Extrinsic and intrinsic factors that shape the life history of the short living scallop Argopecten ventricosus

Abstract

The scallop Argopecten ventricosus is characterized by its high swimming activity, fast growth, high reproductive effort and the early age to get first sexual maturity. These traits may be the result of the adaptation to a specific environment that favors an active lifestyle and a short lifespan (2 years). This opens the question of how environmental factors modulate the way a short living marine ectotherm budget energy investments among life history traits and how this modulation impacts the lifespan within a cohort. Temperature and predation are two key environmental factors that affect physiological and cellular responses in marine ectotherms that have been investigated in the present study. Lifelong investments among life history traits were studied looking at trade-offs among growth, reproduction and cellular maintenance mechanisms under the different environmental conditions. The cellular maintenance mechanisms were studied in different tissues by antioxidant and damage removal capacities. In order to demonstrate the efficiency of cellular maintenance mechanisms, oxidative damage accrual of proteins and lipids and undegradable waste accumulation (lipofuscin) were assessed in parallel. The trade-offs were also investigated within a cohort raised in the field throughout the species record lifespan (2 years). The long-term elevation of temperature (5°C above the temperature measured in the field) enhanced metabolic rates, reproduction effort but also oxidative damage accrual and high mortality rates despites the conjunctly increase in antioxidant capacities. The high mortality probably exerted a strong selection of better-adapted individuals with less oxidative damage and better growth. Scallops exposed to predator pressure (the blue crab: Callinectes sapidus) developed thicker shells and bigger swimming muscles and at the meantime constrained reproduction investment as indicated by the deferment and the lower investment into gametogenesis. Lower reproductive effort was combined with lower oxidative damage accrual especially in mantle and gill tissues, and may have prevented post-spawned mortalities. When studying the trade-offs in scallops reared in the field, it appears that scallops at their first reproductive event (< 1 year of age) showed the highest levels of oxidative damage (protein carbonyls and lipid peroxidation products). While antioxidant capacities did not appear to prevent oxidative damage, young scallops seem to remove damage before the undegradable waste product lipofusin accumulates. In contrast, older individuals (>1 year of age) failed to prevent lipofuscin accumulation. For this species, the applicability of evolutionary theories of aging suggest that a rapid growth and early maturation at young age compromise later cellular maintenance. However, species may have a great variety of strategies in order to deal with the oxidative challenges throughout their lifespan, which depend strongly on the environmental conditions and state of life. The results speak for extrinsic factors (temperature and predation) to have potential roles on the lifespan in A. ventricosus scallops. This makes aging and oxidative stress mechanisms in short living bivalves an interesting but complex process influenced by a variety of interactive intrinsic and extrinsic processes that should be considered in future studies