Thanks for sticking around while I did Black Birders Week planning, events and follow ups. I hope you were able to take part and check out the week. If not, we’ve archived the recordings and they all live somewhere on the internet which we’ve conveniently collected for you over on our website BlackAFinSTEM.com.
Now, for the anoles.
It’s funny how I accidentally did an anole this one is commonly mistaken for twice, but haven’t actually talked about it yet. But, Anolis cybotes is this week’s anole.
Commonly known as the large-headed/largehead anole because the males have really big heads (creative, I know), or the Hispaniolan stout anole, these lizards are native to Hispaniola and small neighbouring islands, but have been introduced to Suriname and everyone’s favourite state, Florida. Largehead anole males can have an SVL of ~65-70mm and females, ~52-60mm. Like many other stout brown patterned anoles, they’re also of the trunk-ground ecomorph and are territorial as adults.
Male largehead anoles have a dirty white dewlap with no patterning, an easy way to tell them apart from the similarly coloured A. sagrei (red-orange dewlap), and A. cristatellus (yellow and orange dewlap). If you are able to take a closer look at its head in comparison with others, you should also be able to notice the blocky shape and size it got its name for.
Anolis cybotes haa been studied with another similar sympatric anole, A. marcanoi, to see if anoles can recognise each other and other species by dewlap, which you can read here.
PS: It’s Pride Month and I am one of 23 scientists featured in the New Science Exhibit at Cal Academy; it’s also virtual so you can check it out here.
Semi-aquatic Anolis lizards have some of the most fascinating ecologies, colour patterns, and behavioural strategies in the genus (though I may be biased). Twelve of these neotropical streamside specialists are distributed across much of mainland Latin America and on the two largest islands of the Caribbean. All are rarely found more than a few meters from a stream and some have been observed to consume semi-aquatic prey (or, in the case of A. vermiculatus, even small fish and freshwater crustaceans).
Range map of all 12 semi-aquatic anole species
A riparian lifestyle is also responsible for the signature move that unites all species of semi-aquatics—escape dives! As anyone who has encountered one of these lizards in the wild can attest, semi-aquatics will readily dive underwater when approached. They can stay down for awhile too—up to 18 minutes by my count (Mexico’s A. barkeri currently holds the record). Diving anoles have attracted the attention of tropical biologists for more than half a century now (e.g., Robinson 1962; Brandon et al. 1966; Campbell 1973; González Bermúdez and Rodríguez-Schettino 1982; Birt et al. 2001; Leal et al. 2002; Henderson and Powell 2009; Muñoz et al. 2015; Herrmann 2017) and this work has begun to fill out our natural history knowledge of these enigmatic lizards. However, understandably, most work to date has focused on what these lizards are doing when they’re not in the water. And, as it turns out, there’s a lot to learn if we look below the surface…
In 2009, while studying Anolis eugenegrahami, an endangered semi-aquatic anole from Haiti, Luke Mahler and Rich Glor noticed that an individual they had just released into a clear, shallow stream proceeded to repeatedly exhale and re-inhale an air bubble as it clung to the rocky bottom. Luke and Rich had to move to their next site later that day, so weren’t able to learn more. Sadly, a follow-up field season was cancelled in the aftermath of the 2010 Haiti earthquake.
Years later, when I started my MSc thesis on aquatic anoles in at the University of Toronto, Luke shared this observation with me. When an anole does something once, another anole somewhere else usually does it convergently, so we couldn’t help but wonder whether aquatic anole species elsewhere also exhibited this apparent “rebreathing” behavior. So, when I was planning my first field season in Costa Rica, on a hunch, we purchased an oxygen microsensor, and I set out to establish whether this intriguing behaviour occurred in any other semi-aquatic anoles.
Costa Rica field team, 2017
Colombia field team, 2018
Mexico field team & friends, 2018
The aquatic anoles did not disappoint! During my Master’s, along with an amazing team of colleagues, I visited stream habitats in Costa Rica, Colombia, and Mexico, studying A. oxylophus, A. aquaticus, A. maculigula, and A. barkeri along with the non-aquatic anoles we were able to find at each site. I found that each of these species routinely performed the same behaviour that Luke and Rich had observed in A. eugenegrahami! We named this phenomenon “rebreathing” after the SCUBA apparatus. All of the semi-aquatics we observed performed rebreathing extensively during experimental submersions and are from five phylogenetically distinct lineages, showing a pattern of remarkable behavioural convergence!
