#DidYouAnole – Anolis stratulus

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On July 15, 2021

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Photo: Chase G Mayers, iNaturalist

On the island of Puerto Rico this trunk-crown anole is locally called lagartijo manchando, but is also known as: the Puerto Rican spotted anole, spotted anole, banded anole, saddled anole, salmon lizard, barred anole, St. Thomas anole and chameleon.

They are possibly the most abundant anole in Puerto Rico but can also be found on the British Virgin Islands and US Virgin Islands. They can be spotted in a number of different habitats including urban environments, though they occupy buildings at a lower frequency than Anolis cristatellus. In Puerto Rico they can often be found in Tabonuco trees.


Photo: Steve Maldonado Silvestrini, iNaturalist

Spotted anoles are active foragers with an apparent preference for ants.

Males have an SVL of 40-44mm, and females an average of 46mm. They have large orange dewlaps that fade into yellow closer to the margins but female dewlaps are smaller and grey with orange near the throat. Spotted anoles are typically brown or pale gray with pale and dark coloured spots along its body. Unlike some of the anoles found in Puerto Rico, they don’t permanent crests but have a nuchal crest that they raise during antagonistic interactions and otherwise ridges down their backs. There is also a patch behind their eyes that darkens during these interactions as well, much like in Green anoles.


Photo: larsonek, iNaturalist

More Astonishing Parallels between Draco and Anolis

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On July 9, 2021

In New Research

Despite being on opposite sides of the world and separated by millions of years of evolution, Draco and Anolis lizards have converged on many common adaptive solutions.

It has long been suspected that the Draco lizards of Southeast Asia were ecological analogues of the Anolis lizards in the Caribbean. But it has only been recently that we’ve started to truly figure out just how similar these two groups actually are. Especially exciting has been the discovery of how lizards in both groups have converged on remarkably similar adaptations: natural selection appears to repeat itself, time and time again.

The classic textbook scenario in anoles is adaptive convergence in ecomorphology, which reflects where lizards tend to hang out in the environment. This is particularly obvious  in the adaptation of Anolis limb morphology to different types of perches. I’m not sure we can say whether Draco exhibit the same ecomorphs as Caribbean anoles just yet, but Draco do exhibit the same adaptive changes in limb morphology as the anoles of the Caribbean.

Then there’s the obvious case of the dewlap, which has evolved separately in both Anolis and Draco as a key component of their territorial and courtship displays.

Most Anolis and Draco lizards also rely heavily on elaborate sequences of head-bobs in these displays as well.

This in itself isn’t unusual. Many lizards head-bob and push-up over territory and mates. Up to now, however, Caribbean Anolis lizards were the only ones known to tailor their display movements to ensure detection. For any visually communicating animal, visual “noise” from windblown vegetation and poor ambient light make it difficult to see visual signals. Anolis lizards were exceptional because they actively monitored environmental conditions and exaggerated their body movements when it was visually noisy (e.g., on windy days) or extended the duration of their displays when light levels diminished (e.g., on cloudy days or deep inside a forest).

There are a countless ways lizards might produce a conspicuous signal. Many Australian and Chinese lizards add arm-waves or elaborate tail-flicks or simply rely on colourful ornamentation that stands out well in the environment. Many North American lizards rely on performing lots of head-bobs or positioning themselves to accentuate a colourful badge on their throat or sides. But anoles seemed unique in both the complexity of their visual displays and their capacity to modify their behaviour to the prevailing conditions in the environment.

But after years of studying Anolis on Jamaica and Puerto Rico, and then even more years studying Draco in the Philippines, Borneo and Malaysia, we have now discovered more astonishing parallels between the two lizard groups that extends beyond just morphology.

Southeast Asian Draco lizards exhibit virtually identical strategies for coping with visually difficult environments as do the Caribbean Anolis lizards. Draco use the dewlap in the same way as the anoles, and change the speed (or exaggeration of movements) and the duration of displays in the same way as anoles, and this capacity to tailor displays to the conditions of the environment has also tended to precede what seems to have been adaptive divergences in display behaviour among species.

To discover all this, we had to study many different species of Draco and Anolis (11 and 12 species respectively), including hundreds and hundreds of lizards (727 to be precise), and then conduct thousands and thousands of hours of video analysis (13,310 hours – !!).

To be perfectly honest, what I was hoping to document from all this work was how differences in evolutionary history between the Anolis and Draco had shaped the trajectory of display evolution. Sure, Draco had evolved a dewlap like Anolis, but how that dewlap has been morphologically constructed was quite different between the two groups. I had become quite interested in these so-called “many-to-one, form-to-function” outcomes in evolution, and I was aiming to show something similar for display behaviour.

To be clear, there were differences in how Anolis and Draco lizards responded to environmental conditions, and how plastic changes in behaviour have contributed to display differentiation among species. In fact, the head-bob component of the territorial display has been entirely lost in some Draco species.

But the similarities were stunning and outweighed the differences by a large margin. Even the loss of headbobs in some Draco have intriguing similarities to how some Anolis species have shifted their display effort to the dewlap, which seems to be a more energetically efficient means of producing a conspicuous, complex visual display, than the more tiresome head-bob and push-up movements.

We have also confirmed experimentally in anoles that the manner in which Anolis lizards tailor their displays does actually improve display detection in visually difficult environments. This took a lot of work in itself and required the development of a robotic playback system, but this is now ancient history.

But to complete the loop, a similar type of playback experiment needed confirm the same adaptive benefit in Draco.

Some years ago we had conducted a lengthy field experiment using robot playbacks that were designed to test the response of Draco lizards to different coloured dewlaps. That experiment showed little effect of dewlap colour on detection, but a tangible effect that once lizards saw the dewlap, they used it to evaluate the species identity of the signaller.

