Evolutionary and ecological insights from vital staining of bivalve oocytes: A Red Queen at the sweepstakes?

Abstract

To determine the proportion of inviable oocytes that are spawned along with normal oocytes in marine bivalves, we turned to a time-honored technique not previously used on invertebrate oocytes: the neutral red vital stain. Despite the difficulty in obtaining induced spawns from field-collected Cerastoderma edule (L), the results and insights from this simple procedure to answer a simple question were unexpected and far-reaching. Mean proportions of inviable oocytes in the spawns of cockle C. edule ranged from 35% to 85%, with the vast majority represented by atresic (autolyzing) oocytes. These levels are in agreement with previous quantitative histological observations of prespawning atresia in both C. edule and the Manila clam Tapes philippinarum. Such elevated prefertilization inviability mirrors the known high level of postfertilization inviability in bivalves. Together, these high levels of inviability may account for much of the early mortality in the type III survivorship curves typical of marine bivalves. The combination of high fecundity and high oocyte inviability suggests a Red Queen-type reproductive dilemma in these species. In addition, the great degree of interindividual variation observed in oocyte inviability suggests that cockles, and perhaps other intertidal bivalves, present a Sweepstakes Reproductive Strategy, in which highly variable individual fecundity confronts a highly variable environment. The neutral red technique promises to be a useful tool for investigating prespawning inviability in other marine taxa, as well as for aquaculture, conservation, restocking, ecophysiology, and environmental monitoring.