Cercariae of intertidal nassariid gastropods: Taxonomy, specificity and ecology

Abstract

Barnett, LJ ORCiD: 0000-0003-4345-3766"The biodiversity and ecology of marine cercariae in Australia is poorly known. Although nassariid gastropods are widely distributed in Australia and are expected to have a diverse parasite fauna similar to that of other nassariids worldwide, their cercariae have not been characterised. Nassarius dorsatus, N. olivaceus and N. pullus were collected at three separate estuarine localities in central Queensland between August 2004 and August 2006 and their emergent cercariae characterised using morphological and molecular methods. Fifteen morphotypes of cercariae from six families that infect fishes and birds as definitive hosts were characterised. The highest richness was within the Acanthocolpidae (nine morphotypes) which comprised three cercariae interpreted as species of Stephanostomum and a complex of six unusual cercariae with a ventral keel. Molecular characterisation of these six cercariae supported their placement in the Acanthocolpidae and indicated that they comprised only three species, two of which displayed marked phenotypic plasticity. Molecular analysis supported the characterisation of the three species of Stephanostomum and suggested that one of the unusual cercariae was a species of Stephanostomoides. Dissection of fish from Sandy Point provided a single match; the sequence for a metacercaria in Valamugil buchanani, the blue-tail mullet, was identical to that of one of the species of Stephanostomum. There were two cercariae from the Echinostomatidae and one from each of the Lepocreadiidae, Microphallidae, Opecoelidae and Zoogonidae. Molecular analyses supported the placement of the cercariae from the Echinostomatidae, Lepocreadiidae, Opecoelidae and Zoogonidae within their respective families. The cercaria from the Lepocreadiidae was identified by comparison to known adult data and putatively corresponds to Prodistomum keyam, a parasite of Monodactylus argenteus, the silver moony or butter bream, common in the study region. Morphological analysis supported the characterisation of both of the Echinostomatidae as species of Himasthla. Although no other cercariae could be characterised to genus level, the opecoelid cercaria was determined to be in the subfamily Opecoelinae. Nassarius olivaceus was infected by three acanthocolpid cercariae and one cercaria from each of the other families. Nassarius dorsatus was infected by five acanthocolpid cercariae and one each from the Echinostomatidae and Lepocreadiidae. Nassarius pullus was infected by a single cercaria from the Echinostomatidae. Most cercariae were specific to a single species of gastropod; only four infected two species and none infected all three. Cercariae that infect fish as a definitive host were found at all three localities; but cercariae that infect birds were restricted to a single locality, Sandy Point at Corio Bay, important for domestic and migratory bird species. These results emphasise the relative significance of Sandy Point as an important bird habitat. In total, 126 infections were diagnosed (115 by cercarial emergence), with both the highest frequency of infection and number of infections in N. olivaceus (frequency 5.3%; n=102; 81% of infections), followed by N. dorsatus (1.1%; 20; 16%) and N. pullus (0.2%; 4; 3%). The highest number of infections occurred at Sandy Point (66; 52% of infections), followed by Cawarral Creek (38; 30%) and then Ross Creek (22; 17%). The highest number of infections was by the Acanthocolpidae (54; 43%). Diagnosis of infection by emergence was suitable for all cercariae except the opecoelid, which was underdiagnosed. Nassarius olivaceus had the longest survival in captivity (~4.5 y), followed by N. dorsatus (~0.8 y) and N. pullus (~0.3 y). Almost all infections remained patent for the life of the gastropod. Families commonly found in nassariids worldwide include Acanthocolpidae, Echinostomatidae, Lepocreadiidae and Zoogonidae. Nassariid gastropods are also the dominant marine first intermediate hosts for the Acanthocolpidae, Lepocreadiidae and Zoogonidae and one of the three most common first intermediate host families for species of marine Himasthla. Molecular relationships also indicate that the Acanthocolpidae and Brachycladiidae may actually be comprised of three discrete groups, the Stephanostomum + Monostephanostomum group, the Brachycladiidae, and a group of non-Stephanostomum species comprising Pleorchis, Tormopsolus and Stephanostomoides. This research adds information about the parasite assemblages of nassariid gastropods in Australia, adding 12 new cercarial species and 16 new host-parasite records. Cercarial reports for the Acanthocolpidae, Echinostomatidae, Lepocreadiidae, Opecoelidae and Zoogonidae have been comprehensively reviewed and patterns of association between nassariids and their common parasite families presented. As well, this research has provided a potential avenue for a review of the Acanthocolpidae, a family which is currently considered a ‘catch-all’ group.

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