Testing the enemy release hypothesis: trematode parasites in the non-indigenous Manila clam Ruditapes philippinarum

The present study tested the 'Enemy Release Hypothesis' (ERH) which states that the success of an introduced species is related to the scarcity of natural enemies in the introduced range compared with the native range. Digeneans are dominant macroparasites of molluscs; therefore, the interaction between R. philippinarum and these parasites was ideal for investigation. A two-year monitoring in Arcachon Bay (SW France) was performed to estimate digenean loads in R. philippinarum and in three infaunal native bivalves (R. decussatus, Paphia aurea, Cerastoderma edule). A laboratory experiment allowed comparison of infection success among these bivalves (except P. aurea) by generalist digenean larvae (Himasthla elongata cercariae). R. philippinarum digenean abundance in Arcachon Bay was much lower than in native bivalves, with values depending on species, sites and time. Similarly, mean digenean species richness per host individual was always lower in R. philippinarum than in sympatric bivalves. A comparison of digenean metacercariae abundance between R. decussatus and C. edule in Mundaka Estuary (Spain) showed that both species had similar digenean loads but that R. decussatus was depleted in digenean species encysting in host tissues (the non-gymnophallid species). Experimental infection confirmed that the two species of the genus Ruditapes (and not R. philippinarum only) were resistant to encysting digeneans, with an infection success 3-5 times lower than that of C. edule. The lack of infection that was observed in the field would therefore be the consequence of a tissue barrier, R. philippinarum epithelium being too tough for cercariae penetration. Concordantly, according to the literature, digenean infection in the native range of R. philippinarum is also low. Consequently, the ERH, as an explanation for R. philippinarum success in Europe, is not totally consistent in the case of digenean trematodes as enemies, R. philippinarum hosting low load of digeneans in its native as well as colonized range.