More Evidence Of Seed Dispersal In Anoles

Anolis porcatus is the most recent Caribbean anole to have been documented to consume and disperse seeds. Natural history research by Armas (2022) observes A. porcatus feeding on West Indian holly, and finds successful germination of the fecal pellets. Credit Thomas Brown (Wikimedia Commons).

Recent research on Anolis lizards has suggested their omnivorous tendencies might aid in the dispersal of seeds. Most recently, this was discussed by Giery et al. (2017), who reported Cuban Knight Anoles (A. equestris) to consume and disperse royal palms. This year, Armas (2022) reports Anolis porcatus consumes and disperses West Indian holly. Check it out!

New literature alert!

Consumption and Dispersal of West Indian Holly (Turnera ulmifolia, Turneraceae) Seeds by Cuban Green Anoles, Anolis porcatus (Squamata: Dactyloidae)

In Reptiles & Amphibians

Armas (2022)

Literature Cited:

de Armas, L. F. (2022). Consumption and Dispersal of West Indian Holly (Turnera ulmifolia, Turneraceae) Seeds by Cuban Green Anoles, Anolis porcatus (Squamata: Dactyloidae). Reptiles & Amphibians, 29(1), 115-116.

Giery, S. T., Vezzani, E., Zona, S., & Stroud, J. T. (2017). Frugivory and seed dispersal by the invasive knight anole (Anolis equestris) in Florida, USA. Food Webs11, 13-16.

How Do Anole Species Tell Each Other Apart?

When it comes to finding a mate or defending a territory, animals need to recognise members of their own species. The reasons are intuitive: you only want to mate with your own species to ensure viable offspring, and you should only invest the effort in being territorial when confronted by rivals from your own species. There are exceptions and these are interesting—hybridization or territorial competition between species—but generally animals need a system for species recognition.

The large, often spectacularly coloured throat fan or dewlap of anoles seems like an obvious way to evaluate species identity. Taxonomists have historically thought so, too. Each species appears to display a dewlap that’s unique in colour and pattern. But there are various Anole Annals posts highlighting this is not always the case. Instead, the colour of the dewlap is often an adaptation to the light environment for enhancing the detection of territorial displays.

So what about those territorial displays? Might anoles use the complex movements of the head-bob and push-up display to figure out species identity?

Classic work by Charles Carpenter and Tom Jenssen revealed how often the head-bob movements of lizards, and anoles in particular, seemed specific to each species. Pioneering experiments using video playback by Joe Macedonia in the ’90s has also provided evidence that anoles are able to distinguish displaying rivals of their own species from those of other species. But what is it about the pattern of movements used in the head-bob and push-up display, or even how the dewlap is extended and retracted, that conveys species identity? Is there one feature that varies the most among species that anoles commonly rely on to identify species?


Display-Action-Pattern graphs (above) showing the complexity of movements used by Puerto Rican anoles for territorial advertisement displays

These are hard questions to answer. Anole displays are complex, using many different types of movements, so there’s a huge number of possibilities. One approach would be to isolate and manipulate each type of movement and use video or robot playbacks to ask the anoles themselves. But doing that would take an entire career. There are a seemingly infinite number of combinations to consider. In fact, it would be impossible without a way to narrow things down.

Claire Nelson is a creative (and courageous!) graduate student who had an eye for solving the challenge. She figured it was possible to leverage the large archive of footage I’d accumulated over many, many years. These videos were of free-living male lizards performing territorial advertisement displays. Her idea was to develop an objective method for identifying which movements used in the head-bob, push-up or dewlap display had the potential to convey species identity. She’s just published her solution in Animal Behaviour.


Claire (above) doing a balancing act with some non-anoles

Claire used this archive of display videos to create Display-Action-Pattern graphs, a method developed by Carpenter back in the 60s. These track the up-and-down movement of head-bobs and push-ups as well as the extensions and retractions of the dewlap during the territorial display. To keep it manageable, she limited her efforts to anole species on Puerto Rico, and graphs of about 10 territorial advertisement displays per male. But there was an important biological reason for selecting this number of displays as well. It effectively mimicked the number of displays an anole might typically see on first encountering another lizard. That is, anoles likely make judgements on species identity from only a handful of displays.

