Anole Annals

Phelsuma laticauda steals the reptilian spotlight on Anole Annals today. This Day Gecko, alongside Anolis carolinensis and A. sagrei, are the focus of a recently conducted  comparative study by Wright et al. (2021) examining the linkage between morphology, performance, and ecology relative to the usage of adhesive digital toepads. Credit Wikimedia Commons.

New literature alert!

A new study by Wright et al. (2021) published in Functional Ecology presents the results of an ambitious and exciting experimental study comprising greater than 9,000 habitat use observations to compare how clinging performance interacts with ecology in Anolis lizards and the iconic Phelsuma laticauda (Day Gecko). The two anoles–A. carolinensis and A. sagrei–along with P. laticauda, have invaded the once squamate-free community of Hawaiʻi, providing the substrate for Wright et al. to examine the interaction between performance, morphology, and ecology.

Clinging performance on natural substrates predicts habitat use in anoles and geckos

 In Functional Ecology

Wright, Kennedy-Gold, Naylor, Screen, Piantoni, and Higham,

Abstract:

1) For arboreal lizards, the ability to cling or adhere to the substrate is critical for locomotion during prey capture, predator escape, thermoregulation, and social interactions. Thus, selection on traits related to clinging is likely strong.

2) Correlations between morphology, performance, and habitat use have been documented in arboreal lizards, providing a framework for using functional traits to predict habitat use in the field.

3) We tested the hypothesis that clinging performance predicts habitat use in an actively assembling community of introduced lizards in Hawaiʻi comprised of anoles (Anolis carolinensis, A. sagrei) and day geckos (Phelsuma laticauda).

4) We measured morphological traits (toepad area and lamellae number) and tested clinging performance on two artificial and eight natural substrates in the lab. We measured habitat use in 10 m x 10 m outdoor enclosures where habitat availability was controlled and the lizard species assemblage was manipulated to reflect all species combinations. The enclosure experiment generated more than 9,000 habitat use observations from 360 lizards.

5) Morphological traits that predict performance in Anolis were not predictive in Phelsuma, indicating that direct measures of performance are necessary for comparisons between the genera.

6) Measuring clinging performance on multiple substrates provided key insights into patterns of habitat use. While all three species performed best on an artificial smooth substrate (acrylic), performance on natural substrates predicted which texture (rough vs. smooth) was most often used by each species.

7) Performance predicted perch height use: species with the greatest clinging performance (A. carolinensis and P. laticauda) across substrates perched twice as high as A. sagrei.

8) We did not observe habitat shifts in the height or texture of perches used by any species in response to experimental manipulation of the lizard species assemblage.

9) Our results highlight the inextricable link between ecology, morphology, and performance, the importance of measuring functional traits in ecologically-relevant ways, and the potential for resource partitioning to be influenced by differences in the ability to attach to different substrates.

Anolis occultus durmiendo en una rama, por Jhan C. Salazar

He tenido la oportunidad de buscar Anolis en tres países diferentes, dos en el Caribe (Puerto Rico y República Dominicana; escribiré sobre mi experiencia en República Dominicana también) y uno en el continente (Colombia), y siempre me sorprende lo diverso que es este grupo de lagartijas. Este año, finalmente fui a una salida de campo luego de la locura de la pandemia, o debería decir durante la locura de la pandemia. Fui por tres semanas a Puerto Rico junto con el increíble grupo de colegas del Laboratorio de Losos (los de Washington University) – Dr. Kristin Winchell (la líder del equipo), Dr. Elizabeth Carlen (la nueva postdoctorado del laboratorio), Ari Miller, Ansley Petherick y yo, y otras tres personas increíbles: Sarah Swiston (estudiante de doctorado en Landis Lab de Washington University), Albert Chung (estudiante de doctorado en Campbell-Staton Lab de Princeton University) y Armando Vera (un microbiólogo de la Universidad de Puerto Rico son que nos estaba ayudando).

