Author: Jhan Salazar

Cuando era estudiante de pregrado en Colombia, estaba tratando de decidir qué hacer para mi tesis. En Colombia—o al menos en mi alma mater, la Universidad Icesi—es obligatorio hacer una tesis para graduarse. Durante ese tiempo, me encontré con tres de mis artículos favoritos: Janzen (1967), Ghalambor et al. (2006) y Muñoz et al. (2014). Después de leer estos artículos, una pregunta surgió en mi mente: ¿Pasa lo mismo en los Andes? Específicamente, ¿la tolerancia al frío disminuye con la elevación mientras que la tolerancia al calor permanece sin cambios?

Compartí esta idea con mis mentores de tesis, María del Rosario Castañeda y Gustavo A. Londoño, y les dije: ¡Quiero hacer esto! Quiero ver cómo los límites térmicos y la rango la tolerancia térmica varían con la elevación tanto dentro como entre las especies de Anolis.

Para abreviar, recolecté datos sobre tolerancia al frío y al calor para 14 especies de anolis en cinco sitios diferentes de Colombia. Sin embargo, debido a restricciones en la Universidad Icesi, solo pude utilizar datos de cuatro especies para mi tesis. Avancemos un año atrás, cuando estaba discutiendo este conjunto de datos con mi mentor de doctorado, Jonathan Losos. Me dijo: deberías usar estos datos para uno de tus capítulos de doctorado. Así que lo hice. Ahora, está publicado en el Evolutionary Journal of the Linnean Society: Salazar et al. 2024.

Ahora, hablemos uno de los Anolis de los Andes colombianos. La mayor parte de lo que sabemos sobre la fisiología térmica de anoles proviene de Anolis caribeños. Hay una notable falta de información sobre los límites térmicos de los anoles que habitan en los Andes. Solo un puñado de artículos se ha publicado sobre este tema: Méndez-Galeano y Calderón-Espinosa 2017, Méndez-Galeano et al. 2020, Montoya-Cruz et al. 2024 y Pinzón-Barrera et al. 2024. Sin embargo, la mayoría de estos se centran en una sola especie.

Entre 2016 y 2017, varios estudiantes de pregrado y yo visitamos cinco localidades diferentes en Colombia para medir la tolerancia al frío y al calor en los anoles andinos. Pasamos casi siete meses en el campo durante un año y medio. Medimos 367 individuos—machos, hembras y juveniles—de 14 especies a lo largo de dos clados: Draconura (cinco especies) y Dactyloa (nueve especies) a lo largo de un gradiente de elevación (200–3000 m). Nuestro estudio abordó dos preguntas clave:

1. ¿Cómo predice la variación térmica a través de la elevación la evolución de dos rasgos fisiológicos clave en los ectotermos tropicales del continente?
2. ¿Cómo ha evolucionado la fisiología térmica en la radiación andina de los anoles?

Antes de adentrarnos en los resultados, permítanme compartir algunas historias de campo. Si alguna vez han buscado Anolis en el Caribe o en los Andes, sabrán lo desafiantes que son. Antes de mis saludas de campo, Rosario me llevó en una de las suyas para enseñarme lo básico. Pasamos unos días en el campo y encontramos un par de lagartijas. En ese momento, pensé: ¡Nunca voy a encontrar suficientes lagartijas para escribir una tesis!

Encontrar anoles en los Andes es difícil. Durante el día, casi son imposibles de ver, y si logras ver uno, atraparlo es otra historia. Como rara vez tuvimos éxito durante el día, cambiamos a trabajo de campo por la noche. Incluso entonces, en algunos lugares no vimos lagartijas durante días. Para maximizar la colecta de datos, decidí capturar y medir a cada individuo que encontrase y evaluar si la lagartija era lo suficientemente grande o saludable para ser medida.

Caminando por la noche en los Andes colombianos; Parque Nacional Natural Tatamá – 2000 m. El anole que tengo en la mano es un Anolis princeps, mi especie favorita.

Aquí va una historia adicional: Rosario una vez me contó lo diferente que era atrapar Anolis en el Caribe. Dijo que allí es más fácil verlos y atraparlos, e incluso puedes decidir en el momento cuál medir. No le creí—hasta que me uní a Kristin Winchell en la República Dominicana. ¡Nunca había visto tantos anoles en un solo lugar—fue increíble! Aún así, me encanta buscar anoles en los Andes, aunque sea más desafiante. No estoy seguro de por qué, pero los Andes siempre tendrán un lugar especial en mi corazón—quizás porque uno de mis sitios de campo está a solo 30 minutos de la casa de mis padres, probablemente nunca lo sabré, jaja.

