Effects of body mass on physiological and anatomical parameters of mature salmon: evidence against a universal heart rate scaling exponent

Farrell, Anthony P.

doi:10.1242/jeb.051607

Cited by 32 publications

(23 citation statements)

References 47 publications

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“…While it was not possible to measure heart rate recovery in jacks in the present study, this is an obvious next step once appropriately-sized technology is developed. Nevertheless, resting heart rate is not dependent on body mass in mature Chinook salmon spanning a mass range of 2.7 to 16.8 kg [33], and cardiac output scales isometrically in Chinook salmon over the body mass range that has been examined to date (2.1–5.4 kg; [5], [33]). Others have demonstrated for a range of fish species that gill surface area generally scales with body mass with an exponent around 0.8 [34], [35], which is expectedly lower than the scaling exponent of 1.06 determined for the gill basket mass of coho salmon in the present study (Fig.…”

Section: Discussionmentioning

confidence: 96%

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Physiological Benefits of Being Small in a Changing World: Responses of Coho Salmon (Oncorhynchus kisutch) to an Acute Thermal Challenge and a Simulated Capture Event

et al. 2012

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Evidence is building to suggest that both chronic and acute warm temperature exposure, as well as other anthropogenic perturbations, may select for small adult fish within a species. To shed light on this phenomenon, we investigated physiological and anatomical attributes associated with size-specific responses to an acute thermal challenge and a fisheries capture simulation (exercise+air exposure) in maturing male coho salmon (Oncorhynchus kisutch). Full-size females were included for a sex-specific comparison. A size-specific response in haematology to an acute thermal challenge (from 7 to 20°C at 3°C h−1) was apparent only for plasma potassium, whereby full-size males exhibited a significant increase in comparison with smaller males (‘jacks’). Full-size females exhibited an elevated blood stress response in comparison with full-size males. Metabolic recovery following exhaustive exercise at 7°C was size-specific, with jacks regaining resting levels of metabolism at 9.3±0.5 h post-exercise in comparison with 12.3±0.4 h for full-size fish of both sexes. Excess post-exercise oxygen consumption scaled with body mass in male fish with an exponent of b = 1.20±0.08. Jacks appeared to regain osmoregulatory homeostasis faster than full-size males, and they had higher ventilation rates at 1 h post-exercise. Peak metabolic rate during post-exercise recovery scaled with body mass with an exponent of b∼1, suggesting that the slower metabolic recovery in large fish was not due to limitations in diffusive or convective oxygen transport, but that large fish simply accumulated a greater ‘oxygen debt’ that took longer to pay back at the size-independent peak metabolic rate of ∼6 mg min−1 kg−1. Post-exercise recovery of plasma testosterone was faster in jacks compared with full-size males, suggesting less impairment of the maturation trajectory of smaller fish. Supporting previous studies, these findings suggest that environmental change and non-lethal fisheries interactions have the potential to select for small individuals within fish populations over time.

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Section: Discussionmentioning

confidence: 96%

“…Since ventricle mass scales isometrically with body mass in salmonids (Fig. 3C; [33]), it may be reasonable to assume that cardiac stroke volume also scales proportionally. While it was not possible to measure heart rate recovery in jacks in the present study, this is an obvious next step once appropriately-sized technology is developed.…”

Section: Discussionmentioning

confidence: 99%

Physiological Benefits of Being Small in a Changing World: Responses of Coho Salmon (Oncorhynchus kisutch) to an Acute Thermal Challenge and a Simulated Capture Event

et al. 2012

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“…heartbeat and breathing rate: see Millidine, Metcalfe & Armstrong, 2008;Green, 2011;Bishop & Spivey, 2013; but note that even variation in heartbeat may not always be congruent with that of metabolic rate developmentally, allometrically or in response to temperature change: Barrionuevo & Burggren, 1999;Clark & Farrell, 2011;. heartbeat and breathing rate: see Millidine, Metcalfe & Armstrong, 2008;Green, 2011;Bishop & Spivey, 2013; but note that even variation in heartbeat may not always be congruent with that of metabolic rate developmentally, allometrically or in response to temperature change: Barrionuevo & Burggren, 1999;Clark & Farrell, 2011;.…”

Section: (8) Temperature Effectsmentioning

confidence: 99%

Is metabolic rate a universal ‘pacemaker’ for biological processes?

