Category: Classics from the Literature Page 1 of 4

In a recent review of old literature for some projects on Cyclura iguanas, I came across some notes from Gosse (1848 ) in which he speculates upon the nature of the lizard dewlap. I think it is fun and fascinating to think about how naturalists approached the idea of deducing what functions these structures might have served! In this narrative about Jamaican lizards, Gosse rather breathlessly describes some exciting correspondence he received from his friend Richard Hill, Esq., of Spanish-Town Jamaica, adjacent to Kingston on the southeast coast:

Hill: “The gular pouch which hangs like the dewlap of a bull beneath its throat can be inflated*. but it is not exactly known under what circumstances, ordinarily, it has recourse to this power of inflation. When filled with air it would give breadth and buoyancy to the body, and if its habits are as aquatic as some accounts make them [those of Iguana proper] to be, it would afford to an herbivorous animal no unimportant aid while swimming and cropping its flowery food.”

Gosse: “*I believe my friend has fallen into a common error here. If I may judge from analogy in the genera Anolis and Dactyloa, the gular pouch in the Iguanidae is extensible but not inflatable, as I hope to show in a future paper on the habits of these genera.”

So, naturalists at the time speculated that the lizard dewlap might be a flotation device! Perhaps a natural explanation for species that readily take to water when they flee, such as Iguana iguana, but potentially applying across lizards with that feature. Gosse has already decided that Anolis dewlaps did not suit this purpose and thus that this seemed less likely for other iguanas as well, but he tees us up for the eventual settling of this issue of inflatable dewlaps.

Gosse continues:

“The notion expressed about the inflation of the gular pouch was the consequence of seeing two very large Iguanas from Cuba, which distended this appendage, and let it collapse again. The skin of these animals hung about them, as if they had been fat, and were, at the time I saw them, emaciated.”

Here Gosse is throwing cold water on this idea again, but you can tell from reading the text relating this correspondence that he must have relished the opportunity to receive such intelligence from the field and then have the opportunity to discuss and evaluate it!

Mr. Hill continues:

“When excited it assumes a menacing attitude, and directs its eye to the object of attack with a peculiarly sinister look. At this time it inflates the throat, erects the crest and dentelations on the back, and opens the mouth, showing the line of those peculiarly-set white teeth, with serrated edges, so excellently made to illustrate the remains of the gigantic fossil Iguanodon. The principle of their construction is so precisely similar, as to leave no doubt of the genuine connection of the extinct with the existing herbivorous lizard. The adaptation of both is for the cropping and cutting of vegetable food.”

Here, just to draw attention to this rather remarkable fact, is an amateur naturalist (although, to be fair, advanced formal training in biology was not available during this time and naturalists were largely self-taught) who in 1847 is pronouncing upon the use of this dewlaps, while also simultaneously acknowledging extinction, evolutionary similarity, and adaptation. We often talk about these latter notions as having crystallized after Charles Darwin and Sir Richard Owen brought ideas regarding natural selection (and adaption) and extinction, respectively, into the mid-19^th Century Victorian intellectual milieu. But Cuvier and others had proposed robust examples of extinction at the turn of the 19^th Century, and millenia of ideas, dating back to Hellenistic Scholars, through the Golden Age of Islamic Scholarship, to the parlors of Renaissance Europe had proposed that some traits proved “favorable.” Further, Iguanodon was discovered in 1822 by Gideon Mantell (not, famously, by Cuvier and Owen). So, such ideas were available to progressively-minded naturalists of the time, and it is refreshing to see such a confirmation in print!

NB: Just to further tempt you to take a dive into this literature, this is also the issue where Sir Richard Owen describes the Moa birds from New Zealand! What epic rainy-day reading! Check out the link to the issue, I recommend it!

With thanks to Ari Miller (WUSTL, Losos Lab) for pointing me toward this reference.

