Oxygen Limitation at the Larval Stage and the Evolution of Maternal Investment per Offspring in Aquatic Environments.

Abstract

Oxygen limitation and surface area to volume relationships of the egg were long thought to constrain egg size in aquatic environments, but more recent evidence indicates that egg size per se does not influence oxygen availability to embryos. Here, we suggest that investment per offspring is nevertheless constrained in aquatic anamniotes by virtue of oxygen transport in free-living larvae. Drawing on the well-supported assumption that oxygen limitation is relatively pronounced in aquatic versus terrestrial environments and that oxygen limitation is particularly severe in warm aquatic environments, we employ comparative methods in the Amphibia to investigate this problem. Across hundreds of species and two major amphibian clades, the slope of species mean egg diameter over habitat temperature is negative for species with aquatic larvae but is positive or neutral for species featuring terrestrial eggs and no larvae. Yet across species with aquatic larvae, the negative slope of egg diameter over temperature is similar whether eggs are laid terrestrially or aquatically, consistent with an oxygen constraint arising at the larval stage. Finally, egg size declines more strongly with temperature for species that cannot breathe aerially before metamorphosis compared with those that can. Our results suggest that oxygen transport in larvae (not eggs) constrains investment per offspring. This study further extends the generality of temperature-dependent oxygen limitation as a mechanism driving the temperature-size rule in aquatic systems.