Immediate and Persistent Effects of Temperature on Oxygen Consumption and Thermal Tolerance in Embryos and Larvae of the Baja California Chorus Frog, Pseudacris hypochondriaca

Abstract

The developmental environment has significant immediate effects on phenotypes, but it may also persistently or permanently shape phenotypes across life history. This study examined how developmental temperature influenced embryonic and larval phenotypes of Baja California chorus frog ( Pseudacris hypochondriaca ), an abundant amphibian in southern California and northern Baja California. We collected egg clutches from native ponds in northern San Diego County within 24 h of fertilization, and clutches were separated and distributed between constant temperatures of 10, 15, 20, and 25°C for incubation. Oxygen consumption rate ( O 2 ), developmental stage, and embryo and yolk masses were measured throughout development. Time to 50% hatch, survival at 50% hatch, and hatch duration were determined. Development rate was strongly affected by temperature, with warmer temperatures reducing time to hatch and hatch duration. Survival to hatch was high across all temperatures, >90%. Mass-specific O 2 of embryos either remained constant or increased throughout development, and by hatching energy demand was significantly increased at higher temperatures. There were limited temperature effects on growth, with embryo and yolk dry mass similar between temperatures throughout embryonic development. To examine long-term effects of embryonic temperature, we reared hatchlings from each temperature until onset of larval feeding. Once feeding, larvae were acclimated to 20 or 25°C (>2 weeks). Following acclimation to 20 or 25°C, we measured larval mass-specific O 2 and critical thermal maximum (CTMax) at a common developmental stage (Gosner stages 32–36, “hindlimb toe differentiation”). Embryonic temperature had persistent effects on larval O 2 and CTMax, with warmer temperatures generally resulting in similar or higher O 2 and CTMax. This partially supported a “warmer is better” effect of embryonic incubation temperature. These results suggest that in a thermally robust amphibian species, temperature may program the phenotype during early development to construct traits in thermal tolerance and energy use that may persist. Overall, P. hypochondriaca displays a thermally robust phenotype, and it is possible that amphibians that possess a wider range of phenotypic plasticity will be relatively more successful mitigating effects of climate change.

Variation in developmental temperature alters adulthood plasticity of thermal tolerance in Tigriopus californicus

“…Consistent with this relationship, several studies have demonstrated loss of ATP synthesis capacity in heart mitochondria at temperatures that are approximately equal to or are immediately below the upper thermal limits in species of fishes (Iftikar and Hickey, 2013;Christen et al, 2018;O'Brien et al, 2018). Temperature-mediated plasticity of mitochondrial functions is also often observed in ectothermic species (e.g., Guderley, 2004;Seebacher et al, 2010;Chung and Schulte, 2015;Chung et al, 2017aChung et al, ,b, 2018Bryant et al, 2018), and our data suggest that this is the case in T. californicus.…”

“…likely increase the concordance between developmental and adulthood temperatures (particularly in the habitats of T. californicus). This may contribute to the effects of developmental temperature on adulthood plasticity of thermal tolerance in this species, because developmental effects are expected to be stronger if conditions in development are predictive of those experienced as adults (Cooper et al, 2010(Cooper et al, , 2012Nettle and Bateson, 2015;Beaman et al, 2016). Consistent with this possibility, in the comparatively longlived zebrafish, Schaefer and Ryan (2006) observed only subtle shifts in CT max plasticity in adults as a result of differences in developmental temperatures.…”

Variation in developmental temperature alters adulthood plasticity of thermal tolerance in Tigriopus californicus

“…Consistent with this relationship, several studies have demonstrated loss of ATP synthesis capacity in heart mitochondria at temperatures that are approximately equal to or are immediately below the upper thermal limits in species of fishes (Iftikar and Hickey, 2013;Christen et al, 2018;O'Brien et al, 2018). Temperature-mediated plasticity of mitochondrial functions is also often observed in ectothermic species (e.g., Guderley, 2004;Seebacher et al, 2010;Chung and Schulte, 2015;Chung et al, 2017aChung et al, ,b, 2018Bryant et al, 2018), and our data suggest that this is the case in T. californicus.…”

