Monday, August 31, 2015

Digestive system's adaptations to island life in Lacerta trilineata

Balkan Green Lizard. Lacerta trilineata.Photo Credit: 
Kostas Sagonas
Life on an island isn't always easy. To make the most of the little there is to eat on many Greek islands, the digestive system of s has evolved considerably compared to family members on the mainland. Surprisingly, many of these insect-eating lizards even have special valves that help to digest plants. These are some of the findings¹ from a study led by Konstantinos Sagonas of the National and Kapodistrian University of Athens in Greece, published in Springer's journal The Science of Nature².
Reptiles can adjust their digestive system and food preferences due to adverse circumstances such as low rainfall and poor food supply. Previous studies, for instance, show that insect-eating Balkan green lizards (Lacerta trilineata) surviving in the harsh environments of various Greek islands have broadened their diet to include more plants. To extend this research, Sagonas' team set out to compare groups of these lizards on the islands of Andros and Skyros with two other populations in mainland Greece.
They found that the island lizards have a longer small intestine and hindgut compared to their mainland counterparts. Those collected from the island of Skyros also have larger stomachs. When the animals were dissected, the researchers made an unusual discovery. Cecal valves, which slow down food passage and provide fermenting chambers, were found in 62 percent of the island-dwelling lizards, compared to 19 percent of the mainland ones. This was a fact not previously known for green lizards.
Cecal valves are typically found in plant-eating lizards, and host micro-organisms that help to ferment and break down plant material into fatty acids.. When these structures do occur in insect-eating lizards, it is generally among populations that have started to eat a varied diet that also includes plants. Sagonas believes the presence of cecal valves among the island lizards therefore reflects their higher consumption of plant material. About 30 percent of their diet consists of plant material, compared to the 10 percent of the mainland reptiles.
Their evolved digestive system therefore makes it possible for island lizards to eat more plants. Because of their longer digestive tract and the presence of cecal valves, it takes up to 26 percent longer for the food of island lizards to pass through their digestive system. In a process which is more common to plant-eating lizards, the ingested food is ultimately exposed far longer to digestive enzymes.
"Such adaptations allow insular populations to take advantage of the limited food resources of the islands and, eventually, overcome food dearth," explains Sagonas. "Energy flow in insular environments, the digestive performance of insular populations and the connections within them, provide insights into how animals are able to colonize islands and maintain viable populations." 


Sagonas K, Pafilis P., Valakos ED. Effects of insularity on digestion: living on islands induces shifts in physiological and morphological traits in island reptilesThe Science of Nature, 2015; 102 (9-10) DOI: 10.1007/s00114-015-1301-8

Saturday, August 29, 2015

A model for managing the Giant Garter Snake, Thamnophis gigas

Thamnophis gigas. Photo by Dave Feliz
The Giant Gartersnake (Thamnophis gigas) is a highly aquatic species that uses marshes and sloughs, low-gradient streams, ponds, and small lakes, with cattails, bulrushes, willows, or other emergent or water-edge vegetation. Because of the direct loss of natural habitat, this snake now relies heavily on rice fields in the Sacramento Valley, but it also uses managed marsh areas in various national wildlife refuges and state wildlife areas. Essential habitat components consist of adequate water during the snake's active season (early spring through mid-fall) to provide adequate permanent water to maintain dense populations of food organisms; emergent, herbaceous wetland vegetation, such as cattails and bulrushes, for escape cover and foraging habitat during the active season; upland habitat with grassy banks and openings in waterside vegetation for basking; and  higher elevation upland habitats for cover and refuge from flood waters during the snake's inactive season in the winter. The Giant Garter Snake is absent from large rivers and other waters with populations of large, introduced, predatory fishes, and from wetlands with sand, gravel, or rock substrates. Riparian woodlands do not provide suitable habitat because of excessive shade and inadequate prey resources. As of 1992, there were 13 known populations. Not all of have good viability. The adult population size is unknown but presumably is at least a few thousand. Estimates of population size for three local populations in the mid-1990s were in the low 100's. The species is now apparently extirpated or very rare in most of the former range in the San Joaquin Valley. Surveys in the 1970s and 1980s yielded some previously unknown localities and several cases of extirpation or at least severe population declines. The area of occupancy, number of subpopulations, and population size are probably continuing to decline, but the rate of decline is unknown.
 Because more than 90 percent of their historical wetland habitat has been converted to other uses, the species has been listed as threatened by the State of California (California Department of Fish and Game Commission, 1971) and the United States (U.S. Fish and Wildlife Service, 1993). Giant Gartersnakes inhabit a highly modified landscape, with most extant populations occurring in the rice-growing regions of the Sacramento Valley, especially near areas that historically were tule marsh habitat. In ricelands and managed marshes, many operational decisions likely impact the health and viability of Giant Gartersnake populations. Land-use decisions, including the management of water, aquatic vegetation, terrestrial vegetation, and co-occurring species, have the potential to affect giant Gartersnake populations. Little is known, however, about the effects of these types of decisions on the viability of the populations.
In a recent report Halstead et al. (2015) recognized that Bayesian network models are a useful tool to help guide decisions with uncertain outcomes. These models require the articulation of what experts think they know about a system, and facilitate learning about the hypothesized relations. Bayesian networks further provide a clear visual display of the model that facilitates understanding among various stakeholders. Empirical data and expert judgment can be combined, as continuous or categorical variables, to update knowledge about the system. The objective of this project was to develop a conceptual model of site-specific ecology of the Giant Gartersnake in the Sacramento Valley of California. The authors chose to develop the model at a site-specific scale because that is the scale at which most management decisions are made and at which Giant Gartersnake responses can be quantified. They used a Bayesian network model, and also quantified uncertainty associated with different nodes affecting ecology of the Giant Gartersnake, and the strength of influence of different variables on population growth rates of the species. This is a preliminary step in an ongoing process to clarify and quantify the effects of management actions on Giant Gartersnake populations.
They found population growth of the Giant Gartersnake was most influenced by demographic parameters, especially adult survival. Directly managing for increased survival or fecundity, however, generally is not feasible. Habitat quality, was strongly influenced by water availability and emergent vegetation and had a strong influence on both adult and first-year survival. Additional research into the effects of specific habitat attributes on Giant Gartersnake fitness is needed to better quantify the qualitative relations hypothesized in the Bayesian network model. In this regard, habitat quality; predator, parasite, and pathogen effects; and prey availability (particularly as it affects fecundity) all would be productive avenues for future research efforts. Alternatively, research could focus on those nodes for which the least information exists. For example, the scenario analysis indicated that changing Giant Gartersnake population growth from increasing to decreasing resulted in little change in many nodes. Competitor effects, other sources of mortality, and nearly all parents of habitat quality were changed little under increasing and decreasing population growth scenarios. This indicates that these variables either are truly unimportant for determining Giant Gartersnake population growth, or uncertainty in the strength of these relations precludes drawing conclusions about how these variables affect population growth of the Giant Gartersnake. The prudent course of action would be to conduct research into the effects of these variables on Giant Gartersnakes to determine which of these alternatives is correct.


