Heidi Fagerberg, a children’s book writer, is in the middle of writing a book featuring the green anole of St. Kitts. Photos below. Can anyone confirm that these are Anolis bimaculatus? More importantly, does anyone know about their color-changing abilities and proclivities? Under what conditions does color change occur?
Some months ago, I posted a quick analysis of a dataset from 2010 on the movement rates of green anoles (Anolis carolinensis) in the presence and absence of brown anoles (Anolis sagrei) on spoil islands in Mosquito Lagoon, FL. At Jonathan Losos’s urging, Yoel Stuart and I turned this blog post into a paper, which was recently published in Breviora.
The story has not changed since the blogpost (though the analyses are now slightly more sophisticated): male and female green anoles seem to respond differently in their movement behaviour to the presence of brown anoles. There are many possible reasons for these differences, discussed in the paper, that can be summarized as “variation in the motivation for movement between the sexes.” Do read the paper if you’re interested in further details, but be forewarned that we engage in quite a bit of speculation because of one simple fact: compared to what is known about movement rates of male anoles, we know much less about how movement rates in female anoles vary with microhabitat.* Similar disparities between what we know about males and females exist in other aspects of anole biology too.
Though the subject matter of our paper is rather niche (anole ecology pun intended), it contains one paragraph that I think is more broadly pertinent:
Much more attention has been paid to the behavioral ecology of male anoles than to that of female anoles (Butler et al., 2007; Losos, 2009). Our results suggest that male and female anoles can differ in their behavioral responses to ecological pressures. Understanding the mechanisms leading to behavioral and ecological variation within a species will therefore depend upon documenting this variation in both males and females, a conclusion that is hardly surprising. It is disappointing that research on fundamental aspects of the biology of even organisms as well-studied as Anolis lizards remains largely focused on males
There are reasonable reasons for focussing research on males. Male anoles are indeed often easier to spot in the field, and are certainly easier to catch. And incorporating an effect of sex into our statisical models will require us to double our sample sizes. But in many species, observing and catching females isn’t so difficult as to excuse not studying them. For example, in the last month or so, my undergraduate collaborator Rachel Moon and field assistant Barbara Da Silva have measured the ecology and morphology of over 300 Anolis sagrei females—an enviable sample size in any circumstances.
Females have been ignored in all sorts of studies of all sorts of organisms. The absence of female subjects in biomedical trials, for instance, has far more serious consequences than the gaps in our knowledge of the biology of female anoles. Nonetheless, given that many of us are dedicating some portion of our lives to understanding these animals, making sure that we don’t ignore half of them seems like a worthwhile goal. 
*This gap exists for two reasons: some previous studies don’t sample females, others sample both sexes but don’t distinguish between them.
I spent most of last week battling a cold. One of those awful, end of the semester, got-a-taste-of-freedom-but-now-I’m-bedridden colds. If you’re anything like me, the first sign of illness sends you scrambling trying to recall what your mother said about coping with illness. I always seem to remember my mother explaining fevers to me.
I was shivering under a pile of blankets, influenza-ridden and miserable, suffering from the worst fever I experienced as a child. My mother described a war being waged inside me, self versus virus, and tried to convince me that this crummy feeling might actually be a good thing. Impossible! I spent that day wrapped up a little too tightly, flashing from hot to cold, cold to hot. The next morning, I was achy and exhausted—a war had taken place in there, after all—but miraculously, I felt better. I was amazed that my body’s response to the flu-y invader had contributed to its eradication!
“Fever” occurs when body temperature is elevated above the normal range, and we have long been intrigued by its function in staving off infection. In our own bodies, the brain can trigger the body to heat up when it detects infection. This temperature elevation seems to facilitate the immune system, and the warm temperatures make the internal environment less favorable for infectious agents such as bacteria or parasites attempting to live there (feverish to know more?). Endothermic creatures such as us, which produce and maintain body heat internally via metabolic activity, frequently battle infection with fever. But what about ectotherms?
