 study used evidence from a single mitochondrial gene to suggest that the Mississippi River seemed to be a more significant genetic barrier and that western foxsnakes east of the Big Muddy in Wisconsin and Illinois were more closely related to eastern foxsnakes than they were to western foxsnakes in Iowa and Minnesota. Because the type specimens for both former foxsnake species were within the eastern lineage, this species became P. vulpinus (the older name), P. gloydi disappeared, and the "new" western foxsnake was named P. ramspotti. Runner up: Massasauga (Sistrurus catenatus), because of the town of Missisauga, Ontario.

    10. Prince Edward Island. Red-bellied Snake (Storeria occipitomaculata)

    Red-bellied Snake (Storeria occipitomaculata)
    Located in the Gulf of St. Lawrence, Prince Edward Island was formed as a sandstone peninsula 250-300 million years ago. The end of the ice age 15,000 years ago and the retreat of the glaciers laid down glacial till and increased the sea level, disconnecting PEI from the mainland. PEI only has three species of snakes, all of which colonized the island within the last 15,000 years. Despite the fact that no lizards or turtles have been able to make the same crossing, PEI is still way ahead of Québec's similarly-sized Île d'Anticosti, which lies ~190 miles (~300 km) to the north and has no native species of amphibians or reptiles. Of the tiny red-bellied snake, PEI naturalist John Mellish wrote in the 1870s "This variety is numerous, is smaller in size, and seems to be less courageous than some of the other species". Although Mellish got this much right, he was as prone to exaggeration as many modern observers, interspersing his species accounts with tales of snakes charming their prey, swallowing their young, and attacking people. In reality, red-bellied snakes mostly attack slugs, and their peculiar lip-curling display is hardly threatening to a human.

    11. Québec. Milksnake (Lampropeltis triangulum)


    Milksnake (Lampropeltis triangulum)
    Québec is best emblematized by the Milksnake, which was first described by a French herpetologist, Bernard Germain de Lacépède, in 1789. Lacépède's two-volume masterpiece, Histoire Naturelle, is a classic work in herpetology. Although Lacépède mostly used French vernacular names,  ("le triangle" for the milksnake, after the double triangles on top of its head), he used Linnaeus's Latin binomial system about 65% of the time in a 59-page table in the third section of the second volume, which covered legless amphibians and reptiles. However, because he was not consistent in his use of Latin binomials, the taxonomic community decided in 1987 that the names in volume two were not valid (volume one, which covers turtles, lizards, and amphibians, contains a 3.5' x 1.75' fold-out table that was consistently binomial, so these names remain valid). Four snake names, including Lampropeltis triangulum, were rescued because of their long history of use. The other three (Agkistrodon piscivorus, Langaha madagascarensis, and Python reticulatus) were much longer-used than L. triangulum, which probably wouldn't have made the cut if not for an earlier decision by the ICZN as part of a case involving the mistaken identity of Linnaeus's scarletsnake (Cemophora coccinea) specimen and the name he gave it, Coluber doliatus, which was mistakenly used for the milksnake for over 150 years. The 1967 case invalidated doliatus and fixed triangulum as the specific epithet of the milksnake, which prevented it from later being invalidated with the rest of Lacépède's snake names. In this way the species is somewhat rebellious (in a nomenclatural sense), which I think would please many Québécois.

    12. Saskatchewan. Gophersnake (Pituophis catenifer)

    Gophersnake (Pituophis catenifer)
    On the first page of one of my favorite novels, Farley Mowat's Owls in the Family, the author describes growing up in Saskatoon, Saskatchewan: "When you stepped off the end of the Railroad Bridge you stepped right onto the prairie and there you were—free as the gophers. Gophers were the commonest thing on the prairie. The little mounds of yellow dirt around their burrows were so thick, sometimes, it looked as if the fields had yellow measles."Although I like owls, these days I more often have another gopher predator in mind—the eponymous gophersnake (Pituophis catenifer), also less-aptly known as the bullsnake. These harmless creatures are often mistaken for rattlesnakes, because they have a superficially similar pattern (and they do rattle their tails, although they have no specialized noise-making structure). Confusion over the common name led Edward Abbey or one of his editors to include the scientific name of the eastern indigo snake (aka the blue gophersnake), Drymarchon corais couperi, for the bullsnake in the essay 'The Serpents of Paradise' in the 1968 edition of Desert Solitaire (although it is correct in 1988 edition).

    13. Yukon. ?

    I hope they find a snake
    The Yukon Territory has no living snakes and no snake fossils (yet). This is actually quite ironic, because most living North American snakes crossed into our continent from Asia over the Bering Land Bridge, and some of them almost certainly slithered through what is today the Yukon. It is possible that somewhere in the southern Yukon exists a population of gartersnakes, which are found in the southern NWT and also possibly in the Alaskan panhandle. Three reliable sight records and one specimen (now lost) from remote areas along Taku & Stikine Rivers in Alaska give us hope, although unfortunately neither basin enters the Yukon. Other snake sightings of snakes from Alaska include odd T. sirtalis and T. ordinoides specimens from more urban areas, which almost certainly represent translocations (genetic evidence supports this in at least one case). T. sirtalis are found just 200 miles (320 km) south of the Yukon border in BC. It isn't completely crazy to imagine snakes living at such northerly latitudes; European Adders (Vipera berus) are found above the Arctic Circle in Scandinavia. If nothing else, gartersnakes from British Columbia will probably disperse there eventually if climate change keeps up with predictions.

    ACKNOWLEDGMENTS

    Thanks to David O'Connor, JD Willson, Todd Pierson, Andy Teucher, Michael, Gary Nafis, and Nick Scobel for the use of their photos, to Jackie Litzgus for helping me make the decision about Ontario, and to Gareth Hopkins for introducing me to Nanaimo bars.

    REFERENCES

    Manitoba Thamnophis on the side of a U-Haul truck
    Anonymous. 1987. Opinion 1463. De Lacépède, 1788-1789, Histoire Naturelle des Serpens and later editions: rejected as a non-binominal work. Bulletin of Zoological Nomenclature 44:265-267 <link>

    Baird, S.F. and C. Girard. 1852. Descriptions of new species of reptiles, collected by the U.S. exploring expedition under the command of Capt. Charles Wilkes, U.S.N. First part. - Including the species from the Western coast of America. Proceedings of the Academy of Natural Sciences of Philadelphia 6:174-177 <link>

    Brongersma, L.D. 1972. On the “Histoire naturelle des Serpens” by de la Cépède, 1789 and 1790, with a request to reject this work as a whole, and with proposals to place seven names of snakes, being nomina oblita, on the Official index of rejected and invalid names in zoology, and to place three names of snakes on the Official list of specific names in zoology (Class Reptilia). Bulletin of Zoological Nomenclature 29:44-61 <link>

    Crother, B.I., M.E. White, J.M. Savage, M.E. Eckstut, M.R. Graham, and D.W. Gardner. 2011. A reevaluation of the status of the Foxsnakes Pantherophis gloydi Conant and P. vulpinus Baird and Girard (Lepidosauria). ISRN Zoology 2011 <link>

    Estes R, Howard Hutchison J, 1980. Eocene lower vertebrates from Ellesmere Island, Canadian Arctic Archipelago. Palaeogeography, Palaeoclimatology, Palaeoecology 30:325-347 <link>

    Gilhen, J. 2011. The Brown Morph of the Northern Ringneck Snake, Diadophis punctatus edwardsii, on Big Tancook Island, Mahone Bay, Nova Scotia. The Canadian Field-Naturalist 125:69-71  <link>

    Hodge, R.P. 1976. Amphibians and Reptiles in Alaska, the Yukon, and Northwest Territories. Alaska Northwest Pub. Co.

    Larsen KW, Gregory PT, Antoniak R, 1993. Reproductive ecology of the Common Garter Snake Thamnophis sirtalis at the northern limit of its range. American Midland Naturalist 129:336-345 <link>

    Leavesley, L.K. 1987. Natural history and thermal relations of the Western Hognose Snake (Heterodon nasicus nasicus) in southwestern Manitoba. MS thesis. University of Manitoba, Winnipeg, Manitoba.

    Rossman, D.A., N.B. Ford, and R.A. Seigel. 1996. The Garter Snakes: Evolution and Ecology. University of Oklahoma Press, Norman, Oklahoma. (Shine quote opens chapter 4, page 55)

    West, R.M., M.R. Dawson, and J.H. Hutchison. 1977. Fossils from the Paleogene Eureka Sound Formation, N.W.T., Canada; occurrence, climatic and paleogeographic implications. Milwaukee Public Museum Contributions in Biology and Geology 2:77-93.

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    Why snakes are long (and other recent updates)

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    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 with 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.

    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>

    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>

    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>

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    Xenophidion: The Snake with the Mystery Penis

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    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 acanthognathusmentions 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-Reptilia16:229-240 <link>

    Lawson, R., J. B. Slowinski & F. T. Burbrink. 2004. A molecular approach to discerning the phylogenetic placement of the enigmatic snake Xenophidion schaeferiamong the Alethinophidia. Journal of Zoology263:285-294 <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-Reptilia19:385-405 <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>

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

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    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>

    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.

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

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    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.

    Life is Short but Snakes are Long 2016 Milestones

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    Dear reader,

    Screenshot from 15 November showing Blogger's estimate
    that Life is Short but Snakes are Long reached one million
    views, which is probably a bit too optimistic.
    As I did last year, I want to thank you for your readership in 2016. Life is Short but Snakes are Long reached three-quarters of a million unique views on September 6th this year, by over 430,000 unique readers from nearly every country. We're currently over 860,000 views and on track to reach one million in 2017. The more liberal Blogger statistics show that we're already at one million, but I suspect that many of these are bots, and I'm sticking with the more conservative estimates provided by Google Analytics. I'm so happy to have reached so many people. Furthermore, at least 34 new species of snakes were described in 2016.