I was in the lab one day looking at these old Draco robots to get some inspiration for designing a new system for some other crazy idea I had. As I was fiddling with the mechanism, I noticed that the robots weren’t exactly the same, with the lever controlling the dewlap of one being slightly longer than another. This meant the display probably differed in speed between the robots. These things happen and I didn’t think much of it at the time. The treatments used in the field experiment were systematically inter-changed across the robots to make sure this type of thing didn’t cause any problems.

Later, however, it occurred to me that perhaps this might offer a serendipitous opportunity to confirm the adaptive benefit of at least one of the key convergences exhibited by Draco lizards. I downloaded the data from the original study from its dryad repository, extracted the response times of lizards to the two robots that differed in dewlap speed, and sure enough, detection times were much quicker to the robot with the faster dewlap display.

The top panel (a) shows the differences in dewlap speed between the two robots, while the bottom panel (b) shows the detection time of free living Draco melanopogon.

If you’re interested in a short video introduction to this work, or want to know more about how these findings relate to our general understanding of adaptation and animal communication, you’ll find some answers in this 5 minute video below.

#DidYouAnole – Anolis sabanus

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On July 8, 2021

In All Posts


Photo: Delano Lewis, iNaturalist

This week’s anole, Anolis sabanus, can only be spotted on the island of Saba (Dutch W.I.).

Also called the Saban anole, this tan to pale grey coloured species is sexually dimorphic with males being covered with black spots/patches at an SVL of 29-72mm and females having a dorsal stripe and an SVL of 23-25mm. Their dewlaps are green or orange tinted.


Photo: Mark Yokoyama

In 2016, there was an introduction of the anole on the neighbouring island of Sint Eustatius. They belong to the bimaculatus series of anoles which includes other island endemics like Anolis oculatus (from my home island of Dominica).

Gina Zwicky, New Orleans based herper, is currently working on a study to see if there is a link between parasite pressure and the rise of immunity in generations of this anole, examining if evidence can be found of fluctuating selection in a natural population. Anoles are incredibly useful for research with their genomes being readily available for reference, how quickly they adapt and other factors. Island endemics especially are great research subjects due to their isolation which helps to eliminate certain other variables.


Photo: iNaturalist

#DidYouAnole – Anolis aeneus

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On July 1, 2021

In All Posts


Photo: Mikel2500, iNaturalist

Happy Thursday!

Today’s anole is the Bronze anole, Anolis aeneus! The Bronze anole can be found on most of the Grenadines (the small islands between St. Vincent and Grenada) and Grenada itself, and has been introduced to Trinidad & Tobago and Guyana.

Bronze anoles can be found in forests and some urban environments, and is one of many anole species that also feed on plant matter (Simmons et al., 2005), like nectar and seeds. Males have an SVL of 77mm while females are 55mm.


Photo: Mark Hulme, iNaturalist

Though called the Bronze anole, not all individuals are brown/bronze; some may be greyish brown or olive and their mottled pattern may be light or dark. The dewlap of the Bronze anole is pale white or green and spots of orange or yellow may be near the front edge. They spend a lot of time in a ‘survey posture’ sitting on tree trunks surveying the habitat for prey items that may come along.

Hybridisation between A. aeneus and A. trinitatis (St. Vincent bush anole) has been found to occur, with the possibility of fertile offspring (Losos, 2009).


Photo: Mike G Rutherford, iNaturalist

#DidYouAnole – Anolis cybotes

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On June 24, 2021

In All Posts


Photo: GotCritters, iNaturalist

Hello!

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.


Photo: Christian Nunes, iNaturalist

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.


Photo: GotCritters, iNaturalist

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.

Ecomorphology of La Selva Anoles

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On June 18, 2021

In All Posts, Natural History Observations, New Research, Species Accounts

Ever since the seminal papers by Williams and Rand [1,2], the Anolis radiation across the West Indies has increasingly established itself as an alluring example of ecomorphological convergence. Considering an Anolis community on one island, sympatric species have undergone niche partitioning, whereby each species has evolved particular behavioral, morphological, and ecological traits well-adapted for the microhabitat it occupies. Pop over to another island, and voilà, similar sets of ecomorphs can be found— their resemblance so striking and uncanny.

But the Anolis story isn’t clean cut. Studies of mainland anoles have yielded equivocal findings for whether they also conform to the beautiful patterns observed in the Caribbean. Much baseline data on mainland Anolis communities are needed to determine the extent to which convergence occurs and what factors drive differences in community structure. To partly address this gap, Jonathan Losos, Anthony Herrel, Ambika Kamath, and I recently published a paper describing the ecological morphology of anoles in a lowland tropical rainforest in Costa Rica, at La Selva Biological Station.

Accumulating field observations from four field seasons ranging from 2005 to 2017, we draw from over 1000 observations to characterize the habitat use of eight Anolis species that occur at La Selva. These species include Anolis humilis, Anolis limifrons, Anolis lemurinus, Anolis oxylophus, Anolis capito, Anolis carpenteri, Anolis biporcatus, and Anolis pentaprion, and we opted to devote a brief section to the co-occurring Polychrus gutturosus. Our results revealed overlapping niches and substantial variability in habitat use across many species. Furthermore, the morphologies of A. humilis and A. limifrons were at odds with microhabitat use following the predictions of Caribbean anole ecomorphology. Among the two most abundant species, relative hindlimb length was greater for the more arboreal A. limifrons, whereas it was shorter for the more terrestrial A. humilis.

