The Biological Impacts of Tropical Climate Warming for Ectothermic Animals

A symposium sponsored by the National Science Foundation with Collaboration of CATEC at the University of Puerto Rico. August 2-3, 2013 San Juan, PR

List of Abstracts by order of Appearance

Opening Remarks
Raymond B. Huey1, Hctor lvarez2, Patricia Burrowes2, Andrs Garcia3, George C. Gorman4, Luisa M. Otero2, Paul E. Hertz5, Bradford Lister6 Department of Biology, University of Washington, Seattle, WA 98195-1800; Department of Biology, University of Puerto Rico, San Juan, P.R. 00931; 3Estacin de Biologa Chamela, Instituto de Biologa, Universidad Nacional Autnoma de Mxico, La Huerta, Jalisco, Mxico; 5Barnard College, 3009 Broadway, New York, NY 10027; 6 Paso Pacfico, PO Box 1244, Ventura, CA, USA, Department of Biology, Rensselaer Polytechnic University, Troy, NY, USA
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This symposium is a special component of a collaborative (NSF) project designed to study the potential impacts of recent climate warming on Puerto Rican Anolis lizards. We introduce the rationale behind the origin of this collaborative project and then provide a brief overview on some of the component projects, all of which are still in progress. Our basic approach involves 'replicating' historical studies that we did back in the early '70s or '80s on the ecology and physiology of these lizards, and then evaluating whether any observed changes might have resulted from recent climate warming. At some sites, conspicuous changes (e.g., in reproduction) are not apparent; but some observed changes contradict expectations. For example, diverse species have shifted their ranges to higher altitude in response to warming, but Anolis gundlachi (classically considered as a montane forest species) appears to have moved downhill to near sea level at least along the north coast, apparently tracking the recent regeneration of lowland forests there. Thus land use changes can profoundly alter the responses of organisms to climate shifts.

Climate change or land cover change? Which is driving some lizards to the lowlands?
Ariel Lugo International Institute of Tropical Forestry; Forest Service, San Juan. P.R. 00926 The forests of Puerto Rico are experiencing the effects of two dramatic forces: those of climate change and those of land cover change. Climate change effects are subtle and occur slowly over time. Scientists have documented changes in air temperatures, rainfall, and atmospheric gas concentrations but are less successful in demonstrating actual forest responses to changing climate, especially in the tree component. Responses in lizards and frogs are however, dramatic, which suggests that different forest compartments respond to different thresholds of changes in temperature, precipitation, and gaseous concentrations. However, forests do responds dramatically to the land cover changes in the Island, a response that can easily overwhelm and possibly mask forest response to climate change variables. I will describe these responses to land cover change and propose that forest response to land cover change might provide the emerging novel forests a leg up when coping with climate change. Land cover changes in forests might also influence the distribution of animals, including lizards, throughout the Island.

Global patterns of thermal tolerance and range limits in ectotherms

Jennifer Sunday Biodiversity Research Centre, University of British Columbia, Canada

Understanding the factors that limits species distributions has been a central goal of ecology since its inception and is of renewed relevance under global climate change. Here we present a comparative analysis of thermal tolerance limits in ectotherms on land in the ocean, testing the hypothesis that species occupy latitudes that correspond to their thermal tolerance windows. We find that marine and terrestrial ectotherms differ in the degree to which they fill their potential thermal ranges. Terrestrial ectotherms are excluded from the warmest regions of their latitudinal range, while marine species more fully occupy the extent of latitudes tolerable within their thermal niche.

On the risk of extinction of tropical ectotherms: Are they buffered against climate?
Barry Sinervo1 and Donald B. Miles2 1 Department of Ecology & Evolutionary Biology, University of California, Santa Cruz; CA; 2Department of Biology Ohio University Athens, OH 45701

Tropical species inhabiting closed canopy forests, such as lizards and frogs, have been suggested to have a higher extinction risk. This elevated risk of extinction arises largely through the proposition that the body temperature of such species conforms to ambient temperatures. That is, they have a lower capacity to buffer against prevailing conditions relative to other taxa that bask in the sun (heliotherms). The basic dichotomy between thermoconformers and heliotherms arises through the exploitation of different thermal environments embedded within the tropical forest ecosystem. Here, we discuss the additional problem regarding how the destruction of tropical forests exacerbates the rise of local temperatures through climate warming, and raises the risk of extinction predicted for thermoconformers, but not heliotherms. The same effects might arise as tropical forests become converted to more open ecosystems due to succession, as climate warms and perturbs tropical ecosystems.

