Zookeeper Amber Carney sent these photos of what is likely Anolis carolinensis. The lizards were spotted in Balboa Park, San Diego, CA, at 3pm on the 19th of April. They’ve been reported in Los Angeles but, to the best of my and Jonathan Losos’s knowledge, never in San Diego. Has anyone else observed wild anoles in San Diego? Range expansion!
A few months back, we had a post on the conservation situation in Jamaica with particular emphasis on the Hellshire Hills, last redoubt of the Jamaican iguana. Now in the journal Oryx, Rick Van Veen and Byron Wilson of the University of the West Indies, along with Tandora Grant and Richard Hudson, of the San Diego and Fort Worth Zoos, respectively, express further concern of the situation. Most of the article can be viewed online; add “and the environmental conventions to which it is a signatory.” to the last line and you’ve got the whole article.
Field research does not always go the way we plan. My research partners and I were reminded of that in 2004, when we tried to use a mark-and-recapture method to determine the population sizes of brown anoles (Anolis sagrei) in a small betelnut palm (Areca catecha L) plantation in Santzepu, Sheishan District, Chiayi County, southwestern Taiwan. We ended up with too low recapture rates for our estimates. Still all was not lost! Of the lizards we did recapture, we were able to calculate monthly growth rates and monthly growth percentages. The results indicated that at least some individuals experienced active growth throughout the year. Our results also supported the findings of Schoener and Schoener (1978) and Cox et al. (2009) that smaller individuals of both sexes grew faster than larger conspecifics of the same gender, and that males grew faster than females. We also determined that growth rates of both sexes decreased during the peak reproductive period, suggesting that available energy is directed primarily to reproduction and the associated to behavior, and that energy is only directed towards growth once the requirements for reproduction are met.
The experience from this study convinced me again that it is important to collect as much data as possible when conducting field studies – it is hard to predict where it may come in handy at a later stage.
When most people think of vertebrate sexual dimorphism (differences between the sexes), they think of elephant seals or red deer. Most of us here, of course, think of the pronounced dimorphism in size and shape in many anole species. Indeed, anoles have served as excellent model systems for the study of sexual dimorphism, particularly the evolutionary forces that give rise to it. Although there has been significant progress since Darwin in our understanding of why sexual dimorphism evolves, we have made less progress in the HOW. That is, what mechanisms during development give rise to what are often extreme differences between the sexes when their genomes are so similar?
When we think of vertebrates where males are larger or shaped differently than females, and have weapons or ornaments, we almost immediately think of testosterone as a mechanism underlying the sex differences. Once sexual maturity happens, the testes start cranking out testosterone, thus causing a change in the male’s phenotypic trajectory. While there is certainly evidence for circulating testosterone to have this effect in some lizards, is this always the case, and does it apply to specific body parts and not just overall size? Aside from the circulating hormone, how are receptors involved in the development of dimorphism? In a new paper by Sanger et al., a novel developmental pathway of sexual dimorphism is described for lizards in the carolinensis clade, which are striking in their elongation of male faces relative to females.
Sanger et al. tested whether sex differences in several different pathways led to the observed head shape dimorphism in A. carolinensis compared to two non-carolinensis species (A. cristatellus and A. sagrei) that exhibit shorter male faces. They show, using a combination of developmental and molecular genetic techniques, that the extreme elongation of male heads in carolinensis lizards is not due to an androgen pathway (i.e., testosterone) or the somatropic axis (i.e., insulin-like growth factor). Instead, they found a significant shift in the estrogen pathway. Specifically, at sexual maturity, males decrease expression of estrogen receptors (erβ), which is the beginning of a signaling cascade, ultimately resulting in up-regulation of genes involved in skeletogenesis in the skull of males.
This identification of a novel mechanism for the development of sexual dimorphism will certainly stimulate further evo-devo research in anoles and beyond. For starters, is the same pathway responsible for male facial elongation in other species in the carolinensis clade, or are more ‘traditional’ mechanisms operating there? This important research highlights that investigators need to consider all aspects of signaling systems, including circulating hormones, their receptors, and signal cascades that result from activation of a particular pathway. Clearly this paper by Sanger et al. is an excellent step in the right direction for understanding how developmental pathways lead to adult difference in anoles, and it will also steer other investigators to consider a diversity of developmental mechanisms in their quest to elucidate how adults end up the way they do.
