Freshwater Mollusk Biology and Conservation 22:85–89, 2019 Ó Freshwater Mollusk Conservation Society 2019 NOTE ARE PARASITES AND DISEASES CONTRIBUTING TO THE DECLINE OF FRESHWATER MUSSELS (BIVALVIA, UNIONIDA)? Andrew McElwain Department of Biological Sciences, College of Liberal Arts and Sciences, State University of New York at Oswego, 392 Shineman Center, Oswego, NY 13126 USA, [email protected] These declines are thought to result primarily from human ABSTRACT activities that fall into one of four general categories. The first Freshwater mussels (Mollusca: Bivalvia: Unionida) includes activities (such as dam construction) that change the consist of 843 species in six families, but many are physical habitat of rivers and lakes. The second includes imperiled. Significant causes of mussel declines include activities that contaminate the benthos with chemical and contaminants and loss of substrate. Potentially, etiological physical waste from industrial and municipal sources (e.g., agents are also contributing factors, but parasites and pathogens of freshwater mussels are understudied relative Hornbach 2001; Grabarkiewicz and Davis 2008). The third to those affecting marine bivalves. Published accounts of category is the extensive harvesting of mussels for the button viral pathogens have been reported exclusively from and pearl industries, which has contributed to declines in some Hyriopsis cumingii (Unionidae) in China. There are species, especially in the USA (Haag 2012). The fourth limited records of possible bacterial and fungal pathogens category is the introduction of nonnative aquatic molluscs, from unionids in the USA and Finland. Parasitic and commensal organisms generally include ciliates (Cilioph- such as the zebra mussel (Dreissena polymorpha) or Asian ora), trematodes (Platyhelminthes: Aspidogastrea and clam (Corbicula fluminea), which compete with native Digenea), roundworms (Nematoda), moss animals (Ecto- mussels for food and available substrate or which foul waters, procta, Entoprocta), oligochaetes and leeches (Annelida: harming indigenous species (Cummings and Graf 2010). Sedentaria: Clitellata), mites (Arthropoda: Acari), cope- pods (Arthropoda: Copepoda), insects (Arthropoda: Additionally, nonnative molluscs potentially can introduce Insecta), and fish eggs (Chordata: Actinopterygii). Para- nonnative etiological agents that might negatively affect native sites injure the host through attachment or feeding or molluscs (Prenter et al. 2004). Although we lack data on the when they invade host tissue to complete their life cycles presence of nonnative etiological agents in freshwater mussels, (e.g., digeneans). Commensals are small organisms living Perkinsus marinus and Haplosporidium nelsoni are good in or on mussels that may use the mantle cavity or shell as a refuge or substrate, and commensals also may feed on examples of introduced pathogens that have affected signif- particulates that have been gathered by their molluscan icantly the USA marine shellfish industry (Burreson and Ford host. Typically, however, the relationship between the two 2004; Villalba et al. 2004). Because of declining populations parties is subject to speculation (e.g., leeches). We are in and mass mortality events known as ‘‘die-offs’’ and ‘‘mussel the midst of a biodiversity crisis, and this minireview kills,’’ the health of wild and hatchery-reared mussels is a highlights the relationships among these organisms and the need to understand the health of wild and captive growing concern (Neves 1987; Fleming et al. 1995; Lydeard et mussels. al. 2004). In an effort to shed light on the possibility of etiological KEY WORDS: freshwater mussels, Unionida, parasites, agents as causative factors of mussel declines, Grizzle and diseases, gross pathology, histopathology Brunner (2009) reviewed the literature regarding parasites and infectious diseases reported from freshwater bivalves. Most of Freshwater mussels are a globally distributed group of the cited literature are observations of single-celled eukaryotic about 843 species in six families (Graf and Cummings 2007; organisms and metazoans that may engage in either a Williams et al. 2017). Approximately 29 species have gone commensal or parasitic relationship with unionids or margar- extinct in the USA as a result of human activities and many itiferids in North America and Europe. The other four families other mussel species have declining populations (Haag 2012). in Unionida are underrepresented in the parasite and disease 85 86 MCELWAIN literature. Additionally, there appears to be almost no peer- damage associated with attached ciliates. Curiously, Coker et reviewed literature on viral, bacterial, or fungal infections in al. (1921) reported Chaetogaster limnaei feeding on