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Remarkable New Giant Anole Discovered in the Dominican Republic

 

Last week, Miguel Landestoy provided the details on the discovery of Anolis landestoyi, the new species from the Dominican Republic. The paper was published recently in The American Naturalist. Here’s what the press had to say:

The Canadian Broadcast Corporation:

A Caribbean lizard that remained undiscovered for many years despite its large size and distinctive looks has been identified as a new species.

The lizard, an anole that looks like a chameleon and has a similar talent for camouflage, lives in the canopy of a rare type of forest in the western Dominican Republic. Adults have a body length of up to 13.5 centimetres and a tail up to 18 centimetres long, making them unusually large for an anole. The new species is described as a “giant chameleon-like lizard” in a study published in the journal The American Naturalist.

The lizard was first spotted in 2007 by Dominican naturalist Miguel Landestoy while he was studying endangered birds called bay-breasted cuckoos.

‘There’s nothing else like that in and around the island.’– Luke Mahler, University of Toronto

“He noticed that these birds were agitated and seemed to be attacking something,” recalled Luke Mahler, a University of Toronto biologist and the lead author of the new study.

When Landestoy got closer, he saw a lizard and snapped a picture of it.

Convinced it was a new species, he showed the photo to Mahler, a lizard researcher who was working in the Dominican Republic at the time. But the photo was so grainy that Mahler couldn’t tell much other than it was an anole. He suggested that Landestoy try to capture a specimen.

Several years later, Landestoy spotted the lizard again and took some better photos.

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Luke Mahler (left) and Miguel Landestoy (right) pose for a photo shortly after capturing the first specimens of Anolis landestoyi. (Luke Mahler)

“As soon as he sent the pictures,” Mahler recalled, “I was like, ‘What the expletive is that? … There’s nothing else like that in and around the island.”

He added that the Caribbean has been very well explored, so that typically, any new species found there are so similar to existing species that they can only be distinguished with DNA testing.

The new lizard was a big anole, with stubby limbs, a short tail, and green-grey and light brown scales that help it blend in among the moss-covered branches of the semi-dry tropical forest where it lives.

“It’s super camouflaged, basically. It looks just like the bark,” said Mahler, who thinks that’s why it’s never been spotted before. “It’ll sit there and hug a branch and very slowly move one limb at a time.”

The lizard is similar to related anoles found in Cuba called chamaeleolisor chamaeleonides because they’re also chameleon-like.

Different islands, similar adaptations

That’s intriguing because biologists have always expected to find a lizard similar to chamaeleonides on Hispaniola, the island shared by Haiti and the Dominican Republic. Islands in the Caribbean tend to have similar environments and tend to evolve species with similar adaptations, even if they are not closely related.

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The newly discovered Hispaniolan lizard Anolis landestoyi (top) is very similar to the Cuban species A. porcus (bottom), part of a group called chamaeleonides. (Miguel Landestoy)

Mahler says more analysis needs to be done to figure out if the new lizard is similar to the chamaeleonides lizards because it’s closely related or because it evolved similar adaptations over time.

The new lizard has been named Anolis landestoyi after its discoverer.

Sadly, even though the new species was so recently discovered, it may not be around for much longer.

“We think that they’re probably quite endangered,” Mahler said.

That’s because it lives in a unique type of forest halfway up a mountain slope close to the border with Haiti. Although the forest is in a reserve called Lomo Charco Azul that’s officially protected, it’s threatened by illegal logging for agriculture, livestock grazing, and firewood.

The researchers are requesting that the new lizard be officially listed as critically endangered. They hope the new discovery will help draw attention to the threats to its habitat and lead to better protection.

Science Newsline:

We tend to think the contours of biodiversity are well known, especially in extensively studied areas. However, this is not necessarily the case and sometimes strikingly new species are discovered even in well-trod areas. A case in point is the country of the Dominican Republic, which has been thoroughly studied by biologists for more than 40 years, particularly by herpetologists who have exhaustively catalogued the reptiles and amphibians there for several decades.

