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Tuesday, October 28, 2014

How to teach yourself about an obscure snake


The world is full of obscure snakes. According to Darren Naish at Tetrapod Zoology, the more you know about them, the better a person you are. Writing this blog, and in my research, I am often confronted with the challenging task of finding out something—anything at all—about a species of snake that I've never heard of before. This post is a walk-through of the process that I usually use to track down even the most basic information about obscure snakes, although it could be used as an example of how to find trustworthy information about any species of plant or animal. I'll use as an example the species Liophidium mayottensis (Peters's Bright Snake) - a lamprophiid colubroid found on the island of Mayotte. If you're like me then you're filled with questions right away: Who was Peters? What is so bright about this snake? Where's Mayotte?

Wikipedia page for Liophidium mayottensis
as of October 2014
I needed to know about this snake as part of a project I'm doing where we compare endangered species of reptiles with those that aren't to try and figure out if there are traits or features that the endangered species have in common (and the same for invasive species and other special groups; the results of the project were eventually published here). This kind of thing has been done for birds and fish, but not really for reptiles. It's a much larger effort than just me, and my part in it is small, usually tracking down basic information about the reptiles so that we can build a database of reptile life history traits. I'm talking about things like size, sexual dimorphism, whether they lay eggs or give birth to live young, how many eggs or young they have at a time and how often, where and in what kind of habitats they live, what they eat, that kind of thing. Sounds simple, right? We'll just go to Wikipedia...well, as of 2014 that wasn't very helpful.

When faced with a species about which I know almost nothing—in this case a species I had never even heard of before—there are a couple of resources that I generally go to first in order to figure out how I should proceed. The first is always The Reptile Database. This wealth of information is curated by Peter Uetz, Jakob Hallermann, and Jiri Hosek, three individuals to whom the whole of the herpetological world is indebted. Using the advanced search feature, you can look up any species of living reptile using its common or scientific name, including by an old scientific name (a "synonym") that is no longer used. This is important because scientific names change all the time, and sometimes the same species has gone by 10 or 20 different names over the course of its taxonomic lifetime. It is particularly important to know about these names because the species may have gone by them for a long time in older literature, which is sometimes the most important literature there is.

Liophidium mayottensis
Before searching TRD, I sometimes try to use the scientific name itself to figure out a little bit about what I'm looking for. It helps to know some Latin and Greek, and a handy reference that I use a lot is Borror's Dictionary of Word Roots and Combining Forms. In this case, the genus name Liophidium told me that this was a snake with smooth scales (the Greek prefix lio- meaning smooth + the Greek root ophid meaning snake + the Latin suffix -ium normally used to form abstract nouns). The specific epithet mayottensis means "from Mayotte" (the -ensis suffix is a common way to form an adjective indicating spatial or geographic origin in Latin, similar to the English suffix -ese, as in Maltese, Chinese, or Portuguese). Although the Latin and Greek origins of the scientific name can be helpful, they can also be misleading (for example, the North American Racer is called Coluber constrictor even though it is not a constrictor) or unhelpful (another familiar North American snake, Storeria dekayi, is named after two 19th century herpetologists, David H. Storer and James E. DeKay), so don't rely too much on these.

The Madagascan Biogeographic Realm
Mayotte is the southeasternmost island in the
Comoros chain, although politically it is part of France.
Many interesting snakes inhabit this realm, including bolyeriids
When searching TRD, I always put the full binomial I'm looking for into the 'Synonym' field of TRD's Advanced Search, because the 'Genus' and 'Species epithet' fields only search the current names, and who knows what name it goes by now. Barring any misspellings, at least one record usually turns up, sometimes more if the name I've used has been split into multiple species. In this case, it's just one, and it matches the name I used. So far, so good. From this record, I can find out the currently accepted higher taxonomy of my species. In addition to being a snake (which I already knew), I can see that it's in the recently-erected family Lamprophiidae, a group of snakes found mostly in Africa. Furthermore, I can see that Liophidium mayottensis is in the subfamily Pseudoxyrhophiinae, a group of snakes found almost exclusively in Madagascar. Because Mayotte is an island in the Comoro Island chain, lying just northwest of Madagascar, this subfamilial designation makes sense—we think that lamprophiids colonized Madagascar, Socotra, and the Comoros from Africa about 30 million years ago, one of several radiations of snakes onto these islands. However, in this case knowing the subfamily doesn't help us much in our search for natural history information. Unlike certain instantly-recognizable groups of snakes such as pareatids or xenodermatids, pseudoxyrhophiines are diverse, including almost 90 species with a wide variety of lifestyles. I've written about the genus Langaha, which belongs to this group, before.