Article:

Gosse, P.H. 1848. On the habits of Cyclura lophoma, an iguaniform lizard. Proceedings of the Zoological Society of London 99–104.

Link: https://archive.org/details/lietuvostsrmoksl48liet/page/n137/mode/2up

Dewlap Displays in Cuban Knight Anoles (A. equestris)

By James T. Stroud

On June 17, 2016

In Anole Photographs, Classics from the Literature, Introduced Anoles, Natural History Observations, Notes from the Field

While exploring the grounds of Fairchild Tropical Botanical Gardens with Janson Jones this past weekend, we extremely fortunately happened upon a large adult male Cuban knight anole (A. equestris) in full displaying swing. Despite the fact that knight anoles have an impressively large dewlap, I have often found this to be a relatively rare event, as large crown-giant species tend to display less than other smaller and more active species. This individual was displaying at a height of ~15 m, just below the fronds of a large Royal Palm (Roystonea regia). We didn’t see any other neighboring knight anoles, so were unsure if this was a directed or passive display series. In all, this lizard performed perhaps 4-5 sets of dewlap displays (each comprising of 4-5 dewlap extensions) before stopping and retreating back into the canopy.

Anoles typically follow a predictable and repeated pattern of display that gradually increases in intensity. Initially, and rather lethargically, an individual will nonchalantly raise its head and extend its dewlap without much extra effort (stage a); described below from Losos (2009).

Adapted from Losos (2009), which itself is adapted from Losos (1985). Aggressive behavior of A. marconoi showing three stages of increasing display intensity – note stage (c) include full body elevation alongside simultaneous tail and dewlap extensions.

This then escalates to include a slight body raise (stage b).

And ultimately results in a dramatic finale – in full display all limbs will be extended to raise both their body from the substrate (in this case the trunk of a palm tree) and elevate their tail (stage c). In the following picture you can see this final stage of displaying where intensity peaks – albeit in this individual with a regenerated (and rather stubby) tail.

Mangrove Twig Anoles

By Graham Reynolds

On April 10, 2015

In Classics from the Literature, Notes from the Field

Anolis angusticeps, South Bimini, Bahamas

One component of our recent field work in Bimini, Bahamas involved gathering data from anoles across various habitat types. We selected four primary habitats for sampling based partly on the notable work by Schoener (1968): blackland forest; incipient blackland; Coccothrinax coastal scrub; and mixed Avicennia, Laguncularia, and Rhizophora mangrove forest.

Mangrove forest nocturnal survey.

South Bimini is an interesting place to study anoles in that it is a relatively small island harboring four species across at least eight different habitat types. Schoener’s excellent study of habitat use in these species indicated that mangrove forests were marginal habitat for anoles, supporting only two of the four species (A. sagrei and A. smaragdinus). During nocturnal surveys, we located both of these species roosting on Avicennia and Laguncularia leaves and branches, though in much lower numbers than other forest types. We found no anoles in Rhizophora mangle at our study site. However, we did find a number of A. angusticeps in this forest, mostly perching horizontally on Avicennia branches. We would like to know, how many others have found twig anoles in mangrove forest?

Classics from the Anolis Literature: the Ethoecology of Anolis nebulosus

By Martha Muñoz

On July 5, 2014

In Classics from the Literature

Image of Anolis nebulosus taken by John Murphy and borrowed from the Reptile Database.

Although anoles are one of the top model systems in evolutionary biology today, it took decades of dedicated and inquisitive research to lay the groundwork. The foundation of understanding that we draw upon today to set up hypotheses, build experiments, and infer the process of evolution was slowly built by numerous researchers, including Ernest Williams, Rodolfo Ruibal, Stan Rand, and Ray Huey, to name only a few. Tom Jenssen, Professor Emeritus at Virginia Tech, stands among these giants – his work on the ethoecology of anoles laid the foundation for how we understand anole behavior, particularly display behaviors, and set up the experimental framework for how we conduct behavioral studies in anoles even today.