From these Display-Action-Pattern graphs, Claire took a host of measures, ranging from the duration and number of movements used, to variation in amplitude and pauses between movements. She also noticed that anoles tend to perform certain combinations of movements together in what she came to call ‘motifs.’ After many many hours of effort, Claire accumulated a huge amount of data for nearly 20 different types of display movement for eight Puerto Rican Anolis species, and in many cases, for different populations of the same species.

Claire asked me for advice on how to analyse it all. I have to admit I was completely useless on this front. I muddled something about using coefficients of variation and some other nonsense, but really I had no idea. I was still in shock over how much data she had accumulated, and the novelty (and implications) of discovering motifs in the displays. She knew what she was doing, though. Her analytical solution was vastly superior to anything I could have suggested.

Claire investigated a variety of approaches, but in the end she settled on the method of random forest tree classification. It’s a sophisticated machine learning algorithm that, in a nutshell, takes data and groups like with like. It doesn’t require any prior direction or preconceived notion on how data should be grouped. It just uses the variation in the data itself. You could view the algorithm as an anole brain using basic rules of variation to make judgements on which displays are likely to be different and which displays are likely to be the same.

The outcome was impressive. The algorithm correctly assigned the vast majority of lizards to their correct species based on just a handful of displays. Where errors occurred, it was partly because lizards were assigned to the right species, but the wrong population. This means anoles from different populations tend to share some display features because they’re still from the same species. Yet the algorithm was able to correctly assign most lizards to the right population. In other words, there was still enough variation in the displays between populations of the same species to identify them as belonging to separate populations. This is very interesting!

Random forest tree classification (above) can assign over two thirds of displaying lizards to their correct species.

The evolution of new species begins with individuals of the same species starting to segregate from each other in some way. Often it’s physical separation (on opposite sides of a mountain range), but changes in social signals can also prompt behavioral separation as well. This could be the case for some anoles on Puerto Rico. Once individuals stop recognising each other as the same species, they no longer reproduce with one another, and the door to speciation is propped open.

The other discovery Claire made was the apparent lack of any common display feature that could be used to identify species (and population identity). Instead, different features were important for different species. The duration and number of headbob movements were features that could be used to identify the territorial displays of Anolis poncensis—a species that is striking in its use of lots of extremely rapid, up and down body movements—whereas the way the dewlap was extended was influential in identifying different populations of Anolis gundlachi—a species that has an unusually long dewlap display. Other species like Anolis pulchellus and Anolis krugi were best identified by effectively considering features of the entire territorial display.

Whether or not anoles actually use the features identified by the algorithm in species recognition remains an open question. But Claire has managed to identify the potential candidate cues that could be used. It is now possible to develop a focussed research program to test whether, and how, anoles used these features to identify species. Again, the obvious way to do this would be to ask the lizards themselves using robot playbacks.

Random forest tree classification sounds awfully complicated, and it is very sophisticated, but it’s actually easy to implement. Any dummy can do it. I taught myself how and wrote a step-by-step tutorial so you can as well. We’ve published this tutorial alongside Claire’s paper in Animal Behaviour. Give it a whirl!

How Many Anoles Are There in Captivity (Pets, Zoos, Labs) Worldwide?

Photo from http://www.petworldshop.com/

Nigel Rothfels, a historian of animals and culture at the University of Wisconsin-Milwaukee, asks:

Given the previous AA post on anoles in the pet trade, the amount of in-country breeding there must be of anoles, the general life-span of anoles, and the general growth in pet-keeping since Covid, what is your highly educated guess on the number of anoles currently being kept in captivity world-wide (as pets, for educational supply companies, in labs, or zoos).  With 350,000/year being collected in just Louisiana in 2006, it makes me think that something like 3-5 million might still be an underestimate.

 

Anyone want to venture an estimate?

Shape Variation of the Pectoral Girdle of Anolis Ecomorphs

The first three paragraphs of Jane Peterson’s contribution to the Second Anolis Newsletter.