He estado en varias salidas de campo en el pasado trabajando con diferentes tipos de organismos, pero este viaje de campo tuvo algo especial; fue el más concurrido que he tenido. No me malinterpreten aquí, realmente disfruté mi tiempo allí. Estábamos haciendo varios experimentos (de los que oirán hablar en el futuro) centrados en las diferencias entre los Anolis urbanos y de bosque.

Ahora, hablemos del por qué estoy escribiendo esta publicación. Llegamos a Puerto Rico en agosto y nos quedamos la mayor parte del mes, alojándonos en la Reserva Natural y Estación de Campo Mata de Plátano. Desde el momento en que aterricé, sentí lo cálida y agradable que es la gente de Puerto Rico, no hay nada mejor que sentirse bienvenido. Una vez que llegamos a la estación de campo, también me di cuenta de lo mucho que me encanta estar rodeado de naturaleza y desconectado del mundo; no tenía recepción telefónica en la estación de campo.

No voy a mentir, una de las razones por las que quería ir a Puerto Rico era para ver algunas o todas las especies de aves endémicas que tiene esta hermosa isla. Vi algunos de ellos, solo para nombrar un par, vi el búho puertorriqueño o múcaro y el cuco lagartijero. Lamentablemente, no vi especies como el san pedrito o tody puertorriqueño o la cotorra puertorriqueña. Sin embargo, esta vez optamos por un tipo diferente de grupo: los Anolis, en particular Anolis cristatellus.

Aunque estábamos buscando Anolis cristatellus, este no era el único Anolis que quería ver. Había otras 9 especies que estaba buscando; lamentablemente, no fuimos a Culebras, Vieques o Mona, supongo que tendré que volver para ver los que me faltan.

En nuestro primer día de muestreo, fuimos a la ciudad de Arecibo para buscar A. cristatellus, y mientras buscábamos esta especie, vi un lagartijo de aspecto extraño con algunas manchas negras en la espalda. Fue entonces cuando me di cuenta de que acababa de divisar mi segunda especie de anole, Anolis stratulus. En la tarde de ese día, estábamos trabajando en Mata de Plátano cuando Ari dijo “Hola Jhan, hay un gigante de corona”, y yo pensé, “no hay forma de que esto suceda tan temprano en nuestro viaje de campo”; eso era cierto. Vimos un hermoso anole de color esmeralda, Anolis cuvieri. Más tarde ese día, vi mi cuarta especie, una pequeña con líneas blancas a cada lado del cuerpo, Anolis pulchellus. ¡Cuatro especies diferentes en un día! ¿Qué tan loco es eso?

No fue hasta nuestra segunda semana que encontré mi quinta especie. Esta vez estábamos en un pequeño bosque en Mayagüez. Caminábamos por el bosque y vi un lagartijo de aspecto familiar, pero no estaba seguro de qué era. Le pregunté a Ari de qué especie era y me dijo: “Ese es Anolis krugi“. En nuestros últimos días en Puerto Rico, fuimos a un par de lugares donde encontramos los anoles que me faltaban por. Nuestra primera parada fue en el Parque Nacional El Yunque; si vas a Puerto Rico, debes ir aquí, totalmente recomendado. Me impresionó lo diferente que son las montañas colombianas de las puertorriqueñas. Incluso antes de que empezáramos a caminar, alguien señaló un anole en una palmera (lamentablemente, no recuerdo quién fue), ¡y era otro anole verde! Pero esta vez fue Anolis evermanni, y una vez más me sorprendió lo fácil que es ver algunas especies cuando solían pasar semanas buscando un individuo de una especie en los Andes.

