Exotic molluscs in the Great Lakes host epizootically important trematodes.
Abstract: One of the most significant ecological and economic impacts of exotic species is associated with their role as vectors for the introduction of parasites into invaded areas. Exotic parasites may have devastating impacts on invaded ecosystems; moreover, invaders may also become hosts for aboriginal parasites, promoting native diseases that otherwise would not have emerged. During 2009 and 2010, exotic molluscs were collected from 27 sites in the Lower Great Lakes and their tributaries, the Finger Lakes, and Lake Oneida. Seven species of exotic molluscs were examined for the presence of trematodes, including the zebra mussel (Dreissena polymorpha), quagga mussel (Dreissena rostriformis bugensis), faucet snail (Bithynia tentaculata), European stream valvata (Valvata piscinalis), Asian clam (Corbicula fluminea), Chinese mystery snail (Cipangopaludina chinensis), and the New Zealand mudsnail (Potamopyrgus antipodarum). Most of the examined molluscs were infected with trematode larvae that may be harmful to their subsequent vertebrate hosts, including fish, birds, and mammals. These included Sphaeridiotrema sp. cercariae and Cyathocotyle bushiensis metacercariae from B. tentaculata, Echinostoma sp. cercariae from V. piscinalis, and echinostomatid metacercariae from Dreissena spp. and C.fluminea. Many exotic molluscs that were believed to be free of parasites have already acquired trematodes native to North America. Hotspots of trematode infections were recorded in the western basin of Lake Erie and in Lake Oneida, where several species of exotic molluscs had a high prevalence of trematodes, and thus potentially pose risk of transmission to definitive hosts.

KEY WORDS: exotic species, parasites, trematodes, molluscs, Great Lakes
Article Type: Report
Subject: Bivalvia (Physiological aspects)
Authors: Karatayev, Alexander Y.
Mastitsky, Sergey E.
Burlakova, Lyubov E.
Karatayev, Vadim A.
Hajduk, Marissa M.
Conn, David Bruce
Pub Date: 08/01/2012
Publication: Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2012 National Shellfisheries Association, Inc. ISSN: 0730-8000
Issue: Date: August, 2012 Source Volume: 31 Source Issue: 3
Topic: Event Code: 690 Goods & services distribution Advertising Code: 59 Channels of Distribution Computer Subject: Company distribution practices
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 303011416
Full Text: INTRODUCTION

Exotic species are considered to be one of the major threats to global biodiversity (Wilcove et al. 1998). Their introduction and proliferation also often result in significant economic damage to industries and livelihoods (Pimentel et al. 2005). One of the most significant ecological and economic impacts of exotic species is associated with their role as vectors for the introduction of parasites into invaded areas (Brooks & Hoberg 2006, Brooks & Hoberg 2007, Hoberg & Brooks 2008). Exotic parasites introduced along with the free-living invaders may have devastating impacts on invaded ecosystems, including a risk to public health (Taylor et al. 2001, Lv et al. 2009), risk of extinction of endangered species (Holmes 1996, Dobson & Foufopoulos 2001, Mitchell et al. 2005), and mass mortalities of native hosts (Burreson et al. 2000, Edgerton et al. 2002, Cole & Franson 2006, Taraschewski 2006). The impact of infections on host populations throughout the world is expected to increase during the next 50-100 y as a result, in part, of the introduction of new disease agents (Scott 1988, Harvell et al. 2002), and will likely be facilitated by global climate change (Harvell et al. 2002, Brooks & Hoberg 2006, Brooks et al. 2006a, Poulin 2006, Brooks & Hoberg 2007, Marcogliese 2008). Dobson and Foufopoulos (2001) found that most of the outbreaks (about 60%) of emerging infectious diseases (EIDs) recorded in the wildlife of North America from 1998 to 2000 were caused by pathogens of exotic or likely exotic origin. Exotic parasites introduced with their exotic hosts may switch to new naive hosts with which they have no previous history of associations via ecological fitting, facilitating EID (Brooks & Hoberg 2007, Agosta et al. 2010, Mastitsky et al. 2010). The geographical scale of these EIDs is extremely wide (Harvell et al. 2002, Cattadori et al. 2005, Kutz et al. 2005, Mouritsen et al. 2005, Hoberg & Brooks 2008).

Invaders may also become hosts for aboriginal parasites, promoting native diseases that otherwise would not have emerged in the invaded regions (Torchin et al. 2003, Hoberg & Brooks 2008, Kelly et al. 2009, Mastitsky & Veres 2010, Mastitsky et al. 2010). All this can render considerable economic costs, especially when commercially exploited populations are under threat (Nepszy et al. 1972, Burreson et al. 2000, Pimentel et al. 2005, Brooks & Hoberg 2006).

Since 1840, the number of aquatic exotic species in the Great Lakes Region has been growing exponentially (Ricciardi 2006), resulting in a parallel growth of the risk of introduction of pathogenic exotic diseases. Some exotic parasites have already been discovered as a result of their significant population effects, such as, for example, the European protozoan Glugea hertwigi, which caused high-rate die-offs of the rainbow smelt in Lake Erie and Lake Ontario during the 1960s and 1970s (Nepszy et al. 1972), or the European trematode Leyogonimus polyoon, which has recently caused mass mortalities of waterfowl in northwestern Wisconsin (Cole & Franson 2006). Less pathogenic exotic parasites may already be present in the Great Lakes Region but remain largely undiscovered because of the lack of attention from the scientific community. New parasites may arrive as a result of continuing introductions of new free-living exotic species or because of repeated introductions of infected exotic hosts that have already been introduced into the region but initially were free of their specific parasites. This article focuses on the occurrence, prevalence, and intensity of infection with trematodes of 7 of the most common exotic molluscs in the Great Lakes Region.