Climate variability in the Caribbean and its possible effect on the biodiversity of the region: the case of Puerto Rico
Elvira Cuevas Department of Biology, University of Puerto Rico, San Juan, PR 00931; Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, San Juan PR 00931 Global climate change affects not only the global climatic patterns but also their regional variability. ENSO, the weakening in Trade Winds and the northward migration of the Intertropical Convergence Zone have created marine and terrestrial conditions that are increasing the temporal and spatial variability in temperature and precipitation. These significant decadal scale trends can have short, medium and long-term effects in the ecosystems of the region. To what extent these changes may play a role in ecosystem dynamics, especially in the behavior and reproduction dynamics of organisms is of great concern and would have to be taken into consideration when establishing management policies for the conservation of our natural resources and its extant biodiversity.

Significant diurnal and seasonal variation in soil CO2 efflux is positively related to temperature in a moist subtropical forest in Puerto Rico.
Omar Gutierrez Department of Biology, University of Puerto Rico, San Juan, PR 00931 Identifying the climatic controls of soil CO2 efflux (Rs) in moist subtropical forests will improve our ability to predict how this large C-flux will respond to climate change. We measured hourly Rs and multiple climatic factors to determine at what time-scale Rs varies and its driving factors. Rs varied significantly at both seasonal and diel timescales in relation to changes in air and soil temperature and soil moisture. The significant positive effect of temperature on Rs in this forest, despite low intra-annual variability (<4C), suggests that soil C loss could increase as global temperatures rise.

Thermal specialization of ecotherms on tropical mountains

Lauren Buckley Department of Biology, University of North Carolina, Chapel Hill, NC What are the implications of elevation gradients in body temperatures for responses to climate change? First, I will discuss the competitive dynamics of Anolis species that differ in thermal preferences along Puerto Rican elevation gradients. Species interactions may have accentuated abundance and distribution shifts in response to recent climate change. Second, I will compare altitudinal trends, including seasonal overlap, between tropical and temperate mountains to ask whether mountain passes are higher in the tropics (Janzens hypothesis). Considering body rather than air temperature generally increases the amount of overlap along elevation gradients and decreases the extent to which mountain passes pose a greater physiological barrier in the tropics.

The thermodynamic niches of tropical ectotherms

Michael Kearney Department of Zoology, University of Melbourne, Melbourne, Australia The impacts of climate change on ectotherms are multifaceted but come most directly through thermodynamic constraints i.e. the balances of heat, water and food. I will illustrate how thermodynamic niche models, which incorporate the biophysics of heat/water balance and metabolic theory, can provide a fundamental basis for inferring climate change impacts. In particular, I will illustrate the power of Dynamic Energy Budget theory for understanding how species respond to variable food, water and temperature, using tropical species as examples.

Life in the boundary zone--the thermal ecology small cursorial insects

Mike Kaspari Department of Biology, University of Oklahoma, Norman OK 73019-0235 Ambient air temperature remains the driving predictive variable in scenarios of global change. But the thermal ecology of terrestrial invertebrates is often far more influenced by surface temperatures. To make matters worse, on sunny days, there is little relation between ambient temperature and surface temperature in tropical forests, save that surface temperatures average 5-10C warmer. In studies of thermal range across 92 ant species, we test three hypotheses: that large body size buffers ants against high surface temperature, that the variable warm canopy selects for broader thermal ranges, and that nutritionally complete diets generate broader thermal ranges.

