Embryonic Developmental Temperatures Modulate Thermal Acclimation of Performance Curves in Tadpoles of the Frog Limnodynastes peronii

Seebacher, Frank; Grigaltchik, Veronica S.

doi:10.1371/journal.pone.0106492

Cited by 46 publications

(43 citation statements)

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“…Even though growth is maximised at warm temperatures in L. peronii (Seebacher and Grigaltchik, 2014), tadpoles in the warm Tadpoles from warm microcosms (red bars) had higher CS activities than those from cold microcosms (blue bars; B), and this pattern was reversed for COX (C; significant differences are indicated by asterisks). There were two-way interactions between incubation temperature and predation for LDH and CS, and in both cases survivors from predation incubated at 25°C had lower activities compared with no-predator controls (D,E).…”

Section: Discussionmentioning

confidence: 99%

“…Metabolic traits parallel locomotor responses and provide fast glycolytic energy (ATP) release to facilitate burst performance, or slower sustained mitochondrial ATP production to support longerlasting movement and growth. There may be a positive relationship between growth rate and temperature (Seebacher and Grigaltchik, 2014). However, often predators have a preference for larger individuals, and tadpoles of Rana sylvatica are smaller in the presence of predators .…”

Section: Introductionmentioning

confidence: 99%

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Developmental thermal plasticity of prey modifies the impact of predation

Seebacher

Grigaltchik

2015

Journal of Experimental Biology

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Environmental conditions during embryonic development can influence the mean expression of phenotypes as well as phenotypic responses to environmental change later in life. The resulting phenotypes may be better matched to their environment and more resilient to environmental change, including human-induced climate change. However, whether plasticity does improve success in an ecological context is unresolved. In a microcosm experiment, we show that developmental plasticity in embryos of the frog Limnodynastes peronii is beneficial by increasing survivorship of tadpoles in the presence of predators when egg incubation (15 or 25°C) and tadpole acclimation temperature in microcosms (15 or 25°C) coincided at 15°C. Tadpoles that survived predation were smaller, and had faster burst swimming speeds than those kept in no-predator control conditions, but only at high (25°C) egg incubation or subsequent microcosm temperatures. Metabolic rates were determined by a three-way interaction between incubation and microcosm temperatures and predation; maximal glycolytic and mitochondrial metabolic capacities (enzyme activities) were lower in survivors from predation compared with controls, particularly when eggs were incubated at 25°C. We show that thermal conditions experienced during early development are ecologically relevant by modulating survivorship from predation. Importantly, developmental thermal plasticity also impacts population phenotypes indirectly by modifying species interactions and the selection pressure imposed by predation.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Developmental thermal plasticity of prey modifies the impact of predation

Seebacher

Grigaltchik

2015

Journal of Experimental Biology

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“…Acclimation allows animals to overcome (to varying degrees) the challenges associated with mean temperature change (Wilson and Franklin, 1999;Seebacher and Grigaltchik, 2014). Many ectotherms, however, appear to lack the capacity to physiologically respond to DTFs in a way that allows them to prevent increased metabolic demands associated with peak environmental temperatures (Henry and Houston, 1984;Kingsolver et al, 2009;Niehaus et al, 2011;Kjörsgaard et al, 2013;Kern et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…These species can breed successfully in a range of habitats from permanent dams and lakes to ephemeral flooded grasslands and pools (Anstis, 2002). Limnodynastes peronii tadpoles have the capacity to acclimate to stable temperatures and have been shown to have thermally sensitive TPCs in the early stages of development (Wilson and Franklin, 1999;Niehaus et al, 2011;Seebacher and Grigaltchik, 2014).…”

