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Showing posts with label Psammophis. Show all posts
Showing posts with label Psammophis. Show all posts

Friday, October 30, 2015

Are there any countries without snakes?


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.




Wednesday, March 19, 2014

Why do snakes have two penises?


Figure from Laszlo 1975
Recently somebody asked me "Why do snakes have two penises?" When I tried to answer, I realized that I didn't really know. I did know that they only use one at a time, and I had once heard that it was so that they could copulate with a female no matter which side she was on, but that doesn't really seem to make sense to me any more, especially considering that lizards also have two penises. Together, the two penises of squamates (snakes and lizards) are called hemipenes, and each individually is called a hemipenis. Each hemipenis is associated with a single testis, meaning that sperm produced in the right testis are ejaculated through the right hemipenis, and those produced on the left come out of the left. Hemipenes are normally stored inside out in the base of the tail, forming a pocket into which a probe can be, well, probed to check the sex of a lizard or snake. This is shown nicely in the above diagram. During mating, one hemipenis or the other is everted in a manner similar to taking off a sock. Sexual dimorphism is rare in snakes, except that male snakes almost always have longer, thicker tails than females, because they need someplace to store their hemipenes.

Some examples of snake hemipenes; photo by Robert Jadin
Hemipenes are one of the shared derived characters of squamates (snakes and lizards), distinguishing them from other reptiles (tuataras, turtles, crocodilians, and birds), all of which have either a single or no penis. In general, snake hemipenes are endowed with a groove, called the sulcus spermaticus, down which the sperm runs. Think of a canal rather than a pipe, although during mating the wall of the female's reproductive tract forms the other part of the tube that we mammals have. Hemipenes often have various spines, knobs, branches, and other projections, which typically correspond with the cloacal anatomy of female snakes of the same species, forming a sort of 'lock-and-key' mechanism that isolates species by discouraging mating among unrelated individuals. The amazingly variable structure of the hemipenes has often been used in snake taxonomy for this reason.

Hemipenes of:
top: Mountain Pit-viper
(Ovophis monticola)
middle: Spotted Slug-eater
(Pareas macularius)
bottom: Siamese Spitting Cobra
(Naja siamensis)
photos by Sjon Hauser
But why two? Wouldn't one penis do just as well, since male snakes only use one at a time anyway? Let's take a quick look at the timeline of snake reproduction. Boy snake meets girl snake. They spend some time together, intertwine their tails, and the male inserts one hemipenis so that his sperm find their way safely from cloaca to cloaca. But unlike in humans, female snakes have a lot of control over whether or not they get pregnant after mating. Because the best conditions for mating are not necessarily the best for ovulation and gestation, female snakes can store sperm for a long time, up to 5 years and possibly longer. They have specialized pockets in their reproductive tract where they do this. It can actually be rather difficult to distinguish between long-term sperm storage and facultative parthenogenesis (a form of asexual reproduction) without using molecular techniques to determine whether the offspring share all or just some of their genes with their mother. This is because in the former case, a female snake sometimes gets pregnant long after mating. If she has mated with multiple males, her clutch (in egg-laying species) or litter (in live-bearers) of offspring might be a mixture of offspring from multiple fathers. Amazingly, she can control which fathers' sperm she uses to fertilize her eggs, although exactly how she does this is still unclear. Because of this potential for delayed fertilization, sperm competition and cryptic female mate choice is thought to be more intense in reptiles than in species that usually follow insemination quickly with fertilization. Female snakes can mate with multiple males, and can then choose at their leisure among their sperm each time they reproduce over the next several years, so some male snakes might mate with many females but never produce offspring because their sperm are always judged to be inferior. This can also result in bizarre situations such as male snakes becoming fathers after they have died.

All this can complicate life for male snakes, because their paternity is even less certain than it is for other male vertebrates. As a result, a male snake's reproductive success is probably tied to the number of sperm he transfers to a female (although this is difficult to measure). This is probably a big part of why male snakes and lizards have two penises. Because each testis is dedicated to a single hemipenis, an alternating pattern of hemipenis use would allow a male a second chance to transfer a fresh batch of sperm if he has just mated recently. In humans and most other mammals, sperm from both testes is mixed together prior to ejaculation, so these species have just one chance to inseminate before they enter a refractory period (you know what I mean, guys). In fact, an alternating pattern is what we see when the kind of experiments every snake dreams of being a part of are conducted (in the spirit of full disclosure, most of these experiments were conducted with lizards, but the principle is similar). A male lizard mates with one female, which depletes sperm from that side of his reproductive tract, but he can then use his other hemipenis to inseminate a different female. He only alternates if the second mating opportunity comes during the refractory period, which lasts a few days. If mating opportunities are frequent and he is prevented from alternating (by placing a small piece of tape over one side of his cloaca), his sperm count is much lower on his second and third mating attempt.