    In addition to defending my dissertation and moving to Germany in 2016, I also published 5 scientific papers and co-authored a book chapter for the new 3rd edition of Mader's Reptile Medicine and Surgery, on the behavior of reptiles and amphibians, which will be published in 2017. I became a lot more active in the Facebook Snake Identification and Wild Snakes: Education and Discussion groups, which are fantastic resources for quick, reputable answers to questions about snakes. I recently accepted a position as an Associate Editor of the Snake Natural History Notes section at the journal Herpetological Review, and I was invited to become a curator at the Encyclopedia of Life project, where I've written several short summaries of snake taxa.

    Life is Short but Snakes are Long was voted one of
    Bel-Rea Vet Tech College's Top 25 Reptile/Amphibian Blogs in 2016
    Life is Short but Snakes are Long was voted one of Bel-Rea Vet Tech College's Top 25 Reptile/Amphibian Blogs. The students and staff wrote that they particularly appreciated my efforts to reference my sources, and I was really glad to know that others appreciate my efforts to provide verifiable information (apparently there's all too little of that on the Internet these days).

    I was particularly glad that the BBC's Planet Earth II featured Galápagos Racers so prominently this year, generating Internet-wide buzz about snakes and their feeding habits, a topic close to my heart. Since I wrote about these interesting snakes back in 2013, a lot of curious people found my blog, inspiring me to write an update and include much more detailed information. I also revisited several other favorite topics, including the relationship between dragonsnakes and filesnakes, rattlesnake roundupssnake penises, and snakes as state/provincial symbols. I have some really good content planned to debut in 2017, including articles on the roles that snakes play in ecosystems, the nitty-gritty details of courtship, sex, and mating in snakes, the little-known and seldom-seen ecology of blindsnakes, profiles of some fossil snakes, and venomous bites from "non-venomous" snakes.

    Life is Short but Snakes are Long would not be possible without support from volunteer translators Alvaro Pemartin& Estefania Carrillo, from Utah State University, particularly my advisor Susannah French and the Ecology Center, and from my loving girlfriend and editor Kendal Morris.

    Thank you, and happy 2017!

    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.

    Do snakes have a third eye?

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    This post will soon be available in Spanish

    Limerick written by Annie Simminger about her nephew,
    Richard Marshall Eakin, and published in his 1983 book The Third Eye.
    Eakin and Robert C. Stebbins performed and published many
    experiments on the structure and function of the third eyes of lizards
    Many lizards have a parietal eye, also known as a third eye or pineal eye. This "eye" is a photosensory organ located on the top of the skull, in the center. It has a well-defined lens, cornea, and retina, and is lined on the inside with photosensitive cells that resemble the cones of the lateral eyes and contain the light-sensitive pigment vitamin A1. These cells are connected by the parietal nerve to the pineal organ in the brain, which produces melatonin2, the hormone that controls sleep patterns, circadian rhythms, and seasonal cycles such as mating, migration, and hibernation. The parietal eye can see light and is primarily used to sense changes in day length. Many lizards have a parietal eye, although it is most well-developed in tuataras, even serving as the inspiration for a New Zealand brewery.



    Parietal eye (black outline) and parietal scale (white outline)
    of Liolaemus bisignatus (Philippi's Tree Iguana).
    From Labra et al. 2010
    Recently, a Twitter conversation led me to evaluate the evidence for a parietal eye in snakes. As with many things, you would assume that if lizards have parietal eyes, then snakes have them too, since snakes are just one group of legless lizards. And, as with many things, you'd be wrong (probably; read on). It turns out that studies on the parietal eyes of snakes are almost non-existent. Maybe this isn't surprising, considering how little we know about other basics of snake physiology, like how well they can hear or whether or not they sleep. The evidence for the existence of  a parietal eye in snakes is scant at best, and despite evidence for its absence, "amazingly few species have been studied", just seven as of 1979, and barely any others since then. Detailed studies have been made on the pineal organ of just one species, Natrix natrix, the European Grass Snake, in contrast to a large body of work on the pineal complex of lizards and tuataras. The tale of the evolution of the parietal eye is helpful in understand the assumptions made about snake parietal eyes, in the absence of much direct research on them.

    The "chimney-like" pineal foramen of
    the extinct 3-foot-long 250 million year old
    South African fossil therapsid Hipposaurus.
    From Haughton 1929
    Tuataras and many lizards have relatively well-developed parietal eyes. These organs face upwards between the parietal bones of the skull, and were it not for their covering of skin they would effectively connect the outside world with the brain (more or less as our "normal" [lateral] eyes do). There are no eyelids, or rather, like the lateral eyes of snakes, there is a fused, clear eyelid. In young lizards, the opening in the skull is large and T-shaped, like the familiar soft fontanelle of an infant human's skull, whereas in adult lizards the opening becomes ossified and may close completely late in life. Some extinct reptiles had bony protuberances around the margins of their parietal eyes: one, Hipposaurus, had a "chimney-like structure". For a long time paleontologists debated whether holes in the parietal bones of fossil skulls were necessarily evidence of ancient parietal eyes. The German-American paleoneurologist and "fossil brain" expert Tilly Edinger3 snarkily wrote that "if one doubts that this association existed also in extinct vertebrates, one may as well doubt that the orbits of fossil skulls contained eyes", because other than lizards and tuatara, no other living animals possess such holes. Many extinct tuatara relatives had even larger and more well-developed parietal eyes than do living tuataras—in some extinct pliosaurs, the opening was as large as 50 mm (2") by 20 mm (almost 1"), whereas in living tuataras it rarely exceeds 3 mm and modern lizards 1 mm. A more useful comparison may be the size of the parietal eye relative to that of the braincase: in living tuataras, this is about 1:7, whereas in living lizards it varies from 1:21 to 1:36 or less. The absence of any traces of musculature in fossil skulls or signs of more a complex past during embryonic development suggests that parietal eyes have never been any more elaborate in structure than they are in modern lizards and tuatara, although the larger parietal eyes of extinct reptiles were probably better at seeing than the tiny ones of living species.

    Endocast of the brain of the dog-sized 250-million-year-old
    dicynodont Lystrosaurus, the "humble badass of the Triassic",
    showing the large parietal eye (dark structure at the top).
    From Edinger 1955
    Iguanids, agamids, varanids, cordylids, lacertids, and shinisaurids are diurnal, surface-active lizards that have well-developed parietal eyes. Several families of lizards that are mostly nocturnal and/or spend a great deal of time underneath cover or beneath the ground also have parietal eyes, including scincids, anguids, anniellids, xantusiids, amphisbaenids, and xenosaurids. Chameleons have a degenerated parietal eye that lies above the foramen; presumably it is redundant with the lateral eyes of chameleons, which can move independently and cover 180° horizontally and 90° vertically. Some surface-active (teiids). burrowing (dibamids), and intermediate nocturnal (geckos) and diurnal (helodermatids and lanthanotids) lineages lack parietal eyes. Many of the lizard genera lacking a parietal eye have more equatorial geographic distributions. It has been suggested that a long evolutionary history in the tropics could lead to the loss of the parietal eye, because changes in day length are so minor close to the Equator. Even though there are seasons in the tropics (normally wet and dry), they are not associated with day length or light level cues that animals could use to know when the switch between the two is going to happen (and alter their lifestyles accordingly). There are no truly polar reptiles or amphibians, but some polar mammals (e.g., walruses, Weddell seals) have unusually large pineal organs, whereas some tropical mammals (e.g., sloths, pangolins) have lost their pineal organs, suggesting that the function of the pineal complex is more important where day length is more variable.

    Paired parietal foramina in the parietal (ptl)
    bone of a Banded Krait (Bungarus fasciatus)
    skull. From Scanlon & Lee 2004
    It's thought that the parietal eye is retained in many burrowing lizards because these animals are occasionally exposed to light, and perhaps the parietal eye is a more suitable photoreceptor for a burrower than are lateral eyes, because it is already oriented upwards. If snakes evolved underground, as the leading hypothesis suggests, then it would make sense that they lost their parietal eye. Their normal eyes appear to have lost some muscles and modern surface-dwelling snakes have lost at least two of the five visual pigment (opsin) genes found in other vertebrates. Fossil and modern osteological evidence shows that a median parietal foramen like that of lizards was lost in an ancestor of all snakes (about 125 million years ago) and is not present in any living or fossil snakes. About 60 million years ago, small, laterally paired foramina evolved in early colubroids, and are present in many, but not all, living elapids, viperids and other colubroid groups. As in lizards, these may be present only in juveniles, becoming obliterated externally by bone growth later in life. Snake osteology expert John Scanlon told me that "Nobody, as far as I'm aware, has investigated whether the paired foramina [of snakes] are homologous or functionally similar to the median foramen of basal lepidosaurs [lizards]." The loss of parietal eyes is also supported by developmental formation and then fusion with the pineal gland in embryonic snakes, birds, and mammals4.

    Developmental origins of the parietal ("median") eye and the lateral eye.
    The cilia are cellular structures that normally function for movement
    (e.g., of debris out of the nose, of water over gills, of eggs into oviducts,
    of sperm cells to the egg). In the eye, they have evolved into photoreceptors.
    So, snakes join most mammals, birds, turtles, and most amphibians5 in having lost their parietal eyes but retaining a photosensitive pineal organ in the brain that is not directly exposed to the outside of the skull. However, a recent review of the function of the pineal complex in reptiles states that the pineal gland of adult snakes does not contain photoreceptor-like cells. Instead, the principal cells are pineal parenchymal cells, which secrete melatonin but do not sense light. Nevertheless, experiments on gartersnakes have shown that removing the pineal organ of male gartersnakes in the fall, before hibernation, alters their melatonin cycle and reduces their courtship behavior when they emerge in the spring, so the pineal organ clearly functions to regulate melatonin and annual cycles in snakes.