MATERIALS AND METHODS

Sampling Protocol

During 2009 and 2010, exotic molluscs were collected for parasitological examination from 27 sites located in 12 waterbodies, including the Lower Great Lakes and their tributaries, Finger Lakes, and Lake Oneida (Table 1). Most sites were sampled once, and 5 sites were sampled twice. Seven species of exotic molluscs were examined for the presence of parasites and commensals during this study, including zebra mussel (Dreissena polymorpha), quagga mussel (Dreissena rostriformis bugensis), faucet snail (Bithynia tentaculata), European stream valvata (Valvata piscinalis), Asian clam (Corbicula fluminea), Chinese mystery snail (Cipangopaludina chinensis), and New Zealand mud snail (Potamopyrgus antipodarum). Although we sampled all locations within the state of New York where the exotic snail Lymnaea auricularia was previously reported, we did not find this species. We suggest that the snail has either been extirpated or that it may be present in extremely low densities below detection level.

In shallow littoral sites (<2 m) molluscs were collected by hand, whereas Ekman and boxcore grabs were used in deeper sites. To standardize our sampling procedure, at each sampling time and at each location, we planned to examine 50 exotic molluscs. However, because of various limitations (e.g., lack of molluscs), this wasn't always possible. For all infected molluscs, the prevalence (percent of infected molluscs) and intensity of infection (number of parasites in the infected individuals) were estimated using the following protocol. Before dissection, we cleaned and dried the shell surface and measured the shell length to the nearest 0.1 mm with calipers. Molluscs were then cut open with a scalpel and dissected in unchlorinated tap water within a plankton-counting chamber or a Petri dish under a stereomicroscope (20-70x). In most cases, the entire soft body of each mollusc was dissected, with special attention given to the gills and digestive gland, each piece of which was carefully checked for the presence of parasites. The number of parasites was counted and identified whenever possible, and photographs were taken using a compound microscope to facilitate further identification. All molluscs were dissected within 72 h of collection. Cercariae and metacercariae were identified to the level of morphotype (e.g., xiphidiocercaria) or family according to the diagnostic keys of Schell (1985), and further to genus or species using primary literature specific to the respective taxa (Burns 1961, McLaughlin et al. 1993, Sudarikov et al. 2002).

RESULTS

Dreissena polymorpha and Dreissena rostriformis bugensis

This is the first report of several taxa of trematodes from the North American populations of zebra and quagga mussels (Table 2). Metacercariae of Echinostomatidae, large metacercariae (unidentified), and small metacercariae (unidentified) were found in both dreissenid species. In addition, the metacercariae of Psilostomatidae, tentatively identified as Sphaeridiotrema sp., were found in D. r. bugensis from Lake Oneida.

Prevalence ofdreissenid infection with trematodes varied from none to virtually 100% within and among the sampled waterbodies. High prevalence of infection of both zebra and quagga mussels was found in the western basin of Lake Erie, whereas no or very low infection was recorded in the central and eastern basins. Similarly high variations were found in Lake Oneida (Table 2). No trematode infection was found in dreissenids from Eighteen Mile Creek or in the Finger Lakes, with the exception of 2 echinostomatid metacercariae found in zebra mussels in Lake Owasco and 2 unidentified metacercariae found in quagga mussels from Lake Cayuga: one in July 2009 and another in July 2010.

Infection intensity of zebra and quagga mussels in Lake Erie was always lower for large metacercariae than for small metacercariae (Table 2). The highest infection intensity of D. polymorpha with large metacercariae (7 cysts per mussel) and small metacercariae (25 cysts per mussel) was found in the same 10.0-mm mussels from the western basin of Lake Erie. At the same exact location, we found the highest infection intensity for D. r. bugensis. In a 14.2-mm-long quagga mussel, we recorded 15 cysts of large metacercariae and 51 cysts of small metacercariae.

Bithynia tentaculata

Five populations of the faucet snail were examined for the prevalence and intensity of infection with trematodes (Table 3). The 4 species of trematodes found were Cyathocotyle bushiensis and Echinostomatidae spp. (metacercariae), Sphaeridiotrema sp. (cercariae and rediae), and Xiphidiocercariae (cercariae), tentatively identified as L. polyoon. The prevalence of infection of B. tentaculata populations infected with C. bushiensis was generally higher compared with the infection of this snail with other trematodes. There was a strong variation of the prevalence of B. tentaculata infection with C. bushiensis within and among the studied waterbodies (Table 3).

Intensity of B. tentaculata infection with Xiphidiocercaria sp. and Echinostomatidae sp. cysts was low, and low to moderate with C. bushiensis (Table 3). The highest number of C. bushiensis metacercariae (45 cysts per snail) was found in B. tentaculata collected from the concrete wall of the Cornell biological station boat ramp on Lake Oneida. In Golden Hill Creek in May 2010, we found a high level of intensity of B. tentaculata infection with rediae and cercariae of Sphaeridiotrema sp. The highest number of cercariae of this parasite (6,850) was found in a 13. l-mm B. tentaculata collected from the mouth of the Golden Hill Creek in Golden Hill State Park.

Other Molluscs

Echinostomatid metacercariae were found in C. fluminea, with 4 of the 33 molluscs dissected from Lake Owasco being infected with echinostomatid cysts. The prevalence of infection was 12.1%, and the intensity of infection did not exceed 1 metacercaria per mussel. The cercariae ofEchinostoma sp. (3.8% prevalence, 178.5 [+ or -] 163.5 cercariae per snail infection intensity, mean [+ or -] SE) and the metacercariae of unidentified digenean trematodes (9.4% prevalence, 1 metacercariae per snail infection intensity) were revealed in V. piscinalis collected at the boat ramp site in Lake Oneida. No trematodes were found in P. antipodarum (270 snails dissected) or in C. chinensis (30 snails dissected).

DISCUSSION

Dreissena polymorpha and Dreissena rostriformis bugensis

In Europe, 7 genera of trematodes have been reported as parasites of Dreissena (Molloy et al. 1997, Stunzenas et al. 2004). For these parasites, dreissenids may serve as the first intermediate host (Bucephalus polymorphus, Phyllodistomum spp.), second intermediate host (Echinoparyphium recurvatum, Echinoparyphium paraulum, and Echinoparyphium echinatoides) or the only host (Aspidogaster spp.). The parasites B. polymorphus, Phyllodistomum spp., and E. recurvatum were reported in Dreissena exclusively from Europe (Molloy et al. 1997, Stunzenas et al. 2004). Although North American populations of zebra mussels were examined repeatedly for the presence of parasites since the introduction of dreissenids during the 1980s (Mills et al. 1996, Carlton 2008), no natural infections of D. polymorpha with echinostomatid and psilostomatid trematodes were found before the beginning of our study (Conn & Conn 1993, Toews et al. 1993, Conn & Conn 1995, Laruelle et al. 2002). Thus far, reports of trematodes in North American Dreissena were limited to Aspidogaster limacoides and unidentified Plagiorchiidae (Toews et al. 1993). The trematode A. limacoides requires only a single host to complete its life cycle; Aspidogaster is not specific to dreissenids and uses a wide variety of freshwater molluscs as hosts (Molloy et al. 1997).