The BHL is also a great source of artwork
in the form of old plates, like this mudsnake
from Duméril's Erpétologie Générale,
which adorns the logo of this blog
In order to go further we need look at the rest of the TRD record. Since we're looking for a description of the species, one of the most helpful pieces of information is the location of the original description in the scientific literature. You'll find the name of the person who originally described the species and the year they did it in the TRD record, right next to the scientific name. This is called the authority, and it's presented in parentheses if the name that person used has subsequently been changed. For instance, 11 of the 139 reptile species described by Linnaeus, the father of modern taxonomy, still retain the original names he gave them. You can tell because these are the ones without parentheses. If you look to the bottom of the record, you'll find a citation for the book or article in which that first description resides, along with other literature pertinent to the species. This literature is usually focused on taxonomic changes, although sometimes more general ecology or natural history literature is included as well. Following up on this literature is easier in some cases than others. One thing TRD has done to make it simple is provide links to the full-text if it's available for free online somewhere. A lot of older literature is becoming available through the Biodiversity Heritage Library, a partnership of libraries that have digitized what they call the "legacy literature" of biodiversity.

Wilhlem C.H. Peters
Our species was originally described in 1874 by Wilhelm Carl Hartwig Peters, a German naturalist and explorer, which explains the first part of the common name Peters's Bright Snake (which was probably not applied until much later, since it's considered presumptuous to name a species for oneself). Peters called it Ablabes (Enicognathusrhodogaster var. mayottensis, a confusing mess if there ever was one. His description was published in the journal Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin (which is obfuscatingly abbreviated Monatsber. Königl. Akad. Wiss. Berlin.), which roughly translates to 'Monthly Reports of the Royal Prussian Academy of Sciences in Berlin'. Not exactly the most widely read journal, even if it has existed in one form or another since 1700 and is still around today. Anyway, it's in German, so it'll prove difficult for us to read Peters's original description even if we can find it (which thanks to the BHL, we can). There's also the little problem of whether the issue it's in was published in 1873 or 1874, because the citation in TRD lists both, but fortunately we can check both quickly since the page numbers are also given (it's '73). The article starts on this page and the description is on this one. These days descriptions of new species usually get their own stand-alone articles, but back then it was common practice to shoehorn them into checklists, expedition reports, and other types of articles. There's a description of a new chameleon in the same article. In a way, it's one explanation for the prolific output of Peters, who described 122 new genera and 649 new species of amphibians and reptiles in his lifetime, 281 of which are still recognized today (only four people, all his contemporaries, have described more). The high attrition is partly because many species were inadvertently described more than once. The guys at TRD have done a fabulous job keeping track of all this confusing literature, and I cannot commend them highly enough for their efforts.