Climate change effects on Caribbean Seasonality and its Implications on an Ectotherm Host-Pathogen Dynamics
Patricia A. Burrowes Department of Biology, University of Puerto Rico, San Juan, PR 00931

Climate warming can increase pathogen development, transmission rates, and host vulnerability. In Puerto Rico, climate change has brought increased periods of drought, and a significant increase of mean minimum temperature. Susceptibility of directdeveloping frogs to the pathogenic chytrid fungus, Batrachochytrium dendrobatidis (=Bd) in the Island, is associated to seasonality, with the highest infection intensities observed during the cool-dry season. Considering that Bd disperses via flagellated spores, this sounds counter-intuitive. However, a combination of factors that influence hosts behavior, stress and immune response, renders this opportunistic pathogen an advantage under these conditions. At the turn of the season, warmer and wetter weather favor frogs immunological response to Bd infections increasing resistance to disease that is characterized by low infection intensities and a decrease in pathogen prevalence. This work documents how global climate change can influence disease dynamics by intensifying seasonal patterns that affect hosts defense mechanisms.

Vulnerability of anuran amphibians to climate change: inferring the impact of water availability and temperature
Carlos A. Navas & Fernando R. Gomes Departamento de Fisiologia, Instituto de Biocincias, Universidade de So Paulo, Brasil Well-supported generalizations are ideal to infer the impact of climate change on organism sharing key aspects of natural history. For anurans the power of inference is limited due to scattered information and amazing diversity in natural history. Although water availability and temperature are likely to affect this taxon, the definition of critical conditions is still under construction. We discuss some of the problems, including 1) how to infer critical conditions from field climatic data?, 2) Does expected impact vary with strategies for hydroregulation and thermoregulation?; 3) How do water & temperature, when varying simultaneously, affect behavioral performance in anurans? We address these questions based on research on three highly different anuran communities, namely the mountains of central and Northern Colombia, the Semi-arid Caatingas from Brazil and the Atlantic forest from Southern Brazil.

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Integrating data sets to validate models of biological response to former climate change in the Brazilian Atlantic Forest
Ana Carnaval1, Craig Moritz2, Eric Waltari1, Miguel Rodrigues3
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Department of Biology, City College of New York, City University of New York, NY 10031, USA, 2Australian National University, 3Universidade de So Paulo.

To study how former climates have impacted the distribution of genetic diversity in the Brazilian Atlantic Forest, we have used correlative models of species and habitat distributions under current and paleoclimates to guide Hierarchical Approximate Bayesian Computation models of historical demography. Such combination of tools validated a hypothesis-testing framework that uncovered historical processes responsible for the spatial re-shuffling of genetic diversity in coastal Brazil during the Last Glacial Maximum and the Holocene. As we are now furthering our paleoclimatic studies and gathering phylogeographical data from species restricted to higher elevations, we realize the need to refine available forest models as to fully capture the history of the biome and identify distinct types of shifting forest refugia through time. In this talk, I present and discuss these results. When analyzed jointly, these environmental analyses and molecular data from amphibians and reptiles suggest a central role for species physiological constrains in shaping biological responses to Late Quaternary climate change, hence defining current diversity patterns in the Brazilian tropics.

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The effects of ocean warming on marine phytoplankton diversity

Mridul Thomas Deptartment of Zoology & W.K.Kellogg Biological Station, Michigan State University. Marine phytoplankton are responsible for nearly half of global primary production and are highly sensitive to temperature changes. As they live in highly stable and predictable thermal environments, we may expect that 1) species will be well-adapted to local temperature regimes, and 2) consequently, they will be sensitive to changes in these regimes. Using thermal reaction norms measured on 194 strains isolated across 150 degrees of latitude, we showed that (1) is true: temperature optima are strongly related to the mean temperature at the isolation location. However, optima were lower than predicted in the tropics. To examine (2), we used temperature time series (recent and projected) across the whole ocean along with the reaction norms to estimate every strains geographical range limits. We found that ocean warming this century may drive dramatic declines in tropical phytoplankton diversity, with approximately one-third of tropical strains likely to go locally extinct.

