You open your eyes, blinking away water, you’re on a beach you don’t recognise, and never set out to visit. You look up and along the coast, it’s an island, the flora is alien to you, the climate hotter, and you’re already sweating. An eldritch cry emanates from the forest near you, new wildlife, things you have never seen before skulk around beyond the vines that lay before you.
Lifting yourself up, you decide to escape the blazing sun. You leave the beach and push through the wall of vegetation that veils the forest from the beach. You expect it to be cooler, but it isn’t. The forest is completely new to you, as you move through the undergrowth, unfamiliar insects dart away, flying past plants you’ve never seen before. As you press on through the undergrowth you wonder how long you will have to spend here? How much more time do you have here?
Upon returning to the first address, I had to search for a long time, 20-30 minutes, before finally stumbling upon one adult male A. Allisoni relaxing on the top of a fence.
I only managed to snap one picture of it in this pose before it hopped onto a palm tree on the other side of the fence. As it slowly made its way up the tree, while cautiously keeping an eye on me, I snapped a few more photos.
After this, I moved on to the next address, about 15 minutes further south in Naples. The area to search was very small, but there were several dense bushes to sift through. After a half-hour spent combing the bushes and peering into the greenery, I finally spotted another adult male A. Allisoni in the underbrush, close to the ground. Unfortunately, he was so deep in the bushes that there was no way to get a clear photo. After an extensive chase, where I scratched myself all over with pointy branches as I tried pursuing the elusive anole through the bushes, he eventually disappeared.
Defeated, I looked up and spotted a small, likely female, A. allisoni hopping from twig to twig much higher in the trees above. This one also completely disappeared as I went to take a picture, unfortunately. However, just as I was about to give up hope and leave, I spotted one final small anole climbing the trunk of a nearby tree at hip level. I crept over and quickly wrapped my arms around the tree where I last saw the anole, and, sure enough, safely snagged it!
Again, at first glance, it appears to be a green anole. But look at the ear cavity. In this observation of a male A. allisoni, the ear cavity is also more of a gash, instead of a hole. And the large scales on the snout would also imply A. allisoni. What do you think?
Join me on Instagram @dailyanole to follow my adventures!
Driven by my quest to find Allison’s anoles (A. Allisoni) in the wild, a few weeks ago I dove into a pit of research papers to look for known sightings and/or colonies of A. Allisoni in Florida. I came upon a few vague notations of a colony in Naples with an address included. So, as part of a herping trip for various anoles and lizards to Miami last week, I stopped in Naples along the way.
I drove to the address and, after parking and entering the area, the first thing I saw was a large male specimen of A. Allisoni perched on the side of a palm tree. Shocked and delighted, I snapped a picture.
To see such a beautiful species of anole in Florida in the wild was breathtaking.
The male allisoni was perched on the palm tree with one large male A. sagrei (brown anole) below him. As I approached the palm to get a clearer picture, the sagrei leaped off the palm onto a smaller scrub, and the allisoni followed right after. The two briefly scuffled, nipping at each other before both went their separate ways and I did not see them again.
Strolling around the area to search for more, I found a very small green juvenile anole. It appeared to be allisoni, but did not give me enough time to properly examine it before scuttling up a tree and into the canopy.
Upon returning to the same spot where the first allisoni was, there was another just a few feet away that I had somehow missed the first time. This one had no hints of blue on its head, but simply from its large size, I took a guess that it was an allisoni. After succeeding at capturing it, I took a picture:
Upon first glance, it seemed to be A. carolinensis. However, on a closer look, both the shape of the ear hole and the large scales on the snout suggested allisoni. Here’s a picture of A. carolinensis for comparison:
For the genetics experts reading this, is there evidence of allisoni interbreeding with carolinensis?
Upon revisiting the address the next day, I searched in the same place I found the first allisoni, and, sure enough, found another one, this time suspected to be a female.