Halstead, B.J., Wylie, G.D., Casazza, M.L., Hansen, E.C., Scherer, R.D., and Patterson, L.C., 2015, A conceptual model for site-level ecology of the giant gartersnake (Thamnophis gigas) in the Sacramento Valley, California: U.S.Geological Survey Open-File Report 2015-1152, 152 p.,

Friday, August 28, 2015

A reassessment of the conservation status of the Central American herpetofauna

Salamanders like this Costa Rican Bolitoglossa striata are 
more susceptible to environmental disturbances than other
amphibians. JCM
A recently published article by Johnson et al. (2015) takes a second look at the herpetofauna of Central America and its conservation needs. The authors found Mesoamerica (the area composed of Mexico and Central America) is the third largest biodiversity hotspot in the world. The Central American herpetofauna has 493 species of amphibians and 559 species of crocodilians, squamates, and turtles.
The authors use a revised EVS measure to reexamine the conservation status of the herpetofauna using the General Lineage Concept of Species to recognize species-level taxa, and employ phylogenetic concepts to determine evolutionary relationships among the taxa.
Since the publication of Conservation of Mesoamerican Amphibians and Reptiles, in 2010, 92 species of amphibians and squamates have been described, resurrected, or elevated from subspecies to species level, and one species of anuran has been synonymized. The herpetofaunal diversity of Central America is comparable to that of Mexico, a significant finding because the land area of Mexico is 3.75 times larger. The number of amphibian species is 1.3 times greater in Central America, whereas the number of species of turtles, crocodilians, and squamates is 1.5 times greater in Mexico. Endemicity is also significant in Central America (65.6% of amphibians, 46.5% of turtles, crocodilians, and squamates), with a combined average of 55.6%.
The authors regard the IUCN system as expensive, time-consuming, and behind advances in systematics and over-dependent on the Data Deficient and Least Concern categories. Conversely, the EVS measure is economical, it can be applied when species are described, is predictive, simple to calculate, and does not “penalize” poorly known species.
The EVS analysis of amphibians demonstrates that on average salamanders are more susceptible to environmental deterioration, followed by caecilians, and anurans. Among the remainder of the herpetofauna, crocodilians are the most susceptible and snakes the least, with turtles and lizards in between.
Biodiversity decline is an environmental problem of global dimensions, comparable to the more commonly publicized problem of climate change. Both of these environmental super-problems exist because of human action and inaction, exacerbated by humanity’s anthropocentric focus.


Johnson, J. D., Mata-Silva, V., & Wilson, L. D. (2015). A conservation reassessment of the Central American herpetofauna based on the EVS measure. Amphibian & Reptile Conservation, 9(2), 1-94.

Wednesday, August 26, 2015

Gueragama sulamericana a Late Cretaceous stem iguanid from southern Brazil

Gueragama sulamerica. Credit: Julius Csotonyi
University of Alberta paleontologists have discovered a new species of lizard, named Gueragama sulamericana, in the municipality of Cruzeiro do Oeste in Southern Brazil in the rock outcrops of a Late Cretaceous desert, dated approximately 80 million years ago.

"The roughly 1700 species of iguanas are almost without exception restricted to the New World, primarily the Southern United States down to the tip of South America," says Michael Caldwell, biological sciences professor from the University of Alberta and one of the study's authors. Oddly however, iguanas closest relatives, including chameleons and bearded dragons, are all Old World. As one of the most diverse groups of extant lizards, spanning from acrodontan iguanians (meaning the teeth are fused to the top of their jaws) dominating the Old World to non-acrodontans in the New World, this new lizard species is the first acrodontan found in South America, suggesting both groups of ancient iguanians achieved a worldwide distribution before the final break up of Pangaea.

"This fossil is an 80 million year old specimen of an acrodontan in the New World," explains Caldwell. "It's a missing link in the sense of the paleobiogeography and possibly the origins of the group, so it's pretty good evidence to suggest that back in the lower part of the Cretaceous, the southern part of Pangaea was still a kind of single continental chunk."

Distributions of plants and animals from the Late Cretaceous reflect the ancestry of Pangaea when it was whole. "This Gueragama sulamericana fossil indicates that the group is old, that it's probably Southern Pangaean in its origin, and that after the break up, the acrodontans and chameleon group dominated in the Old World, and the iguanid side arose out of this acrodontan lineage that was left alone on South America," says Caldwell. "South America remained isolated until about 5 million years ago. That's when it bumps into North America, and we see this exchange of organism north and south. It was kind of like a floating Noah's Arc for a very long time, about 100 million years. This is an Old World lizard in the new world at a time when we weren't expecting to find it. It answers a few questions about iguanid lizards and their origin."

The University of Alberta is a world leader in paleontology. This study was a collaboration between the University of Alberta and scientists in Brazil. Caldwell says of the collaboration, "It's providing an opportunity for our students and research groups to expand our expertise and interests into an ever-increasing diversity of organisms within this group of animals called snakes and lizards."

The lead author of the paper is Caldwell's PhD student, Tiago Simoes, a Vanier scholar. "As with many other scientific findings, this one raises a number of questions we haven't previously considered," says Simoes. "This finding raises a number of biogeographic and faunal turnover questions of great interest to both paleontologists and herpetologists that we hope to answer in the future."

