Freshwater Biology ( IF 2.8 ) Pub Date : 2022-05-23 , DOI: 10.1111/fwb.13919 Amy E. Fowler 1 , Grace A. Loonam 1 , April M. H. Blakeslee 2
1 INTRODUCTION
Globally, freshwater biodiversity is at risk from anthropogenic forces (e.g., climate change, water pollution, flow modification, habitat degradation; Dudgeon et al., 2006; Reid et al., 2019), with non-indigenous species being a leading cause of these declines (Dudgeon et al., 2006; Parker et al., 1999; Reid et al., 2019). Parasites are integral ecosystem members and, like hosts, can be introduced to novel locations via numerous anthropogenic mechanisms (i.e., introduction vectors; Blakeslee et al., 2013; Keller et al., 2009). While much of our understanding of invasion ecology relates to the direct effects of novel organisms on native communities, co-introduced parasites can have strong effects on existing relationships within the larger multi-host, multi-parasite community (Lymbery et al., 2014; Prenter et al., 2004). However, in many cases, non-indigenous species experience a respite from parasite burdens in introduced ranges (Ebbs et al., 2018) because just a subset of individuals entrained in an introduction vector will be parasitised (Torchin et al., 2003). Additionally, the likelihood for successful parasite invasion is lessened by the invasion process itself (infected hosts may die or be lost) and the limitations imposed by parasite life cycle requirements (competent hosts, entrained life stages of hosts, etc.; Blakeslee et al., 2020). In some cases, parasites do successfully establish with non-indigenous hosts and may then take advantage of novel, indigenous hosts. Additionally, non-indigenous species can act as novel hosts for indigenous parasites (i.e., host-switching), which could ultimately induce broad ecosystem changes (Barse & Secor, 1999; Font & Tate, 1994; Goedknegt et al., 2016; Holmes & Minchin, 1995; Kelley et al., 2009a). This can be especially important for the organisms that are directly involved in the symbiosis, resulting in novel interactions that can alter native host–native parasite infection dynamics and population dynamics of all parties (Lagrue, 2017; Tompkins et al., 2011). However, our understanding of the role of parasitism in species invasions is generally lacking, particularly in describing interactions of co-invasive parasites and native parasites (Poulin, 2017; Telfer & Bown, 2012). Broadening this knowledge is crucial to characterise the impact of invasions on the direct and indirect effects of both the invader and co-invader within and across communities (Telfer & Bown, 2012).
Varying infection susceptibilities to parasites between indigenous and non-indigenous hosts can modulate invasions (Torchin et al., 2005). Lower parasite burdens (i.e., parasite escape) in non-indigenous species may provide non-indigenous hosts with an edge over indigenous species with a full complement of parasites (Larson & Krist, 2020; Torchin et al., 2005). Because parasites may negatively affect growth, reproduction, and competitiveness of hosts, parasite loss could contribute to successful establishments of non-indigenous hosts via enhanced biological, ecological, or physiological performance (= parasite release; Blakeslee et al., 2013; Torchin et al., 2003). For example, non-indigenous populations of the freshwater snail Melanoides tuberculata are parasite free in Lake Malawi, resulting in larger snails that produce more juveniles in areas where indigenous snails have more parasites (Genner et al., 2008). Furthermore, parasites can mediate interactions between indigenous species and non-indigenous species; for example, when indigenous amphipods Gammarus duebeni celticus are parasitised by an indigenous microsporidian parasite, they exhibit a reduced feeding response and are preyed upon more often than uninfected, non-indigenous amphipods (MacNeil et al., 2003).
Like hosts, parasite prevalence can vary spatially (Shaw & Dobson, 1995) and is driven by biotic (e.g., host–parasite specificity, distribution and abundance of hosts, inter-specific relationships between parasites, host size, life cycle stage of the parasite) and abiotic factors (e.g., salinity, temperature, physical structure, stream drift; Hechinger & Lafferty, 2005; Karvonen & Valtonen, 2004; Marcogliese & Cone, 1991; Thieltges & Reise, 2007). For example, Blasco-Costa et al. (2013) found a longitudinal gradient in trematode parasite prevalence in fish in a New Zealand river, with highest prevalence downstream and lowest prevalence upstream. Other studies have linked spatial differences in parasite prevalence in flowing freshwater systems to salinity and eutrophication gradients (e.g., Blanar et al., 2011), host community assemblage (e.g., Kelly et al., 2009b), and distance from final host colonies (e.g., Marcogliese et al., 2001), among others. Such heterogeneity is critical for maintaining spatial refuges for hosts from parasites, allowing host populations to thrive while maintaining parasite populations in other locations distinct from these refuges; ultimately promoting stable populations of both host and parasite (Brockhurst et al., 2006; Maynard-Smith, 1974; Schrag & Mittler, 1996).
