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

Abstract

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) and common toad (Bufo bufo) 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 adversely affected 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.

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free‐living common toads in both natural and anthropogenic habitats

“…If sex reversal in free‐living amphibians occurs mostly due to extreme temperatures (Lambert et al, 2018; Mikó et al, 2021), the lack of sex reversal in common toads might be explained by their higher tolerance to heat. In line with this idea, the breeding season starts ~1 month later in spring for common toads than for agile frogs in our study region; accordingly, we found female‐to‐male sex reversal in agile frogs (Nemesházi et al, 2020) but not in common toads among free‐living adults, and we found the same difference between the two species in an experimental study of heat‐induced sex reversal (Ujszegi et al, 2021). Similarly, evolution of different temperature thresholds for sex reversal was suggested to explain the finding that in a reptile, Pogona vitticeps , sex reversal is absent in the hottest part of the species’ range (Castelli et al, 2021).…”

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free‐living common toads in both natural and anthropogenic habitats

“…If sex reversal in free‐living amphibians occurs mostly due to extreme temperatures (Lambert et al, 2018; Mikó et al, 2021), the lack of sex reversal in common toads might be explained by their higher tolerance to heat. In line with this idea, the breeding season starts ~1 month later in spring for common toads than for agile frogs in our study region; accordingly, we found female‐to‐male sex reversal in agile frogs (Nemesházi et al, 2020) but not in common toads among free‐living adults, and we found the same difference between the two species in an experimental study of heat‐induced sex reversal (Ujszegi et al, 2021). Similarly, evolution of different temperature thresholds for sex reversal was suggested to explain the finding that in a reptile, Pogona vitticeps , sex reversal is absent in the hottest part of the species’ range (Castelli et al, 2021).…”

Asymmetrical sex reversal: Does the type of heterogamety predict propensity for sex reversal?

“…For example, we recently found that sex ratio in the toad Bufo bufo (ZW/ZZ) was not affected by exposure to 30°C, a temperature high enough to cause up to 100% female‐to‐male sex reversal in the frog Rana dalmatina (XX/XY) in the same experiment. [ 51 ] This contradicted the broadly cited study by Piquet, [ 53 ] where 25°C produced male excess in Bufo vulgaris (a synonym for Bufo bufo ). The contradiction can be resolved by realizing that Piquet captured her animals near Geneva, in a hybrid zone of Bufo bufo and Bufo spinosus , [ 78 ] two species that were thought to be one at the time.…”

“…[ 12 ] Detailed searching methods are described in Supplement 1, and the data extracted in Supplementary Table 1. We found only four experiments in which anuran species with both male and female heterogamety were studied for sex‐reversal propensity, [ 22,49–51 ] although heterogamety was not in their focus. Other studies were usually restricted to a single species.…”

Amphibian larvae benefit from a warm environment under simultaneous threat from chytridiomycosis and ranavirosis

“…On day 20, we started thermal treatments as described in Ujszegi et al [52] (for details, including slight modifications, see the Supplementary material) and monitored tadpoles daily to record any mortality events. Water temperatures were kept at 22, 28, and 30 °C in the three thermal treatment groups, respectively (Table S1).…”

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free‐living common toads in both natural and anthropogenic habitats

“…If sex reversal in free‐living amphibians occurs mostly due to extreme temperatures (Lambert et al, 2018; Mikó et al, 2021), the lack of sex reversal in common toads might be explained by their higher tolerance to heat. In line with this idea, the breeding season starts ~1 month later in spring for common toads than for agile frogs in our study region; accordingly, we found female‐to‐male sex reversal in agile frogs (Nemesházi et al, 2020) but not in common toads among free‐living adults, and we found the same difference between the two species in an experimental study of heat‐induced sex reversal (Ujszegi et al, 2021). Similarly, evolution of different temperature thresholds for sex reversal was suggested to explain the finding that in a reptile, Pogona vitticeps , sex reversal is absent in the hottest part of the species’ range (Castelli et al, 2021).…”

Asymmetrical sex reversal: Does the type of heterogamety predict propensity for sex reversal?

“…For example, we recently found that sex ratio in the toad Bufo bufo (ZW/ZZ) was not affected by exposure to 30°C, a temperature high enough to cause up to 100% female‐to‐male sex reversal in the frog Rana dalmatina (XX/XY) in the same experiment. [ 51 ] This contradicted the broadly cited study by Piquet, [ 53 ] where 25°C produced male excess in Bufo vulgaris (a synonym for Bufo bufo ). The contradiction can be resolved by realizing that Piquet captured her animals near Geneva, in a hybrid zone of Bufo bufo and Bufo spinosus , [ 78 ] two species that were thought to be one at the time.…”

“…[ 12 ] Detailed searching methods are described in Supplement 1, and the data extracted in Supplementary Table 1. We found only four experiments in which anuran species with both male and female heterogamety were studied for sex‐reversal propensity, [ 22,49–51 ] although heterogamety was not in their focus. Other studies were usually restricted to a single species.…”

Amphibian larvae benefit from a warm environment under simultaneous threat from chytridiomycosis and ranavirosis

“…On day 20, we started thermal treatments as described in Ujszegi et al [52] (for details, including slight modifications, see the Supplementary material) and monitored tadpoles daily to record any mortality events. Water temperatures were kept at 22, 28, and 30 °C in the three thermal treatment groups, respectively (Table S1).…”

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free‐living common toads in both natural and anthropogenic habitats

“…If sex reversal in free‐living amphibians occurs mostly due to extreme temperatures (Lambert et al, 2018; Mikó et al, 2021), the lack of sex reversal in common toads might be explained by their higher tolerance to heat. In line with this idea, the breeding season starts ~1 month later in spring for common toads than for agile frogs in our study region; accordingly, we found female‐to‐male sex reversal in agile frogs (Nemesházi et al, 2020) but not in common toads among free‐living adults, and we found the same difference between the two species in an experimental study of heat‐induced sex reversal (Ujszegi et al, 2021). Similarly, evolution of different temperature thresholds for sex reversal was suggested to explain the finding that in a reptile, Pogona vitticeps , sex reversal is absent in the hottest part of the species’ range (Castelli et al, 2021).…”

Asymmetrical sex reversal: Does the type of heterogamety predict propensity for sex reversal?

“…For example, we recently found that sex ratio in the toad Bufo bufo (ZW/ZZ) was not affected by exposure to 30°C, a temperature high enough to cause up to 100% female‐to‐male sex reversal in the frog Rana dalmatina (XX/XY) in the same experiment. [ 51 ] This contradicted the broadly cited study by Piquet, [ 53 ] where 25°C produced male excess in Bufo vulgaris (a synonym for Bufo bufo ). The contradiction can be resolved by realizing that Piquet captured her animals near Geneva, in a hybrid zone of Bufo bufo and Bufo spinosus , [ 78 ] two species that were thought to be one at the time.…”

“…[ 12 ] Detailed searching methods are described in Supplement 1, and the data extracted in Supplementary Table 1. We found only four experiments in which anuran species with both male and female heterogamety were studied for sex‐reversal propensity, [ 22,49–51 ] although heterogamety was not in their focus. Other studies were usually restricted to a single species.…”

Amphibian larvae benefit from a warm environment under simultaneous threat from chytridiomycosis and ranavirosis

“…On day 20, we started thermal treatments as described in Ujszegi et al [52] (for details, including slight modifications, see the Supplementary material) and monitored tadpoles daily to record any mortality events. Water temperatures were kept at 22, 28, and 30 °C in the three thermal treatment groups, respectively (Table S1).…”