If you’re familiar with Tom’s research, then you’ll know he’s worked on Anolis carolinensis for more than two decades and, before that, he studied several species of Caribbean anoles. But back when he was a graduate student, Tom’s main focus was on a little-known anole from Mexico, Anolis nebulosus. During this time, he tracked a single population of A. nebulosus for over three years, and examined the behavior of hundreds of lizards. In 1970 he published some of the results from this long-term study in the Journal of Herpetology.

Anole Celebration of Darwin’s Day

By Ramon E. Martinez-Grimaldo

On February 12, 2014

In Anole Art, Literature, and Humor, Classics from the Literature

Happy Darwin’s day everybody!

This is the third serial year in which I have remembered Darwin Day in Anole Annals. In the first time, Jonathan Losos made a wise comment in citing the words of Darwin about an anole (read his comment here). That’s why, this year, I have added two pages from ‘The Descent of Man, and Selection in Relation to Sex’ in which Darwin wrote about the sexual selection of Anolis cristatellus and Sitana.

Historical Perspective On Anole Genera

By Rich Glor

On October 1, 2012

In Classics from the Literature, New Research

Anole taxonomists: Richard Etheridge, Jay Savage, Ernest Williams, S. Blair Hedges, Craig Guyer, Steve Poe

Anolis has been recognized as an extraordinarily large genus for decades, but Nicholson et al. (2012) are not the first to propose recognition of multiple anole genera. Indeed, all of the generic epithets used in Nicholson et al.’s new classification were coined in 1934 or earlier and most are from the early 19th century. This early proliferation of generic epithets resulted primarily from the fact that a comprehensive systematic treatment of anoles did not appear until the mid-20th century. My purpose here is to review the history of generic level anole classification in the years following Richard Etheridge’s pioneering PhD thesis of 1959/60. I believe that this historical perspective provides necessary context for evaluation of Nicholson et al.’s proposed revisions, and helps explain why the genera in their revised classification appear so rarely in the literature relative to Anolis (see Mahler’s recent post on the topic of genus name usage).

To briefly summarize the history of anole genera, the vast majority of work published over the past half century has formally assigned all, or nearly all, anole species to Anolis. The only noteworthy exceptions to this include (1) assignment of a small number of morphologically unusual species from the mainland, Cuba, or Hispaniola to Phenacosaurus, Chamaelinorops or Chamaeleolis into the 1990s and (2) assignment of species belonging to Etheridge’s β section of Anolis to Norops by some anole biologists working primarily in Central America during the 1990s through the 2000s.

Etheridge’s dissertation, which was completed in 1959 but not available until 1960.

In 1959, Richard Etheridge, a PhD student with Norman Hartweg at the University of Michigan, submitted a thesis that relied on remarkably thorough analyses of skeletal morphology to revise anole classification. At the beginning of this study, Etheridge recognized Anolis as a diverse genus containing over 200 species, but also identified ten other anole genera that contained only one or a few species: Chamaeleolis, Phenacosaurus, Chamaelinorops, Tropidodactylus, Audantia, Mariguana, Diaphoranolis, Xiphocercus, Deiroptyx, and Norops. Etheridge found the first four genera listed above to be “so unusual” morphologically that they warrant continued recognition, but the rest were synonomized with Anolis because his morphological analyses found them “to be not at all separable from Anolis, or to be based on characters so trivial that they are here considered as identical with Anolis.”

Etheridge left the large genus Anolis intact in spite of the fact that, at the beginning of his study, he “thought it very likely that the great number of species in the genus Anolis might be dividied into several groups, and that each of these might reasonably be accorded generic status.” His reason for leaving Anolis intact was that “the relationships of the various species of Anolis have proven to be far too complex to be treated in so simple a manner as the proposal of formal generic groupings.” Rather than naming new genera, Etheridge informally characterized sets of species at “several different hierarchical positions between the genus and species” as “groups,” “complexes,” “sections,” or “series.” The aspect of Etheridge’s classification that drew the most attention was his division of Anolis into α and β sections distinguished primarily on the basis of basis of a striking difference in the morphology of tail vertebrae (see figure above from Etheridge’s disseration).