If mainland and island anoles exhibit divergent ecomorphological patterns, this begs the question of how selective pressures differ between mainland and island habitats to drive these differences. Andrews [3] proposed that predation may more strongly influence Anolis diversification on the mainland, because in comparison to islands, predators are far more abundant, anole population densities are lower, and arthropod prey is plentiful. In contrast, Caribbean anoles are thought to be food limited and there may be stronger selection for niche partitioning. Through examining variation in species’ habitat use relative to the abundance of other co-occurring species at La Selva, our data suggests a low level of interspecific competition for this mainland community, corroborating the hypotheses Andrews set forth.

In recent years, the study of mainland anoles has received more attention. We are in great need of ecological, morphological, and life history trait data for Anolis communities throughout Central and South America to further our understanding of the evolutionary trajectories of mainland and island anoles. So, anole biologists, you can throw out your boats and steer clear of the oceanic divide!

 

[1] Rand, A. S., and E. E. Williams. 1969. The anoles of La Palma: aspects of their ecological relationships. Breviora 327:1–17.

[2] Williams, E. E. 1972. The origin of faunas. Evolution of lizard congeners in a complex island fauna: a trial analysis. Evolutionary Biology 6: 47–89.

[3] Andrews, R. M. 1979. Evolution of life histories: a comparison of Anolis lizards from matched island and mainland habitats. Breviora 454: 1–51.

Dirt Determines Developmental Directions: Natural Nest Substrates Influence Anole Embryo Development

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On June 10, 2021

In New Research

Brown anole eggs in the field. Photo by Jenna Pruett.

Most oviparous reptiles (excluding birds) bury their eggs in the ground. Usually, after laying, females abandon the eggs and provide no parental care thereafter. As such, non-avian reptiles (henceforth “reptiles”) have often served as model organisms to understand how the environment influences embryo development. Environmental factors of interest are usually temperature and moisture. Indeed, nest temperature can have large effects on development. For example, warm incubation temperatures often result in hatchlings that can run relatively fast while cool temperatures result in hatchlings that run slow. Moisture is also important during development since relatively wet incubation conditions improve the conversion of yolk to body mass resulting in larger hatchlings compared to dry conditions. This process by which the environment has lasting effects on development is known as developmental plasticity. Despite decades of research concerning developmental plasticity in reptiles, there are still many aspects of natural nest environments that are understudied.

One example of such an understudied environmental factor is the type of substrate (i.e. soil) in which females bury eggs. Although many field studies demonstrate that females lay eggs in a diversity of substrates, very few studies have considered exactly how these different substrates might influence development. These few existing studies have focused on turtles. For example, Mitchell and Janzen (2019) buried turtle eggs in three types of substrates in the field: loam, sand, and gravel. Despite all nests experiencing the same prevailing weather conditions, important aspects of the nest environment like moisture available to eggs and temperature differed among the substrates. This resulted in important differences among the hatchling turtles. Indeed, because this species exhibits temperature-dependent sex determination (i.e. the egg temperature determines if hatchlings are male or female), the sex ratios of the hatchlings differed according to the type of substrate in which the eggs were buried.

No study has rigorously considered how substrate types influence development of squamates (lizards and snakes). Therefore, my research associates and I decided to conduct a lab experiment using our good friend the brown anole (Anolis sagrei). This study was recently published in the journal Integrative Zoology (Hall et al. 2021). At our field site in Florida, female anoles lay eggs in two main types of substrates: sand/crushed sea shells and organic debris (Figure 1). We collected male and female lizards from one of our study islands and brought them back to our lab at Auburn University. We also collected a few buckets of the two substrates in which females commonly nest. We collected eggs from the breeding colony and incubated them in each substrate at 4 different moisture concentrations. The goal was to understand if these two substrates had any important effects on development. Moreover, using different moisture concentrations in each substrate allowed us to see if the two substrates might have similar effects on development given particular moisture concentrations.

Figure 1. Representative photos of (a) a female brown anole (Anolis sagrei), (b) aerial view of the substrate collection island, (c) ground view of substrate collection island, (d) organic substrate, and (e) sand/shell substrate. In panel (b), the area inside the red circle is the portion of the island that is most densely populated with lizards. The area within the black line is an example of open canopy habitat where substrate is primarily sand and crushed shell. The area inside the white line is an example of closed canopy habitat with dark, organic substrate. Panel (c) shows the ground view of the same open and closed canopy sites outlined in panel (b).

We measured a variety of traits including water uptake by eggs (eggs absorb water during development), developmental rates of embryos, egg survival, hatchling body size, and hatchling performance (i.e. endurance). The amount of moisture available to eggs provided expected results: greater moisture content resulted in greater water absorption by eggs and larger hatchling body size. We found that the two substrates had little effect on most traits; however, egg survival and developmental rate differed between the substrates: eggs were more likely to die and developed more slowly in the organic substrate than in the sand/crushed shell. Although statistically significant, these effects were not large. The difference in egg survival was about 6% and the difference in developmental rates between the substrates resulted in a one-day difference in the incubation period (i.e. the number of days it takes for the egg to hatch).

It isn’t completely obvious why we observed these differences in egg survival and physiology (i.e. developmental rate). We think the organic substrate might support a greater load of microbes (i.e. fungal spores and bacteria) than the sand/shell substrate. Thus, in the organic substrate, eggs may compete with microorganisms for resources like oxygen during development. Additionally, when exposed to an abundance of microorganisms, eggs may expend energy to fight infection which could slow development and reduce survival. Regardless, other studies have also found that developmental rate can be influenced by the type of incubation substrate, but no mechanism has yet been rigorously tested. Thus, there is still much to learn about how reptile embryos interact with natural nest environments!

In conclusion, the type of incubation substrate can have important effects on embryo physiology and survival, but only a few studies have explored these relationships. What would be most helpful now is a series of studies that consider how microbial communities differ among substrates and how these communities might interact with eggs. Perhaps this work will rest on the shoulders of Kaitlyn Murphy who is currently using microbiology techniques to understand effects of the microbiome on embryo development using brown anoles. If so, the future of this unexplored area of research is in capable hands.

