American Society of Naturalists

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“Oxygen limitation at the larval stage and the evolution of maternal investment per offspring in aquatic environments”

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Njal Rollinson and Locke Rowe (May 2018)

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Maternal effects on body size are constrained in aquatic systems by O2 transport in larvae, not by the geometry of eggs

Aquatic life histories are shaped by oxygen limitation that arises at the larval stage

Green Frog (<i>Lithobates clamitans</i>).<br />Gouache and art marker. By Melanie Massey, 2016.
Green Frog (Lithobates clamitans).
Gouache and art marker. By Melanie Massey, 2016.

In aquatic environments, a common observation is that mothers produce small eggs under warm conditions, a pattern that loosely comprises part of the well-known “temperature-size rule”. For decades, it was emphasized that oxygen limitation may drive this pattern in ectotherms: small eggs and embryos evolve in warm environments because metabolic rate of the embryo is high, and large eggs with low surface-area-to-volume ratios would become oxygen-limited. More recently, however, this idea has been turned on its head, as several studies have suggested that egg size per se does not influence the availability of oxygen to embryos, mainly because embryonic oxygen consumption increases with egg size more slowly than does the surface area of the egg that is available for gas exchange. Why then might egg size, and hence maternal investment per offspring, decrease as environmental temperature increases? Drawing from hundreds of amphibian species across two major clades, the authors use comparative methods to show that oxygen limitation at the larval stage, not the egg stage, helps explain variation in investment per offspring in aquatic environments. Large larvae may be oxygen limited because respiratory features, such as gills, are underdeveloped in early life, resulting in diffusive cutaneous oxygen uptake as a primary means of sustaining aerobic activity during a life stage where predation risk is high. This work helps extend the generality of temperature-dependent oxygen limitation as a mechanism driving the temperature-size rule in aquatic systems.


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 vs 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 prior to metamorphosis, compared to those that can. Our results suggest 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.