Macho adulto de Anolis cooki tomando el sol en un tronco, por Jhan C. Salazar

Cuando estábamos a punto de comenzar a caminar, escuché decir a Kristin en el fondo, “ese es Anolis gundlachi, ¡mira esos ojos azules!”. Una vez escuché esto, corrí a ver a este lagartijo; cuando lo vi, me di cuenta de que los anoles son un grupo extraordinario de lagartijas. No sabía que podían tener ojos azules, o tal vez nunca lo noté hasta ese momento. Al día siguiente fuimos a Cabo Rojo, y allí encontramos dos especies: Anolis cooki y Anolis poncensis. En este lugar, Sarah, Armando, Kristin y yo estábamos caminando por un pequeño bosque y encontramos un lagartijo gris, A. cooki, y nuevamente, me sorprendí. ¡Nunca pensé que los anoles pudieran ser grises también! ¿Qué puedo decir sobre A. poncensis? Bueno, lo vi por un breve período, es una especie rápida; cuando caminábamos, Armando gritó “¡Anolis poncensis! ¡Te dije que estaba aquí!”. Armando me señaló, pero no lo vi sino hasta que empezó a correr; luego, se detuvo por un segundo, y en ese segundo, vi lo hermosa que es esa especie, tan pequeña, pero tan rápida.

Solo me faltaba una especie, pero esta historia es única. Al comienzo de la salida de campo, estaba hablando con Armando sobre los anoles que vio cuando estaba trabajando con Anna Thonis (una estudiante de posgrado en Akçakaya Lab en Stony Brook University) solo unas semanas antes, y dijo que le faltaba por ver solo una especie, Anolis occultus – esa fue la primera vez que escuché sobre esa especie; Ni siquiera sabía cómo se veía. El día que Armando me contó esa historia, comenzamos a planear la búsqueda para encontrar esa especie. Mientras estábamos en Mata de Plátano, había otro equipo trabajando también en Anolis, y uno de ellos, Alejandro, nos dijo dónde podíamos encontrar esta especie. Esa noche Armando y yo fuimos al bosque a buscar A. occultus; comenzamos a buscarla a las 9:00 pm y regresamos a las 12:30 am con las manos vacías; no lo vimos. Unos días después, Armando fue por su cuenta a buscar esta especie ootra vez, y nuevamente, no lo encontró. Otra noche, Albert y el otro equipo fueron a buscar A. occultus y nos preguntaron a Armando y a mí si queríamos unirnos a ellos, pero estábamos cansados; Al día siguiente, Albert nos mostró una foto de A. occultus; sí, la encontraron. Le pedí a Albert que se uniera a Armando y a mí para buscar esta especie tan misteriosa; esa noche fuimos a buscarla, desde las 10:00 pm hasta casi la 1:00 am, y una vez más fuimos derrotados.

En nuestra última noche, un sábado por la noche, Armando, Ansley, Ari, Sarah y yo estábamos decididos a encontrar A. occultus. Empezamos a mirar a las 8:00 pm más o menos. Caminamos y caminamos, mirando aquí y allá, pasaron minutos y nada. Pensé que íbamos a irnos de Puerto Rico sin ver esta especie, ya las 9:25 pm – sí, registré la hora – miré una rama con algo en ella, y me di cuenta de que lo habíamos encontrado, después de todos estos intentos allí estaba, Anolis occultus. Dije “lo encontré, finalmente lo encontramos”; todos estaban emocionados, especialmente Armando. Ari dijo entonces, “debe haber más individuos alrededor”, y efectivamente, ¡Ari encontró otro! Tomamos cientos de fotos de esos dos Anolis, y fue entonces cuando me di cuenta de que en tres semanas, ¡vi las 10 especies de Anolis que tiene Puerto Rico!

Me siento agradecido de visitar y trabajar en un lugar tan impresionante como Puerto Rico, con gente cálida, y playas y comida increíbles, en particular el mofongo y Church’s Chicken (nunca hicieron bien mi pedido, pero todavía me gusta). Ojalá pueda volver a trabajar en tan hermoso lugar, pero por ahora: “Con un cariño profundo en ti la mirada fija” – poema a Puerto Rico de José Gautier Benítez.