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Long Term Declines in Arthropod Abundance Restructure a Rainforest Food Web

Bradford C. Lister1, Andres Garcia2 1 Department of Biology, Rensselaer Polytechnic University, Troy, NY, USA 2 Estacin de Biologa Chamela, Instituto de Biologa, Universidad Nacional Autnoma de Mxico, La Huerta, Jalisco, Mxico. Despite generally lower rates of warming in tropical habitats, a growing body of theory and data suggests that tropical insects and other ectotherms may be particularly vulnerable to climate change. Recently, Deutsch et al (2008) also predicted that for tropical insects, rates of population growth would fall by as much as 20%. If these predictions are realized, there will be profound impacts on the structure and functioning of tropical ecosystems as the planet warms. Although insects comprise over two thirds of all terrestrial species, and are centrally important to the ecological well-being of the planet, long term data connecting predicted changes in population abundance and extinction rates with recent climate change are severely limited. Here we compare recent data on arthropod and Anolis lizard abundances in the Luquillo rainforest in northeast Puerto Rico with data taken in the same study area over 35 years ago. We also analyze several data sets on invertebrate, bird, and frog abundances in the Luquillo rainforest gathered by various researchers as part of the El Verde Long Term Ecological Research program. Our analyses indicate that, over the past three decades, major declines in arthropod abundance within the Luquillo forest have occurred in parallel with significant declines in forest insectivores. We evaluate possible drivers of these trends, including climate change, and discuss the implications of our results for the future functioning and biodiversity of rainforest ecosystems.

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Evolutionary stasis and lability in thermal physiology in a group of tropical lizards

Martha M. Munoz1, Maureen Stimola2, Adam C. Algar3, George Bakken4, and Jonathan B. Losos1 1 Harvard University, 2Columbia University, 3University of Nottingham, 4 Indiana State University

There is increasing interest in understanding how quickly physiological traits tend to evolve, particularly in the context of adaptation to warming temperatures. Diversification into new climatic habitats is expected to occur either through behavioral adjustments (thermoregulation) or physiological adaptation, which tend to lead to contrasting patterns of lability and stasis in physiological traits. The cybotoids are a clade of Anolis lizards from Hispaniola distributed in markedly different thermal environments. Here we test whether divergence into new thermal habitats is characterized by physiological evolution (higher trait lability) or behavioral thermoregulation (lower trait lability). Our results suggest that daytime behavioral thermoregulation buffers selection on body temperature and heat tolerance, while nighttime temperatures can only be partially buffered by behavior and likely drive cold tolerance evolution. These results can improve our understanding of diversification in the tropics, the mechanisms of adaptive radiation, and the potential for evolutionary response to climate warming.

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Effects of Recent Climate Warming on The Reproductive Phenology of Puerto Rican Anolis Lizards
Luisa Otero1, Raymond Huey2, George Gorman3 Department of Biology, University of Puerto Rico, San Juan, P.R. 00931; 2Department of Biology, University of Washington, Seattle, WA 98195-1800; 3Paso Pacfico, PO Box 1244, Ventura, CA, USA Reproductive cycles of Puerto Rican Anolis lizards are cyclical and are highly influenced by environmental temperature (Gorman and Licht, Ecology 1974): female reproduction peaks in summer but drops in summer, especially at altitude. If recent climate warming has affected reproduction in these lizards, we expected that winter warming would foster female reproduction (especially at high altitude) but that summer warming (and attendant heat stress) would depress female reproduction (at least at low altitude). To test these expectations, we sampled female reproduction in multiple populations of Puerto Rican Anolis lizards at monthly intervals over two years and compare these contemporary data with historical data documented for some of the same sites and species sampled by Gorman and Licht. Some new data reinforce Gorman and Licht's conclusion that temperature drives reproduction in Puerto Rican Anolis: at two lowland sites (Pta. Salinas, Monagas), lizards in shaded forests had much lower body temperatures and lower rates of reproduction throughout the year than did lizards in adjacent open (sunny) habitats. Nevertheless, we found no clear differences in reproductive phenologies between contemporary and 1970s comparisons, suggesting that Anolis lizards in Puerto Rico have so far been able to cope with recent climate warming.
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Behavioral responses to thermal variation: implications for predicting the biological impacts of climate change
Alex Gunderson Department of Biology, Duke University, Durham, North Carolina, 2770 Predicting when ectotherms will be active as thermal environments change is crucial for estimating the direct and indirect effects of warming on populations. Most models of temperature-dependent activity are constructed around estimates of the preferred temperature (Tp) of a population. In addition, activity is typically considered a categorical variable with two potential states: active or inactive. I evaluated the agreement between observed temperature-dependent activity of the Puerto Rican lizard Anolis cristatellus under natural conditions and three models of temperature-dependent activity with varying levels of thermal constraint. I found that no models adequately predicted the temperature-dependent activity pattern of A. cristatellus: lizards were active at body temperatures (Tbs) several degrees above and below the Tp range. In addition, activity rates demonstrated a graded response to temperature: mean activity rates were highest within the Tp range, but decreased gradually as Tbs increased above or decreased below Tp. Based on the observed data, I conducted simulations of the activity of A. cristatellus under warmer conditions. These simulations demonstrated that the mismatch between expected activity patterns and models of temperaturedependent activity increase as temperatures warm. Based on the results from A. cristatellus, I propose a new graphical model of temperature-dependent activity and test the model using previously published data in other lizard species. This model may represent of more biologically meaningful framework for predicting the activity budgets of ectotherms under climate change.

