Intraspecific metabolic scaling exponent depends on red blood cell size in fishes

Abstract

The metabolic-level boundaries (MLB) hypothesis and the cell metabolism (CM) hypothesis have been proposed to explain the body mass scaling of metabolic rate. The MLB hypothesis focuses mainly on the influence of the metabolic level on the relative importance of volume and surface area constraints. The CM hypothesis focuses on the variation of cell size as the body grows. The surface area to volume ratio of individual cells may vary among species with different cell sizes, by which surface area constraints on metabolic scaling may change according to the MLB hypothesis. The present study aimed to extend the MLB and the CM hypotheses by proposing that, in addition to metabolic level, the varying cell surface area constraints among species also influence the intraspecific scaling exponents. The red blood cell area (S), and intraspecific scaling exponents for resting (b R ) and maximum metabolic rates of four species of cyprinids were assessed. The scaling exponents varied among species, but mass-specific resting metabolic rates (RMR) of each species were similar. No significant correlation was found between S and mass-specific RMR among species. As predicted, a significantly negative relationship exists between S and b R among species. The results suggest that the varying b R could be attributed to cell size differences among species, as those with larger cells may face stronger surface boundary limits, as predicted by the MLB hypothesis. This mechanism represents an additional way of relating the MLB and the CM hypotheses and does not exclude another mechanism based on the recent contextual multimodal theory.

Rediscovering and Reviving Old Observations and Explanations of Metabolic Scaling in Living Systems

“…For example, integration of the MLBH with the cell-size model helps explain why the cell-size model by itself is unsuccessful in explaining specific metabolic scaling relationships (e.g., of resting endotherms, as compared to dormant, hibernating or strenuously active animals [56]). This integration also deepens our understanding of why the scaling slope for resting metabolic rate decreases with increasing metabolic level: it may be the result of increased effects of SA-related processes at not only the organismal level, but also the cellular level [56,147]. Furthermore, when metabolic level is controlled, an increase in cell size (entailing a decrease in cellular SA/volume) should cause the metabolic scaling slope to decrease toward 2/3, as shown by a comparison of four cyprinid fish species [147].…”

“…This integration also deepens our understanding of why the scaling slope for resting metabolic rate decreases with increasing metabolic level: it may be the result of increased effects of SA-related processes at not only the organismal level, but also the cellular level [56,147]. Furthermore, when metabolic level is controlled, an increase in cell size (entailing a decrease in cellular SA/volume) should cause the metabolic scaling slope to decrease toward 2/3, as shown by a comparison of four cyprinid fish species [147].…”

“…However, this model received little attention (but see [21,141]) until it was rediscovered nearly 50 years later [142]. Since that time, many investigators have discussed the cell-size model, including providing additional theoretical formulations, conceptual justifications, and empirical tests [19,20,56,97,105,106,130,[143][144][145][146][147][148]. However, so far the model has received mixed empirical support [19,20,97,105,106,[139][140][141][142][143]145,[149][150][151][152][153][154][155].…”

Effects of Contingency versus Constraints on the Body-Mass Scaling of Metabolic Rate

“…In addition, attempts should be made to synthesize multiple models and mechanisms [10,32]. For example, synthesizing the MLBH with cell-size theory may expand the predictive power of both [26,129]. Although cell-size theory by itself cannot explain effects of T a on the metabolic scaling exponent (see Section 3.1), it can, if combined with the MLBH.…”

“…Although cell-size theory by itself cannot explain effects of T a on the metabolic scaling exponent (see Section 3.1), it can, if combined with the MLBH. Thermally increased metabolic level may cause decreases in the scaling exponent for resting metabolic rate, not only because of the increased influence of surface-area related metabolic processes at the whole body level, but also at the cellular level, a hypothesis requiring testing [10,26,129]. Other examples of multi-mechanistic models of metabolic scaling are reviewed in [10,32].…”