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

Abstract

Background: In species with complex life cycles, size at metamorphosis is a key life-history trait which reflects the complex interactions between costs and benefits of life in the aquatic and terrestrial environments. Whereas the effects of a deteriorating larval habitat (e.g. pond desiccation) on triggering an early metamorphosis have been extensively investigated in amphibians, the consequences of the resulting reduced size at metamorphosis on fitness in the post-metamorphic terrestrial stage remain poorly understood. We tested the hypothesis that a smaller size at metamorphosis negatively affects performance and survival in the ensuing terrestrial stage. Using as model a tropical amphibian (Ceratophrys stolzmanni) showing a large phenotypic plasticity in metamorphosing traits, we evaluated the effects of size at metamorphosis on fitness-related trophic and locomotor performance traits, as well as on growth and survival rates. Results:Our results support the hypothesis that a larger size at metamorphosis is correlated with better survival and performance. The survival rate of large metamorphosing individuals was 95%, compared to 60% for those completing metamorphosis at a small size. Locomotor performance and gape size were positively correlated with body size, larger animals being more mobile and capable to ingest larger prey. However, smaller individuals achieved higher growth rates, thus reducing the size gap. Conclusions:Overall, size at metamorphosis affected profoundly the chances of survival in the short term, but smaller surviving individuals partly compensated their initial disadvantages by increasing growth rates. BackgroundSpecies with complex life cycles, such as biphasic amphibians and insects, are able to exploit different ecological niches and optimize their life-history in discrete developmental stages [1,2]. The transition occurring at metamorphosis usually requires dramatic and irreversible morphological transformations, and is frequently accompanied by a complete change of the ecological niche [3,4]. Pond-breeding amphibians, which in their post-larval stages become terrestrial, represent ideal models to investigate the independence of pre-and postmetamorphic life-stages and the presence of carry-over effects from one stage to the other, affecting the overall fitness of individuals [5]. The most evident trade-off between the aquatic and terrestrial stages is reflected in body size at metamorphosis. When the aquatic larvae are confronted with unfavourable conditions, such as food shortage [6,7], high density [8], desiccation risk

Effects of Desiccation on Metamorphic Climax in Bombina variegata: Changes in Levels and Patterns of Oxidative Stress Parameters

“…Smaller body sizes without accelerated developmental rates at the end of the metamorphosis of B. variegata individuals during a period of desiccation when compared to individuals developing under steady water availability were reported by Sinsch et al [ 7 ] and Böll [ 45 ]. The body size can reflect on various processes and fitness traits in amphibian larvae, including metabolism, resistance to pathogens, feeding behavior, locomotion, escape from predators [ 6 , 20 ]. In adults, body size can also affect mortality rate, age and size at first reproduction or fecundity [ 6 , 13 ].…”

“…The body size can reflect on various processes and fitness traits in amphibian larvae, including metabolism, resistance to pathogens, feeding behavior, locomotion, escape from predators [6,20]. In adults, body size can also affect mortality rate, age and size at first reproduction or fecundity [6,13].…”

“…There is evidence that climate change, especially temperature-related change, can alter reproductive phenology, body condition and sensitivity to disease in amphibians [ 5 ]. The shortening of wetland hydroperiods has resulted in an increased frequency of reproductive failure for many amphibian species that use temporary or even ephemeral aquatic habitats for reproduction [ 5 , 6 ]. In particular, pond drying is affecting the development of anuran larvae [ 7 ].…”

“…It can lead to changes in water temperature, larval densities, food availability and host-pathogen or predator-prey interactions—all of which are directly linked to survival [ 8 ]. Larvae exposed to desiccation pressure need to make an ontogenetic niche shift before a pond dries up [ 6 ]. This shift, however, carries trade-offs that may have short- and long-term costs [ 9 ].…”

“…This shift, however, carries trade-offs that may have short- and long-term costs [ 9 ]. Costs could be seen in various morphological and physiological traits, e.g., reduced size at metamorphosis, leading to smaller maturation size, lower fecundity, reduction of hindlimb length, accelerated development, higher metabolic rates and alterations in oxidative metabolism and the immune system [ 6 , 7 , 8 , 10 , 11 , 12 , 13 ].…”