Mating Western Diamondbacks, Crotalus atrox (from Clark et al. 2014)
It's advantageous for a female snake to mate with as many males as she can, so that she has a wide variety of sperm to choose from. Female adders with more mates have higher offspring survival, probably due to less inbreeding and more genetic diversity to choose from, especially in regions of the genome where diversity is important, such as the MHC, which codes for proteins involved in recognizing pathogens and initiating an immune response. Many species, including humans, select their mates at least partly on the basis of MHC dissimilarity (which they can judge by smell), and this may also be the case in snakes. However, many male and female snakes often have pretty limited time to get together, since they're only in the same place at the same time for short periods in spring and fall when they're entering and leaving hibernation sites, which might mean that they have to make rapid decisions about who to mate with. However, a recent paper by Rulon Clark and others showed that male Western Diamondback Rattlesnakes have distinct mating strategies depending on their body size. Larger males were more likely to guard their mates throughout the active season. Curiously, this behavior did not result in their fathering more offspring, possibly due to sperm the females had stored from previous years. In one of the most extreme examples of clustered mating, Common Gartersnakes in Canada emerge in huge numbers in spring and mate immediately upon emergence. Unlike in most snakes, there is conflict between males and females over how each sex best maximizes their reproductive success. There's also some evidence that male gartersnakes are "right-handed", preferring to use their right hemipenis unless they have just used it recently (it's connected to the larger right testis in this species). There are fewer studies of the mating systems of tropical snakes, which do not hibernate at all, but I suspect there is more diversity in parts of the world where it is always warm (we just don't know about it yet). One study found that larger male Slatey-grey Snakes (Stegonotus cucullatus) from tropical Australia fathered more offspring than smaller males, which is similar to the situation in many temperate snakes, but the exact evolutionary causes of this phenomenon are complex and have yet to be explained.

Hemipenes of:
top: Indo-chinese Ratsnake
(Ptyas korros)
middle: Banded Kukrisnake
(Oligodon fasciolatus)
bottom: Common Blackhead
(Sibynophis collaris)
All this raises some questions regarding the evolution of penises in vertebrates. I looked but could not find a single instance where a species of squamate had lost their hemipenes. The closest I came are snakes in the African subfamily Psammophiinae (which also includes the enigmatic scale-polishing snakes), which have small hemipenes and peculiar copulatory behavior, the causes and consequences of which are only two of the many things we don't know about psammophiines. The asymmetrical testes of male gartersnakes might be another example, but their left and right hemipenes are of equal size. Because penises don't fossilize well, we don't know very much about the anatomy of ancient snakes and lizards, but it's safe to assume that the common ancestor of all squamates had hemipenes. Although several other reptiles have lost their penises (and in some cases re-evolved some truly bizarre structures, such as the penises of ostriches, emus, ducks, alligators, turtles, and maybe even dinosaurs), there are some similarities between squamate hemipenes and the male reproductive organs of some of the most primitive mammals, the monotremes. Like snakes but unlike other mammals, echidnas have internal testes connected separately to a four-headed penis, similar to the hemipenes of snakes and lizards but joined at the base. Male echidnas only use one side (bearing two heads) at a time (video here), alternate sides just like snakes, and their sperm work cooperatively to reach the egg. The other monotremes, platypuses, have a forked penis, but only the left side is functional, because only the female's left ovary is functional. Many marsupials also have bifurcated penises, with scrotums that hang down in front of them. This suggests that a bifurcated penis might have appeared much earlier in amniote evolution than we think, although it could also be a case of convergent evolution caused by intense post-mating sexual selection on males. Detailed histological, embryological, and genetic studies would be required to answer this question, which would probably constitute the dissertation project you'd least want your family to know about. (update: I found out that Casey Gilman. a PhD student at UMass Amherst is working on this for his dissertation as we speak. You can donate to his crowd-funded project here).

ACKNOWLEDGMENTS

Thanks to Robert Jadin and Sjon Hauser for use of their photographs.

REFERENCES

Booth, W. and G. W. Schuett. 2011. Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long-term sperm storage and facultative parthenogenesis. Biological Journal of the Linnean Society 104:934–942 <link>

Clark, R. W., G. W. Schuett, R. A. Repp, M. Amarello, C. F. Smith, and H.-W. Herrmann. 2014. Mating Systems, Reproductive Success, and Sexual Selection in Secretive Species: A Case Study of the Western Diamond-Backed Rattlesnake, Crotalus atrox. PLoS ONE 9:e90616 <link>

Dubey, S., G. P. Brown, T. Madsen, and R. Shine. 2009. Sexual selection favours large body size in males of a tropical snake (Stegonotus cucullatus, Colubridae). Animal Behaviour 77:177-182 <link>

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

S. D. Johnston, B. Smith, M. Pyne, D. Stenzel, and W. V. Holt. 2007. One‐Sided Ejaculation of Echidna Sperm Bundles. The American Naturalist 170:E162-E164 <link>

Laszlo, J. 1975. Probing as a practical method of sex recognition in snakes. International Zoo Yearbook 15:178-179.