Jane Peterson’s contribution to The Second Anolis Newsletter remains one of the most comprehensive exemplars of functional-morphological research of the anoline appendicular girdles. In just a few short paragraphs Peterson (1974) outlined the key differences in pectoral girdle morphology between the Anolis ecomorphs, drawing information from both field observations and anatomical dissections of anoles from all four Greater Antillean islands. The outlined study could have formed a major contribution to our understanding of ecomorphology, had these brief observations ever been expanded into a scientific publication. Sadly, they remained as notes, confined to a brief communique on an informal basis (that continues to be formally cited). Several intriguing studies hence have examined anole appendicular morphology, but rarely allowed for implications that reach across multiple island radiations (e.g. Anzai et al. 2014, Herrel et al. 2018).

With my 2016 Ph.D. thesis, I set out to quantify what Jane Peterson had observed forty years prior, and must confess that I still fall short of reproducing the multitude of implications that Peterson’s (1974) brief descriptions alluded to. Instead of combining video-recorded movement cycles with morphological descriptions, my comparisons are solely based on three-dimensional shape analysis of the skeletal elements that comprise the breast-shoulder apparatus (BSA): the clavicle, interclavicle, presternum, and scapulocoracoid (Fig. 1). Employing the power of computed tomography scanning, and geometric morphometric analysis, I quantified the shapes of the central elements of the pectoral girdle, and compared these across anole radiations.

As with earlier work, I focused on the Jamaican ecomorph representatives, and sought out their ecomorph counterparts from Hispaniola and Puerto Rico, particularly targeting those species that are the most and least similar to the Jamaican forms. That last line of thought did not reveal any straightforward answers, as the complex structural shape of the BSA allows these anoles to be relatively distinct in some aspects, while being quite similar in others. For example, the general shape of the presternum and interclavicle are quite similar between the two trunk-ground anoles Anolis lineatopus (Jamaica) and A. gundlachi (Puerto Rico), while that of the scapulocoracoid differs quite remarkably between the two. These complex associations will take a more detailed analysis than what is warranted here, so I’ll focus on the bigger picture instead.

Fig. 1: BSA of Anolis baleatus

Fig. 1: CT-rendition of the skeletal components of the breast-shoulder apparatus of Anolis baleatus in lateromedial view, depicting all anatomical features described in the text. The gray arrow denotes anterior.

Skeletal elements of the BSA in isolation

Previous analysis of the scapulocoracoid in isolation revealed that its shape differs between Anolis habitat specialists, and resembles a particularly dorsoventrally tall shape in twig anoles (Tinius et al. 2020). The other ecomorph groups (trunk-ground, trunk-crown, and crown-giant) show obvious tendencies towards a particular structural organization, but in none of these does the scapulocoracoid resemble a truly characteristic shape.

The New Yorker Features an Anole Cartoon

John David Curlis

Where do you work and what do you do?

 I am currently a graduate student at the University of Michigan, but I conduct most of my research in the tropics of Central and South America. I am broadly interested in trying to answer the question of how to explain patterns of phenotypic diversity found in nature, especially in the context of color and signaling. In other words, why do organisms look the way they do – why do they have certain colors over others, and what sort of information are they conveying by showing off those colors? When not focusing on my research, I spend virtually all of my free time photographing as many animals as I can find, as well as spending countless hours sorting said photos into their respective taxonomic groups. What can I say, I’m a biodiversity nerd!

What aspects of anole biology do you study, and what have you learned? 

I study the evolution of color in anole dewlaps. Even with over 400 species, all anoles possess this extendable throat fan, and it’s often brightly colored. Although we have some understanding of how the dewlap functions as a signal (e.g., species recognition, competitive interactions, courtship, predator avoidance/deterrence), it remains unclear why there are so many different colors of dewlaps. To try to tackle this question, I am looking at how the evolution of these colors may be influenced by the light environment. Since the reproduction and/or survival of an anole can depend on whether its dewlap is serving as an efficient signal, it’s easy to see how the light environment might determine which colors are favored by selection. For instance, a bright orange dewlap would likely show up much better than a dull green one under the dense canopy of the rainforest, just as a pitch-black dewlap would probably be an excellent signal in a bright, open field. I am testing this idea using an experimental island study in the Panama Canal. My study species is the Panamanian slender anole, males of which can have a mostly orange dewlap or a mostly white dewlap. By introducing these lizards onto a multitude of very tiny, highly variable islands in the canal, I can test which color will “win out” over time in different light environments. 

How and why did you start studying anoles? 