Because metacercariae of many Echinostomatidae species are known from North American freshwater molluscs (Conn & Conn 1995), it was not surprising to find echinostomatid trematodes in dreissenids during our study. The prevalence of infection of dreissenid species with these trematodes in the Great Lakes Region was higher than that generally reported from Europe (Table 2). In contrast, low to moderate prevalence of infection was usually found in European zebra mussel populations. Ginezinskaja (1959) reported less than 1% infection of D. polymorpha with E. recurvatum, Chernogorenko and Boshko (1992) reported less than 1% infection with E. echinatoides, and Kochnev (1977) reported less than or equal to 8.5% of mixed infection with E. recurvatum and E. paraulum. In their study in Belarus, Karatayev et al. (2000) found echinostomatid metacercariae in zebra mussels in 10 of the 17 waterbodies studied, with the prevalence ranging from 0.3-8.5%. In only 2 waterbodies in Belarus was the prevalence of the zebra mussel infection with echinostomatids as high as 100% (Mastitsky 2005, Mastitsky & Veres 2010). The effect of echinostomatids on Dreissena and other intermediate hosts is usually benign (Molloy et al. 1997, Laruelle et al. 2002); however, infection of amphibian kidneys by metacercariae can result in severe pathology (Martin &Conn 1990), and definitive hosts can be affected negatively. The parasite E. recurvatum is common and, at times, fatal in North American waterfowl (McDonald 1969, Roscoe & Huffman 1982). Other echinostomatids could also be moderately to highly pathogenic to their definitive hosts (McDonald 1981). In Lake Oneida, high prevalence of echinostomatid infection coupled with the high density of dreissenids may result in a substantial increase of waterfowl infection, as they prey heavily on zebra mussels (Molloy et al. 1997).

Bithynia tentaculata

From the standpoint of diversity and adverse impacts on their vertebrate hosts, the trematode fauna of B. tentaculata in their native range far exceeds all other exotic molluscs examined in this study. At least 73 trematode taxa are known from the native range of B. tentaculata, and 4 of them have been documented to cause pathogenic effects in their definitive hosts, such as aquatic birds and mammals (Mastitsky et al. 2010). The faucet snail trematode B. tentaculata was first recorded in North America in Lake Michigan in 1871, but was probably introduced in 1870 (Mills et al. 1993). Three host-specific trematode species nonnative to North America have already been reported in the Great Lakes Region from populations of B. tentaculata, including C. bushiensis, Sphaeridiotrema sp., and L. polyoon (Cole & Friend 1999). In contrast to their native range in Europe, in North America--and especially in the Great Lakes Region--C. bushiensis and Sphaeridiotrema globulus infections have periodically caused mass mortalities in waterfowl since 1928 (reviewed in Herrmann and Sorensen (2009)). During the 2006 migration, an estimated 22,000-26,000 birds died in the Upper Mississippi River National Wildlife and Fish Refuge (Sauer et al. 2007). High levels of B. tentaculata infection with C. bushiensis found in 2 of the 5 populations sampled in this study, coupled with a high level of the faucet snail density, suggest that there is a serious risk for epizootics among waterfowl in the examined Lower Great Lakes Region.

Corbicula fluminea

In their native range, C. fluminea has been reported to host Phyllodistomum mingensis (Tang 1985), 5 species of Echinostoma (Echinostoma cinetorchis, Echinostoma lindoensis, Echinostoma macrorchis, Eehinostoma melis, and Echinostoma revolutum) (Keeler & Huffman 2009), and 7 species of Aspidogastrea (Tang 1992). The definitive host of P. mingensis is the fish Lateolabrax japonicus (Tang 1992), and vertebrate hosts of the Echinostoma species may include fish, amphibians, turtles, and humans (Chai 2009, Keeler & Huffman 2009). Despite a long history of C. fluminea research since their introduction into North America in 1938 (reviewed in McMahon (1999)), only aspidogastrid trematodes Aspidogaster conchicola and Cotylapsis insignis have been reported so far from North America (Danford & Joy 1984). Fried et al. (1987) infected North American C. fluminea experimentally with Echinostoma metacercariae in the laboratory, but noted no natural infections. Our discovery of the echinostomatid metacercariae naturally occurring in a single sampled population of C. fiuminea indicate that these trematodes already use the Asian clam as their intermediate host in the Great Lakes Region. Additional studies are necessary to estimate how widely these trematodes are distributed across North American populations of C. fluminea, and further taxonomic identifications of the metacercariae are required to evaluate potential pathogenic impacts on their vertebrate hosts.

Valvata piscinalis

At least 12 trematode taxa have been reported from the European stream valvata in its native range (Ginetzinskaja 1959, Sudarikov et al. 2002), including C. bushiensis, E. recurvatum (Sudarikov et al. 2002), and a sanguinicolid species (Ginetzinskaja 1959). Thus far, none of these trematodes has been reported for North American populations since the initial introduction of the snail in Lake Ontario in 1897 (reviewed in Grigorovich et al. (2005)). However, as V. piscinalis is known to host C. bushiensis and E. recurvatum in its native range (Sudarikov et al. 2002), and because these 2 parasites are present in the Great Lakes Region, we suggest that their finding in North American populations of the snail is only a matter of time. The ability of the European valvata to host C. bushiensis is especially alarming because, in addition to B. tentaculata, V. piscinalis can contribute to the circulation of this highly pathogenic trematode in the Great Lakes Region. Our discovery of Echinostoma sp. cercariae along with unidentified digenean metacercariae indicates that V. piscinalis in the Great Lakes Region already hosts at least 2 species of trematodes that may pose a risk to their vertebrate hosts.

