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Steve Arnold, snake biologist extraordinaire, has a secret love of anoles. Or at least he takes pictures of them on his travels. Here are two anoles from Pico Bonito National Park in northwestern Honduras. Anyone know what they are?

Last month I spent a week in Bocas del Toro for a marine invertebrate biology course. However, I made some obligatory terrestrial excursions in search of our favorite vertebrate, the anoles! The habitat surrounding the STRI facility was secondary forest, and anoles were most commonly seen at forest edges. On one tree I found two A. limifrons scurrying about. They both promptly flattened their bodies against the thin branches when they detected my presence. A few seconds later, I noticed that a slightly larger anole was staring right at me from several inches away. I haven’t been able to get a solid ID on this female yet, and I would appreciate any input!

Photo by Barb Karl

Everyone who has studied anoles in the field has had the experience of an anole displaying towards him- or herself. Do anoles actually display to real predators in the field? We’ve even had one AA post reporting a test of that. But there are few observations of such displays. So we were delighted to receive the following note from Barb Karl of Leland, North Carolina:

I was mowing my lawn and was startled by a green lizard that jumped to a nearby tree. I researched what type of lizard it was since we just moved to North Carolina a short while ago and wanted to see what it was.  I found that it was an anole.  I felt bad that I had startled him, so put some live mealworms on the fence as a peace offering.  I checked a little bit later and he was back on the fence, hopefully eating the mealworms.  Then a short distance away a wren appeared in the bird feeder tray.  I watched the anole, he was still on the fence and started going up and down (almost like he was doing pushups and his throat pouch would go in and out). It was like he was trying to make himself bigger so the bird would not want to mess with him.  It was an awesome sight!

I spotted a second Anole on a tree a distance away from the first one.  Can’t wait till they visit again.  Next time I will try and catch a video if it happens again.

Tobias Uller at Lund University is studying phenotypic plasticity in anoles to address the evolutionary significance of such plasticity. He’s interviewed at David Sloan Wilson’s site, This View of Life. The whole interview is interesting, but here’s the snippet on anoles:

One of my projects, with evolutionary developmental biologist Nathalie Feiner, will test if plasticity shaped diversification of Anolis lizards. These lizards are textbook examples of an adaptive radiation because, across the Caribbean, a single species gave rise to multiple species, each locally adapted to a different habitat. We are particularly interested in limb morphology since it is a defining feature of adaptive differences between species; lizards that run around on broad surfaces, such as tree trunks, have longer limbs than those who cling onto twigs, for example.

Anolis equestris. Image used with permission of Tobias Uller.

We already know from work by Jonathan Losos and others that limb growth is plastic in Anolis. What we do not know is if evolutionary diversification of limbs took place through modification of those particular components of bones that respond to mechanical stress during growth – as would be predicted if plasticity ‘took the lead’ in evolution – or if adaptive divergence between species is unrelated to plastic responses within species. To test the concordance between plasticity and evolutionary diversity we rear a lot of lizards from several species on different surfaces and combine this with detailed measures of skeletons of very many species across the entire Anolis group.

We should also remember that plastic responses in some cases can carry over to the next generation. In experiments on water fleas, which have the advantage that they can reproduce clonally so we can rear genetically identical individuals in the lab, we will test the hypothesis that such maternal effects (or non-genetic inheritance) facilitate adaptation to new environments. In some ways, this works just like plasticity within a generation. That is, successful accommodation of environmental stressors enables populations to persist and gives natural selection something useful to work with, thereby providing directionality to evolution.

But here there is another twist that has to do with the evolution of inheritance. As populations adapt, selective removal of costs and negative side-effects should make maternal effects behave like signals, sent from mothers to tell offspring about the environment they are likely to encounter. This process, therefore, describes the evolution of a type of inheritance system.

We cannot study the conversion of an environmentally induced stress response to a detection-based inheritance system in the lab. But we can compare water flea populations that have been exposed to the same stressor, such as metals or toxins, for a different number of generations in the wild. Ultimately, this should give insights into how inheritance systems evolve and how they come to transmit information.

