Gills, growth, and activity across fishes

Abstract Life history theory argues that an organism’s maximum size and its corresponding growth rate have evolved to maximize lifetime reproductive output. The Gill Oxygen Limitation Theory suggests that in aquatic organisms, maximum size is instead constrained by the surface area of the gills, the primary site of gas exchange with the environment. A central prediction of this theory is a tight relationship among maximum size, growth, and gill surface area. Yet since this idea was first tested in the early 1980s, data availability has increased and analytical methods have advanced considerably. Here, we revisit this relationship with new data and a novel phylogenetic Bayesian multilevel modeling framework that allows us to understand how individual variation in gill surface area confers relationships of maximum size, growth, and gills across species. Specifically, we bring gill surface area into an allometric context and examine whether the gill surface area for a given body size (intercept) and the rate at which gill surface changes with size (slope), for a given species, explains growth performance -- an index integrating the life history tradeoff between growth and maximum size -- across fish species. Additionally, we assess whether variation in von Bertalanffy growth coefficients across species can be explained by gill surface area. Finally, we explore whether additional factors – here, activity and evolutionary history -- explain variation in maximum size and growth across species. Overall, we find that although a positive relationship exists among maximum size, growth, and gill surface area across fishes, it is weak. Additionally, gill surface area does not explain much variation in growth coefficients across species, especially for those that reach the same maximum size. However, we find that the activity level of a fish explains more variation in maximum size and growth across species compared to gill surface area. Our results support the idea that in fishes, growth and maximum size are not simply related to gill surface area, and that other covariates—both tractable (e.g., activity, metabolic rate, temperature) and less tractable (e.g., predation risk, resource availability, and variation)—appear to explain more variation in life history traits across species.