Anole Annals

Male Anolis cristatellus showing off his crest.

Anolis cristatellus is a great study species for investigating the effects of urbanization. They are widely distributed across the island of Puerto Rico, and occur at high densities in both forests and urban areas. By comparing the morphology, behavior, and physiology of lizards in these two habitat types, a number of anole researchers are currently learning about the effects of urbanization on this species and how the species is responding to these novel environments.

Anolis cristatellus is also named for the huge, beautiful tail crests that males often possess. They are one of a number of anole species to possess a tail crest (25 of ~425 described species have crests), but the function of the crest is still unknown. One of the only studies addressing anole tail crest function suggests that they might be used for signaling across large distances (Charles & Ord 2012), but other possibilities have not been tested. We thought that temperature may play a role as well, with the tail crest allowing increased heat transfer between the anole and its environment (similar to mechanisms that have been proposed for the dorsal fans on Permian synapsids). 

My first Anolis, captured in 2012!

In our recent paper, we ( Kristin Winchell, Liam Revell and I) decided to study how these tail crests vary across Puerto Rico in urban and forested areas and test whether any variation we observe in crest morphology is associated with environmental variables that differ across these urban and forested habitats. To do this, we measured tail crest size across three populations using scans of lizard tails that I collected during my summer undergrad REU at UMass Boston many years ago. ‘Twas the first time I ever caught anoles! Sigh, memories… 

We then tested whether tail morphology varied across our three sampled municipalities or across habitats types (urban and forest), and whether any observed variation was associated with temperature, precipitation, or openness (i.e. perch isolation).

A typical image of a scanned crest used in our analyses.

We found that tail crest size does vary across the three populations, but in each locality we sampled, urban lizards had larger crests. Interesting! Why might that be ? Well, it turns out that the environmental factors we measured also differ between urban and forest areas. The urban areas we sampled have higher temperatures than the forest areas. The larger tail crests in urban areas could therefore suggest a potential thermoregulatory role. But that’s not the only possibility presented by our data. Urban habitats tend to be more open, which could allow for longer sight lines between individuals, potentially supporting the hypothesis that larger tail crests are used for communication in open environments. But so far, our conclusions are necessarily limited. Nonetheless, even though we don’t know the function of the crest, the fact that crest size differs between urban and forested areas suggests that it’s under some sort of differential selection in these different habitats, which is quite intriguing. 

We hope this paper can be a part of a larger body of research around Anolis (and squamate) tail crest function and evolution.  Quite a few species have crests, but very few have been studied. If you have tail crest data/pics lying around, I encourage you to get them out there! In the meantime, feel free to read our full paper here.

Many factors contribute to colonization success in novel habitats. Anoles, as a group, are particularly adept at establishing in new areas. Urban ecosystems are no exception. A diversity of studies have sought to understand how adult anoles conquer human-modified habitats, but relatively little attention has been given to earlier life-stages (e.g., eggs). The brown anole (Anolis sagrei) and the crested anole (Anolis cristatellus) (Figure 1) are two species that have received considerable attention. Although these two species are quite similar in morphology and habitat preference (i.e. both trunk-ground anoles), work from Jason Kolbe’s lab (e.g. Battles and Kolbe 2019), shows that adults differ in thermal preference: A. sagrei prefers warmer, open-canopy habitats while A. cristatellus prefers cooler, closed-canopy habitats. Because temperatures are unusually high in urban areas (i.e. the urban heat island), the spread of A. cristatellus may be limited throughout the urban matrix compared to A. sagrei.

But what about eggs? Two recent studies suggest that A. sagrei nests reach warmer temperatures than those of A. cristatellus (Sanger et al., 2018, Tiatragul et al., 2019), thus, like adults, A. sagrei embryos may be more robust to high temperatures. Is it possible that thermal tolerance of embryos differ between these two species? If so, this may also help explain why A. sagrei has been much more successful at colonizing urban habitats where ground (and nest) temperatures are usually much warmer than in adjacent rural or natural areas (Tiatragul et al., 2017).

In a study recently published in the Journal of Experimental Biology (Hall and Warner 2019), we subjected eggs of A. sagrei and A. cristatellus to extreme fluctuations in temperature modeled from nests in urban environments. We found that A. sagrei embryos have a thermal tolerance approximately 2 degrees Celsius higher than A. cristatellus. This indicates that the thermal physiology of embryos is adapted to species-specific nest temperatures (though we discuss other possible explanations as well). Regardless, thermal tolerance differs widely between these two species, and this may help explain species-specific patterns of occupancy throughout the urban matrix.