Sanger TJ, Seav SM, Tokita M, Langerhans RB, Ross LM, Losos JB, Abzhanov A. 2014. The oestrogen pathway underlies the evolution of exaggerated male cranial shapes in Anolis lizards. Proceedings of the Royal Society B 281:20140329.
Let’s face it, “squamate” doesn’t work. It’s an ugly word, and most people don’t know what it means–if anything, it conjures up “squamous cell carcinoma,” a type of skin cancer.
More importantly, the term is not needed. Squamate comes from the scientific order Squamata, the lizards and snakes. But we know that snakes evolved from lizards–they are one type of lizard. In other words, lizards do not form a monophyletic group; they are paraphyletic with respect to snakes.
Does this remind you of any other major group of vertebrate? Say, birds and dinosaurs? We all know that birds evolved from dinosaurs, they are a type of dinosaur; dinosaurs are paraphyletic with respect to birds. And so, what is the solution to this problem? We now realize that birds are dinosaurs, members of the Dinosauria. Indeed, failing to recognize birds as a type of dinosaur commits the sin of paraphyly, obscuring the fact that some dinosaurs (in the old sense) are more closely related to birds than they are to some other dinosaurs.
And so, for the same reason, we should start referring to snakes as one type of lizards and, in turn, when we use the term “lizard,” we should understand that we are referring to snakes as well. In other words “Lizard” = Squamata. And, hence, we have no need to use the term “squamate” in common discourse.
We all know that many anoles species are very good at behaviorally regulating their body temperature by moving from an area that is too hot or too cold to another area that is just right. But how do they actually judge the thermal properties of a particular microsite? There’s been a lot of work on the sensation of temperature in mammals, but not so much in reptiles.
Recently, Erkin Kurganov and colleagues at the National Institutes of Natural Sciences, in Okazaki, Japan began to rectify this shortcoming, and their paper has just been published in Pflügers Archiv – European Journal of Physiology. Here’s the abstract:
Transient receptor potential ankyrin 1 (TRPA1) is a member of the large TRP super family of ion channels and functions as a Ca2+-permeable nonselective cation channel that is activated by various noxious stimuli. TRPA1 was initially identified as a potential mediator of noxious cold stimuli in mammalian nociceptive sensory neurons, while TRPA1s from nonmammalian vertebrates (snakes, green anole lizards, and frogs) were recently reported to be activated by heat, but not cold stimulus. In this study, we examined detailed properties of the green anole TRPA1 channel (gaTRPA1) related to thermal and chemical stimulation in whole-cell and single-channel recordings. Heat activates gaTRPA1 with a temperature threshold for activation of 35.8 °C, while heat together with allyl isothiocyanate (AITC), a chemical agonist, had synergistic effects on gaTRPA1 channel activation in that either the temperature threshold or activating AITC concentration was reduced in the presence of the other stimulus. Significant heat-evoked gaTRPA1 activation was observed in the presence but not absence of extracellular Ca2+. gaTRPA1 channels were also activated by heat and AITC in excised membrane patches with an inside-out configuration. By comparing the kinetics of heat- and AITC-evoked singlechannel currents, we defined similarities and differences of gaTRPA1 channel responses to heat and AITC. We observed similar current-voltage relationship and unitary amplitudes for heat- and AITC-evoked currents and found that heat-activated currents showed shorter durations of both open and closed times. Our results suggest that the gaTRPA1 channel is directly activated by heat and chemical stimuli.
Ron Savage, who works for USAID and is currently posted in Haiti, reports “I haven’t been getting out herping in Haiti much since I sold my car but today I managed to go out and check out some relictual forest (at about 2,700 ft elev.) not too far from Port au Prince and photographed these two anoles. This is the first time that I’ve seen this species in Haiti or the DR come to think of it. They were both up a tree about 15-20 feet and I would say that they were both about 8-9″ long including their tails. As you can see, one has a stump tail. He was higher in the tree keeping his eye on the greener one. I honestly don’t know what these are, do you have any idea? It could actually be two species. I’m not familiar with A. ricordii, but I suppose this could be one.”
Reports Pat Shipman in Little Cayman, adding “Notice the difference between her expression and his. Anolis maynardi on Little Cayman, just after a nice rain.”
And notice that sexual dimorphism in snout length!
