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First published online October 5, 2007
Journal of Experimental Biology 210, 3644-3660 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.008516

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Sex and flow: the consequences of fluid shear for sperm–egg interactions

Jeffrey A. Riffell^1,*, and Richard K. Zimmer^1,2,

¹ Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095-1606, USA
² Neurosciences Program and Brain Research Institute, University of California, Los Angeles, CA 90095-1606, USA

View larger version (123K): [in this window] [in a new window]   Fig. 1. (A). Open habitat of giant kelp forest in shallow (10–15 m depth), coastal waters offshore of Point Loma, San Diego, California (photo credit: Eric Hanauer). Bar, 25 cm. (B) Within this forest, adult red abalone aggregate underneath ledges and in crevices among rocky reefs. Hydrodynamic measurements characterized the physical properties of adult microhabitats and the open forest environment (photo credit: Eric Hanauer). Bar, 15 cm. (C) Each adult male or female spawns gametes into the sea via excurrent tremata, small holes in the shell that connect the mantle cavity (exit site for reproductive products) and surrounding ocean. The epipodium (lateral lobe of the foot) contains many small tentacles that are used in sensing water motion; two large cephalic tentacles (not shown) protrude from the head (to the left, arrow) and function primarily in olfaction (photo credit: L. Ignacio Vilchis). Bar, 1.0 cm. (D) Spawning of sperm by a single adult male. Propulsive forces generated by the muscular contractions of its foot ultimately produce a gamete jet, or plume (photo credit: Larry Friesen). Bar, 0.5 cm.

View larger version (25K): [in this window] [in a new window]   Fig. 2. (A) Side-view of the experimental set-up for imaging sperm-egg interactions (not drawn to scale). Here, the Taylor-Couette apparatus is mounted vertically for use in fertilization experiments. It consists of two nested cylinders, with an 8 mm wide seawater-filled gap between them. Rin and Rout refer to the radii of the inside (6.1 cm) and outside (6.9 cm) cylinders, respectively. Counter-rotation of the two cylinders produces a steady laminar flow over a wide range of shears (0–10 s–1) at low Reynolds numbers (Re<150). Further details are provided in the text. (B) Top view of the seawater gap between vertically mounted cylinders with arrows denoting flow velocity vectors. A cross-over point of no translational velocity occurs between the counter-rotating flows. (C) A sequence of overlaid, digitized images (at 0.1 s intervals) of a single sperm, as it slips past an egg at 2 s–1. The egg is positioned at the cross-over point, and thus remains stationary, while rotating from right to left. Bar, 100 µm.

View larger version (7K): [in this window] [in a new window]   Fig. 3. Two representative spectra (with wave energy subtracted) describing the relationship between power, Suu (y axis), and frequency (x axis) of turbulent fluctuations in flow speed along a principal axis. Measurements were taken within a microhabitat harboring abalone (solid line), and 3 m away on the seafloor of an open kelp forest (dotted line). Energy dissipation rates and fluid shears were estimated from the spectral intensities of the inertial subrange (i.e. where the spectra exhibit the –5/3 slope; broken lines), following published methods (Hinze, 1975; Trowbridge, 1998).

View larger version (5K): [in this window] [in a new window]   Fig. 4. Effects of fluid shear on fertilization success. Egg concentration was held constant (103 cells ml–1), and three sperm concentrations were assayed in separate tests (see text for details). Fertilization is described as a function of log-shear, using least-squares regression to identify the best fits (106 sperm ml–1: y=83–7log10(x), r2=0.76, F1,83=166.1, P<0.001; 105 sperm ml–1: y=42.6–12.2log10(x), r2=0.81, F1,88=151.7, P<0.001; 104 sperm ml–1: y=17.9–5.7log10(x), r2=0.80, F1,87=157.7, P<0.001). Each symbol is a mean ± s.e.m.; error bars are smaller than symbol sizes in some cases.

View larger version (10K): [in this window] [in a new window]   Fig. 5. Characterization of fluid shear across the gap within a Taylor-Couette flow tank. (A) Using dead sperm as passively transported particles, results are provided for a single trial at a predicted shear of 0.5 s–1 (see Eqn 1 and Eqn 2). Each data point is the speed of a single cell, plotted as a function of position along a cross-gap transect, beginning at the cross-over point of no translational velocity and running in a straight line towards the outer wall (perpendicular to the direction of fluid motion). The slope of the line is the fluid shear, and least-squares regression indicates an excellent fit of empirical and theoretical values (ANCOVA: F1,12=0.45, P=0.50). (B) The entire data set for dead sperm trials (N=60), showing close agreement between predicted and experimental observations (ANCOVA: F1,58=0.01, P=0.92).

