Scaling relationships of metabolic rate and gill surface area: Is oxygen demand limited by oxygen supply as fish grow?

Abstract

Metabolic rates of fish scale with body mass according to power-law relationships with a scaling exponent generally lower than 1. This means that animals use proportionally less oxygen as they grow; a concept which is widely accepted in experimental biology. The mechanisms driving this relationship, however, are hotly debated. The gill surface area (GSA) dictates the oxygen availability for metabolic processes and thus represents a promising candidate for explaining potentially “supply-limited” metabolic scaling relationships in fish. Here, we conducted a literature review to explore the relationships between body mass, GSA and metabolic rates of various fish species. Furthermore, we reared barramundi under optimal (29℃), warm (35℃) and cold (23℃) conditions and measured metabolic rate and GSA on multiple occasions throughout the trial. In our analyses, we introduced a new parameter, the ratio S, which provides a measure of GSA in relation to the metabolic requirements for maintenance (SSMR) and maximum activity (SAMR). We show that the scaling exponents for SSMR and SAMR are consistently close to zero, with only a few exceptions where S either increased or decreased. We furthermore show that S only decreases with body size when fish are acclimated to cooler-than-optimal temperatures. These findings suggest that GSA is sufficient to meet fish oxygen requirements throughout life, even if the temperature rises, and that growth is not universally restricted by oxygen supply limitations at the gills.