Before leaving for Cuba, Martha and I discussed our anole wish-list. Figuring prominently were Cuba’s legendary sister-species, A. bartschi and A. vermiculatus. Also swiftly declared were the beautiful A. allisoni and anything in the erstwhile genus Chamaeleolis (alas, we found none of the snail-eating giants). However, I must admit — I had no idea A. lucius existed until I first laid eyes on it!
After encountering A. lucius in a patch of mature forest along a slow-moving stream, my first impression was that it looked and behaved like a trunk anole, if trunk anoles were 150% bigger and had zebra stripes on their heads. Indeed, at the first locality we encountered them, they seemed to favor perching head-down on trunks 1-3m high (with one individual spotted almost 5m high.)
Although I’m still fond of my initial diagnosis of “giant zebra-headed A. distichus,” we proceeded to encounter A. lucius in a variety of other habitats. For instance, we found them scrambling over limestone karst and taking refuge in sea cliff caves on Cuba’s southern coast, a habit described in Schwartz & Henderson’s Amphibians and Reptiles of the West Indies. Later I would wonder what A. bartschi, were it to occur syntopically, would have to say about that.
We also found A. lucius near human habitation, on the streets of Trinidad and the home of a coffee farmer in Cuba’s Topes de Collantes nature reserve park.
So it seems clear that this anole is jack of at least a few trades. But wait, there’s more!
A. lucius has a bizarre trait, one that’s shared with a close relative already featured on Anole Annals, A. argenteolus. Can you guess what it is? If you guessed translucent scales on the lower eyelid, you win! The function of these “shades” is not entirely clear, with one obvious idea being that they block harsh sunlight. For what it’s worth, we almost never saw A. lucius close its eyes during the day.
A. lucius was, dare I say, a dark-horse third-place finisher on the list of coolest species we managed to see. I’ll (probably) finish off the top three next time with A. vermiculatus!
Anoles with sunglasses…just stop, evolution.
Some people think so, such as this posting on the Association of South Eastern Herpetogists website. I have my doubts about the presence of porcatus in Florida. Anolis carolinensis, after all, is derived from A. porcatus. In reality, it is simply a population of A. porcatus, perhaps smaller than most of their Cuban comrades. Suppose for some reason A. carolinensis started growing larger–wouldn’t they look like the green anoles on Cuba? Anyone have thoughts on whether Cuban porcatus are really in Florida and, if so, how easy it is to identify them?
If I were to take survey of Anole Annals readers regarding the factors that regulate aggressive and showy behaviors, I suspect that the vast majority of you would implicate testosterone as the primary culprit. Whether we are discussing humans or nearly any other vertebrate, there is a common societal notion that testosterone fuels these behaviors like oxygen fuels fire. The widespread belief is simple: individuals with more testosterone tend to exhibit more aggressive, ostentatious, and risky behaviors.
For decades researchers have investigated the link between testosterone and behavior in a variety of biological contexts – including different behaviors, experimental manipulations, environmental conditions, and life history parameters – but rarely in wild animals or within an evolutionary context. If the supposed testosterone-behavior correlation is extended to a broader, comparative context, it would suggest that aggressive species should also have higher levels of circulating testosterone than more placid species. But, in an upcoming paper, Husak and Lovern test the testosterone-behavior supposition among Anolis lizards and, quite frankly, turn it right on its head. To give away their conclusion at the outset, three of the four “aggressive” anole lineages examined have evolved this behavior without a clear correlation with circulating levels of testosterone.
Anolis lizards are renowned for their convergent anatomical evolution (reviewed in Lizards in an Evolutionary Tree), but these species have also independently evolved similar behaviors. In a study that was one of the first of its kind, Johnson et al. showed that the Anolis ecomorphs exhibit evolutionary convergence towards similar patterns of aggressive display and territorial behaviors. Trunk-ground anoles tended to be the most “aggressive” ecomorphs, consistently exhibiting higher display rates and territoriality than the trunk-crown, grass-bush, or twig ecomorphs. Twig species tended to exhibit the least aggressive behavior in the analysis. (Also see Ord et al. 2013 for a more fine-scale dissection of display behavior.) Using this pattern of convergent behavior as a foundation, Husak and Lovern predicted that trunk-ground anoles would have higher levels of circulating testosterone than other ecomorphs from the same island, twig anoles the least. The absolute levels of testosterone might vary depending on the specific lineage in question, but they predicted that the rank-order of testosterone on each island would follow the behavioral continuum described in Johnson et al. In total the authors surveyed circulating levels of testosterone and corticosterone, an adrenal steroid hormone associated with stress, in 18 Anolis species!
