Spawning events in small and large populations of the green sea urchin Strongylocentrotus droebachiensis as recorded using fertilization assays

During the winter and spring of 2002 and 2003, we used time-integrated fertilization assays to monitor sperm availability in three populations of the green sea urchin Strongylocentrotus droebachiensis in Maine: a naturally occurring population of .40,000 urchins and two smaller groups (,1,000) of transplanted urchins isolated from other aggregations. Episodes of sperm release coincided in two populations 10 km apart, suggesting that urchins were responding to a widespread environmental signal. We observed significant lunar periodicity in sperm release events for both of these populations. However, extensive spawning as shown by fertilization rates near 100% and a dramatic drop in gonad mass only occurred in the large natural population around the onset of thermal stratification and the spring phytoplankton bloom. By contrast, in the two small populations we observed low fertilization rates and little or no change in gonad mass. We speculate that a subset of males in these populations responded to a common external spawning signal, but that mass spawning is more likely to occur in large, dense populations where sperm concentrations reach high enough levels to trigger spawning in less responsive urchins. For benthic free-spawning organisms that release gametes in the water, timing of spawning is critical to reproductive success, especially with respect to two processes: fertilization and larval development. First, the degree of spawning synchrony between males and females will strongly influence fertilization rates because of the limited longevity and rapid dilution of gametes (Pennington 1985; Levitan 1995). Second, spawning should occur at a time of year when pelagic larvae have a high probability of surviving and developing (Himmelman 1999). One way to synchronize gamete release and ensure early survival is to link the spawning process to environmental cues that predict favorable conditions (Giese and Kanatani 1987; Pearse 1990; Himmelman 1999). Despite the vast literature on reproduction in broadcast spawners, our understanding of environmental cues remains speculative largely because of the difficulty of recording spawning events with high temporal resolution. Although the literature on reproduction in marine organisms reflects a long-standing interest in environmental spawning cues (e.g., Giese and Kanatani 1987; Himmelman 1999), our understanding of the dynamics of fertilization during spawning has mainly developed over the past two decades. The influence of the physical environment, particularly advection and diffusion, on fertilization success has been studied intensively (Pennington 1985; Denny and Shibata 1989; Yund and Meidel 2003). Because of the rapid dilution of gametes, marine free-spawners at low population density or in smaller aggregations may face severe fertilization failure (i.e., Allee effect; Petersen and Levitan 2001). Consequently, low per-capita reproductive performance may prevent depleted populations from recovering and even lead to local extinction (Quinn et al. 1993; Pfister and Bradbury