One group of parasites—trematodes in the subclass Digenea—have been used in multiple past studies to explore relationships between non-indigenous hosts and parasites (e.g., Blakeslee & Byers, 2008; Lively et al., 2004; Sorensen & Minchella, 2001). Most trematodes have complex life cycles with invertebrate and vertebrate hosts (Shoop, 1988). A simplified life cycle starts with eggs shed in faeces by vertebrate hosts. Ingested eggs hatch into miracidia larvae that actively penetrate a mollusc host. The miracidia metamorphose in gonad tissue and release cercarial stages into the water column, which infect a second-intermediate host and encyst as metacercariae. The infected host must be consumed by vertebrate final hosts. However, some trematodes in the sister subclass to the Digenea, the Aspidogastrea, have a simpler life cycle, often using one or two hosts, in which molluscs can serve as intermediate or final hosts (Schell, 1985). Trematodes generally have negative effects on mollusc host survivorship, fecundity, growth rates, behaviour, and morphology, thus influencing hosts' competitive abilities and population abundances (Byers & Goldwasser, 2001; Fredensborg et al., 2005; Sorensen & Minchella, 2001).
Globally, exotic freshwater gastropods have invaded ecosystems through multiple introduction vectors, including deliberate introductions and accidental anthropogenic transfer (Padilla & Williams, 2004). One such invader, the Japanese mystery snail (Heterogen japonica, synonym Cipangopaludina japonica; Saito & Kagawa, 2020), was intentionally transported from Japan to North America in c. 1911 to be cultivated for human consumption (Clench & Fuller, 1965; Prashad, 1928), but is now found in tributaries throughout North America (Jokinen, 1982; USGS, 2021). Due to its feeding habits (i.e., filter feeder and detritivore), Heterogen japonica can improve overall water quality and productivity in invaded freshwater systems (Solomon et al., 2010; Van Bocxlaer & Strong, 2016); however, it can also negatively impact indigenous snail populations, partly due to exponential population growth in invaded systems (Johnson et al., 2009; Wolfert & Hiltunen, 1968). Parasitism can control host population growth, and if a host population escapes much of its parasite load, it may be relieved of a substantial pressure (Torchin & Mitchell, 2004). Heterogen japonica is infected by four castrating digenean species in its native range (Table 1), while only one trematode species (the aspidogastrean Aspidogaster conchicola) has been recorded in North America from one non-indigenous population (Massachusetts, U.S.A.; Michelson, 1970). However, to date, little effort has been made to characterise parasite infection, or associates more generally, in mystery snails in the non-indigenous range.
| Host snail | Trematode Genus or Species | Trematode Type: Family | Region/State | Citations |
|---|---|---|---|---|
| Indigenous species | ||||
| Campeloma decisum (Say, 1817) | Amblosoma suwaense (Pojmanska, 1972) | Digenea: Leucochloridiomorphidae | WI | Fried et al., 1981 |
| Aspidogaster conchicola (von Baer, 1827) | Aspidogastrea : Aspidogastridae | PA | Alves et al., 2015 | |
| Azygia acuminata (Goldberger, 1911) | Digenea: Azygiidae | Cape Cod, MA | Wootton, 1957 | |
| Leucochloridiomorpha constantiae (Mueller, 1935) | Digenea: Leucochloridiomorphidae | Eastern North America; MI | Allison, 1943; Fried & Bradford, 1984; Johnson, 1992 | |
| Ptyalincola ondatrae (Wootton & Murrell, 1967) | Digenea: Leucochloridiomorphidae | MI | Wootton & Murrell, 1967 | |
| Sanguinicola occidentalis (van Cleave & Mueller, 1932) | Digenea: Aporocotylidae | MI | Muzzall, 2000 | |