In terms of next steps, Caldwell notes "Each answer only rattles the questions harder. The evolution of the group is much older than has been previously thought, which means we can push an acrodontan to 80 million years in South America. We now need to focus on much older units of rock if we're going to find the next step in the process."

The findings, "A stem acrodontan lizard in the Cretaceous of Brazil revises early lizard evolution in Gondwana," were published in the journal Nature Communications, one of the world's top multidisciplinary scientific journals.


Tiago R. Simões, Everton Wilner, Michael W. Caldwell, Luiz C. Weinschütz, Alexander W. A. Kellner. A stem acrodontan lizard in the Cretaceous of Brazil revises early lizard evolution in Gondwana. Nature Communications, 2015; 6: 8149 DOI: 10.1038/ncomms9149

Wednesday, August 19, 2015

Embryonic lizards may not survive global warming

Currently, three percent of land in the US is inhospitable to 
lizards (orange areas). In the next century, the scientists say 
the areas where lizards may not thrive could grow to 48 
percent (purple area). Map Credit: Ofir Levy; Lizard Photo
 - The Tree Lizard, Urosaurus ornatus. JCM
The expected impact of climate change on North American lizards is much worse than first thought. A team of biologists led by Arizona State University investigators has discovered that lizard embryos die when subjected to a temperature of 110 degrees Fahrenheit even for a few minutes.

The researchers also discovered a bias in previous studies, which ignored early life stages such as embryos. Embryonic lizards are immobile and cannot seek shade or cool off when their surrounding soil becomes hot.

This bias produced overly optimistic forecasts about the fate of lizards during climate change. Given the potential impacts on embryos, many more places in the United States could become uninhabitable for lizards than previously expected.

"Lizards put all of their eggs in one basket, so a single heat wave can kill an entire group of eggs," said Ofir Levy, lead investigator of the study and postdoctoral fellow with ASU School of Life Sciences. "If mothers don't dig deeper nests to lay their eggs, we expect this species to decline throughout the United States."

The findings appear today online in the journal Proceedings of the Royal Society B.

After finding that lizard embryos cannot tolerate 110 degrees Fahrenheit for even a short period, the researchers used a climate model to predict how often heat waves in the past and future would kill developing lizards. Areas in the U.S. reaching lethal temperatures, even in the shade, could spread from 3 percent currently to 48 percent of the country in the next century.

Female lizards lay eggs in spring and summer, digging nests and then leaving their offspring to develop for more than two months. Mothers may choose shadier soils or dig deeper nests to help their offspring avoid the heat. But even if lizards lay eggs in cooler places, nests may still exceed the temperatures that embryonic lizards can tolerate. And, assuming that baby lizards could reach the surface after hatching from a deeper nest, that still may not offer enough protection. Repeated exposure to above average, but not lethal temperatures, can negatively affect a lizard's physiology and behavior.

"Since this year promises to be the hottest on record, we are asking whether organisms, like lizards, can adjust to their warming world," said Michael Angilletta, professor and senior sustainability scientist with ASU School of Life Sciences. "It's critical that we acquire detailed knowledge about what temperatures these lizards and other animals can tolerate throughout the life cycle, not just as adults."

Levy added: "Because lizards are prey for animals such as birds, snakes and mammals, the harmful effects of climate change on embryonic lizards could also negatively affect other species."

Levy O,  Buckley LB,  Keitt TH,  Smith CD, Boateng KO, Kumar DS,  Angilletta MJ. 2015. Resolving the life cycle alters expected impacts of climate change. Proceedings of the Royal Society B, August  DOI: 10.1098/rspb.2015.0837

Thursday, August 13, 2015

New book: Atlas Serpientes de Venezuela - Price Reduced

Atlas Serpientes de Venezuela by Marco Natera Mumaw, Luis Felipe Esqueda, González and Manuel. The book's size is 32x25, full color, dust jacket, it contains 456 pages,>400 photos, >60 maps on geographic distribution and assembled in four chapters and four thematic appendices. For requests send an email to Luis Felipe Esqueda, Co-author and Editor or directly to Marisol Diaz Astorga (responsible for final acceptance and shipping, see instructions). General cost of book is 60$ + 10$ PayPal or Western Union (charges a commission) + shipping costs depending on the location (certified by Correos de Chile).

Friday, August 7, 2015

Venomous frogs

Corythomantis greeningi greening was found to have spines extending from  its skull that can poke through the skin to deliver poison into potential predators (left). Corythomantis greeningi greening, or Greening's frog (middle). Aparasphenodon brunoi, or Bruno's Casque-headed Frog (right.).
Photo Credit: Carlos Jared.

Venomous animals have toxins associated with delivery mechanisms that can introduce the toxins into another animal.

Although most amphibian species produce or sequester noxious or toxic secretions in the glands of the skin to use as antipredator mechanisms, they have been considered poisonous rather than venomous because delivery mechanisms are absent.

The frogs in question – the Greening’s frog (Corythomantis greeningi) and the Bruno’s casque-headed frog (Aparasphenodon brunoi) – produce potent toxins and also have a mechanism to deliver those harmful secretions into another animal using bony spines on their heads.

“Discovering a truly venomous frog is nothing any of us expected, and finding frogs with skin secretions more venomous than those of the deadly pit vipers of the genus Bothrops was astounding,” said  Edmund Brodie, Jr. from Utah State University, a team member and a co-author on the study.

The Greening’s frog and the Bruno’s casque-headed frog have both been known for many decades, if not centuries. But scientists have known little of their biology.

The team’s calculations suggest that a single gram of the toxic secretion from the Bruno’s casque-headed frog would be enough to kill more than 300,000 mice or about 80 humans.

“It is unlikely that a frog of this species produces this much toxin, and only very small amounts would be transferred by the spines into a wound. Regardless, we have been unwilling to test this by allowing a frog to jab us with its spines,” said lead author Dr Carlos Jared from the Instituto Butantan in São Paulo, Brazil.

The researchers, whose findings are published in the journal Current Biology, only discovered they were venomous while collecting amphibians for study. Jared was injured by a spine from Corythoimantis greeingi while handling it, leading to intense spreading pain in his hand for around five hours. Fortunately for him, the frog was the less toxic of the two. He said: 'The action should be even more effective on the mouth lining of an attacking predator.'