One of our favorite topics here at Anole Annals is adaptive radiation. Don’t believe me? Just type adaptive radiation into the search bar on the right and see all the interesting posts that come up. And why shouldn’t we be interested in AR? After all, anoles are one the great examples of the phenomenon.
So, it seems relevant to notice that two new review papers just appeared on the topic, both of which mention anoles at least in passing. Tom Givnish, in a paper in New Phytologist stemming from a conference on plant radiations last year, provides the most convincing analysis to date about why the term “adaptive radiation” should be reserved for clades that have diversified to occupy a wide range of ecological niches, regardless of how fast they have done so and how many species the clade contains (title of paper: Adaptive radiation versus ‘radiation’ and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution).
Some pithy quotes encapsulate his points:
“Of the early writers on adaptive radiation (Osborn, 1902; Huxley, 1942; Lack, 1947; Simpson, 1953; Carlquist, 1965; Mayr, 1970; Stebbins, 1974), only Simpson included what we might term explosive speciation in his concept of the process.”
“Definitions of adaptive radiation that require accelerations of species diversification relative to sister groups will thus fail to identify Darwin’s finches and Brocchinia as adaptive radiations; excluding such iconic examples of adaptive radiation makes such diversification-based definitions untenable.”
“Why should we care about this distinction? Nothing could be more pointless than a pedantic debate about definitions that goes nowhere. I would argue, however, that making a distinction between adaptive radiation and explosive diversification is fundamental to understanding evolution, and that failure to make such distinctions can blur such understanding and hinder progress.”
Givnish goes on to suggest that “we might consider re-defining adaptive radiation as ‘the rise of a diversity of ecological roles and associated adaptations within a lineage, accompanied by an unusually high level or rate of accumulation of morphological/physiological/behavioral disparity and ecological divergence compared with sister taxa or groups with similar body plans and life histories.’ Such a definition would retain traditional components of adaptive radiation, while suggesting a way forward that includes tempo, not in species diversification, but in the rate of accumulation of disparity.”
Meanwhile, Soulebeau et al., in a new “Forum Paper” in Organisms Diversity & Evolution, conduct a review of the use of the term “adaptive radiation” in the period of 2003-2012 (title: The hypothesis of adaptive radiation in evolutionary biology: hard facts about a hazy concept). Givnish would say that it is hard to draw conclusions from a meta-analysis that lumps different concepts all under one name, but the review does show some patterns in how research is trending. If nothing else, the number of papers purporting to study adaptive radiation doubled over the time period. Moreover, the paper makes an important point that the number of studies that investigate whether adaptive evolution has occurred in a putative adaptive radiation is very low.
The California Academy of Sciences in San Francisco has just opened a new exhibit, The Color of Life. You can read more about it at their website. Naturally, anoles played a prominent role in the exhibit, as the panel above attests. The small print says: “Anole lizards regularly advertise their ownership of their territories. They bob their heads and extend a colorful flap of skin called a dewlap, just in case another male is watching.”
Notably, the anole gets much more prominent billing than frogs, which are relegated to a panel further back in the exhibit, as the photo to the right illustrates. Perhaps it’s not surprising, then, that Cal Acad Herpetology Curator Dave Blackburn has just inked a deal to move to the University of Florida where, sources say, he will not only become the Curator of Herpetology at the UF Museum of Natural History, but will also switch his research program from frogs to the local anoles. A wise move, indeed, and we look forward to his further explanation in the Comments section.
Anolis maynardi–doing just fine alongside brown anoles on Little Cayman
Two days ago, Ambika Kamath posted an entry in which she observed that the green anoles in her study site in Gainesville are doing just fine, they’re just high up in the trees and harder to spot than the abundant browns. She concluded that, contrary to what many think, brown anoles are not threatening greens in Florida with extinction.
I’d like to add to Ambika’s conclusion by pointing out how browns and greens interact throughout the natural range. Both species evolved in Cuba. There members of the sagrei group coexist widely with carolinensis’s relatives. Where they co-occur, brown anoles are very abundant and are found on the ground and low in vegetation. Greens, primarily A. allisoni and A. porcatus are seemingly less abundant (population estimates are not available) and they occur on tree trunks on up into the canopy.