    Diagram of the lizard parietal eye
    From Solessio & Engbretson 1993
    At first glance, it doesn't seem to make sense to have a deep brain photoreceptor that isn't connected to the outside world, because it doesn't seem possible for it to be able to sense light or darkness from inside of your skull. But, don't forget that the two lateral eyes allow light to enter the brain; it is this light that the pineal organ is sensing. Humans have pineal organs too, and clearly we have no third eye (except in Greek mythology and Grimm's fairytales). Think of how sleepy you feel when you have to get up before the sun, or how awake you feel when a bright light is turned on at night. This is because your pineal organ senses the ambient light or darkness and adjusts your melatonin levels, telling you (if it's bright) to wake up or (if it's dark) to stay asleep. Although the pineal organ can only sense light and dark, there is evidence that the the parietal eye can also detect different colors of light, including ultraviolet but not infrared light, and that it may be especially sensitive to the order of appearance of  light of different wavelengths, enabling lizards to detect dawn and dusk with great precision. Detailed anatomical studies have shown that the pineal organs of certain lizards possess either a finger-like projection that extends toward the parietal eye, or convolutions of the pineal wall, both of which result in exposing and orienting more photoreceptor cells towards the skull roof, where they can detect light. Although these are sometimes occluded by cartilage or blood sinuses, their existence suggests that the pineal organ of lizards is a more important photoreceptor than previously realized. Melatonin is synthesized by both the pineal organ and the parietal eye.

    Comparative morphology of the pineal complex in A) lamprey,
    B) frog, C) lizard, and D) human. From Edinger 1955
    The parietal eye of a Western Fence Lizard (Sceloporus occidentalis)
    C = cornea; CC = connective tissue; L = lumen;
    LS = lens; PN = parietal nerve; R = retina
    Light micrograph from Eakin 1970
    Many hypotheses have been put forth to explain the exact function of the parietal eye, which in some ways is still unclear. Rejected hypotheses include that the parietal eye is used for detection or deterrence of aerial predators. Even in tuataras, the parietal eye is barely noticeable (it wasn't described until the 1870s), so predator deterrence is unlikely. It may play a minor role in predator detection, because the photoreceptive cells can respond to changes in light intensity as quickly as those of the lateral eyes, but sending sleepiness signals by initiating a melatonin cascade would be counterproductive to predator avoidance, to say the least. The most straightforward hypothesis is that it measures light intensity, functioning in regulating seasonal seasonal behaviorphysiology, and thermoregulation. Although reptiles do have thermally sensitive neurons in their brains, we now know that the pineal complex does not directly sense heat. Instead, reptiles have specially-adapted transient receptor potential ion channels (TRPs), which are proteins found throughout the body that act as internal thermometers and external temperatures sensors. Blocking the genes that make these proteins causes crocodiles to abandon their typical regime of behavioral thermoregulation and leads to significantly altered body temperature patterns. Changes in melatonin levels also affect the body temperatures selected by some reptiles, but in opposite ways in lacertids and iguanids. There is also a great deal of evidence that the parietal eye is sensitive to polarized light: blocking the parietal eye disrupts sun-compass orientation and homing ability of displaced individuals in several lizard species. This makes sense because there is no evidence that lizards can see polarized light with their lateral eyes. 

    Parietal spots of a Copperhead
    (Agkistrodon contortrix)
    One study of thirty species of South American Liolaemus lizards found that parietal eye size did not vary meaningfully with latitude, altitude, environmental temperature, thermal tolerance, or body size, and that there was no evidence of phylogenetic inertia and high intraspecific variation in parietal eye size, suggesting that parietal-eye size may not be under strong selection for accuracy. Another detailed study found that removal of the parietal eye and pineal organ did not prevent 8 species of lizards from four families from carrying out their normal circadian rhythms. They concluded that other photoreceptors within the brain were compensating, although the aforementioned extensions of the pineal organ may also be a factor in the occasional “failure” of parietalectomy experiments. It's actually not clear that we even have enough baseline data on seasonal changes in snake circadian rhythms to correctly interpret the results of experiments that attempted to manipulate the pineal organs of snakes.

    Dorsal view of a Copperhead skull, from DigiMorph

    Pigmented apical pits of a ratsnake
    But could the paired parietal formaina of some snakes function as parietal eyes? The question that started me looking into this was about Copperheads (Agkistrodon contortrix), which usually have a pair of small dark spots on their parietal scales. Evidently a National Geographic documentary called them nostrils, which is totally absurd. But, the spots do seem to be in the approximate location of the parietal foramina in other snakes. The DigiMorph scan of a copperhead skull does not show any parietal foramina, although if it is of an adult specimen (not stated) then they may have closed up on top. A few other snake species also have such spots, and many snakes have pigmented sensory or apical scale pits elsewhere on their bodies. The parietal eyes of some lizards are also differentially pigmented. Do we need to open our (lateral) eyes to some new possibilities? I think it's clear that snake photoreception, although well-known in species with pit organs, is still relatively poorly understood for snakes as a whole.



    1 The function of vitamin A in eyesight was the basis for a WWII propaganda campaign that eating more carrots could improve human night vision. Although it's true that carrots and vitamin A are essential for good eyesight, the extent to which eating more carrots can improve a person's eyesight was apparently greatly exaggerated in 1940 to create a cover story for the novel abilities of Allied pilots to pinpoint Axis fighter jets at night, which in reality was due to on-board Airborne Interception Radar (although there is in turn some disagreement among historians as to how purposeful the deception was and how much both sides knew about the other side's radar capabilities).



    2 Melatonin is synthesized from the amino acid tryptophan, which is the origin of another common myth: that eating a ton of turkey causes you feel sleepy.



    3 Tilly Edinger was among the very last scientists of Jewish ancestry to leave pre-WWII Germany. A 1938 letter to the U. S. State Department in support of her immigration application from George Gaylord Simpson read "She is a research scientist of the first rank and is favorably known as such all over the world. She is everywhere recognized as the leading specialist on the study of the brain and nervous system of extinct animals and on the evolution of the gross structure of the brain. She is so preeminent in this field that she may really be said to have created a new branch of science, that of paleo-neurology, a study of outstanding value and importance”. She was the first female president of the Society of Vertebrate Paleontology, and authored over 1200 scientific papers and books, many sprinkled with sharp-witted, humorous phrases and observations. Her pioneering work in paleoneurology is well-chronicled here.



    4 During embryonic development, the parietal eye and the pineal organ form together from a pocket formed in the brain ectoderm. The ancestral state is presumed to have been a possibly paired photosensory organ, as seen in extant lampreys. The parietal eye and the pineal gland of tetrapods are probably the descendants of the left and right parts of this organ, respectively. Some Devonian fishes have two parietal foramina in their skulls, suggesting an ancestral bilaterality of parietal eyes.



    5 Crocodilians and some tropical lineages of mammals (xenarthrans [sloths, armadillos, anteaters], pangolins, and sirenians [manatees & dugongs]) have lost both their parietal eye and their pineal organ. All amphibians have a pineal organ, but some frogs and toads also  have what is called a "frontal organ", which is essentially a parietal eye. The word "pineal" comes from the shape of the human pineal organ, which resembles a pine cone.


    ACKNOWLEDGMENTS

    Thanks to Daniel, Helen Plylar, and David Steen for initiating a discussion of this topic on Twitter, to John Scanlon for providing additional details about the evolution of parietal bone anatomy in squamates, and to Sandy Durso and J. D. Willson for the use of their photos.

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    Underwood, H. 1989. The pineal and melatonin: regulators of circadian function in lower vertebrates. Cellular and Molecular Life Sciences 45:914-922 <link>

    Ung, C. Y. J. and A. C. Molteno. 2004. An enigmatic eye: the histology of the tuatara pineal complex. Clinical & Experimental Ophthalmology 32:614-618 <abstract>

    Vivien-Roels, B., P. Pévet, M. Dubois, J. Arendt, and G. Brown. 1981. Immunohistochemical evidence for the presence of melatonin in the pineal gland, the retina and the Harderian gland. Cell and Tissue Research 217:105-115.

    Wurst, G. and G. Gundy. 1982. Pineal morphology in amphisbaenians. Page 908 in Annual Meeting of the American Society of Zoologist. American Society of Zoologists, Louisville, Kentucky.

    Zimmerman, K. and H. Heatwole. 1990. Cutaneous photoreception: a new sensory mechanism for reptiles. Copeia 1990:860-862.

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    Shield-tailed snakes (Uropeltidae)

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    This post will soon become available in Spanish
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    Large-scaled Earth Snake (Uropeltis macrolepis)
    Shield-tailed snakes (family Uropeltidae) are poorly studied, fossorial snakes endemic to montane regions of peninsular India & Sri Lanka. Together with the families Cylindrophiidae (14 species) and Anomochilidae (3 species) they make up the superfamily Uropeltoidea, which is named for them because they are the most diverse subgroup, with 55 species in 8 genera (9 until recently, more below). Most phylogenetic studies suggest that Uropeltoidea is the sister group to Pythonoidea, although these two lineages share only a few obvious features and likely diverged at least 60 and possibly up to 85 million years ago. If it's true, this relationship is pretty interesting because it means that the familiar giant pythons are more closely related to the ~18" long burrowing uropeltoids than they are to their most obvious ecological analogues, the giant Neotropical boas. However, this kind of relationship is not unprecedented: the emerging picture of henophidian taxonomy is that constriction and large gape size have evolved at least three or four times within snakes, a good example being the sister relationship now widely accepted between the "pipesnake" family Aniliidae and the "dwarf boa" family Tropidophiidae (the "Amerophidia"), both of which were formerly considered members of the Uropeltoidea. Even some species of Cylindrophis (and, possibly, Anilius) immobilize their prey with their coils, although they have small gapes.

