The invasive round goby Apollonia melanostoma (Actinopterygii: Gobiidae) - a new intermediate host of the trematode Neochasmus umbellus (Trematoda: Cryptogonimidae) in Lake Erie, Ohio, USA

Abstract

Trematodes belonging to the genus Neochasmus van Cleave and Müller, 1932 are common intestinal parasites of fishes and reptiles (Hoffman, 1999). Four species comprise this genus in North American waters: Neochasmus ictaluri Sogandares-Bernal, 1955; N. olmecus Lamothe-Argumedo et al., 1989; N. sogandaresi Overstreet, 1971; and N. umbellus van Cleave and Müller, 1932 (Hoffman, 1999). Of these, N. umbellus is the sole species that has been described to parasitize fishes in Lake Erie of the Great Lakes (Dechtiar and Nepszy, 1988). The metacercariae of N. umbellus are located in the muscles of relatively small-sized fishes [including the emerald shiner Notropis atherinoides (Rafinesque, 1818), johnny darter Etheostoma nigrum (Rafinesque, 1820), and blackside darter Percina maculata (Girard, 1859)]. Adult N. umbellus are commonly found in piscivorous fishes [e.g. the least darter Etheostoma microperca Jordan and Gilbert, 1888; tessellated darter E. olmstedi Storer, 1842; smallmouth bass Micropterus dolomieu Lacépède, 1802; white perch Morone americana (Gmelin, 1789); white bass M. chrysops (Rafinesque, 1820); and yellow bass M. mississippiensis Jordan and Eigenmann, 1887] (Muzzall and Peebles, 1987; Dechtiar and Christie, 1988; Dechtiar and Nepszy, 1988; McLaughlin et al., 2006). The first intermediate host of this parasite is unknown. A progenetic life cycle, in which the reproductive organs of the parasite develop during the metacercariae stage (Poulin and Cribb, 2002), is typical for N. umbellus (McLaughlin et al., 2006). The round goby Apollonia melanostoma (Pallas, 1811), formerly known as Neogobius melanostomus (Stepien and Tumeo, 2006), is a Ponto-Caspian fish species that invaded the Great Lakes in the early 1990s via ballast water (Jude et al., 1992). Parasites of the round goby in the Great Lakes are poorly studied to date. Investigations of round goby parasites by Muzzall et al. (1995), Pronin et al. (1997), and Camp et al. (1999) focused on specimens from Lake St Clair, the St Clair River (the original area of the round goby introduction), and southern Lake Michigan; and did not document Neochasmus trematodes. Fishes were sampled using seines in Maumee Bay of Lake Erie off the City of Oregon, Ohio, USA (41°41.423′N, 83°23.953′W), in October–November 2006. Specimens included 30 round goby A. melanostoma, 15 white perch M. americana, 17 white bass M. chrysops, and 10 emerald shiner N. atherinoides. Specimens were measured (standard length, SL), killed, and immediately examined. The skin, fins, gills, muscles, brain, eyes, gut, liver, spleen, kidneys, body cavity, and mesentery were examined for metazoan parasites. The metacercariae were first isolated from cysts. Parasite larvae and adults were fixed in heated 70% ethyl alcohol, stained in acetic carmine, dehydrated in a series of increasing alcohol concentration and then mounted in Canada balsam for species identification. Parasitological indices were calculated according to Bush et al. (1997), including prevalence (P, %), intensity (as intensity range, IR), mean intensity (MI), and abundance (A). The standard deviation (SD) of the parameter mean values (M) was calculated. Metacercariae were identified in muscle, eye, and brain tissues of the round goby, as well as in muscles of the emerald shiner (Table 1). The round goby was found to be a newly described host for Neochasmus umbellus. The muscles were the predominant location for the metacercariae, rarely appearing in the brain or eyes. The round goby appeared to be less infected than were the shiners. According to published data, shiners Notropis spp. and darters Etheostoma spp. are the most common hosts of metacercariae (Muzzall and Peebles, 1987; McLaughlin et al., 2006). The metacercariae often are found in many other smaller-sized fishes, but rarely occur in predatory fishes, such as yellow perch Perca flavescens (Mitchill, 1814) and smallmouth bass Micropterus dolomieu (Carney and Dick, 2000; McLaughlin et al., 2006). Adult N. umbellus were identified in the intestines of Moronidae (white bass and white perch; Table 1). Examination of white perch specimens yielded only two immature specimens of N. umbellus in the gut. However, white bass specimens were infected with greater numbers of N. umbellus (Table 1). According to several authors (Dechtiar and Christie, 1988; Dechtiar and Nepszy, 1988; also see van Cleave and Müller, 1934; Bangham and Venard, 1942; McReynolds and Webster, 1980; Anthony, 1985), the white bass is one of the most heavily parasitized fishes in the Great Lakes. In the Canadian waters of Lake Erie and Lake Ontario, the white bass has been noted as the sole host of N. umbellus (Dechtiar and Christie, 1988; Dechtiar and Nepszy, 1988). Thus, the white bass appears to be the primary definitive host of this parasite. The metacercariae of two species belonging to the Cryptogonimidae family are common parasites of the round goby in its native habitats in the Black Sea basin, including Metadena pauli (Vlasenko, 1931) and Timoniella imbutiforme (Molin, 1859) (Naidenova, 1974; Kvach and Korniychuk, 2002; Kvach, 2005). Those parasites appear ecologically similar to N. umbellus (i.e. are located mostly in muscles and rarely in the eyes or brain). Thus, in their new invasive habitat, the round goby is infected by a species of parasite that appears ecologically analogous to parasitic species in its native range. In both its native and exotic habitats (Black Sea and Lake Erie), the round goby is not the main host of the trematodes. In the Black Sea, the main definitive host of T. imbutiforme is the pipefish Syngnathus typhle L., 1758, and the main secondary intermediate hosts are small gobiids belonging to the genus Pomatoschistus that are consumed by the pipefish. Because large-sized gobies cannot be consumed by the pipefish for food, the round goby host thus prevents the metacercariae from completing their life cycle (i.e. the goby grows too large to be eaten by the pipefish). In Lake Erie, a similar situation may occur with N. umbellus. The main hosts of the N. umbellus metacercariae are shiners and darters, in whose muscles the larvae develop to maturity. In our study, round goby samples housed metacercariae without developed sexual organs. Further study from additional sampling sites is recommended to determine whether any of these parasites develop sex organs in the round goby, in Lake Erie or other areas of the Great Lakes. Shiners are common prey for white bass (the main definitive host of N. umbellus), which also consume a variety of other small fishes, including the round goby. However, since many round gobies are larger than shiners, it is possible that the round goby may circumvent more of the metacercariae from completing their life cycle. The study was funded by the National Science Foundation (NSF) grants #DEB-0456972 and #DEB-0630172 (a supplement for support of YK) to CAS through Systematic Biology in the Biotic Systems and Resources Division. We thank Matthew Neilson, Joshua Brown, Douglas Murphy, Amanda Haponski, and Jhonatan Sepulveda Villet of Great Lakes Genetics Laboratory for laboratory and collection help. We also thank Oregon fisherman Frank Reynolds for collecting the white perch and white bass. This is contribution #2007-011 from the Lake Erie Research Center.