Effects of Salinity on Sperm Motility, Fertilization, and Development in the Pacific Herring, Clupea pallasi

Abstract

We investigated the effects of salinity on fertilization and early development in a population of Pacific herring, Clupea pallasi, that migrate from oceanic waters into the San Francisco Bay estuary to spawn. The salinity range for fertilization fell between 8 and 28 ppt, with an optimal range of about 12 to 24 ppt. In comparison, the range for a population of C. harengus membras (Airisto Sound, Finland) that reside year-round in the Baltic Sea was 4 to 24 ppt. Roles for both Na+ and K+ were indicated in C. pallasi fertilization since increasing Na+ in the presence of 10 mM K+ (concentration of seawater) mimicked the effects of increased overall salinity, whereas reduced effects were obtained if [K+] was held at 5 mM (that of half-strength seawater). The initiation of C. pallasi sperm motility by components of the egg chorion, a prerequisite for fertilization, was inhibited at both elevated (28 and 32 ppt) and reduced (4 and 8 ppt) salinities. Embryonic development through larval hatching in C. pallasi exhibited a salinity tolerance similar to that of fertilization; optimum development was obtained at salinities between 8 and 24 ppt. A comparison of developmental progression in 3.5, 14, and 28 ppt seawater revealed that salinity effects became evident during the post-gastrulation stages of development and that progression to hatching was delayed in both the lower and higher salinities for those embryos that completed development.

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

“…Sperm motility was assessed with either a 10ϫ or 20ϫ objective lens by using the following qualitative index: 0 ϭ no motility, 1ϩ ϭ Ͻ25% motility, 2ϩ ϭ 25-50% motility, 3ϩ ϭ 50-75% motility, 4ϩ ϭ Ͼ75% motility (13,14,16 (23). In some experiments, the Ca 2ϩ channel blockers nifedipine (100 M) or flunarizine (10 M) or the Na ϩ ͞Ca 2ϩ exchange inhibitors bepridil (50 M), dichlorobenzamil (10 M), or KB-R7943 (10 M) were preincubated (5 min) with sperm before Ca 2ϩ i measurements.…”

“…This range of salinities correlates with the optimal salinity regime for fertilization and early development in Pacific herring (14). Previous studies have shown that extracellular Na ϩ ([Na ϩ ] o ) and extracellular Ca 2ϩ ([Ca 2ϩ ] o ) influence both sperm motility and fertilization (11)(12)(13)(14)18). Sperm motility can be initiated in the absence of SMIF by low-Na ϩ (2 mM) seawater (NaF; ref.…”

“…Both in vivo (around the chorion) and in vitro sperm motility is reduced at salinities Ͻ 8 parts per thousand (ppt) or Ͼ 24 ppt (14,18,19). This range of salinities correlates with the optimal salinity regime for fertilization and early development in Pacific herring (14). Previous studies have shown that extracellular Na ϩ ([Na ϩ ] o ) and extracellular Ca 2ϩ ([Ca 2ϩ ] o ) influence both sperm motility and fertilization (11)(12)(13)(14)18).…”

“…Upon spawning, herring sperm (Clupea pallasi) are intrinsically motionless over a wide range of salinities (11)(12)(13)(14). This immotility may be related to the unique reproductive biology of herring in which male fish spawn first, with sperm remaining in the water column for extended periods, followed by the spawning of females (15).…”

“…Although nondiffusible in vivo, SMIF can be extracted in acid seawater, and soluble SMIF retains its motility-initiating properties. Both in vivo (around the chorion) and in vitro sperm motility is reduced at salinities Ͻ 8 parts per thousand (ppt) or Ͼ 24 ppt (14,18,19). This range of salinities correlates with the optimal salinity regime for fertilization and early development in Pacific herring (14).…”