Again, I notice the oddly-shaped ear holes and eyes that seem too large for the head, more characteristic of allisoni than carolinensis.
In total, at this colony, I observed four possible A. allisoni, including two adult males, one adult female, and one juvenile.
I plan to return to check for more allisoni before the warm weather ends and anole activity decreases for the winter.
Male of A. oculatus (background), displaying to the conspecific robot (foreground). Credit: Claire M.S. Dufour
Invasive species can have large negative effects on the environment and the economy, and this is a major driver of research interest. We want to understand what makes invasive species succeed or fail, so that we can tip the balance in favor of native counterparts. Increasingly, biological invasions are also recognized for their research value. These “accidental experiments” can help us answer questions about community assembly, species interactions and evolution (Losos et al. 1993; Stuart et al. 2014; Stroud 2019).
Much of the research on introduced species has focused on obtaining information that can help us predict the next invasion event. This includes efforts to understand pathways of invasion (which can be done using population genetic data) or to identify the traits that make invasive species so successful (which can be done by comparing invasive and non-invasive taxa). Less research has focused on what happens shortly after an invasive species gains a foothold. In particular, we know little about early behavioral interactions between invasive and native species. Might these exchanges determine invasion outcomes and patterns of spread?
Enter the anoles of Dominica
In a recent paper, Dufour and collaborators address this gap using native and invasive anoles in Dominica. The authors built lizard robots that mimic the morphology and display behavior of the invasive species (A. cristatellus) and the endemic species (A. oculatus). With these robots, they tested the responses of A. oculatus males when presented with conspecific and heterospecific displays. The authors used sites where both species are found, and sites where only the endemic is found. Therefore, they could contrast the responses of A. oculatus with and without prior experience with the invader.
Interspecific fight between A. oculatus (left) and A. cristatellus (right). Credit: Claire M.S. Dufour
Robots elicited the expected response. In addition, A. oculatus could discriminate a conspecific robot from a heterospecific robot. Intriguingly, a response to heterospecific displays was recorded even in A. oculatus populations with no prior experience with A. cristatellus. This finding is surprising given the lack of shared evolutionary history of the two species, and remains to be explained. Lastly, A. oculatus males that co-occur with A. cristatellus had a more aggressive display response.
A. oculatus are typically larger and are expected to be the dominant species during aggressive encounters (Dufour et al. 2018a,b). Therefore, it is possible that observed behavioral shifts will impact species coexistence and ultimately decide the long-term outcome of this invasion. Read all about Claire’s exciting new study!
When I hear or read Salmonella, I think of my mom explaining to my 7-year-old self why I shouldn’t eat raw chicken (to be clear, I never expressed interest in doing this, but lesson learned nonetheless). According to the U.S. Centers for Disease Control and Prevention, most instances of Salmonella bacteria making people sick do in fact result from transmission by food. But Salmonella infection can come from other sources, including direct contact with living animals, particularly reptiles (including birds which, in case you haven’t heard, are reptiles). So I was only a little surprised when I came across a recent paper in the Journal of Veterinary Medical Science, based in Japan, documenting the prevalence of Salmonella in the green anole, Anolis carolinensis, on Okinawa Island, Japan.
Of the 706 green anoles from Okinawa Island whose intestinal contents were analyzed for Salmonella presence between 2009 and 2014, only 2.1% tested positive. That number is low compared with published results for green anole populations in Florida (7.5%), Chichi Island in Japan (34.2% – this study was highlighted here on Anole Annals when it came out in 2013), and Guam (76.2%). I’m struck by how much these percentages vary. Green anoles have been in Florida for millions of years, whereas populations in the other locations have only been established for tens of years. The authors hypothesize that infection rate in recently introduced populations should correlate with how long the population has been established. Testing this hypothesis will require data from more populations. It also appears that we know little about whether anoles are affected by carrying Salmonella, although a quick search did reveal this study involving the brown anole, Anolis sagrei.