Cipangopaludina chinensis

At least 9 species of trematodes use C. chinensis as their host in the native range of the Chinese mystery snail, including three species of Echinochasmus (Echinochasmus elongatus, Echinochasmus redioduplicatus, and Echinochasmus rugosus), 2 species of Echinoparyphium (E. recurvatum and Echinoparyphium ilocanum), and 4 species of Echinostoma (E. cinetorchis, E. macrorchis, E. melis, and E. revolutum) (Pace 1973, Keeler & Huffman 2009). Vertebrate hosts of these trematodes may include fish, amphibians, turtles, waterfowl, and humans (Chai 2009, Keeler & Huffman 2009). Although first records of C. chinensis in the North America date back to 1892, and sometime between 1931 and 1942 in the Great Lakes Region (reviewed in Mills et al. (1993)), none of these trematodes has ever been reported from the North American population of C. chinensis. Even the cosmopolitan E. recurvatum, commonly reported from freshwater molluscs of North America, has never been found in Chinese mystery snails in the New World. Thus far, only 1 trematode, A. conchicola, has been reported in C. chinensis in North America (Michelson 1970). The trematode A. conchicola is a cosmopolitan species, commonly occurring in freshwater molluscs of this region (Hendrix & Short 1965, Michelson 1970, Huehner & Etges 1977). We did not find any trematodes in C. chinensis during our survey. However, low sample size (only 30 snails were dissected) prevents us from a definite conclusion. Additional populations of the Chinese mystery snail should be examined for the presence of trematodes.

Potamopyrgus antipodarum

Fourteen species and higher taxa of trematodes were reported from native populations of the New Zealand mud snail (Macfarlane 1939, Winterbourn 1973, MacArthur & Featherston 1976, Jokela & Lively 1995, Dybdahl & Lively 1998). None of these species was associated with pathogenic impacts on their definitive hosts in the P. antipodarum native range. At the same time, in its invaded range in Europe, P. antipodarum acquired several parasites that are potentially pathogenic to their definitive hosts, including parasites from the family Sanguinicolidae (Gerard & Le Lannic 2003, Pointier et al. 2005, Morley 2008, Zbikowski & Zbikowska 2009) and E. recurvatum (Evans et al. 1981). Thus far, no parasites have been reported from North American populations of P. antipodarum since its initial introduction in 1987 (Bowler 1991). We also failed to find any parasites in 270 New Zealand mud snails dissected from Unnamed Creek in the Lake Ontario watershed. However, because P. antipodarum is known to host E. recurvatum, which is native to North America, we suggest that in the future this trematode may be discovered in the New Zealand mud snail.

General Findings

The average richness of trematode taxa per exotic mollusc found in this study (2.29 [+ or -] 0.29) was 8.5 times lower than in their native range (19.43 [+ or -] 3.40; P = 0.018, Wilcoxon's matched pairs test). The substantial reduction in parasite diversity associated with exotic species in introduced regions is a well-known phenomenon (Torchin et al. 2002, Torchin et al. 2003, Colautti et al. 2004, Prenter et al. 2004, Kelly et al. 2009, Mastitsky et al. 2010). However, it has also been shown that the reduction of parasite diversity in invaded areas occurred mainly as a result of the loss of low-impact species, whereas the number of high-impact parasite species (those documented as causing a distinct pathological effect in a large proportion of an infected host's population (e.g., livestock and wildlife), but not the exotic host of the parasite) did not differ significantly between the native and recipient areas (Mastitsky et al. 2010). Three mechanisms acting either individually or in combination can explain the similar numbers of high-impact parasites associated with freshwater exotic invertebrates in their native and invaded areas: (1) acquisition by the invaders of new high-impact parasites in the invaded regions, (2) high abundance of the invaders in their new ranges, and (3) high susceptibility of novel hosts to exotic parasites because of the "naive host syndrome" (Hoberg & Brooks 2008, Mastitsky et al. 2010). Our data provide evidence that all 3 of these mechanisms are taking place in the Great Lakes Region.

Mastitsky et al. (2010) found that 19 of the 22 examined freshwater invertebrates acquired parasites in the invaded regions, including those previously documented to cause epizootics. We found that at least 6 of the 7 examined species of exotic molluscs have already acquired novel trematode parasites in North America. The process of acquisition of aboriginal trematodes by exotic hosts, however, may be quite long. The Asian clam C. fluminea was first recorded in North America in 1938 (Burch 1944), but before our study, no trematodes with complex life cycles were reported from this species (Danford & Joy 1984). Similarly, early examinations of both Dreissena species in North America failed to reveal echinostomatid and psilostomatid trematodes (Conn & Conn 1993, Conn & Conn 1995, Laruelle et al. 2002). However, our discovery of high levels of infection by echinostomatid and other trematodes in both zebra and quagga mussels prove that they have also acquired trematodes that may be detrimental to their vertebrate hosts. We suggest that other exotic molluscs that are not yet known to host trematodes may acquire them in the future, or may already host such trematodes but remain largely undiscovered because of the lack of attention from the scientific community. This is especially probable for exotic molluscs, which are known in their native range to host cosmopolitan parasites like E. recurvatum and E. revolutum (Sorensen et al. 1997, Chai 2009).

The host population density is one of the major biotic factors promoting the transmission and persistence of parasitic diseases (Anderson & May 1981). As a result, outbreaks of native diseases can be facilitated by the high abundance of their novel exotic hosts (Kelly et al. 2009, Mastitsky & Veres 2010). In our study, most of the examined exotic molluscs were found to form high population densities. We also found that, at least in some cases, the prevalence of infection of exotic molluscs in the Great Lakes Region may exceed that usually reported from their native range. High host density coupled with the high level of infection can result in the high risk of parasite transmission to the subsequent vertebrate hosts.