| Elimia (=Pleurocera) Goionbasis virginica (Gmelin, 1791) | Aspidogaster conchicola (von Baer, 1827) | Aspidogastrea: Aspidogastridae | NJ | Huffman & Fried, 1983 |
| Lecithodendriid trematode | Digenea: Lecithodendriidae | NJ | Huffman & Fried, 1983 | |
| Microphallid sporocysts, cercariae of ubiquita type | Digenea: Microphallidae | NJ | Huffman & Fried, 1983; Paseka & Grunberg, 2019 | |
| Philophthalmus megalurus (Looss, 1899) | Digenea: Philophthalmidae | NJ | Huffman & Fried, 1983; Paseka & Grunberg, 2019 | |
| Sphaeridiotrema globulus (Rudolphi, 1819) | Digenea: Psilostomidae | NJ | Huffman & Fried, 1983 | |
| Strigeidae sporocysts | Digenea: Strigeidae | NJ | Paseka & Grunberg, 2019 | |
| Physella (=Physa) acuta (Draparnaud, 1805) | Cotylurus cornutus (Rudolphi, 1809) | Digenea: Strigeidae | MD | Graczyk & Shiff, 1993 |
| Cotylurus sp. | Digenea: Strigeidae | Central and eastern U.S.A. | Zimmermann et al., 2016 | |
| Echinostoma paraensei (Lie & Basch, 1967) | Digenea: Echinostomatidae | NM | Schultz et al., 2020 | |
| Lechriorchis primus (Stafford, 1905) | Digenea: Ochetosomatidae | W | Talbot, 1933 | |
| Notocotylus attenuatus (Rudolphi, 1809) | Digenea: Notocotylidae | MD | Graczyk & Shiff, 1993 | |
| Notocotylus sp. | Digenea: Notocotylidae | Central and eastern U.S.A. | Zimmermann et al., 2016 | |
| Plagiorchis sp. | Digenea: Plagiorchiidae | Central and eastern U.S.A. | Zimmermann et al., 2016 | |
| Posthodiplostomum minimum (MacCallum, 1921) | Digenea: Diplostomatidae | IN; WI | Miller, 1954; Bernot & Lamberti, 2008 | |
| Stichorchis subtriquetrus (Rudolphi, 1814) | Digenea: Echinostomatidae | Albuquerque, NM | Kraus et al., 2014 | |
| Solenorchis travassosi (Hilmy, 1949) | Digenea: Cladorchiidae | Albuquerque, NM | Kraus et al., 2014 | |
| Telorchis sp. | Digenea: Telorchiidae | Central and eastern U.S.A. | Zimmermann et al., 2016 | |
| Trichobilharzia querquedulae (McLeod, 1937) | Digenea: Schistosomatidae | North America | Ebbs et al., 2016 | |
| Vasotrema robustum (Stunkard, 1928) | Digenea: Spirorchiidae | Albuquerque, NM | Kraus et al., 2014 | |
| Vasotrema sp. | Digenea: Spirorchiidae | Central and eastern U.S.A. | Zimmermann et al., 2016 | |
| Planorbella (=Heliosoma) trivolvis (Say, 1817) | Alaria marcianae (La Rue, 1917) | Digenea: Diplostomatidae | MI | Johnson, 1968; Klockars et al., 2007 |
| Allassostomides parvus (=Allassostoma parvum) (Stunkard, 1916) | Digenea: Paramphistomidae | U.S.A. | Klockars et al., 2007 | |
| Alloglossidium corti (Lamont, 1921) | Digenea: Macroderoididae | U.S.A. | Klockars et al., 2007 | |
| A. macrobdellense (=A. macrobdellensis) (Beckerdite & Corkum, 1974) | Digenea: Macroderoididae | U.S.A.; Canada | Klockars et al., 2007 | |
| Bolbophorus confusus (Krause, 1914) | Digenea: Bolbophoridae | MT; WY | Klockars et al., 2007 | |
| B. damnificus (Overstreet et al. 2002) | Digenea: Bolbophoridae | MS; LA | Klockars et al., 2007 | |
| Cephalongonimus americanus (Lang, 1968) | Digenea: Cephalogonimidae | MI | Klockars et al., 2007 | |
| H. brevicirrus (Brooks & Welsh, 1976) | Digenea: Cephalogonimidae | NE | Klockars et al., 2007 | |
| H. salamandrus (Dronen and Lang, 1974) | Digenea: Cephalogonimidae | Eastern WA | Klockars et al., 2007 | |
| H. vesicaudus (Dronen & Underwood, 1977) | Digenea: Cephalogonimidae | TX | Klockars et al., 2007 | |
| Clinostomum attenuatum (Cort, 1913) | Digenea: Clinostomidae | U.S.A. | Klockars et al., 2007 | |
| H. complanatum (Rudolphi, 1814) | Digenea: Clinostomidae | U.S.A. | Klockars et al., 2007 | |
| Cyclocoelum mutabile (Zeder, 1800) | Digenea: Cyclocoelidae | Canada | Klockars et al., 2007 | |