    The southern Western Ghats
    Uropeltids are the Darwin's Finches of snakes. They have radiated spectacularly across an archipelago of "sky islands", reaching their highest diversity and endemism in the mountain ranges of India's southern tip. These volcanic mountains run parallel to the coast, creating a rain shadow of dry plains to the east and generating torrential rainfall within their hills as trade winds blow monsoonally wet air northeast from the Arabian Sea. Known as the Great Escarpment of India, these mountains are an ancient coastline, formed during the break-up of the supercontinent Gondwana some 150 million years ago. Uropeltids are especially diverse in the high, wet 'shola' forests of the Anai Malai Hills (also known as the Elephant Hills), but are also highly diverse in the the Pothigai (Agasthyar Malai), Nilgiri, and Cardamom Hills, as well as the northern and central Western Ghats, the Eastern Ghats, and on Sri Lanka. Many of these mountain ranges are part of the UNESCO World Network of Heritage Sites and are among the "hottest hot-spots" of biological diversity in the world. They're home to the world's largest wild population of Indian Elephants, the second largest wild tiger population, and even more critically-endangered, endemic mammals such as Nilgiri tahr and Malabar large-spotted civets. Sixty-five percent of reptile species in this area are found nowhere else. In addition to uropeltids, the Ghats are home to diverse radiations of endemic freshwater crabs and shrimps, minnows and carps, tree frogs, and caecilians. Other endemic reptiles include the cane turtle (Vijayachelys silvatica) and travancore tortoise (Indotestudo travancorica), two genera of skinks (Ristella and Kaestlea), spiny tree lizards (genus Salea), and wood snakes (genus Xylophis, also named by Beddome, which were thought to be xenodermids but from which we have just recently obtained the first DNA sequences, placing at least one species with pareids and another with natricines). Besides Xylophis and uropeltids, there are at least 29 other species of endemic snakes, ranging from blindsnakes to sand boas, vine snakes, coral snakes, and vipers.

    Col. Richard H. Beddome
    Perhaps it isn't surprising that most species of uropeltids "were described in a burst of activity in the 19th century", because British colonials cleared large swaths of mountain forest for timber and tea, coffee, and teak plantations between 1860 and 1950. Forty percent (22) of the known species were discovered and described by Colonel Richard Henry Beddome, a naturalist who "…exploited the South Indian Hills, including the Palni Hills, to such purpose in the seventies and eighties of the last century, that he has hardly left a snake for any later enthusiast to discover" wrote distinguished herpetologist Frank Wall in 1922.1 Perhaps somewhat ironically, Beddome's 1911 obituary states that his career as a naturalist and forester coincided with "the first systematic steps to save the forests of Southern India from the denudation at the hands of the rural population to which they had long been exposed". However, Beddome used his tours in the montane forests to carefully document, describe, and make exhaustive and useful collections of plants, land snails, amphibians, and reptiles. In his lifetime Beddome described over a thousand species of animals and plants, and many others have been named for him.2

    Heads and tails of uropeltids. 
    The blade-like, "boomerang rostral" and polygonal eye shield
    of Rhinophis punctatus (top left [top] and top right [side]).
    Shield-like tail of Uropeltis rubromaculata (bottom left)
    and
     Rhinophis philippinus (bottom right). From Pyron et al. 2016
    Uropeltids are supremely adapted for burrowing, perhaps more so than any other snake. They construct a network of burrows during the rainy season, when the soil is soft, and wander through them after they harden. They can dig as deep as two meters and for extended periods of time. They have stout, relatively lizard-like skulls with few teeth, and conical, slender heads that are much narrower than their thick bodies. The eyes of some species are protected by polygonal scalesRhinophis and some Uropeltis have keeled, blade-like rostral scales that give the head a distinct pointed appearance. Uropeltids have narrow ventral scales similar to their dorsal scales, and short, blunt, often shield-like tails, from which they get their common name. Uropeltid tail morphology ranges from relatively normal (in Brachyophidium, Platyplectrurus, and Teretrurus) or somewhat compressed with a multi-pointed scute on the end (in Melanophidium, Plectrurus, and Pseudoplectrurus), through decidedly unusual, including tails terminating in a projecting, rugose, keratinous disc (in Rhinophis and Pseudotyphlops), to the classic, highly modified “shield” tail of some Uropeltis, in which the body appears to have been sliced off at a ~45° angle, leaving a flattened disc covered with rugose scales. However, the real specializations for burrowing are hidden within.

    Diagram of  a dissected Rhinophis drummondhayi
    showing the extent of red and white muscle along the body
    and in 
    two cross-sections. From Gans et al. 1978
    Firstly, the heads of uropeltids are battering rams that are used against the soil. They are the only amniotes whose skulls are supported at the base by two vertebrae: that is, both the first and second vertebra (the human atlas and axis) articulate directly with the occipital condyle at the base of the skull. Furthermore, their braincases are reinforced and many other skull bones are strong and stout, especially for a snake. The anatomy and physiology of the anterior third of a uropeltid's body is adapted for driving this strong head forward into the soil. The muscles along the anterior portion of the trunk are large, thick, deep red, and rich in myoglobin, catalytic enzymes, and mitochondria, all biochemical or cellular adaptations that permit sustained activityThese muscles are loosely attached to the rest of the body, so they can simultaneously push the sides of the body against the tunnel walls and move the head forward, without pushing the rest of their bodies backwards. To accomplish this, muscles in the posterior body squeeze the anterior vertebral column into a sequence of hairpin turns, not unlike those formed in the vertebrae of large, elongate prey when they are eaten by snakes.3 Because the tip of the nose creates a narrow burrow that is later widened by the flexing of the body, uropeltids can burrow effectively among rocks and roots.4 Like a freight train, the anterior fifth of the body is like a locomotive in that it contains almost all of the propulsive machinery, and pulls along behind it the mostly-inert posterior trunk like the other train cars, containing viscera, embryos, food, etc., all protected on the end by a caboose-like caudal shield. 

    Schematic diagram of a uropeltid burrowing, from Gans et al. 1978.
    The dark black areas between the snake and the tunnel wall indicate
    firm contact. In A) the snake's vertebral column is curved and pushing
    against the sides of the tunnel. In B) the firm contact between the curved spine
    and the tunnel walls acts as a base against which the head can push,
    extending the tunnel forward. The widened body narrows as the spine uncurves.
    In C) the snake pulls its vertebral column forward and reintroduces
    the curves, which widen the body and the tunnel. The rest of the body
    is pulled along without doing any work or needing to resist any force.
    This division of labor is similar to that seen in some caecilians, which burrow in a similar way and thereby create tunnels that are wider than their bodies.  And, unlike scolecophidians and amphisbaenians5, they can burrow without pushing against their tails, which leads to the question of what exactly their weird, shield-like tails are for, if not being pushed against? It is thought that the function of these eponymous tails is to collect dirt as the snakes burrow, forming a "plug" that protects the snake from behind. The scale texture of the tail shield scales is deeply ridged, in sharp contrast to the texture of the body scales, which instead bear regular microstructure that inhibits wetting, sheds dirt, reduces friction, and produces iridescent colors. There is also evidence that the tail disc develops over the lifetime of some species, because juveniles do not have modified tails (although they do have large, deep red axial muscles like those of adults).

    Uropeltids from Duméril, Bibron, & Duméril's
    1854 Erpetologie Générale


    Top left and top right: Rhinophis philippinus
    Center left and center right: Rhinophis saffragamus
    (formerlyPseudotyphlops philippinus)
    Bottom left and bottom right: Uropeltis ceylanica
    Center top and center bottom: Plectrurus perroteti
    A new phylogeny, the most comprehensive yet, nevertheless includes DNA from just five of the eight genera of uropeltids. The most diverse and well-known genera are Uropeltis and Rhinophis, containing 24 and 19 species respectively. These are also the most highly specialized for burrowing. Rhinophis is so bizarre that it was originally described as a subgenus of the legless lizard genus Anguis. In contrast, the smaller and more poorly-known genera Brachyophidium (1 species), Melanophidium (4 species), Platyplectrurus (2 species), Plectrurus (4 species), and Teretrurus (1 species) have less highly modified heads, tails, and body musculature. Apparently these species are unable to tunnel in dry grassland soils, instead remaining belowground until rain softens the soil. Although the 'shola' forests have been greatly reduced, in recent years many of the remnants have been protected. In contrast, the high-altitude grasslands favored by certain species have, like grasslands all over the world, been largely ignored from a conservation standpoint. A single species in an eighth genus, Pseudoplectrurus, is known only from the original specimens collected by Beddome in 1870, from atop the 6000' Mount Kudremukh. It seems that uropeltids first evolved in India at least 37 million years ago, and crossed only once onto Sri Lanka, an island with one of the most phylogenetically diverse snake faunas in the world, but which has maintained its distinctiveness from the Indian mainland despite several extended periods of land connection during the past 500,000 years.

    Uropeltis macrolepis eating an earthworm
    Unfortunately, we still know precious little about the ecology of uropeltids. Most species eat 80-90% earthworms, but they may snack upon the occasional earwigs, termites, or caterpillars. They are eaten by kraits (genus Bungarus), as well as wild boars, mongoose, owls, and galliform birds. They mate during the rainy season and females give birth to 3-9 live young at a time. Like many fossorial snakes, some species are brightly colored on the underside, especially on the tail and neck. These colors may send warning signals to predators, including possibly mimicking the coloration of some venomous kraits or centipedes. It's likely that a high amount of diversity remains to be described. If you want to read about the current state of our knowledge of uropeltid diversity and taxonomy, including outlines of the genus-level groups that are supported by molecular and morphological phylogenies, not to mention numerous color photographs, you can do so here.