¿Qué encontramos? Como esperábamos, descubrimos que la tolerancia al frío (CTmin) y la tolerancia al calor (CTmax) aumentan con las temperaturas ambientales y operativas, pero disminuyen con la elevación. Sin embargo, contrariamente a lo que han reportado otros estudios, la tolerancia al calor no permanece sin cambios con la elevación. A diferencia de sus contrapartes caribeñas, los anoles andinos no parecen usar un mecanismo de regulación conductual para limitar la divergencia en la tolerancia al calor a través de las elevaciones—un fenómeno conocido como el efecto Bogert (Muñoz et al. 2022). Es posible que los anoles andinos no regulen su temperatura conductualmente de la misma manera que lo hacen las especies caribeñas, aunque esto aún requiere más investigación (pero véase Méndez-Galeano y Calderón-Espinosa 2017).

También encontramos que la tolerancia al frío y al calor evolucionaron a tasas similares. El análisis filogenético reveló que los límites térmicos pueden variar entre especies estrechamente relacionadas, lo que desafía la idea del conservadurismo de nicho y señala la flexibilidad en la tolerancia fisiológica a medida que las especies se diversifican a lo largo de los gradientes de elevación. Además, la compleja geografía de los Andes jugó un papel significativo en la diversidad de la fisiología térmica dentro de estos anoles. Comprender cómo la diversidad fisiológica influye en la diversificación de especies podría darnos luz sobre cómo dos clados del mismo género, con historias evolutivas distintas, muestran respuestas similares a la adaptación a ambientes montañosos. Nuestros datos sobre los anoles andinos son consistentes con esta perspectiva: ya sea cerca del nivel del mar o varios kilómetros por encima de él, las especies están fisiológicamente especializadas para sus condiciones térmicas locales y exhiben un rango de tolerancia relativamente estrecho, como se predice para los lagartos tropicales (Huey et al. 2009).

Para responder a esas dos preguntas:

1. ¿Cómo predice la variación térmica a través de la elevación la evolución de dos rasgos fisiológicos clave en ectotermos tropicales de tierras continentales? La tolerancia al frío y al calor disminuye con la elevación.
2. ¿Cómo ha evolucionado la fisiología térmica en la radiación andina de los anoles? Ambos rasgos evolucionan a tasas similares, pero su evolución es independiente de la filogenia.

En un mundo que se calienta rápidamente, la pregunta crítica es si estas especies podrán mantener el ritmo con los impactos acelerados del cambio climático en sus ambientes naturales. La investigación futura debe centrarse en comprender cómo el aumento de las temperaturas y los patrones cambiantes de lluvia influirán en los patrones de actividad, el equilibrio energético y las tasas de crecimiento poblacional de los anoles andinos. Al vincular la variación fisiológica con las tendencias demográficas, podremos predecir mejor cómo estas notables especies de lagartos podrían enfrentar las presiones del cambio global.

Espero que este estudio despierte la curiosidad por explorar más a fondo los anoles andinos—y también los anoles amazónicos, que siguen siendo sorprendentemente poco estudiados.

Una última historia adicional—no estoy seguro de cuántos de ustedes han visto esta foto, pero tomé esa hermosa imagen de Anolis chloris durante uno de mis viajes de campo cuando era estudiante de pregrado.

 

References:

Salazar JC, Londoño GA, Muñoz MM, et al. The Andes are a driver of physiological diversity in Anolis lizards, Evolutionary Journal of the Linnean Society 2025; 4(1): kzae040. https://doi.org/10.1093/evolinnean/kzae040

Ghalambor CK, Huey RB, Martin PR, et al. Are mountain passes higher in the tropics? Janzen’s hypothesis revisited, Integrative and Comparative Biology 2006; 46: 5-17. https://doi.org/10.1093/icb/icj003

Janzen DH. Why mountain passes are higher in the tropics, The American Naturalist 1967; 101: 233-249. https://www.jstor.org/stable/2458977