This mostly peaceful coexistence is repeated in other places the two species co-occur. In the Bahamas, it’s A. smaragdinus and A. sagrei, on Little Cayman, it’s A. maynardi and A. sagrei. In both cases, sagrei is apparently much more abundant, and the two species occupy different parts of the habitat.
Some time ago (possibly several million years, according to genetic data), green anoles colonized Florida from Cuba. In the absence of browns, the greens took the arboreal to increase their habitat use, a phenomenon termed “ecological release.” Then the browns arrived, thanks to us. They have moved into their ancestral niche and the ancient order has been restored. Greens have moved back up in the trees and, yes, their populations are probably now smaller, because some of the resources they were using are now taken by browns. But they’re not going extinct. Greens and browns stably coexist throughout their range. That’s what they’ll do in Florida, too, as long as all the trees aren’t cut down for shopping malls and parking lots.
Tell almost anyone in Florida that you’re doing research on brown anoles (Anolis sagrei), and they’ll express some distaste for your study organism. “I don’t like them,” they’ll say, “they’re invasive. Aren’t they driving the native green anoles extinct?” Everyone—literally everyone who has lived in Florida for a while—will tell you how their backyards used to be full of green anoles (Anolis carolinensis). Today, they report, these green anoles have disappeared and been replaced by the invading browns.
Green anoles, increasingly elusive in Florida
These backyard tales are supported by some scientific evidence for shrinking populations of green anoles . On spoil islands in Mosquito Lagoon, Dr. Todd Campbell documented precipitous declines in green anole densities following the experimental introduction of brown anoles [1]. In southwest Florida, Cassani et al. repeated surveys of reptile and amphibian abundance fifteen years apart, using identical methods in exactly the same locations [2]. They found a drop in green anole numbers and a sharp rise in brown anole numbers between 1995 and 2011. Based on their results, both Campbell and Cassani et al. suggest that the persistence of green anoles in Florida has been jeopardized by the invasion and spread of brown anoles.
But both Campbell and Cassani et al. acknowledge a second possible explanation for the apparent disappearance of the green anoles: the lizards may simply have shifted upwards, out of sight.* As Cassani et al. put it, “the hope remains that these lizards persist in the face of competition and predation from A. sagrei by shifting habitat use.” We already know that green anoles shift upwards at least a bit in the presence of brown anoles, and have evolved morphological features that likely help them survive at these higher perches [3]. Could green anoles have shifted so high as to be nearly invisible to us, from our vantage points near the ground?
A bead-tagged brown anole
When I started studying brown anoles in Gainesville, FL, in 2014, I was convinced that the green anoles were all gone. But as we spent many hours marking individual brown anoles and repeatedly surveying their habitat to re-spot them, we began to spot a few green anoles too. I guessed that these green anoles were the last few holdouts against the invaders, and that we were seeing the same individuals again and again. To prove this, all we needed to do was catch and individually mark these green anoles using permanent bead-tags, in exactly the same way that we were catching and marking the brown anoles. It didn’t seem like too much extra work, so once I realised that my 2015 fieldsite was also home to quite a few green anoles, we began catching and tagging them as well.
In two months of sampling, we either caught or re-spotted green anoles a mere 52 times. In the same period and location, we caught or re-spotted brown anoles 4369 times, which certainly seems to suggest more brown anoles than green anoles in this site. But to compare the population sizes of brown and green anoles, you need to compare how often you see new, unmarked individuals relative to how often you see already-marked individuals for each species**. In the graphs below, I’ve plotted the total number of observations against the total number of marked individuals for both A. carolinensis and A. sagrei***, and then zoomed in to just the first 52 observations for both.
Zoomed in, you notice that the curves for the brown and green anoles look quite similar. If anything, we see more new individuals per observation for green anoles than for brown anoles. Neither of these curves has begun to plateau (i.e. we’re still seeing lots of new individuals), so we cannot quantify the difference in total population size of these two species. But these limited data suggest that this population of green anoles is not doing that badly.
