Thermal ecology of Stejneger’s robber frog Craugastor stejnegerianus (Anura: Craugastoridae) in the tropical dry forest of Parque Nacional Guanacaste, Costa Rica

Ecología térmica de la rana de hojarasca de Stejnegers Craugastor stejnegerianus (Anura: Craugastoridae) en el bosque seco tropical del Parque Nacional Guanacaste, Costa Rica

Diego A. Gómez-Hoyos1, Margarita Gil-Fernández2, Sergio Escobar-Lasso2,3
1    ProCAT Internacional/The Sierra to Sea Institute, Las Alturas, Puntarenas, Costa Rica. e-mail: dagomezh@uqvirtual.edu.co (corresponsal author). Grupo de Estudio     en Herpetología, Universidad del Quindío, Armenia, Colombia/Red Mesoamericana y del Caribe para la Conservación de Anfibios y Reptiles (MesoHERP). Grupo         de Investigación y Asesoría en Estadística, Universidad del Quindío, Armenia, Colombia.
2    Programa de Posgrado en Conservación y Manejo de Vida Silvestre, Instituto Internacional de Conservación y Manejo de Vida Silvestre.
     ICOMVIS, Heredia, Costa Rica.
3    Fundación RANA (Restauración de Ambientes Neotropicales Alterados), San José, Costa Rica.
    Date received: September 8, 2015          Date approval: December 10, 2015        Associated Editor: Moreno JN.

Abstract
Introduction: In a climate changing world it is indispensable to know the behavioral and physiological responses of amphibians to environmental temperature variation. Even so, thermal ecology is unknown for many species, including Craugastor stejnegerianus. Therefore, it is important to describe the patterns and mechanisms that influence body temperature and if these obey to the environmental temperature or to thermoregulation actions. Objective: The aim of this paper is to describe the relationship between environmental and substrate temperatures, as well as the behavior and substrate use with the body temperature of C. stejnegerianus. Methodology: The body temperature of individuals of C. stejnegerianus was monitored 13.4 h, along with measures of environmental temperature, substrate use and behavior observations. Results: the results obtained were that the body temperature is related to the substrate temperature but it does not depend on the variations of environmental temperature nor behavior or substrate use. Conclusion: Based in our findings we propose that the body temperature variation of this frog is circumstantial and there is not behavior of thermoregulation.

Keywords: Leaf-litter frog, Maritza Biological Station, Microhabitat, Thermoregulation.

Resumen

Introducción: En un mundo de clima cambiante, es indispensable conocer las respuestas fisiológicas y comportamentales de los anfibios a la variación ambiental de temperatura. Sin embargo, la ecología térmica es desconocida para muchas especies, incluyendo a Craugastor stejnegerianus. Por lo tanto, es importante describir los patrones y mecanismos que influyen sobre la temperatura corporal o sobre acciones de termorregulación. Objetivo: Se busca describir las relaciones de la temperatura ambiental y de sustrato, así como del comportamiento y uso de sustratos con la temperatura corporal de C. stejnegerianus. Metodología: La temperatura corporal de individuos de C. stejnegerianus fue monitoreada 13.4 h, junto con medidas de la temperatura ambiental, humedad relativa, uso de sustratos y observaciones de comportamiento. Resultados: Se obtuvo que la temperatura corporal está relacionada con la temperatura del sustrato y esto no depende de las variaciones de temperatura ambiental, ni del comportamiento o uso de sustrato. Conclusión: De acuerdo con los hallazgos, se propone que las variaciones de la temperatura corporal de esta rana son circunstanciales y no hay comportamientos de termorregulación.

Palabras clave: Estación Biológica Maritza, Microhábitat, Rana de hojarasca, Termorregulación.

Introduction

Amphibians are ectothermic animals which depend on environmental temperature to develop its physiological functions and behavioral activities (Köhler et al. 2011). The body temperature of these organisms is closely related with environmental temperature; nevertheless, some species have a complex thermoregulation behavior (Rowley and Alford 2009). Thermoregulation in amphibians is based on direct exposure to sunlight and absorption of solar radiation (heliothermia) (Brattstrom 1979). The thermoregulation behavior in amphibians determines, most of the times, the use of microhabitats (tigmothermia) and the activity patterns of the species (Brattstrom 1979, Navas 1996, Navas et al. 2013).

In tropical amphibians the body temperature is influenced by natural history and the ecology of the species (Navas et al. 2013). Besides, it has been registered that, in some cases, body temperature is closely related to substrate temperature, in spite of elevation differences, biome and species habits (Navas 1996, Navas et al. 2013). This relationship responds to thermoregulation behavior to face environmental conditions. In this paper, we classify the temperatures relation in: a) obeys to thermoregulation actions and b) circumstantial relation. Response “a” can be seen in stenothermal frogs exposed to wide ranges of environmental temperature or in eurythermal frogs when its activities are determined by body temperature (Navas 1996). On the contrary, response “b” is shown when frogs are exposed to less variable environmental conditions.