As I was conducting these experiments, “rebreathing” was independently discovered in Anolis aquaticus by Lindsey Swierk (see image below, and Lindsey’s 2018 AA post). Lindsey is the world authority on Costa Rica’s diving anoles, and has reams of firsthand knowledge about their ecology and behavior. So we did the obvious thing when we found out about her observation – we invited her to join our project. We managed to deliver our oxygen sensor to Lindsey in Costa Rica via a colleague with overlapping travel plans, and she helped fill out our oxygen use data set for the Costa Rican diving anole species. In addition, Luke tested Anolis lynchi in Ecuador, and various non-aquatic species during fieldwork there and elsewhere (Dominican Republic, Jamaica) to help round out the data set.
A diving A. aquaticus performing rebreathing (Photo: Lindsey Swierk)
Speaking of non-aquatic anoles, what role do they play in this story? An interesting one, as it turns out. Rebreathing clearly seemed fascinating, but one possibility was that it was relatively ubiquitous and that all anoles would rebreathe if you submerged them. To find out, we did just that, carefully dunking aquatic and non-aquatic anoles alike in aquaria or buckets at our field sites.
What we discovered is that most non-aquatic anole species are indeed capable of basic rebreathing, but for the most part, they don’t rebreathe anything like the semi-aquatics do. If they rebreathed at all, non-aquatic species tended to do so only occasionally and irregularly (usually only one or a few re-inhalations). Since semi-aquatic anoles performed rebreathing extensively and consistently, while non-aquatics were capable of the basic components of rebreathing, but did not rebreathe regularly, we think consistent rebreathing may have evolved when natural selection found a new utility for a trait that all anoles possess—hydrophobic skin. The hydrophobicity of anoles’ scales is likely what enables the air bubble to adhere to the diving anoles’ heads (and thereby also enables re-inhalation). All anoles therefore appear to be capable of forming a thin layer (or ‘plastron’) of air along their scales during submersion, but only semi-aquatics appear to make regular use of this ability (see plot below). Hydrophobic skin evolved in anoles long before it was co-opted for rebreathing in stream-dwelling species, and likely had nothing to do with the use of aquatic habitats. In this way, the innovation of underwater rebreathing apparently owes its origins to a fortuitous ‘evolutionary accident.’
Semi-aquatic anoles rebreathed more frequently than non-aquatics (from Boccia et al. 2021)
Although we observed regular rebreathing in all aquatic anole species we studied, we discovered some interesting differences in the way they go about it. There were three main locations along the head to which diving anoles would exhale bubbles (see image below). We noted some variation in the bubble positions used by semi-aquatics, perhaps indicating that are multiple ways to achieve the same rebreathing function.
Bubble positions and use percentages for five semi-aquatic anole species (Drawing credit: Claire Manglicmot)
To determine if ‘rebreathing’ was truly involved in respiration, we used our oxygen sensor to measure the oxygen concentration of the bubbles produced by diving semi-aquatics. This is not as easy as it sounds; bubbles were frequently re-inhaled quickly and diving anoles do not take kindly to being accidentally poked in the nose with a probe. But we persevered, and found that bubble oxygen levels decreased through time, consistent with the respiration hypothesis!
Experimental submersion of an A. maculigula male in Colombia; field assistant James is holding oxygen and temperature sensors ready.
We found some evidence that oxygen decrease followed an exponential decline curve, suggesting either that anoles extract some additional oxygen from the surrounding water by rebreathing (thus slowing the rate of oxygen loss from the bubble), or that metabolic rate (and thus oxygen demand) drops over time during submersion (see figure below). We compared our results to diving insects that use a similar rebreathing apparatus while submerged and found that anole oxygen use matches up well with our expectations for their sizes, and that the metabolic rate of anoles is probably too high for them to remain underwater indefinitely using oxygen captured from the water by the rebreathing bubble (the same is true for the largest diving insects).
Plots A-E show bubble oxygen concentrations through time for five species of semi-aquatic anole. Plot F shows a sham trial (in which I mimicked the bubble movements of diving anoles with a submerged syringe; no oxygen declines were observed). Plot G shows semi-aquatics (blue) and diving insect oxygen consumption rates (black) by mass. The dotted line indicates the theoretical limit of oxygen replenishment per second that could be supported by a bubble gill structure. From Boccia et al. 2021.
