Pathobiology and first report of larval nematodes (Ascaridomorpha sp.) infecting freshwater mussels (Villosa nebulosa, Unionidae), including an inventory of nematode infections in freshwater and marine bivalves

Abstract

Little information is available on host-parasite relationships between bivalves and larval nematodes. Herein, we describe nematode larvae (likely stage 2) in the infraorder Ascaridomorpha infecting the foot, intestine, and mantle of a freshwater mussel (Alabama rainbow, Villosa nebulosa [Conrad, 1834]) and detail histopathological changes to infected tissues. A total of 43 live mussels from the South Fork of Terrapin Creek, Alabama, were collected between 2010 and 2014, with 14 sectioned for histopathology and 29 dissected. Of the 14 sectioned mussels, 5 appeared to be uninfected, and 7, 1, and 1 had histozoic infections observed in the foot and intestine, intestine only, and mantle edge and foot, respectively. Twenty-three of 29 (79%) of the mussels dissected were infected by live nematodes, and mean nematode abundance was 8.3 (CL = 5.23–13), with 2 mussels infected with >100 nematodes each. Thus, with a total of 32 of the 43 collected mussels observed with nematodes, overall infection prevalence was 74.4% (CL = 0.594–0.855). The 18S rDNA of this nematode was 99% similar to that of several ascaridids (species of Kathlaniidae Lane, 1914 and Quimperiidae Baylis, 1930) that mature in aquatic/semi-aquatic vertebrates; the recovered 18S phylogenetic tree indicated this nematode from V. nebulosa shares a recent common ancestor with Ichthyobronema hamulatum (Ascaridomorpha: Quimperiidae; GenBank Accession Number KY476351). Pathological changes to tissue associated with these infections comprised focal tissue damage, but a cellular response was not evident. The Alabama rainbow possibly represents an intermediate or paratenic host. Given these results, the nematode is likely not pathogenic under normal stream conditions; however, high intensity infections in the foot could inhibit pedal extension and retraction; which would have demonstrable health consequences to a freshwater mussel. Based on our review of the bivalve mollusc parasite literature, a collective biodiversity of 61 nematodes reportedly exhibit some degree of symbiosis (from commensal to parasitic) with 21 bivalves (28 nematode spp. from 17 marine bivalve spp.; 33 nematode spp. from 4 freshwater bivalve spp.); only four records exist of putatively parasitic nematodes from Unionida. The present study represents the first description of a nematode species that invades the tissues of a Unionidae species. Keywords: Unionidae, Histopathology, Histozoic nematodes, Ascaridomorpha