In the native range, hosts and their parasites are usually coadapted as a result of the long history of coevolution, so that parasites are rarely highly virulent to their hosts (May & Anderson 1983, Taraschewski 2006). In contrast, exotic parasites in invaded areas can infect "naive hosts" that lack historically evolved resistance, and therefore can severely affect these novel hosts, often in the form of mass mortalities (Alderman et al. 1987, Burreson et al. 2000, Taraschewski 2006). The faucet snail B. tentaculata is suspected to be responsible for the introduction of 3 species of parasites new to the Great Lakes: Sphaeridiotrema sp., C. bushiensis, and L. polyoon (Cole & Franson 2006, Sauer et al. 2007). The transmission of L. polyoon from B. tentaculata to its vertebrate host caused mass mortalities of American coot in north-central Wisconsin (Cole & Franson 2006). In its native range, however, this parasite has never been reported to cause such mortalities. Host switching of exotic parasites to naive hosts via ecological fitting in invaded areas is very common across many taxa, including phytophagous insects and their host plants (reviewed in Brooks et al. (2006b), Agosta (2006), Agosta and Klemens (2008), Janz and Nylin (2008), and Brooks and Hoberg (2008)), and occurs on wide temporal and spatial scales (Hoberg & Brooks 2008, Agosta et al. 2010). This process is thought to be facilitated by global climate change, and is predicted to cause a sharp increase in EID in the future (Brooks & Hoberg 2007, Brooks & Hoberg 2008, Agosta et al. 2010).

In conclusion, our study demonstrates that most of the examined exotic molluscs in the Great Lakes Region host trematodes that may be harmful for their vertebrate hosts, including fish and waterfowl. Many exotic molluscs that were believed to be free of parasites have already acquired trematodes native to North America, and other exotics may acquire them in the future. Hotspots of trematode infections were recorded in the western basin of Lake Erie and Lake Oneida, where several species of exotic molluscs had a high prevalence of trematodes, and thus posed high risks of transmission of the parasites to definitive hosts. Nevertheless, our study doesn't represent a complete assessment of the role of exotic molluscs as hosts for pathogenic parasites, and additional surveys are urgently necessary, as is a thorough identification of trematodes using molecular techniques. Risk assessment of the parasitological consequences of the introduction of exotic species requires more attention from aquatic ecologists and parasitologists. We suggest that parasitological assessment be an integral part in assessing the ecological and economic risks these species pose.

ACKNOWLEDGMENTS

We thank the staff and the director of the Cornell University Biological Station Lars Rudstam for providing space and field support for this project, as well as the captain and crew of the U.S. EPA R/V Lake Guardian. This project was funded by the New York Great Lakes Protection Fund Small Grants Program administered by the Great Lakes Research Consortium, in cooperation with the New York Department of Environmental Conservation and the New York Great Lakes Basin Advisory Council ("Preliminary risk assessment of the parasites of aquatic exotic invertebrates in the Great Lakes Region" to L. E. B. and A. Y. K.), and in part by the U.S. Environmental Protection Agency ("The nearshore and offshore Lake Erie nutrient study" to C. Pennuto, A. Y. Karatayev, A. PerezFuentetaja, and L. E. Burlakova). We thank Robbyn J. Drake (Buffalo Niagara Riverkeeper) for help in sampling. L. E. B. and S. E. M. were also supported by the Research Foundation of SUNY.

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ALEXANDER Y. KARATAYEV, (1) * SERGEY E. MASTITSKY, (1,2,3) LYUBOV E. BURLAKOVA, (1,2) VADIM A. KARATAYEV, (4) MARISSA M. HAJDUK (1,5) ([dagger]) AND DAVID BRUCE CONN (6,7)

(1) Great Lakes Center, Buffalo State College, 1300 Elmwood Avenue, Buffalo, NY 14222; (2) The Research Foundation of The State University of New York, Buffalo State College, Office of Sponsored Programs, Buffalo, NY; 3 RNT Consulting, Ontario, Canada," 4 University Honors College, State University of New York at Buffalo, Buffalo, NY 14260; (5) Department of Biology, Buffalo State College, 1300 Elmwood Avenue, Buffalo, NY 14222; (6) One Health Center, School of Mathematical and Natural Sciences, Berry College, Mount Berry, GA 30149; (7) Department of Invertebrate Zoology, Museum of Comparative Zoology, Harvard University, 26 Oxford St., Cambridge, MA 02138

* Corresponding author. E-mail: karataay@buffalostate.edu

([dagger]) Present address: School of Fisheries and Ocean Sciences, PO Box 757220, University of Alaska Fairbanks, Fairbanks, AK 99775-7220

DOI: 10.2983/035.031.0337
TABLE 1.
Occurrence of exotic molluscs examined for trematodes in the
Great Lakes Region in 2009 and 2010.

Sampled Sites                             Bithynia     Cipangopaludina
and Coordinates                          tentaculata      chinensis