You can read the full article here: http://doi.org/10.1111/1749-4877.12553

Hall, J. M., Miracle, J., Scruggs, C. D., & Warner, D. A. (2021). Natural nest substrates influence squamate embryo physiology but have little effect on hatchling phenotypes. Integrative Zoology.

Mitchell, T. S., & Janzen, F. J. (2019). Substrate influences turtle nest temperature, incubation period, and offspring sex ratio in the field. Herpetologica, 75(1), 57-62.

Robot Lizard Army versus Deadly Predators

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On June 9, 2021

In New Research, Notes from the Field, Research Methods

Over the years, there has been a lot of discussion on Anole Annals about the large, conspicuous dewlap. And rightly so because it is arguably the most evocative feature of the anoles. Much of this discussion has focussed on its function, such as its role in species recognition, mate choice, and territorial communication. But is there a cost to having such an audacious visual signal?

We needn’t isolate this question to just Anolis lizards. All socially communicating animals need to produce a signal that will be obvious to conspecifics. There’s little point producing a mating or aggressive signal if females or rivals never detect it. But there is a cost to being conspicuous and it can be a matter of life and death: the unintended attraction of predators.

Generally, the assumption has been that animals just incur the potential risk of predation for the sake of successful communication. But just how risky is it? The dewlap is often large and brightly coloured, but when it’s not being used in display, you’d never know anoles even had one.

There are also at least two other independent origins of the dewlap, including in the gliding lizards of Southeast Asia, the Draco. In these lizards, the dewlap is again large and often conspicuously coloured.

For both Anolis and Draco, one of the best ways to find lizards in the wild is by the quick flash of colour as males rapidly extend and retract the dewlap during their territorial displays. In fact, it is often the only way to find Draco, which are camouflaged and extremely difficult to spot, even when you happen to be staring right at them.

I had this crazy idea a few of years ago… Would it be possible to build an army of robotic Draco lizards with plasticine bodies that could retain impressions of predator attacks and measure the risk of predation from performing a conspicuous dewlap display?

It really was a ridiculous thought, but my long-time collaborator Indraneil Das was game.

And it worked, with the results just published.


Robotic lizards compared to the real thing in (a) morphology and (b) behaviour (robots were modelled on Draco sumatranus from Borneo).

It was an awful experiment to do. Building the robot army turned out to be the easy bit. To be clear, it took months of development and manufacture, all of which I did in my garage (long story). It then took years to run the experiment, with multiple replications across two continents because the data was puzzling. There were bushfires, floods, battles with swarming wasps and kamikaze leafcutter ants, chipped teeth, falls from ladders, bogged car rentals, hammered thumbs, and in the end I only just managed to get it finished before the world turned side-ways in 2020.


Left: fresh-faced and optimistic in June 2018; Right: brave-faced but really a little shellshocked with the retrieval of robot 2,120 in February 2020 (NB: batteries have a habit of failing and parts started to corrode so only 1,566 robots were fully functional in the experiment).

It turns out that prey that can produce a signal intermittently — effectively turning their conspicuous display on and off at strategic moments, like the dewlap — can drastically reduce their risk of predation. In fact, attack rates by predators on dewlapping robotic lizards were no different to robots that remained unmoving and cryptic in the environment. Which means there doesn’t really seem to be a large cost from increased predation for animals that perform bouts of conspicuous behaviour.

But this wasn’t the biggest surprise.

The experiment included robotic lizards that kept the large, conspicuously coloured dewlap permanently extended so it was always visible. Think of peacocks with their massive tail trains or other animals that are spectacularly ornamented. These features are always visible and are not signals that can be turned on and off. My assumption was that these robotic lizards would be the hardest hit by predators.

This wasn’t the case at all. Predators actually avoided these robotic prey and to such an extent that the probability of attack was lower than the robotic lizards that remained cryptic and didn’t perform any conspicuous behaviour.


Photo montage of predator attacks left in the plasticine body of the robotic lizards

At first, I found this to be confusing and replicated the experiment over and over again. I even called in my partner Katrina Blazek who is a biostatistician to blind the data and independently perform the analyses (Katrina is also a skilled tailor and made all the robot dewlaps). I also dragged in my colleague Tom White who is an expert on animal colour discrimination to confirm that the dewlap really was as conspicuous to predators as I thought it was.

The data was robust.

This type of predator phobia actually helps explain the evolution of a completely different type of animal signal in nature: aposematic signals or warning signals that some prey evolve to explicitly advertise their location to predators to warn them against attack, usually because they’re toxic. Conspicuous poison dart frogs are an obvious example, so are ladybirds (or ladybugs).

The paradox is how these warning signals could evolve in the first place given the first individuals that tried to advertise their warning would be quickly eaten by predators that had no idea the signal was meant to advertise unprofitably until after the attack.

One of the key hypotheses that has been proposed to resolve this evolutionary paradox is that predators are highly conservative in the types of prey they go for. That is, they tend to avoid prey that look unusual in some way, even if those prey are more easily detected.

This is exactly what happened in this experiment. The robotic lizard with the permanently extended dewlap was ‘weird’ and so predators instead targeted the robotic lizards that either displayed intermittently or remained cryptic, both of which were more typical of their familiar prey.

The take home message is:

Follow your ridiculous idea and call on your friends to help.

(But don’t hold metal tools between your teeth. Your dentist will be very annoyed with you.)

