The effect of near‐bed turbulence on sperm dilution and fertilization success of broadcast‐spawning bivalves

Abstract

Lay Abstract Many marine and some freshwater bottom‐dwelling (benthic) invertebrates broadcast their gametes into the water column where fertilization occurs. The relatively slow swimming speed and rapid dilution of sperm by water currents is thought to limit fertilization, even though species that reproduce this way can be extremely successful. We examined how water velocity and bottom roughness affected the fertilization success of zebra and quagga mussels (Dreissena polymorpha and D. bugensis) in a laboratory flow chamber and in Lake Erie. Our results demonstrate that velocity gradients dilute the concentration of sperm to levels that can lead to sperm limitation. We also found that the strength and pattern of the turbulence in the water flow near the bottom had a strong effect on fertilization. Bottom roughness that led to the ejection of fluid away from the bottom—such as what occurs downstream of a patch of mussels—contributed to higher fertilization success than bottom roughness that led to skimming flows or sweeps of flow toward the bed. Bottom roughness needs to be considered in biological and other transport processes occurring near the bottom. Biologically, dreissenid mussels are the first freshwater benthic organisms that have been shown to be sperm limited. Ecologically, the presence of their shells in the flow chamber and on the lakebed in Lake Erie created sufficient roughness to affect fertilization success. In other words, the mussels had changed the physical environment in a way that favored their reproduction. This new observation helps to explain why dreissenid mussels are successful invaders of freshwater ecosystems.

Effect of steady and unsteady flow on chemoattractant plume formation and sperm taxis

“…The paths of swimming sperm have been observed in the field (Babcock et al, 1994;Miller and Mundy, 2005;Quinn and Ackerman, 2011), and more typically under a microscope (Böhmer et al, 2005;Cosson et al, 1984;Evans et al, 2012;Guerrero et al, 2010a;Himes et al, 2011;Inamdar et al, 2007;Morita et al, 2006;Riffell and Zimmer, 2007;Riffell et al, 2002Riffell et al, , 2004Wood et al, 2005;Yoshida et al, 1993;Zimmer and Riffell, 2011) leading to a basic understanding of swimming patterns and parameters. Two distinct sperm behaviors have been observed: one (called loitering behavior) corresponding to sperm exposed to a chemoattractant concentration below the response threshold, and the other (called response behavior) corresponding to exposure above the threshold.…”

“…Fertilization was enhanced for shear rates less than α = 1 s −1 , yet fertilization decreased in shear rates exceeding α = 1 s − 1 (Riffell and Zimmer, 2007;Zimmer and Riffell, 2011). Increases in energy dissipation rates (Denny et al, 2002), bed roughness (Quinn and Ackerman, 2011), flow velocity (Levitan et al, 1992) and turbulence (Denny and Shibata, 1989;Denny et al, 1992;Levitan and Young, 1995) have also been shown to decrease success rates. Additionally, the preference of a sperm for certain eggs within a single species (Evans et al, 2012), and viability of both the egg and sperm (Giorgi and DeMartini, 1977) can decrease actual and predicted fertilization rates.…”

The effect of bottom roughness on scalar transport in aquatic ecosystems: Implications for reproduction and recruitment in the benthos

“…Such flow would allow gametes to enter and be retained in areas (i.e., spaces between roughness elements) where gametes could become concentrated, as well as allowing some gametes to be transported downstream where there may encounter gametes from other individuals. In the field, however, local populations of dressenid mussels appear to exist under conditions of skimming flow, i.e., k¼10 to 15 cm and λ $ 30 cm (Quinn and Ackerman, 2011). It remains to be determined whether gamete release in benthic organisms occurs under flow conditions that enhance gamete encounter via wake interference flow (e.g., marine algae; Pearson et al, 1998).…”

“…However, it should be noted that an alternate choice of λ and k could have resulted in different λ/k ratios leading to isolated-roughness and wake-interference flows, where settlement would likely increase. Quinn and Ackerman (2011, 2012, 2014, found that mussel shells placed uniformly at high density on the bottom of a flow chamber led to skimming flow, in contrast to wake-interference flow observed under a low mussel-density configuration.…”

“…In terms of the roughness spacing, λ, seven values at 10-cm intervals from 20 to 80 cm were used, which were combined with seven values of the roughness height, k, at 2-cm intervals from 2 to 14 cm, to provide a total of 49 combinations of λ/k ranging from 1.43 to 40. This range of parameters was used to match the biologically-relevant roughness spacings and heights that have been observed for freshwater dreissenid mussels (Quinn and Ackerman, 2011) and would also apply to other benthic organisms occupying the space between roughness elements or attached to their surface. A subset of 16 out of the 49 λ/k values was examined for the triangle and round (hemispherical) roughness geometries in order to determine the influence of angularity of roughness shape.…”