Lake Erie, western basin, June 2009
  Station ER60, 41[degrees]53.470 N,         nf              nf
    083[degrees]11.700 W
Lake Erie, eastern basin, July 2009
  Station E1, 42[degrees]06.310 N,           nf              nf
    080[degrees]18.070 W
  Station E2, 42[degrees]10.080 N,           nf              nf
    080[degrees]09.760 W
  Station E3, 42[degrees]12.200 N,           nf              nf
    080[degrees]02.600 W
  Station E7, 42[degrees]25.010 N,           nf              nf
    079[degrees]29.260 W
Lake Erie, central basin, July 2009
  Station C3, 41[degrees]32.200 N,           nf              nf
    081[degrees]57.870 W
  Station C6, 41[degrees]46.860 N,           nf              nf
    081[degrees]19.570 W
  Station C9, 41[degrees]58.870 N,           nf              nf
    080[degrees]40.170 W
Lake Erie, western basin, July 2009
  Station W1, 41[degrees]53.050 N,           nf              nf
    083[degrees]05.010 W
  Station W3, 41[degrees]50.220 N,           nf              nf
    083[degrees]07.600 W
  Station W5, 41[degrees]46.200 N,           nf              nf
    083[degrees]05.440 W
  Station W7, 41[degrees]44.980 N,           nf              nf
    082[degrees]56.060 W
  Station W10, 41[degrees]45.200 N,          nf              nf
    082[degrees]45.310 W
18 Mile Creek (Lake Ontario tributary)
  July 2009, 43[degrees]20.116 N,            nf              nf
  078[degrees]42.899 W
Golden Hill Creek,
    Golden Hill State Park, NY
  July 2009, 43[degrees]22.266 N,            15              nf
    078[degrees]28.540 W
  May 2010, 43[degrees]22.281 N,             57              nf
    078[degrees]28.611 W
Unnamed Creek
    (Lake Ontario tributary), NY
  May-July 2009,43[degrees]16.230 N,         nf              nf
    079[degrees]01.271 W
Lake Cayuga, NY
  July 2009,42[degrees]53.901 N,             nf              nf
    076[degrees]44.969 W
  July 2010,42[degrees]28.266 N,             nf              nf
    076[degrees]30.211 W
  July 2010,42[degrees]27.754 N,             50              nf
    076[degrees]30.289 W
Lake Seneca, Geneva, NY, July 2009,
  42[degrees]52.341 N,                       nf              nf
    076[degrees]57.315 W
Lake Canandaigua, NY, July 2009
  42[degrees]52.448 N,                       nf              nf
    077[degrees]16.337 W
Lake Otisco, NY, July 2009
  42[degrees]50.670 N,                       nf              nf
    076[degrees]15.909 W
Lake Oneida, NY, Cornell biological
    station boat ramp,
  43[degrees]17.334 N,
    075[degrees]93.066 W
  June 2010                                  30              nf
  July 28, 2010                              20              nf
  July 23, 2010                              nf              nf
Dump place, 43[degrees]22.377 N,
    076[degrees]01.186 W
  June 2010                                  25              nf
  July 2010                                  nf              nf
Lake Owasco, Auburn, NY, August 2010
  Melrose Park, 42[degrees]90.257 N,         nf              nf
    076[degrees]54.063 W
  Boat channel, 42[degrees]92.331 N,         nf              10
    076[degrees]53.910 W
Niagara River, Beaver Island, NY,
    July 2010
  42[degrees]96.897 N,                       49              nf
    078[degrees]94.334 W
Woods Creek, Niagara River tributary,
    NY
  June 2010,43 3.603 N,                      nf              20
    078[degrees]58.694 W

Sampled Sites                            Corbicula   Dreissena
and Coordinates                          fluminea    polymorpha

Lake Erie, western basin, June 2009
  Station ER60, 41[degrees]53.470 N,        nf           30
    083[degrees]11.700 W
Lake Erie, eastern basin, July 2009
  Station E1, 42[degrees]06.310 N,          nf           5
    080[degrees]18.070 W
  Station E2, 42[degrees]10.080 N,          nf           20
    080[degrees]09.760 W
  Station E3, 42[degrees]12.200 N,          nf           nf
    080[degrees]02.600 W
  Station E7, 42[degrees]25.010 N,          nf           nf
    079[degrees]29.260 W
Lake Erie, central basin, July 2009
  Station C3, 41[degrees]32.200 N,          nf           nf
    081[degrees]57.870 W
  Station C6, 41[degrees]46.860 N,          nf           nf
    081[degrees]19.570 W
  Station C9, 41[degrees]58.870 N,          nf           4
    080[degrees]40.170 W
Lake Erie, western basin, July 2009
  Station W1, 41[degrees]53.050 N,          nf           18
    083[degrees]05.010 W
  Station W3, 41[degrees]50.220 N,          nf           10
    083[degrees]07.600 W
  Station W5, 41[degrees]46.200 N,          nf           nf
    083[degrees]05.440 W
  Station W7, 41[degrees]44.980 N,          nf           4
    082[degrees]56.060 W
  Station W10, 41[degrees]45.200 N,         nf           nf
    082[degrees]45.310 W
18 Mile Creek (Lake Ontario tributary)
  July 2009, 43[degrees]20.116 N,           nf           20
  078[degrees]42.899 W
Golden Hill Creek,
    Golden Hill State Park, NY
  July 2009, 43[degrees]22.266 N,           nf           nf
    078[degrees]28.540 W
  May 2010, 43[degrees]22.281 N,            nf           nf
    078[degrees]28.611 W
Unnamed Creek
    (Lake Ontario tributary), NY
  May-July 2009,43[degrees]16.230 N,        nf           nf
    079[degrees]01.271 W
Lake Cayuga, NY
  July 2009,42[degrees]53.901 N,            nf           20
    076[degrees]44.969 W
  July 2010,42[degrees]28.266 N,            nf           33
    076[degrees]30.211 W
  July 2010,42[degrees]27.754 N,            nf           nf
    076[degrees]30.289 W
Lake Seneca, Geneva, NY, July 2009,
  42[degrees]52.341 N,                      nf           nf
    076[degrees]57.315 W
Lake Canandaigua, NY, July 2009
  42[degrees]52.448 N,                      nf           2
    077[degrees]16.337 W
Lake Otisco, NY, July 2009
  42[degrees]50.670 N,                      nf           20
    076[degrees]15.909 W
Lake Oneida, NY, Cornell biological
    station boat ramp,
  43[degrees]17.334 N,
    075[degrees]93.066 W
  June 2010                                 nf           nf
  July 28, 2010                             nf           nf
  July 23, 2010                             nf           33
Dump place, 43[degrees]22.377 N,
    076[degrees]01.186 W
  June 2010                                 nf           nf
  July 2010                                 nf           33
Lake Owasco, Auburn, NY, August 2010
  Melrose Park, 42[degrees]90.257 N,        33           33
    076[degrees]54.063 W
  Boat channel, 42[degrees]92.331 N,        nf           nf
    076[degrees]53.910 W
Niagara River, Beaver Island, NY,
    July 2010
  42[degrees]96.897 N,                      nf           nf
    078[degrees]94.334 W
Woods Creek, Niagara River tributary,
    NY
  June 2010,43 3.603 N,                     nf           nf
    078[degrees]58.694 W

Sampled Sites                                            Potamopyrgus
and Coordinates                          D.r. bugensis   antipodarum