Another difference between the 1800s and now is that species descriptions today are generally much more complete. You might be surprised to learn that the International Commission on Zoological Nomenclature, which advises, arbitrates, and recommends rules for the zoological community on describing new species of animals, stipulates only that in order for a species description to count as official, it must include at a bare minimum just "a description or definition that states in words characters that are purported to differentiate the taxon", and even this 'strict' definition applies only to names published after 1930. Peters's description of Liophidium mayottensis (translated) reads:
17. Ablabes (Enicognathus) rhodogaster Schlegel var. mayottensis: 
Two young specimens from Mayotte seem to me to belong to the above species, although they do not have red coloration on the belly. Frontal a little longer than high; 8 supralabials, of which the 4th and 5th touch the eye; temporals 1+2+2; infralabials 9, the first pair of which is in contact behind the tapered mental; two pairs of chin shields. Body scales smooth, without apical pits, in 19 longitudinal rows. Ventrals 190, divided anal, subcaudals 99 pairs. Above olive-brown, a little darker along the middle and fourth-to-last row of scales. From the snout through the eye and the frenal region there is a black band which is indistinct on the side of the neck and disappears in the penultimate row of scales on the side of the body. Under this there is a bright yellow band, which goes to the mouth. There are three black spots on the rostral and upper lip. The chin and infralabials are spotted or marbled with black and yellow. On the neck are fine yellowish transverse lines. Ventral scales with 4-6 black dots; posterior ventral scales and subcaudals yellowish-white.
Liophidium rhodogaster
Gold-collared Snake
So we've got counts of the scales and descriptions of their position relative to one another, which is considerably more than it took back in the 1870s to name a new species. No drawings, no information on size, habitat, reproduction, nothing. It's forgivable when you know that Peters, by then a museum curator, was merely reporting on a collection of amphibians and reptiles he had been sent from Madagascar and nearby islands by two guys named Pollen and van Dam. Peters thought the snakes they had collected on Mayotte were a variant of a species that had already been described, the Gold-collared Snake of Madagascar, known then as Enicognathus rhodogaster and today as Liophidium rhodogaster (rhodogaster meaning 'red belly'). We learn from TRD that twenty years later Belgian-British zoologist George Boulenger (writing, mercifully, in English) elevated Ablabes (Enicognathusrhodogaster var. mayottensis to its own species and changed the genus so that it was known as Polyodontophis mayottensis. Boulenger is even lighter on details than Peters, saying only that it is very similar to rhodogaster but differs in that it has one more pair of dorsal scale rows, about 11 more ventrals, and about 15 more subcaudals, and that its neck pattern includes the same yellow lines mentioned by Peters. Since he's not trying to describe a new species, it's OK, but it's frustrating since we're looking for more detail about the animal's ecology and natural history.

It's likely that neither Peters nor Boulenger ever saw Liophidium mayottensis, or many of the other species they described, alive, so we can forgive them for not mentioning its habitat or patterns of activity (although they could have at least measured the specimen). Sometimes museum specimens yield information about diet (via stomach contents) or reproduction (via eggs or embryos in utero), but this does not seem to be the case for Peters's Bright Snake. To learn about these things, we'll have to sleuth out some other papers. The other two listed at TRD don't look too promising - one is a biography of Peters that's only available in print, and the other focuses on a different genus, Sibynophis, that's superficially similar to Liophidium but distantly related.

We can do a little better by checking some other common sources of information on the web. We already know that Wikipedia's useless (although the links at the bottom of some pages can be quite useful), but a general Google search for the scientific name typically turns up links to the pages for a species on several authoritative sites that aggregate biodiversity information online. In no particular order, I often check the University of Michigan Museum of Zoology's Animal Diversity Web. This is a great student-authored resource but it's still incomplete, and it doesn't even have a page for our genus yet (but check out their detailed pages on all three Acrochordus species). Other similar sites include the Encyclopedia of Life (species page incomplete for L. mayottensis, but check out Laticauda colubrina for a fairly good page), DiscoverLife (which is mostly links with little original content, and is unhelpful for our species, although they host a cool ID guide for North American snakes), and Map of Life (which has lots of cool mapping capabilities but not for our species). Citizen science projects can be a rich source of information on distribution, but such projects are in their infancy for herps. Two of the best are iNaturalist and HerpMapper, neither of which has any data on our species [Edit 11/4/2015: there is now a single iNaturalist record; a second record was entered on January 22, 2017]. Remember that none of these sources are peer-reviewed, so they may propagate misinformation (although I have found this to be rare).

One of Pagale Bacha's Flickr photos of L. mayottensis
ARKive is a film and image archive that generally has pictures of rare species when most other websites fail, and that is the case here, but as of 2014 it contained no additional information (contrast with their excellent accounts for snakes like Natrix natrix and Macroprotodon cucullatus). Flickr can be a good source of images too, in this case providing us with four additional images, all taken by the same person of the same individual snake. I have noticed that a culture of accurate species identification exists on Flickr that isn't found elsewhere on the Internet. For instance, don't ever trust Google Images when searching for rare species - in this case, only one of the hundreds of images returned is actually of our snake [Edit 11/4/2015: it's gotten a little better since I put up this post.]. Earlier I mentioned the Biodiversity Heritage Library, one of the most consistently useful resources on the web, and their search feature leads us to one new resource: a mention in a paper by John Cadle from 1999, focusing on morphological taxonomy of  Malagasy snakes (which states that Liophidium are diurnal and led me to a paper describing the smooth, hinged, spatula-shaped teeth of Liophidium and other snakes, an adaptation for grasping and swallowing hard-bodied prey, such as skinks their teeth fold backwards when forces are applied to their leading surface, but lock into an erect position if forces come from behind).

