Differential Plasticity in Response to Simulated Climate Warming in a High-Elevation Amphibian Assemblage
Climate change is expected to increase amphibian extinction rates; however, little is known about the physiological responses of amphibian populations to climate change projections for their region. For the Cascade Mountain Range of the U.S. Pacific Northwest, high-resolution climate models predict temperature increases during summer months. We evaluated phenotypic plasticity in larval growth and development in response to this projected increase in temperature in three co-occurring Anuran species: Cascades Frogs (Rana cascadae), Western Toads (Anaxyrus boreas), and Pacific Chorus Frogs (Pseudacris regilla). We exposed each species to two temperature regimes: the control treatment simulated the historical summer temperatures for the decade of 2001–11; the warmed treatment mirrored this seasonal trend but simulated a 4°C average increase in temperature. To quantify the magnitude of plasticity and any consequences to body size, we measured growth characteristics throughout larval development and metamorphosis. We found significant acceleration in larval developmental rates and increased larval body mass under the warmed temperature treatment for all three species. When compared across Gosner developmental stages, however, the perceived weight gain in the warmed treatment was largely because of the advancement in development triggered by warming. As a consequence of rapid development, we observed differential shifts in body size features. We further identified an optimal temperature range (22–25°C) within which all three species showed maximum weight gain and development rates and above which performance plateaued. We provide empirical evidence for species-specific thermal tolerances and the potential for individualistic responses to climate change among co-occurring amphibian species. El cambio climático podría incrementar las tasas de extinción de anfibios, sin embargo se conoce muy poco sobre las respuestas fisiológicas de poblaciones frente a las proyecciones de cambio climático. En la cadena montañosa del Pacífico Noroccidental (Estados Unidos), modelos climáticos de alta resolución predicen incrementos en la temperatura durante los meses de verano. Evaluamos la plasticidad fenotípica en el crecimiento y desarrollo larval en respuesta al incremento proyectado en la temperatura en tres especies de anuros co-ocurrentes: Rana cascadae, Anaxyrus boreas y Pseudacris regilla. Expusimos cada especie a dos regímenes de temperatura: el tratamiento control simulando temperaturas históricas de verano para la década 2001 a 2011; y el tratamiento cálido correspondiente a la tendencia estacional pero simulando un incremento promedio de 4 °C de temperatura. Medimos características a través del desarrollo larval para cuantificar la magnitud de la plasticidad fenotípica y consecuencias en el tamaño corporal. Las tasas de desarrollo larval y la masa corporal de las tres especies incrementaron significativamente en el tratamiento cálido. Al comparar a través de estados de desarrollo (Gosner), el peso obtenido en el tratamiento cálido es explicado por el rápido desarrollo causado por el calentamiento. Como consecuencia del rápido desarrollo observamos cambios diferenciales en características del tamaño corporal. Identificamos un rango óptimo de temperatura (22- 25 °C) en el cual las tres especies maximizaron su peso y tasas de desarrollo. Por encima de dicho rango, el peso y las tasas de desarrollo se estabilizaron. Proporcionamos evidencia empírica de la tolerancia térmica de las especies y el potencial de respuestas individuales al cambio climático entre especies de anfibios co-ocurrentes.Abstract
Resumen
Experimental temperature regimes and historical temperature conditions. Control temperature treatment indicated by solid black line and warmed temperature treatment indicated by dashed red line. Mean daily maximum temperatures (solid black line with open circles) for the summer months averaged for the decade 2001–11 taken from SNOTEL site 815 (http://www.wcc.nrcs.usda.gov/snow/); represents historical temperature conditions upon which the temperature treatments were based. Warmed temperature treatment was 4°C warmer than the control temperature treatment.
Species-level effects of warming on larval characteristics. Coefficient values and 95% confidence intervals for (A) increases in larval body weight, and (B) increases in developmental stage by day 30 (n = 12 for each species). Species include the Western Toad (Anaxyrus boreas), Cascades Frog (Rana cascadae), and Pacific Chorus Frog (Pseudacris regilla).
Mean larval duration (d) in the control and warmed temperature treatments. (A) Western Toads (n = 12/treatment), (B) Cascades Frogs (n = 12/treatment), and (C) Pacific Chorus Frogs (n = 12/treatment). The color gradient represents 1°C temperature ranges for the mean temperature at emergence for each treatment tub. The horizontal dashed line indicates the day of peak temperature (day 44) during the experiment. All individuals in the control treatment emerged after the peak temperature (26°C) and individuals in the warmed treatment emerged around the time of peak temperature (30°C).
Difference in average weight gain (g) between the control and warmed temperature treatments over the course of the experiment for Western Toad larvae. The control temperature treatment is represented by shaded circles with a solid line and the warmed temperature treatment is represented by unshaded circles with a dashed line (n = 12/treatment). The size of the circle indicates Gosner developmental stage.
Difference in average weight gain (g) between the control and warmed temperature treatments over larval development. (A) Western Toads (n = 12/treatment), (B) Cascades Frogs (n = 12/treatment), and (C) Pacific Chorus Frogs (n = 12/treatment). The control temperature treatment is represented by the black circles with a solid line and the warmed temperature treatment is represented by the white circles with a dashed line.
Differences in larval development rates and growth characteristics over the control and warmed experimental temperature gradients for Western Toads (A–C), Cascades Frogs (D–F), and Pacific Chorus Frogs (G–I). The control temperature treatment is represented by black circles with a solid line and the warmed temperature treatment is represented by white circles with a dashed line. The point of instantaneous maximum growth or development rate (calculated from the tangent line to the curve at each point along the curve) is indicated by a blue diamond for the control treatment and a red diamond for the warmed treatment.
Species-level effects of warming on juvenile (metamorph) characteristics. Coefficient values and 95% confidence intervals for (A) body weight and (B) length (n = 12 for each species). Species include the Western Toad (Anaxyrus boreas), Cascades Frog (Rana cascadae), and Pacific Chorus Frog (Pseudacris regilla). The Western Toad did not exhibit a significant reduction in body weight at emergence in the warmed temperature treatment.
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