Identification of a new gregarine parasite in mass mortality events of freshwater pearl mussels (Margaritifera margaritifera) in Sweden

Abstract

Freshwater bivalves play key ecological roles in lakes and rivers, largely contributing to healthy ecosystems. The freshwater pearl mussel,Margaritifera margaritifera,is found in Europe and on the East coast of North America. Once common in oxygenated streams,M. margaritiferais rapidly declining, and consequently assessed as a threatened species worldwide. Deterioration of water quality has been considered the main factors for the mass mortality events affecting this species. Yet, the role of parasitic infections has not been investigated. Here, we report the discovery of three novel protist lineages found in Swedish populations ofM. margaritiferabelonging to one of the terrestrial groups of gregarines (Eugregarinorida, Apicomplexa). These lineages are closely related–but clearly separated– from the tadpole parasiteNematopsis temporariae. In one lineage, which is specifically associated with mortality events ofM. margaritifera,we found using microscopy andin situhybridization cysts in the gills and other organs of diseased individual, containing single vermiform zoites. This represents the first report of a parasitic infection inM. margaritiferathat may be linked to the decline of this mussel species. We propose a tentative life cycle with distribution of different developmental forms and potential exit from the host into the environment.