2014

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A common, long-held belief is that metabolic rate drives the rates of various biological, ecological and evolutionary processes. Although this metabolic pacemaker view (as assumed by the recent, influential 'metabolic theory of ecology') may be true in at least some situations (e.g. those involving moderate temperature effects or physiological processes closely linked to metabolism, such as heartbeat and breathing rate), it suffers from several major limitations, including: (i) it is supported chiefly by indirect, correlational evidence (e.g. similarities between the body-size and temperature scaling of metabolic rate and that of other biological processes, which are not always observed) - direct, mechanistic or experimental support is scarce and much needed; (ii) it is contradicted by abundant evidence showing that various intrinsic and extrinsic factors (e.g. hormonal action and temperature changes) can dissociate the rates of metabolism, growth, development and other biological processes; (iii) there are many examples where metabolic rate appears to respond to, rather than drive the rates of various other biological processes (e.g. ontogenetic growth, food intake and locomotor activity); (iv) there are additional examples where metabolic rate appears to be unrelated to the rate of a biological process (e.g. ageing, circadian rhythms, and molecular evolution); and (v) the theoretical foundation for the metabolic pacemaker view focuses only on the energetic control of biological processes, while ignoring the importance of informational control, as mediated by various genetic, cellular, and neuroendocrine regulatory systems. I argue that a comprehensive understanding of the pace of life must include how biological activities depend on both energy and information and their environmentally sensitive interaction. This conclusion is supported by extensive evidence showing that hormones and other regulatory factors and signalling systems coordinate the processes of growth, metabolism and food intake in adaptive ways that are responsive to an organism's internal and external conditions. Metabolic rate does not merely dictate growth rate, but is coadjusted with it. Energy and information use are intimately intertwined in living systems: biological signalling pathways both control and respond to the energetic state of an organism. This review also reveals that we have much to learn about the temporal structure of the pace of life. Are its component processes highly integrated and synchronized, or are they loosely connected and often discordant? And what causes the level of coordination that we see? These questions are of great theoretical and practical importance.

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“…However, b m values far from 1.0 have also been observed in some species [4], [7], [32]. It has been suggested that further experimental analysis is required to study the intraspecific scaling exponents in species that span a wide range of M [33]–[34].…”

Section: Introductionmentioning

confidence: 99%

Intraspecific Scaling of the Resting and Maximum Metabolic Rates of the Crucian Carp (Carassius auratus)

et al. 2013

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The question of how the scaling of metabolic rate with body mass (M) is achieved in animals is unresolved. Here, we tested the cell metabolism hypothesis and the organ size hypothesis by assessing the mass scaling of the resting metabolic rate (RMR), maximum metabolic rate (MMR), erythrocyte size, and the masses of metabolically active organs in the crucian carp (Carassius auratus). The M of the crucian carp ranged from 4.5 to 323.9 g, representing an approximately 72-fold difference. The RMR and MMR increased with M according to the allometric equations RMR = 0.212M 0.776 and MMR = 0.753M 0.785. The scaling exponents for RMR (b r) and MMR (b m) obtained in crucian carp were close to each other. Thus, the factorial aerobic scope remained almost constant with increasing M. Although erythrocyte size was negatively correlated with both mass-specific RMR and absolute RMR adjusted to M, it and all other hematological parameters showed no significant relationship with M. These data demonstrate that the cell metabolism hypothesis does not describe metabolic scaling in the crucian carp, suggesting that erythrocyte size may not represent the general size of other cell types in this fish and the metabolic activity of cells may decrease as fish grows. The mass scaling exponents of active organs was lower than 1 while that of inactive organs was greater than 1, which suggests that the mass scaling of the RMR can be partly due to variance in the proportion of active/inactive organs in crucian carp. Furthermore, our results provide additional evidence supporting the correlation between locomotor capacity and metabolic scaling.

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Effects of body mass on physiological and anatomical parameters of mature salmon: evidence against a universal heart rate scaling exponent

Cited by 32 publications

References 47 publications

Physiological Benefits of Being Small in a Changing World: Responses of Coho Salmon (Oncorhynchus kisutch) to an Acute Thermal Challenge and a Simulated Capture Event

Physiological Benefits of Being Small in a Changing World: Responses of Coho Salmon (Oncorhynchus kisutch) to an Acute Thermal Challenge and a Simulated Capture Event

Is metabolic rate a universal ‘pacemaker’ for biological processes?

Intraspecific Scaling of the Resting and Maximum Metabolic Rates of the Crucian Carp (Carassius auratus)

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