Mechanical versus physiological determinants of swimming speeds in diving Brunnich's guillemots

Abstract

For fast flapping flight of birds in air, the maximum power and efficiency of the muscles occur over a limited range of contraction speeds and loads. Thus, contraction frequency and work per stroke tend to stay constant for a given species. In birds such as auks (Alcidae) that fly both in air and under water, wingbeat frequencies in water are far lower than in air, and it is unclear to what extent contraction frequency and work per stroke are conserved. During descent, compression of air spaces dramatically lowers buoyant resistance, so that maintaining a constant contraction frequency and work per stroke should result in an increased swimming speed. However, increasing speed causes exponential increases in drag, thereby reducing mechanical versus muscle efficiency. To investigate these competing factors, we have developed a biomechanical model of diving by guillemots (Uria spp.). The model predicted swimming speeds if stroke rate and work per stroke stay constant despite changing buoyancy. We compared predicted speeds with those of a free-ranging Brunnich's guillemot (U. lomvia) fitted with a time/depth recorder. For descent, the model predicted that speed should gradually increase to an asymptote of 1.5-1.6 m s-1 at approximately 40 m depth. In contrast, the instrumented guillemot typically reached 1.5 m s-1 within 10 m of the water surface and maintained that speed throughout descent to 80 m. During ascent, the model predicted that guillemots should stroke steadily at 1.8 m s-1 below their depth of neutral buoyancy (62 m), should alternate stroking and gliding at low buoyancies from 62 to 15 m, and should ascend passively by buoyancy alone above 15 m depth. However, the instrumented guillemot typically ascended at 1.25 m s-1 when negatively buoyant, at approximately 1.5 m s-1 from 62 m to 25 m, and supplemented buoyancy with stroking above 25 m. Throughout direct descent, and during ascent at negative and low positive buoyancies (82–25 m), the guillemot maintained its speed within a narrow range that minimized the drag coefficient. In films, guillemots descending against high buoyancy at shallow depths increased their stroke frequency over that of horizontal swimming, which had a substantial glide phase. Model simulations also indicated that stroke duration, relative thrust on the downstroke versus the upstroke, and the duration of gliding can be varied to regulate swimming speed with little change in contraction speed or work per stroke. These results, and the potential use of heat from inefficient muscles for thermoregulation, suggest that diving guillemots can optimize their mechanical efficiency (drag) with little change in net physiological efficiency.