Abstract
Oyster aquaculture is expanding worldwide, where many farms rely on seed produced by artificial spawning. As sperm motility and velocity are key determinants for fertilization success, understanding the regulation of sperm motility and identifying optimal environmental conditions can increase fertility and seed production. In the present study, we investigated the physiological mechanisms regulating sperm motility in Eastern oyster, Crassostrea virginica. Sperm motility was activated in ambient seawater with salinity 4–32 PSU with highest motility and velocity observed at 12–24 PSU. In artificial seawater (ASW) with salinity of 20 PSU, sperm motility was activated at pH 6.5–10.5 with the highest motility and velocity recorded at pH 7.5–10.0. Sperm motility was inhibited or totally suppressed in Na+, K+, Ca2+, and Mg2+-free ASW at 20 PSU. Applications of K+ (500 μM glybenclamide and 10–50 mM 4-aminopyridine), Ca2+ (1–50 μM mibefradil and 10–200 μM verapamil), or Na+ (0.2–2.0 mM amiloride) channel blockers into ASW at 20 PSU inhibited or suppressed sperm motility and velocity. Chelating extracellular Ca2+ ions by 3.0 and 3.5 mM EGTA resulted in a significant reduction and full suppression of sperm motility by 4 to 6 min post-activation. These results suggest that extracellular K+, Ca2+, and Na+ ions are involved in regulation of ionic-dependent sperm motility in Eastern oyster. A comparison with other bivalve species typically spawning at higher salinities or in full-strength seawater shows that ionic regulation of sperm motility is physiologically conserved in bivalves. Elucidating sperm regulation in C. virginica has implications to develop artificial reproduction, sperm short-term storage, or cryopreservation protocols, and to better predict how changes in the ocean will impact oyster spawning dynamics.
Highlights
Similar to vertebrates [1,2,3,4], sperm of most invertebrates including bivalves are non-motile in the testis and reproductive tract [5]
Among 15,000 bivalve species from the phylum “Mollusca” possessing about 100,000 species [31], sperm motility has only been studied in a few ecologically and economically important species that typically spawn at higher salinities or in full-strength seawater, including the Atlantic surf clam (Spisula solidissima) [32], Pacific oyster (Crassostrea gigas) [28,33,34,35,36], black-lip pearl oyster (Pinctada margaritifera) [37], Japanese pearl oyster (Pinctada fucata martensii) [38], European flat oyster (Ostrea edulis) [39], Manila clam (Ruditapes philippinarum) [28], great scallop (Pecten maximus) [40], and Japanese scallop (Patinopecten yessoensis) [28]
Mg2+ may not play a key role in sperm motility signaling since Pacific oyster sperm motility has been initiated in Mg2+-free seawater [36]. These studies illustrate how sperm motility activation occurs in bivalve species that typically spawn at higher salinities or in full-strength seawater, but still raises the question as to whether it will follow a similar trend for a species that can spawn at lower salinities
Summary
Similar to vertebrates [1,2,3,4], sperm of most invertebrates including bivalves are non-motile in the testis and reproductive tract [5]. Once sperm motility in aquatic animals is activated by environmental osmolality or ions [4,5,6,7,8,9,10,11,12,13], sperm subsequently have a limited period of motility to reach an oocyte [4,14,15]. This is due to rapid depletion of energy required for the activity of the sperm motility apparatus called the axoneme [4,16]. Sperm motility kinematics can be assessed using computer-assisted sperm analysis (CASA) software that tracks sperm head trajectories [25]
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