Méndez-Galeano MA, Calderón-Espinosa ML. Thermoregulation in the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) at high elevation in the Eastern Cordillera of Colombia, Iheringia, Série Zoologia 2017; 107: e2017018. https://doi.org/10.1590/1678-4766e2017018  

Méndez-Galeano MA, Paternima-Cruz RF, Calderón-Espinosa ML. The highest kingdom of Anolis: Thermal biology of the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) over an elevational gradient in the Eastern Cordillera of Colombia, Journal of Thermal Biology 2020; 89: 102498. https://doi.org/10.1016/j.jtherbio.2019.102498

Montoya-Cruz A, Díaz-Flórez RA, Carvajalino-Fernández JM. Thermal balance in Andean lizards: A perspective from the high mountains, Austral Ecology 2024; 49: 313578. https://doi.org/10.1111/aec.13578

Muñoz MM, Stimola MA, Algar AC, et al. Evolutionary stasis and lability in thermal physiology in a group of tropical lizards, Proceedings of the Royal Society B 2014; 281: 20132433. https://doi.org/10.1098/rspb.2013.2433

Muñoz MM. The Bogert effect, a factor in evolution, Evolution 2022; 76: 49-66. https://doi.org/10.1111/evo.14388

Pinzón-Barrera C, Suárez-Ayala N, Carrillo-Chávez LM, et al. Unveiling critical thermal limits of Anolis tolimensis (Squamata, Anolidae) across an elevational landscape, Current Herpetology 2024; 43: 155-134. https://doi.org/10.5358/hsj.43.115

When I was an undergrad student back in Colombia, I was trying to decide what to do for my thesis. In Colombia—or at least at my alma mater, Universidad Icesi—it’s mandatory to complete a thesis to graduate. During this time, I stumbled upon and read three of my favorite papers: Janzen (1967), Ghalambor et al. 2006, and Muñoz et al. (2014). After reading those papers, a question popped into my mind: Does the same happen in the Andes? Specifically, does cold tolerance decrease with elevation while heat tolerance remains unchanged?

I shared this idea with my thesis mentors, María del Rosario Castañeda and Gustavo A. Londoño, and told them, I want to do this! I want to test how thermal limits and thermal tolerance breadth vary with elevation both within and among anole species.

Long story short, I collected data on cold and heat tolerance for 14 anole species across five different sites in Colombia. However, due to restrictions at Universidad Icesi, I could only use data from four species for my thesis. Fast forward to over a year ago, when I was discussing this dataset with my PhD mentor, Jonathan Losos. He said, you should use this data for one of your PhD chapters. So, I did. Now, it’s published in the Evolutionary Journal of the Linnean Society: Salazar et al. 2024.

Now, let’s talk about Colombian Andean anoles. Most of what we know about the thermal physiology of anoles comes from Caribbean species. There’s a noticeable gap in information about the thermal limits of Andean-dwelling anoles. Only a handful of papers have been published on this topic: Méndez-Galeano and Calderón-Espinosa 2017, Méndez-Galeano et al. 2020, Montoya-Cruz et al. 2024, and Pinzón-Barrera et al. 2024. However, most of these focus on a single species.

Between 2016 and 2017, several undergrad students and I visited five different locations in Colombia to measure cold and heat tolerance in Andean anoles. We spent nearly seven months in the field over a year and a half. We measured 367 individuals—males, females, and juveniles—from 14 species across two clades: Draconura (five species) and Dactyloa (nine species) along an elevation gradient (200–3000 m). Our study addressed two key questions:

1. How does thermal variation across elevation predict the evolution of two key physiological traits in tropical mainland ectotherms?
2. How has thermal physiology evolved in the Andean radiation of anole lizards?

Before diving into the results, let me share some fieldwork stories. If you’ve ever searched for anoles in the Caribbean or the Andes, you’ll know the challenges. Before my trips, Rosario took me along on one of hers to teach me the basics. We spent a few days in the field and found a couple of lizards. At the time, I thought, I’ll never find enough lizards to write a thesis!

Finding anoles in the Andes is tough. During the day, they’re almost impossible to spot, and if you do see one, catching it is another story. Since I rarely succeeded during the day, we shifted to fieldwork at night. Even then, in some locations we didn’t see lizards for days. To maximize data collection, I decided to capture and measure every individual I found and assess whether the lizard was big or healthy enough to be measured.