Is There a Crisis in Anolis Taxonomy? Part 2

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In a (somewhat) recent blog post entitled “Is there a crisis in Anolis taxonomy?”, Julian Velasco invited discussion on a perceived decline in the number of new anole taxonomists.  While it was a fun look at the dynamics of anole taxonomy over time, I couldn’t help but feel like there is a more pressing taxonomic crisis going on right now, and it affects many of the researchers that frequent this blog.

I fear too many species of Anolis are being described based on questionable evidence.  While this problem is not unique to anoles (a common term for it is “taxonomic inflation”; Isaac et al. 2004), a number of recently described anole species may be the result of overzealous taxonomic splitting.  I will give some examples below and then briefly discuss two lines of evidence that I believe are often used to divide species inappropriately.  Before I do so, it’s worth stating up front that I’ll focus on the work of Dr. Gunther Köhler and colleagues. This shouldn’t be surprising, as Dr. Köhler is the most prolific living describer of anole species.  The following criticisms should not be seen as personal, as Köhler is not unique on any of the points I discuss below.  But with many cryptic species described or resurrected over the past 10-15 years, his work has the largest impact on anole taxonomy and the science that depends on it.

I’ll start with the revision of the Anolis tropidonotus complex published in Mesoamerican Herpetology (Köhler et al. 2016).  Below I provide a quick breakdown of the paper.  I hope that others will contribute their own views on this work in the comments.  The A. tropidonotus group is one that I am well-acquainted with, having spent months of field time collecting individuals across the distribution of the group.  Köhler et al. (2016) raise a subspecies (A. tropidonotus spilorhipis) to species status while describing two new species, A. wilsoni and A. mccraniei.  Unfortunately, the data presented–morphology and DNA–do not appear to strongly support the recognition of any new species level taxa.  I argue that the inference of four species within A. tropidonotus sensu lato should require stronger evidence than that presented.

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The authors sequenced 16S mitochondrial DNA for molecular analyses and present a consensus tree from Bayesian analyses of these data. This tree recovers four well-supported and geographically circumscribed mtDNA haplotype clades that correspond with the four new species. A table following the tree reveals the genetic distances between putatively new species topped out at 4.5%. This level of mitochondrial divergence is significantly less than intraspecific variation observed in other anoles (Malhotra & Thorpe 2000; Thorpe & Stenson 2003; Ng & Glor 2011). Moreover, Köhler et al.’s (2016) sampling map reflects sparse sampling of molecular data.

Based on Figure 3, morphology (other than perhaps hemipenes, which I discuss below) does not provide any support for delimitation of those populations characterized by distinct mtDNA haplotypes. The dewlap differences reported are slight and appear to fall within the type of variation observed within and among other populations of species in this group (see photos at the top of this post for an example of two spilorhipis males that came from the same locality; photos courtesy Luke Mahler). Bottom line–we see several populations with mitochondrial haplotypes that cluster together geographically with little to no morphological evidence for divergence.

The phylogenetic and morphological patterns displayed in Köhler et al. (2016) are consistent with patchy sampling of a widespread and continuously distributed species with potentially locally-adapted populations. The authors cite “the high degree of genetic distinctiveness… as evidence for a lack of gene flow, and conclude that these four lineages represent species-level units” (Köhler et al. 2016). This assumption is questionable, as researchers have long known of the pitfalls of using mtDNA to determine gene flow (Avise et al. 1983; Avise et al. 1984; Funk & Omland 2003) and supporting evidence from morphology is lacking. The different hemipenial types represent the strongest evidence for recognizing the lineages mtDNA haplotype groups. Below I will discuss the utility of those traits for species delimitation.

Finally, the authors did not compare their purported new tropidonotus-like species to Anolis wampuensis, a morphologically indistinguishable (McCranie & Kohler 2015) form that is potentially codistributed with the new species A. mccraniei. This should have been done to avoid the possibility that A. wampuensis is conspecific with one of the newly named forms.

Another example of taxonomic inflation in Anolis is from a 2014 monograph in Zootaxa (Köhler et al. 2014).