    1 In the same issue, sandwiched between "Alpine Orthoptera from central Asia" and "Hand-list of the Birds of India, Part IV", appears an article with the nonchalant title "A few hints on crocodile shooting (with two Plates)", as well as a short note by a Miss Kennion called "Crocodile shooting in Nepal". Sport hunting of predators was common during the British colonial period, and evidently human babies were sometimes used as bait. It's a good thing Beddome and Wall were paying attention to uropeltids back then, because nobody else was.



    2 Interestingly, a children's book written in 1947 by Vera Barclay contains a possible description of Col. Beddome. The book is called "They Met a Wizard" and the titular wizard is a zoologist living in colonial India with a special interest in snakes. Ms. Barclay was the great niece of Col. R.H. Beddome and it's likely that she knew him growing up and based her description of the zoologist in the story at least in part on her memories of him.



    3 As a result, some early descriptions of uropeltids, such as Günther's The Reptiles of British India or Wall's Ophidia Taprobanica, contained erroneous claims that the neck was "swollen and knuckled" or that the head was very frequently bent to one side, as a result of the snake being preserved with the axial muscles contracted and unconstrained by tunnel walls.



    4 I cannot improve upon the ingenious phrasing used by Carl Gans to describe the burrowing of uropeltids: "The burrowing method provides an ideal tunneling device for an unpredictably inhomogeneous substratum. The initial divot driven by the head is quite narrow and will be deflected by roots or rocks. When it passes close to such effectively nondeformable and nondisplacable objects, the opposite wall of the tunnel will be compressed unevenly so that the final tunnel achieves its full if meandering diameter by extra asymmetric compression of the softer zones."



    5 Most amphisbaenians bite pieces out of their prey rather than swallowing it whole, so they are less likely to be impeded by a food bolus while burrowing.


    ACKNOWLEDGMENTS

    Thanks to Sara Ruane, Satyen Mehta, and M for the use of their photos, and to the Rare, Endangered and Threatened Plants of Southern Western Ghats database for sharing their beautiful map.

    REFERENCES

    Extremely similar head (top) and tail (bottom) of
    Uropeltis macrorhynchus
    Beddome, R. H. 1886. An account of the earth-snakes of the peninsula of India and Ceylon. Annals and Magazine of Natural History 17:3-33 <Biodiversity Heritage Library>

    Bossuyt, F., M. Meegaskumbura, N. Beenaerts, D. J. Gower, R. Pethiyagoda, K. Roelants, A. Mannaert, M. Wilkinson, M. M. Bahir, K. Manamendra-Arachchi, K. L. N. Peter, C. J. Schneider, V. O. Oommen, and M. C. Milinkovitch. 2004. Local endemism within the Western Ghats-Sri Lanka biodiversity hotspot. Science 306:479-481 <download>

    Comeaux, R. S., J. C. Olori, and C. J. Bell. 2010. Cranial osteology and preliminary phylogenetic assessment of Plectrurus aureus Beddome, 1880 (Squamata: Serpentes: Uropeltidae). Zoological Journal of the Linnaean Society of London 160:118-138 <ResearchGate>

    Gans, C. and D. Baic. 1977. Regional specialization of reptilian scale surfaces: relation of texture and biologic role. Science 195:1348-1350 <abstract>

    Gans, C., H. C. Dessauer, and D. Baic. 1978. Axial differences in the musculature of uropeltid snakes: the freight-train approach to burrowing. Science 199:189-192 <abstract>

    Ganesh, S. 2010. Richard Henry Beddome and south India’s herpetofauna—a tribute on his centennial death anniversary. Cobra 4:1-11 <link>

    Ganesh, S. 2015. Shieldtail snakes (Reptilia: Uropeltidae)–the Darwin’s finches of south Indian snake fauna? Pages 13-24 in P. Kannan, editor. Manual on identification and preparation of keys of snakes with special reference to their venomous nature in India. Proceedings by Govt. Arts College, Udhagamandalam, Tamilnadu, India <ResearchGate>

    Ganesh, S. R. and S. R. Chandramouli. 2013. Endangered and Enigmatic Reptiles of Western Ghats – An Overview. Pages 35-61 in N. Singaravelan, editor. Rare Animals of India. Bommanampalayam Bharathiyar University (Post), Tamil Nadu, India <Google book>

    Gaymer, R. 1971. New method of locomotion in limbless terrestrial vertebrates. Nature 234:150-151 <abstract>

    Gower, D. J. 2003. Scale microornamentation of uropeltid snakes. Journal of Morphology 258:249-268 <full-text>

    Günther, A. 1864. The Reptiles of British India. Robert Hardwick, London <Biodiversity Heritage Library>

    Olori, J. C. and C. J. Bell. 2012. Comparative skull morphology of uropeltid snakes (Alethinophidia: Uropeltidae) with special reference to disarticulated elements and variation. PLoS ONE 7:e32450 <full-text>

    Smith, M. A. 1943. The Fauna of British India. Volume III. Serpentes. Taylor & Francis, London <full-text>

    Pyron, R. A., S. R. Ganesh, A. Sayyed, V. Sharma, V. Wallach, and R. Somaweera. 2016. A catalogue and systematic overview of the shield-tailed snakes (Serpentes: Uropeltidae). Zoosystema 38:453-506 <link>

    Rajendran, M. 1985. Studies in uropeltid snakes. Madurai Kamaraj University, Madurai.

    Rieppel, O. and H. Zaher. 2002. The skull of the Uropeltinae (Reptilia, Serpentes), with special reference to the otico-occipital region. Bulletin of the Natural History Museum: Zoology 68:123 <download>

    Shanker, K. 1996. Nature watch: secrets of the shieldtails. Resonance 1:64-70 <full-text>

    Wall, F. 1921. A new snake of the family Uropeltidae. Journal of the Bombay Natural History Society 28:41-42 <Biodiversity Heritage Library>

    Wall, F. 1921. Ophidia Taprobanica, or the Snakes of Ceylon. H. R. Cottle, Govt. Printer, Colombo <Biodiversity Heritage Library>

    Wall, F. 1922. Acquisition of four more specimens of the snake Brachyophidium rhodogaster Wall. Journal of the Bombay Natural History Society 28:556-557 <Biodiversity Heritage Library>

    Williams, E. E. 1959. The occipito-vertebral joint in the burrowing snakes of the family Uropeltidae. Breviora 106:1-10 <Biodiversity Heritage Library>


    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.

    Snakebite, antivenom research, and basic science

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    Soon available in Spanish
    Pronto disponibile en Español

    In the past few weeks, a peculiar congruence of several seemingly-unrelated events took place. (At least) two new scientific papers about snake biology were published, a new video series was announced, some scientists entered contests, and the U.S. executive branch announced a budget proposal with deep cuts to science funding. However, these events aren't as unrelated at they might seem at first glance, and they have something to tell us about where snake biology, and science in general, are going in the future.

    The science: part I (puff adders)

    A puff adder (Bitis arietans)
    Puff Adders (Bitis arietans) are among Africa's most widespread vipers. They are heavy-bodied snakes that are found in savannas and open woodlands. Like most vipers, they eat mostly rodents as adults, which they ambush from carefully-selected sites, which they sometimes occupy for weeks at a time. Recently, Xavier Glaudas and Graham Alexander published a new study showing that, even though Puff Adder strikes last less than two seconds, they can choose to either hold onto or let go of the prey depending on its size. Specifically, they hold onto small mice, shrews, birdstoads, and lizards, but strike & release larger rodents and rabbits, because retaliatory rat bites are dangerous to them. After they let go of these larger prey, which usually run off a short distance before the venom kills them, they track them down again using stereotypic strike-induced chemosensory searching behavior to locate the scent of non-toxic components of their own venom. This is really similar to findings by Bree Putman and Rulon Clark that Southern Pacific Rattlesnakes (Crotalus oreganus) were more likely to hold onto smaller rodents than to larger ground squirrels. You can watch 26 awesome videos selected from an archive of thousands of hours of video taken in the wild over more than two years.1

    This research matters because venomous snakes and their prey are in constant evolutionary arms races, leading to:
    1. a mosaic of new biochemical compounds that are often useful in treating disease
    2. a mosaic of new biochemical compounds that can make venomous snakebite really hard to treat
    We'll come back to the second one in a minute. The obvious importance of human medicine and venomous snakebite treatment overshadow a third important reason to study snakes and what they eat. Although the beneficial role of snakes in rodent control is taken as gospel by many advocates of snake conservation, the amount of data that we actually have on what snakes eat in the wild is surprisingly small. For many species, we don't even have a general idea of what kinds of prey they like to eat. Given recent estimates that spiders eat about as much meat as people do worldwide, and the potential for snakes to reach very high population densities in certain habitats, it's likely that the top-down effects of snakes as predators are significant ecosystem services that most humans aren't aware of and thus undervalue. Indirect effects on other aspects of the ecology of snake prey species, such as predation release and disease transmission, link snake predation even more strongly to human health. This is particularly timely in light of recent predictions that 2017 will be a big year for white-footed mice and thus for Lyme disease in the northeastern USA, controversy over the reintroduction of Timber Rattlesnakes, one of the white-footed mouse's top predators, to Quabbin Island in Massachusetts2, and the continuation of both the infamous Sweetwater Rattlesnake Roundup3 and the reformed Claxton Wildlife Festival and Lone Star Rattlesnake Days earlier this month.

    The science: part II (how cobras got their flesh-eating venoms)

    A Mozambique spitting cobra (Naja mossambica) spitting its venom
    Spitting cobras are even more well-known than puff adders because of their defensive venom spitting abilities, showcased on the BBC's Life in Cold Blood. They are found in Africa and Asia and are thought to have evolved two or three times from non-spitting cobras. A new paper from the lab of Bryan Fry at the University of Queensland sheds some light on when and why venom spitting evolved. Elapid snakes, including cobras, have venoms rich in neurotoxins, which are highly potent toxins that are very effective at paralyzing their prey. Cobras also have less potent cytotoxins that kill cells directly, which is a bit weird. What is the function of these toxins?