Some L. mayottensis DNA. It looks just like the DNA
of any other species, although there's a lot it can tell us.
Two other online databases are more authoritative than those previously mentioned, in that they are reviewed by experts. One is GenBank, the NIH genetic sequence database. A GenBank search reveals that five genes have been sequenced from L. mayottensis, which is more than for most reptilesThese include four mitochondrial genes (ND4CO1, and cyt-b, which are essential to the electron transport chain of cellular respiration, and 16S, part of the protein synthesis machinery of ribosomes) and one nuclear gene (c-mos, which plays a role in mitosis). These genes were chosen for their conserved functions and relatively slow rates of evolution, which makes them useful for phylogenetic purposes (except for CO1, which evolves at just the right rate for DNA barcoding, a technique which is used, among other things, to monitor trade of reptiles without specialized expert knowledge). A phylogenetic analysis was done to determine the relationship of Liophidium pattoni, a new species discovered in Madagascar in 2009, to the other species in the genus. The results placed L. pattoni as sister to L. rhodogaster, and L. mayottensis as sister to two other Malagasy species, L. torquatum and L. chabaudi. This may seem like a dry, mundane detail, but it actually tells us something very interesting about our species: it probably colonized Mayotte from Madagascar after the ancestors of Liophidium had already radiated there. It also says that Peters, who thought that L. mayottensis was a subspecies of L. rhodogaster, was way off - it's actually more closely related to almost any other member of the genus (although to be fair to Peters, none of those other members had been described yet when he named L. mayottensis — and morphology might lead you to believe that L. mayottensis was the most basal member of the group, since it has 19 dorsal scale rows whereas every other species has 17).

Liophidium pattoni and its relationship to some of its closest relatives, including L. mayottensis
From Vieites et al. 2010
IUCN categories
The other more authoritative online database is the IUCN Red List. The Red List assesses the conservation status of species and often includes a distribution map (although not in this case), some ecological information, and a short bibliography focused on ecology and conservation rather than on taxonomy. The IUCN page contains several useful nuggets, most of which come to us by way of expert knowledge and may or may not be published elsewhere. For instance, we learn that our species is classified as Endangered under the IUCN categories, which are based on quite rigorous and quantitative criteria. Peters's Bright Snake qualifies as Endangered despite very limited data because all known records are from a forested area of about 65 km2 in the center of Mayotte, which is subject to a continuing decline in quality (criterion B2b(iii)) and within which the actual occurrence records of the snake suggest that its populations are severely fragmented (criterion B2a). Even if the area of occupancy is underestimated, the entire terrestrial area of Mayotte is only 365 km2, which is still less than the minimum of 500 km2 that a species must exceed unless both it and its habitat are known to be contiguous and stable.

Hinged teeth of Liophidium rhodogaster
From Savitzky 1981
The IUCN record also lists several other pieces of information. It tells that the known records are all between 144 and 653 meters above sea level. It states that "this snake is diurnal, ground-dwelling and very secretive", "observed in natural forests and plantations", and is egg-laying. This last tidbit is pretty helpful, and it's no surprise that we haven't encountered it before—it's from a field guide written in French by Danny Meirte, covering the terrestrial fauna of the Comoros, published in 1999 and updated in 2004. As for conservation, it says that our species is not used by humans for any known purpose, but that an introduced civet may be a threat. All native reptile species on Mayotte are protected by law, and several nature reserves may benefit L. mayottensis, but no data is available on the snake's occurrence at these sites.