A Newly Found Anole Is Not Necessarily Good News: the Brown Anole Is a New Invader in Israel

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On June 6, 2021

In All Posts

A brown anole in its unnatural habitat; Rishon LeZion, Israel. Photo: Aviad Bar

Shai Meiri, School of Zoology & the Steinhart Museum of Natural History, Tel Aviv University
uncshai@tauex.tau.ac.il

In late April 2021, someone posted a facebook image of a lizard seen in a residence garden in Rishon LeZion, a satellite city of Tel-Aviv, Israel (approximately 31.9611N, 34.7889E). Aviad Bar, one of the best herpetologists in Israel, identified it as a brown anole (Anolis sagrei Duméril & Bibron, 1837) and went there to investigate. He found around ten lizards in that garden, and managed to catch two of them. The preliminary identification was verified, and the lizards were later deposited in the national collections at the Steinhardt Museum of Natural History, Tel Aviv University, after the Israeli Nature and Parks Authority (INPA; the governmental body in charge of protecting nature in Israel) were consulted.

Anolis sagrei is potentially very bad news. It is one of the best models for the study of evolution in nature over short time scales across the animal kingdom (a more or less random sample of works includes: Losos et al. 2004, Schoener et al. 2005, Calsbeek and Cox 2010, Losos and Pringle 2011, Stuart et al. 2014, Kamath et al. 2020, Stroud et al. 2020, Donihue et al. 2021). But it is also one of the worst reptile invaders worldwide, alongside flowerpot snakes (Indotyphlops braminus), the mourning gecko (Lepidodactylus lugubris) red-eared sliders (Trachemys scripta – we have those in Israel now too) and some Hemidactylus geckos (e.g., H. turcicus, which we may have helped to provide; H. frenatus). To date Anolis sagrei has invaded several states in continental USA (e.g., Florida, Louisiana, Texas), as well as Grand Cayman Island, Bermuda, Jamaica, Grenada, St. Vincent, the Canary Islands, multiple areas in Mexico, Belize, Honduras, Costa Rica, Panama, Ecuador, Hawaii, Taiwan, and Singapore (Sexton and Brown 1977, Kraus 2009, Norval et al. 2012, Amador et al. 2017, Capinha et al. 2017, Stroud et al. 2017, Solis et al. 2017, Batista et al. 2019).

A brown anole caught in Rishon LeZion. Photo: Aviad Bar.

Furthermore, Anolis sagrei is known to compete with native anoles, mainly Anolis carolinensis a system very frequently studied (reviewed in Kraus 2009, and see e.g., Echternacht 1999, Losos and Spiller 1999, Gerber and Echternacht 2000, Stuart et al. 2014, Kamath et al. 2020). Effects on other anoles were also suggested (Losos et al. 1993 for A. conspersus; Batista et al. 2019 for Anolis gaigei), and competition with other lizards has been hypothesized (e.g., Stroud et al. 2017, Batista et al. 2019). Thus, a new record of A. sagrei from outside its native range is no cause for a celebration.
How did A. sagrei reach Israel? One hypothesis, raised by INPA, is that eggs have been transported accidentally in shipments, likely from the USA. We know A. sagrei eggs remain viable for weeks, and can even withstand some exposure to sea water (Hsu et al. 2021). There is a plant nursery not far from the place where A. sagrei was found in Israel, and reptiles have often been accidentally transported with plant shipments (e.g., the flowerpot snake; see e.g., Perry et al. 2006, Losos 2013, Auguste et al. 2018). Indeed, a shipment of wood from Italy arriving in Israel early in 2019 contained live Podarcis siculus (specimens were transferred to the Steinhardt Museum of Natural History, and I identified them there). The USA is the #1 exporter of goods to Israel and considering A. sagrei is widespread in the US, it is a reasonable assumption.

A more plausible explanation soon emerged, however. Anolis sagrei has been in the pet trade in Israel for some time. Some third-party reports to Aviad Bar suggested that a private reptile enthusiast living in Rishon LeZion has been very successful in breeding Anolis sagrei and has simply been releasing juveniles or hatchlings into his back garden. Apparently, this has been going on for at least two and potentially 4-5 years. Thus, the source of the invasion seems to have been intentional (and illegal) introduction of individuals to nature.

The INPA asked me to write a report on potential threats posed by the brown anole and its chances of establishment and spread (Meiri 2021), then held a consultation, and commissioned Aviad Bar to survey the anole population in Rishon LeZion, and adjacent natural areas. Additionally, other Israeli herpetologists have tried to find the species around the area where it was first reported. The survey encountered some unexpected difficulties. For one, the recent horrible and useless spat of fighting between Israel and Hamas, which could and should have been avoided by both sides, caused unnecessary suffering on both, and seemed to have served only the extremely short-term purposes of “leaders” of both sides. Lizards had nothing to do with this apparently. The fighting forced the surveyors to stop the survey multiple times to take cover in shelters of complete strangers from incoming rockets. Luckily, none of them was hurt. Many people welcomed the surveyors into their garden and allowed them to look for and collect lizards. The survey (Bar 2021) was recently submitted to the INPA.

Anoles have been found in five streets in Rishon LeZion, with a maximum linear extent of ~500 m. Lizards have been found active by day on walls, fences, vegetation and on the ground, and to sleep on branches at night – typical anole behavior. Worryingly, anoles of all sizes, from adults >60 mm SVL to small hatchling-sized individuals, were found throughout the study area, strongly suggesting the lizards breed in Israel. Anolis sagrei breeds extremely fast, especially in regions where it is invasive where it matures early and reduces its already incredibly short inter-laying interval (e.g., Jensen et al. 2008, Fetters and Mcglothlin 2017). Basically, one gets the impression (or at least I do) that introduced Anolis sagrei lay eggs (almost) as fast as domestic chickens. It seems to further be helped by light pollution – growing faster and reproducing earlier where artificial lights are available at night (Thawley and Kolbe 2020) – like they are in Rishon LeZion.

