Martha Muñoz: Vulnerability of tropical anoles to environmental warming

In this blog post, Dr. Martha Muñoz, Assistant Professor of Ecology and Evolutionary Biology at Yale University, USA, discusses her recent paper, “The multidimensional (and contrasting) effects of environmental warming on a group of montane tropical lizards.”

Este blog también está disponible en español aquí.

About the paper

Our study centred around exploring vulnerability to environmental warming in a group of montane tropical anoles (lizards) from the Caribbean island of Hispaniola. In particular, we were interested in exploring whether signatures of vulnerability varied among different ecological axes. We found that these montane anoles (Anolis shrevei and A. armouri) are behaviourally resilient to warming—they are quite warm-adapted, both in their upper physiological limits and their preferred environmental temperatures. In spite of this, their habitats are often stressfully cold. Our biophysical models predict that warming should release these montane lizards from cold stress without also amplifying heat stress. Therefore, they might actually benefit from warming in terms of expanded hours of potential activity. Yet, we found that potential behavioural resilience to warming is met with vulnerability along different ecological axes. In particular, we found that the macrohabitat to which these montane lizards are inexorably linked (high-montane pine forest) is poised to shrink as warming pushes the cloud forest upslope. Likewise, a rising broadleaf forest and warmer environmental temperatures also make high elevation habitats more hospitable to a close relative (Anolis cybotes).

Anolis armouri, a high-montane anole from the Dominican Republic (Credit: Martha Muñoz)

While predicting the ultimate fate of these montane anoles under warming remains an n-dimensional challenge, we were struck by how different the signatures of vulnerability are depending on the axes one examines. Correspondingly, a multidimensional perspective can help researchers identify the more proximate axes of concern. In the case of the high-montane anoles, habitat loss might be a key pressure under environmental warming, perhaps more so than the direct effects of warming on patterns of activity.

About the research

For several years I have been visiting the Dominican Republic to study the ecophysiology and behaviour of Anolis lizards. A few things stuck with me from all these field expeditions. First, the temperature is extremely cold at high elevation. Hispaniola is topographically complex, and its montane summits exceed the highest peaks elsewhere in the Caribbean by several hundred meters. However, you can observe tropical anoles living at even the highest elevations of the island—in particular Anolis armouri (endemic to the Sierra de Baoruco) and A. shrevei (endemic to the Cordillera Central).

A topographic map showing elevation across Hispaniola, with labels denoting the major mountain ranges of the island. Credit: Vincent Farallo

That these lizards are found at such high elevations is quite remarkable. These species are part of a broader radiation of anoles known as the ‘cybotoids’, which are endemic to the island. Within this diverse group (9 species), only A. armouri and A. shrevei can be found at such high elevation. Given just how thermally challenging high elevation environments are, one might anticipate that the lizards’ physiology is correspondingly cool-adapted, meaning these montane species might behaviourally prefer cooler body temperatures, or exhibit reduced heat tolerance than their close relatives at lower elevations (like Anolis cybotes).

In fact, nothing could be farther from the case—conversely, I was struck by how warm-adapted A. armouri and A. shrevei are. In fact, if someone were to give me an observed value for heat tolerance, a preferred body temperature, or a field-estimated body temperature from a cybotoid anole, I could not reasonably pinpoint the species from which those data were gathered. That is how similar, even at high elevation, these cybotoid anoles are in ecophysiology! The lone exception is cold tolerance, which is stronger (i.e., lower) in the high elevation anoles. Therefore, the first foray into this work was curiosity-based. I set about finding the answer to whether warming really was a proximate threat for these lizards? Here, I teamed up with Dr. Vinny Farallo (Assistant Professor at the University of Scranton), then a postdoc in my lab, to build a series of biophysical models to explore the impacts of warming on activity and thermal stress in the montane anoles. Given the preference for relatively warm temperatures, and high heat tolerances of these anoles, we found that warming should not generally constrain activity or impose heat tolerance. By contrast, release from cold stress under warming actually increases hours of potential activity.