Section: Study Speciesmentioning

confidence: 99%

Physiological responses of ectotherms to daily temperature variation

Kern

Cramp

Franklin

2015

Journal of Experimental Biology

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Daily thermal fluctuations (DTFs) impact the capacity of ectotherms to maintain performance and energetic demands because of thermodynamic effects on physiological processes. Mechanisms that reduce the thermal sensitivity of physiological traits may buffer ectotherms from the consequences of DTFs. Species that experience varying degrees of DTFs in their environments may differ in their responses to thermally variable conditions, if thermal performance curves reflect environmental conditions. We tested the hypothesis that in response to DTFs, tadpoles from habitats characterised by small DTFs would show greater plasticity in the thermal sensitivity of physiological processes than tadpoles from environments characterised by large DTFs. We tested the thermal sensitivity of physiological traits in tadpoles of three species that differ naturally in their exposure to DTFs, raised in control (24°C) and DTF treatments (20-30°C and 18-38°C). DTFs reduced growth in all species. Development of tadpoles experiencing DTFs was increased for tadpoles from highly thermally variable habitats (∼15%), and slower in tadpoles from less thermally variable habitats (∼30%). In general, tadpoles were unable to alter the thermal sensitivity of physiological processes, although DTFs induced plasticity in metabolic enzyme activity in all species, although to a greater extent in species from less thermally variable environments. DTFs increased upper thermal limits in all species (between 0.89 and 1.6°C). Our results suggest that the impact of increased thermal variability may favour some species while others are negatively impacted. Species that cannot compensate for increased variability by buffering growth and development will probably be most affected.

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“…These responses buffer organisms from the energetic costs and physiological constraints of environmental variation by optimising physiological function in the new environment and increasing physiological tolerance to these conditions. The capacity to flexibly alter phenotypes in response to environmental perturbation is widespread, and can involve changes in behaviour, physiology and gene expression, which buffer fitness under new conditions (Wilson and Franklin, 1999;Podrabsky and Somero, 2004;Seebacher and Grigaltchik, 2014). While physiological adjustments are unlikely to fully overcome the consequences of environmental variation, the capacity to mitigate the associated costs may be important in determining species persistence in the future (Seebacher et al, 2015).…”

Section: Environmental Variationmentioning

confidence: 99%

Physiological responses to daily temperature variation and ultraviolet radiation in amphibian larvae

Kern¹

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Understanding how environmental variability influences species fitness is important for predicting species persistence in changing environments. Environments are highly variable and organisms have discrete physiological limits which determine the range of conditions they can tolerate. Daily thermal fluctuations (DTFs) impact the capacity of ectotherms to maintain performance and energetic demands due to thermodynamic effects on physiological rates. However, organisms can also flexibly alter their phenotype in order to maintain fitness in variable environments. Ectotherms experiencing DTFs would benefit from mechanisms which reduce the thermal sensitivity of physiological traits and buffer energetic costs. Furthermore, energetic consequences of DTFs may be exacerbated by the presence of additional stressors. Exposure to ultraviolet radiation (UVR) can increase energy requirements due to the repair of UVR induced damage. The costs of UVR exposure may cause energy trade-offs which exacerbate consequences of DTFs, and reduce the capacity to flexibly alter phenotypes. Importantly, temperature and UVR are also linked in their effects on cellular function as exposure to temperature extremes and UVR causes cellular damage that induces common protective mechanisms. Interactive effects of these environmental drivers on mechanistic traits may explain whole animal responses. Understanding what drives responses to temperature variation and the interactive effects between environmental stressors will broaden our understanding of how animals respond to environmental variation. The overarching aim of this thesis was to investigate physiological mechanisms underlying responses to DTFs and exposure to UVR in amphibian larvae. The capacity to flexibly alter the thermal sensitivity of traits in response to DTFs may depend on the degree of environmental DTF species experience. The first specific aim of this thesis was to investigate whether plasticity in response to DTFs is influenced by the thermal variability of a species' habitat (Chapter 2). Tadpoles of three related species whose habitats vary in the degree of DTF were raised in stable temperatures and conditions in which temperatures fluctuated daily. Plasticity of upper thermal limits and the thermal sensitivity of swimming performance, resting metabolic rate and metabolic enzyme activity were examined. Environmental variation in species habitats did not predict the capacity to alter physiological rate processes. Tadpoles were unable to reduce the thermal sensitivity of physiology traits, which led to smaller body sizes and altered the length of development in a species specific fashion. DTFs increased upper thermal limits which may ii buffer tadpoles from the lethal consequences of temperature extremes. The effects of DTFs on growth and development however, will likely negatively impact individual fitness. The second specific aim of this thesis was to investigate whether UVR exposure alters the physiological response to DTFs (Chapter 3). Tadpoles were raised in stable or dai...

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Embryonic Developmental Temperatures Modulate Thermal Acclimation of Performance Curves in Tadpoles of the Frog Limnodynastes peronii

Cited by 46 publications

References 47 publications

Developmental thermal plasticity of prey modifies the impact of predation

Developmental thermal plasticity of prey modifies the impact of predation

Physiological responses of ectotherms to daily temperature variation

Physiological responses to daily temperature variation and ultraviolet radiation in amphibian larvae

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