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

Abstract

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.

How life history contributes to stress response in the Manila clam Ruditapes philippinarum

“…Clams from Arguin resisted better to trematode experimental infestation compared to those from Andernos. One possible explanation is that throughout their lifetime, clams from Arguin experienced an environment with a higher abundance of cercariae compared to what is shown at Andernos (Dang et al 2009a;Desclaux 2003). Similar local adaptation was also highlighted in populations used to experience trematode parasite infestation compared to populations without prior exposures (Bryan-Walker et al 2007).…”

“…The bodies of water at both sites are sufficiently remote to exhibit different physical parameters, like temperature and salinity (Dang 2009), different benthic communities (Blanchet et al 2005), or planktonic assemblages (Glé 2007). It was also demonstrated that clams from Arguin and Andernos fed on different trophic sources (Dang et al 2009b) and that they were infested, like their surrounding cockles (C. edule), by different parasite propagules (Dang et al 2009a). Consequently, we presume that our adult individuals from Arguin and Andernos spent their lifetime (38 mm corresponds to an age of 3.4 years; Dang 2009) under different stressors.…”

“…Among the trematode species that occur in Arcachon Bay, Himasthla elongata was collected because (1) many bivalves are its potential second intermediate host (Werding 1969), (2) it is a widespread species ), (3) experiment process is controlled (Wegeberg et al 1999), and (4) our host populations are free of this trematode (Dang et al 2009a). The H. elongata life cycle involves marine birds as final host, periwinkles (Littorina littorea) as first intermediate host, and bivalves (mostly cockles and mussels) as second intermediate host.…”

“…Previous studies showed that the Manila clam, an introduced species, was resistant to trematodes (Dang et al 2009a) but there are some reports of such infestation in their native area (Lee et al 2001;Ngo and Choi 2004). In Arcachon Bay, Manila clam infestation by trematodes is also very low, but slightly higher at Arguin (Dang et al 2009a). Nevertheless, in a context of poor environmental conditions or poor individual health, parasite infestation could increase considerably even in nonspecifically sensitive species.…”

Parasites and marine invasions: Ecological and evolutionary perspectives

“…The lack of a co-evolutionary history may often render invasive species non-competent hosts and thus acquisition of native parasite species may not take place. For example, the invasive Manila clam (Ruditapes phillipinarum) could not be artificially infected with the native trematode Himasthla elongata, while in the native common cockle (Cerastoderma edule) infection success was high (Dang et al, 2009). Free-living infective stages of the parasite were not able to infiltrate the epithelium of the invasive bivalve and thereby the low infections in the lab and the field resulted from a host (tissue) barrier (Dang et al, 2009).…”