Anolis Electrum: The Amber Anole From Mexico

By Jonathan Losos

On September 22, 2012

In Classics from the Literature

A recent photograph by Emma Sherratt. Amber tends to darken over time, which explains the deep orange color.

We’ve had previous posts on fossil anoles in amber. Emma Sherratt is currently studying them and has examined some three dozen specimens. All of these are from the Dominican Republic. Except the first one ever discovered, a Mexican piece described by Skip Lazell in 1965. Anolis electrum, as it was named, has had a pretty quiet scientific life. Now middle aged, the species has not been the subject of any subsequent research in the 47 years of its existence. But now it’s in the spotlight, as its phylogenetic position and dating may be pivotal for the recent calculation by Nicholson et al. that anoles originated more than 100 million years ago. In this post, I summarize what is known about A. electrum (examine the short original paper for yourself!). No doubt, we’ll be hearing more soon about the relevance of this species–specifically its phylogenetic placement and age–for dating anole diversification.

As you can see for yourself in the photo above, there are actually two pieces, a front half of a lizard and a back half a lizard. Since they were found together (or at least made it to the Paleontology Museum at UC-Berkeley together) and are matching in size, it seems like too much of a coincidence for them not to come from the same animal. Various aspects of the animal’s scalation are discernible, including some nicely visible toepads. Lazell stated that all that was left was skin, or the impression of skin, the bones having been eaten away, but Emma’s cat scanning has shown that this is not quite correct (see below).

Based on the specimen, what can be said about its phylogenetic placement? All anoles in Mexico today are from the Norops clade. Unfortunately, the primary character for identifying Norops is the shape of the caudal vertebrae, which cannot be discerned in this tailless specimen. Lazell compared the scalation of this specimen (a 26 mm juvenile) to various species, and found that the scalation was unlike most species. He concluded that electrum was most similar in scalation to A. fuscoauratus, A. maculiventris, and A. chloris, and among species found in Mexico, to A. limifrons (full quotations at the bottom of this post).

What should we make of all of this? It’s important to remember that this paper was published in 1965, prior to the description of many extant anole species and a year before Willi Hennig’s classic introduction to cladistic analysis was translated into English. This is a purely phenetic comparison of the amber baby lizard to known species, clearly non-phylogenetic and utilizing characters that now are recognized to generally have little higher level systematic utility in anoles. And the conclusion is that it is either a Norops clade anole (fuscoauratus, limifrons or maculiventris) or a Dactyloa species (chloris).

The other question one might have is: how old is this fossil? Dating amber is notoriously difficult. Solórzano Kraemer reviewed all of the data on Mexican amber bearing deposits in the 2010 volume Biodiversity of Fossils in Amber from the Major World Deposits and concluded: “In summary, it can be said that Mexican amber can be correlated with Dominican amber, with an age of approximately 15-20 million-years-old.” In other words, Mexican and Dominican amber anoles were contemporaneous.

Did anyone notice anything odd on the fossil of the lizard posterior (B, above)?

The Gray-Dewlapped Anole: Anolis Carolinensis Seminolus

By Jonathan Losos

On June 11, 2012

In Classics from the Literature

Head variation in Anolis carolinensis. From T. Vance (1991).

