Response of Red Abalone Reproduction to Warm Water, Starvation, and Disease Stressors: Implications of Ocean Warming

Abstract

Changes in ocean temperature can have direct and indirect effects on the population dynamics of marine invertebrates. We examined the impacts of warm water, starvation, and disease on reproduction in red abalone (Haliotis rufescens). We found that sperm production was highly sensitive to warm water and starvation, suggesting there may be a dramatic temperature threshold above which sperm production fails. Wild males from northern (72%) and southern (81%) California had sperm. In contrast, only 30% of the males exposed to warm water (18C) for 6 mo or starvation for 13 mo had sperm, with spermatogenesis dropping dramatically from 300,000 presperm cells/mm 3 (wild) to 46,000 presperm cells/mm 3 (warm water) and 84,000 presperm cells/mm 3 (starvation). In a longer warm-water experiment (12 mo), males had total reproductive failure in temperatures greater than 16C, irrespective of food treatment. Egg production was less sensitive to warm water, but was impacted more by starvation, especially food quantity relative to quality. Wild females from northern (97%) and southern (100%) California had mature oocytes averaging 3 million eggs and 21 million eggs, respectively. Females exposed to 18C water for 6 mo had diminished fecundity, averaging only 400,000 mature eggs whereas females in the starvation experiment did not produce any mature eggs. Normal sperm and egg production was found in abalone testing positive for Rickettsiales-like-prokaryote (RLP), the agent of Withering Syndrome in cool water. However, abalone with RLP also exposed to warm water developed the disease withering syndrome and did not produce any mature gametes. The temperature-mediated lethal and sublethal effects on red abalone reproduction described here, combined with temperature's known impacts on abalone growth, kelp abundance, and disease status, clearly demonstrate population-level consequences. We suggest that temperature needs to be explicitly incorporated into red abalone recovery and management planning, because California's ocean has warmed and is predicted to warm in the future.