How a Well-Hidden Giant Got Uncovered: the Discovery of a New Anole Species from Hispaniola

Anolis landestoyi. Photo by Miguel Landestoy

My first encounter with the new Hispaniolan giant anole species was in December 2005, when leading a birdwatching tour west of Puerto Escondido, Sierra de Bahoruco, for a group from Scotland. Early one morning, just before dawn, we stopped at what was to become the type locality of the new lizard species and stayed for several minutes searching for some night birds (nightjars, poorwills and potoos) which are most active during crepuscular time windows. It became light, though still without sun. While standing next to the forest edge, the crawling of one of these giant lizards caught my eye. It was moving from a lower tree branch (presumably its roosting perch) towards the trunk and the treetop. It quickly moved out of view, disappearing within seconds. There were no chances for photography or capture.

One and a half years later, in May 2007, I was conducting a nest search for the endangered endemic Bay-breasted Cuckoo at the same locality. Starting at around 9 am, I hiked the trail that goes north in the bottom of the canyon, and nearly one hour later, I spotted two of these fairly large forest birds, foraging in the well wooded area. Closely and silently following the pair, I hid in a stalking manner behind vegetation and logs, occasionally getting my small binoculars out from my shirt pocket to see in detail behavioral events (feeding and mating were observed). This forest is pretty lush during the rainy season, and mosquitoes were everywhere, covering all exposed areas of one’s body. Somewhere between 11 and noon, on a sunny day, the pair seemed to have had enough activity and their stomachs may have been full (with all the cicadas around, that wouldn’t have been too hard). The birds were resting, not high in the trees, and away from sun. One of them was closer to me, well in view, and this same bird took off from its branch once, striking and trying to pull something off of a branch… It happened so fast that I could only pay attention to the bird. But my curiosity was piqued: there should be something on that branch… Binoculars out again, with cautious moves, I examined the branch. A slow scan revealed an extremely well camouflaged lizard, head facing down, that was also getting away from the sunny tree canopy. At first glance it resembled one of these large, big-headed anoles (wait, this looks like one of those barahonae-ricordii giants), but it was distinctly and unusually ashy and pale in coloration. I stared at the anole for some time, and when the birds were gone, it started moving lower down slowly. It came as close as 2 meters from ground, the right moment to attempt capture. Fortunately I had a bit of more luck than the birds had, and I captured the animal. Briefly studying the animal in hand, I noted the large dewlap and odd pattern, and took a few photos, but the lizard was faster than it looked! In a matter of seconds it quickly ran along the branch and then up the trunk and escaped!

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The giant Anolis ricordii, from a population not previously reported, east of the type locality. Males are usually pale-grayish like the one in this photo.

One year later, I met some great friends and professionals. Rich Glor was visiting with some students, as was Luke Mahler and some of his (Losos) lab mates and field assistants. I showed them a photo of the animal from my laptop, that only depicted the front part of the animal (head and anterior half). They had a very tight and ambitious schedule to complete during that visit, and unfortunately they weren’t able to visit that fairly distant locality.

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First photograph of the recently described Hispaniolan giant species.

The following year I was taking a workshop on natural history and scientific illustration given by the acclaimed Cuban naturalist and artist Nils Navarro, and while choosing some photos for an illustration, one from the strange anole came in view. Nils, who knows the Cuban fauna very well, immediately noted its similarity with Cuban Chamaeleolis-clade anoles. To his chagrin, I told him I hadn’t secured a specimen yet, but that I would try.

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Nearly fully extended dewlap of a captured Anolis landestoyi.

No more news from the odd looking anole, until March 2010, when I had the opportunity to re-visit the locality on my own, and dedicated some time to search for the beast. After three hours of night herping, scanning many epiphytes, tree branches, twigs, vines, leaves and trunks, I found one individual, very close from the 2005 encounter! This individual was captured and photographed. The more detailed images of the new individual revealed more unique characters, strongly pointing out the argument that was in fact a new species, and its resemblance in many aspects to the Cuban Chamaeleolis-clade was already obvious. Those photos were sent to the authors, which prompted a visit by Luke.