mussel freshwater mussels. A few exceptions include reports of RNA parasites but provided no other supporting details. Overall, few and DNA viruses infecting the digestive system of Hyriopsis studies have used light or electron microscopy to document the cumingii in China (Grizzle and Brunner 2009; Lei et al. 2011). pathological changes to tissues associated with pathogens, In 1931 mussel propagation personnel reported ‘‘adult mussels parasites, or commensals. became sterile through bacterial attacks on larval mussels’’ Since the publication of the work of Grizzle and Brunner in (Pritchard 2001). Intracellular microorganisms have been 2009, a few noteworthy studies have been published regarding observed in histological sections of the digestive gland of parasites in freshwater mussels. Levine et al. (2009) reported Elliptio complanata in the USA, but it was unclear if they Gomphus militarus (Arthropoda, Insecta, Odonata) as poten- were prokaryotic or eukaryotic (see Fig. 5 in Chittick et al. tially feeding on the gills of Popenaias popeii (Unionidae), a 2001). Fungal hyphae were observed in the marsupia of Unio critically endangered species restricted to two populations in pictorum, U. tumidus (Pekkarinen 1993a), and Pseudoano- the Rio Grande basin (Carman 2007). Some mussels were donta complanata in Finland (Pekkarinen 1993b). These latter missing the entire outer gills or all four gills. It is unclear how three studies or observations appear to have been overlooked often odonates occur in the mantle cavity of mussels, as there by Grizzle and Brunner (2009). It is possible that some appears to be no other literature on this topic (Grizzle and parasite or disease records may be missed because they appear Brunner 2009). Lopes et al. (2011) found third-stage larvae of in literature in which characterizing parasites or diseases was Hysterothylacium sp. (Nematoda, Anisakidae) in the pericar- not the primary objective, such as reports on surveys that detail dial cavity of Diplodon suavidicus (Hyriidae) in Brazil and population or community structure. Pekkarinen (1993a) presented photographs of nematodes coiled in the pericardial reported fungi and ciliates in the marsupium associated with cavity. In the early 20th century, Ascaris sp. or Ascaris-like degenerating glochidia, but it was unclear if the fungi were worms were reported in the digestive tract of unspecified pathogenic or saprophytic. Overall, parasitic or commensal unionids in the USA, but there were no accompanying species organisms have been reported primarily in wild mussels; there descriptions, no information about pathology, and no indica- is little information about disease problems that may occur in a tion that any specimens were deposited in a museum (Clark hatchery. and Wilson 1912; Wilson and Clark 1912; Coker et al. 1921). Ciliates (Ciliophora), trematodes (Platyhelminthes: Aspi- McElwain et al. (2016) described histopathological changes dogastrea, and Digenea), moss animals (Ectoprocta, Ento- associated with the eggs and larvae of Unionicola sp. from procta), roundworms (Nematoda), oligochaetes and leeches Strophitus connasaugaensis and provided a literature review (Annelida: Sedentaria: Clitellata), mites (Arthropoda: Acari), regarding pathologies associated with Unionicola spp. in copepods (Arthropoda: Crustacea: Copepoda), insects (Ar- unionids. Similarly, Abdel-Gaber et al. (2018) described thropoda: Insecta), and fish eggs (Chordata: Actinopterygii) injuries to the tissues of Coelatura aegyptiaca (Unionidae), are associated with the soft tissues or shells of freshwater Mutela rostrata, and Chambardia rubens (Mutelidae) associ- mussels (Grizzle and Brunner 2009; Wisniewski et al. 2013). ated with eggs and larvae of Unionicola tetrafurcatus.Muller¨ Aspidogastreans, digeneans, nematodes, mites, insect larvae, et al. (2015) described histopathological changes to the gonad and fish eggs either infect mussels or have been reported as and hepatopancreas associated with Rhipidocotyle campanula injurious agents. Interestingly, the eggs of both mites and Phyllodistomum sp. Few studies have demonstrated tissue (Najadicola ingens) and fishes (Rhodeus sericeus) sometimes damage associated with digeneans in unionids. may obstruct the water tubes of a marsupium and prevent or Parasite-induced pearl formation, shell deformities, and hinder the development of glochidia (Stadnichenko and neoplasms received little or no treatment by Grizzle and Stadnichenko 1980; McElwain et al. 2016 and references Brunner (2009). Mussels may form pearls in response to therein). Ciliates, oligochaetes, leeches, insect larvae, and digeneans (Clark and Wilson 1912; Wilson and Clark 1912; copepods have been found in the mantle cavity of mussels, but Gentner and Hopkins 1966; Hopkins