    Toxicity of snake venom to human cells grown in culture.
    Warm colors indicate higher toxicity.
    From Panagides et al. 2017
    The hypothesis put forth here is that the first step towards venom spitting was the evolution of hooding behavior and morphology, which happened twice in elapids: once in "regular" cobras and once in King Cobras, which are more closely related to mambas. Only once a conspicuous visual display was present was there selective pressure for cytotoxic venom components delivered to the eyes of potential predators via spitting. Although the venom of both groups is cytotoxic, Hemachatus (rinkhals) and Naja cobras use three-finger toxins, whereas King Cobras use L-amino acid oxidase enzymes, consistent with the undirected, opportunistic nature of our current model of venom evolution by gene duplication and mutation. The authors suggest that further elevations in cytotoxicity are linked to bright bands and other aposematic colors or hood markings, although their paper did not attempt to quantify these attributes of cobra displays, which can be quite diverse even within species. Further evidence in support of the hypothesis is that Naja naja and Naja oxiana seem, based on their nested position, to have lost spitting but to have retained cytotoxicity, and their close relatives Naja atra and Naja kaouthia might represent steps down this evolutionary path, being capable of spitting only in some populations and with less accuracy than the African and southeast Asian clades of true spitting cobras.

    This is an extremely cool and popular topic. It was covered by IFLS, The Wire, Gizmodo, and the Washington Post. It goes to show that people worldwide are fascinated by venomous snakes, and the Fry lab has done a great job capitalizing on that interest (among other accolades, Fry's graduate student Jordan Debono recently won the Queensland Women in Science Peoples' Choice Award ([ contest that was decided by an online popular vote; more on this later] for her research on global snakebite treatments). One reason for this fascination has to do with the question of who, exactly, these cobras are defending themselves from? The most reasonable hypothesis, given the timing and geography of the diversification of spitting cobras and the precision with which they can target forward-facing eyes and hominoid faces, is primates. Us, and our ancestors, who have eaten and been eaten by snakes for millions of years. Studying spitting cobras is a window into our own evolutionary past, a way for us to learn about ourselves. But, let us not be misled into thinking that interactions between humans and cobras are a thing of the past.

    The upshot: the truth about snakebite

    You can follow the ASV @Venimologie
    If you haven't read the blog by medical toxinologist Leslie Boyer, you really should. Earlier this month she wrote about the vicious circle of antivenom shortage in sub-Saharan Africa, where millions of people are bitten by venomous snakes every year, many of which die or suffer awful injuries because they lack access to good antivenom. This crisis has prompted the creation of the African Society of Venimology and a new series of snakebite training videos in English, French, and Spanish. The politics and economics of antivenom are complicated and reflect larger issues in medicine, education, quality control, supply and demand, and how global economics and corporations have failed to respond to the needs of local communities and consumers. In a nutshell, the issue is that antivenom manufacturers don't make enough good antivenom, because not enough people buy it. People don't buy it because it's expensive, and it's expensive because not that much is made. This is despite a huge need for it—but not everybody with a snakebite goes to a hospital and gets antivenom in Africa, partially because it's not certain there will be any and partially because a lot of patients and doctors don't know about antivenom, because it's not in widespread use (which is mostly because of the reasons above). Other exacerbating problems include that it's often not certified, fake products can price the real antivenom out of the market, and the infrastructure for distributing antivenom and information in Africa is sub-optimal (but improving). Fixing any one or even most of these problems won't fix the whole system—if any one of them break down, supply and demand will be out of balance and people won't get the care they need.

    A lot of the same issues used to be present in Mexico, but product improvements, government outreach, and massive education efforts in the 1980s and 1990s dramatically reduced mortality from venomous snakebite and led Mexico to become a major producer and consumer of high-quality, affordable antivenom, so much so that the USA now imports some of these drugs from Mexico. This is particularly important because medically-serious venomous snakebites (and scorpion stings) in the USA are mostly confined to the southwest, so the domestic market for American antivenom manufacturers is small. You may have heard about the controversy surrounding the discontinued coralsnake antivenom made by Wyeth, and there are compelling arguments that the Mexican polyvalent antivenoms Anavip (made by Bioclon for humans) and ViperSTAT (made by Veteria Labs for cats and dogs) are more effective and much less expensive than the only FDA-approved viper antivenom, CroFab (although BTG, the maker of CroFab, filed a complaint asserting that these Mexican products infringe on its patent).

    Finally, the global importance of the availability of high-quality, affordable antivenom for Latin American, African, and other exotic snakes is only going to increase as venomous snakes become more popular as pets and in zoos. This is particularly true in parts of the world completely lacking venomous snakes or with only very benign, non-life-threatening species, such as northern EuropeScandinavia and northern North America, where doctors may be totally unprepared for a snakebite emergency and may not have appropriate antivenom on hand.

    For a great introduction to and more in-depth coverage of these issues, you should watch The Venom Interviews or read their coverage of the recent video series.

    The future: sequence the Temple Pitviper genome


    Temple or Wagler's Pitvipers (Tropidolaemus wagleri)
    at the famous Temple of the Azure Cloud in Penang, Malaysia
    You can vote to sequence their genome here!
    Genomics of snakes is taking off in a big way, and we stand to learn a lot more about the evolution and function of snake venoms and the treatment of their effects. But, funding for basic science isn't a priority for many people, and more and more scientists are turning to crowd-funding their research or relying on limited funding from private foundations, which often decide which projects to fund through a crowd-sourced voting process. This isn't necessarily a bad thing; in fact, I think it's a great thing in many cases. But, it's important to realize that government funding for science is different from private funding in two crucial ways: 1) there is a lot more of it (at least for now), and 2) it's not driven by specific, private interests. A great example is the Orianne Society, a non-profit reptile conservation organization whose founding purpose was preventing the extinction of Eastern Indigo Snakes (Drymarchon couperi). Thanks to generous donations from private funding sources, the Society succeeded in purchasing large areas of critical habitat for this endangered snake and protecting them in perpetuity, probably the most effective and laudable conservation goal in existence. Another good example is the work of the Durrell Wildlife Conservation Trust, who have essentially saved a globally-rare snake, Casarea dussumieri, from extinction in the wild. I wish the quality conservation work that these organizations have become well-known for were more common, but to date their donors are some of the only large private backers of reptile research and conservation in the world.

    Snakes are part of human economics, albeit to a lesser extent than many insects, fishes, birds, and mammals—they are hunted for food (although there are many issues surrounding better management of unsustainable harvests), kept as pets, their skins made into leather, and their venom harvested to make antivenom and other drugs. But, in their current form, these industries place very little emphasis on finding out more about snake biology in the wild; it just isn't necessary for them to make a profit, even though the information is important for what they do. Antivenom manufacturers are accountable to their shareholders, but trying to block FDA approval of Mexican antivenom is certainly not going to result in better treatment for snakebite victims in the USA, and American companies aren't investing in any research to create new, better products themselves, since drug development is expensive and risky, and they already have a monopoly on antivenom in the USA.

    It's no secret that snakes and snake research have a PR problem: even scientific journals are less likely to publish research articles about snakes than about mammals and birds (although the bias is likely subliminal). Many people prefer cute fuzzy animals that are similar to humans, but research into the biology of un-fuzzy animals is equally important. There's a parallel to the divide between funding for basic and applied science. Basic science isn't usually as sexy as the exciting, fun applications that come later, like saving lives, curing diseases, or discovering new complex biological phenomena. However, important applied science like antivenom creation cannot happen without basic science, in particular basic science on snakes. Private companies can't afford to invest in basic science the way they once did. Which leaves government funding and that from a limited number of interested, private backers.

    We should support public funding for science and elect politicians who will do the same; better treatment for snakebite should be the least partisan and most universally-agreed-upon goal in the world. I think the path between basic (snake ecology, venomics, and genomics) and applied (antivenom manufacturing and public health) science is shorter and clearer in this context than in many, but the same principles apply—you cannot have medicine, conservation, and the other good parts of civilization without science.

    You can vote now through April 5th 2017 for a project sequencing the entire genome of the Temple Pitviper (Tropidolaemus wagleri) co-led by Ryan McCleary.

    Stay tuned for more about the role of snake venom proteins in treating human diseases, and the role of snakes as predators in ecosystems.



    1 Naturally, I wanted to link to the full-text of the paper so that anyone interested in learning more could read it, but the publisher (Wiley) has a 12-month embargo on posting the PDF anywhere online. They actually expect you to pay between $6 and $38 to read the article. Now, I think it's great research, and it probably cost Glaudas, Alexander, and their university thousands of dollars and thousands of hours to do it. But, if you pay Wiley to read their paper, none of that money will go to them, nor to the scientists who peer-reviewed their work for free. It will go to Wiley, who Xav paid (maybe) to publish. They could have paid $3,000 to make it open access, but you can understand why they didn't. No wonder most most science is read by fewer than 10 people. It's an outdated model that can't go away fast enough. In contrast, the spitting cobra paper is open access, which cost its authors over $1,500. This is typical; academic authors almost always lose money on a publication.



    2 Recent update here; you can write the governor of Massachusetts here.



    3 Reports suggest that this year, like last year, a much larger number of live rattlesnakes were collected than markets could support, and at least one person died from a snakebite sustained while trying to capture a rattlesnake for a roundup.

    ACKNOWLEDGMENTS

    Thanks to Bryan Fry for alerting me in advance of his publication, and to Colin Donahue, Markus Oulehla, and Ian Glover for the use of their photos.