All told, we have a lot to learn about anoles and Salmonella. In the meantime, please protect yourself from Salmonella infection by following basic food safety precautions: refrigerate foods adequately, wash fruits and vegetables and cook meat and eggs thoroughly, and clean potentially contaminated cookware and utensils with soap and water. Most importantly, WASH YOUR HANDS, although I assume that like me, you are already doing this approximately a hundred times per day (for those of you reading this in the future, I’m not a weirdo. We’re in the middle of a pandemic).
For those who may be interested, green anoles became established in and around Japan several decades ago and are considered an ecologically disruptive pest. If you want to read more, here are links to some old Anole Annals posts on various topics related to the region’s green anoles: trapping efforts, population age structure, range expansion. Enjoy!
Interactions between native Anolis carolinensis (green anoles) and invasive Anolis sagrei (brown anoles) in the United States are discussed often here on Anole Annals. Most recently, this blog featured a local news broadcast from Louisiana and newspaper article from Florida, both of which describe a pattern that is repeated across the southern United States: When brown anoles invade a habitat, green anoles begin perching higher off the ground and thus become more difficult for anole enthusiasts to find.
Why do green anoles and brown anoles tend to occupy different perch heights in areas where they co-occur? By far the most popular explanation is that these species partition space as a means of partitioning resources, namely arthropod food. In simpler terms, they are competitors. But competition itself is not always simple. To better understand and study competition, biologists often classify competition as one of two types. Species can compete directly via aggressive encounters (termed “interference competition”) or indirectly through their shared use of a limited resource (termed “exploitative competition”). We know that green and brown anoles eat similar prey, suggesting that their competition is at least partly exploitative. Do they also engage in direct interference?
In a recently published paper in Oecologia, Katherine Culbertson (Harvard ESPP ‘18, former undergrad researcher in the Losos lab) and I tested the hypothesis that interference competition between native green anoles and invasive brown anoles occurs in the field. More specifically, we wondered if an asymmetry in interference competition might contribute to the vertical displacement of green anoles by brown anoles. To test for competitive asymmetries between the species, we used a classic method in behavioral ecology: tethered intruder trials. We presented adult male intruders to previously undisturbed focal individuals of the opposite species and videotaped the interactions. Intruders were tied around the waist with string at the end of a fishing pole with enough slack to move freely. We analyzed several aspects of the behavior of the focal lizards to evaluate asymmetries in interspecific aggression between the species: how often they attacked, how often they displayed (throat fan extensions, headbobs, and pushups), how often they retreated, and in what direction they retreated. (Disclaimer: Whenever an attack occurred, we ended the trial immediately so no lizards were harmed.)
As anticipated, we found that interference competition is asymmetric in favor of brown anoles, which are more likely to display and less likely to retreat from interactions than green anoles. In line with their arboreal tendencies, male green anoles also trend toward retreating upward more often than expected by chance. Somewhat surprisingly, these asymmetries are prevalent despite the almost complete absence of physical attacks (there were only two attacks in nearly one hundred trials, both by brown anoles). All told, our results suggest that signaling between the species and avoidance behavior by green anoles resolve most potential conflicts before they escalate to combat.
Figure 2 from our paper, which displays posterior predictions for the (a) probability of display, (b) display rate, and (c) probability of retreat of male Anolis sagrei (brown anoles, “SA”) and male Anolis carolinensis (green anoles, “CA”) when presented with a male intruder of the opposite species. Brown anoles were more likely to display and less likely to retreat than green anoles.
Many Floridians I’ve met in the course of my fieldwork have described brown anoles as bullies. Although anecdotal observations of animal behavior do not always reliably represent biological truths, in this case, the collective of observations made the residents I’ve spoken with are concordant with our data. Kudos to the many local naturalists who’ve shared their stories!