Walking through the night in the Colombian Andes; Parque Nacional Natural Tatamá – 2000m,. The anole I have in my hand is an Anolis princeps, my favorite species.

Here’s a side story: Rosario once told me how different it was to catch anoles in the Caribbean. She said it’s easier to see and catch them there, and you can even decide on the spot which one to measure. I didn’t believe her—until I joined Kristin Winchell in the Dominican Republic. I had never seen so many anoles in one place—it was unbelievable! Still, I love searching for anoles in the Andes, even though it’s more challenging. I’m not sure why, but the Andes will always hold a special place in my heart—maybe it’s because one of my field sites is just 30 minutes from my parents’ house, probably I’ll never know haha.

What did we find? As expected, we found that cold tolerance (CTmin) and heat tolerance (CTmax) increase with environmental and operative temperatures but decrease with elevation. However, contrary to what other studies have reported, heat tolerance does not remain unchanged with elevation. Unlike their Caribbean counterparts, Andean anoles do not appear to use behavioral buffering to limit divergence in heat tolerance across elevations—a phenomenon known as the Bogert effect (Muñoz et al. 2022). It’s possible that Andean anoles do not thermoregulate behaviorally in the same way Caribbean species do, though this still requires further investigation (but see Méndez-Galeano and Calderón-Espinosa 2017).

We also found that cold and heat tolerance evolved at similar rates. Phylogenetic analysis revealed that thermal limits can vary among closely related species, challenging the idea of niche conservatism and pointing to flexibility in physiological tolerance as species diversified along elevation gradients. In addition, the Andes’ complex geography played a significant role in driving the diversity of thermal physiology within these anoles. Understanding how physiological diversity influences species diversification could shed light on how two clades from the same genus, with distinct evolutionary histories, exhibit similar responses to adapting to mountainous environments. Our data on Andean anoles are consistent with this perspective: whether near sea level or several kilometers above it, species are physiologically specialized to their local thermal conditions, and exhibit relatively narrow tolerance breadth, as predicted for tropical lizards (Huey et al. 2009).

To answer those two questions:

1. How does thermal variation across elevation predict the evolution of two key physiological traits in tropical mainland ectotherms? Cold and heat tolerance decreases with elevation.
2. How has thermal physiology evolved in the Andean radiation of anole lizards? Both traits evolve at similar rate, but their evolution is independent of the phylogeny.

In a rapidly warming world, the critical question is whether these species can keep pace with the accelerating impacts of climate change on their natural environments. Future research should focus on understanding how rising temperatures and shifting rainfall patterns will influence the activity patterns, energy balance, and population growth rates of Andean anoles. By linking physiological variation to demographic trends, we can better predict how these remarkable lizards might fare under the pressures of global change.

I hope this study sparks curiosity to further explore Andean anoles—and even Amazonian anoles, which remain surprisingly understudied.

One last side story—I’m not sure how many of you have seen this picture, but I took that beautiful shot of Anolis chloris during one of my field trips as an undergrad.

 

References:

Salazar JC, Londoño GA, Muñoz MM, et al. The Andes are a driver of physiological diversity in Anolis lizards, Evolutionary Journal of the Linnean Society 2025; 4(1): kzae040. https://doi.org/10.1093/evolinnean/kzae040

Ghalambor CK, Huey RB, Martin PR, et al. Are mountain passes higher in the tropics? Janzen’s hypothesis revisited, Integrative and Comparative Biology 2006; 46: 5-17. https://doi.org/10.1093/icb/icj003

Janzen DH. Why mountain passes are higher in the tropics, The American Naturalist 1967; 101: 233-249. https://www.jstor.org/stable/2458977

Méndez-Galeano MA, Calderón-Espinosa ML. Thermoregulation in the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) at high elevation in the Eastern Cordillera of Colombia, Iheringia, Série Zoologia 2017; 107: e2017018. https://doi.org/10.1590/1678-4766e2017018  

Méndez-Galeano MA, Paternima-Cruz RF, Calderón-Espinosa ML. The highest kingdom of Anolis: Thermal biology of the Andean lizard Anolis heterodermus (Squamata: Dactyloidae) over an elevational gradient in the Eastern Cordillera of Colombia, Journal of Thermal Biology 2020; 89: 102498. https://doi.org/10.1016/j.jtherbio.2019.102498

