Role of spermatozeugmata in the spawning ecology of the brooding oyster Ostrea edulis.

Abstract

Ostrea edulis spawns spermatozeugmata, each composed of radially arrayed sperm cells attached by an extracellular matrix (ECM) to a core of acellular vesicles. The acellular vesicles are formed from excess nuclear and plasma membranes produced during spermatid condensation, and the ECM is topologically restricted to the interstices between acellular vesicles and sperm heads, being absent from the flagellar surface. When released into seawater, spermatozeugmata retain their structural integrity for varying periods (up to 24 hours) and become demersally distributed in still water. The flagella activate, initially beating in a non-synchronized, languid manner; however, both the tempo and amplitude of the flagellar action gradually increase to resemble that of typical "primitive" sperm once the cells are released from the spermatozeugma. This increase in flagellar activity and subsequent gamete release coincide with an erosion of the ECM and suggest that the ECM may modulate sperm motility in addition to adhering the cells to the spermatozeugma. Sperm are capable of fertilizing eggs only after dissociating from the spermatozeugma. The net effect of spermatozeugma formation in Ostrea edulis may be the retention of viable sperm in high concentrations at the benthic/water column interface for prolonged periods after spawning, at least in low current regimes. Unfertilized O. edulis eggs are also concentrated at this location, in the inhalent chambers of female oysters. Spermatozeugmata are entrained by the inhalent current of females and carried into the brood chamber where fertilization occurs. The Ostrea edulis spermatozeugma likely functions as an efficient sperm transfer mechanism if two conditions are met: 1) eggs are retained as broods within benthic females, 2) egg masses are at intermediate distances from spawning males.