In closing, I’ll attempt to refine the metaphor of brown anoles as bullies, in acknowledgement that metaphors are often imperfect and with apologies to those who bristle at any attempt to anthropomorphize non-human animals. First, what makes a bully effective? On the playground, a bully might gain a reputation as such by initiating and winning a fight. Afterward, the mere threat of physical combat is often enough for the bully to exert his or her will on others. At our study sites, where green anoles and brown anoles have co-existed for several generations, brown anoles tend to dominate interactions with green anoles without attacking them. Perhaps physical combat is more common during the incipient stages of brown anole invasion, a hypothesis which could be tested by applying our methods across sites that vary in their invasion history.
Second, what’s the best way to deal with a bully? Many children learn to ignore bullies, a strategy rendered possible by the existence of alternative space to play or activities to engage in. Green anoles appear to find refuge in the canopy, where brown anoles seldom venture. Anecdotally, areas where no such canopy exists (i.e. areas with few plants or with only short, shrubby vegetation) are the areas where green anoles are most likely to disappear entirely following brown anole invasion. This hypothesis deserves a formal test.
Special thanks to the Aquatic Preserve Program run by the Florida Department of Environmental Protection for making this work possible. Check out the paper to learn more about our methods, results, and the implications of our findings.
Katherine Culbertson marking the location of a captured green anole in the field.
Aging theory predicts that organisms will age faster when the probability of survival to old age is low. As a result, males and females of a species may age at distinct rates if they experience different rates of mortality due to environmental factors. Postdoctoral researcher Dr. Aaron Reedy (Auburn University) and colleagues tested this idea by performing a mark-recapture study of introduced Anolis sagrei in the small Island H in Florida, an island that is approximately the size of a baseball field.
Location of island H in Florida.
The team tracked 6,591 individuals of A. sagrei from hatchling to death through a near-complete sampling of the population four times a year between 2015 and 2019 (!!). The research group measured the body condition of individuals based on the residuals of mass on body length and estimated the rate of aging based on chromosomal telomere length from real-time qPCR.
The results suggest that males have higher mortality and shorter lifespans than females; most males die within two years, while females can live up to three and even four years. The study also found that males suffer a decline in body condition with age that females don’t seem to – Aaron even mentioned that he is often capable of predicting how old a male individual is based on how haggard it looks! Preliminary data suggests no statistical differences in telomere length between males and females, although there seems to be a trend of decreasing telomere length with age in males only.
Male brown anole.
In conclusion, Dr. Reedy and colleagues found that males have increased mortality and shorter lifespans than females, but it is unclear whether males senesce more rapidly. The next steps of this investigation will include longitudinal studies in both the field and lab to follow how fast single individuals age over their lifetimes.
The brown or festive anole, Anolis sagrei, is an invasive species in several countries in the Americas and Asia. This species is native to Cuba, the Bahamas, and the Cayman islands. Following introductions, A. sagrei can reach high population densities and undergo rapid range expansion. In a recently published contribution, we provide the first record of this aggressive invasive lizard in Brazil.
In 2017, we recorded specimens of A. sagrei within the limits of an International Airport in the metropolitan area of the city of Rio de Janeiro, southeastern Brazil. The observation of juveniles and mating couples suggests that the species is established locally.
The origin, geographic extent, and potential for spread of A. sagrei in Rio de Janeiro and Brazil are currently unclear. It is also unclear whether this species will be able to colonize natural habitats, such as the surrounding Atlantic Rainforest.
The establishment of brown anole populations elsewhere has led to shifts in substrate use by native anoles and promoted major shifts in the structure of local insect assemblages. As such, this species has the potential of affecting local ecological communities in Brazil. However, the effects of A. sagrei on the local fauna – including native lizards that we sampled in the area – are difficult to predict.
This is the second case of an established exotic anole species in Brazil. Populations of the Cuban green anole, Anolis porcatus, were recently detected in several sites in the Baixada Santista coastal region, state of São Paulo.