The knowledge about thermic ecology is not existent or scarce for many species of amphibians. This animals are especially sensitive to long-term global climate change because warming temperatures and altered hydrologic cycles are expected to increase thermal stress, affect disease susceptibility, desiccate breeding habitats, reduce availability of critical microhabitats, and alter foraging behavior and efficiency (Ryan et al. 2014). Therefore it is important to describe the mechanisms and patterns that regulate their body temperature, and if these involve thermoregulation behavior or are circumstantial. The aim of this paper is to describe the body temperature variation in Stejneger’s Robber Frog Craugastor stejnegerianus during its nocturnal activity in the dry tropical forest of Costa Rica.

The Stejneger’s Robber Frog C. stejnegerianus (Figure 1) can be found in humid lowlands and premontane slopes on the Pacific versant of western Panama and Costa Rica (Solís et al. 2008). This is a diurnal leaf litter species found in humid lowland and dry forest, and may be present in different vegetation cover types such as secondary forest, plantations and pastureland. It is an important predator in the leaf litter environment and plays a crucial role in nutrient cycling, energy flow, and carbon storage of forest ecosystems (Ryan et al. 2015). This species breeds by direct development (Solís et al. 2008).



Study area. The Maritza Biological Station (10°57’N, 085°29’W; 570 masl) is located in the Pacific slope of the Orosí Volcano, in Guanacaste National Park, Costa Rica (Figure 2). The mean annual precipitation is 3000 mm, and the temperature varies among 19-28 °C (ACG 2013). The station is composed by tropical dry forest in transition with rainforest. The study area corresponds to a site in early regeneration or secondary forest (10°57’18.4’’N, 085°29’33.4’’W; 583 masl).


Methodology

The thermal ecology of 7 individuals of C. stejnegerianus was studied between the 23 and 24 of July 2013. Even when this species is considered diurnal, it was found completely active at night (Figure 1A). The effort of nocturnal monitoring was 13.4 h. The individuals were monitored in an area of 36 m2. Every 20 minutes several variables were recorded for each individual: 1) substrate used, 2) behavior, 3) body temperature, 4) microhabitat temperature, and 5) environmental temperature.
The microhabitats were categorized as: leaf litter (individuals found in the leaf litter or in the ground), leaf (individuals located on leaf or stem of standing plants). The behavior was classified as “jump”, “call” and “perching” for non-active individuals.

The body temperature was registered telemetrically with an infra-red thermometer of 0.1°C precision, located on the back of the frog at a minimum distance of 15 cm, which allowed a temperature lecture of 2 cm of diameter (Figure 1B). The same equipment was used to measure the substrate temperature, taken from the place where the frog was found. The environmental temperature was obtained with a thermohigrometer of 0.1°C precision, placed 0.5 m above the ground.

Because the data obtained in this study does not meet the assumptions for statistical tests, data were analyzed descriptively. Environmental, substrate, and body temperature were plotted to see if these were related. In addition, box-and-whisker plots were used for comparison samples between substrate and activity; herein notches were drawn in order to regard differences among data (Chambers et al. 1983). The box-and-whisker plots construction requires a sample of at least 5 by comparison (Krzywinski and Altman 2014). This is adequate for the sample size in the present study. The graphics were developed in R language with ggplot2 package (Wickham 2009)

Results

A total of 37 records of body temperature of C. stejnegerianus was obtained. The mean body temperature of the frogs was 21.4±0.66°C (mean±SD, range: 20.1-22.7°C), the mean microhabitat temperature was 21.58±0.67°C (20-22°C) and the mean environmental temperature was 22.32±0.57°C (21.2-23.4°C). The body temperature does not appear to be related to environmental temperature oscillations (Figure 3A), but it is related to microhabitat temperature (Figure 3B).
It appears that the body temperature of frogs located in leaves is higher and less variable compared to the frogs found on leaf litter (Figure 4A). Compared with the activity of the frogs it is observed that the body temperature is lower in those frogs in call activity, nevertheless the temperature is more variable during this activity according to data dispersion (Figure 4B). However, according to the overlap of notches in the box-and-whisker plots, there is not difference among body temperature neither by substrate nor by activity. Range in body temperature, though closely related to substrate temperature (Figure 3A, B), does not depend on substrate use or activity (Figure 4A, B). 





Discussion

Body temperature variation of C. stejnegerianus coincides with the estimated for anurans of tropical dry forest at moderate elevations (700-900 masl) in Colombia (Navas et al. 2013). Moreover, its high relationship with substrate temperature agrees with those found for other species of the family Craugastoridae with terrestrial and nocturnal habits (Navas et al. 2013). Taking this into account, thermal ecology of C. stejnegerianus seems usual and obeys to the general pattern presented by other tropical anurans of similar habits.

It has been reported that amphibians do not present thermoregulation, therefore, its body temperature is influenced mainly by the environmental temperature (Rowley and Alford 2009). Nevertheless, this study shows that body temperature was not related to environmental temperature overall, and the species did not have evident thermoregulation behavior (Brattstrom 1979, Navas 1996, Navas et al. 2013). The results point out that the body temperature of C. stejnegerianus is related circumstantially to the substrate temperature, regardless of the environmental temperature.

Acknowledgment

The authors thank Rocio Seisdedos, Joel Sáenz and two anonymous reviewers for their valuable comments and inputs for improvement of the manuscript.

Literature cited