Anoles were also highly abundant. Aviad (Bar 2021) found 101 anoles during his survey, and Akiva Topper and Oren Kolodny have found 28 in a single night. For comparison, the second most abundant reptile found during Aviad’s survey was the common chameleon, Chamaeleo chamaeleon – with 15 specimens. The third most abundant was the commensal (and in Israel, native) house gecko, Hemidactylus turcicus (10 animals). In fact, only 41 reptiles other than A. sagrei were found in the survey, of all species (including those identified only from tracks!). Thus in terms of abundance, A. sagrei seems to outclass all other reptiles put together by a factor of at least 2.5-to-1. That this species can be extremely abundant in places it has invaded is well known (e.g., Campbell and Echternacht 2003).

While A. sagrei has invaded many places the world over, it seems to have been confined to tropical or subtropical countries (and the subtropical parts of the USA), and this is the first report of it inhabiting higher latitudes and non-tropical climates (except perhaps some potential places in the USA). One hope expressed early was that the relatively cool Mediterranean winters prevailing in central Israel will prove detrimental for anoles. Yet, like it probably does in some cities in the USA, A. sagrei seem not to mind what goes for winters near the Mediterranean coastlines of Israel. A combination of the climatic effects of the warm puddle that is the eastern Mediterranean Sea and warm microhabitats likely found in urban residential gardens seem to allow it to easily survive the winter. Watering of said gardens likely allows it to easily survive the arid climate of the long Israeli summers (where very little rain, if any, falls in April or October, and virtually none in between). Thus, urban areas seem to present for the anoles the kind of climate and microhabitats it thrives in in its native and introduced range.

Could it spread outside of the cities? As far as we know following Aviad’s survey (Bar 2021), no anoles were found in natural areas bordering its current urban distribution. The little water available there for most of the year may preclude its establishment. But it is highly likely that, if accidentally transported, it could easily establish in habitats where abundant water is available year-round. Such as streams and pools, artificial and natural.

How much of a threat is posed by Anolis sagrei to Israeli nature is less certain. As far as I know few have tried to estimate its effect on arthropod and other prey-species communities (but see Losos 2011,2020). I certainly cannot guess it. Actual reports of Anolis sagrei impacting other vertebrate taxa seem to be confined to its effect on congenerics (even Stroud et al., 2017, only mentions potential impacts), of which Israel has none. But a super-fecund, and highly abundant, species such as the brown anole could potentially compete with other small terrestrial and arboreal lizards (and juveniles of larger species), of which the Israeli coastal plain has many (Bar et al. 2021). I can easily envision it competing with, and potentially preying on lizards such as Mediodactylus orientalis, Hemidactylus turcicus, Phoenicolacerta laevis and Heremites vittatus – at least juvenile ones (and it could easily prey on adult Ablepharus rueppellii, if it can find it in the grass and leaf litter).

Aviad Bar with other lizards he recently caught (Varanus griseus). These ones are unlikely to be harmed by any anole and in fact are totally unrelated to this story. But Aviad sent the picture to me alongside the anole photos, and it was just too good to waste.

Right now, probably 2-5 years after it first invaded, A. sagrei seems to be doing extremely well in its new introduced range in Israel – but it is still probably very localized. This means that we have a unique opportunity to deal with it before it spreads further. Our record of dealing with reptile invasions in Israel is abysmal. Few reptile species have been introduced to Israel: Cyrtopodion scabrum, Trachemys scripta and more recently (Jamison et al. 2017) Tarentola annularis (Meiri et al. 2019, Bar et al. 2021). As far as I know, no attempt has been made to stop the spread of C. scabrum and T. scripta. The story of T. annularis is even more telling. Despite being larger, meaner, and potentially far more aggressive species than A. sagrei, and being introduced to a single locality, very little has been done to try and curb its invasion. One person was employed, for a few months, to try to control what was already a population numbering in the thousands – and even this effort was stopped for lack of funding (read: being of very low perceived priority).

I hope this will not be the case with Anolis sagrei too. We have the potential to stop the invasion, still in its infancy, in its tracks. The INPA seem to have the will (and certainly has the means) to do it, and I wish them luck and perseverance. This is an outlet of anole lovers so please don’t get me wrong. I do not wish for Israel to be the next test case of fascinating scientific work on the rapid evolution of Anolis sagrei. We want to keep anoles those wonderful and lizards we read about in papers and books (e.g., Roughgarden 1995, Losos 2009). I want us to keep on having to go and find them in places we find exotic (if there is anything Rishon LeZion is not, it is exotic). I want to engage with the scientists who study them on their own turf. Let’s keep anoles in the Neotropics where they belong.


References
Amador, L., Ayala-Varela, F., Narvaez, A. E., Cruz, K. and Torres-Carvajal, O. 2017. First record of the invasive brown anole, Anolis sagrei Dumeril & Bibron, 1837 (Squamata: Iguanidae: Dactyloinae), in South America. Check List 13: 2083.

Auguste, R.J., Dass, K. and Baldeo, D. 2018. Discovery of the Puerto Rican crested anole, Anolis cristatellus Duméril & Bibron, on Trinidad. Caribbean Herpetology, 63: 1-2.

Bar, A. 2021. Summary of a preliminary survey to evaluate the establishment and distribution of the species brown anole (Anolis sagrei). Report to the chief ecologist of the Israeli Nature and Parks Authority, Pazbar, Herzlia. In Hebrew.