 I have loved reptiles since I was a child, so it was by no coincidence that the very first lab I worked in as an undergraduate had a breeding colony of anoles. While there, I studied physiology and metabolic rates. While I can say that metabolism work is not for me (shout out to the scientists who love it!), I very much enjoyed taking care of and working with the anoles, so I decided to stick with them throughout my undergraduate and graduate career.

What do you love most about studying anoles? 

 As someone interested in color, I think that dewlaps are anoles’ coolest feature. I love studying anoles and their dewlaps because I am constantly amazed by the astounding amount of diversity in this little flap of skin. In addition, as a researcher, it’s hard to complain about the incredibly high abundance and ease of capture for many of these species.

What is your favorite anole species? 

My favorite anole species would have to be the Meyer’s anole, Anolis johnmeyeri (named after the scientist, not the singer). This species, found in Honduras, has an absolutely gorgeous dewlap in both males and females. While large, colorful dewlaps are possessed exclusively by males in many anole species, female Meyer’s anoles have a dewlap that’s almost as large and equally as beautiful. Female dewlaps are bright yellow with a brilliant blue spot, and male dewlaps are bright red with the same blue spot. 

Where can people learn more about you and follow you online? 

Website: www.colorinnature.org

Instagram: @johndavidcurlis

SICB 2022: Ecological and Genetic Basis of a Sexual Signal

This year at SICB, I had the great opportunity to talk about part of my work as a postdoctoral researcher in the lab of Dr. Michael Logan at the University of Nevada, Reno. In collaboration with John David Curlis (University of Michigan), Christian Cox (Florida International University), W. Owen McMillan (Smithsonian Tropical Research Institute), and Carlos Arias (STRI), we have been studying the Panamanian slender anole Anolis apletophallus, which has a dewlap polymorphism: males either have a solid orange dewlap (solid morph) or a white dewlap with an orange spot (bicolor morph). Preliminary results from John David Curlis’ PhD dissertation research suggests that, in our mainland study population, the frequencies of these morphs change in conjunction with understory light levels—the solid morph is more frequently observed in brighter areas where more light reaches the understory, whereas  the opposite is true for the bicolor dewlap, which is more frequently observed in darker areas of the forest. Thus, it seems possible that selection is maintaining this polymorphism following the predictions of the sensory drive hypothesis, which states that sexual signals should have characteristics that make them the most transmissible given the physical characteristics of the local habitat.

As part of an effort to understand how this trait is evolving in the wild, I set out to understand the genetic basis of this dewlap polymorphism. To do this, my collaborators and I first assembled the full slender anole genome which we then used as a reference for a pooled population sequencing (Pool-Seq) approach using half individuals with solid dewlaps and half individuals with bicolor dewlaps to identify the genomic region underlying this dewlap polymorphism.

Our genome assembly showed pretty good results (Scaffold N50 154,613,287). The Pool-Seq results presented a clear peak of differentiation between solid and bicolor morph groups that corresponded to a region on Scaffold 3. We have a promising candidate gene within this region that may underly the dewlap polymorphism, but will continue to explore these data further to understand the genetic basis of this charismatic trait.

Making the Fancy Feet of Anoles and Geckos

A mourning gecko (Lepidodactylus lugubris) climbing vertically on glass with the help of its impressive toe pads.

I think most people visiting Anole Annals could argue that the adhesive digits of anoles are some of the most fascinating aspects of their biology (or maybe I’m just biased). Digital adhesion is accomplished through toe pads: a collection a broad, modified plantar scales which bear thousands upon thousands of microscopic, hair-like structures (i.e. setae). Through frictional and van der Waals forces, these collections of setae allow toe pad-bearing lizards to easily access vertical surfaces and exploit habitats many lizards cannot. Shockingly, adhesive toe pads have independently evolved several times across lizard evolutionary history (at least 16 times by recent estimates) — once in the common ancestor of anoles, once in a clade of southeast Asian skinks, and 14 times in geckos. Both within and between the different evolutionary origins of toe pads, there is substantial variation in toe pad size, shape, number of scansors/lamellae, and position of the adhesive apparatus.