The consistency with which unrelated semi-aquatic anoles rebreathed suggests that rebreathing is adaptive for semi-aquatic living; however, our data currently do not allow us to favour a particular physiological functionality for this behaviour. Our top three (not mutually exclusive) hypotheses are: 1) rebreathing allows anoles to access air trapped in their head cavities or within the plastron, which might otherwise not be incorporated into their air supply; 2) the rebreathing bubble functions as a physical gill (as has been observed in diving insects), allowing diving semi-aquatics to extract some oxygen from the surrounding water; and 3) bubble exhalation and re-inhalation allows anoles to remove excess carbon dioxide which builds up during dives. We hope to investigate these possibilities during future work!
We published this work in Current Biology (Boccia et al., Repeated evolution of underwater rebreathing in diving Anolis lizards, Current Biology (2021), https://doi.org/10.1016/j.cub.2021.04.040)
Birt RA, Powell R, Greene BD. 2001. Natural History of Anolis barkeri: A Semiaquatic Lizard from Southern México. Journal of Herpetology. 35(1):161. doi:10.2307/1566043.
Brandon RA, Altig RG, Albert EH. 1966. Anolis barkeri in Chiapas, Mexico. Herpetologica. 22(2):156–157.
Campbell HW. 1973. Ecological observations on Anolis lionotus and Anolis poecilopus (Reptilia, Sauria) in Panama. Am Mus Novit. 2516:1–29.
González Bermúdez F, Rodríguez-Schettino L. 1982. Datos etoecologicos sobre Anolis vermiculatus (Sauria: Iguanidae). Poeyana. 245:1–18.
Henderson RW, Powell R. 2009. Natural history of West Indian reptiles and amphibians. Gainesville: University Press of Florida.
Herrmann NC. 2017. Substrate availability and selectivity contribute to microhabitat specialization In two Central American semiaquatic anoles. Breviora. 555(1):1–13. doi:10.3099/MCZ33.1.
Leal M, Knox AK, Losos JB. 2002. Lack of convergence in semi-aquatic Anolis lizards. Evolution. 56(4):785–791. doi:10.1111/j.0014-3820.2002.tb01389.x.
Muñoz MM, Crandell KE, Campbell-Staton SC, Fenstermacher K, Frank HK, Van Middlesworth P, Sasa M, Losos JB, Herrel A. 2015. Multiple paths to aquatic specialisation in four species of Central American Anolis lizards. Journal of Natural History. 49(27–28):1717–1730. doi:10.1080/00222933.2015.1005714.
Robinson DC. 1962. Notes on the Lizard Anolis barkeri Schmidt. Copeia. 3:640–642.
This week we are going back up the tree to a trunk-crown anole, Anolis chlorocyanus.
The Hispaniolan green anole is endemic to the island of Hispaniola and has been introduced to Florida. The males are bright green, sometimes being mistaken for the American green anole, but dewlaps that have black. Females and juveniles are the same shade of green, but often have darker green lateral stripes.
Hispaniolan green anoles inhabit orchards and gardens, in addition to forests. They are one of the few species of anoles that have been reported to vocalise (as noted in this past post and another found here). Like many other anoles, they are capable of rapid colour change to brown, depending on temperature, mood or other factors.
This anole is also part of an eponymous series with several closely related anoles, and there has been some talk of renaming them as new research is done about their genetics.
Hi! It’s been brought to my attention that I haven’t done a small anole in a while. Today’s anole is a grass-bush anole, Anolis olssoni, also known as the Desert Grass or Monte Cristi anole.
This anole is native to Hispaniola (Haiti and the Dominican Republic). There are eightsubspecies of the Desert Grass anole found in different locations on the island.
Like other grass-bush anoles, Anolis olssoni has a slender body and a very long tail, as well as brown colouring and lateral striping. Grass-bush anoles tend to move by hopping and have long hindlimbs. For this ecomorph, the SVL ranges from 33-51 mm, with the Desert Grass anole somewhere around 39-50 mm, depending on the subspecies.
Subspecies vary from each other by colour, either being darker or paler, as well as by scale pattern. Lighter-coloured Desert Grass anole subspecies are found in xeric areas, while darker-coloured subspecies are found in more mesic areas. The dewlap of this species is a rusty orange with yellow scales.
Hello, it’s me your favourite PhD student!