Montoya-Cruz A, Díaz-Flórez RA, Carvajalino-Fernández JM. Thermal balance in Andean lizards: A perspective from the high mountains, Austral Ecology 2024; 49: 313578. https://doi.org/10.1111/aec.13578

Muñoz MM, Stimola MA, Algar AC, et al. Evolutionary stasis and lability in thermal physiology in a group of tropical lizards, Proceedings of the Royal Society B 2014; 281: 20132433. https://doi.org/10.1098/rspb.2013.2433

Muñoz MM. The Bogert effect, a factor in evolution, Evolution 2022; 76: 49-66. https://doi.org/10.1111/evo.14388

Pinzón-Barrera C, Suárez-Ayala N, Carrillo-Chávez LM, et al. Unveiling critical thermal limits of Anolis tolimensis (Squamata, Anolidae) across an elevational landscape, Current Herpetology 2024; 43: 155-134. https://doi.org/10.5358/hsj.43.115

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.

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.

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?

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

 

We all know that anoles have subdigital lamellae; however, there is one species in which these lamellae are lacking: Anolis onca, which is known for being a sand-dwelling anole. In 2011, Dr. Jennifer Velásquez and colleagues published a paper in SABER, in which they studied the differences in thermal ecology and the activity pattern of male and female Anolis onca in Araya Peninsula, Venezuela, during the dry and wet season in a dry forest (10 m a.s.l). This study was conducted from September 2004 to April 2005, during which time 56 individuals were captured (15 females and 41 males). Dr. Velásquez and colleagues measured body temperature (T_b), substrate temperature (T_s) on the capture site, and air temperature (T_a).

Dr. Velásquez and colleagues found that in males and females, the T_b was higher during the dry season compared to the wet season: 33.6 ºC (30.0 – 37.2; n = 23) and 33.6 ºC (30.0 – 35.5; n = 7) for males and females, respectively, during the rainy season, and 34.4 ºC (33.0 – 35.8; n = 18) and 34.3 ºC (34.0 – 35.7; n = 8) during the dry season. Mean T_a and T_s were also higher during the dry season compared to the rainy season; during the dry season, T_a was 37.4 ± 0.69 ºC (n = 30) and T_s was 38.4 ± 0.69 ºC (n = 30), while during the rainy season, T_a was 33.9 ± 0.82 ºC (n = 26) and T_s was 34.9 ± 1.58 ºC (n = 26). In addition, Dr. Velásquez and colleagues found that A. onca changes its timing of activity depending on the season. During the rainy season, A. onca is more active from 9:00 am to 10:00 am, and during the dry season from 12:00 am to 1:00 pm; during both seasons, there is low activity from 3:00 pm to 5:00 pm.

The authors argued that there is a relationship between Tb, Ta and Ts during the rainy and the dry season, in which the thermophysiology of A. onca is influenced by the climate variability of the microhabitat it occupies, suggesting that this species is a thermoconformer. In conclusion, the body temperature of this species varies during the day and across seasons, and it also varies as air and substrate temperature vary.

Abstract:

Aspects of the thermal ecology and activity pattern of the lizard, Anolis onca, during the dry and rainy season, and both periods in a belt of xerophytic forest located in the Araya Peninsula, Sucre state, Venezuela. The mean body temperature of A. onca was 33.9 ± 1.50 ºC in both periods to A. onca, while it reached 34.4 ± 0.75 ºC during the drought period and 33.6 ± 1.87 °C during the rainy period. In both climate periods, we found positive and significant correlations between body temperature with air and substrate temperature. The results suggest that thermoregulation is done passively, influenced by microhabitat temperature (air and substrate). There was a unimodal daily activity pattern during both periods. The thermal niche breadth was greater in males, while niche overlap between sexes was higher during the rainy period.

Read the full paper here!

Last year, Rafael Alejandro Lara Resendiz (Centro de Investigaciones Biológicas del Noroeste and Instituto de Diversidad y Ecología Animal) published a paper in Acta Biológica Colombiana, in which he summarizes nocturnal activities in exclusively diurnal reptiles and addresses the question of how this behavior affects their ecophysiology.