Bar, A., Haimovitch, G. and Meiri, S. 2021. Field guide to the amphibians and reptiles of Israel. Edition Chimaira, Frankfurt Am Main. In Press.
Batista, A, Ponce, M., Garces, O., Lassiter, E. and Miranda, M. 2019. Silent pirates: Anolis sagrei Dumeril & Bibron, 1837 (Squamata, Dactyloidae) taking over Panama City, Panama. Check List 15: 455-459.
Calsbeek, R. and Cox, R. M. 2010. Experimentally assessing the relative importance of predation and competition as agents of selection. Nature 465: 613-616.
Campbell, T. S. and Echternacht, A. C. 2003. Introduced species as moving targets: changes in body sizes of introduced lizards following experimental introductions and historical invasions. Biological Invasions 5: 193-212.
Capinha, C., Seebens, H., Cassey, P., Garcia‐Diaz, P., Lenzner, B., Mang, T., Moser, D., Pysek, P., Rodder, D., Scalera, R. and Winter, M. 2017. Diversity, biogeography and the global flows of alien amphibians and reptiles. Diversity and Distributions 23: 1313-1322.
Donihue, C. M., Kowaleski, A. M., Losos, J. B., Algar, A. C., Baeckens, S., Buchkowski, R. W., Fabre, A. C., Frank, H. K., Geneva, A. J., Reynolds, R. G., Stroud, J. T., Velasco, J. A., Kolbe, J. J., Mahler, D. L. and Herrel, A. 2020. Hurricane effects on Neotropical lizards span geographic and phylogenetic scales. Proceedings of the National Academy of Sciences, USA, 117: 10429-10434.
Echternacht, A. C. 1999. Possible causes for the rapid decline in population density of green anoles, Anolis carolinensis (Sauria: Polychrotidae) following invasion by the brown anole, Anolis sagrei, in the southeastern United States. Anolis Newsletter 5: 22–27.
Fetters, T. L. and Mcglothlin, J. W. 2017. Life histories and invasions: accelerated laying rate and incubation time in an invasive lizard, Anolis sagrei. Biological Journal of the Linnean Society 122: 635-642.
Gerber, G. P. and Echternacht, A. C. 2000. Evidence for asymmetrical intraguild predation between native and introduced Anolis lizards. Oecologia 124: 599–607.
Hsu, M. H., Lin, J. W., Liao, C. P., Hsu, J. Y. and Huang, W. S. 2021. Trans-marine dispersal inferred from the saltwater tolerance of lizards from Taiwan. PLoS One, 16: e0247009.
Jamison, S., Tamar, K., Slavenko, A. and Meiri, S. 2017. Tarentola annularis (Squamata: Phyllodactylidae): a new invasive species in Israel. Salamandra 53: 299-303.
Jensen, J. B., Camp, C. D., Gibbons, W. and Elliot, M. J. 2008. Amphibians and reptiles of Georgia. University of Georgia Press, Athens.
Kamath, A., Herrmann, N. C., Gotanda, K., Shim, K. C., LaFond, J., Cottone, G., Falkner, H., Campbell, T. S. and Stuart, Y. E. 2020. Character displacement in the midst of background evolution in island populations of Anolis lizards: a spatiotemporal perspective. Evolution 74: 2250-2264.
Kraus, F. 2009. Alien reptiles and amphibians. A scientific compendium and analysis. Springer Verlag, Berlin.
Losos, J. B. 2009. Lizards in an evolutionary tree: ecology and adaptive radiation of Anoles. University of California Press, Berkeley.
Losos, J. B. and Pringle, R. M. 2011. Competition, predation and natural selection in island lizards. Nature 475: E1-E2.
Losos, J. B. and Spiller, D. A. 1999. Differential colonization success and assymmetrical interactions between two lizard species. Ecology 80: 252-258.
Losos, J. B., Marks, J. C. and Schoener, T. W. 1993. Habitat use and ecological interactions of an introduced and a native species of Anolis lizard on Grand Cayman, with a review of the outcomes of anole introductions. Oecologia 95: 525-532.
Losos, J. B., Schoener, T. W. and Spiller, D. A. 2004. Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432: 505-508.
Meiri, S., Belmaker, A., Berkowic, D., Kazes, K., Maza, E., Bar-Oz, G. and Dor, R. 2019. A checklist of Israeli land vertebrates. Israel Journal of Ecology and Evolution 65: 43-50.
Meiri, S. 2021. The brown anole in Israel, assessing the invasion pathway, establishment potential and potential threats. Report to the chief ecologist, Israel Nature and Parks Authority. In Hebrew.
Norval, G., Huang, S.-C., Mao, J.-J., Goldberg, S. R. and Slater, K. 2012. Additional notes on the diet of Japalura swinhonis (Agamidae) from southwestern Taiwan, with comments about its dietary overlap with the sympatric Anolis sagrei (Polychrotidae). Basic and Applied Herpetology, 26: 87-97.

Perry, G., Powell, R. and Watson, H. 2006. Keeping invasive species off Guana Island, British Virgin Islands. Iguana, 13: 273-277.

Roughgarden, J. 1995. Anolis lizards of the Caribbean: ecology, evolution, and plate tectonics. Oxford University Press, Oxford.
Schoener, T. W., Losos, J. B. and Spiller, D. A. 2005. Island biogeography of populations: an introduced species transforms survival patterns. Science 310: 1807-1809.
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Solis, J. M., Ayala-Rojas, C. G. and O’Reilly, C. M. 2017. New records for two reptiles from the Bay islands, Honduras. Mesoamerican Herpetology 4: 669-671.
Stroud, J. T., Giery, S. T. and Outerbridge, M. E. 2017. Establishment of Anolis sagrei on Bermuda represents a novel ecological threat to Critically Endangered Bermuda skinks (Plestiodon longirostris). Biological Invasions, 19: 1723-1731.
Stroud, J. T., Mothes, C. C., Beckles, W., Heathcote, R. J., Donihue, C. M. and Losos, J. B. 2020. An extreme cold event leads to community-wide convergence in lower temperature tolerance in a lizard community. Biology Letters, 16: 20200625.
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New Research Explores Evolutionary History of Central and South American Anoles

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On June 3, 2021

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The mainland ground anole Anolis tandai from Brazil. (Photo: Ivan Prates)

The mainland ground anole Anolis tandai from Brazil. (Photo: Ivan Prates)

From GW Today:

June 02, 2021

By Kristen Mitchell

A George Washington University Columbian College of Arts and Sciences Ph.D. student recently published a paper about the evolution of Central and South American anoles, a group of tropical lizards that have been historically understudied compared to their distant relatives in the Caribbean. The study was a collaboration with researchers from the Smithsonian National Museum of Natural History.

