Fish gill surface area can keep pace with metabolic oxygen requirements across body mass and temperature

Abstract

Abstract Climate warming is driving the maximum attainable size of many fish species to decrease, yet the mechanisms underlying this ‘shrinking’ phenomenon are not well understood. The gill oxygen limitation (GOL) hypothesis is perhaps the most prominent mechanistic proposition, asserting that, as fish grow, the two‐dimensional gill surface area (GSA) progressively fails to supply enough oxygen to support the continued growth of the three‐dimensional body—a process exacerbated by increased metabolism associated with warming. However, these ideas have been hotly debated owing to limited empirical understanding of how GSA develops with respect to a fish's body mass and oxygen requirements. For the first time, we addressed this knowledge gap by rearing Galaxias maculatus for 5 months at normal (15°C) and elevated (20°C) summer temperatures, with (hyperoxia) or without (normoxia) supplementary oxygen. Quantifying individual metabolic rate and GSA traits across body sizes encompassing most of the species' ontogeny, we found little evidence for a change in the proportion of GSA available per unit of metabolic rate (termed the S metric) and no improvements under hyperoxia. Importantly, at the elevated temperature where gill oxygen limitation should be most pronounced, the S metric did not change across body mass in either oxygen treatment (allometric exponents were no different from 0). These results indicate that the gills can grow in ways that support an individual's oxygen requirements, contrasting with the suggestion that size reductions of fish in response to climate warming are driven by an insurmountable geometric constraint at the gills. Read the free Plain Language Summary for this article on the Journal blog.