The researchers say they have still to find out exactly how much toxin the frogs can deliver in one go. However, they believe there may be other species of frog that are also venomous. Dr Brodie added: 'It is unlikely that a frog of this species produces this much toxin, and only very small amounts would be transferred by the spines into a wound. 'Regardless, we have been unwilling to test this by allowing a frog to jab us with its spines.'

“The new discovery is important for understanding the biology of amphibians and their interactions with predators in the wild,” the scientists said.

Jared et al. 2015. Venomous Frogs Use Heads as Weapons. Current Biology, doi: 10.1016/j.cub.2015.06.061

Wednesday, August 5, 2015

Snakes & Palm Oil Plantations in Colombia

The most commonly encountered snake in oil palm plantations
was Ninia atrata.
Rainforest in the tropics is frequent cut to make way for the African oil palms, Elaeis guineensis. The plant is most often grown for cooking oil but has recently attracted the attention of the alternative energy industry as a source of biofuel. While the plant is native to sub-Saharan Africa, it has now spread to tropical Asia and the Neotropics.
Lynch (2015) analyzes the snake species found during student field trips to Colombian oil palm plantations between 2006-2013. They visited 30 palm plantations varying in size from 0.02-20,000 hectares. These include small privately held palm trees groves as well as large commercial plantations. Success-rates varied with less success in the dry season and greater success in the wet season. Thirty-five snake species were found. Widespread lowland species (Boa constrictor, Clelia clelia, Corallus hortulanus, Imantodes cenchoa, Leptophis ahaetulla, Ninia atrata, Oxyrhopus petola, Tantilla melanocephala, and the species pairs of Bothrops asper or B. atrox, Epicrates cenchria or E. maurus, and Leptodeira annulata or L. septentrionalis). Seven other species (Chironius carinatus, Erythrolamprus bizona, Lampropeltis cf. triangulum, Mastigodryas boddaertii, M. pleei, Sibon nebulata, and Typhlops reticulatus) occur across the regions sampled but do not occupy all lowlands of Colombia. All of these except Imantodes cenchoa, Lampropeltis cf. triangulum, and Sibon nebulata were captured in at least one plantation. Of the 35 species of snakes captured in palm trees, fourteen were diurnal activity or crepuscular, the remaining 21 species are exclusively nocturnal.
To date, there are no reliable data on population sizes of any snake species in Colombia. In point of fact, the impression of collectors is that densities are very low. This impressions is contradicted by our work in palm plantations. Collecting in natural habitats by other researchers has produced success rates equivalent or superior to our work in palm trees.
The Colombian African palm oil industry could be a major factor in conserving snakes. Snake mortality from rural workers exceeds 100 million/year and no fewer than 50,000 snakes die/year due to traffic. However, to be a partner in snake conservation will require two changes in the industry: (1) all waste be fronds need to be piled into mounds on the plantation and allowed to decompose slowly. This provides refuges for snakes, easy access to prey, and reduces human encounters, Secondly, stop converting parcels of secondary forest into more monoculture of palms. Leaving patches of secondary forest and scrub increases microhabitats and the prey base.

Lynch, J. D. (2015). The role of plantations of the African palm (Elaeis guineensis Jacq.) in the conservation of snakes in Colombia. Caldasia, 37(1), 169-182.

Sunday, July 26, 2015

A Four-legged fossil snake discovered, and a growing controversy regarding its legal status in Europe

