Relationship between growth and standard metabolic rate: measurement artefacts and implications for habitat use and life‐history adaptation in salmonids

Abstract

Summary1. Mass-specific standard metabolic rate (SMR, or maintenance metabolism) varies greatly among individuals. Metabolism is particularly sensitive to variation in food consumption and growth creating the potential for significant bias in measured SMR for animals that are growing (e.g. juveniles) or of uncertain nutritional status. 2. Consequently, interpreting individual variation in metabolism requires a sound understanding of the potentially confounding role of growth and the relative importance of fixed (genetic) vs. environmental drivers of SMR variation. 3. We review the role of growth in measured SMR variation in juvenile salmonids, with the goals of (i) understanding the contribution of growth (and food consumption) to SMR variation through ontogeny, (ii) understanding the relative contributions of tissue maintenance and biosynthesis (overhead costs of growth) to apparent SMR variation, and (iii) using intrinsic growth effects on SMR to model how alternate life-history strategies may influence growth and measured SMR in juvenile salmonids. 4. SMR measures on juveniles, even when post-absorptive, may be inflated by delayed growthassociated overhead costs, unless juveniles are on a maintenance ration (i.e. not growing). Empirical measurements of apparent SMR in food restricted vs. satiated 2-5 g juvenile salmon demonstrate that estimates may be inflated by as much as 67% due to delayed overhead costs of growth, even when SMR measurements are taken 35 h post-feeding. 5. These results indicate that a substantial component of variation in apparent SMR among juvenile salmonids may be associated with (i) environmentally driven variation in ration (where elevated SMR measurements are an artefact of delayed growth overhead costs), (ii) intrinsic (genetic) or plastic organ-system trade-offs related to increasing investment in metabolically expensive digestive tissue responsible for processing food and (iii) intrinsic (genetic) variation in maximum body size and growth among individuals or life-history types. We suggest that selection for differences in adult body size among resident and anadromous forms leading to differences in juvenile growth trajectories may contribute to both SMR variation and habitat segregation in freshwater, where juveniles with higher growth are constrained to foraging in high velocity habitats to meet their greater consumption needs.

Fundamental insights into ontogenetic growth from theory and fish

“…5 and 6). We believe that this phenomenon results from two trade-offs: (i) Between growth and maintenance/reproduction such that individuals of smaller species start to produce more mature kinds of cells, tissues, and organs at sizes when individuals of larger species are still allocating mostly to structures and functions devoted to growth (8,25). A dwarf goby (m ∞ = 5 mg) is already slowing growth and allocating to maintenance and reproduction when it weighs only 2.5 mg, whereas a 2.5-mg tuna (m ∞ = 500,000 g) is still a tiny larva allocating to juvenile structures and functions so as to grow at near-maximal rate.…”

“…This suggests that the fundamental features of growth may be universal or nearly so (1-7; www.fishbase.org). Nevertheless, how energy and materials are processed to regulate growth as body size changes over both ontogeny and phylogeny remain poorly understood (8). Because growth is powered by metabolism, scaling of metabolic rate, both within individuals over ontogenetic development and across species over phylogenetic evolution, is relevant.…”

Variation in Metabolic Rate among Individuals Is Related to Tissue-Specific Differences in Mitochondrial Leak Respiration

“…SMR and MMR were measured as the rate of whole-body oxygen consumption at 11.57 5 0.57C (mean 5 actual range) following a 48-h fasting period to exclude the effects of specific dynamic action (Rosenfeld et al 2015). SMR was measured first, in undisturbed fish in an open-flow system over a 20-h period.…”

Developmental and Immediate Thermal Environments Shape Energetic Trade-Offs, Growth Efficiency, and Metabolic Rate in Divergent Life-History Ecotypes of the Garter SnakeThamnophis elegans

“…While snakes are growing, we would expect to see a positive relationship between metabolic rate and growth, as has been demonstrated in field studies of garter snakes (Peterson et al 1999). Even during short-term fasting, metabolic measurements can be upwardly influenced by delayed overhead costs of growth resulting from tissue synthesis (Rosenfeld et al 2015). That our animals were on a maintenance ration and did not gain weight during the month before metabolic measurements allows us to test for trade-offs in metabolic rate and first-year growth efficiency without the confounding effect of biosynthesis associated with growth.…”

“…22.66 to 1.36 g; SD: 0.71 g), thus reducing the risk of confounding our measures of resting metabolic rate with delayed overhead costs of growth (Rosenfeld et al 2015). Metabolic chambers consisted of darkened metal cans sealed with modified lids to include a tube with a stopcock on the end.…”