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ABSTRACT The gill surface area of aquatic ectotherms is thought to be closely linked to the ontogenetic scaling of metabolic rate, a relationship that is often used to explain and predict ecological patterns across species. However, there are surprisingly few within-species tests of whether metabolic rate and gill area scale similarly. We examined the relationship between oxygen supply (gill area) and demand (metabolic rate) by making paired estimates of gill area with resting and maximum metabolic rates across ontogeny in the relatively inactive California horn shark, Heterodontus francisci. We found that the allometric slope of resting metabolic rate was 0.966±0.058 (±95% CI), whereas that of maximum metabolic rate was somewhat steeper (1.073±0.040). We also discovered that the scaling of gill area shifted with ontogeny: the allometric slope of gill area was shallower in individuals <0.203 kg in body mass (0.564±0.261), but increased to 1.012±0.113 later in life. This appears to reflect changes in demand for gill-oxygen uptake during egg case development and immediately post hatch, whereas for most of ontogeny, gill area scales in between that of resting and maximum metabolic rate. These relationships differ from predictions of the gill oxygen limitation theory, which argues that the allometric scaling of gill area constrains metabolic processes. Thus, for the California horn shark, metabolic rate does not appear limited by theoretical surface-area-to-volume ratio constraints of gill area. These results highlight the importance of data from paired and size-matched individuals when comparing physiological scaling relationships.
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White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals
Abstract Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g., basal, resting, field, and maximally active). The scaling of metabolism is usually highly correlated with the scaling of many life-history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to (a) lower contents of expensive tissues (brains, liver, and kidneys), and (b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. An additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include (1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries; (2) studies linking scaling to ecological or phylogenetic context; (3) studies that consider multiple, possibly interacting hypotheses; and (4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate, and reproduction.
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- PAR ID:
- 10372233
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- ISSN:
- 1540-7063
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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