The taller tree was home to at least three different green anoles
But if the population is doing okay, then why weren’t we spotting green anoles all that often? The most logical explanation is that the green anoles have shifted up to very high perches, and only rarely descend to heights at which we can observe and catch them easily. Moving a bit beyond the numbers, we find another piece of evidence that supports the idea of a perch height shift—of the 40 green anoles we caught, only eight were males!
We know that male anoles usually perch higher than female anoles [4], that female anoles will often search for and feed on insects on the ground, and that females must descend to the ground to lay their eggs. Males, on the other hand, often move to higher perches to display, seem to feed more opportunistically than females, and are not necessarily compelled to return to the ground after they hatch. Though sex ratios can deviate quite a bit from 1:1 in natural populations of anoles [5], it seems unlikely that a population of green anoles could be comprised of one male for every four females. Taking the sex differences in perch height into account, it makes sense that for every female green anole we spotted, there’s a male green anole perching really high up whom we simply did not see.
None of this means that green anole densities aren’t declining due to the presence of brown anoles in some habitats. In particular, because brown anoles can perch as high as 4 m off the ground, there may be many places in which green anoles previously thrived but where there is simply no “up” for them to escape to once the brown anoles arrive. I suspect that many backyards are exactly such places, and that some reports of local declines in green anole population sizes may in fact be well-founded.
But it’s also certainly possible that, in habitats with sufficiently tall trees, brown anoles are not driving green anoles to extinction. Instead, brown anoles may simply have precipitated a substantial upward shift in the perch height of green anoles towards their ancestral trunk-crown niche. It’s therefore possible that green anoles are thriving, just out of our sight. If that’s the case, then brown anoles don’t deserve quite so much of our animosity after all!
A brown anole perching pretty high.
References:
[1] CAMPBELL, T.S. 2000. Analyses of the effects of an exotic lizard (Anolis sagrei) on a native lizard (Anolis carolinensis) in Florida, using islands as experimental units. Unpublished Ph.D. Thesis. Knoxville, USA, University of Tennessee
[2] CASSANI, J.R., D.A. CROSHAW, J. BOZZO, B. BROOKS, E.M. EVERHAM, D.W. CEILLEY, AND D. HANSON. 2015. Herpetofaunal community change in multiple habitats after fifteen years in a southwest Florida preserve, USA. PLoS One 10(5): e0125845.
[3] STUART, Y.E., T.S. CAMPBELL. P.A. HOHENLOHE, R.G. REYNOLDS, L.J. REVELL, AND J.B. LOSOS. 2014. Rapid evolution of a native species following invasion by a congener. Science 346: 463-466.
[4] SCHOENER, T.W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49: 704-726
[5] SCHOENER, T.W., AND A. SCHOENER. 1980. Densities, sex ratios, and population structure in four species of Bahamian Anolis lizards. Journal of Animal Ecology 49: 19-53.
*Cassani et al., in particular, trapped reptiles and amphibians in ground-level traps, and very likely missed many anoles. Campbell, however, did sample in arboreal habitats, and did not find this explanation compelling in the context of his study. Trees on the islands he sampled were relatively short (~6 m), “allowing the vertical habitat to be searched thoroughly with small binoculars and some healthy tree climbing.”
**The logic is this: once you’ve marked every individual in a population, you will only re-spot marked individuals and not see new individuals, and the size of your population will be equal to the number of individuals you’ve marked. In reality, you’ll almost never mark every individual, but the rate at which you spot new individuals relative to the total number of individuals you observe (new and marked) can still be revealing. Say you have two populations, A and B. If population A is much smaller than population B, then you will reach the point of mostly re-spotting marked individuals and not seeing new individuals more quickly in population A than in population B.
We obviously could not catch every lizard, and we were better at catching brown anoles than green anoles, so don’t use these data for any serious estimates of population size. But, if anything, our relative inability to catch green anoles means that there are more green anoles in this site than we document.
***Sampling for A. sagrei began about a month before sampling for A. carolinensis, explaining the mismatch in numbers between graph and text.