Lake Erie, western basin, June 2009
  Station ER60, 41[degrees]53.470 N,           3              nf
    083[degrees]11.700 W
Lake Erie, eastern basin, July 2009
  Station E1, 42[degrees]06.310 N,            15              nf
    080[degrees]18.070 W
  Station E2, 42[degrees]10.080 N,            15              nf
    080[degrees]09.760 W
  Station E3, 42[degrees]12.200 N,            15              nf
    080[degrees]02.600 W
  Station E7, 42[degrees]25.010 N,            15              nf
    079[degrees]29.260 W
Lake Erie, central basin, July 2009
  Station C3, 41[degrees]32.200 N,             4              nf
    081[degrees]57.870 W
  Station C6, 41[degrees]46.860 N,             3              nf
    081[degrees]19.570 W
  Station C9, 41[degrees]58.870 N,            11              nf
    080[degrees]40.170 W
Lake Erie, western basin, July 2009
  Station W1, 41[degrees]53.050 N,            15              nf
    083[degrees]05.010 W
  Station W3, 41[degrees]50.220 N,            13              nf
    083[degrees]07.600 W
  Station W5, 41[degrees]46.200 N,            15              nf
    083[degrees]05.440 W
  Station W7, 41[degrees]44.980 N,            10              nf
    082[degrees]56.060 W
  Station W10, 41[degrees]45.200 N,           15              nf
    082[degrees]45.310 W
18 Mile Creek (Lake Ontario tributary)
  July 2009, 43[degrees]20.116 N,             nf              nf
  078[degrees]42.899 W
Golden Hill Creek,
    Golden Hill State Park, NY
  July 2009, 43[degrees]22.266 N,             nf              nf
    078[degrees]28.540 W
  May 2010, 43[degrees]22.281 N,              nf              nf
    078[degrees]28.611 W
Unnamed Creek
    (Lake Ontario tributary), NY
  May-July 2009,43[degrees]16.230 N,          nf             270
    079[degrees]01.271 W
Lake Cayuga, NY
  July 2009,42[degrees]53.901 N,              20              nf
    076[degrees]44.969 W
  July 2010,42[degrees]28.266 N,              33              nf
    076[degrees]30.211 W
  July 2010,42[degrees]27.754 N,              nf              nf
    076[degrees]30.289 W
Lake Seneca, Geneva, NY, July 2009,
  42[degrees]52.341 N,                        20              nf
    076[degrees]57.315 W
Lake Canandaigua, NY, July 2009
  42[degrees]52.448 N,                        20              nf
    077[degrees]16.337 W
Lake Otisco, NY, July 2009
  42[degrees]50.670 N,                        nf              nf
    076[degrees]15.909 W
Lake Oneida, NY, Cornell biological
    station boat ramp,
  43[degrees]17.334 N,
    075[degrees]93.066 W
  June 2010                                   nf              nf
  July 28, 2010                               nf              nf
  July 23, 2010                               34              nf
Dump place, 43[degrees]22.377 N,
    076[degrees]01.186 W
  June 2010                                   nf              nf
  July 2010                                   33              nf
Lake Owasco, Auburn, NY, August 2010
  Melrose Park, 42[degrees]90.257 N,          nf              nf
    076[degrees]54.063 W
  Boat channel, 42[degrees]92.331 N,          nf              nf
    076[degrees]53.910 W
Niagara River, Beaver Island, NY,
    July 2010
  42[degrees]96.897 N,                        nf              nf
    078[degrees]94.334 W
Woods Creek, Niagara River tributary,
    NY
  June 2010,43 3.603 N,                       nf              nf
    078[degrees]58.694 W

Sampled Sites                             Valvata
and Coordinates                          piscinalis

Lake Erie, western basin, June 2009
  Station ER60, 41[degrees]53.470 N,         nf
    083[degrees]11.700 W
Lake Erie, eastern basin, July 2009
  Station E1, 42[degrees]06.310 N,           nf
    080[degrees]18.070 W
  Station E2, 42[degrees]10.080 N,           nf
    080[degrees]09.760 W
  Station E3, 42[degrees]12.200 N,           nf
    080[degrees]02.600 W
  Station E7, 42[degrees]25.010 N,           nf
    079[degrees]29.260 W
Lake Erie, central basin, July 2009
  Station C3, 41[degrees]32.200 N,           nf
    081[degrees]57.870 W
  Station C6, 41[degrees]46.860 N,           nf
    081[degrees]19.570 W
  Station C9, 41[degrees]58.870 N,           nf
    080[degrees]40.170 W
Lake Erie, western basin, July 2009
  Station W1, 41[degrees]53.050 N,           nf
    083[degrees]05.010 W
  Station W3, 41[degrees]50.220 N,           nf
    083[degrees]07.600 W
  Station W5, 41[degrees]46.200 N,           nf
    083[degrees]05.440 W
  Station W7, 41[degrees]44.980 N,           nf
    082[degrees]56.060 W
  Station W10, 41[degrees]45.200 N,          nf
    082[degrees]45.310 W
18 Mile Creek (Lake Ontario tributary)
  July 2009, 43[degrees]20.116 N,            nf
  078[degrees]42.899 W
Golden Hill Creek,
    Golden Hill State Park, NY
  July 2009, 43[degrees]22.266 N,            nf
    078[degrees]28.540 W
  May 2010, 43[degrees]22.281 N,             nf
    078[degrees]28.611 W
Unnamed Creek
    (Lake Ontario tributary), NY
  May-July 2009,43[degrees]16.230 N,         nf
    079[degrees]01.271 W
Lake Cayuga, NY
  July 2009,42[degrees]53.901 N,             nf
    076[degrees]44.969 W
  July 2010,42[degrees]28.266 N,             nf
    076[degrees]30.211 W
  July 2010,42[degrees]27.754 N,             nf
    076[degrees]30.289 W
Lake Seneca, Geneva, NY, July 2009,
  42[degrees]52.341 N,                       nf
    076[degrees]57.315 W
Lake Canandaigua, NY, July 2009
  42[degrees]52.448 N,                       nf
    077[degrees]16.337 W
Lake Otisco, NY, July 2009
  42[degrees]50.670 N,                       nf
    076[degrees]15.909 W
Lake Oneida, NY, Cornell biological
    station boat ramp,
  43[degrees]17.334 N,
    075[degrees]93.066 W
  June 2010                                  53
  July 28, 2010                              nf
  July 23, 2010                              nf
Dump place, 43[degrees]22.377 N,
    076[degrees]01.186 W
  June 2010                                  nf
  July 2010                                  nf
Lake Owasco, Auburn, NY, August 2010
  Melrose Park, 42[degrees]90.257 N,         nf
    076[degrees]54.063 W
  Boat channel, 42[degrees]92.331 N,         nf
    076[degrees]53.910 W
Niagara River, Beaver Island, NY,
    July 2010
  42[degrees]96.897 N,                       nf
    078[degrees]94.334 W
Woods Creek, Niagara River tributary,
    NY
  June 2010,43 3.603 N,                      nf
    078[degrees]58.694 W

Cell values are numbers of molluscs dissected. nf, host mollusc
not found and/or not examined at the station.