“…likely increase the concordance between developmental and adulthood temperatures (particularly in the habitats of T. californicus). This may contribute to the effects of developmental temperature on adulthood plasticity of thermal tolerance in this species, because developmental effects are expected to be stronger if conditions in development are predictive of those experienced as adults (Cooper et al, 2010(Cooper et al, , 2012Nettle and Bateson, 2015;Beaman et al, 2016). Consistent with this possibility, in the comparatively longlived zebrafish, Schaefer and Ryan (2006) observed only subtle shifts in CT max plasticity in adults as a result of differences in developmental temperatures.…”

Differential sensitivity to warming and hypoxia during development and long-term effects of developmental exposure in early life stage Chinook salmon

“…Stage-specific responses and sensitivity to higher temperatures during development could be influenced by differences in cellular stress defence mechanisms such as the heat shock protein response, which can vary over development ( Whitehouse et al , 2017 ). Similar studies in other ectotherms, including invertebrates ( Healy et al , 2019 ) and amphibians ( Mueller et al , 2019 ) also found increases in the thermal tolerance of later life stages after exposure to warm temperatures during development. Further research on the persistent effects of developmental warm temperature exposures on juvenile fish thermal tolerance is needed to understand the variability across fish species and life stages as the carry-over effects of embryonic temperature may become more important in the thermal tolerance of species under temperatures that are predicted to increase and become more variable with climate change.…”

Ontogeny of the Heat‐Induced Hatching Response in the Red‐Eyed Treefrog, Agalychnis callidryas

“…Higher temperatures increase embryos' metabolic rates, increasing oxygen demand and waste production; simultaneously, they reduce oxygen availability, due to lower solubility in warmer water (Mueller et al 2019). The risk of toxicity from accumulating ammonia is exacerbated by the concentrating effect of egg dehydration (Méndez-Narváez and Warkentin 2022), and warming speeds evaporative water loss (Guevara-Molina et al 2022;and unpublished data).…”

“…Although embryonic acclimation can affect CT Max in later stages, studies rarely assess thermal tolerance across embryonic development itself, focusing instead on broad stage comparisons (i.e., embryos vs. larvae vs. adults, e.g., Cowan et al 2023;Lechner et al 2024;Mueller et al 2019;Ruthsatz et al 2022). Thus, our findings of consistent VT Max across embryonic development in A. callidryas may represent the first evidence of ontogenetic stability of thermal tolerance within the embryonic stage.…”

Variation in developmental temperature alters adulthood plasticity of thermal tolerance in Tigriopus californicus

“…Consistent with this relationship, several studies have demonstrated loss of ATP synthesis capacity in heart mitochondria at temperatures that are approximately equal to or are immediately below the upper thermal limits in species of fishes (Iftikar and Hickey, 2013;Christen et al, 2018;O'Brien et al, 2018). Temperature-mediated plasticity of mitochondrial functions is also often observed in ectothermic species (e.g., Guderley, 2004;Seebacher et al, 2010;Chung and Schulte, 2015;Chung et al, 2017aChung et al, ,b, 2018Bryant et al, 2018), and our data suggest that this is the case in T. californicus.…”

“…likely increase the concordance between developmental and adulthood temperatures (particularly in the habitats of T. californicus). This may contribute to the effects of developmental temperature on adulthood plasticity of thermal tolerance in this species, because developmental effects are expected to be stronger if conditions in development are predictive of those experienced as adults (Cooper et al, 2010(Cooper et al, , 2012Nettle and Bateson, 2015;Beaman et al, 2016). Consistent with this possibility, in the comparatively longlived zebrafish, Schaefer and Ryan (2006) observed only subtle shifts in CT max plasticity in adults as a result of differences in developmental temperatures.…”

Differential sensitivity to warming and hypoxia during development and long-term effects of developmental exposure in early life stage Chinook salmon

“…Stage-specific responses and sensitivity to higher temperatures during development could be influenced by differences in cellular stress defence mechanisms such as the heat shock protein response, which can vary over development ( Whitehouse et al , 2017 ). Similar studies in other ectotherms, including invertebrates ( Healy et al , 2019 ) and amphibians ( Mueller et al , 2019 ) also found increases in the thermal tolerance of later life stages after exposure to warm temperatures during development. Further research on the persistent effects of developmental warm temperature exposures on juvenile fish thermal tolerance is needed to understand the variability across fish species and life stages as the carry-over effects of embryonic temperature may become more important in the thermal tolerance of species under temperatures that are predicted to increase and become more variable with climate change.…”