There was some talk a while back about the fabled gray-dewlapped anole of Florida (and, according to the comments, elsewhere). Amidst this discussion, one commenter referred to it as Anolis carolinensis seminolus. Many of us, even experienced anole hands, were unaware that A. carolinensis had subspecies. After a little bit of poking around, we’ve discovered the answer. Indeed, there are described subspecies. Thomas Vance, in a paper in the Bulletin of the Maryland Herpetological Society in 1991 described the gray-dewlapped form as A. c. seminolus, relegating the rest of the species to A. c. carolinensis. The paper, which can be downloaded here, is not as overwhelming as its 47-page length might imply. There’s a nice discussion of the history of the species name A. carolinensis (turns out that it’s quite a confusing trail of names), followed by a detailed comparison of morphological variation, focusing primarily on scale characters and based on the examination of nearly a thousand specimens. There’s a lot of molecular phylogeographic work on carolinensis in the works right now, and it’ll be interesting to see how the genetic data square with Vance’s taxonomy (my guess: not so well). More generally, it’s surprising how little work on variation in this species has been conducted. For anyone interested in this fascinating and underappreciated lizard, this paper is worth a look.

Anole Classics: Ray Huey (1974) on the Cost of Behavioral Thermoregulation (or, What’s the Deal with Thermoconformity?)

By Alex Gunderson

On April 30, 2012

In Classics from the Literature

A male Anolis cristatellus from Puerto Rico. Photo by Dave Steinberg.

It is somewhat intuitive to assume that the body temperatures of “cold-blooded” animals like anoles must closely match ambient temperatures. For example, lizards from cold climates should be active at colder body temperatures than those from warm climates, and body temperature should change throughout the day in concert with air temperature. As Martha Muñoz has discussed, Cowles and Bogert laid this expectation to rest in 1944. They demonstrated that lizards can behaviorally thermoregulate, altering the effective thermal environment that they experience to remain within a “preferred” temperature range while active.

The potential benefits of behavioral thermoregulation are pretty obvious. Seek out a little sunlight on a cold day and you can go from freezing your hemi-penes off to enjoying a fulfilling day of doing whatever a lizard might find fulfilling. So for many years after Cowles and Bogert, observing patterns consistent with behavioral thermoregulation became the expectation.

A Changing Climate – The Birth of Biophysical Ecology and Modern Reptile Thermobiology

By Martha Muñoz

On April 15, 2012

In Classics from the Literature

Anolis armouri basking on a rock.

Our era of human-mediated climate change has brought startling new realities that we must face – ocean acidification, desertification, and receding ice caps, among others. For those of us who study lizards, one message is pervasive and clear – many species are being pushed to their thermal limit, and it is likely that many lizards, especially those that prefer cooler temperatures, won’t be able to take the heat. But, how do we know this? One of the main methods used to determine how reptiles will respond to climate change is to compare their preferred temperature (i.e., where lizards would like to keep their body temperature, given the option) to a random sampling of the thermal environment.

From a lizard’s eye view, though, the thermal environment is more complex than just air temperature. Lizards have volume, shape, and color, all of which affect their core temperature. Essentially, the operative temperature (Te) describes a lizard’s thermal environment as the sum total of many different interactions, such as radiation and convection, among others. Because it describes how temperature is shaped by everything except behavior and physiology, the operative temperature essentially describes how a perfect thermoconformer instantaneously perceives the environment. As such, it has been used as the null hypothesis for behavioral thermoregulation – if we can describe the thermal environment by recording Te, then we can use field-measured body temperature to determine the degree to which animals are thermoregulating. Here on the Anole Annals I’ve considered how devices have evolved to capture the operative temperature. The earliest prototype was a water-filled beer can, and we now have copper models painted to match the organism’s reflectance and HOBO devices.

Copper models of Anolis cybotes in the making.

But just where did these devices come from? I’ve been in Terre Haute, Indiana working with Dr. George Bakken at Indiana State University for the past two weeks making copper models of Anolis cybotes for my field research in the Dominican Republic. Dr. Bakken, along with Dr. David Gates, operationalized the term “operative temperature” for the ecological community in a seminal 1975 paper. I sat down with Dr. Bakken for an interview to learn how the intellectual climate promoted this and other important foundational works for biophysical ecology and reptilian thermobiology.