Macho adulto Anolis gundlachi tomando el sol en un tronco, por Jhan C. Salazar

Anolis occultus sleeping on a branch. Photo by Jhan C. Salazar

I have had the opportunity to search for anoles in three different countries— two in the Caribbean (Puerto Rico and the Dominican Republic; I will write about my experience in the Dominican Republic, too) and one on the mainland (Colombia)— and it always surprises me how diverse this group of lizards is. This year, I finally went on a field trip after the craziness of the pandemic—or should I say, during the craziness of the pandemic? I went for three weeks to Puerto Rico along with the incredible Losos Lab combo (the ones at Washington University): Dr. Kristin Winchell (the leader of the team), Dr. Elizabeth Carlen (the new postdoc of the lab), Ari Miller, Ansley Petherick and me—and three other incredible people: Sarah Swiston (a grad student in the Landis Lab at Washington University), Albert Chung (a grad student in the Campbell-Staton Lab at Princeton University) and Armando Vera (a microbiologist from Universidad de Puerto Rico).

I have been on several field trips in the past working with different kind of organisms, but this field trip had something special; it was the busiest one I have ever participated in. Do not get me wrong here: I really enjoyed my time there. We were doing several experiments (that you will hear about in the future) focused on differences between urban and forest anoles.

Now, let’s talk about why I am writing this post. We arrived in Puerto Rico in August and stayed for most of the month, staying at Mata de Plátano Field Station and Nature Reserve. Since the moment I landed, I felt how warm and nice people from Puerto Rico are—there is nothing better than feeling welcome.  Once we got to the field station, I also realized how much I love to be surrounded by nature and disconnected from the world—I did not have phone reception in the field station.

I am not going to lie: one of the reasons I wanted to go to Puerto Rico was to see some or all the endemic bird species this beautiful island has. I saw a few of them—the Puerto Rican owl or múcaro and the Puerto Rican lizard cuckoo or cuco lagartijero, just to name a couple. Sadly, I did not see species such as the Puerto Rican tody or the Puerto Rican parrot. However, this time we went for a different kind of group: anoles, particularly Anolis cristatellus.

Even though we were looking for Anolis cristatellus, this one was not the only anole that I wanted to see. There were another nie species that I was looking for—sadly, we did not go to Culebras, Vieques, or Mona, so I guess I’ll have to go back to see the ones I’m missing!

On our first day of sampling, we went to the city of Arecibo to look for A. cristatellus, and while we were looking for this species, I saw a weird-looking anole with some black spots in the back. This was when I realized that I had just spotted my second anole species, Anolis stratulus. In the afternoon of that day, we were working in Mata de Plátano when Ari said “Hey Jhan, there’s a crown giant,” and I thought, “there’s no way this is happening so early on our field trip”; but it was true! We saw a beautiful emerald-colored anole, Anolis cuvieri. Later that day, I spotted my fourth species, one small with white lines on each side of the body, Anolis pulchellus. Four anoles in one day! How crazy is that?

Adult male Anolis cooki basking on a tree trunk. Photo by Jhan C. Salazar.

It was not until our second week that I found my fifth species. This time we were in a small forest patch in Mayagüez. We were walking in the forest, and I saw a familiar-looking anole, but I was not sure what it was. I asked Ari which species it was, and he said “that’s Anolis krugi.” On our last days in Puerto Rico, we went to a couple of places where we found the anoles that were missing from my checklist. Our first stop was El Yunque National Park—if you go to Puerto Rico, you should go there. I was impressed by how different the Colombian mountains are from the Puerto Rican ones. Before we even started to hike, someone pointed out an anole on a palm tree (sadly, I do not remember who it was), and it was another green anole! But this time, it was Anolis evermanni, and once again I was amazed by how easy it is to see some species when I used to spend weeks looking for even one individual of one species in the Andes.

When we were about to start hiking, Kristin said, “that’s Anolis gundlachi, look at those blue eyes!”. Once I heard that, I ran to see this anole; when I saw it, I realized that anoles are a crazy group. I did not know they could have blue eyes, or maybe I never noticed it until that moment. The next day, we went to Cabo Rojo, and there we found two species: Anolis cooki and Anolis poncensis. In this place, Sarah, Armando, Kristin, and I were walking on a small forest patch, and we found a grey anole, A. cooki—and again, I was surprised. I never thought anoles could be grey too! What can I say about A. poncensis? Well, I saw it for a brief period—it is a fast species. When we were walking, Armando yelled “Anolis poncensis! I told you it was here!”. Armando pointed the lizard out to me, but I did not see it until it started running; then, it stopped for one second, and in that second, I saw how beautiful that species is—so small, yet so fast.