If you don’t follow me on Twitter I was celebrating getting into a PhD program last week. I’m still really excited but the anoles wait for no one and I found an anole I really like so I’m here to pass this knowledge on to you.
This week’s anole is Anolis landestoyi, another chameleon-like anole, and closely related to the anoles of the chamaeleonidesclade of Cuba.
These anoles, found in the forest of the Dominican Republic, have an SVL of 122-135 mm and short tails. Similar to the chamaeleonides anoles, they have large heads, though not quite as large as the snail-eating anoles.
Photo: Miguel Landestoy
Anolis landestoyi is a mossy green in colour with spotches of brown, giving it a similar appearance to tree bark covered in the lichen or moss that are abundant in its range. Males have a pale coloured dewlap with some light blue and white stripes, while females have smaller slightly lighter coloured dewlaps. Like other chameleon-like anoles, their diet includes various species of arthropods, but no mention of snails sadly.
Hope you all are doing great. I just finished my finals and two applications to PhD programs (so far) so fingers crossed for me???
I wanna talk about another (mostly) brown-coloured anole today since I feel like there’s not enough appreciation for them.
Anolis distichus, the Bark Anole, is a trunk anole with about 16 subspecies, that ranges in colour from brown to grey to green. Their dewlaps also vary in colour and pattern with their population. Males and females look the same, but in this species only males have a dewlap.
Found in Haiti, Dominican Republic, central Bahamas and, of course, Florida, these anoles can be found in range of habitats. Bark anoles are kind of on the small side at about 127mm in length.
My favourite thing about the Bark Anole is the patterning that gives it its name. The striping mimics the roughness and shapes found in tree bark, making it kind of invisible sometimes. Quite an example of perfect camouflage.
There’s been a lot of research on the anole, particularly looking into its subspecies and if any of them are their own species. Currently, this doesn’t seem to be the case quite yet.
Maybe. There’s a lot of conversation about just how muchvariation there is or isn’t with this species.
We all know that the anoles of the Caribbean partition the habitat based on structural environment and microclimate, leading to patterns of correlated morphology and habitat use within these ecomorphs. While we know a substantial amount about the morphological aspect of the ecomorph concept, many questions remain concerning the patterns of physiological trait evolution across Caribbean anoles and how this relates to habitat use and ecomorphology.
Brooke Bodensteiner, a PhD student in the Muñoz lab at Virginia Tech, is digging into this topic for her doctoral research. In her presentation at Evolution 2019, Brooke told us about two key questions she is attempting to address in her research: (1) Do ecomorphs overlap in physiological trait space or do they neatly differentiate into distinct groups as they do with morphology? and (2) Do thermal traits evolutionarily respond to the same microhabitat predictors?
Brooke measured thermal physiology of anoles in the Dominican Republic, including Anolis cybotes, shown here.
Brooke is investigating these questions in Hispaniolan anoles and has so far sampled 28 of the 41 species found in the Dominican Republic with representatives from all 6 ecomorphs! The Hispaniolan anoles are particularly good for this research topic since there are representatives of each ecomorph in very diverse habitats islandwide, providing many opportunities for physiological diversification. Building on a large dataset of morphological traits, Brooke collected thermal physiology data from all 28 of these species including critical thermal minimum and maximum and preferred temperature, to try to understand the patterns of physiological diversification and how they are correlated with morphological diversification.
Brooke’s results were fascinating, but more complex and nuanced than expected. Consequently, we will only tell you that her findings are intriguing and will give us a lot to ponder regarding patterns of correlated trait evolution and environmental factors driving physiological evolution. I look forward to seeing the finalized results published soon!
Climate change on earth is accelerating. These changes will have important impacts on all species, but some types of organisms are predicted to be affected more strongly than others. One such group is ectotherms which use the temperatures available in surrounding habitats to regulate their body temperatures. Another such group is mountaintop endemics. These species are restricted to one or several mountain peaks by climate and/or competition with other organisms. As such, they cannot easily disperse to other areas if climate makes their current habitat unsuitable!
Mountaintop endemic species may be particularly vulnerable to climate change (Chand Alli, CC BY SA).
Hispaniola contains several high elevation areas home to mountaintop endemic species, including anoles (NASA).
