Investigating the gill-oxygen limitation hypothesis in fishes: intraspecific scaling relationships of metabolic rate and gill surface area

Abstract Many ectotherms have shown a reduction in maximum body size in the past decades in parallel with climate warming. Indeed, some models forecast a maximum body size decline of 14%–24% by 2050 for numerous fish species. The gill-oxygen limitation (GOL) hypothesis is perhaps the most prominent concept regarding the physiological mechanisms underlying the observed trends, implicating oxygen uptake limitations in driving the decline in fish body size with warming. Current scientific debates, however, demonstrate a clear need for a synthesis of existing empirical evidence to test the fundamental assumptions of the GOL hypothesis. Here, we perform a systematic literature review of the intraspecific allometry of gill surface area (GSA) and metabolic rate. Additionally, we introduce 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). Support for the GOL hypothesis would be evidenced by a universal decline in S with increasing body mass within each species, such that gills become less equipped to supply metabolic requirements as fish grow. In contrast to the predictions of the GOL hypothesis, 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. These findings suggest that the GSA of each species is sufficient to meet its oxygen requirements throughout life, and that growth is not universally restricted by oxygen uptake limitations across the gills. We identify the need to investigate hypotheses other than the GOL hypothesis to help explain the observed declines in maximum fish body sizes concurrent with climate warming, in order to facilitate accurate predictions of fish community structure and manage fisheries in the face of climate change.