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Wednesday, August 17, 2016

Why snakes are long (and other recent updates)

This post will soon be available in Spanish 

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

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

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

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

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

Conservation Successes with Indigo Snakes

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

Malagasy Leaf-nosed Snakes

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

Do Snakes Sleep?

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

The 9,999th Reptile

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

Identifying Snake Sheds

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

ACKNOWLEDGMENTS

Thanks to John Iverson for the use of his photo.

REFERENCES

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

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

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

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

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

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

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

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

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

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

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

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

Creative Commons License

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

Friday, July 1, 2016

What the Provincial Snakes of Canada Should Be

This post will soon be available in Spanish!

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

Wednesday, June 8, 2016

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

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

Saturday, May 28, 2016

Rattlesnake Roundups Revisited

This article will soon be available in Spanish

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 21,000 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. [Edit: An analysis from 2000 showed that imposing size restrictions on rattlesnake harvests to individuals >90 cm in SVL (the size at maturity for most females) would earn hunters 19% more money.] 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.

Fitzgerald, L.A. and C.W. Painter. 2000. Rattlesnake commercialization: Long-term trends, issues, and implications for conservation. Wildlife Society Bulletin 28:235-253 <link

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.