| H. oculeum (Kossack, 1911) | Digenea: Cyclocoelidae | IA | Klockars et al., 2007 | |
| Echinostoma trivolvis (Beaver, 1937) | Digenea: Echinostomatidae | Canada; NJ | Klockars et al., 2007 | |
| Halipegus occidualis (Stafford, 1905) | Digenea: Hemiuridae | PA | Klockars et al., 2007 | |
| Lissorchis fairporti (Magath, 1917) | Digenea: Lissorchiidae | U.S.A. | Klockars et al., 2007 | |
| Macroderoides typicus (Winfield, 1929) | Digenea: Macroderoididae | U.S.A. | Klockars et al., 2007 | |
| Megalodiscus (=Diplodiscus) temperatus (Stafford, 1905) | Digenea: Paramphistomidae | MI | Klockars et al., 2007 | |
| Megalodiscus sp. | Digenea: Paramphistomidae | NY | Klockars et al., 2007 | |
| Ophthalmopagus singularis (Stossich, 1903) | Digenea: Cyclocoelidae | WI | Klockars et al., 2007 | |
| Petasiger nitidus (Linton, 1928) | Digenea: Echinostomatidae | Canada; U.S.A. | Klockars et al., 2007 | |
| Ribeiroia ondatrae (Price, 1931) | Digenea: Psilostomidae | Western U.S.A.; NY; PA | Klockars et al., 2007 | |
| Spirorchis artericola (Ward, 1921) | Digenea: Spirorchiidae | U.S.A. | Klockars et al., 2007 | |
| S. parvus (Stunkard, 1923) | Digenea: Spirorchiidae | U.S.A. | Klockars et al., 2007 | |
| S. scripta (Stunkard, 1923) | Digenea: Spirorchiidae | KY | Klockars et al., 2007 | |
| Typhlocoelum sisowi (Skrjabin, 1913) | Digenea: Cyclocoelidae | U.S.A. | Klockars et al., 2007 | |
| Uvulifer ambiloptus (Lemly & Esch 1984) | Digenea: Diplostomidae | Canada; U.S.A. | Klockars et al., 2007 | |
| Uvitellina (=Cyclocoelum) vanelli (Rudolphi, 1819) | Digenea: Cyclocoelidae | SD | Klockars et al., 2007 | |
| Zygocotyle lunata (Willey, 1941) | Digenea: Paramphistomidae | Canada; NJ | Klockars et al., 2007 | |
| Unidentified Vivax | Digenea: Cyathocotylidae | NJ | Klockars et al., 2007 | |
| Non-indigenous species | ||||
| Heterogen (=Bellamya/Cipangopaludina) japonica (von Martens, 1861) | Aspidogaster conchicola (von Baer, 1827) | Aspidogastrea: Aspidogastridae | MA | Michelson, 1970 |
| Asymphylodora japonica (Yamaguti, 1938) | Digenea: Lissorchiidae | Korea | Lee, 1964 | |
| Azygia gotoi (Ariake, 1922) | Digenea: Azygiidae | Nagano Prefecture, Japan | Shimazu, 2014 | |
| Echinostoma cinetorchis (Ando & Ozaki, 1923) metacercariae | Digenea: Echinostomatidae | Korea | Chung & Jung, 1999 | |
| Echinocasmus macrorchis (Ando & Nazaki, 1923) | Digenea: Echinostomatidae | Xiengkhuang Province, Laos | Sohn et al., 2019 | |
Here, we examined the symbiont diversity of non-indigenous Japanese mystery snails and co-occurring indigenous snails to help understand impacts of invasion on aquatic community ecology. We collected snails from six freshwater populations in Virginia and Washington, D.C. over two years. We dissected snails to determine symbiont diversity. Given the global, common signature of parasite escape detected in non-indigenous populations (e.g., Blakeslee et al., 2013; Keller et al., 2009; Torchin et al., 2003), we predicted that mystery snails would have fewer associates, be parasitised by fewer taxa and have an overall lower prevalence of infection than co-occurring indigenous snails. Aside from trematode parasites, we also noted other symbiont taxa, including ciliates, nematodes, and oligochaetes, in the snails. In addition, we performed a literature review of trematode parasites previously detected in snail species found during the field surveys. Our study represents the first compilation of known symbionts in mystery snails in indigenous and non-indigenous ranges and the first comparison of prevalence and diversity of trematode parasites in mystery snails and co-occurring indigenous snails in North America.