Madsen, T., R. Shine, J. Loman, and T. Håkansson. 1992. Why do female adders copulate so frequently? Nature 355:440-441 <link>

Olsson, M. and T. Madsen. 2001. Promiscuity in Sand Lizards (Lacerta agilis) and Adder Snakes (Vipera berus): Causes and Consequences. Journal of Heredity 92:190-197 <link>

Sever, D. M. and W. C. Hamlett. 2002. Female sperm storage in reptiles. Journal of Experimental Zoology 292:187-199 <link>

Shine, R., M. M. Olsson, M. P. LeMaster, I. T. Moore, and R. T. Mason. 2000. Are snakes right-handed ? Asymmetry in hemipenis size and usage in gartersnakes (Thamnophis sirtalis). Behavioral Ecology 11:411-415 <link>

Tokarz, R. R. and J. B. Slowinski. 1990. Alternation of hemipenis use as a behavioural means of increasing sperm transfer in the lizard Anolis sagrei. Animal Behaviour 40:374-379 <link>

Tokarz, R. R. and S. J. Kirkpatrick. 1991. Copulation frequency and pattern of hemipenis use in males of the lizard Anolis sagrei in a semi-natural enclosure. Animal Behaviour 41:1039-1044 <link>

Zweifel, R. G. 1980. Aspects of the biology of a laboratory population of kingsnakes. Pages 141-152 in J. B. Murphy and J. T. Collins, editors. Reproductive biology and diseases of captive reptiles. Society for the Study of Amphibians and Reptiles, Lawrence, Kansas.

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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, November 10, 2012

Snakes that polish their scales, and why they do it


Psammophis schokari eating a lizard, Phrynocephalus
mystaceus
, in Kazakhstan
I really like these snakes, and they have about them a pretty interesting mystery. In the tribe Psammophiini (in family Lamprophiidae), there are at least 50 species of snake in 8 genera native to Africa, the Mediterranean, the Middle East, and central Asia. They are united by several unusual synapomorphies, the most unique of which is the presence of a morphological feature called the external narial valve. This structure, located in the loreal region between the eye and the nostril, is the outlet of a special nasal gland that secretes fluid containing long-chain fatty acids. The function of this secretion is enigmatic. Some experiments show that it can serve to retard evaporative water loss, and some evidence suggests that some of these molecules could be pheromones used in marking territories. Territoriality is only slightly less non-existent among snakes than herbivory, but according to some it is apparently present among certain psammophines, few of which have been well-studied in the wild. Aside from a very interesting study suggesting that releasing small mammals from competition with large herbivores can indirectly increase the abundance of their snake predators (including Psammophis mossambicus), we don't know much about their ecology, but careful observations have revealed a little about the lives of these intriguing snakes.

Subadult Montpellier snake, Malpolon monspessulanus
The external narial valve was described in 1956 by renowned Russian herpetologist Ilya Darevsky, the second person ever to earn a PhD in the Soviet Union and the discoverer of parthenogenesis and polyploidy in reptiles. Darevsky described the gland from a specimen of the Montpellier snake (Malpolon monspessulanus), and such glands have now been reported from all eight genera in the Psammophini. In addition to the gland, psammophines also share peculiar hemipene morphology - that is, the male reproductive organs are unusually thin and smooth for an advanced snake, most of which possess thick, spiny hemipenes that enable prolonged copulation. Sexual dimorphism is also quite pronounced in many of these snakes, although not of tail length (typically, the tails of male snakes are longer and thicker than those of females). For example, male M. monspessulanus are stout, uniformly colored, and up to 2.3 m long, whereas females are slender, spotted, and reach only 1.4 meters.

Beginning in 1898, the earliest observations of these snakes mention their peculiar behavior. Psammophines press the outlet of their narial valve to their skin and thoroughly apply a coating of colorless, fast-drying valve secretion all over their body. Watch this Malpolon insignitus to get an idea, because it's hard to describe.




This behavior has been variously called self-rubbing, self-polishing, or  grooming, and seems to be present in all species of psammophine observed. Several keepers in Europe have made extensive efforts to acquire and videotape species of psammophines, and self-rubbing has now been documented in seven of the eight genera. More intriguing, conspecific psammophines housed together occasionally rub one another, presumably anointing the other snake with secretion from their narial valve. What could this mean?