Nearly a week later, on April 1st, Luke was already sitting at the ministry office when we first spoke by phone that day. To Luke’s unfortunate coincidence with the current date’s event, I told Luke that I did not believe that he could take a plane so fast to the DR… “Wait, what? Luke, don’t tell me you actually came all the way down here man!” Luke responded: Yes man, I told you I would.” Me: “But I couldn’t believe you were so decided, and so responsive to those photos. Luke, honestly, those were actually taken in Cuba during my last visit to the land of Chamaeleolis.” Luke: “Are you serious man? Don’t tell me that now, Jesus!”… When I was convinced he had enough torturing, I came clean and told him it was a just a joke: “Happy April’s Fools Day amigo!” Luke was still skeptical, since he wasn’t sure I was still playing the prank, nor I was just revealing that I was in fact playing a prank to him. Bad (or actually good, indeed) timing, I guess.

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The senior author of the paper, Luke Mahler (left), and a local who happened to have some luck.

Luke came not only to see the specimen I had in captivity, but also to personally visit the locality and get to know the habitat and the species in the field. After several hours of traveling, we arrived just before evening, right after a light rain shower. We began our search once Luke took some habitat photos at the day’s last light. It may have taken nearly two hours to find the first one, a male that I spotted at about 1.5 m of height, head down. Luke secured a female some minutes after, and there they were, a pair of adults!

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The “mystical” forest at the type locality. There are parts of this forest with plenty of the bromeliad plant commonly called “Spanish Moss.”

Finally, after some years of hard field and lab work, the species came out of the anonymity, even though it must still be hiding deep into the dense viney and undergrowth transitional vegetation of the well wooded canyon (or more technically proper, “polje”), where the spanish moss and other epiphytes hang paradoxically within the cacti and hardwood forest surrounded by the big blocks of limestone that characterize this yet remote mountain chain. Threats are not too far from this rarity: in spite of this area being protected (Reserva Biológica Loma Charco Azul), due its proximity to the Haitian border, there is intense slash and burning agriculture in the hills west, and wood charcoal is produced in large amounts and taken to Haiti where it is the basic fuel for cooking. Is the species confined to the bottom valley of this canyon? All current knowledge point it out as very possible, which would mean that the species has a very small and highly vulnerable range.

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Forest burning near the type locality of the recently described anole. In the hills of western Sierra de Bahoruco.

Parasitic Fly Larva in Anolis cristatellus?

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This was a first for me: an anole with an odd, tic-tac sized growth on its lower left jaw. Though it is difficult to see in the image, there appears to be a small hole or opening in the cyst-like growth, potentially where a little sarcophagid larva will emerge from. (I’m not sure of the identity of the parasite, if indeed that is what is causing the growth – more information on the topic can be found in an older Anole Annals post).

As for the identity of the anole itself, I managed to catch a nearby individual (lacking any cysts) that I believe is the same species. It had a beautiful yellow dewlap, leading me to believe they are Crested Anoles (Anolis cristatellus).

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Insights from Three Years of Measuring Anolis sagrei Reproductive Success

Female Festive Anole (photo: Ambika Kamath)

Female Festive Anole (photo: Ambika Kamath)

Sexual dimorphism–differences between the sexes in what they look like–is rampant across animals. But how do these differences arise? Why and how might natural selection or sexual selection act differently on males and females? In a new paper from Duryea et al. (2016) published last month, we begin to see what answers to these questions look like in our very favourite organism, the festive anole, Anolis sagrei.

The data presented in this paper is unprecedented in anoles–by catching every lizard on Kidd Cay for four successive years, the authors assigned parentage to three generations of offspring, and thus assigned reproductive success to three generations of adults. Using these measures of reproductive success for males and females, they ask a straightforward question: is reproductive success correlated with body size, and do these relationships differ between males and females?

The results, however, are not straightforward: patterns of selection differ quite a bit across the three years of sampling, especially in females. But overall, we see directional selection on body size in males (bigger males father more offspring who survive to adulthood than smaller males), possibly explaining why male festive anoles are 30% larger than females.

We don’t yet understand the origins of sexual size dimorphism in anoles–why in particular, does the shape of selection on female body size vary so much? Do large males sire more offspring who survive to adulthood because they mate more often, or because their offspring are somehow better at surviving? Duryea et al. have propelled forward the state of our knowledge with a formidable dataset that raises exciting new questions.

