Fertilization in an Egg-Brooding Colonial Ascidian Does Not Vary With Population Density

Abstract

The possibility that free-spawning marine organisms may be subject to fertilization failure at low population density (due to the effects of sperm dilution) has sparked much interest, but these effects have been demonstrated only in a few species that broadcast their eggs. Some egg-brooding species may overcome dilution effects by filtering low concentrations of sperm from seawater and fertilizing eggs throughout an extended period of time. We examined the effects of population density and size on fertilization in Botryllus schlosseri, a hermaphroditic colonial ascidian that free-spawns sperm, but broods eggs. We experimentally manipulated the size and density of mating groups and surveyed fertilization levels in natural populations that varied in density. Fertilization was not affected by variation in population size or density in either the experimental or natural populations. Near the end of the reproductive season, some eggs may have been fertilized too late to complete development, suggesting a temporal form of sperm limitation that has not been considered in other systems. We also detected greater variability in fertilization levels at lower population density. Nevertheless, these results suggest that caution must be used in extrapolating reported density effects on fertilization to all taxa of free-spawners; density effects may be reduced in brooders that have efficient sperm collection mechanisms.

Spatial distribution of ascidian sperm: two-dimensional patterns and short vs. time-integrated assays

“…Sperm are extremely long-lived and apparently filtered from the water at very low concentrations (Johnson & Yund 2004). Populations do not appear to be sperm-limited, although individual colonies sometimes exhibit fertilization failure (Phillippi et al 2004). Near neighbors tend to dominate fertilizations (Yund 1995), but colonies with access to little local sperm can acquire sperm from very distant sources (Yund 1998).…”

“…Fertilization appears to be a very efficient process, with long-lived, dilute sperm (Johnson & Yund 2004) captured throughout a 24 h period of egg viability (Stewart-Savage et al 2001). As a consequence, most eggs in natural populations are fertilized (generally > 85%; Phillippi et al 2004).…”

“…In contrast to previous studies that sampled sperm downstream of 1 or a few isolated males, we focused on dilution patterns downstream of discrete populations. Past work has shown that the long-lived sperm of this species are widely dispersed and captured by female-phase colonies at extremely low concentrations (Johnson & Yund 2004, Phillippi et al 2004, making it very difficult to isolate unique sperm sources and requiring biochemical or molecular markers to distinguish sperm from specific males (Yund 1998). With minimal sperm limitation occurring within populations (Phillippi et al 2004), only isolated colonies on the fringe of established populations are expected to be sperm-limited.…”

“…Concerns about the fertilization consequences of rapid sperm dilution with distance from sperm source have led to an ongoing debate about the extent to which fertilization in these systems is limited by sperm availability (reviewed in Levitan & Petersen 1995, Yund 2000. In general, egg brooders that possess mechanisms to filter dilute sperm from the water appear to be less sperm-limited than egg broadcasters (Bishop 1998, Yund 2000, Pemberton et al 2003, Johnson & Yund 2004, Phillippi et al 2004. However, experimental approaches that incorporate life history adaptations that minimize gamete dilution effects (e.g.…”

Sexual reproduction in octocorals

“…In free-spawning marine organisms, extreme dilution of sperm to levels that limit fertilization (Denny & Shibata 1989) can exert extremely strong selective pressure on reproductive strategies to maximize reproductive success (Oliver & Babcock 1992, Levitan 1995, Levitan & Petersen 1995, Yund 2000. For sessile marine invertebrates these strategies include spawning synchrony during times of low water motion, non-neutrally buoyant gametes, self-compatibility in hermaphrodites, and sperm concentrating mechanisms for enhancing internal fertilization (Denny & Shibata 1989, Levitan 1991, Phillippi et al 2004. Given the very limited period of viability of spawned coral eggs in the water column (e.g.…”