中文翻译：
揭开另一个谜团：日本神秘蜗牛的非土著种群中的寄生虫逃逸和宿主转换在空间上有所不同
1 简介
在全球范围内，淡水生物多样性受到人为因素的威胁（例如，气候变化、水污染、流量改变、栖息地退化；Dudgeon 等人， 2006 年；Reid 等人， 2019 年），非本土物种是造成这些下降（Dudgeon 等人， 2006 年；Parker 等人， 1999 年；Reid 等人， 2019 年）。寄生虫是不可或缺的生态系统成员，与宿主一样，可以通过多种人为机制（即引入载体；Blakeslee 等人， 2013 年；Keller 等人， 2009 年）引入新地点）。虽然我们对入侵生态学的大部分理解都与新生物对本地群落的直接影响有关，但共同引入的寄生虫会对更大的多宿主、多寄生虫群落内的现有关系产生强烈影响（Lymbery 等人， 2014 年； Prenter 等人， 2004 年）。然而，在许多情况下，非本土物种在引入范围内的寄生虫负担得到缓解（Ebbs 等人， 2018 年），因为只有一部分被引入载体中的个体会被寄生（Torchin 等人， 2003 年））。此外，入侵过程本身（受感染的宿主可能死亡或丢失）和寄生虫生命周期要求（有能力的宿主、宿主的夹带生命阶段等）所施加的限制降低了寄生虫成功入侵的可能性；Blakeslee 等人。 , 2020 年）。在某些情况下，寄生虫确实成功地与非本土宿主建立了联系，然后可能会利用新的本土宿主。此外，非本土物种可以作为本土寄生虫的新宿主（即宿主转换），最终可能导致广泛的生态系统变化（Barse & Secor, 1999 ; Font & Tate, 1994 ; Goedknegt et al., 2016 ; Holmes & Minchin， 1995 年；Kelley 等人， 2009a )。这对于直接参与共生的生物体尤其重要，从而产生新的相互作用，可以改变所有各方的本地宿主-本地寄生虫感染动态和种群动态（Lagrue， 2017 年；Tompkins 等人， 2011 年）。然而，我们对寄生在物种入侵中的作用的理解普遍缺乏，特别是在描述共同入侵寄生虫和本地寄生虫的相互作用方面（Poulin, 2017 ; Telfer & Bown, 2012）。拓宽这些知识对于描述入侵对社区内和跨社区的入侵者和共同入侵者的直接和间接影响的影响至关重要（Telfer & Bown， 2012 年）。
本土和非本土宿主之间对寄生虫的感染敏感性不同可以调节入侵（Torchin 等人， 2005 年）。非本土物种中较低的寄生虫负担（即寄生虫逃逸）可能会为非本土宿主提供优于本土物种的优势（Larson & Krist, 2020 ; Torchin et al., 2005）。由于寄生虫可能对宿主的生长、繁殖和竞争力产生负面影响，因此寄生虫损失可能通过增强生物、生态或生理性能（= 寄生虫释放；Blakeslee 等人， 2013 年；Torchin 等人）促进非本土宿主的成功建立 ., 2003）。例如，淡水蜗牛Melanoides tuberculata的非土著种群在马拉维湖中没有寄生虫，导致在土著蜗牛有更多寄生虫的地区产生更多幼体的蜗牛更大（Genner 等人， 2008 年）。此外，寄生虫可以调解本地物种和非本地物种之间的相互作用；例如，当本土片脚类动物Gammarus duebeni celticus被本土微孢子虫寄生时，它们的摄食反应会降低，并且比未感染的非本土片脚类动物更容易被捕食（MacNeil 等人， 2003 年）。
与宿主一样，寄生虫的流行在空间上可能会有所不同（Shaw & Dobson， 1995 年），并且受生物（例如宿主-寄生虫特异性、宿主的分布和丰度、寄生虫之间的种间关系、宿主大小、寄生虫的生命周期阶段）驱动。 ) 和非生物因素（例如，盐度、温度、物理结构、溪流漂移；Hechinger 和 Lafferty， 2005 年；Karvonen 和 Valtonen， 2004 年；Marcogliese 和 Cone， 1991 年；Thieltges 和 Reise， 2007 年）。例如，Blasco-Costa 等人。( 2013) 发现新西兰河流中鱼类吸虫寄生虫流行率存在纵向梯度，下游流行率最高，上游流行率最低。其他研究已将流动淡水系统中寄生虫流行率的空间差异与盐度和富营养化梯度（例如，Blanar 等人， 2011 年）、宿主群落组合（例如，Kelly 等人， 2009b）以及与最终宿主菌落的距离联系起来（例如，Marcogliese 等人， 2001) 等。这种异质性对于维持宿主免受寄生虫侵害的空间避难所至关重要，允许宿主种群茁壮成长，同时将寄生虫种群维持在与这些避难所不同的其他位置；最终促进宿主和寄生虫的稳定种群（Brockhurst 等人， 2006 年；Maynard-Smith， 1974 年；Schrag 和 Mittler， 1996 年）。