In our recent study, my collaborators and I took the first steps to characterize how embryonic development is modified to achieve this incredible diversity. Using embryonic material my coauthor Thom Sanger collected as a postdoctoral researcher in Marty Cohn’s lab, in addition to embryonic material I collected over the course of my Ph.D. training in Tony Gamble‘s lab, we aimed to compare embryonic digit development of ancestrally non-padded lizards with that of anoles and padded geckos. We used a model clade approach to broadly sample anoles and geckos, although some species breed more easily in the lab and have more embryological resources than others. All together, we sampled a range of toe pad morphologies in both clades (trunk-ground and trunk-crown Anolis ecomorphs and leaf-toed and basal pads in geckos). To help polarize the developmental changes leading to the origin of toe pads, we also included two ancestrally padless species in our comparisons. After the collection of these diverse embryos, we used scanning electron microscopy (SEM) to characterize scale morphology of the digits throughout embryonic development.

By comparing embryonic material of anoles and geckos, we essentially span the diversity of squamates in a single comparison.

Because of the ~200 million year divergence between anoles and geckos and dramatic differences in adult morphology, we anticipated that we would see stark differences in the developmental origins of toe pads in these species. To our surprise, we found striking similarities in toe pad development between all of the pad-bearing species we examined. We found that toe pads develop after digit webbing recesses. In all pad-bearing species, ridges that become the adhesive scansors and lamellae first form in the distal half of the digit. Throughout development, new ridges begin forming in the proximal direction while the previous ridges begin to grow laterally. Elaborations and derivations in toe pad form, such as bifurcation, occur in the latter-half of embryonic development. The presumably ancestral pattern of plantar scale development we observed in our leopard gecko and fence lizard embryos (both species lacking adhesive digits) demonstrated that scale ridges form all at once along the length of the digit. These differences are similar to those documented between developing non-padded gecko tails and padded tails of crested geckos. This means that anoles and geckos have converged on a similar developmental process! We suggest that toe pads are initially formed through a major repatterning of digital development and then variation is achieved through relatively minor “tinkering,” through either timing or location of developmental patterns.

Scanning electron micrographs (SEMs) of embryonic lizard digit development, progressing from early development (left) to late development (right). The pad-bearing brown anole (Anolis sagrei) and mourning gecko (Lepidodactylus lugubris) have converged on scansor ridges forming in a distal-to-proximal direction, while the paddles leopard gecko (Eublepharis macularius) has scale rows forming all at once along the length of the digit. Lizard photos courtesy of Dr. Stuart Nielsen.

This is by no means the end of this story. We’ve just scratched the surface and there are a several directions to head in. A logical next step is to characterize histological organization through toe pad development. From there, characterizing the genes involved in toe pad morphogenesis, in tandem with the possibilities of new gene editing technologies, would allow us to test mechanisms of toe pad formation and how variation is generated. And, of course, characterizing toe pad development in other species (such as the secondarily padless Anolis onca) may elucidate further conservation or derivation from the trends we found. This is an exciting time to be a toe pad biologist!

Joe Macedonia

Where do you work and what do you do?  

 I’m a retired Associate Professor at Florida Southern College in Lakeland, FL. While at FSC from 2007 through 2016, I conducted research and taught courses in animal behavior, zoology, evolution, and ecology, as well as a capstone course in undergraduate research. I also took students to Jamaica and Bermuda to conduct field research on anoles.

What aspects of anole biology do you study, and what have you learned? 

 I’ve worked mainly on the production and perception of color and motion displays. Most of this research has been conducted collaboratively with my colleague Dave Clark and has been experimental in nature, e.g., video playbacks and anole robots. Leo Fleishman’s work on Anolis sensory ecology has been a major influence on my thinking about how lizards perceive their color displays. I’ve learned that working on anole behavior can be challenging and that, in fact, most experiments fail! But I’ve also learned that it is well worth the effort in the end.

How and why did you start studying anoles? 

 When I was a kid growing up in the 1950’s and 1960’s in central Pennsylvania, individual Anolis carolinensis used to be sold at the circus in little “animal cracker” boxes. I still remember bringing one home. My father built a small cage for it and tirelessly caught insects for it. Much later, as a postdoc at U.C. Davis in 1992, I was reintroduced to magic of anoles by none other than Jonathan Losos. At that time, Jonathan was a postdoc with Tom Schoener and heard about the video playback work that we were doing in Peter Marler’s Lab. Jonathan was interested in figuring out two things: First, would anoles respond to video recordings of other anoles displaying? And second, if they did respond to video, could anoles discriminate conspecific from heterospecific displays? With our Marler Lab colleague Chris Evans, we showed that A. marcanoi males spent more time displaying in synchrony with video clips of conspecific male displays than heterospecific male (A. cybotes) displays. Soon after that, Judy Stamps and I conducted an even more successful video playback experiment on species recognition, in which we used Anolis grahami from Jamaica as subjects.