    REFERENCES

    Bonnet, X., R. Shine, and O. Lourdais. 2002. Taxonomic chauvinism. Trends in Ecology & Evolution 17:1-3 <link>

    Boyer, L. V. 2016. On 1000-Fold Pharmaceutical Price Markups and Why Drugs Cost More in the United States than in Mexico. The American Journal of Medicine 128:1265-1267 <full-text>

    Boyer, L. V. and A.-M. Ruha. 2016. Pitviper Envenomation Guidelines Should Address Choice Between FDA-approved Treatments for Cases at Risk of Late Coagulopathy. Wilderness and Environmental Medicine. 27:341–342 <full-text>

    Boyer, L. V., P. B. Chase, J. A. Degan, G. Figge, A. Buelna-Romero, C. Luchetti, and A. Alagón. 2013. Subacute coagulopathy in a randomized, comparative trial of Fab and F (ab′) 2 antivenoms. Toxicon 74:101-108 <full-text>

    Cao, N. V., N. T. Tao, A. Moore, A. Montoya, A. Rasmussen, K. Broad, H. Voris, and Z. Takacs. 2014. Sea snake harvest in the Gulf of Thailand. Conservation Biology 28:1677-1687 <full-text>

    Chew, M., A. Guttormsen, C. Metzsch, and J. Jahr. 2003. Exotic snake bite: a challenge for the Scandinavian anesthesiologist? Acta Anaesthesiologica Scandinavica 47:226-229 <full-text>

    Chippaux, J.-P. 2012. Epidemiology of snakebites in Europe: a systematic review of the literature. Toxicon 59:86-99 <full-text>

    Glaudas, X., T. C. Kearney, and G. J. Alexander. 2017. To hold or not to hold? The effects of prey type and size on the predatory strategy of a venomous snake. Journal of Zoology 10.1111/jzo.12450 <abstract>

    Glaudas, X. and G. Alexander. 2017. Food supplementation affects the foraging ecology of a low-energy, ambush-foraging snake. Behavioral Ecology and Sociobiology 71:5 <link>

    Margres, M. J., J. J. McGivern, M. Seavy, K. P. Wray, J. Facente, and D. R. Rokyta. 2015. Contrasting modes and tempos of venom expression evolution in two snake species. Genetics 199:165-176 <full-text>

    McCleary, R. J. and R. M. Kini. 2013. Non-enzymatic proteins from snake venoms: a gold mine of pharmacological tools and drug leads. Toxicon 62:56-74 <full-text>

    Natusch, D. J. D., J. A. Lyons, Mumpuni, A. Riyanto, S. Khadiejah, N. Mustapha, Badiah, and S. Ratnaningsih. 2016. Sustainable Management of the Trade in Reticulated Python Skins in Indonesia and Malaysia. IUCN, Gland, Switzerland <full-text>

    Nyffeler, M. and K. Birkhofer. 2017. An estimated 400–800 million tons of prey are annually killed by the global spider community. The Science of Nature 104:30 <full-text>

    Panagides, N., Timothy N. Jackson, R. Pretzler, M. P. Ikonomopoulou, Kevin Arbuckle, D. C. Yang, S. A. Ali, I. Koludarov, J. Dobson, B. Sanker, A. Asselin, R. C. Santana, I. Hendrikx, Harold van der Ploeg, J. Tai-A-Pin, R. v. d. Bergh, H. M. I. Kerkkamp, F. J. Vonk, A. Naude, M. Strydom, L. Jacobsz, N. Dunstan, M. Jaeger, W. C. Hodgson, J. Miles, and Bryan G. Fry. 2017. How the cobra got its flesh-eating venom: cytotoxicity as a defensive innovation and its co-evolution with hooding and spitting. Toxins 9 <full-text>

    Putman, B. J., M. A. Barbour, and R. W. Clark. 2016. The foraging behavior of free-ranging Rattlesnakes (Crotalus oreganus) in California Ground Squirrel (Otospermophilus beecheyi) colonies. Herpetologica 72:55-63 <full-text>

    Stock, R. P., A. Massougbodji, A. Alagon, and J.-P. Chippaux. 2007. Bringing antivenoms to Sub-Saharan Africa. Nature Biotechnology 25:173-177 <full-text>

    Wade, L. 2014. For Mexican antivenom maker, US market is a snake pit. Science 343:16-17 <full-text>

    Willson, J. D. 2016. Indirect effects of invasive Burmese pythons on ecosystems in southern Florida. Journal of Applied Ecology 10.1111/1365-2664.12844 <full-text>

    Willson, J. D. and C. T. Winne. 2016. Evaluating the functional importance of secretive species: A case study of aquatic snake predators in isolated wetlands. Journal of Zoology 298:266-273 <full-text>

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    The 21st century blindsnake revolution

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    This post will soon become available in Spanish

    Brongersma's Wormsnake (Amerotyphlops brongersmianus),
    a widespread species from South America
    Blindsnakes (Scolecophidia) don't get enough attention. They include the world's most widespread snake species, the world's smallest living snake species, and a diversity of jaw-raking feeding mechanisms unrivaled in bizarreness among land vertebrates. I recently noticed, much to my surprise, the the number of described species of blindsnakes has doubled in the last 13 years, from 305 in 2004 to 599 today; that's 16.5% of all snakes! There are certainly many undiscovered species of blindsnakes, so it's likely that their numbers will continue to grow (as one recent study put it, "...even our most liberal estimates of species numbers will likely prove to be an underestimate of the true diversity...of secretive blind snakes").

    Blindsnake evolutionary tree.
    Extinction of the dinosaurs (K-T boundary) was
    between the green and pink-shaded areas.
    From Vidal et al. 2010
    One of the biggest phylogenetic rearrangements within the Scolecophidia was the recognition of two new families in 2010. The new families Gerrhopilidae and Xenotyphlopidae were formerly part of Typhlopidae, but were discovered to be distantly related to other typhlopids and were separated, although these three families are grouped together in the superfamily Typhlopoidea to emphasize their closer relationship to one another than to the other two families of scolecophidians (Leptotyphlopidae and Anomalepididae). The original diversification of blindsnakes is thought to have been caused by the breakup of Gondwana, whereas the later diversification of Typhlopoidea is associated with the breakup of East Gondwana into Antarctica, Madagascar, India, and Australia (with subsequent colonization by typhlopids from West Gondwana [Africa/South America]). Subsequent diversification within the Typhlopidae coincides with the early Paleozoic Era, just after the extinction of the dinosaurs, and includes four major groups: a Eurasian-Australasian one, an African one, a Malagasy one, and a South American-West Indian one. Because sea levels were low at this time, dispersal among continents and islands was relatively easy, at least for a small vertebrate with low metabolism and most likely travelling along with their invertebrate prey. The relationships of blindsnakes track plate tectonics better than those of any other vertebrate group, perhaps because of their tendency to stay put.

    Gerrhopilus mirus from Sri Lanka
    The two "new" families probably originated on the ancient landmass "Indigascar" (modern India and Madagascar, which were physically connected long after their isolation from other continents and India's subsequent unification with Asia). One family, Gerrhopilidae ("Indo-Malayan blindsnakes"), were formerly known as the Typhlops ater species group. They differ from other blindsnakes in having gland-like structures ‘peppered’ over the head scales. Many species also have a divided preocular and/or ocular scale, and the second supralabialal scale overlaps the preocular in all species but one (G. tindalli). The family contains at least 16 species in the genus Gerrhopilus, and possibly others (the most-recently described species are from 1996 and 2005). This is where it starts to get really weird.

    The 1811 Freycinet map of Australia, where
    Cathetorhinus melanocephalus was not found
    There is another candidate member of the family Gerrhopilidae. The genus Cathetorhinus contains a single species, known from only a single specimen (Natural History Museum, Paris RA-0.138, an adult male). It was collected by French zoologists François Péron and Charles-Alexandre Lesueur on a scientific expedition to Australia led by Nicolas Baudin between 1801 and 1803, and scientifically described (along with an unprecedented and unqeualed number of other new snake species) in the 1844 volume of Duméril & Bibron's opus Erpetologie Générale(the series is also the provenance of the mudsnake plate that I use as a logo for this blog). Cathetorhinus melanocephalus was the only blindsnake they collected, despite visiting the Canary Islands, Mauritius, Timor, and South Africa in addition to Australia (of which members of the expedition later produced the first complete map). Unfortunately, for reasons lost to history and despite their general habits as conscientious collectors1, the location where they found Cathetorhinus melanocephalus was not recorded (I'm speculating here, but it may have been because they were distracted by fearing for their lives—of a total of 24 scientists who went on the expedition, 5 died and 10 disembarked at Mauritius due to illness).

    Cathetorhinus melanocephalus
    From Wallach & Pauwels 2008
    This wouldn't be such a problem (lots of type specimens have vague or missing type localities; Linnaeus correctly attributed fewer than half of his snakes to the right continent "Indiis") except that no other specimens have ever been found. It is taxonomically unique based on its morphology, descriptions of which have been rather inconsistent over the decades, partially because blindsnakes are really small and their scales are really hard to count, especially given the crummy optics of the 19th century. Except for the head glands, Cathetorhinus shares more anatomical characteristics with Gerrhopilus than with any other blindsnakes. A 2008 study reviewed the history of the Baudin expedition and concluded that “the provenance of this species remains unknown: it is certainly Old World, and may be from (in order of probability) Timor, Australia, Mauritius or Tenerife”. And so it would have remained, if not for some really excellent bibliographical sleuthing by biologist and scholar Anthony Cheke, an expert on Mascarene fauna. Cheke reviewed the unpublished original notes made by Lesueur on the voyage, and found a reference to "a very small [snake] species 4–5 inches maximum...the only one found during our stay [on Mauritius in 1803]...found amongst stones while clearing some land...about 8 inches be-low the soil surface". This tantalizing description suggests a blindsnake in size, habitat, and behavior, and although Cheke himself had assumed that it referred to the Brahminy Blindsnake (Indotyphlops braminus), he later realized that the first records of introduction of this widespread species were from 1869, 66 years later.2 Although this isn't concrete proof, it's highly suggestive that Lesueur's blindsnake was Cathetorhinus melanocephalus, since it was the only blindsnake collected on the entire journey.3nbsp;Fossils of an endemic Mauritian typhlopid were discovered around 1900 and described as Typhlops cariei, but direct comparison of the bones with those of Cathetorhinus has not been made. Could Cathetorhinus still survive in the wild? Many non-native blindsnake predators were already introduced to Mauritius when Lesueur and Péron visited, including rats, shrews, and tenrecs, and others have since become established, such as mongeese. Only time, and further field work on Mauritius, will tell.