Ectotherms – reptiles, amphibians, fish, and most invertebrates – need environmental temperature to produce heat internally, meaning that these organisms depend upon an external source of heat to regulate their internal functions. Thermoregulation is a complex physiological process that is involved in every activity that allows ectotherms to survive in nature (e.g., feeding and reproductive behavior, growth patterns, locomotion, digestion). In this regard, ectotherm species differ in their thermoregulation behaviors; some species are more active during the day while others are active during the twilight. However, some species that are known to be diurnal have been found active during the twilight. Lara-Resendiz (2020) address four-point in his work. Specifically, he 1) reviews nocturnal activity events in reptiles considered exclusively diurnal; 2) discusses the ecophysiological implications on this topic; 3) identifies the aspects that have not yet been approached in-depth; and 4) proposes possible directions for future lines of research.

Several species that are known to be exclusively diurnal have been observed carrying out nighttime activities, including lizards (e.g., Agama, Anolis, Callisaurus, Dipsosaurus, Gerrhonotus, Liolaemus, Ophisaurus, Phrynosoma), snakes (e.g., Charina, Contia, Masticophis), tortoises (e.g., Gopherus, Geochelone), marine turtles (e.g., Chelonia). Particularly, reptiles inhabit a wide variety of habitats including tropical and cold areas, desserts, high and low elevation areas, and the sea. Living in this different environment may cause lizards to have different patterns of activities throughout the daytime or nighttime: geographical location and thermal environmental variability have a tight relationship with the period of activities of all ectotherms.

One hypothesis has been proposed to explain the nocturnal behavior in diurnal species, in which ectotherm species have different optimal temperatures in the photophase (daytime) and scotophase (nighttime). In this regard, by selecting different environmental temperatures during each phase species that are active during the day can also be active during the night. In some other cases, species that are known to be strictly diurnal can behave opportunistically during the night due to ecological or physiological conditions – high levels of humidity and/or low predation rate, and prey can be easily spotted. Another possible explanation of this change in the time of activity in lizards and snakes is the heterogeneity or homogeneity in the temperature variation in the environment, where species that inhabit stable habitats cannot increase the length of their foraging time, while those species in more heterogenous habitats have more opportunities to extend their activity period due to their wide-body temperature range; this hypothesis has not been tested yet.

Currently, ectotherm species are facing the consequences of the change in the global temperature because they depend on the temperature of their habitat. Climate change is causing species to overheat, therefore, changing their diurnal activity and increasing vulnerability in their population structure. Particularly, these effects have been stronger in the atropical ectotherms which are inhabiting places where the temperature is near their optimal temperature. This suggests that the nocturnal opportunistic behavior of some ectotherm species could be a response to the increasing temperatures.

In conclusion, we need to address questions regarding why these changes in the foraging activity of ectotherm is occurring, and how their ecology and physiology is or could be affected by foraging during the nighttime.

Abstract:

This review is the first to summarize published studies that document nocturnal activity events in reptiles previously considered exclusively diurnal. The ecophysiological implications of this nocturnal activity in tropical and high-latitude environments are described and discussed from the perspective of optimal activity temperature ranges, tolerance thresholds, activity periods, cathemerality, voluntary hypothermia, and its importance in the face of global climate change. Gaps in the research field are finally identified, and new lines of study are proposed.

Read the full paper here!

Carlos Guarnizo along with several other scientists created Ciencia Café, pa’ Sumercé, which is a space where citizens can access first-hand (directly from researchers) excellent research in science and technology that Colombians are doing inside and outside the country. At the same time, this space offers scientists and researchers the opportunity to meet citizens and understand the concerns and interests of the public; all of this through respectful dialogue, promoting an appreciation for science and technology by encouraging everyone to participate.

Two weeks ago, I was invited to one of the interviews from Ciencia Café, pa’ Sumercé, in which I talk about two different things that are not necessarily exclusive: science and racism. During the interview, Carlos asked me about why I decided to study biology and lizards, especially, he was interested in knowing how I ended up doing a Ph.D. with Jonathan Losos. After I talked about that part of my professional life, Carlos asked me about the BLM movement and its consequences in Colombia. I told him that despite the miles apart that Colombia is from the USA, we – the black community – suffer from the same kind of discrimination (punctual and systemic racism) in our daily bases, and I also told him that it is important to talk about racism in our families and in our work areas. At the end of the interview, I told a short story about how the Anolis chloris photo I took in 2016 ended up as the cover image in Evolution in 2019.