The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe

Abstract

Interspecific symbiotic relationships involve a complex network of interactions, and understanding their outcome requires quantification of the costs and benefits to both partners. We experimentally investigated the costs and benefits in the relationship between European bitterling fish (Rhodeus sericeus) and freshwater mussels that are used by R. sericeus for oviposition. This relationship has hitherto been thought mutualistic, on the premise that R. sericeus use mussels as foster parents of their embryos while mussels use R. sericeus as hosts for their larvae. We demonstrate that R. sericeus is a parasite of European mussels, because it (i) avoids the cost of infection by mussel larvae and (ii) imposes a direct cost on mussels. Our experiments also indicate a potential coevolutionary arms race between bitterling fishes and their mussel hosts; the outcome of this relationship may differ between Asia, the centre of distribution of bitterling fishes, and Europe where they have recently invaded.

Phylogenetic relationships of Acheilognathidae (Cypriniformes: Cyprinoidea) as revealed from evidence of both nuclear and mitochondrial gene sequence variation: Evidence for necessary taxonomic revision in the family and the identification of cryptic species

“…Fertilization occurs in the mussel gill cavity and development is completed in the host mussel gill chamber (Smith et al, 2004). This breeding association makes species of bitterlings a focus of research aimed at understanding coevolutionary dynamics, life-history evolution, sexual selection, sperm competition, development and mate choice (Agbali et al, 2011;Casalini et al, 2009;Kitamura et al, 2012;Mills et al, 2005;Reichard et al, 2006Reichard et al, , 2007Reichard et al, , 2012; .…”

Population-specific responses to an invasive species

“…Rhodeus amarus is not a suitable host of parasitic larvae of European mussels [28]; attached larvae (both Anodonta and Unio) are typically rejected within the first day of infection and R. amarus thereby avoid costs associated with mussel larvae infection [29].…”

An invasive species reverses the roles in a host–parasite relationship between bitterling fish and unionid mussels

“…Bitterling (Acheilognathinae) are cyprinid fishes that oviposit into the gills of live mussels where their embryos complete development. Hosting bitterling embryos is costly to mussels [6] and they have evolved adaptations to eject bitterling eggs and embryos, mirrored by counteradaptations in bitterling embryos to avoid ejection [6,7]. Bitterling are of east Asian origin, with more than 50 species distributed in east Asia and a single species in Europe [7].…”

“…Glochidia attach to host fish and encyst, but may be rejected, indicating that glochidia infection is costly to the host [11]. Both bitterling and mussels can be host specialists or generalists [12,13] and the nature of their relationship varies from mutualism to one-sided or reciprocal parasitism [6]. Unionids are abundant throughout the Palearctic, but more diverse in east Asia [12].…”

“…Rhodeus amarus parasitize all sympatric European mussels [7,9], but avoid infection by their glochidia [6]. Anodonta woodiana is common and widely distributed in its natural range in east Asia and elsewhere where it has invaded [14].…”