SUMMARYMany larvae and other plankton have complex and variable morphologies of unknown functional significance. We experimentally and theoretically investigated the functional consequences of the complex morphologies of larval sand dollars, Dendraster excentricus (Eschscholtz), for hydrodynamic interactions between swimming and turbulent water motion. Vertical shearing flows (horizontal gradients of vertical flow) tilt organisms with simple geometries (e.g. spheres, ellipsoids), causing these organisms to move horizontally towards downwelling water and compromising their abilities to swim upwards. A biomechanical model of corresponding hydrodynamic interactions between turbulence-induced shear and the morphologically complex four-, six-and eight-armed stages of sand dollar larvae suggests that the movements of larval morphologies differ quantitatively and qualitatively across stages and shear intensities: at shear levels typical of calm conditions in estuarine and coastal environments, all modeled larval stages moved upward. However, at higher shears, modeled four-and eight-armed larvae moved towards downwelling, whereas six-armed larvae moved towards upwelling. We also experimentally quantified larval movement by tracking larvae swimming in low-intensity shear while simultaneously mapping the surrounding flow fields. Four-and eight-armed larvae moved into downwelling water, but six-armed larvae did not. Both the model and experiments suggest that stage-dependent changes to larval morphology lead to differences in larval movement: four-and eight-armed stages are more prone than the sixarmed stage to moving into downwelling water. Our results suggest a mechanism by which differences can arise in the vertical distribution among larval stages. The ability to mitigate or exploit hydrodynamic interactions with shear is a functional consequence that potentially shapes larval evolution and development.

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Understanding evolutionary mechanisms constraining larval morphology is challenging, both because morphology has many potential functional consequences and because the impacts of morphological variation on most functions are difficult to quantify. We assessed the potential importance of swimming as a factor driving larval morphology by hypothesizing that larvae of the sand dollar Dendraster excentricus are at or near a local maximum in swimming performance as a function of their morphological characteristics. To test this hypothesis, we used a hydrodynamic model parameterized to represent the 4-armed larval stage to predict the consequences of morphological changes on larval movement in still water and shear flows. We created 3 morphological families, consisting of series in which either larval body skeleton volume, relative arm length, or arm elevation angle were incrementally altered from observed morphologies, and used upward swimming velocity as a metric of performance. For each morphological family, a wide subset of alternate morphologies performed better than the observed morphology in still water. However, in shear flows, the observed morphology consistently fell within the narrow morphological range that minimized rapid downward velocities. These results suggest that larval swimming performance, especially performance in moving water, is a driving factor in the evolution of D. excentricus larval morphology. Further, our results suggest that small morphological changes resulting from environmental shifts, such as those predicted to result from ocean acidification, may have potentially large deleterious ecological consequences.

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