Jonathan Huie, a Ph.D. candidate in the Department of Biological Sciences, got involved in this work as an undergraduate student through a National Science Foundation research internship at the Smithsonian National Museum of Natural History. This research sparked his passion for lizards and ultimately guided him toward a doctoral program studying salamanders at GW.

Mr. Huie is lead author of the new paper, published in The Biological Journal of the Linnean Society on Wednesday. Mr. Huie spoke to GW Today about the impact of this research.

Q: Why has there historically been such a significant gap between what researchers know about Caribbean anoles and what they know about anoles found in Central and South America?
A: Most of the 400-plus species of anoles live in Central and South America, and yet the lion’s share of anole research has focused on Caribbean species. There are likely several reasons why, but ease and accessibility are definitely important factors. In the Caribbean, anoles are quite abundant and easy to find but mainland anoles are more secretive, likely because they have more predators to hide from. It’s difficult to study what you can’t see.

Another reason may be because islands themselves are excellent study systems. They’re small and easier to make sense of compared to mainland systems. There’s also a lot of them, which is ideal for replication and hypothesis testing. Lastly, science is often conducted where it’s easiest or most desirable to establish a field site so it’s probably no coincidence that many well-studied anoles occur near vacation spots.

With that said, there’s been a huge push in recent years to learn more about mainland anoles. Our study wouldn’t have been possible otherwise, but there is still a lot we don’t know about mainland anoles.

Q: What did your research reveal about how anoles in Central and South America have evolved to fill various ecological niches?
A: Anoles originated on the mainland, then they colonized the Caribbean, and eventually re-invaded the mainland. Caribbean anoles are well-known among biologists for repeatedly evolving sets of species with similar ecologies and morphologies on Cuba, Hispaniola, Jamaica and Puerto Rico. For example, some species live on thin perches like twigs and have convergently evolved short limbs and well-developed toe pads. Other species specialize in living in tree-crowns, on tree trunks, grasses and bushes. We found that when anoles diversified on the mainland the second time, they convergently re-evolved all of the same habitat specialists and morphological adaptations found in the Caribbean—but this time in Central and South America. This is fascinating given what we often believe to be true about islands and continents.

Our second main finding was that ground-dwelling anoles are really common on the mainland and have their own set of morphological adaptations. Many Caribbean anoles forage on the ground, but very few live there full-time. Mainland ground anoles, on the other hand, really took off. We hypothesized that ground anoles are common on the mainland—at least among the group that re-invaded the mainland—because most arboreal niches were already occupied by other lizards. It’s unclear why Caribbean ground anoles are not more abundant.

GW Ph.D. student Jonathan Huie (center) poses with his mentors Ivan Prates (left) and Kevin de Queiroz (right) at the Smithsonian’s National Museum of Natural History in 2018. (Photo: Smithsonian)

Q: How do your findings challenge long-held assumptions made about evolution on islands compared to mainland habitats?
A: We found that island and mainland anoles are more similar than previously thought. For a long time, it was believed that islands were hotbeds for extreme morphologies and that continents lacked the necessary conditions. In the context of anoles, island species were considered to be unique—that the relationship between habitat and morphology was fundamentally different on islands versus the mainland. However, we found strong evidence that this is not the case.

That is not to say that everything we once thought to be true is now wrong—there are still many differences between island and mainland anoles. However, our research shifts how we should view island and mainland comparisons. Our paper joins other recent studies in suggesting that the mainland is equally good at cultivating morphological diversity as island environments.

Q: How did you get involved in this research, and how did it shape the kind of research you are doing now as a Ph.D. candidate?
A: I got involved as an undergraduate National Science Foundation Research Experiences for Undergraduates (REU) intern at the Smithsonian’s National Museum of Natural History in 2018, under the co-mentorship of Ivan Prates and Kevin de Queiroz. I was a total fish geek and had never studied anoles, but I signed on to investigate the link between habitat and morphology in a handful of mainland anoles.

I measured their body proportions using the museum’s natural history collection but finished quickly. So, we started adding more and more species, and even after the internship was over, I continued to visit other natural history collections to measure even more lizards. The next thing I knew, I had looked at more than 200 species. Natural history collections like the Smithsonian were absolutely critical for this work and fostering my interests beyond fishes.

As a Ph.D. student, I am currently studying salamander limbs to better understand the type of adaptations needed to make the water-to-land transition. The kinds of questions I am interested in for my dissertation are similar to the ones we approached with the anole project. Without my internship, it’s very unlikely that I would have ended up at GW studying salamanders.

Q: How are you planning to build on this research moving forward?
A: There is still so much left to do. In our recent paper, we only published about half of the data I initially collected. We are excited to dive deeper and look at how body size influences patterns of morphological adaptation.

There’s also the other group of mainland anoles that we didn’t look at. I am interested in knowing more about how these other mainland species fit into the puzzle. Did they adapt in a similar manner as the group of mainland anoles we looked at? Or are they doing something different? We would like to know how often evolution repeats itself to produce similar outcomes.

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