To know more:
Oliveira J.C.F., Castro T.M., Drago M.C., Vrcibradic D., Prates I. (2018). A second Caribbean anole lizard species introduced to Brazil. Herpetology Notes, 11: 761-764.
PDF available here (at the bottom of the webpage).
The nursery trade is a known vector for many invasive species including anoles. Anoles have quite the affinity for laying eggs in the moist soil of potted plants, which may then be transported to various locations. Indeed, the nursery trade is the suspected vector for introductions to Hawaii and California of A. carolinensis and A. sagrei and likely accelerated their spread within those states. In fact, citizen scientists on iNaturalist document a reasonable number of brown anoles well outside their normal range. These observations have a distribution that suspiciously coincides with locations of Home Depots and Lowes. However, while the nursery trade is a suspected vector for other species of anoles, verified instances of long-distance transport via the trade are fewer and farther between.
An (as yet) unidentified anole hatchling transported from Puerto Rico to Virginia. From user kimjy3 on iNaturalist.org
One recent observation on iNaturalist documented a hatchling anole that popped out of a potted plant shipped from Puerto Rico as the user unwrapped it…in Alexandria, Virginia. Can anyone on Anole Annals having experience with Puerto Rican anoles and their hatchlings help ID this little one? The user reports that the anole does not have blue eyes; instead they are brown or black.
Claire Dufour, Postdoctoral Fellow at Harvard University, presents her research at the 2018 Joint Congress on Evolutionary Biology in Montpellier, France.
In another excellent study exploring the effects of anthropogenic activity on evolution in anoles, Postdoctoral Fellow Claire Dufour is investigating how the recent introduction of Anolis cristatellus from Puerto Rico to the island of Dominica may be driving changes in the display behavior of Anolis oculatus, a Dominica native. Specifically, Dufour is asking whether interactions between the A. cristatellus and A. oculatus are consistent with patterns of Agonistic Character Displacement, in which interference competition between the newly sympatric species results in shifts in traits affecting the rate, intensity, and outcome of interspecific aggression.
To begin, Dufour and colleagues constructed a pair of robots that mimicked the typical look and display behavior of a male A. oculatus and A. cristatellus. She then traveled across Dominica and presented over 130 wild male A. oculatus with one of the two robots, and recorded the display behavior exhibited in response. Beyond measuring the duration of the response display, Dufour also tracked the proportion of time spent by the A. oculatus engaging in any of nine specific display behaviors, such as dewlap extensions, push ups, nuchal crest presentations, and others. By repeating this experiment among populations of A. oculatus existing sympatrically with A. cristatellus, as well as populations not yet invaded by A. cristatellus, Dufour was then able to ask whether variation in display time or composition among the native anoles could be attributed to the presence of A. cristatellus. Indeed, this turned out to be the case.
Anolis oculatus living in allopatry from the introduced A. cristatellus were found to engage in longer display bouts when presented with the conspecific robot, and shorter display bouts when presented with the unfamiliar A. cristatellus robot. Alternatively, A. oculatus occupying habitats already intruded by the A. cristatellus increased the duration of time spent displaying, regardless of which robot was presented. In addition, A. oculatus were also found to alter the behavioral composition of their displays when occupying habitats shared by the introduced A. cristatellus.
Dufour and colleagues capitalized on a rare opportunity to document the very early stages of a species invasion, and in turn improve our understanding of how human-mediated species introductions can promote evolutionary change. As changes in behavior are often the first response to novel competition, these results are consistent with the criteria of Agonistic Character Displacement, and support the claim that the introduction of crested anoles in Dominica has indeed driven a shift in the behavior of native anole communities. While the consequences of these shifts on the outcome of interspecific competition are still unclear, it will be interesting to see how differences in display behavior develop over time, and further, whether these initial changes in display behavior could lead to additional shifts in behavior or morphology among these newly interacting species.
