Environmental conditions experienced during the tadpole stage alter post-metamorphic glucocorticoid response to stress in an amphibian.

Abstract

Exposure to adverse environmental conditions during early development can shape life-history traits and have lasting effects on physiological function in later life. Although findings within the biomedical literature have shown that environmentally induced elevations in glucocorticoids (GCs) during critical developmental windows can cause persistent carry-over effects (i.e., developmental programming), little is known about whether such effects of GCs can be generalized to wildlife species. Using wood frogs as a study species, we conducted an experiment with a split-plot design to assess the short-term and the long-term physiological consequences of availability of food, hydroperiod length (i.e., pond drying), and the interaction between these two environmental conditions. In outdoor experimental ponds, we reared tadpoles in chronically high or low-food conditions, and tadpoles from each pond experienced either high water until metamorphosis or a reduction in water volume during late developmental stages (after Gosner stage 38). After metamorphosis, animals were housed individually and fed ad libitum for 10 weeks, and growth rate, fat content, and resting and acute stress-induced GC levels were measured. We found that tadpoles experiencing low availability of food and reduced water volume had elevated GC levels, reduced mass, and body condition as they approached metamorphosis. At 10 weeks after metamorphosis, we found that these two conditions also had persistent interactive effects on post-metamorphic allocation of resources to growth, energy storage, and responsiveness of GCs to a novel stressor. Of individuals that experienced reduced water volume, only those that experienced high food as tadpoles were able to catch up to individuals that did not experience reduced water volume in terms of body mass, femur length, and body condition, and they allocated more resources to fat storage. By contrast, 10-week old frogs with low-food and that experienced low water volume and low-food levels as tadpoles allocated fewer resources to mass-specific growth, stored less fat, and exhibited blunted GC response to a novel stressor relative to those that did not experience water-reduction. Our findings demonstrate that environmental conditions experienced prior to and during important developmental transitions shape resource allocation and the ability to physiologically respond to future stressors in juvenile and potentially adult animals. These results suggest that chronic and acute environmental stressors experienced during early life stages can have cumulative and interactive effects that need to be considered when modeling the ecological and evolutionary consequences of environmental change on populations.