TABLE 2.
Prevalence and intensity of infection of Dreissena polymorpha and
Dreissena rostriformis hugensis with trematodes in the Great Lakes
Region.

                                     D. polymorpha

                           Large                    Small
Sampled Sites          Metacercariae            Metacercariae

Lake Erie,        53.3                     4.5
    western       1.81 [+ or -] 0.34 (6)    4.00 (4)
    basin,
    June 2009
Lake Erie,
    eastern
    basin,
    June 2009
  Station E1       0                        0

  Station E2       0                       75.0
                                            3.27 [+ or -] 0.69 (9)
Lake Erie,
    western
    basin,
    July 2009
  Station W1      27.8                     55.66
                   1.20 [+ or -] 0.20 (2)   2.00 (2)
  Station W3      70.0                     80.0
                   3.71 [+ or -] 0.75 (7)  11.75 [+ or -] 2.86 (25)
  Station W5                nf                        nf

  Station W7      25.0                     50.0
                   1.00 (l)                 9.00 [+ or -] 8.00 (17)
Lake Cayuga,       0                        0
    July 2009
    July 2010      0                        0

Lake Oneida,       0                        0
    boat ramp,
    July 2010

Lake Owasco,       0                        0
    August 2010

                        D. polymorpha              D. r. bugensis

                            Other                       Large
Sampled Sites           Metacercariae               Metacercariae

Lake Erie,         0                          100.0
    western                                     1.33 [+ or -] 0.33 (2)
    basin,
    June 2009
Lake Erie,
    eastern
    basin,
    June 2009
  Station E1       0                            6.7
                                                4.0
  Station E2       0                            0

Lake Erie,
    western
    basin,
    July 2009
  Station W1       0                           73.3
                                                1.18 [+ or -] 0.18 (3)
  Station W3       0                           92.3
                                                4.67 [+ or -] 1.12 (15)
  Station W5       0                           13.3
                                                1.00 (1)
  Station W7       0                           10.0
                                                2.00 (2)
Lake Cayuga,       0                            0
    July 2009
    July 2010      0                            0

Lake Oneida,      63.6                          0
    boat ramp,     2.57 [+ or -] 0.50 (11) *
    July 2010

Lake Owasco,      6.1                                    nf
    August 2010    1.00 (1) *

                                    D. r. bugensis

                          Small                       Other
Sampled Sites         Metacercariae               Metacercariae

Lake Erie,        0                         0
    western
    basin,
    June 2009
Lake Erie,
    eastern
    basin,
    June 2009
  Station E1      0                         0

  Station E2      0                         0

Lake Erie,
    western
    basin,
    July 2009
  Station W1      0                         0

  Station W3     84.6                       0
                 10.64 [+ or -] 4.22 (51)
  Station W5     60.0                       0
                  2.11 [+ or -] 0.42 (4)
  Station W7     90.0                       0
                  5.00 [+ or -] 1.44 (16)
Lake Cayuga,      0                         5.0
    July 2009                               1.00 (1) ([dagger])
    July 2010     0                        33-0
                                            1.00 (1) ([dagger])
Lake Oneida,      0                        24.2
    boat ramp,                              1.13 [+ or -] 0.13 (2)*
    July 2010                              3.0
                                            2.00 (2) ([double dagger])
Lake Owasco,                nf              0
    August
    2010

* Echinostomatidae.

([dagger]) Unidentified digenean metacercaria.

([double dagger]) Psilostomatidae (Sphaeridiotrenna sp.?).

Cell values are prevalence (above the line) and intensity (below the
line, mean f SE); maximum values are in parenthesis. Only sites
where infected mussels were found are included. nf, host dreissenid
not found at the station.

TABLE 3.
Prevalence and intensity of infection of Bithynia tentaculata with
trematodes in the Great Lakes Region.

                                                    Cyathocotyle
                      Sphaeridiotrema sp.,           bushiensis,
  Sampled Sites       Cercariae and Rediae          Metacercariae

Golden Hill Creek
  July 2009            0                       33.3
                                                1.8 [+ or -] 3.7 (3)
  May 2010            12.3                      7.0
                   2,499 [+ or -] 877 (6,850)   7.0 [+ or -] 3.3 (15)
Lake Cayuga,           0                        0
  July 2010
Lake Oneida, 2010
  Boat ramp, June      0                       13.3
                                               13.5 [+ or -] 10.5 (45)
  Boat ramp, July      0                       60.0
                                                4.9 [+ or -] 1.7 (17)
Niagara River,         0                        6.1
  July 2010                                     4.0 [+ or -] 1.5 (6)

                    Xiphidiocercariae      Echinostomatidae
                       (Leyogonimus           gen. spp.,
  Sampled Sites    polyoon?), Cercariae     Metacercariae

Golden Hill Creek
  July 2009        0                     0

  May 2010         3.5                   0
                   4.0 [+ or -] 1.0 (5)
Lake Cayuga,       0                     4.0
  July 2010                              1.0 (1)
Lake Oneida, 2010
  Boat ramp, June                        0

  Boat ramp, July                        0

Niagara River,                           4.1
  July 2010                              5.5 [+ or -] 0.5 (6)

Cell values are prevalence (above the line) and intensity (below the
line, mean [+ or -] SE), with maximum values in parentheses. Only
sites where infected  snails were found are included.
Gale Copyright: Copyright 2012 Gale, Cengage Learning. All rights reserved.