Psammophis leightoni from Namibia
Several hypotheses have been put forth to explain this unique and intriguing behavior. To date, none have been sufficiently tested to unequivocality, nor are they mutually exclusive. Prior to the 1970s, the prevailing thought was that, since psammophines generally inhabit arid regions, the gland might aid in salt excretion, evaporative cooling, or water retention. In 1978, William Dunson and colleagues published their work on the histology of the gland, and concluded that it did not contain the specialized cytological features associated with salt secretion in the salt glands of reptiles such as sea snakes and marine iguanas. Dunson also characterized the chemical composition of the secretion for the first time, and suggested that the long-chain fatty acids he found might help retard water loss through the skin.


Dunson tested five Malpolon to see if their dermal water loss was unusually low, and indeed it was, approximately ten times lower than that of Kingsnakes (Lampropeltis getula), although water loss rate varied depending on where in the shedding cycle the snakes were. Malpolon also lost proportionally more water via the mouth and cloaca (and less via the skin) than did other reptiles. Dunson also kept Malpolon without giving them access to water, and they did not lose weight, indicating that they were capable of obtaining all the water they needed from their prey. In another experiment, he showed that dehydrated Malpolon did not secrete salt from their narial valve. He made the interesting observation that several frog species of the genus Phyllomedusa decrease their dermal water loss by wiping lipid secretions from skin glands over the surface of their skin:




Could psammophids be accomplishing the same thing with their narial valve secretions? Dunson did not test whether snakes that had just applied the secretion lost less water than those that had not. The snakes polish themselves frequently, especially after ecdyisis and feeding, so water loss rate could be tracked over time. 

Other mysterious pits have been described from the head scales of psammophines: parietal pits on the top of the head and infralabial pits on the lower jaw, both of which seem to be sporadically occurring. Series of shed skins from the very same snake sometimes show these features and sometimes do not. Because histology is lacking for these features, it is difficult to say what they might represent.


Dipsina multimaculata
Because of the remote areas inhabited by many of these snakes, most studies to date are insufficiently replicated to permit concrete conclusions about the function of the polishing behavior. Furthermore, determining the sex of living psammophines is quite difficult on account of their small hemipenes, so behavioral studies are often hampered by inadequate knowledge of the sex of the animals involved. Observations of captive psammophines suggest that these snakes have complex social behaviors, not the least of which is their tendency to polish one anothers' scales. Could this behavior represent mate guarding? A nuptial gift from males to females of fatty acids to help them avoid water loss during pregnancy? Do these snakes mark their territories? Only replicated, scientific studies will tell; until then, competing hypotheses will continue to wax on and wax off.


ACKNOWLEDGMENTS

Thanks to Heather Heinz for drawing my attention to this fascinating system, to Jane Bugaeva for translating Darevsky's 1956 article from Russian, and to photographers Bernard Dupont, Altyn Emel, Michael & Patricia Fogden, and Jeremy Holden, and videographer Ton Steehouder.

REFERENCES

Microdermatoglypic SEM photograph of Dipsina scale.
The lipid layer covering the scale is visible.
From de Pury 2010
Darevsky IS (1956) O stroyenni i funktsionirovani nosovoy zhelezy u yashtsheritsnoy zmei Malpolon monspessulanus Herm. (Reptilia, Serpentes). [On the structure and function of the nasal gland in the lizard snake Malpolon monspessulanus Herm. (Reptilia, Serpentes)] Zoologicheskij Zhurnal-Moskva 35:312-314

Dunson WA, Dunson MK, Keith AD (1978) The nasal gland of the Montpellier snake Malpolon monspessulanus: fine structure, secretion composition, and a possible role in reduction of dermal water loss. Journal of Experimental Zoology 203:461-473

de Grijs P (1898) Beobachtungen an reptilien in der gefangenschaff. Zoologischer Garten 39:233-247

de Haan CC, Aymerich M (2012) Des comportements frotteur et marqueur, pour la chasse et la vie sociale. In: Aymerich M (ed) A la Découverte de la Faune du Maroc Oriental

de Haan CC, A Cluchier (2006). Chemical marking behaviour in the psammophiine snakes Malpolon monspessulanus and Psammophis phillipsi. Proceedings of the 13th Congress of the Societas Europaea Herpetologica, 211-212. <link>

Mimophis mahfalensis killing a chameleon in Madagascar
de Haan CC (2003) Extrabuccal infralabial secretion outlets in DromophisMimophis and Psammophis species (Serpentes, Colubridae, Psammophiini). A probable substitute for ‘self-rubbing’ and cloacal scent gland functions, and a cue for a taxonomic account. Comptes Rendus Biologies 326:275-286. <link>

de Pury S (2010) Analysis of the Rubbing Behaviour of Psammophiids: A Methodological Approach. PhD dissertation, Rheinischen Friedrich-Wilhelms-Universität Bonn, Bonn, Switzerland.

McCauley, D. J., Keesing, F., Young, T. P., Allan, B. F. & Pringle, R. M. 2006: Indirect effects of large herbivores on snakes in an African savanna. Ecology 87, 2657-2663. <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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