一组寄生虫——Digenea 亚纲中的吸虫——已在过去的多项研究中用于探索非本土宿主和寄生虫之间的关系（例如，Blakeslee & Byers, 2008 ; Lively et al., 2004 ; Sorensen & Minchella, 2001） . 大多数吸虫与无脊椎动物和脊椎动物宿主具有复杂的生命周期（Shoop， 1988）。简化的生命周期始于脊椎动物宿主粪便中的卵。摄入的卵孵化成能积极穿透软体动物宿主的毛蚴幼虫。毛蚴在性腺组织中变态，将尾蚴阶段释放到水柱中，感染第二中间宿主并形成囊蚴。受感染的宿主必须被脊椎动物最终宿主消耗。然而，Digenea 的姊妹亚类 Aspidogastrea 中的一些吸虫具有更简单的生命周期，通常使用一个或两个宿主，其中软体动物可以作为中间或最终宿主（Schell， 1985 年）。吸虫通常对软体动物宿主的存活率、繁殖力、生长速度、行为和形态有负面影响，从而影响宿主的竞争能力和种群丰度（Byers & Goldwasser， 2001；Fredensborg 等人， 2005 年；索伦森和明切拉， 2001 年）。
在全球范围内，外来淡水腹足动物通过多种引入媒介入侵生态系统，包括故意引入和意外的人为转移（Padilla & Williams, 2004）。其中一种入侵者是日本神秘蜗牛（Heterogen japonica，同义词Cipangopaludina japonica；Saito 和 Kagawa， 2020 年），在c . 1911 年种植供人类食用 (Clench & Fuller, 1965 ; Prashad, 1928 )，但现在在整个北美的支流中发现 (Jokinen, 1982 ; USGS, 2021）。由于其摄食习性（即滤食器和碎屑动物），Heterogen japonica可以改善入侵淡水系统的整体水质和生产力（Solomon 等人， 2010 年；Van Bocxlaer & Strong， 2016 年）；然而，它也可能对本土蜗牛种群产生负面影响，部分原因是入侵系统中的种群呈指数增长（Johnson 等人， 2009 年；Wolfert & Hiltunen， 1968 年）。寄生可以控制宿主种群的增长，如果宿主种群逃脱了大部分的寄生虫负荷，它可能会减轻巨大的压力（Torchin & Mitchell， 2004 年）。杂粳被其原生范围内的四种去势性双基因物种感染（表 1），而在北美仅记录了来自一个非土著种群 的一种吸虫物种（aspidogastrean Aspidogaster conchicola ）（马萨诸塞州，美国；迈克尔逊， 1970 年）。然而，迄今为止，几乎没有努力在非本土范围内的神秘蜗牛中描述寄生虫感染或更普遍的关联。
| 寄主蜗牛 | 吸虫属或种 | 吸虫类型：家庭 | 地区/州 | 引文 |
|---|---|---|---|---|
| 土著物种 | ||||
| Campeloma decisum (说, 1817) | Amblosoma suwaense (波伊曼斯卡, 1972) | Digenea：Leucochloridiomorphidae | 威斯康星 | 弗里德等人， 1981 |
| Aspidogaster conchicola (von Baer, 1827) | Aspidogastrea：Aspidogastridae | 功放 | 阿尔维斯等人， 2015 | |
| Azygia acuminata (戈德伯格, 1911) | Digenea：Azygiidae | 马萨诸塞州科德角 | 伍顿， 1957 | |
| Leucochloridiomorpha constantiae (Mueller, 1935) | Digenea：Leucochloridiomorphidae | 北美东部；心肌梗死 | 艾莉森， 1943 年；弗里德和布拉德福德， 1984 年；约翰逊， 1992 | |
| Ptyalincola ondatrae (Wootton & Murrell, 1967 ) | Digenea：Leucochloridiomorphidae | 心肌梗死 | 伍顿和穆雷尔，1967 | |
| Sanguinicola occidentalis (van Cleave & Mueller, 1932) | Digenea：Aporocotylidae | 心肌梗死 | 穆扎尔， 2000 | |
| Elimia ( = Pleurocera ) Goionbasis virginica (Gmelin, 1791) | Aspidogaster conchicola (von Baer, 1827) | Aspidogastrea：Aspidogastridae | 新泽西州 | 霍夫曼和弗里德， 1983 |
| 卵磷脂吸虫 | Digenea：Lecithodendriidae | 新泽西州 | 霍夫曼和弗里德， 1983 | |
| Microphalid 孢子囊，普遍型尾蚴 | Digenea：Microphallidae | 新泽西州 | 霍夫曼和弗里德， 1983 年；帕塞卡和格伦伯格， 2019 | |
| Philophthalmus megalurus (卢斯, 1899) | Digenea：Philophthalmidae | 新泽西州 | 霍夫曼和弗里德， 1983 年；帕塞卡和格伦伯格， 2019 | |
| Sphaeridiotrema globulus (鲁道夫, 1819) | Digenea：Psilostomidae | 新泽西州 | 霍夫曼和弗里德， 1983 | |
| Strigeidae孢子囊 | Digenea：Strigeidae | 新泽西州 | 帕塞卡和格伦伯格， 2019 | |