The Evolution of Variation in Back Patterns in Anolis

Many species of anoles exhibit distinctive dorsal patterns, including spots (e.g. A. sabanus), stripes (A. krugi) or chevrons (A. sagrei) (Figure 1). Dorsal patterns are highly variable in anoles, presenting not only variation across species, but also within species (sexual dimorphism) and within sexes (polymorphism). So why is there such a large variation in dorsal pattern?

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Figure 1. Examples of dorsal pattern in Anolis lizards. A, A. sagrei, B, A. krugi, C, A. sabanus (photograph by B. Falk). D, A. pulchellus. Photographs A, B and D by D. L. Mahler.

Previous posts (1,2) explain the extent of the variation in dorsal pattern within females, a phenomenon known as female-pattern polymorphism (FPP), where females are more likely to present variation in dorsal patterns than males. Other studies have tried to explain within-population variation in dorsal pattern in several Anolis species with montane and xeric distributions. These studies suggest that habitat and crypsis could be an important factor explaining variation in dorsal pattern in Anolis.

Anoles are famous for having evolved convergent ecomorphs in different islands in the Caribbean. Each ecomorph is associated with a suit of adaptive traits that has evolved in response to their ecology. Some years ago, I went to the Losos Lab to explore, using several species of Anolis and hundreds of museum species, whether ecomorphs could explain variation in dorsal pattern. Namely, we wanted to know whether differences between ecomorphs could explain the degree of sexual dimorphism in dorsal pattern and female polymorphism, using 36 species of Anolis from the Greater Antilles.

In our paper, published on early view in the Biological Journal of the Linnean Society, we built a matrix with 11 different characters that described dorsal pattern. We used this matrix to construct a principal coordinate space, and in this space we calculated distances between male and female dorsal pattern for each species  (amount of dorsal pattern sexual dimorphism) and the variation in dorsal pattern within each sex (amount of polymorphism within sex).

We found that species perching closer to the ground have higher degrees of sexual dimorphism, and males and females from these species usually present different patterns (Figure 2). For example, in A. bahorucoensis, a grass-bush species, females present a dorsal stripe, while males have chevrons. We also found that size dimorphism is correlated to dorsal pattern dimorphism, and species perching closer to the ground have larger differences in size and dorsal pattern between sexes, suggesting that both types of dimorphism are evolving together. We suspect that larger differences in habitat use between males and females in low-perching species may explain why some species are more dimorphic in dorsal pattern that others.

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Figure 2. Association between sexual dimorphism in dorsal pattern and ecomorph in 36 species of Anolis. A, Phylogenetic tree with coloured branches representing values of dimorphism in dorsal pattern (Euclidean distance). Circles at tips represent ecomorph and the colour legend is the same as in (B). B, Values of dorsal pattern dimorphism according to ecomorph class.

On the other hand, ecomorph could not explain why some in some species there is higher variation in dorsal pattern in females (FPP). In our study, 44% of the species presented significantly higher female polymorphism than male polymorphism, reflecting how widespread is this phenomenon, but this was not related to ecomorph type. However, species with higher female polymorphism also had males that were more variable, suggesting that they might be under similar selective pressures. More precise information on habitat preferences within sexes, especially in  females, will be required in order to fully understand the mystery of female-biased polymorphism.

Reference

Medina, I., Losos, J.B. & Mahler, D.L. 2016. Evolution of dorsal pattern variation in greater Antillean Anolis lizards. Early view, Biological Journal of the Linnean Society.

Rodolfo Ruibal, R.I.P.

AA is sorry to learn of the passing of Rodolfo Ruibal, an eminent Cuban herpetologist based at UC-Riverside for many years. Rodolfo did important early work on thermal biology andsocial behavior of Caribbean anoles. For example, 1961 paper showed thermoconformity in some lizards (when everyone though that lizards always thermoregulate carefully), it showed that physiology can evolve faster than morphology, and it proposed that only thermoregulators (not thermoconformers) could invade the temp zone.

You can find transcripts from a 1998 interview with Rodolfo as part of a UC-Riverside history project. Here’s the obituary that recently appeared in UCR Today:

Professor Emeritus Rodolfo “Rudy” Ruibal, a founding member of UC Riverside’s Biology department whose passions included lizards, frogs and making beautiful jewelry, died Aug. 30 at the age of 88, just six months after the death of his wife of 68 years, Irene Shamu Ruibal.