I had just one species missing, but this story is unique. At the beginning of the field trip, I was talking with Armando about the anoles he saw when he was working with Anna Thonis (a grad student at Akçakaya Lab at Stony Brook University) just a few weeks before, and he said he was missing Anolis occultus—that was the first time I heard about that species. I did not even know how it looked. We made our quest to find that species. While we were in Mata de Plátano, there was another team working on anoles too, and one of them, Alejandro, told us where we could find this anole. That night, Armando and I went to the forest to look for A. occultus; we went at 9:00 pm and returned at 12:30 am empty-handed; we did not see it. A few days later, Armando went on his own to look for A. occultus, and again, he did not find it. Another night, Albert and the other team went looking for A. occultus, and they asked Armando and I if we wanted to join them, but we were tired; the next day, Albert showed us a picture of A. occultus—yes, they found it. I asked Albert to join Armando and I to look for this occult species; that night, we went to look for A. occultus from 10:00 pm to almost 1:00 am, and once again, we were defeated, with no clue where this species was.

On our last night, a Saturday night, Armando, Ansley, Ari, Sarah, and I were determined to find A. occultus. We started looking at 8:00 pm or so. We walked and walked, looking here and there, minutes passed and nothing. I thought we were going to leave Puerto Rico without seeing this species, and at 9:25 pm—yes, I recorded the time—I looked at a branch with something in it, and there it was. I realized that we had found it; after all these attempts, there it was, Anolis occultus. I said “found it, we finally found it”; everyone was excited, especially Armando. Ari then said, “there must be more individuals here,” and sure enough, Ari found another one! We took hundreds of pictures of those two anoles, and that was when I realized that in three weeks, I saw all ten anoles species that Puerto Rico has!

I feel thankful to visit and work in such an amazing place like Puerto Rico, with amazing people, amazing beaches, and food—particularly, mofongo and Church’s Chicken (they never got my order right, but I still like it). Hopefully, I will be back to work a little bit more, but for now: “Con un cariño profundo en ti la mirada fijo”—“With deep affection fixed gaze on you”—poem to Puerto Rico by José Gautier Benítez

Adult male Anolis gundlachi basking on a tree trunk, by Jhan C. Salazar.

Ground-dwelling lizard A. tandai.

From the pages of Natural History magazine.

Ivan Prates

With over 400 species of anoles (Anolis) scattered from Florida to Bolivia, these slen­der lizards, widely sold in pet stores, have long been model subjects in evolutionary biology—keys to ecomorphology, adaptive radiation, and convergent evolution. Yet there is still much to discover about them.

Jonathan Huie, a doctoral candidate at George Washington University, while an intern at the Smithsonian’s National Muse­um of Natural History, set out to determine whether the less-studied anoles of main­land Central and South America have evolved the six ecomorphs—forms adapted to microhabitats, from treetops to trunks to undergrowth—recognized in the much-studied species found on Caribbean islands.

Huie examined 347 anoles preserved in four natural history museums; they represented 205 spe­cies, 99 of them from the mainland clade. He mea­sured thirteen morpho­logical traits associated with habitats and modes of locomotion, including the lengths of tails, bodies, snouts, heads, hands, feet, and limb bones and the width of the toe and finger pads anoles use to cling to vertical surfaces. After averaging these values for each species and correct­ing for body size, he plotted their positions in a multidimensional “morphospace.” He tested their resultant assignments to eco­morphs against available field data.

Mainland anoles were previously consid­ered less ecologically diverse than their Ca­ribbean cousins. But Huie’s findings suggest they occupy all of the same microhabitats; the two groups underwent similar radia­tion—i.e., convergent evolution—over the approximately 30 million years since anoles from the islands recolonized the mainland. He also found evidence of a previously un­recognized ground-dwelling ecomorph in both groups.