Aposematic warning patterns are supposed to have evolved to warn potential predators to stay away. But do they work? An experimental study at the La Selva Biological Station in Costa tested that hypothesis on common ground anoles, Anolis humilis. Baruch et al., writing in the Journal of Herpetology, presented the anoles with clay models painted in an aposematic or cryptic color. The models were dangled in front of the lizards and wiggled around, simulating a flying insect. Sure enough, the lizards went after the cryptic models nearly half the time, but almost completely ignored the orange and black ones. Aposematic patterns work!

Here at AA, we love lizards with horns on the tip of their snouts. The horned anole, Anolis proboscis, is of course our favorite, but there are others. For example, Sri Lanka is home to the little known Ceratophora stoddardi. Anima Mundi, an online magazine produced by an Italian husband-and-wife team, just had a nice seven page spread on this species, which it dubs the “rhino lizard,” replete with beautiful photos and a bit of natural history information. Like the horned anole, the rhino lizard can move its horn! I wonder what would happen if they ever met. Who knows? But if you want to learn more about the rhino lizard, check out our previous post on the species.

Two years ago, the Museum of Comparative Zoology published Randy McCranie’s book on the anoles of Honduras. Now, the MCZ is soon to publish Randy’s latest work, a massive compilation on the lizards, crocs and turtles of Honduras, to be titled, appropriately enough, The Lizards, Crocodiles, and Turtles of Honduras: Systematics, Distribution, and Conservation. 

How would you like your photograph to grace the front or back of this forthcoming volume? We’re looking for beautiful photos of Honduran lizards, crocs or turtles. The front cover photo must be vertical in aspect, the back cover horizontal. We can’t offer to pay you, but we’d be happy to provide you with a copy of the volume when it appears.

Please send photos to anoleannals@gmail.com

Thanks!

Back cover of Anoles of Honduras

The use of programmable robots (‘mechanical models’ is more accurate) to minimise disturbance while observing wildlife, or to run behavioural experiments in the field, has slowly increased in the last decade and studies across many taxa have utilized this approach (Martins et al., 2005; Partan et al., 2009; Cianca et al., 2013; Macedonia et al., 2013; Clark et al., 2015). I’d argue that “robots” are one for the most important tools for behavioural ecologists studying communication or display behaviour, as they are one of the few ways in which we can conduct field-based experiments – mimicking or manipulating animal behaviour, colour or morphology in any way – in the animal’s natural environment.

We recently published a paper in the Journal of Evolutionary Biology, using robots in playback experiments to test the importance of ornament design for signal detection and conspecific recognition.

Many factors potentially affect signal design, including the need for rapid signal detection and the ability to identify the signal as conspecific. As understanding these different sources of selection on signal design is essential in the larger goal of explaining the evolution of both signal complexity and signal diversity, here we assessed the relative importance of detection and recognition for signal design in the Black-bearded gliding lizard, Draco melanopogon (fig. 1). Lizards of the species-rich genus Draco use large extendible dewlaps for communication, that differ in colour pattern and size between species – in a similar fashion to the anoles.

Figure 1 A. Male D. melanopogan, dewlap naturally extended (image a still from behavioural trials) and the angle of dewlap extension as measured from still; B. robot, dewlap treatments (Bi) solid colour and Bii) two-coloured); and C. artificially extended dewlaps of a male and female D. melanopogan.

To test whether the dewlap colour and pattern function more to facilitate 1. signal detection and 2. conspecific recognition, we presented free-living lizards with robots displaying dewlaps of six different designs, varying in the proportion of the black and white components.

In this case, our robots were just ‘visual flags’ that mimicked the dewlap size and shape, as well as the speed and display pattern of live Draco melanopogan lizards (video 1). Having only the dewlap / visual flag and not the rest of the lizard body allowed us to look solely at the salience of the dewlap colour and pattern itself – without adding any identifying or qualifying information in the form of a body.

Video 1: ‘The floating dewlap’

Our experiment had six colour treatments ranging from “natural” (population typical design, fig. 1) to unnatural (wrong colour, no pattern) – and from very conspicuous (high internal contrast and high contrast against the background for each colour) to very inconspicuous (matching the luminance of the background). Thus, we could test both the ‘detection’ and ‘conspecific recognition’ hypotheses with the same set of treatments.