As a side note (that I reluctantly removed from the manuscript during the review process – long sigh), although the Anolis radiation, which includes nearly 400 species, is considered a model system for studying adaptive radiation, to our knowledge, studies never consider that embryo phenotypes and egg survival may be an important driver of speciation. This is particularly important for two reasons. First, egg survival is a vital determinant of population cycles for these lizards (Andrews 1988), and likely plays a vital role in population viability, survival, and colonization success (Losos et al., 2003). Second, this adaptive radiation is characterized by many dispersal events, often from and to small islands throughout the Caribbean (Poe et al., 2018). Although key innovations, phenotypic plasticity, niche expansion and other processes are considered important in such dispersals, these processes are always evaluated from the perspective of adult phenotypes. Successful embryo development, however, is a requirement for persistence in every environment. Given that general protocols exist for embryo collection and analysis (Sanger et al., 2008a,b), we suggest this system is ripe for a relatively broad phylogenetic analysis of embryo physiology. Such work would illuminate the importance of embryo adaptation in colonizing novel environments (e.g. urban landscapes) and responding to environmental perturbances (e.g. climate change), and give us something to talk about other than dewlaps and limb lengths (which would make me happy).

Andrews, R.M., 1988. Demographic correlates of variable egg survival for a tropical lizard. Oecologia, 76(3), pp.376-382.

Battles, A.C. and Kolbe, J.J., 2019. Miami heat: Urban heat islands influence the thermal suitability of habitats for ectotherms. Global Change Biology, 25(2), pp.562-576.

Hall, J.M. and Warner, D.A., 2019. Thermal tolerance in the urban heat island: thermal sensitivity varies ontogenetically and differs between embryos of two sympatric ectotherms. Journal of Experimental Biology, 222(19), p.jeb210708.

Losos, J.B., Schoener, T.W. and Spiller, D.A., 2003. Effect of immersion in seawater on egg survival in the lizard Anolis sagrei. Oecologia, 137(3), pp.360-362.

Poe, S., de Oca, A.N.M., Torres-Carvajal, O., de Queiroz, K., Velasco, J.A., Truett, B., Gray, L.N., Ryan, M.J., Köhler, G., Ayala-Varela, F. and Latella, I., 2018. Comparative evolution of an archetypal adaptive radiation: innovation and opportunity in Anolis lizards. The American Naturalist, 191(6), pp.E185-E194.

Sanger, T.J., Hime, P.M., Johnson, M.A., Diani, J. and Losos, J.B., 2008a. Laboratory protocols for husbandry and embryo collection of Anolis lizards. Herpetological Review, 39(1), pp.58-63.

Sanger, T.J., Losos, J.B. and Gibson‐Brown, J.J., 2008b. A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology. Journal of Morphology, 269(2), pp.129-137.

Sanger, T.J., Kyrkos, J., Lachance, D.J., Czesny, B. and Stroud, J.T., 2018. The effects of thermal stress on the early development of the lizard Anolis sagrei. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 329(4-5), pp.244-251.

Tiatragul, S., Kurniawan, A., Kolbe, J.J. and Warner, D.A., 2017. Embryos of non-native anoles are robust to urban thermal environments. Journal of Thermal Biology, 65, pp.119-124.

Tiatragul, S., Hall, J.M., Pavlik, N.G. and Warner, D.A., 2019. Lizard nest environments differ between suburban and forest habitats. Biological Journal of the Linnean Society, 126(3), pp.392-403.

Anole Annals readers no doubt recall All-America Park, where so many anole species cavort in South Miami. Turns out the city is “cleaning it up” which spells no good for our favorite lizards. Local A-A Park resident Christopher Cooke writes:

“I live next door to All America Park in South Miami (6820 SW 64th. Avenue), a formerly well known habitat for lizards – I’ve met people from everywhere who have come to study the lizards here.  I’m battling the City which is “sanitizing” the park and I’m looking for any information or references (past or present) in  lizard literature which  highlights the importance of this property as a wildlife environment.  My goal is to stop the “sanitizing” l and replant habitat material so as to restore a conducive environment for lizards and other wildlife.  Any help you can offer will be much appreciated.    Christopher Cooke, neighbor of Neil Losin – for those who know him.”

Please make comments on anything that may be useful. Good luck, Christopher!

And while on the topic, here’s a lovely photo by South Miami mayor and neuroethologist extraordinaire Phil Stoddard, taken near the park.