Why was this mainland diversity over­looked? Perhaps because it is much easier to study anoles on the islands, which are celebrated evolutionary hotbeds where, with fewer predators, they are more abundant and visible. “Mainland anoles are a lot more secretive and inhabit more complex envi­ronments, such as heavy forest,” Huie noted.

Huie suggests the methods he and his coauthors developed could be applied to study “the relationships between form and function” in other morphological features of organisms, whether plant leaves, frog limbs, or the pharyngeal jaws of fish—especially cichlids, the fast-evolving, highly diverse piscine counterparts of anoles. (Biological Journal of the Linnaean Society)

For more commentary on this paper, see a previous AA post.

Anolis planiceps. Photo by Renoir Auguste.

Hello Anolis network,
I’m interested in networking with fellow native Caribbean-based Anolis researchers (born in the Caribbean, working or worked on anoles). I’m one (from Trinidad), and thought why not reach out to those who follow Anole Annals. If you are a current or recent grad student, or also those who have moved up the ladder to PI, please do reach out if you want to. This is geared towards having general conversations about the work you have, or are doing, and perhaps how we can all help each other and fellow/future Caribbean-based Anolis researchers in some way. Looking forward to virtually networking!
Renoir Auguste, MSc.

In a new study hot off the press at Evolution, Stuart and colleagues experimentally test the dimorphism-richness hypothesis using several mangrove islands in south Florida inhabited by Anolis carolinensis (pictured; credit Wikimedia Commons) and A. sagrei.

New literature alert!

Male and female Anolis carolinensis maintain their dimorphism despite the presence of novel interspecific competition

In Evolution

Stuart, Sherwin, Kamath, and Veen

Abstract:

Natural selection favors sexual dimorphism that reduces resource competition between the sexes of the same species. However, niche partitioning among interspecific competitors should counter such divergence, as partitioning the niche results in smaller total niche widths for each individual species, leaving less room for the sexes to diverge. A straightforward (and long-standing) hypothesis emerges: species in competitor-rich ecological communities should show less sexual dimorphism than species in competitor-poor ecological communities. Here, we test this prediction using a well-documented natural experiment generated by the recent arrival of Anolis sagrei to a set of small islands in Mosquito Lagoon, Florida, containing Anolis carolinensis. Despite known interspecific habitat partitioning and rapid evolution in habitat-use traits by A. carolinensis in this system, sexual dimorphism between male and female A. carolinensis was not reduced as predicted on two-species islands relative to islands with only A. carolinensis. This is consistent with a small but growing body of empirical tests of the dimorphism-richness hypothesis that have been ambiguous in their support at best. A rethinking of the validity of this intuitive hypothesis is needed.

Anolis sagrei (pictured) is the star of a new study by Kahrl et al. (2021) examining selection pressures on sperm. Credit Wikimedia Commons.

New literature alert!

Selection on Sperm Count, but Not on Sperm Morphology or Velocity, in a Wild Population of Anolis Lizards

In Cells

Kahrl, Kustra, Reedy, Bhave, Seears, Warner, and Cox

Abstract:

Sperm competition is a widespread phenomenon that shapes male reproductive success. Ejaculates present many potential targets for postcopulatory selection (e.g., sperm morphology, count, and velocity), which are often highly correlated and potentially subject to complex multivariate selection. Although multivariate selection on ejaculate traits has been observed in laboratory experiments, it is unclear whether selection is similarly complex in wild populations, where individuals mate frequently over longer periods of time. We measured univariate and multivariate selection on sperm morphology, sperm count, and sperm velocity in a wild population of brown anole lizards (Anolis sagrei). We conducted a mark-recapture study with genetic parentage assignment to estimate individual reproductive success. We found significant negative directional selection and negative quadratic selection on sperm count, but we did not detect directional or quadratic selection on any other sperm traits, nor did we detect correlational selection on any trait combinations. Our results may reflect pressure on males to produce many small ejaculates and mate frequently over a six-month reproductive season. This study is the first to measure multivariate selection on sperm traits in a wild population and provides an interesting contrast to experimental studies of external fertilizers, which have found complex multivariate selection on sperm phenotypes.