The following has been adapted from a press release and a blog post, with some light editing by me (JCM).
A new fossil, named Tetrapodophis amplectus, claims to be a four-legged, burrowing snake. (A) Counterpart, showing skull and skeleton impression. (B) Main slab, showing skeleton and skull impression. Figure 1 from Martill et al. 2015.  (C) The snake has small ‘hands’ that are approximately 1cm long. Credit: Image courtesy of University of Portsmouth.
The first known fossil of a four-legged snake, and the team -- led by Dr. Dave Martill from the University of Portsmouth -- say that this discovery could help scientists to understand how snakes lost their legs. The research was published in the journal Science.
Dr Martill said: "It is generally accepted that snakes evolved from lizards at some point in the distant past. What scientists don't know yet is when they evolved, why they evolved, and what type of lizard they evolved from. This fossil answers some very important questions, for example it now seems clear to us that snakes evolved from burrowing lizards, not from marine lizards."
The fossil, from Brazil, dates from the Cretaceous period and is 110 million years old, making it the oldest definitive snake. Martill discovered the fossil as part of a routine field trip with students to Museum Solnhofen, Germany, a museum that is well-known for its prestige with regard to fossils.
Dr Martill said: "The fossil was part of a larger exhibition of fossils from the Cretaceous period. It was clear that no-one had appreciated its importance, but when I saw it I knew it was an incredibly significant specimen."
Martill worked with expert German palaeontologist Helmut Tischlinger, who prepared and photographed the specimen, and Nick Longrich from the University of Bath's Milner Centre for Evolution, who studied the evolutionary relationships of the snake.
Dr Longrich, who had previously worked on snake origins, became intrigued when Martill told him the story over a pint at the local pub in Bath.
He said: "A four-legged snake seemed fantastic and as an evolutionary biologist, just too good to be true, it was especially interesting that it was put on display in a museum where anyone could see it."
He said he was initially skeptical, but when Dr Martill showed him Tischlinger's photographs, he knew immediately that it was a fossil snake.
The snake, named Tetrapodophis amplectus by the team, is a juvenile and very small, measuring just 20 cm from head to toe, although it may have grown much larger. The head is the size of an adult fingernail, and the smallest tail bone is only a quarter of a millimeter long. But the most remarkable thing about it is the presence of two sets of legs, or a pair of hands and a pair of feet.
The front legs are very small, about 1cm long, but have little elbows and wrists and hands that are just 5mm in length. The back legs are slightly longer and the feet are larger than the hands and could have been used to grasp its prey.
Dr Longrich said: "It is a perfect little snake, except it has these little arms and legs, and they have these strange long fingers and toes.
"The hands and feet are very specialized for grasping. So when snakes stopped walking and started slithering, the legs didn't just become useless little vestiges -- they started using them for something else. We're not entirely sure what that would be, but they may have been used for grasping prey, or perhaps mates."
Interestingly, the fossilized snake also has the remains of its last meal in its guts, including some fragments of bone. The prey was probably a salamander, showing that snakes were carnivorous much earlier in evolutionary history than previously believed.
Helmut Tischlinger said: "The preservation of the little snake is absolutely exquisite. The skeleton is fully articulated. Details of the bones are clearly visible and impressions of soft tissues such as scales and the trachea are preserved."
Tetraphodophis has been categorized as a snake, rather than a lizard, by the team due to a number of features:
· The skeleton has a lengthened body, not a long tail.
· The tooth implantation, the direction of the teeth, and the pattern of the teeth and the bones of the lower jaw are all snake-like.
· The fossil displays hints of a single row of belly scales, a sure fire way to differentiate a snake from a lizard.
Tetrapodophis would have lived on the bank of a salt lake, in an arid scrub environment, surrounded by succulent plants. It would probably have lived on a diet of small amphibians and lizards, trying to avoid the dinosaurs and pterosaurs that lived there.
At the time, South America was united with Africa as part of a supercontinent known as Gondwana. The presence of the oldest definitive snake fossil in Gondwana suggests that snakes may originally have evolved on the ancient supercontinent, and only became widespread much more recently.
However there is a controversy brewing around the specimen, and it is not the creationist controversy you might expect.
Discover Magazine’ blog has a piece by Christie Wilcox  titled “Four-Legged Snake Shakes Up Squamate Family Tree – Or Does It?” (posted July 24, 2015)
Ancestral state analyses, use math and science to estimate the biological and ecological traits of the most recent common ancestor of a group of species, suggested that early snakes were nocturnal hunters, preying upon the small vertebrates of their era through stealth, not constriction. Their analysis didn’t find that snakes were burrowers, however — there was no strong support of a fossorial lifestyle, just that the snakes lived on land.
According to Hsiang, morphological data “strongly influenced” the snake tree. “Our study helped to demonstrate how important and essential it is to include fossils when we are trying to understand how and when organisms evolved.” In the paper, the author’s note that the inclusion of fossil data resulted in relationships that would be “unexpected” given current snakes, and that the fossils’ influence was sustained “even when such data are vastly outnumbered by genetic sequence data,” thus including the new fossil in a similar analysis might be even more informative.
“Now that Martill et al.’s paper on Tetrapodophis has been published, the obvious next step is to include it in large-scale, comprehensive analytical studies looking at snake evolutionary history and phylogenies.”
Though there was some excitement when Hsiang and her colleagues published their analysis in May, a paper published a little over a month earlier in PLoS ONE slipped by the press unnoticed. The analysis, led by Tod Reeder from San Diego State University, looked beyond snakes to reconstruct the evolutionary relationships within the squamates, the group of reptiles that contains lizards and snakes. Using the largest dataset to date which, like Hsiang, included both genetic and morphological markers, Reeder and his colleagues affirmed one of the crucial pieces of evidence of a marine snake origin: the close relationship between mosasaurs and snakes.
“The most comprehensive analysis of the lizard evolutionary tree now reinstates these aquatic mosasaurs as the nearest relatives to snakes,” explains Michael Lee, associate professor at the University of Adelaide, who was one of the first scientists to suggest that snakes may have started in the water.
The lizard tree, which found the aquatic mosasaurs (Mosasauria) to be sister to modern snakes (Serpentes).
The lizard evolutionary tree, which places the aquatic mosasaurs (Mosasauria) sister to modern snakes (Serpentes) rather than the group used by Hsiang et al. (Anguimorpha).
Because of this, Reeder et al. calls into question the methods used by Hsiang et al., specifically one of the core assumptions in the paper: the closest relatives of snakes. When constructing evolutionary trees, assumptions have to be made to “root” the tree, or put the relationships into the context with regards to time. Scientists must compare their data to what is called an “outgroup”, which is ideally the closest relative or relatives to the group of interest. Hsiang and her colleagues used a subset of a group of lizards called anguimorphs, which includes land dwelling lizards like varanids that includes the Komodo dragon.
“The Hsiang paper was a terrific analysis of the evolution within snakes, but the fundamental core assumption they made in the paper was that terrestrial lizards were ancestral to snakes,” said Lee. “The direction of evolution was determined by that assumption. But if you assume, as the Reeder paper suggests, that mosasaurs are ancestral to snakes, then some of the inferences by Hsiang might not hold.”
Hsiang admits that there are differences between the phylogenies in her paper and Reeder’s, and that the choice of outgroup may have skewed their results. “There are differences between the Reeder et al. phylogeny and our phylogeny — it would be interesting to conduct an in-depth analysis to try and determine why the differences in phylogeny exist,” she said. While her team’s tree was strongly influenced by morphology, Reeder’s team found that genetics most strongly predicted the results. “In fact, the morphological data are really ambiguous,” co-author John Wiens said in a press release. “Or in some cases, even worse than ambiguous.”
“There’s certainly a possibility that our results would have been different if we had used different outgroups, as phylogenetic and ancestral state reconstruction analyses use the outgroup to determine the direction and polarity of character state evolution,” said Hsiang. However, she doubts the impact would have been large, as other close relatives of mosasaurs are land-lubbers. “Though the inclusion of mosasaurs would likely have increased the probability of an aquatic lifestyle for early snakes somewhat, this would probably have been “balanced out” by the many anguimorph lizards that are not aquatic.”
“Of course, we’d have to actually run the analysis to know for sure.”
Meanwhile, Bruno Simões from the Natural History Museum, London, UK and his colleagues were taking a very different approach to understanding snake evolution. Instead of looking at bones and unrelated genes, they very specifically examined the genes encoding for visual pigments in lizards and snakes. These genes are well-studied, and in other groups like mammals, are correlated with behaviors like burrowing and nocturnal activity.
“Visual pigments, like opsin and rhodopsin, are basically the business front-ends of the visual pathway,” says Simões. “So basically if anything is happening in the visual system, the visual pigments will be the first to be impacted.” Burrowing mammals, for example, have lost some visual pigment genes, as they no longer need them underground. But even more impressively, scientists can connect genetic changes in these pigment genes to ecology and function. “By checking their amino acid composition, you can estimate what kind of wavelengths the animal can see,” says Simões.
When Simões et al. compared the visual pigment genes in snakes to other lizards, they found something exciting: snakes have lost two of the five pigments found in the rest of the squamates. They retain the same three that we have. Simões explained that this means snakes likely went through an “ancestral nocturnal bottleneck,” just like mammals did. “Snakes have this contrasting pattern from lizards that converges with mammals.”
Evolutionary tree for the Rhodopsin 1 gene, the only one left in the most underground snakes.
Interestingly, in fossorial lizards, all five pigments were still around, but in fossorial snakes like the termite-decapitating blindsnakes, only one pigment remained. “The fact that the visual system was not so reduced suggests that the ancestor for all snakes was nocturnal, not fossorial” — a finding which coincides with the ancestral state reconstructions found by Hsiang et al.
As for the question of marine origins, Simões says that he “didn’t find evidence that it was a marine animal.” Marine environments have very different light conditions than terrestrial ones, with a quick loss of red wavelengths with depth, followed by an eventual loss of all light in the deep sea. Marine animals eyes often show a “shift in spectral tuning to a marine environment,” says Simões, which includes a higher sensitivity for blue wavelengths. In sea snakes, for example, the shorter-length opsin 1 becomes blue sensitive instead of UV sensitive. But Simões found no such shift in all snakes.
“I think that it’s a really interesting paper, in that they’ve discovered that snakes have lost a whole bunch of visual genes that are found in other lizards, which does suggest they went through some kind of semi-blind phase in their evolution,” says Lee. But he still would like to see more research before discounting the aquatic hypothesis. “One thing I’d like to see done is what genes are lost in living marine reptiles like sea turtles,” said Lee, to see if there are any opsin genes lost in other marine reptiles like the ones lost in snakes.

