Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels

Significance Body reorganization in eels during gametogenesis can induce undesired side effects with possible pathological significance. This study provides analytical evidence for the maternal transfer of toxic metals from soft and hard tissues to the ovaries of mature females. By illustrating the metabolic fluxes and fate of mobilized minerals and metals in the fishes’ bodies during sexual development, we have identified a previously unreported aspect of anthropogenic impact on endangered anguillid eels. Furthermore, our findings suggest a physiologically connected interplay of energy metabolism and bone resorption in the reproductive strategy of eels. Consequently, we propose the eel as an interesting model organism for investigating the physiological pathways connecting lipid metabolism and mineral retention, known also to affect the health state of humans.
During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels’ bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species.