Morphology–flow interactions lead to stage-selective vertical transport of larval sand dollars in shear flow

Abstract

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.

Behavioral responses of invertebrate larvae to water column cues

“…However, the additions of arms and increased size could also compromise stability by affecting the separation distance between the center of gravity and center of buoyancy [78]. Individuals with longer or a wider spread of arms might also more readily cross stream lines, thus experiencing a larger fluid torque [57,46]. These biomechanical constraints may help account for the observation that 6-armed larvae were more prone to tilting in higher turbulence compared to smaller 4-armed larvae.…”

“…If our observations in the laboratory can translate to the water column in the coastal ocean, older, 6-armed larvae would be more likely to be tilted, have slower vertical velocity and be downwardly transported in these energetic environments [46]. This differential swimming could result in selective transport, leading to ontogenetic differences in depth distribution [79,78].…”

“…Larval swimming behaviors in response to various chemical, biological, and physical cues have important implications for the adult populations [45]. For planktonic, pre-competent larvae, swimming behaviors significantly impact vertical distribution patterns which in turn shape dispersal [46,47]. For older, competent larvae, behaviors around settlement sites could significantly affect recruitment patterns [48,49,50].…”

“…For moderate swimming larvae such as oyster larvae, a plasticity in response to turbulence has been observed, where competentto-settle larvae have been observed both to sink [27] and swim upward [56,28] in high turbulence; these active behavioral responses may be regulated by body size. For weaker swimming plankton, such as larval sand dollars, it has been observed that their morphologies primarily interact passively with ambient flow [57,46]. Plutei of larval sand dollars represent an "armed morphology", for which organisms use ciliated extensions (such as arms or lobes) for feeding and swimming.…”

“…Clay and Grünbaum [46] reported that 4 and 8-armed larval sand dollars are more likely than 6-armed larvae to be passively reoriented into downwelling regions by tilting in shear flow. This tilting in shear suggests an inability to maintain a stable orientation (hereafter stability) -the larva's usual vertically-directed swimming with arms in an upright position.…”