A Four-Legged Snake?
Which brings us back to the most recent finding, what Martill and his colleagues claim is a four-legged snake ancestor from Brazil. Though there’s no concrete information about where this fossil originated, the color and texture of the limestone it is encased in suggests it’s from the Crato Formation, a fossil deposit which was laid down some 100 million years ago when the area was a shallow sea.
“The Crato formation is about 20 million years older than the oldest fossil snake,” Martill explained. Thus this ten centimeter-long fossil, which Martill and his colleagues named Tetrapodophis amplectus, may shed light on the earliest snakes.
 “The Martill paper is going to be one of the most controversial papers around for a long time,” said Lee. “I’ve already had about 50 emails from colleagues about it, all expressing really different views.”
“It is a very unusual specimen,” Lee said, “because if it is a snake, it’s a tremendous missing link between lizards and snakes.”
But there are several lineages of lizards with lost or reduced limbs and longer bodies, so the evidence to place it as a snake ancestor must be more than just that. Martill notes that the short length of the tail in relation to the body, structure of the pelvis, impressions of body scales, recurved teeth, high vertebral count and the shape of the vertebrae all make Tetrapodophis a snake. “This thing is much much more of a snake than it is of a lizard,” he concluded. But some scientists don’t buy it. “I think the specimen is important, but I do not know what it is,” University of Alberta paleontologist Michael Caldwell told Ed Yong from National Geographic. But Lee is willing to give Martill the benefit of the doubt. “I’m prepared to provisionally accept that it’s a very unusual small snake,” he said. “But the specimen is so small and the skull is so badly crushed that I think there is going to be a lot of debate until all interested researchers are able to look at it.”
“It does seem to have some pretty intriguing snake features,” Lee admits. “Snake teeth have a very distinct curvature to them… and this animal does seem to have that. So that’s one feature that really makes me think this is probably a snake.” He’s also impressed by the animal’s spine. “It’s got a very large number of vertebrae — 160 backbone elements — which is also a very snake-like feature,” he added. “None of the other features that they list do I find particularly compelling.”
Hsiang, on the other hand, is entirely convinced. “Tetrapodophis does seem to possess many anatomical features that are unique to snakes — the recurved teeth, intramandibular joint, vertebral characters, et cetera,” she said. “So, based on Martill et al.’s report of the anatomy, it seems likely that Tetrapodophis is indeed an early snake.” She’s especially intrigued by what else is visible in the new fossil: its last meal. Martill et al. report that inside the snake’s stomach are a collection of vertebral bones, likely from a small mammal or lizard that it ate just before it died — the same diet that Hsiang et al. predicted with their ancestral state analyses. “The new fossil provides empirical confirmation of some of our results,” she noted. “For instance, the discovery of vertebrate bones in the stomach contents of Tetrapodophis aligns with our inference that the earliest snakes likely ate small vertebrates.”
According to Martill et al., the short tail and reduced limbs are evidence that Tetrapodophis was a burrowing snake. “Although this thing has been found in sediments that were laid down in water,” Martill says, “the shortened limbs and the little scoop-like feet that it’s got on its hind limbs look much more like they’re for burrowing than they are for swimming.”
“Also, they wouldn’t really function for swimming,” Martill said. “This thing is almost certainly using lateral undulatory locomotion to burrow through soft sand and leaf litter.”
“I think that’s fairly weak evidence,” said Lee. “There’s no living burrowing lizard or snake with those type of body proportions,” he added. “We can’t really say what it did at the moment, because there are too many contradictory traits in this animal.”
Lee similarly points to the shape and size of the limbs and feet, but says they provide evidence of an aquatic lifestyle rather than a fossorial one. Species known for their burrowing habits, like moles, have short, squat, strong limb bones, but Tetrapodophis has “long, delicate fingers and toes.” There are also questions about the composition of the bones themselves; bones can vary in the amount of calcium they contain, with more calcium or “more ossified” bones resisting breakage better than less ossified ones. Lee notes that the limbs of Tetrapodophis seem to be “fairly poorly ossified.” “That’s not what you find in burrowers because you want your hands and feet to be as robust as possible to push through the soil.” Reduced ossification of limb bones is, however, a trait shared by other aquatic organisms. Furthermore, in the hind feet, two ankle bones that are fused in most lizards are separate. The only other group of lizards where these bones are apart? The aquatic mosasaurs. Rather than seeing the feet as scoop-like, Lee sees them as “paddle-like.” He also noted that the bones of the fingers and toes are perfectly aligned in parallel with one another. “That leads me to think that they were held together in something, like a flipper or sheath.”
All of that and the fact that the animal was found in what, at the time, was a shallow sea, does give credence to the idea that it could be an aquatic snake. “I wouldn’t come out and say that it’s aquatic, because I don’t think we can say that either,” Lee said, “but I don’t think that we can conclude that it’s burrowing.”
The aquatic idea of snake origins might be the minority view, but there’s enough accumulating evidence now that it needs to be reexamined rather than dismissed out of hand.”
So how die Brazil’s Big Discovery end up in Germany?
Though Tetrapodophis is perhaps the most scientifically-intriguing snake fossil to date, questions about how it arrived in Germany are already beginning to overshadow its scientific importance. Even before the paper officially published, rumors swirled about whether the remarkable specimen was illegally poached from Brazil. When I asked Martill about the specimen’s discovery, he was disturbingly cavalier about the fossil’s origins. “More or less, I discovered it,” he said, “I actually found it in a museum collection.”
“It was one of those serendipitous things,” he continued.  “I actually worked on fossils from this location in Brazil for many many years.” But Martill didn’t find Tetrapodophis on an excursion to the jungle; he found it labeled as an “Unknown Fossil” in the Bürgermeister-Müller Museum in Solnhofen, Germany on a routine class trip for his students. It just so happened that when he took his students to see the museum, on display was an exhibit on Brazilian fossils, which Martill — having written a book about the Crato formation — was excited to see. “All of a sudden, my jaw just dropped to the floor,” he recounts. “This looks like a snake!”
When pressed, he admitted that there was no information about the fossil’s origins — when it was found, who pulled it from the earth, and how or why it made its way across the ocean to a small museum in Germany. He was blunter when he spoke to Herton Escobar (quoted by Herton Escobar for Science). Martill told him that questions about legality are ‘irrelevant to the fossil’s scientific significance’ and said: “Personally I don’t care a damn how the fossil came from Brazil or when.”
As Shaena Montanari explains for Forbes, given the laws in Brazil since 1942, it’s likely that Tetrapodophis found its way to Europe illegally. Brazilian officials have gone as far as to say they’re certain the specimen illegally left the country. Many scientists are expressing their outrage that a prestigious journal like Science would even publish a paper based upon what is likely a black market specimen.
Thus, the specimen is controversial by its very nature but the issue of it being in Germany illegally also raises questions about the fossil trade.