As I already stated, the authors found no support for the idea that elevated levels of circulating testosterone consistently drive aggressive behavior in Anolis lizards. Instead they found that three out of the four clades of trunk-ground anoles had the lowest levels of testosterone, the opposite pattern than would be predicted based on their behavior. Continue reading
Check out this green anole photographed at the Archbold Biological Station in Florida by Nick Fletcher, participating in a Cornell University field trip led by Harry Greene.
And here’s one more by Nick, taken a day later.
Spring is the season for spotting crown-giant anoles in Miami!
I was hosting (recently graduated Lacertid-ophile, although closet anologist) Dr. Robert Heathcote for a few days this week, and after his failed attempt at catching a Cuban knight anole (A. equestris) a fortnight previous, I had promised to deliver him another! Now, I imagine many AA readers may chuckle at someone foolish enough to promise a crown-giant observation (myself included). Much to my relief luck was on our side and we managed to spot not one, but TWO species practically on top of each other!
Cuban knight anoles (A. equestris) and Jamaican giant anoles (A. garmani) are both non-native introduced species to south Florida.
I was recently in St.lucia travelling around photo-documenting the local Anolis luciae which seem to be rapidly being displaced by the invasive A. wattsi from Antigua. While exploring the southwestern town of Soufriere, I came upon a few specimens of this species in the backyard workshop of the sculptor host of mine.
I have showed the photos to a few herpetologists at UWI (St. Augustine) and they are as baffled as I am; for the closest-looking possibility, A. richardi, native to Grenada and the Grenadines, is not noted to have migrated this far north.
Any takes on what species it could possibly be?
A few months ago, I ran into Nicholas Dawidoff, the author of the fabulous new book Collision Low Crossers: A Year Inside the Turbulent World of NFL Football. Seeing Nicholas reminded me of the article he wrote for Sports Illustrated at the very dawn of his writing career, 25 years ago today. The article was on the then developing field of performance studies, measuring the sprinting, jumping, clinging and other capabilities of small ectotherms, and featuring none other than yours truly, as well as Ray Huey, Al Bennett, and Sharon Emerson. Written tongue-in-cheek, but accurately and respectfully, the article was a very nice overview of that emerging field of study. It’s worth checking out the article just to see the wacky pictures taken by the SI photographer sent out on assignment to Seattle and Berkeley.
If you followed the barrage of blogposts we wrote from SICB 2014, you might recall some discussion of the information actually conveyed by anole displays and dewlaps (1, 2). The upshot of these studies is that anole displays are complex. We see unexpected relationships between various traits and the probability of success in male-male competition, and different traits correlate with different measures of male success. A recent study by Steffen and Guyer (2014) adds to our growing knowledge of the information conveyed by different dimensions of multimodal anole displays. When viewed together with previous research, this study presents us with an even messier picture than before of how Anolis lizards communicate with each other.
Steffen and Guyer (2014) set up paired competitions between size-matched male Anolis sagrei in a lab setting, implementing two treatments–males either compete for access to a single perch, or for mating access to a single female. All interactions were recorded, and display behaviours–headbobs, push-ups, dewlap extensions–were quantified. Further, the spectral reflectance of both the centre and the margin of the dewlap (which can be strikingly different in A. sagrei) was also measured. The question asked by the paper was straighforward: which display and dewlap traits are related to an individual lizard’s status as a winner or loser of competitions?
In both competitive contexts, only two traits seem to be important–a composite axis of behavioural variation, and one of three composite axes describing the colour of the margin of the dewlap. Lizards who headbob, push-up, and extend their dewlaps more during competitive interactions are more likely to win than lizards who display less. Curiously, lizards with lower UV reflectance of the dewlap margin are more likely to win than lizards with brightly UV-reflecting dewlap margins.
Of the two variables, display behaviour was more highly correlated with the probability of success than dewlap margin UV-reflectiveness. I’m curious about how the two variables are themselves related–do lizards that display more also have less bright dewlap margins? The authors propose that a dewlap’s reflectance might relate to its conspicuousness, and it would be interesting to know if different individuals are conspicuous in different ways.
