Dehydration-Induced Mortality and Premature Hatching in Gliding Treefrogs with Even Small Reductions in Humidity
Climate change is affecting rainfall patterns and increasing dry spells in the tropics. Although many environmental conditions can affect the hatching timing and survival of amphibian embryos, increased variation in rainfall and humidity can have particularly strong effects on species facing higher risk from dehydration, such as those with terrestrial eggs. Thus, it is important to understand how these environmental changes may affect the development, behavior, and immediate and long-term survival of amphibian embryos. We investigated whether Gliding Treefrog embryos (Agalychnis spurrelli) adaptively shift their hatching timing in response to dehydration risk, at the cost of smaller hatchling size. We raised embryos under three humidity levels and assessed egg and clutch hydration, hatching timing, and egg mortality. Mean humidity of 92% in Experiment I led to over 98% egg mortality by dehydration. A decrease from over 99 to 96% mean relative humidity in Experiment II induced premature hatching and reduced hatchling size across ages. Both clutch thickness and egg size increased at 99% and decreased at 96% humidity. Our results suggest that embryos of A. spurrelli are extremely dependent on consistent precipitation and particularly vulnerable to climate change. Although we did not directly measure differences in hatchling fitness, our results and previous findings suggest that small, premature hatchlings of A. spurrelli from dehydrated eggs would suffer higher mortality as tadpoles, thus embryos' self-defense against dehydration likely carries a delayed cost. These findings add to our understanding of how predicted climate changes may impact anuran early life stages.
El cambio climático está afectando los patrones de lluvias e incrementando los periodos de sequía en los trópicos. Aunque muchas condiciones ambientales afectan la sobrevivencia y el tiempo de eclosión en embriones de anfibios, mayor variación en la lluvia y la humedad puede tener efectos particularmente fuertes en especies que enfrentan un mayor riesgo de deshidratación, como las que tienen huevos terrestres. Por tanto, es importante entender como estos cambios ambientales pueden afectar el desarrollo, el comportamiento y la sobrevivencia inmediata y a largo plazo de embriones de anfibios. Investigamos si los embriones de la rana planeadora (Agalychnis spurrelli) cambian adaptativamente su tiempo de eclosión en respuesta al riesgo de deshidratación, al costo de nacer más pequeños. Criamos embriones bajo tres niveles de humedad y evaluamos la hidratación de huevos y nidadas, el tiempo de eclosión y la mortalidad de los huevos. La humedad al 92% en Experimento I indujo más del 98% de la mortalidad de huevos por deshidratación. Una disminución de más del 99 al 96% de la humedad relativa en Experimento II indujo la eclosión prematura y redujo el tamaño de renacuajos a través de las edades. Tanto el grosor de la nidada como el tamaño del huevo aumentaron al 99% y disminuyeron al 96% de humedad. Nuestros resultados sugieren que los embriones de A. spurrelli son extremadamente dependientes de precipitación constante y particularmente vulnerables al cambio climático. Aunque no medimos directamente las diferencias en fitness de los renacuajos, nuestros resultados y previas investigaciones sugieren que embriones prematuros y pequeños de A. spurrelli de huevos deshidratados podrían sufrir una mayor mortalidad como renacuajos, por lo que el nacimiento prematuro de los embriones ante la deshidratación probablemente conlleve un costo posterior. Estos resultados amplían nuestro entendimiento de cómo los cambios climáticos previstos puedes afectar las primeras etapas de vida de los anuros.

(A–C) Time series of eggs of A. spurrelli drying in the field taken at ages 3, 5, and 6 days at Shampoo Pond. Many embryos that hatched from dried eggs got stuck and died on the clutch jelly or leaf. Black and red arrows indicate recently and long-dead eggs, respectively. (D) Hatched embryos of A. spurrelli on the dry pond floor 5 days after a breeding event at Shampoo Pond. Embryos pictured died of dehydration and predation by ants, spiders, and other invertebrates; note green yolks on leaf litter. Photographs taken by B. Güell on 31 May, 2 June, 3 June, and 18 June 2019.

Relative humidity and temperature in experimental bins for Experiments I and II. Points in Experiment I (A, B) are variables measured every 30 minutes (total n = 423) throughout the course of the experiment. Open (block 1) and closed (block 2) data points in Experiment II (C, D) are variables measured every 30 minutes (total n = 871) throughout the course of experiment.

Egg clutch thickness, egg diameter, and proportion of embryos of A. spurrelli that survived to hatch in Experiments I and II over development. Data are means±s.e. across 12 clutches per treatment in Experiment I and 23 split-clutches in two time blocks of Experiment II.

(A) Cumulative proportion of embryos of A. spurrelli hatched and (B) hatchling size in high and medium humidity treatments over time since oviposition (age). Arrows indicate the mean onset of hatching for each treatment. Asterisks indicate mean hatching age for each treatment. Data are means±s.e. across 23 split-clutches in two time blocks of Experiment II.