Martill, Tischlinger & Longrich. (2015). A four-legged snake from the Early Cretaceous of Gondwana. Science. doi: 10.1126/science.aaa9208
Hsiang et al. (2015). The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC evolutionary biology, 15(1), 87. doi: 10.1186/s12862-015-0358-5
Reeder et al. (2015) Integrated Analyses Resolve Conflicts over Squamate Reptile Phylogeny and Reveal Unexpected Placements for Fossil Taxa.PLoSONE 10(3): e0118199. doi: 10.1371/journal.pone.0118199
Simões et al. (2015). Visual system evolution and the nature of the ancestral snake. Journal of evolutionary biology 28(7): 1309-1320. doi: 10.1111/jeb.12663
 Read the full interview between Martill and Escobar here

Sunday, July 5, 2015

More on Pseustes poecilonotus as a nest predator

Fragmented tropical forest landscapes are becoming more abundant, and loss of species following fragmentation are often predictable. Larger animals, tend to disappear first from fragments due to the bushmeat trade. However,  another vulnerable group includes understory, insectivorous birds, and ant-following birds. Nest predation is one mechanism that may limit bird populations and has long been suspected as a factor threatening bird populations in temperate  and tropical forest fragments.  A potential influence on nest predation that remains understudied in the tropics is density dependence. Dense territories can increase predators’ ability to find the closely-spaced nests. Yet bird density and nest predation are not always positively correlated, and multiple life-history traits and contexts are relevant.

In a forthcoming paper in Biological Conservation Visco and Sherry (2015) compared nest predation rates, bird density, and predator identities in three habitats of lowland Caribbean Costa Rica: two fragments, a peninsular reserve (La Selva Biological Station), and unfragmented rainforest. Their results suggest an inversely density-dependent nest predation pattern: In fragments, chestnut-backed antbirds reached their highest density and—contrary to predictions—experienced their lowest nest predation rates; La Selva, on the other hand, experienced the lowest density and highest predation rate. Because nest predation decreased with fragmentation, it appears not to explain declines of understory insectivores from forest fragments generally. 

Nest survival models indicated that habitat best-described nest predation likelihood. Video surveillance of nests documented the bird-eating snake (Pseustes poecilonotus) causing 80% of nest loss (37 of 46 nests) and a larger variety of predators in fragments; thus, landscape factors influenced an understory bird’s nest predation. Given the large effect on our focal species, Pseustes likely affects other understory nesters, a topic warranting further study. Tropical reserve conservation plans should consider potential impacts of specialized nest predators on vulnerable understory birds

Visco, D. M., & Sherry, T. W. (2015 in press). Increased abundance, but reduced nest predation in the chestnut-backed antbird in Costa Rican rainforest fragments: surprising impacts of a pervasive snake species. Biological Conservation.pseutes

Sex reversal triggers rapid transition from genetic to temperature-dependent sex.

Hatchling Bearded Dragon
A climate-induced change of male dragons into females occurring in the wild has been confirmed for the first time, according to University of Canberra research recently published on the cover of international journal Nature.

The researchers, who have long studied Australia's bearded dragon lizards, have been able to show that a reptile's sex determination process can switch rapidly from one determined by chromosomes to one determined by temperature.

Lead author Dr. Clare Holleley, a postdoctoral research fellow at the University of Canberra's Institute for Applied Ecology, explained: "We had previously been able to demonstrate in the lab that when exposed to extreme temperatures, genetically male dragons turned into females."

"Now we have shown that these sex reversed individuals are fertile and that this is a natural occurring phenomenon."

Using field data from 131 adult lizards and controlled breeding experiments, Dr Holleley and colleagues conducted molecular analyses which showed that some warmer lizards had male chromosomes but were actually female.

"By breeding the sex reversed females with normal males, we could establish new breeding lines in which temperature alone determined sex. In doing so, we discovered that these lizards could trigger a rapid transition from a genetically-dependent system to a temperature-dependent system," she said.

