Sea urchin spawning in benthic boundary layers: Are eggs fertilized before advecting away from females?

Past work on fertilization in echinoids and other egg-broadcasting, free-spawning invertebrates suggests that these organisms might be extremely sperm limited in the field unless individuals spawn in close proximity and under nearly ideal flow conditions. However, virtually all previous experiments have used one or more techniques (surrogates for males and females, and short sampling duration) that bypassed two potentially important aspects of echinoid reproductive biology: the release of gametes in viscous fluids that cling to tests and spines, and extended longevity of eggs and undiluted sperm. We hypothesized that these attributes might interact with some flow regimes to facilitate time-integrated fertilization. Consequently, we explored fertilization processes in sea urchins induced to spawn in a benthic boundary layer in a flow-through flume, with a male 0.5 m upstream of a female. Our observations and data suggest that at free–stream flow velocities of 2.5 and 8.5 cm s21, gametes were slowly and continually advected from the aboral surfaces of spawning animals. Eggs on the surface of the aboral mass were often fertilized before they ablated from the surface; many advected eggs were fertilized after being trapped in the vortex downstream of the female. Gamete advection and fertilization continued for several hours, with the actual time course depending on flow velocity. Fertilization levels declined only slightly with increasing flow velocity. These results suggest that fertilization in echinoderms and other free-spawners with viscous, long-lived gametes could be much less sperm-limited than currently envisioned and have additional implications for population dynamics and selection on gamete characteristics. Sexual reproduction via the release of sperm into the water column (free-spawning) is widespread among sessile and sedentary invertebrates and other marine organisms (e.g., algae, fish). The potential for gametes to be rapidly diluted after release and for sperm availability to limit successful fertilization has led to considerable recent interest in assessing fertilization levels under field conditions (reviewed in Levitan and Petersen 1995; Levitan and Sewell 1998; Yund 2000). Many free-spawners that brood eggs appear to possess sophisticated mechanisms for filtering dilute sperm out of the water and, hence, exhibit high fertilization levels under a broad range of ecological conditions (reviewed in Yund 2000). However, fertilization in egg broadcasters is generally thought to be extremely sensitive to short-term ambient sperm concentrations; hence, fertilization in these systems is expected to be sperm limited (Levitan and Sewell 1998). If sperm availability limits reproductive success at the population level, sperm limitation could affect population dynamics by reducing population growth at low density (a form of the Allee effect; Levitan 1991; Pfister and Bradbury 1996). Even intermittent sperm limitation of some individuals could have implications for the evolution of gamete characteristics (Levitan and Irvine 2001; but see Podolsky 2001; Randerson and Hurst 2001) and other aspects of life history strategies (Yund 2000). Fertilization in broadcast-spawning echinoids is widely 1 Corresponding author ([email protected]).