Gill surface area allometry does not constrain the body mass scaling of maximum oxygen uptake rate in the tidepool sculpin, Oligocottus maculosus

The gill oxygen limitation hypothesis (GOLH) suggests that hypometric scaling of metabolic rate in fishes is a consequence of oxygen supply constraints imposed by the mismatched growth rates of gill surface area (a two-dimensional surface) and body mass (a three-dimensional volume). GOLH may, therefore, explain the size-dependent spatial distribution of fish in temperature-and oxygen-variable environments through size-dependent respiratory capacity, but this question is unstudied. We tested GOLH in the tidepool sculpin, Oligocottus maculosus, a species in which body mass decreases with increasing temperature-and oxygen-variability in the intertidal, a pattern consistent with GOLH. We statistically evaluated support for GOLH versus distributed control of ?Mo-2 allometry by comparing scaling coefficients for gill surface area, standard and maximum ?Mo-2( ?Mo(2,Standard )and ?Mo-e,Mo-Max, respectively), ventricle mass, hematocrit, and metabolic enzyme activities in white muscle. To empirically evaluate whether there is a proximate constraint on oxygen supply capacity with increasing body mass, we measured ?Mo-2,Max across a range of Po(2)s from normoxia to P-crit, calculated the regulation value (R), a measure of oxyregulatory capacity, and analyzed the R-body mass relationship. In contrast with GOLH, gill surface area scaling either matched or was more than sufficient to meet ?Mo-2 demands with increasing body mass and R did not change with body mass. Ventricle mass (b = 1.22) scaled similarly to ?Mo-2,Mo-Max (b = 1.18) suggesting a possible role for the heart in the scaling of ?Moe,Max. Together our results do not support GOLH as a mechanism structuring the distribution of O. maculosus and suggest distributed control of oxyregulatory capacity.

Automated summary

The gill oxygen limitation hypothesis suggests that the scaling of metabolic rate in fishes is limited by oxygen supply due to mismatched growth rates of gill surface area and body mass. This study tested the hypothesis in Oligocottus maculosus and found no support for it, suggesting a distributed control of oxyregulatory capacity instead. Gill surface area scaling was sufficient to meet oxygen demand and respiratory capacity did not change with body mass. These results indicate that the hypothesis does not explain the distribution of O. maculosus.