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Rapid evolution in response to climate change: natural selection on the thermal physiology of Anolis sagrei
Michael Logan Department of Biological Sciences, Dartmouth College, NH USA. Many biological climate models ignore the potential for evolutionary responses to environmental change. An often cited reason for this is the rapid nature of anthropogenic warming relative to the generation times of most organisms. Nevertheless, the extent to which wild populations can adapt to changes in temperature on short time scales is largely unknown. We measured natural selection on the thermal performance curves of two populations of the lizard Anolis sagrei in The Bahamas. We quantified selection gradients for maximal performance, the optimal temperature for performance, and performance breadth on an unmanipulated baseline population, and on a population that we transplanted from a cooler, less thermally-variable site, to a warmer, more variable site. Despite the fact that A. sagrei is an accurate behavioral thermoregulator, we detected strong selection gradients in both populations in directions consistent with theory. Moreover, the fitness landscape appeared to be constrained by both a specialist-generalist trade-off and a thermodynamic effect. Although data on the underlying genetic architecture and heritability of thermal performance curves are needed, our results suggest that some populations may have the capacity to evolve rapidly in response to anthropogenic warming.

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Thermal ecology of Bolivian lizards of the genus Liolaemus: Will climate warming drive them to extinction?
Ignacio De La Riva and Octavio Jimnez-Robles Museo Nacional de Historia Natural, CSIC, 28006 Madrid, Spain Bolivian lizards of the genus Liolaemus are extremely poorly known both from taxonomic and ecological standpoints. We are conducting a field study on comparative thermal ecology of an assemblage of four species occurring in the high Andean puna of the southern portion of the Cordillera Oriental. In addition, we are investigating a rare species from Central Bolivia whose populations at the type locality might have been extirpated due to climate change. These data will serve to test Sinervo et al.s extinction predictive model and determine if populations within an elevation gradient present patterns indicative of climate-driven physiological stress.

Sunshine, on a cloudy day

Mat Vickers School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia Global average temperature is increasing, threatening ectotherms through its impact on potential activity period. Higher temperatures means longer shelter time through the middle of the day, reducing foraging time, impacting fitness and causing population decline. But what will the average day look like? It is easy to imagine clear skies and soaring temperatures but for much of the tropics, and in particular tropical savannahs, average cloudiness has increased over the last 30 years. I use a mechanistic model to compare the effect of climate change on potential activity period of small skinks on cloudy and sunny days, asking how much can cloudy days buffer the effect of climate change for small ectotherms?

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A Summary of the Symposium Highlights will be kindly presented by:

Michael Angiletta School of Life Sciences, Arizona State University, Tempe, AZ.

I hope these guys can help us before it is too late!

Lizard photos : Anolis cuvieri by R. L. Joglar

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