What do you love most about studying anoles? 

 What’s not to love? I recall Chris Evans calling them “magnificent beasts”, as well as Duncan Irschick referring to them as “mini gods”. Anoles are endlessly fascinating, and you could never run out of species to research.

What is your favorite anole species? 

 Regarding species that I’ve worked with personally, Anolis grahami is probably my favorite. They are reliable performers in behavioral experiments and are always up to the challenge of responding to another anole (or a video of one, or an anole robot!). There are two runners up, however. Anolis conspersus with its blue dewlap (actually a UV-reflecting dewlap whose wavelengths extend into the blue range) is quite photogenic, as a number of contributors to Anole Annals have noted. The other runner up would be Anolis extremus. Their complex color pattern is exceptional, and although they are frustratingly squirrelly to approach in the field, male tail lifting contests can be spectacular. Anolis extremus really are extreme!

Where can people learn more about you and follow you online? 

Website: www.macedonialab.com

Lindsey Swierk

Where do you work and what do you do?  

I am an Assistant Research Professor in the Department of Biological Sciences at Binghamton University, State University of New York. I am also the Associate Director of Research of the Amazon Conservatory for Tropical Studies, outside Iquitos, Peru. My research group studies ecology at the organismal level, with a focus on behavior and herpetology. I primarily conduct fieldwork in Costa Rica and Peru. At the university, I teach courses in animal behavior and ecology, and I am involved with initiatives to promote underrepresented students in biology. I was a postdoctoral fellow at Yale University and received my PhD in Ecology from Penn State in 2013.

What aspects of anole biology do you study, and what have you learned? 

 My background in behavioral ecology first nudged my interest in anoles towards communication and reproductive behavior. I have a particular interest in understanding how sexual signals function and evolve. My group studies anole dewlaps and their costs and benefits. The use of color and patterns, both on the dewlap and the entire body, is also a focus in my group. We use both observational and experimental techniques to better understand how anoles use sexual coloration and behavioral displays to maximize fitness. We’ve found that there are some significant risks posed by bearing conspicuous sexual signals, and that there is a variety of ways in which body color can be used plastically to benefit anoles.

Our work is based on natural history observations, and so we tend to follow where the anoles lead. Lately, that has led us down the path of examining their antipredator adaptations. We are investigating the fascinating underwater diving and rebreathing behaviors of the semi-aquatic anoles, from ecological and physiological perspectives. We documented that some semi-aquatic anole species spend considerable time underwater when pursued. Our interest in antipredator strategies includes a focus on the mechanics of escaping predators, whether that is by swimming, diving, running, or leaping. Semi-aquatic anoles are also remarkably cold tolerant and have very low body temperatures, and so we also investigate their thermal ecology and possible effects of climate change. 

How and why did you start studying anoles? 

 Allergies, initially! I kept anoles as pets almost my entire childhood because a cat or dog was out of the question. Back then, I spent an embarrassing number of hours just watching what anoles did in their tanks. This cemented anoles in my head as the coolest possible lizards Years later, after spending all of my research life studying other cool herps, I stumbled upon anoles again on a teaching trip to Costa Rica. From the moment I saw Anolis aquaticus in the streams, they completely captured my attention. Their habitat and behaviors were so unique from what I had learned about anoles, I knew I had to make them a priority.

What do you love most about studying anoles? 

Two things. Their remarkable adaptations – how evolution has so astoundingly shaped them to particular environments. I love how much is known, but also how much is still unknown about their morphological, physiological, and behavioral traits – I love the element of surprise! Second, I’m still fascinated by simply watching their interactions with one another, which I could do for hours. 

What is your favorite anole species? 

 I absolutely have a favorite – Anolis aquaticus. They’re such quirky representatives of the mere handful of semi-aquatic anoles out there.

Where can people learn more about you and follow you online? 

Website: www.lindseyswierk.com

Twitter: @LindseySwierk

Instagram: lindseyswierk

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