Post‐metamorphic carry‐over effects of larval digestive plasticity

Abstract

1.For animals with complex life cycles, conditions in the larval environment can have important effects that persist after metamorphosis. These carry-over effects may influence juvenile growth plasticity and have important fitness consequences. 2. Small juvenile red-eyed treefrogs, Agalychnis callidryas, grow faster than larger ones. We examined to what extent this growth pattern is due to carry-over effects of intraspecific larval competition. In particular, we assessed larval gut plasticity and determined whether carry-over effects could persist given the extensive gut remodelling that occurs when herbivorous larvae transition to carnivorous juveniles. 3. We reared larvae in mesocosms at low, medium and high densities and measured the size of both larval and juvenile guts, livers and fat bodies. We also monitored the timing of the onset of juvenile feeding post-metamorphosis and, after the onset of feeding, we measured intake rate and mean diet retention time. Finally, we measured juvenile metabolic rates to determine whether any organ size plasticity contributed to metabolic carry-over effects. 4. Larval density had strong effects on larval morphology with higher densities increasing gut length and decreasing liver and fat body sizes. The effects of this plasticity carried over postmetamorphosis. High larval densities produced smaller juveniles with proportionately longer guts and extremely small livers and fat bodies. There were no apparent carry-over effects on size-specific metabolic rate. 5. Differences in larval density were also associated with differences in post-metamorphic feeding. Small juveniles from high larval densities began feeding even before metamorphosis was complete, whereas large juveniles from low larval densities experienced a significant 2-week delay. Although juvenile body mass varied over threefold across treatments, once feeding was initiated, neither intake nor mean diet retention time scaled with body size. 6. Overall, high larval densities produced small juveniles with very low lipid reserves that may have stimulated hyperphagia relative to larger juveniles. Longer guts carried over from the larval stage could facilitate this by allowing small juveniles to elevate intake without sacrificing diet retention time. Patterns of intake coupled with differences in the onset of feeding explain the size-dependent growth pattern previously reported in this and other species.

How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian

“…The existence of compensatory growth (i.e. an increase in growth rates once the conditions are favourable in order to compensate partly or completely the deprivations experienced in younger stages) has been reported in various taxa [37] and can be the result of behavioural modifications, such as prolonged foraging activity and higher ingestion rates [6,38,39], or morphological adaptations that allow digestion of larger quantities of food [40]. However, a higher than optimal growth rate comes at a fitness cost, reflected in decreased survival [37].…”

“…However, a higher than optimal growth rate comes at a fitness cost, reflected in decreased survival [37]. Along with ecological factors, such as increased exposure to predators and competitors because of prolonged foraging [38], several other components can contribute to the lower fitness associated with accelerated growth rates, amongst which a lower resistance to starvation because of intense metabolism and low lipid reserves [40], delayed ossification [41], depressed immunological function [42], or cellular oxidative stress [43]. Some of the intrinsic costs mentioned above might have contributed to the observed higher mortality in the froglets that had metamorphosed at a small size in our study.…”

Altered thyroid hormone levels affect body condition at metamorphosis in larvae of Xenopus laevis

“…As TH is not only critical for amphibian metamorphosis but also for the regulation of energy metabolism (Frieden, ; McNabb & King, ; Sheridan, ), altered TH levels as caused by several environmental stressors may also affect energetic body condition (i.e., maintenance costs and energy stores) at metamorphosis. Larval anurans fuel the energy required for metamorphosis by resorbing their tail muscle as well as by using stores of fat in the liver, a key organ for lipid storage in ectothermic animals (Bouchard, O'Leary, Wargelin, Charbonnier, & Warkentin, ; Jelodar & Fazli, ; Sheridan & Kao, ). The higher the energy metabolism, and thus, animals' maintenance costs, the less energy can be stored in tail and liver tissue (Orlofske & Hopkins, ; Sheridan & Kao, ).…”

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

“…However, these smaller sized individuals from ephemeral conditions then demonstrated increased growth rates immediately after emergence, possibly to compensate for suboptimal size at metamorphosis. Compensatory growth of smaller individuals exposed to stressful larval conditions has been observed in other frog species (Boone, 2005;Bouchard et al, 2016). The increased growth rates of the individuals from ephemeral conditions may explain why larval hydroperiod was not significant in our analysis of individual movement.…”

“…Early life stages can be more susceptible to shifting environmental conditions than adults, an effect that has been observed in diverse taxa from reptiles to butterflies (Radchuk et al, 2013;Levy et al, 2015). Several carryover effects to larval stress in anurans have been observed: for example, drying conditions experienced by developing Túngara frog tadpoles reduced leg length and jumping performance (Charbonnier and Vonesh, 2015), and high larval densities of Red-eyed treefrogs resulted in smaller juveniles with reduced livers and fat bodies (Bouchard et al, 2016).…”