| Physella ( =Physa ) acuta (德拉帕诺, 1805) | Cotyluruscornutus (鲁道夫, 1809) | Digenea：Strigeidae | 医学博士 | Graczyk & Shiff, 1993 |
| Cotylurus sp。 | Digenea：Strigeidae | 美国中部和东部 | 齐默尔曼等人， 2016 | |
| Echinostoma paraensei (Lie & Basch, 1967) | Digenea：棘口虫科 | 纳米 | 舒尔茨等人， 2020 | |
| Lechriorchis primus (斯塔福德, 1905) | Digenea：Ochetosomatidae | W | 塔尔博特， 1933 年 | |
| Notocotylus attenuatus (鲁道夫, 1809) | Digenea： 条子科 | 医学博士 | Graczyk & Shiff, 1993 | |
| 带子菌属 | Digenea： 条子科 | 美国中部和东部 | 齐默尔曼等人， 2016 | |
| Plagiorchis sp。 | Digenea: Plagiorchiidae | 美国中部和东部 | 齐默尔曼等人， 2016 | |
| Posthodiplostomum 最小值(MacCallum, 1921) | Digenea：Diplostomatidae | 在; 威斯康星 | 米勒， 1954 年；伯诺和兰伯蒂， 2008 | |
| Stichorchis subtriquetrus (Rudolphi, 1814) | Digenea：棘口虫科 | 新墨西哥州阿尔伯克基 | 克劳斯等人， 2014 | |
| Solenorchis travassosi (Hilmy, 1949) | Digenea：枝条科 | 新墨西哥州阿尔伯克基 | 克劳斯等人， 2014 | |
| Telorchis sp . | Digenea：Telorchiidae | 美国中部和东部 | 齐默尔曼等人， 2016 | |
| Trichobilharzia querquedulae (麦克劳德, 1937) | Digenea：血吸虫科 | 北美 | 埃布斯等人， 2016 | |
| 粗壮血管(Stunkard, 1928) | Digenea：螺旋体科 | 新墨西哥州阿尔伯克基 | 克劳斯等人， 2014 | |
| 血管痉挛属 | Digenea：螺旋体科 | 美国中部和东部 | 齐默尔曼等人， 2016 | |
| Planorbella ( =Heliosoma ) trivolvis (Say, 1817) | Alaria marcianae (La Rue, 1917) | Digenea：Diplostomatidae | 心肌梗死 | 约翰逊， 1968 年；Klockars 等人， 2007 年 |
| Allassostomides parvus (=Allassostoma parvum) (Stunkard, 1916) | Digenea：Parmphistomidae | 美国 | Klockars 等人， 2007 年 | |
| Alloglossidium corti (拉蒙特, 1921) | Digenea: 巨蜥科 | 美国 | Klockars 等人， 2007 年 | |
| A. macrobdellense (=A. macrobdellensis) (Beckerdite & Corkum, 1974) | Digenea: 巨蜥科 | 美国; 加拿大 | Klockars 等人， 2007 年 | |
| Bolbophorus confusus (克劳斯, 1914) | Digenea: Bolbophoridae | 公吨; 怀俄明 | Klockars 等人， 2007 年 | |
| B.damnificus (Overstreet et al. 2002) | Digenea: Bolbophoridae | 多发性硬化症; 洛杉矶 | Klockars 等人， 2007 年 | |
| 美洲头龙（Lang，1968） | Digenea：头孢亚目科 | 心肌梗死 | Klockars 等人， 2007 年 | |
| H. brevicirrus (Brooks & Welsh, 1976) | Digenea：头孢亚目科 | 网元 | Klockars 等人， 2007 年 | |
| H. salamandrus (Dronen 和 Lang, 1974) | Digenea：头孢亚目科 | 东华盛顿 | Klockars 等人， 2007 年 | |
| H. vesicaudus (Dronen & Underwood, 1977) | Digenea：头孢亚目科 | 德克萨斯州 | Klockars 等人， 2007 年 | |
| Clinostomum attenuatum (Cort, 1913) | Digenea：Clinostomidae | 美国 | Klockars 等人， 2007 年 | |