“He was instrumental in forging the department in the directions and expertise that form its center now,” said Professor Michael Allen, chair of UCR’s biology department.

Ruibal was a native of Cuba who conducted research in several parts of South America with fellowships from the National Science Foundation and the John Simon Guggenheim Memorial Foundation. He was an early student of temperature regulation in reptiles and amphibians, said friend and colleague Professor Mark Chappell, and was also known for his work with water loss in amphibians and their ability to waterproof their skin by using waxy glandular secretions the animals wipe over themselves.

“He taught the Biology 161 course, on functional vertebrate morphology, or ‘Vert’ to generations of premeds and other life science students, and was renowned for both the clarity of his lectures and for his skill in drawing structures on the blackboard,” said Chappell.

During Ruibal’s 42 years at UCR, he helped establish the Philip Boyd Desert Research Center and spent a year as the acting director of UC MEXUS, created to stimulate teaching and research between California and Mexico. Ruibal also spent a year advising a man he much admired—UC President Clark Kerr—about faculty requests and concerns.

“He always had one faculty member in his office,” Ruibal said during an oral history interview in 1998. “It was his way of simply making sure his faculty were being treated by an academic who knew what the score was, rather than somebody who was just a bureaucrat.”

Ruibal’s life read like a novel. He was born in Cuba on Oct. 27, 1927, an only child who attended the same Jesuit school as Fidel Castro. The budding scientist had an early fascination for animals, said his son, Claude Ruibal of Zurich, Switzerland. Rudy Ruibal’s earliest memories were of watching fish swimming in the waters of Cuba, and chasing lizards in his yard, something his aunt remembered years later, when he returned to Cuba for research on an NSF grant project.

Reptiles and research always fascinated Ruibal, and he excelled at an early age. He enrolled in Harvard when he was just 16 years old, after completing high school at the prestigious McBurney School in Manhattan.

Ruibal took a break from Harvard when he was 18, to serve in the military at the tail end of World War II. But he returned to school a year later and married his wife, Irene, a secretary in the Department of Herpetology in the American Museum of Natural History.

By the time he was 21, Ruibal had finished his BA at Harvard and enrolled at Columbia University for graduate studies in biology. At 26, Ruibal completed his PhD and accepted a position at a new liberal arts college called UC Riverside, where Howard Spieth, one of his former professors at Columbia, had become the chair of the life science’s department, and would later become the university’s first chancellor.

Ruibal began teaching in the fall of 1954, the second semester for a school so new that it had no landscaping or trees. Their son was born the following year, in 1955. Claude Ruibal said his parents were loving but not overbearing. His father, he said, “was a thoughtful guy, a moral guy—very rational and not very emotional. I don’t think I ever heard my parents argue.”

His mother loved to cook and throw dinner parties, and they cultivated a diverse group of close friends—artists, business people, even the publisher of the newspaper. His father loved tennis, playing into his 80s, and did a lot of reading about history and politics.

Ruibal also was a noted local artist. Shortly after he arrived in Riverside, he successfully lobbied the Riverside Art Museum to have real nude models available for sketching (instead of women in bathing suits). He later branched into candle making, ceramics —complete with his own kiln—and finally, making brass and silver jewelry, which were top sellers at the Riverside Art Museum, Mission Inn Museum and other locations.

Anole Fashion: Dorsal Crests and Curlicue Tails

Daffodil’s Photo Blog has some nice photos of stylish anoles. Some anoles–the festive anole (A. sagrei) being a prime example, seem to have a penchant for sitting with their tails hanging in a lovely. Why do they do it? Got me.

We do know why they raise their dorsal crests–to look fearsome, as this mini-dinosaur does. How they do it, though, is another matter, when discussed previously in these pages (1,2).

Best Anole Dewlap of All Time?

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There are many contenders, but my favorite is Anolis sericeus, seen above from the Kanahau research station on the Honduran island of Utila, and another photo below from Chiapas, Mexico.

Lizards Running (and Slipping) in Ultra-Slo-Mo!

Day’s Edge Productions has done it again (again? see here and here).

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