Anolis cristatellus snoozing on a dragonfruit. Photo by Philip Stoddard

Photo by Dee Jacobsen

Dee Jacobsen from southeastern Louisiana sent in these lovely photos. Here’s what went down:
“I came across your site and wondered if you would be interested in see this photo I took in southeast Louisiana of an anole eating and being stung in the tongue by a bee. I was sitting on my porch and this little guy came running toward me to grab that bee by my foot. Scurried off with it and I grabbed the camera. We have so many anoles here that I take lots of shots of them but this one was most unique.”

Charles Leeper from San Antonio writes:
There appears to be a high population of green anoles on our property. While watering some plants, I sometimes spray a large patch of common ivy. What I’ve noticed is green anoles leaping from the above tree limbs onto the ivy leaves in order to drink the water I’ve just sprayed on them. At first, I heard thuds on the ivy and didn’t know what it was, but then I started watching the tree limbs and saw anoles climbing to the edge and leaping off – probably from a height of ten feet. I only notice them jumping from the trees after I’ve watered. I imagine this is typical behavior after a rain, and my water-spraying replicates such an event? I’m sure this is well-documented behavior, but in the case that it isn’t or is unique to a ground covered in a soft landing pad like ivy, I thought I would share it.
Nonetheless, I enjoy observing them and wanted to let you know there is a solid population here!
Charles kindly agreed to take video of some of the action. Thanks, Charles! And here’s his commentary on th videos (two more below):
I captured some footage of the anoles leaping off the trees. The first two videos (the one at the top of the page and the second one below) document them jumping from a branch of only about 4 to 5 feet, and the third one (the first one below) is from a height of perhaps 9 feet (it’s a bit tough to see, but this one shows a very young anole on the center branch – what a dive it takes!). I have seen many more than this (and from heights of probably 15 to maybe 20 feet), but only managed to record these occurrences.
I have not observed them much while it’s raining (a rarity down here in the summer!), but I would imagine they don’t partake in this jumping during or following a rain because either they don’t have to drink from the ivy as the raindrops hit the trees, or they’re already on the ground and not perched/basking in the trees during a storm.
The following is just conjecture, but possibly they smell, hear, or see the water hitting the ivy, and it’s not sprinkling the trees, so they’re drawn down for a drink. As for why they leap off as opposed to crawling down the tree, which does sometimes happen, perhaps they’ve learned the ivy is a soft landing pad and it’s just less energy-intensive to jump, or they’re avoiding bigger green anoles that may be near the base or brown anoles. Although, I’m not sure there are many brown anoles here as I don’t think I have seen them, but I certainly could be wrong.

And here’s a lizard drinking post-spraying:

Communication is a prerequisite of human society. But when you look, smell and hear around, you rapidly realize that we are not the only ones to communicate. Indeed, plants, fungus, animals and other living things such as bacteria show extraordinary ways to “talk” to each other.

The diversity of animal signals  (e.g. visual, acoustic, chemical) and their evolution has particularly fascinated biologists for decades. Etymologically, the term “communication” implies to share information between a signaler and a receiver, but the interplay between the two remains extremely challenging to study, especially in animals in their natural environment.

The use of robots in ecology is in its infancy, but promises great advances in the study of animal communication. Lizards are not outdone with this robotic revolution (see previous AA posts and several others should be forthcoming!). The use of lizard robots allows researchers to control the signal stimulus directly in the field and to address questions related to species recognition, mate choice and evolution of aggressiveness, for instance.

In a recent paper, Dave Clark and collaborators went further by designing an interactive lizard robot! Yes, the study is about Galapagos lava lizards, but it deserves great attention in the Anole Annals community as understanding the processes underlying lizard communication is of pressing interest in anole research and the interactive robot may help to understand its evolution. The authors presented a bio-mimetic conspecific robot and tested whether an immediate or a postponed 30s response of the robot to the subject’s display influenced the display latency and duration of the focal individual. They found that immediate display response by the robot to a subject’s bobbing display stimulated the focal lizard to display more rapidly and more often than when the robot’s response was delayed. These results suggest that subjects perceived a rapid response from their robotic contestant as being more aggressive than a delayed response.

This study is the first interactive robot playback experiment with lizards in natural conditions and it demonstrates that the response ‘timing of the receiver is a crucial factor of lizard communication.

Reference:

Clark, D.L., Macedonia, J.M., Rowe, J.W., Austin, M.R, Centurione, I.M, Valle, C.A. (2019). Galápagos lava lizards (Microlophus bivittatus) respond dynamically to displays from interactive conspecific robots.  Behav Ecol Sociobiol 73: 136. https://doi.org/10.1007/s00265-019-2732-6