Post-Metamorphic Carry-Over Effects in a Complex Life History: Behavior and Growth at Two Life Stages in an Amphibian,<i>Anaxyrus fowleri</i>

Yagi, Katharine T.; Green, David M.

doi:10.1643/ce-17-593

Cited by 15 publications

(11 citation statements)

References 81 publications

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“…This study offers a physiological-based understanding of how environmental stressors can dramatically disturb the balance among growth, development, cardiac activity and energy storage during amphibian ontogeny by endocrine disruption. Even if juveniles disperse from their larval habitat, they might suffer from direct and indirect carry-over effects of endocrine disruption experienced during metamorphosis ( Ruthsatz et al, 2019 ; Yagi and Green, 2018 ; Bouchard et al, 2016 ; Sinsch et al, 2020 ). Moreover, metamorphosis is not a new beginning ( Pechenik et al, 1998 ), since migration capacity in amphibians is often limited ( Yu et al, 2013 ; Sinsch, 2014 ) and metamorphs might also experience stressful environmental conditions in terrestrial habitats continuing endocrine disruption of TH and other hormone systems.…”

Section: Discussionmentioning

confidence: 99%

Shifts in sensitivity of amphibian metamorphosis to endocrine disruption: the common frog (Rana temporaria) as a case study

Ruthsatz

Dausmann

Paesler

et al. 2020

Conservation Physiology

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Effective conservation actions require knowledge on the sensitivity of species to pollution and other anthropogenic stressors. Many of these stressors are endocrine disruptors (EDs) that can impair the hypothalamus–pituitary–thyroid axis and thus alter thyroid hormone (TH) levels with physiological consequences to wildlife. Due to their specific habitat requirements, amphibians are often sentinels of environmental degradation. We investigated how altered TH levels affected the bioenergetics of growth and development (i.e. age, size, metabolism, cardiac function and energy stores) before, during and after metamorphosis in the European common frog (Rana temporaria). We also determined how ontogenetic stage affected susceptibility to endocrine disruption and estimated juvenile performance. TH levels significantly affected growth and energetics at all developmental stages. Tadpoles and froglets exposed to high TH levels were significantly younger, smaller and lighter at all stages compared to those in control and low TH groups, indicating increased developmental and reduced growth rates. Across all ontogenetic stages tested, physiological consequences were rapidly observed after exposure to EDs. High TH increased heart rate by an average of 86% and reduced energy stores (fat content) by 33% compared to controls. Effects of exposure were smallest after the completion of metamorphosis. Our results demonstrate that both morphological and physiological traits of the European common frog are strongly impacted by endocrine disruption and that ontogenetic stage modulates the sensitivity of this species to endocrine disruption. Since endocrine disruption during metamorphosis can impair the physiological stress response in later life stages, long-term studies examining carry-over effects will be an important contribution to the conservation physiology of amphibians.

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Section: Discussionmentioning

confidence: 99%

Shifts in sensitivity of amphibian metamorphosis to endocrine disruption: the common frog (Rana temporaria) as a case study

Ruthsatz

Dausmann

Paesler

et al. 2020

Conservation Physiology

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“…Higher larval temperatures generally produce smaller and younger metamorphs (see meta-analysis by Ruthsatz et al, 2018), but the functional consequences of this beyond metamorphosis is unclear; in our present study high embryonic incubation temperature did not affect hatchling size of these eurythermal frogs. Larval density has been shown to influence size and digestive morphology after metamorphosis (Bouchard et al, 2016; Yagi and Green, 2018). A recent study with R. temporaria suggests larval thermal tolerance may not persist beyond metamorphosis, and therefore water temperature exposure during larval development may not confer protective or deleterious effects on juveniles (Enriquez-Urzelai et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…There is evidence that embryonic temperature has impacts on amphibian physiology beyond hatching. Such alterations in performance due to previous life history or conditions have been referred to as “carry-over effects” (O’Connor et al, 2014; Yagi and Green, 2018). Amphibians have shown carry-over/persistent effects from the thermal conditions of embryonic and/or larval development.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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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.

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“…Evidence from other amphibian species have also found reduced growth rates in dry conditions creating potential multiplicative effects of environmental conditions, as size was the central determinant of movement (Gomez-Mestre and Tejedo, 2005;Charbonnier et al, 2018). Other research on carry-over effect in amphibians has supported the need for longitudinal studies (Johansson et al, 2010;Charbonnier and Vonesh, 2015;Yagi and Green, 2018). With this broader understanding, we would be better able to combine aquatic structure with terrestrial habitat management to provide for essential habitat components of threatened species (Fellers and Kleeman, 2007;Bartelt and Klaver, 2017).…”

Section: Discussionmentioning

confidence: 98%

Starting on the Right Foot: Carryover Effects of Larval Hydroperiod and Terrain Moisture on Post-metamorphic Frog Movement Behavior

et al. 2019

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Changing patterns of precipitation and drought will dramatically influence the distribution and persistence of lentic habitats. Pond-breeding amphibians can often respond to changes in habitat by plastically shifting behavioral and developmental trait response. However, fitness tradeoffs inherent in life history strategies can carry over to impact development, behavior, and fitness in later life stages. In this experiment, we investigated carryover effects of hydroperiod permanence on the movement behavior of newly-metamorphosed juvenile Northern Red-legged Frogs (Rana aurora). Frogs were raised through metamorphosis in mesocosms under either permanent or ephemeral hydroperiod conditions. After metamorphosis, individuals were removed from the mesocosms, measured, uniquely tagged with elastomer, and moved to holding terrariums. Movement behavior was quantified under two terrain conditions: a physiologically-taxing, dry runway treatment, or a control, moist runway treatment. Individuals were given 30 min to move down the 1 × 20m enclosed structure before distance was measured. We applied a hurdle model to examine two distinct components of movement behavior: (1) the probability of moving away from the start location, and (2) movement distance. We found that hydroperiod condition had an indirect carryover effect on movement via the relationship between individual size and the propensity to move. Individuals from ephemeral mesocosm conditions metamorphosed at a smaller size but showed increased growth rates as compared to individuals from permanent hydroperiod conditions. Individual snout-vent length and runway condition (moist or dry) were significant predictors of both aspects of movement behavior. Larger individuals were more likely to move down the runway and able to move a farther distance than smaller individuals. In addition to the influence of size, dry runway conditions reduced the probability of individuals moving from the start location, but increased the distance traveled relative to the moist runway. The demonstrated cumulative impact of stressors suggests the importance of addressing direct, indirect, and carryover effects of stressors throughout ontogeny.

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Post-Metamorphic Carry-Over Effects in a Complex Life History: Behavior and Growth at Two Life Stages in an Amphibian,Anaxyrus fowleri

Cited by 15 publications

References 81 publications

Shifts in sensitivity of amphibian metamorphosis to endocrine disruption: the common frog (Rana temporaria) as a case study

Shifts in sensitivity of amphibian metamorphosis to endocrine disruption: the common frog (Rana temporaria) as a case study

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

Starting on the Right Foot: Carryover Effects of Larval Hydroperiod and Terrain Moisture on Post-metamorphic Frog Movement Behavior

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