Ontogeny of the Heat‐Induced Hatching Response in the Red‐Eyed Treefrog, Agalychnis callidryas

“…Higher temperatures increase embryos' metabolic rates, increasing oxygen demand and waste production; simultaneously, they reduce oxygen availability, due to lower solubility in warmer water (Mueller et al 2019). The risk of toxicity from accumulating ammonia is exacerbated by the concentrating effect of egg dehydration (Méndez-Narváez and Warkentin 2022), and warming speeds evaporative water loss (Guevara-Molina et al 2022;and unpublished data).…”

“…Although embryonic acclimation can affect CT Max in later stages, studies rarely assess thermal tolerance across embryonic development itself, focusing instead on broad stage comparisons (i.e., embryos vs. larvae vs. adults, e.g., Cowan et al 2023;Lechner et al 2024;Mueller et al 2019;Ruthsatz et al 2022). Thus, our findings of consistent VT Max across embryonic development in A. callidryas may represent the first evidence of ontogenetic stability of thermal tolerance within the embryonic stage.…”

Variation in developmental temperature alters adulthood plasticity of thermal tolerance in Tigriopus californicus

“…Consistent with this relationship, several studies have demonstrated loss of ATP synthesis capacity in heart mitochondria at temperatures that are approximately equal to or are immediately below the upper thermal limits in species of fishes (Iftikar and Hickey, 2013;Christen et al, 2018;O'Brien et al, 2018). Temperature-mediated plasticity of mitochondrial functions is also often observed in ectothermic species (e.g., Guderley, 2004;Seebacher et al, 2010;Chung and Schulte, 2015;Chung et al, 2017aChung et al, ,b, 2018Bryant et al, 2018), and our data suggest that this is the case in T. californicus.…”

“…likely increase the concordance between developmental and adulthood temperatures (particularly in the habitats of T. californicus). This may contribute to the effects of developmental temperature on adulthood plasticity of thermal tolerance in this species, because developmental effects are expected to be stronger if conditions in development are predictive of those experienced as adults (Cooper et al, 2010(Cooper et al, , 2012Nettle and Bateson, 2015;Beaman et al, 2016). Consistent with this possibility, in the comparatively longlived zebrafish, Schaefer and Ryan (2006) observed only subtle shifts in CT max plasticity in adults as a result of differences in developmental temperatures.…”

Differential sensitivity to warming and hypoxia during development and long-term effects of developmental exposure in early life stage Chinook salmon

“…Stage-specific responses and sensitivity to higher temperatures during development could be influenced by differences in cellular stress defence mechanisms such as the heat shock protein response, which can vary over development ( Whitehouse et al , 2017 ). Similar studies in other ectotherms, including invertebrates ( Healy et al , 2019 ) and amphibians ( Mueller et al , 2019 ) also found increases in the thermal tolerance of later life stages after exposure to warm temperatures during development. Further research on the persistent effects of developmental warm temperature exposures on juvenile fish thermal tolerance is needed to understand the variability across fish species and life stages as the carry-over effects of embryonic temperature may become more important in the thermal tolerance of species under temperatures that are predicted to increase and become more variable with climate change.…”

Ontogeny of the Heat‐Induced Hatching Response in the Red‐Eyed Treefrog, Agalychnis callidryas

“…Higher temperatures increase embryos' metabolic rates, increasing oxygen demand and waste production; simultaneously, they reduce oxygen availability, due to lower solubility in warmer water (Mueller et al 2019). The risk of toxicity from accumulating ammonia is exacerbated by the concentrating effect of egg dehydration (Méndez-Narváez and Warkentin 2022), and warming speeds evaporative water loss (Guevara-Molina et al 2022;and unpublished data).…”

“…Although embryonic acclimation can affect CT Max in later stages, studies rarely assess thermal tolerance across embryonic development itself, focusing instead on broad stage comparisons (i.e., embryos vs. larvae vs. adults, e.g., Cowan et al 2023;Lechner et al 2024;Mueller et al 2019;Ruthsatz et al 2022). Thus, our findings of consistent VT Max across embryonic development in A. callidryas may represent the first evidence of ontogenetic stability of thermal tolerance within the embryonic stage.…”