“Heat waves” experienced during larval life have species-specific consequences on life-history traits and sexual development in anuran amphibians

Extreme temperatures during heat waves can induce mass-mortality events, but can also exert sublethal negative effects by compromising life-history traits and derailing sexual development. Ectothermic animals may, however, also benefit from increased temperatures via enhanced physiological performance and the suppression of cold-adapted pathogens. Therefore, it is crucial to address how the intensity and timing of naturally occurring or human-induced heat waves affect life-history traits and sexual development in amphibians, to predict future effects of climate change and to minimise risks arising from the application of elevated temperature in disease mitigation. We raised agile frog (Rana dalmatina; Bonaparte, 1840) and common toad (Bufo bufo; Linnaeus, 1758) tadpoles at 19 °C and exposed them to a simulated heat wave of 28 or 30 °C for six days during one of three ontogenetic periods (early, mid or late larval development). In agile frogs, exposure to 30 °C during early larval development increased mortality. Regardless of timing, all heat-treatments delayed metamorphosis, and exposure to 30 °C decreased body mass at metamorphosis. Furthermore, exposure to 30 °C during any period and to 28 °C late in development caused female-to-male sex reversal, skewing sex ratios strongly towards males. In common toads, high temperature only slightly decreased survival and did not influence phenotypic sex ratio, while it reduced metamorph mass and length of larval development. Juvenile body mass measured two months after metamorphosis was not altered by temperature treatments in either species. Our results indicate that heat waves may have devastating effects on amphibian populations, and the severity of these negative consequences, and sensitivity can vary greatly between species and with the timing and intensity of heat. Finally, thermal treatments against cold-adapted pathogens have to be executed with caution, taking into account the thermo-sensitivity of the species and the life stage of animals to be treated.

热浪期间的极端高温既可引发大量死亡事件，也可通过损害生活史特征（life-history traits）、干扰性腺发育（sexual development）而产生亚致死负面影响（sublethal negative effects）。不过，变温动物（ectothermic animals）也可通过高温提升生理机能、抑制适冷病原体（cold-adapted pathogens）而从中获益。因此，阐明自然发生或人为引发的热浪的强度与发生时机如何影响两栖动物（amphibians）的生活史特征与性腺发育，对于预测气候变化（climate change）的未来影响、降低病害防控（disease mitigation）中应用高温措施带来的风险至关重要。本研究将敏捷蛙（Rana dalmatina; Bonaparte, 1840）与普通蟾蜍（Bufo bufo; Linnaeus, 1758）的蝌蚪（tadpoles）置于19℃环境下饲养，并在三个个体发育阶段（ontogenetic periods，即幼体早期、中期或晚期发育阶段）中的任意一个阶段，将其暴露于28℃或30℃的模拟热浪环境中持续6天。针对敏捷蛙的实验显示，在幼体发育（larval development）早期暴露于30℃环境会提升其死亡率。无论热浪暴露的时机如何，所有高温处理组均延缓了变态发育（metamorphosis），且暴露于30℃环境会降低变态完成时的个体体重。此外，在任意发育阶段暴露于30℃环境，以及在幼体发育晚期暴露于28℃环境，均会引发雌性向雄性的性反转（sex reversal），使种群性比（sex ratios）显著偏向雄性。针对普通蟾蜍的实验显示，高温仅会小幅降低其存活率，且不会影响表型性比（phenotypic sex ratio），但会降低变态个体的体重并延长幼体发育时长。两个物种在变态完成两个月后测得的幼体体重，均未受高温处理的影响。本研究结果表明，热浪可能对两栖动物种群造成毁灭性影响，且这类负面影响的严重程度、物种的热敏感性（thermo-sensitivity）会因物种差异以及热浪的发生时机与强度不同而存在显著区别。最后，在采用高温措施防控适冷病原体时，必须谨慎行事，充分考量目标物种的热敏感性以及受试动物的发育阶段。