"We also found that sex-reversed mothers -- females who are genetic males -- laid more eggs than normal mothers," Dr Holleley said. "So in a way, one could actually argue that dad lizards make better mums."

University of Canberra Distinguished Professor Arthur Georges, senior author of the paper, also highlighted the importance that these discoveries have in the broader context of sex determination evolution.

"The mechanisms that determine sex have a profound impact on the evolution and persistence of all sexually reproducing species," Professor Georges said.

"The more we learn about them, the better-equipped we'll be to predict evolutionary responses to climate change and the impact this can have on biodiversity globally."

Holleley CE, O'Meally D, Sarre SD, Marshall Graves JA, Ezaz T, Matsubara K, Azad B, Zhang X, Georges A.
Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature, 2015; 523 (7558): 79 DOI: 10.1038/nature14574

Thursday, June 18, 2015

A preliminary revision of Asian Pipe Snakes, Cylindrophis

An undescribed pipe snake from Thailand (JCM) and a map 
showing the known taxa.
The Asian Pipe Snake of the Cylindrophiidae contains about ten species. These are burrowing, semi-aquatic snakes that are basal to most other living snakes. Linnaeus (1758) described Anguis maculata from Sri Lanka, Laurenti (1768) described Anguis ruffa described by Laurenti (1768). In 1818 Wagler established the  genus Cylindrophis based upon a type species from Java, Cylindrophis resplendens which was later synonymized with Cylindrophis ruffus by Schlegel (1844). Several additional taxa were described in the 19th and 20 centuries (e.g., Cylindrophis melanotus Wagler 1830, Cylindrophis lineatus Blanford 1881, Cylindrophis isolepis Boulenger 1896, Cylindrophis opisthorhodus Boulenger, 1897, Cylindrophis boulengeri Roux 1911, Cylindrophis aruensis Boulenger 1920, Cylindrophis celebensis Smith 1927, Cylindrophis heinrichi Ahl 1933, Cylindrophis engkariensis Stuebing 1994, Cylindrophis yamdena Smith and Sidik 1998) and one subspecies, Cylindrophis rufus burmanus, Smith 1943). Most taxa are endemic to one island or small island group with the exception of Cylindrophis ruffus which is widespread, in Thailand, Laos, Vietnam, Myanmar, Cambodia, China, Malaysia, Singapore, and several Indonesian islands including Sumatra, Borneo, Java, and Sulawesi.

In a new paper Amarasinghe et al. (2015) examine the systematics of the genus and redefine based only uon specimens from Java Cylindrophis ruffus, they C. burmanus using the type series collected from Myanmar, and designate a lectotype. They identified four groups based on the number of scale rows around the midbody (17, 19, 21, and 23). Among the Cylindrophis examined they discovered two new species: C. jodiae sp. nov. from Vietnam and C. mirzae sp. nov. from Singapore. This paper is a good start on revising the genus but it leaves many undescribed species in places like Sumatra. Borneo, and most of the Indochinese peninsula.

Amarasinghe AAT, Campbell PD, Hallermann J, Sidik I, Supriatna J, Ineich I. 2015. Two new species of the genus Cylindrophis Wagler, 1828 (Squamata: Cylindrophiidae) from Southeast Asia. Amphibian & Reptile Conservation 9(1): 34–51 (e98).

Friday, June 12, 2015

Feeding system of the Eastern Diamondback Rattlesnake

The Eastern Diamondback Rattlesnake, Crotalus adamanteus, is the largest rattlesnake species and has an exclusively endothermic diet. Although native to seven states in the southeastern Coastal Plain, the species has been extirpated from Louisiana, is listed as endangered in North Carolina, and is currently under consideration for listing as threatened under the Endangered Species Act.

The question of how all of the parts of an organism work together with environmental factors, even when they are changing during an individual’s life is fascinating.  In venomous snakes, ontogenetic changes in diet and intraspecific variation in venoms have been documented. However, the timing of such changes in a life history context and a comparison of the extent of ontogenetic and geographical variation in natural populations have not been investigated.

In an early on-line version of a new paper by Margres et al. (2015), the authors examine the feeding system of the Eastern Diamondback Rattlesnake. They combine venom, morphology (head shape and fang length) and ontogeny over the various environments and geography the snake inhabits. Using a genotype-phenotype map approach, protein expression data, and morphological data they found: ontogenetic effects explained more of the variation in toxin expression variation than geographic effects; both juveniles and adults vary geographically; variation in toxin expression was a result of directional selection; and different venom phenotypes co-varied with morphological traits also are associated with feeding in temporal (ontogenetic) and geographic (functional) contexts.

Venom is ultimately responsible for knocking down prey, and a suite of morphological traits such as gape and fang length should be equally important to the feeding ecology of venomous species. Phenotypic integration is the dependent relationship between different traits that collectively produce a complex phenotype. In venomous snakes, phenotypic integration includes characters as diverse as venom, head shape, and fang length. The optimal depth of venom injection (i.e., fang length) may depend on venom composition which, along with the head shape, may vary with prey size. Morphological differences are associated with variation in venom composition, and phenotypic integration of the complete feeding system, have not been investigated at any level.

This appears to be the first demonstration of phenotypic integration between multiple morphological characters and a biochemical phenotype across populations and age classes. The authors identified copy number variation as the mechanism driving the differences in the venom phenotypes associated with these morphological differences. They also found parallel mitochondrial, venom, and morphological divergence between northern and southern clades suggests that each clade may warrant classification as a separate evolutionarily significant unit.

Sampling sites for Crotalus adamanteus. The authors collected venom and blood samples from 123 C. adamanteus from seven putative populations; 127 preserved C. adamanteus specimens were used for morphological analyses. Phylogenetic analyses identified two distinct clades, one north of the Suwannee River and one south of the Suwannee River, with dating estimates placing the split at approximately 1.27 Ma. Abbreviations: AR, Apalachicola River; Ca, Crotalus adamanteus; SMR, Saint Mary's River; SR, Suwannee River.


Margres MJ, Wray KP, Seavy M, McGivern JJ, Sanader D, Rokyta DR. (2015). Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus). Molecular Ecology.