Each of the studies conducted so far on how anoles convey information to each other has examined different dewlap and display variables, studied different competitive contexts, and used different measures of male quality. It therefore isn’t surprising that we seem far from reaching a consensus on what the dewlap says.
Recognize that Lizard?
I actually read this book a long time ago, I loved the series; basically the premise was that a bunch of children were given a space cube by an alien that allowed them to change into any animal for two hours. The kids would then use the abilities of these animals to thwart the various plans of a race of alien, mind-controlling parasitic slugs.The idea was original and the books were an interesting read too.
The picture on the cover is of one of the main characters morphing into a Cuban (specifically mentioned) green anole; unfortunately, I don’t remember what it was that he did with this morph.
A common concept in ecology is that predators have a strong influence on the behaviour of prey species. Anolis lizards have been used as a classic model system to investigate the effect of predator presence on the behavioural response of prey species. On small experimental islands in the Bahamas the manipulated introduction of curly-tailed lizards (Leiocephalus carinatus), a large terrestrial anole-predator, has resulted in brown anoles (Anolis sagrei) shifting higher up in the vegetation, presumably in an understandable effort to avoid being eaten (1, 2, 3). However, predator-prey interactions such as these which may shape community structure are often difficult to observe.
Here in Miami FL we have a rich and diverse, although largely non-native, lizard community. There are two species of “crown-giant” anoles, the Cuban knight anole (A. equestris) and the Jamaican giant anole (A. garmani), that could be potential predators of smaller anoles in the canopy of trees and upper half of tree trunks (although see Giery et al. 2013 for an empirical analysis that suggests this may not be the case). Additionally, there are several large, terrestrial lizards present which may be filling a similar role to curly-tails in the Bahamas.
Potential lizard predators in south Florida:
- *Red-headed agama (Agama agama)
- *Cuban knight anole (Anolis equestris)
- Jamaican giant anole (Anolis garmani)
- *Brown basilisk (Basiliscus vittatus)
- Spiny tailed iguana (Ctenosaura similis)
- Curly-tail lizard (Leiocephalus carinatus)
- Giant day gecko (Phelsuma grandis)
- Black and white tegu (Tupinambis merianae)
*Present at Fairchild Tropical Botanical Gardens
Earlier this afternoon, while taking a break from my office at Fairchild Tropical Botanical Gardens (a hot spot for any anologist visiting Miami; 1, 2, 3, 4) in a typical graduate student effort to put off work that I should be doing instead, fellow lab member Evan Rehm and I noticed some scuffling in a nearby bush. At around 2.5m, and admittedly on relatively precarious branches by this stage, sat an adult female African red-headed agama (A. agama) around 30cm from an adamantly motionless adult male Cuban brown anole (A. sagrei)! As we moved towards the bush the agama was quick to ungraciously thump itself to the floor, while the brown anole remained still. On closer inspection, it soon became apparent why both lizards were so high.
The significance of tail loss/damage in a population is still debated. The classical view argues that high proportions of tail damage indicates high predation pressure, therefore prey populations are under high predation stress (1). Alternatively, high proportions of tail damage could indicate low predator efficiency, which would suggest prey populations are experiencing low predation stress (1, 2). But the debate doesn’t stop there! Having already lost a tail, a lizard may experience either a resulting increase or decrease in predation depending on the predator species and its associated foraging tactic (1).
African red-headed agamas (A. agama) are similar morphologically to curly-tailed lizards (L. carinatus), although are taxonomically distinct (Agamidae and Leiocephalidae, respectively). Predation of anoles by agamas in Miami has not previously been officially recorded, and the impact of these large predators remains unclear. Unlike in the Bahamas, there are multiple predators in the same geographic vicinity that anoles need to be aware of. For example, at Fairchild, brown anoles (A. sagrei) could be eaten from below by agamas, eaten at intermediate levels by basilisks and eaten from above by knight anoles!
South Florida is a tough place to be an anole!
Recently, frequent Anole Annals contributor Martha Muñoz and I had the opportunity to visit Cuba as part of a licensed trip through the Harvard Museum of Natural History. During our two weeks on the island, we visited many localities and had the opportunity to photograph and observe some of Cuba’s most beautiful anoles. In the coming weeks, I’ll be spotlighting some of our favorites. All images presented are © Shea Lambert 2014.
First up: Cuba’s Western cliff anole, Anolis bartschi.