    Malayotyphlops luzonensis (L), M. denrorum (C), and M. andyi (R)
    From Wynn et al. 2016
    As if that wasn't strange enough, there is a third possible candidate member of Gerrhopilidae: the species known as either Typhlops manilae, Malayotyphlops manilae, or Gerrhopilus manilae. The taxonomic status of this species is currently unclear. It was described by American herpetologist and spy Edward H. Taylor in 1919, from a specimen that was "discovered in the Santo Tomas Museum" in Manila, although even then nobody knew when, where, or by whom it was collected. It appears to have been barely mentioned in the scientific literature until 2014, when its morphological distinctiveness from other members of the Typhlops ater species group/Gerrhopilidae was noted as part of a massive review of typhlopid snakes led by Pennsylvania State University blindsnake specialist and evolutionary biologist Blair Hedges. They suggested it belonged instead to another new genus, Malayotyphlops, also mostly from the Philippines, because it has 28 scale rows (vs. 18 in Gerrhopilus) and a short tail, and because a subocular scale is not unique to Gerrhopilus. Later the same year, a different study disagreed and moved the species back to Gerrhopilus based on the statement from the original description that it has a subocular. However, yet a third study took a close look at Taylor's original description, which contains no illustration, and noted several areas of potential confusion, concluding that without examination of the original specimen, which is still in Manila, "it is not possible to determine to which genus, or even family, T. manilae...belongs".

    The three reptile species originally described by Mocquard
    and re-discovered at Baie de Sakalava in northern Madagascar
    after more than 100 years without records.
    The blindsnake Xenotyphlops grandidieri (pink), and two
    legless skink species: Paracontias minimus (brown with
    longitudinal lines of dark spots) and P. rothschildi
    (beige with black flanks). From Wegener et al. 2013
    Before you get too discouraged, remember that snake biology is replete with tales of rediscovery. Case in point: the other "new" family, Xenotyphlopidae. This bizarre snake has completely lost any traces of visible eyes. It was known solely from the type specimens, described by French zoologist François Mocquard in 1905 and 1906, for more than 100 years. Their precise locality was unknown. However, Hanna Wegener and a term of German, Belgian, and American herpetologists rediscoveredXenotyphlops in 2013 on a coastal dune under a piece of wood in the sand in a littoral forest at Baie de Sakalava in northern Madagascar, along with two endemic legless skinks in the genus Paracontias also described by Mocquard. Because the new specimens of X. grandidieri overlapped the other species in this genus (X. mocquardi) in most morphological characteristics, the two have now been synonymized, making the family Xenotyphlopidae monotypic (for now). These blindsnakes are unique in having a greatly enlarged and nearly circular rostral scale and an enlarged anal shield, and in lacking a tracheal lung.

    The number of less-phylogenetically-distinct but poorly-known blindsnakes is not small. These have received renewed attention due to their placement in new families, but the 21st century blindsnake revolution is just getting started.



    1 Péron and Lesueur also collected the first and some of the only specimens of Bolyeria multicarinata from Mauritius, which is now thought to be extinct, although they mistakenly labeled it as being from Australia.



    2 Today, only I. braminus and another introduced species, I. porrectus, are found on Mauritius; the latter may have also been introduced in the 1800s but was first conclusively documented only in 1993.



    3 A few pieces of evidence against: a length of 4–5 French inches corresponds to 109–136 mm, which is just right for I. braminus but a tad small for the Cathetorhinus specimen, which measures 178 mm (6.6 French inches). Cheke thought that"Lesueur appeared to be writing from memory without the specimen actually before him, so, impressed by its small size, he may have exaggerated how tiny his snake actually was.", maybe the last time in history that somebody underestimated the size of a snake. The other point of confusion is over the exact locality: Lesueur and Péron were clearing land with an upland planter, Toussaint de Chazal, at whose estate in the area now known as Mondrain they were staying. Mondrain is on a plateau adjacent to the Tamarin Gorge, which is 9 km from Grand Bassin, where Lesueur stated that they found the snake.

    ACKNOWLEDGMENTS

    Thanks to Ruchira Somaweera and Sumaithangi Ganesh for the use of their photos.

    REFERENCES

    Cheke, A. 2010. Is the enigmatic blind snake Cathetorhinus melanocephalus (Serpentes: Typhlopidae) an extinct endemic species from Mauritius? Hamadryad 35:101-104 <full-text>

    Duméril, C., G. Bibron, and A. Duméril. 1854. Erpetologie Générale on Histoire Naturelle Compléte des Reptiles. Librairie Encyclopédique de Roret, Paris <link to Cathetorhinus description>

    Hedges, S., A. Marion, K. Lipp, J. Marin, and N. Vidal. 2014. A taxonomic framework for typhlopid snakes from the Caribbean and other regions (Reptilia, Squamata). Caribbean Herpetology 49:1-61 <full-text>

    Kraus, F. 2005. New species of blindsnake from Rossel Island, Papua New Guinea. Journal of Herpetology 39:591-595 <abstract>

    Pyron, R. and V. Wallach. 2014. Systematics of the blindsnakes (Serpentes: Scolecophidia: Typhlopoidea) based on molecular and morphological evidence. Zootaxa 3829:1-81 <full-text>

    Taylor, E. H. 1919. New or rare Philippine reptiles. Philippine Journal of Science 14:105-125 <full-text>

    Vidal, N., J. Marin, M. Morini, S. Donnellan, W. R. Branch, R. Thomas, M. Vences, A. Wynn, C. Cruaud, and S. B. Hedges. 2010. Blindsnake evolutionary tree reveals long history on Gondwana. Biology Letters 6:558-561 <full-text>

    Wallach, V. 1996. Two new Blind snakes of the Typhlops ater species group from Papua new Guinea (Serpentes: Typhlopidae). Russian Journal of Herpetology 3:107-118 <full-text>

    Wallach, V. and O. Pauwels. 2008. The systematic status of Cathetorhinus melanocephalus Duméril & Bibron, 1844 (Serpentes: Typhlopidae). Hamadryad 33:39-47 <full-text>

    Wegener, J. E., S. Swoboda, O. Hawlitschek, M. Franzen, V. Wallach, M. Vences, Z. T. Nagy, S. B. Hedges, J. Köhler, and F. Glaw. 2013. Morphological variation and taxonomic reassessment of the endemic Malagasy blind snake family Xenotyphlopidae. Spixiana 36:269-282 <full-text>

    Wynn, A. H., R. P. Reynolds, D. W. Buden, M. Falanruw, and B. Lynch. 2012. The unexpected discovery of blind snakes (Serpentes: Typhlopidae) in Micronesia: two new species of Ramphotyphlops from the Caroline Islands. Zootaxa 3172:39–54 <full-text>

    Wynn, A. H., A. C. Diesmos, and R. M. Brown. 2016. Two new species of Malayotyphlops from the northern Philippines, with redescriptions of Malayotyphlops luzonensis (Taylor) and Malayotyphlops ruber (Boettger). Journal of Herpetology 50:157-168 <full-text>

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    Snakes of Morocco

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    Earlier this month I went to Morocco to attend the 5th Biology of the Vipers conference. The conference was organized by Fernando Martínez-Freiría and Soumia Fahd and featured a fantastic three-day scientific program in Chefchaouen followed by a six-day field excursion to southern Morocco to look for snakes. I learned a lot and got lots of great feedback on Life is Short but Snakes are Long, but unfortunately I didn't have time to finish writing May's article, which I aim to put up next week. On the way back, I also stopped by Jerez de la Frontera and finally met Alvaro Pemartin and Estefania Carrillo, whose dedicated translations have brought Life is Short but Snakes are Long to Spanish-speaking readers around the world!

    Montpellier snake (Malpolon monspessulanus)

    Saharan horned viper (Cerastes cerastes)

    Puff Adder (Bitis arietans)

    Egyptian Cobra (Naja haje)
    Me on the streets of Chefchaouen

    Me looking for vipers in  Toubkal National Park
    Estefania and I in Jerez
    We also met with an Aisaoua, a member of the traditional brotherhood of snake hunters in Morocco, who collect the snakes that are used by the snake charmers who put on shows. This tradition is at least 800 years old, and possibly as old as 2,000 years, and is an example of a human-reptile interaction with both positive and negative aspects. It was really interesting to see their method for finding snakes—they are very effective! More on this in a future article.

    ACKNOWLEDGMENTS

    Thanks to Konrad Mebert and Alvaro Pemartin III for allowing me to use their photographs, 

    REFERENCES

    Bons, J., P. Geniez, A. Montori, V. Roca, and E. Asociación Herpetológica. 1996. Amphibiens et reptiles du Maroc (Sahara Occidental compris) : atlas biogéographique = Anfibios y reptiles de Marruecos (incluido Sáhara Occidental) : atlas biogeográfico = Amphibians & reptiles of Morocco (including Western Sahara) : biogeographical atlas.

    Pleguezuelos, J. M., M. Feriche, J. C. Brito, and S. Fahd. 2016. Snake charming and the exploitation of snakes in Morocco. Oryx :1-8 <link>

    Tingle, J. L. and T. Slimani. 2017. Snake charming in Morocco. The Journal of North African Studies :1-18 <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.
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