Parasite interactions in the bioturbator Upogebia pusilla (Decapoda: Gebiidae): a case of amensalism?

The mud shrimp Upogebia pusilla is a deep-burrowing bioturbator widespread along the Northeast Atlantic and Mediterranean coasts, where it is recognized as an ecosystem engineer. Parasitism is an important factor impacting such species’ activities, and thus ecosystem functioning. At least two parasite species occur in U. pusilla: the bopyrid isopod Gyge branchialis and an undescribed trematode. This study, carried out in Arcachon Bay, France (44°40′N, 1°10′W), over 2 years (2014–2015), had two goals: (1) to identify the trematode occurring in U. pusilla and (2) to assess the interactions between the two parasites within their host. Using molecular techniques, the trematode was identified as Maritrema sp. (Microphallidae). Monthly samples taken over 2 years at a single site, and a ten-site spatial survey in June 2014 showed that there was a negative association in the occurrence of the two parasites in their host over time and amongst sites: bopyrid-infested mud shrimp harbored lower trematode infections compared to bopyrid-free individuals. In addition, the abundance of trematodes was lower in the bopyrid-infested gill compared to the uninfested gill of bopyrid-infested individuals. It suggests that G. branchialis interferes with Maritrema sp. establishment in the mud shrimp. Conversely, the trematode appeared not to have a negative effect on bopyrid presence. The reduction of Maritrema sp. infection by G. branchialis is mainly due to the alteration of U. pusilla fitness (indirect interaction), and to a lesser extent, to overlap of parasites’ niches (direct interaction). Accordingly, interactions between these two parasites can be classified as amensalism