Abstract

Explanations for the hypoallometric scaling of metabolic rate through ontogeny generally fall into two categories: supply-side constraints on delivery of oxygen, or decreased mass-specific intrinsic demand for oxygen. In many animals, supply and demand increase together as the body grows, thus making it impossible to tease apart the relative contributions of changing supply and demand to the observed scaling of metabolic rate. In larval insects, the large components of the tracheal system are set in size at each molt, but then remain constant in size until the next molt. Larvae of Manduca sexta increase up to ten-fold in mass between molts, leading to increased oxygen need without a concomitant increase in supply. At the molt, the tracheal system is shed and replaced with a new, larger one. Due to this discontinuous growth of the tracheal system, insect larvae present an ideal system in which to examine the relative contributions of supply and demand of oxygen to the ontogenetic scaling of metabolic rate. We observed that the metabolic rate at the beginning of successive instars scales hypoallometrically. This decrease in specific intrinsic demand could be due to a decrease in the proportion of highly metabolically active tissues (the midgut) or to a decrease in mitochondrial activity in individual cells. We found that decreased intrinsic demand, mediated by a decrease in the proportion of highly metabolically active tissues in the fifth instar, along with a decrease in the specific mitochondrial activity, contribute to the hypoallometric scaling of metabolic rate.

Highlights

  • The scaling of metabolic rate with body size has been the subject of many empirical and theoretical studies [1,2,3,4,5,6,7,8,9,10,11,12,13]

  • Scaling exponent based on the primary hypothesis that the transport of rate-limiting metabolites constrains nutrient usage due to the geometry of a space-filling distribution network with the following properties: the terminal branches of the fractal supply network are invariant with body size, the energy required to circulate fluid through the system is minimized, and the volume of the network occupies a constant proportion of the total body volume

  • The pre-critical weight, within-instar scaling exponents are higher than the whole-instar scaling exponents measured by [13]; the difference is due to the fact that metabolic rate levels off after critical weight in each instar [23], so the exponent is lower when the post-critical weight data are included

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Summary

Introduction

The scaling of metabolic rate with body size has been the subject of many empirical and theoretical studies [1,2,3,4,5,6,7,8,9,10,11,12,13]. Brown and Enquist (1997) (WBE) argued that the hypoallometric scaling of metabolic rate is a necessary consequence of fractally branching supply networks They derive the L scaling exponent based on the primary (albeit somewhat implicit) hypothesis that the transport of rate-limiting metabolites constrains nutrient usage due to the geometry of a space-filling distribution network with the following properties: the terminal branches of the fractal supply network are invariant with body size, the energy required to circulate fluid through the system is minimized, and the volume of the network occupies a constant proportion of the total body volume. The supply-based constraint hypothesis assumes that the metabolic rate is somehow restricted by the rate at which the material needs for metabolism can be supplied and that this constraint results in the observed hypoallometric relation between mass and metabolic rate

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