Mechanisms and Consequences of Developmental Acceleration in Tadpoles Responding to Pond Drying

Abstract

Many amphibian species exploit temporary or even ephemeral aquatic habitats for reproduction by maximising larval growth under benign conditions but accelerating development to rapidly undergo metamorphosis when at risk of desiccation from pond drying. Here we determine mechanisms enabling developmental acceleration in response to decreased water levels in western spadefoot toad tadpoles (Pelobates cultripes), a species with long larval periods and large size at metamorphosis but with a high degree of developmental plasticity. We found that P. cultripes tadpoles can shorten their larval period by an average of 30% in response to reduced water levels. We show that such developmental acceleration was achieved via increased endogenous levels of corticosterone and thyroid hormone, which act synergistically to achieve metamorphosis, and also by increased expression of the thyroid hormone receptor TRΒ, which increases tissue sensitivity and responsivity to thyroid hormone. However, developmental acceleration had morphological and physiological consequences. In addition to resulting in smaller juveniles with proportionately shorter limbs, tadpoles exposed to decreased water levels incurred oxidative stress, indicated by increased activity of the antioxidant enzymes catalase, superoxide dismutase, and gluthatione peroxidase. Such increases were apparently sufficient to neutralise the oxidative damage caused by presumed increased metabolic activity. Thus, developmental acceleration allows spadefoot toad tadpoles to evade drying ponds, but it comes at the expense of reduced size at metamorphosis and increased oxidative stress.

The ‘male escape hypothesis’: sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian

“…Our experiment mimics an extreme, but natural and frequent situation, i.e. the end of pond drying (see also [24] for a similar setting). The fact that very few newts metamorphosed in the high water level treatment-which remains relatively low in comparison with the range of values found in the field [35]-is likely adaptive.…”

“…Their expression in populations depends on the advantages of living in the aquatic and terrestrial habitats [4]. Because environmental cues play an important role in pushing amphibian larvae to metamorphose in most species [2,23,24], environmental variations are supposed to maintain the two phenotypes in populations because each one is adapted to specific conditions.…”

Compensating for delayed hatching reduces offspring immune response and increases life‐history costs

“…Elevated corticosteroid levels may interact with the immune system and act as immunostimulants, although chronically high expression of corticosteroids leads to immunosuppression (Dhabhar , Martin ). As rapidly developing, compensating tadpoles are expected to have higher corticosteroid concentrations (Gomez‐Mestre et al ), it seems possible that their immune defence could be compromised. The only study we are aware of that examined amphibian immune response in relation to growth and development found that accelerated development in response to pond desiccation risk reduced immune response in postmetamorphic wood frogs (Gervasi and Foufopoulos ).…”

Effects of Water Loss on New Mexico Spadefoot Toad (Spea multiplicata) Development, Spleen Cellularity, and Corticosterone Levels

“…As previously stated, CORT induces apoptosis of lymphocytes in many organisms and spikes during amphibian metamorphic climax (Rollins‐Smith et al., ; Rollins‐Smith, ; Verburg‐Van Kemenade et al., ). Thus, exposure to high CORT levels earlier than normal is predicted to cause premature immunosuppression in developing amphibian larvae (Rollins‐Smith and Blair, ; Rollins‐Smith, ; Gomez‐Mestre et al., ). We observed fewer leukocytes/μg spleen in Experiment 1 GS 36 and post‐meta individuals reared in a declining versus constant water environment, with a greater difference in Group 2 tadpoles.…”

“…Although corticosterone (CORT) can aid in expediting amphibian metamorphosis, numerous studies have revealed a decrease in metamorphic size with accelerated development (Hayes and Licht, ; Wright et al., ; Glennemeier and Denver, ). This type of phenotypic plasticity is present in many amphibian species, but can have trade‐offs (Newman, ; Gray and Smith ; Gervasi, ; McMurry et al., ; Gomez‐Mestre et al., ; Warne and Crespi, ). These carryover effects can have direct influence on body size, survival, immunocompetence, and fitness potential of juvenile frogs and can potentially remain into adulthood (Chelgren et al., , ; Boes and Bernard, ; Crespi and Warne, ; Krynak et al., ; Tarvin et al., ; Warne and Crespi, ).…”