Revised estimates of the effects of turbulence on fertilization in the purple sea urchin, Strongylocentrotus purpuratus.

Turbulent water motion can either aid or hinder external fertilization in aquatic organisms. On one hand, turbulence provides the mixing necessary to bring eggs and sperm together; on the other, the forces imposed by turbulent eddies may interfere with the attachment of sperm to eggs and may even damage zygotes. Mead and Denny (1) explored this dichotomy by measuring the efficacy of fertilization in the purple sea urchin (Strongylocentrotus purpuratus) while gametes were subjected to sheared flow in a Couette cell. When calculated rates of turbulent energy dissipation exceeded 100 W/m, fertilization and early development were severely affected. Dissipation rates of this magnitude are common in breaking waves, and Mead and Denny therefore concluded that turbulent flow could be a substantial environmental hindrance to sexual reproduction in nearshore urchins. However, the rates of energy dissipation calculated by Mead and Denny for the Couette cell were erroneously small. Here we use direct measurements of energy dissipation rates to show that fertilization success can exceed 80% even when dissipation is as high as 2200 W/m, higher than the dissipation likely to be found in breaking waves. Thus, many energetic flow environments that were previously thought to be detrimental to external fertilization may instead be benign or advantageous. The majority of benthic marine invertebrates reproduce sexually via external fertilization. The effectiveness of this strategy has been the subject of much recent research, and the roles of water motion in “fertilization ecology” have been debated (for a review, see (2)). Given the limited swimming capabilities of sperm, if adults are separated by more than a few centimeters some water motion is required to bring sperm and eggs together. To this end, turbulence (and the bulk mixing that it causes) are advantageous. However, this mixing can occur only if water is sheared, and as a result, turbulence inevitably imposes viscous forces on gametes (3). If these forces inhibit the attachment of sperm to eggs or damage the gametes or zygote, the advantages of mixing can be negated. Whether turbulence is an aid to fertilization or a hindrance thus depends in part on where the line is drawn between effective mixing and shearinduced damage. Mead and Denny (1) and Mead (4) examined this issue by measuring the ability of sea urchin gametes to fertilize under the controlled imposition of turbulent flow. Eggs of S. purpuratus were introduced into a volume of water contained in the space between two coaxial cylinders (a Couette cell, Fig. 1A). When the outer cylinder was rotated, the water was sheared, and, by varying the rate of rotation, the shear stress imposed on gametes could be controlled. Once the apparatus was up to speed, sperm were introduced at a concentration sufficient to result in 80%–90% fertilization in still water, and fertilization was allowed to proceed for 2 min. A volume of KCl solution was then introduced into the cell to prohibit further fertilization, and the percentage of eggs fertilized was determined. With these results in hand, the turbulence intensity in the Couette cell was compared to the intensity characteristic of the wave-swept habitat in which S. purpuratus is found. The translation from laboratory to field conditions was made via the turbulent dissipation rate (measured in W/m), the rate at which turbulence-induced shear stress in the water converts the energy of the moving fluid into heat (1, 5): Received 25 July 2002; accepted 16 October 2002. * To whom correspondence should be addressed. E-mail: mwdenny@ leland.stanford.edu 1 Present address: Department of Integrative Biology, University of California, Berkeley, California 94720. Reference: Biol. Bull. 203: 275–277. (December 2002)