Finally, the IUCN record notes that "the extreme scarcity of observations may be attributed to the cryptic habits of this snake, but also suggests that L. mayottensis is not common". No shock there. The short bibliography includes both the old and new editions of the field guide and a paper by Oliver Hawlitschek in the journal ZooKeys that used field surveys and remotely sensed data to assess the conservation status of Comoran reptiles, upon which most of the conservation assessment is based. The profile also cites another work in preparation by Hawlitschek, who was also an expert reviewer for the species and took the Arkive photograph. I visited his website and was able to learn that he is a German PhD student studying herp conservation & phylogeography in the Comoros.

Phylogenetic tree of Malagasy reptiles based on CO1 DNA barcodes
Liophidium is near the top right
From Nagy et al. 2012
Now we're getting somewhere, although we're still looking for body size and clutch size, two of the most basic species attributes. Usually, after checking all off the above sources, I repeat the whole process on Google Scholar and track down any promising articles. Often, I'll add a search term for the particular attribute I'm looking for (e.g., "clutch size", "svl") to see if that helps. In this case, even Google Scholar didn't turn up much specific to our species. I was about to give up when I decided to contact Oliver Hawlitschek. When I went to look up his email address, I noticed that he recently published a paper in the journal PLoS ONE, which of all places is known for its free and open accessibility to all. The paper, titled "Island Evolution and Systematic Revision of Comoran Snakes: Why and When Subspecies Still Make Sense", includes supplementary material that finally gives us the answer to our seemingly simple question of "how long is Liophidium mayottensis"? The average adult total length is about 80 cm for both sexes, maximum 1 meter  (3 feet), with the tail making up about 30% of the body. When I contacted Oliver he confirmed this, and he also told me that as far as he knew no information on clutch size was available (although he expected it would be small, like that of most other island snakes). From reading his paper, I also learned that this is by far the largest species of Liophidium (the next is L. therezieni at 72.6 cm) and the only one with 19 dorsal scale rows instead of 17. Oliver's paper suggested that Comoran Liophidium (and the snake Lycodryas and lizard Oplurus) are larger than their Malagasy congeners because they are released from competition with larger species that do not occur in the Comoros.

Liophidium mayottensis skull (with tooth closeup, inset)
Image by Cynthia Wang
Oliver also put me in touch with Cynthia Wang, another graduate student who is using high-resolution X-ray computed tomography to make 3-D scans of the skulls of snakes. Turns out she recently scanned a L. mayottensis skull. You can see the spatula-shaped, hinged teeth characteristic of the genus, although the connective tissue is missing. He also told me that he will be returning to the Comoros this November, and that L. mayottensis will be his #1 target while he's there. All in all, a pretty satisfying conclusion.

This was a long article; congratulations if you made it to the end! I justified the length partly in celebration of my birthday this month and partly in celebration of this blog reaching 250,000 views! I hesitated writing this article because I base a lot of my articles around obscure snakes and I was afraid that writing a how-to would amount to writing myself out of a lot of subject matter. On the other hand, I suppose I enjoy the chase, and I think this overly-long article's length goes to show just how much actually is out there, even for really obscure species, if you're willing to look (and there are certainly resources I've missed! Let me know about them in the comments). I also think that this process is easily generalizable to non-reptiles—there are some great resources out there for amphibians, birds, algae, echinoderms, insects, and much else. Whatever you're interested in, happy researching!

Update: In December 2014, Ludovic Montfort, Cynthia Wang, Oliver Hawlitschek, and Mark Scherz found a L. mayottensis atop Mt. Benara during their field work on Mayotte!

Cynthia Wang with L. mayottensis in December, 2014.
Photo by Matthias Deuss
ACKNOWLEDGMENTS

Thanks to Oliver Hawlitschek, Cynthia Wang, Matthias DeussHenry Cook, and Pagale Bacha for the use of their images.

REFERENCES

Bauer, A. M., R. Günther, and M. Klipfel. 1995. The Herpetological Contributions of Wilhem CH Peters (1815-1883). SSAR Facsimile Reprints in Herpetology:114.

