Biophysical model of oxygen transport and metabolic regulation in the bluegill

Abstract

Consideration of biophysical mechanisms and fish anatomy leads to a plausible model of oxygen transport and metabolic regulation. The first of the model's five major components is a cardiovascular regulation submodel describing steady-state blood flow through a purely resistive vascular network. Blood flow is driven by non-pulsatile blood pressures generated by an aneural heart obeying Laplace's Law and Starling's Law of the Heart. In the second submodel, steady-state oxygen uptake is described as a counter-current, bulk-flow, mass-transport process. The third submodel implements tissue autoregulation of blood flow based on changes in the number of open capillaries in response to tissue levels of dissolved oxygen. The fourth component regulates tissues metabolic rate and performance based on oxygen availability within the tissue. The final component is an osmoregulation model describing water and solute flux between the fish and the medium. The submodels are combined in a computer program for simulating routine metabolism of bluegill (Lepomis macrochirus). Agreement between simulated and observed responses to progressive hypoxia supports the assumptions and mechanisms incorporated in the model. Simulation results indicate that the response of the oxygen-transport system to reduction in ambient dissolved oxygen is the exchange of branchial diffusive limitation for tissue diffusive limitation. Tissues respond to hypoxia by opening more capillaries, thereby enhancing diffusion gradients and exchange characteristics both of branchial and tissue exchangers. Oxygen-transport costs are reduced by enhanced diffusive characteristics and elevated by convective costs and oxygen-utilization inefficiency. The net cost of the oxygen-transport system is roughly equal to the cost required to elevate the ambient concentration of dissolved oxygen to that which would generate spontaneous diffusion of oxygen to the tissues at the metabolic rate. The oxygen-transport and metabolic-regulation model invokes only fundamental biophysical mechanisms. The model's realistic performance suggests that extrinsic hormonal or neural influences--while they may condition or enhance the control inherent in the oxygen-transport system--are not required to produce fishes' characteristics responses to progressive hypoxia at constant temperatures.