Martha Muñoz with a male Anolis cybotes from the Dominican Republic (Credit: R. Castañeda)

After this, Vinny and I started to wonder if there was more to the picture. I knew that the montane anoles were inexorably linked to the edges of pine forest. At lower elevations, they are parapatrically replaced by their close relative, Anolis cybotes, at the ecotone that separates high-montane pine forest from broadleaf forest below. We decided to join forces with two botanists, Dr. Patrick Martin (University of Denver) and Dr. Ken Feeley (University of Miami), to explore what might happen to forest distributions under warming. Patrick, along with his colleagues, had been monitoring Dominican forest plots across large elevational transects for nearly two decades, so he had an exceptional dataset of occurrences that we could use for the task. Using these data, Ken built a series of distribution models under current and future climate scenarios. We found that the cloud forest is expected to track climate upslope, which has the potential to constrict the availability of pine forest. Due to the fact that broadleaf was poised to shift upslope, Vinny then built a series of additional biophysical models to determine how rising temperatures might affect the suitability of high-montane habitats for Anolis cybotes. Warming transforms high-elevation areas into more thermally hospitable environments, similar to habitats within the species’ current core range. These two factors—the potential loss of macrohabitat and upslope transport of a close relative—could pin the montane endemics into shrinking ranges, despite behavioural resilience to warming. To be clear, these are all projections based on current data. Ultimately, it is not clear what might happen to these montane anoles. We examined three of many potentially important factors for these lizards under warming. However, in general, we were struck by how varied the patterns of vulnerability are under warming. Furthermore, and this is essentially our broader message: predicting the future of species in a rapidly changing climate is a multidimensional (perhaps n-dimensional) challenge. Embracing this nuance allows us, for example, to hone conservation efforts on the more salient axes of vulnerability like (in this case) the potential for critical macrohabitat loss.

Martha Muñoz waiting for Anolis armouri to emerge on a cold, rainy summer morning in the Sierra de Baoruco (Credit: E. Cook)

We have a few takeaways we’d like to share. First, some tropical ectotherms, especially those in environments much colder than their preferred thermal ranges and heat tolerances, are likely to be behaviourally and physiologically resilient to warming, at least more so than other types of tropical ectotherms (e.g., species adapted to relatively cool forest interiors). Second, potential resilience in some ecological dimensions can be undermined by vulnerability along others. Lastly, simultaneously exploring vulnerability along multiple ecological axes can help identify more proximate variables of conservation concern. In the case of our montane Hispaniolan anoles, habitat loss appears to be a more immediate concern under warming than constriction on activity.

View of the Cordillera Central, in the Dominican Republic (Credit: M. Muñoz)

With reference to questions raised by our research, we explored patterns of vulnerability to warming for montane Hispaniolan anoles along three ecological axes; however, vulnerability to warming is an inherently multidimensional problem which encompasses numerous potential direct and indirect effects. We would love to know, for example, how prey availability (like insect abundances) or predator distributions will be altered under warming. Additionally, how do patterns of vulnerability compound, or balance each other out? And, how can we turn inferences into climate-based conservation action? While anyone drawn to biology might like to read this paper, I think the study will be of particular interest to folks interested in reptiles, climate change, ecophysiology, Caribbean biology, and distribution modelling.

About the author

Currently, I am Assistant Professor at the Department of Ecology & Evolutionary Biology at Yale University, USA, and Assistant Curator of Vertebrate Zoology at Yale Peabody Museum of Natural History. I was drawn to biology mostly because of an intense desire to better understand the natural world. This led me to pursue field ecology opportunities and engage in research that relied on inferences based on field observations. My research integrates behaviour, ecophysiology, and evolution. Absolutely vital to my research program are the ecological observations we make in the field—Every major project we work on in my lab ultimately ties back to ecology, and from the time we spend in the company of the organisms in the field.

Martha Muñoz (Credit: Dan Miller)

If I had to give advice to someone in my field, one of the pressures faced by scientists in ecology and evolution is to publish ‘positive’ results using hypothesis testing approaches. This is certainly an important dimension to research. however, ‘negative’ results are also important, and can often tell us something just as important about biological phenomena as ‘positive’ results. Likewise, hypothesis testing approaches require us to work within the framework of existing observations. Despite all of the hypotheses we already have about biology, there are more yet to be discovered. Natural history and curiosity-based exploration in the field are the catalysts of new observations and ideas. Ecologists should embrace both hypothesis testing and hypothesis ‘discovery’.

In my personal life, I love to read, hike, and spend time with my family.

Enjoyed this blog post? Read the research here.

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