Predictions for Hypothesis 1: We predicted that should the dewlap colour pattern function in signal detection, that more conspicuous dewlap treatments would be detected sooner than less conspicuous dewlaps. Each of the two-coloured treatments were more conspicuous than the single-coloured treatments, as they had the same high contrast black and white elements, but they also had the high internal contrast of the black against the white (75.02 JND). Provided the receiver has sufficient visual acuity at the viewing distance to be able to distinguish the two colours from one another, internal contrast increases signal conspicuousness, and the more equal the two adjacent colour patches are in size (i.e. 50% of the dewlap black – 50% of the dewlap white) the greater the internal contrast. There is no existing data on the visual acuity of Draco lizards, so for this experiment we stuck to the natural dewlap size and viewing distances, with small oscillations around the natural proportions of black and white.

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Habitat characteristics influence the efficacy of animal signals, which means that populations of the same species occurring in distinct habitats are likely to show differences in signal structure as a form of local adaptation. This kind of variation in signal structure has been well-studied for sound and colour signals, including in several species of anoles, but had not been reported for motion-based signals until recently.

Jacky dragons (Amphibolurus muricatus) are Australian agamid lizards well-known for the complex motion-based displays performed by males. These displays comprise five distinct motor patterns utilised in sequence: tail flicks, backward limb wave, forward limb wave, push up and body rock (A. muricatus display video). A study conducted by Barquero et al. (2015) found evidence of temporal and structural variation in the core display of three populations of A. muricatus. These differences were not related to genotypic differences between populations, so they suggested they might be a consequence of local habitat structure.

The Jacky dragon

Concurrently, Richard Peters and I were developing a methodology to accurately quantify the effect of background noise on the motion based signals of different Australian agamids (see Ramos & Peters 2017a; b). Our approach calculates the speed distributions of the motion produced by lizard signals and the environmental noise independently. It then compares these distributions to obtain a measure of signal-noise contrast. This is accomplished by recording lizard behaviour and reconstructing its motion in three dimensions before comparing it against the motion produced by the surrounding windblown plants, which are the main source of noise for motion based lizard signals. This methodology stands out from other approaches for quantifying motion signals because it does not assume that the camera is ideally placed when recording the displays, but instead provides an accurate representation of the motion from any angle or viewing position.

Building upon the work by Barquero et al. (2015), we applied our novel approach to a couple of populations of Jacky dragons with distinct habitat characteristics. Croajingolong National Park in Victoria (Australia) is densely vegetated coastal heath with tall grasses and shrubs on a sandy substrate. Conversely, Avisford Nature Reserve in New South Wales (Australia) is mostly open woodland with an understory of scattered grasses and small shrubs, and rocky outcrops spread throughout the park.

The habitats of (a) the Jacky dragon. (b) Croajingolong National Park, in coastal Victoria, Australia. (c) Avisford Nature Reserve, in New South Wales, Australia.

Our results revealed that lizards from the densely vegetated habitat (Croajingolong NP) performed displays of longer duration and introductory tail flick components, and also produced a significantly greater amount of high speeds. However, when we calculated the signal-noise contrast for both populations at their respective habitat, we found no difference. This means that the signals from both populations are equally effective when used within their intended habitat, regardless of their structural differences.

Differences in signal structure between populations. (a) Mean bout and tail flick durations for both lizard populations. (b) Mean tail flick to bout ratio for both lizard populations. (c) Average kernel density functions for both lizard populations.

As mentioned before, our approach records animal signals and environmental noise independently, which allowed us to consider signals not only in the environment where they were filmed, but also in the habitat of the other lizard population. Consequently, to highlight the effects of the environment on lizard signals, we calculated signal-noise contrast for the signals belonging to one population in both habitats (densely vegetated vs. open woodland). As expected, both lizard populations performed worse in densely vegetated habitat, probably because the complex understory is producing greater motion noise and negatively affecting signal efficacy. Another way of looking at these data, but this time focusing on the displays rather than the habitat, was to compare the signal-noise contrast of both lizard populations in a single habitat. Lizards originating from the densely vegetated habitat produced higher contrast scores in both habitats, indicating that their displays are more effective overall.

Taken together, our results are consistent with the local adaptation hypothesis. Lizards from Croajingolong NP produce displays with longer durations and characterised by faster speeds in order to communicate effectively in a dense and noisy habitat. Conversely, lizards from Avisford NR have adapted to a less noisy environment and do not require such lengthy or energetically expensive displays. Such population level differences in signal structure due to habitat variation represent novel findings for motion-based lizard signals.