Many studies use correlative modeling approaches (often termed ecological niche models [ENMs] or species distribution models [SDMs]) to assess a species’ current distribution and predict its future distribution by projecting it into simulated future climate scenarios. This approach has some advantages including ease of implementation across many species. However, it has at least two potential drawbacks: the environmental data used in building such models are often measured at a fairly coarse scale that does not represent how many organisms use their environments, and the models do not explicitly include biological processes such as physiology and behavior.
Anolis armouri in a montane rock meadow (Reptile Database).
Vincent Farallo, a post doc at Virginia Tech, and his advisor, Martha Muñoz (both moving to Yale in a few weeks!), investigated whether incorporating physiology and behavior into modelling might affect predictions of climate change impacts on two mountaintop endemic anoles of Hispaniola, Anolis armouri and Anolis shrevei. Correlative SDMs (via BioMod2) predicted both species would lose much or all of their suitable habitat under climate change, perhaps leading to extinction. However, when Vincent constructed mechanistic niche models (via NicheMapR) that included knowledge about the thermal physiology and habitat use behavior of these species to predict activity time, they showed that habitat would increase in suitability under climate change, the opposite result! Interestingly, these models also predicted increased suitability for a widespread anole, A. cybotes. This result suggests that while climatic changes may not be a direct threat to these mountaintop anoles, increased competition with another anole, an indirect impact of climate change, may be.
Activity time of Anolis shrevei is predicted to increase across its range in Hispaniola with climate change (Farallo and Munoz).
As a whole, Vincent and Martha’s work shows that incorporating more mechanistic knowledge into models, including physiology and behavior, may be critical to predicting the impacts of climate change on organisms and making sound conservation decisions.
Dewlap and genetic differences between Anolis distichus and A. brevirostris at sites where they co-occur on Hispaniola.
Here at Anole Annals, we’re all familiar with the replicated evolution of different anole ecomorph types in the Greater Antilles. However, divergence into these different ecomorph classes is not enough to explain how the group became so speciose on these islands. Additional factors must therefore have promoted speciation throughout the history of the group.
One potential factor is the flashy anole dewlap. Dewlap diversification across anoles has led to the remarkable array of dewlap color, pattern and size we see today. If dewlap differences did indeed drive speciation in anoles, or are involved with the maintenance of species boundaries, we might expect that as differences in dewlap color and pattern increases between species, genetic differentiation will also increase through fewer hybridization events.
In our study that just came out in the Journal of Herpetology, Rich Glor, Anthony Geneva, Sabina Noll and I set out to test this using two widespread species from the Anolis distichus species complex, A. distichus and A. brevirostris. These two species co-occur in many locations on Hispaniola and, while they often differ in dewlap color where they do co-occur (yellow with an orange patch vs. all pale yellow), in other areas, they co-occur with similarly pale dewlaps. Using mitochondrial DNA, microsatellite and AFLP data, we investigated patterns of genetic differentiation at four sites: two where the species differ in dewlap color, one where the species share the same dewlap color, and another where pale dewlapped A. brevirostris co-occurs with two A. distichus subspecies (one with a similarly pale dewlap and the other with an orange dewlap).
In general, we found that A. distichus and A. brevirostris looked like “good species,” with strong genetic differentiation and little evidence of hybridization, even at a site where they share the same dewlap color. This suggests that dewlap color differences are not associated with genetic differentiation in a manner one might expect if dewlaps were involved in the speciation process or in maintaining species boundaries. However, at the site where A. brevirostris co-occurs with two A. distichus subspecies with both similar and dissimilar dewlap colors, we found some evidence of hybridization and the species were not as highly genetically differentiated. This discrepancy suggests that site-specific factors could be influencing the dewlap’s role in speciation or maintaining species boundaries. For example, as Leo Fleishman’s and Manuel Leal’s work has shown (e.g. 1, 2, 3), the dewlap’s effectiveness as a signal is dependent on the light environment. Further understanding about the environmental differences among our study sites, how species utilize the available light microhabitats within each site, and how the dewlap looks to anoles at each site could provide more insight into our findings.
On the other hand, perhaps we need to be looking beyond the dewlap and focusing instead on whole signaling displays. Anole behavioral displays can also be strikingly different among species (e.g. 1) and may instead be the key to understanding species diversification in Greater Antillean anoles.
![Anolis landestoyi (2 of 2) [image] | EurekAlert! Science News](https://i0.wp.com/www.eurekalert.org/multimedia/pub/web/117940_web.jpg?w=629&ssl=1)