View larger version (16K): [in this window] [in a new window]   Fig. 6. Effects of fluid shear on sperm swim speed and direction. The mean direction of swimming is expressed in a circular coordinate system (see Table 2 and text for details). (A) Sperm swimming trajectory as evaluated with respect to the nearest egg surface. The unit vector length (r) is described as a function of log-shear, using least-squares regression to identify the best fits (live sperm, abalone eggs: y=–0.20log10(x)+0.53, r2=0.91, F1,5=30.5, P<0.01; live sperm, brine shrimp eggs: y=0.03log10(x)+0.16, r2=0.53, F1,5=4.63, P=0.10; dead sperm, abalone eggs: y=0.008log10(x)+0.17, r2=0.09, F1,5=0.40, P=0.55). (B) Sperm swimming trajectory is evaluated as in A, but with the origin facing directly into flow (live sperm, abalone eggs: y=0.15log10(x)+0.47, r2=0.92, F1,5=52.35, P<0.01; live sperm, brine shrimp eggs: y=0.19log10(x)+0.52, r2=0.90, F1,5=36.26, P<0.01; dead sperm, abalone eggs: y=0.001log10(x)+0.95, r2=0.03, F1,5=0.14, P=0.72). (C) Translational swimming speeds of sperm (live sperm, abalone eggs: y=47.6–7.8log10(x), r2=0.44, F1,199=48.4, P<0.001; live sperm, brine shrimp eggs: y=34.–0.6log10(x), r2=0.04, F1,119=0.44, P=0.49; dead sperm, abalone eggs: y=0.67–0.003log10(x), r2<0.01, F1,118=0.004, P=0.95). Each symbol is a mean ± s.e.m.; error bars are smaller than symbol sizes in some cases.

View larger version (7K): [in this window] [in a new window]   Fig. 7. Effects of fluid shear on sperm–egg encounter rate. Encounter rate is described as a function of log-shear, using least squares-regression to identify the best fits (live sperm, abalone eggs: y=1.29–0.56log10(x), r2=0.82, F1,68=86.6, P<0.001; live sperm, brine shrimp eggs: y=0.55–0.16log10(x), r2=0.67, F1,42=72.1, P<0.001; dead sperm, abalone eggs: y=0.22–0.29log10(x), r2=0.16, F1,35=10.4, P<0.01). Each symbol is a mean ± s.e.m.; error bars are smaller than symbol sizes in some cases.

View larger version (43K): [in this window] [in a new window]   Fig. 8. (A) Abalone egg rotation rate and instantaneous rotational velocity as a function of fluid shear. The line is predicted from theory (see Eqn 6 and Eqn 7), and symbols (closed circles) are values obtained in experiments. Each symbol is a mean ± s.e.m.; error bars are smaller than symbol sizes in each case. (B) The flow fields surrounding an abalone egg, solved numerically (see Eqn 7 and Eqn 8) using the Navier–Stokes equation and the finite element method. Model outputs are displayed as velocity color maps for a non-rotating (Left) and rotating (Right) egg. The x and y axes are oriented parallel or perpendicular to the direction of flow, respectively. G (s–1) is fluid shear generated in the Taylor-Couette flow tank. (C) Close-ups of flow fields shown in B.

View larger version (8K): [in this window] [in a new window]   Fig. 9. (A) Abalone sperm rotation rate as a function of fluid shear, with male gametes modeled as prolate spheroids. The line is predicted from theory (see Eqn 6), and symbols are values obtained in experiments using dead (closed circles) or live (open triangles) cells. Each symbol is a mean + s.e.m.; error bars are smaller than symbols in some cases. (B) The relationship between Fswim/Fshear and fluid shear within the Taylor-Couette apparatus. Fswim was calculated using sperm swimming speeds in the presence of abalone (filled circles, solid line) or brine shrimp (filled squares, broken line) eggs.

View larger version (32K): [in this window] [in a new window]   Fig. 10. (A) The shear stresses surrounding a rotating abalone egg. Model output is displayed as a pressure map, with x and y axes oriented parallel or perpendicular to the direction of flow, respectively. Relative to flow, two 45° transects (broken lines) were established upstream and downstream of the modeled egg surface. G (s–1) is fluid shear generated in the Taylor-Couette flow tank. (B) The relationship between Fswim/Fshear and distance from the modeled egg surface along a downstream (Left) or upstream (Right) transect. Sperm were modeled as prolate spheroids. (C) Distance from the modeled egg surface along a upstream transect where Fswim/Fshear=1, as a function of G. Local shears vary substantially near an egg surface and are incorporated into our models. Three specific conditions were evaluated: an abalone (Ab) egg (with or without rotation) and a brine shrimp (BS) egg (with rotation).