For decades, we anole scientists have been fascinated by the marvelous throat fans, called ‘dewlaps,’ characterizing Anolis lizards. A bunch of brilliant studies have therefore focused on the origin, evolution, diversity and function of this structure, revealing important pieces of what seems to be a complex ‘dewlap puzzle.’ And I think you all agree that the answer to what might look like a rather simple question at first, i.e., ‘what does the dewlap say,’ is not evident at all. So, with our study we aimed to add an ‘extra’ piece to the puzzle, which may help to further unravel the exact nature of information conveyed by the Anolis dewlap.
We specifically focused on what is signaled by various components of the dewlap in the brown anole and whether diverse aspects of dewlap signaling provide additive information or highlight different characteristics of the sender. We therefore measured several dewlap components involving design (i.e., dewlap area, patterning, and color) and use (i.e., dewlap extension frequency during intersexual interactions), and linked these to information a sender may need to transmit in order to increase its fitness (i.e., sexual identity, individual quality, and social status). We used several performance (i.e., bite force, sprint speed, and clinging capacity) and health state parameters (i.e., immunocompetence, hematocrit, and swelling response) as a measure of individual quality, whereas mirror-motivated aggressiveness was used as a measure of social status. Due to their fundamentally divergent reproductive roles, we expected males and females to differ with respect to what is signaled by the dewlap, and therefore performed separate analyses per sex. For the male sex, we additionally distinguished between the color of the dewlap center and edge region.
What did our results show?
First, we found that body size together with relative dewlap area and color act as redundant messages in the advertisement of sexual identity. Depending on the distance between signaler and receiver and prevailing environmental conditions, recognizing a potential mating partner based on the estimation of its body size only may be a hard task to fulfill. We therefore suggest that repeating the same message in different ways using body size together with dewlap traits is a highly appropriate strategy to get information about sexual identity accurately across.
Second, we found that dewlap coloration is primarily responsible for signaling aspects of individual quality, but only in males. Our results show that individual health state parameters are reflected in the color components of both male dewlap center and edge and that multiple different messages are conveyed by dewlap color. Specifically, we found that males bearing dewlaps with higher amounts of yellow and red and lower amounts of UV show higher body condition indexes, and that individuals with generally brighter dewlaps have lower immunocompetence. In addition, males with more yellow and UV chroma in dewlap edge only exhibit higher hematocrit values.
Surprisingly, none of the tested components of dewlap design in A. sagrei males conveyed information on performance capacities and aggressive behavior, and the same result was found for dewlap use. Also, no links were observed between components of dewlap design and use during intersexual interactions.
Third, for females, neither dewlap design nor use were related to any of the tested individual quality measurements and mirror-induced aggression. However, in contrast to males, correlations between components of dewlap design and use were found in A. sagrei females. Female individuals with larger dewlaps showed higher dewlap extension frequencies during intersexual interactions only and the same is true for individuals with less bright dewlap centers, suggesting an important signaling function of the female dewlap during courtship.
What can be concluded?
Our study confirms that the dewlap signaling device is a very complex integrated system consisting of different components transferring redundant (sexual identity) as well as non-redundant information (individual quality). We found that both the dewlap center and edge bear a signaling function, but this was only tested in males. As expected, male and female dewlaps differ in the messages they convey and further research is absolutely necessary to get insights in ‘what the dewlap exactly says’.
Driessens, T., Huyghe, K., Vanhooydonck, B. and Van Damme, R. (2015). Messages conveyed by assorted facets of the dewlap, in both sexes of Anolis sagrei. Behav. Ecol. Sociobiol. DOI 10.1007/s00265-015-1938-5
Bonnie Kircher found this image inside the cover of Florida’s Fabulous Reptiles and Amphibians. Pay close attention to the last lines of the quotation and you will realize that this is a most well-placed anole photograph. 
Battling brown anoles. Photo by Karen Cusick
Over on Daffodil’s Photo Blog, Karen Cusick has documented a knock-down, drag out fight between two brown anoles (which we have elsewhere suggested should be re-branded as “festive” anoles). Check out the dorsal and nuchal crests!
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