Boulenger, G. A. 1893. Catalogue of the snakes in the British Museum (Natural History). Trustees of the British Museum, London <link>

Cadle, J. E. 1999. The Dentition, Systematics and Phylogeny of Pseudoxyrhopus and Related Genera from Madagascar (Serpentes: Colubridae) with Descriptions of a New Species and a New Genus. Bulletin of the Museum of Comparative Zoology at Harvard College 155:381-443 <link>

Hawlitschek, O., B. Brückmann, J. Berger, K. Green, and F. Glaw. 2011. Integrating field surveys and remote sensing data to study distribution, habitat use and conservation status of the herpetofauna of the Comoro Islands. ZooKeys 144:21–78 <link>

Hawlitschek, O., Nagy, Z., & Glaw, F. 2012. Island evolution and systematic revision of Comoran snakes: why and when subspecies still make sense. PLoS ONE 7:e42970 <link>

Hedges, S. B. 2013. Revision shock in taxonomy. Zootaxa 3681:297-298 <link>

Meirte, D. 2004. Reptiles. Pages 201-224 in M. Louette, D. Meirte, and R. Jocqué, editors. La faune terrestre de l'archipel des Comores. MRAC, Tervuren.

Nagy, Z. T., U. Joger, M. Wink, F. Glaw, and M. Vences. 2003. Multiple colonization of Madagascar and Socotra by colubrid snakes: evidence from nuclear and mitochondrial gene phylogenies. Proceedings of the Royal Society of London. Series B: Biological Sciences 270:2613-2621 <link>

Peters, W. C. H. 1873. Über eine von Hrn. F. Pollen und van Dam auf Madagascar und anderen ostafrikanischen Inseln gemachte Sammlung von Amphibien. Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin 1873:792-795 <link>

Savitzky, A. H. 1981. Hinged teeth in snakes: an adaptation for swallowing hard-bodied prey. Science 212:346-349 <link>

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

Vieites, D. R., F. M. Ratsoavina, R.-D. Randrianiaina, Z. T. Nagy, F. Glaw, and M. Vences. 2010. A rhapsody of colours from Madagascar: discovery of a remarkable new snake of the genus Liophidium and its phylogenetic relationships. Salamandra 46:1-10 <link>

Zaher, H., F. G. Grazziotin, R. Graboski, R. G. Fuentes, P. Sánchez-Martinez, G. G. Montingelli, Y. P. Zhang, and R. W. Murphy. 2012. Phylogenetic relationships of the genus Sibynophis (Serpentes: Colubroidea). Papeis Avulsos de Zoologia (Sao Paulo) 52:141-149 <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.

6 comments:

Gareth Hopkins said...

Great post and insights, Andrew! My oh my you have some dedication tracking down all that information!

john said...

I typed Peters's Bright Snake into the Bing search engine on my computet at work, (my boss is out of the office).
I got 1,290,000 results. I only looked up a few of the websites,(some of the same ones that you mentioned in your post, and saw the same photo). The stuff you can so easily access online just amazes me.

Mark Scherz said...

Good read, Andrew! The amount of detail in Peters' description of L. mayottensis is astounding! I've just been working on another of his species, Geckolepis maculata, and its description is no more than three lines of text. You were fortunate there!

Also, iNaturalist is to some extent peer-reviewed, especially considering records from Madagascar. The HerpetoGasy BioBlitz has several regional experts who go over observations and either confirm or recommend IDs.

Just a note: Olly finished his PhD not too long ago - no longer a student! He's now running the Fauna Bavarica barcoding project at the ZSM. Our website is critically out of date, but hopefully will be updated soon!

If you ever need details on any snakes (or other herps) from Madagascar, shoot me a message. Might be faster than tracking things down this way :P

Olly, Cynthia and myself leave for Mayotte in a week! We're hopeful that we will find these enigmatic snakes, and be able to keep some for a short while to study them in greater detail. We shall see!

(P.S. Sorry for double comment - had to fix my Blogspot account! I've not used it in five years)

Andrew Durso said...

Thanks all for the feedback!

Gareth: it's certainly something I enjoy doing so that helps a lot.

John: Indeed it is. I suspect many of those hits were not specific to L. mayottensis, but probably many of them were.

Mark: Didn't realize you knew Oliver, although I should've guessed. Best of luck tracking one of these down! I'll feature some photos on here if you get some. Also, I see that among other things your hairstyle has changed quite a bit in those 5 years.

Przemysław Damian Puszkiewicz said...

I struck with similar problem when I and doing research for my Master Thesis but I already finished it. There are really a lot of useful information's.

Unknown said...

Great stuff, Andrew, and nice sleuthing.