| H. complanatum (鲁道夫, 1814) | Digenea：Clinostomidae | 美国 | Klockars 等人， 2007 年 | |
| Cycloccoelum mutabile (Zeder, 1800) | Digenea: Cyclocoelidae | 加拿大 | Klockars 等人， 2007 年 | |
| H. oculeum (科萨克, 1911) | Digenea: Cyclocoelidae | IA | Klockars 等人， 2007 年 | |
| 棘口棘蚴(Beaver, 1937) | Digenea：棘口虫科 | 加拿大; 新泽西州 | Klockars 等人， 2007 年 | |
| Halipegus occidualis (斯塔福德, 1905) | Digenea：Hemiuridae | 功放 | Klockars 等人， 2007 年 | |
| Lissorchis fairporti (马加特, 1917) | Digenea：Lissorchiidae | 美国 | Klockars 等人， 2007 年 | |
| 典型大角鱼(Winfield, 1929) | Digenea: 巨蜥科 | 美国 | Klockars 等人， 2007 年 | |
| Megalodiscus (=Diplodiscus) temperatus (Stafford, 1905) | Digenea：Parmphistomidae | 心肌梗死 | Klockars 等人， 2007 年 | |
| Megalodiscus sp。 | Digenea：Parmphistomidae | 纽约 | Klockars 等人， 2007 年 | |
| 奇异眼鳖 (Stossich, 1903) | Digenea: Cyclocoelidae | 威斯康星 | Klockars 等人， 2007 年 | |
| Petasiger nitidus (林顿, 1928) | Digenea：棘口虫科 | 加拿大; 美国 | Klockars 等人， 2007 年 | |
| Ribeiroia ondatrae (价格, 1931) | Digenea：Psilostomidae | 美国西部；纽约；功放 | Klockars 等人， 2007 年 | |
| Spirorchis artericola (沃德, 1921) | Digenea：螺旋体科 | 美国 | Klockars 等人， 2007 年 | |
| S. parvus (Stunkard, 1923) | Digenea：螺旋体科 | 美国 | Klockars 等人， 2007 年 | |
| S. scripta (Stunkard, 1923) | Digenea：螺旋体科 | 肯塔基州 | Klockars 等人， 2007 年 | |
| Typhlocoelum sisowi (Skrjabin, 1913) | Digenea: Cyclocoelidae | 美国 | Klockars 等人， 2007 年 | |
| Uvulifer ambiloptus (Lemly & Esch 1984) | Digenea: Diplosttomidae | 加拿大; 美国 | Klockars 等人， 2007 年 | |
| Uvitellina (= Cyclocoelum ) vanelli (Rudolphi, 1819) | Digenea: Cyclocoelidae | 标清 | Klockars 等人， 2007 年 | |
| Zygocotyle lunata (威利, 1941) | Digenea：Parmphistomidae | 加拿大; 新泽西州 | Klockars 等人， 2007 年 | |
| 身份不明的 Vivax | Digenea: Cyathocotylidae | 新泽西州 | Klockars 等人， 2007 年 | |
| 非本土物种 | ||||
| Heterogen ( =Bellamya/Cipangopaludina ) japonica (von Martens, 1861) | Aspidogaster conchicola (von Baer, 1827) | Aspidogastrea：Aspidogastridae | 嘛 | 迈克尔逊， 1970 |
| Asymphylodora japonica (Yamaguti, 1938) | Digenea：Lissorchiidae | 韩国 | 李， 1964 年 | |
| Azygia gotoi (有明, 1922) | Digenea：Azygiidae | 日本长野县 | 岛津, 2014 | |
| Echinostoma cinetorchis (Ando & Ozaki, 1923) 囊蚴 | Digenea：棘口虫科 | 韩国 | 钟和荣， 1999 | |
| Echinocasmus macrorchis (Ando & Nazaki, 1923) | Digenea：棘口虫科 | 老挝，川圹省 | 孙等人， 2019 | |
在这里，我们检查了非本土日本神秘蜗牛和同时出现的本土蜗牛的共生多样性，以帮助了解入侵对水生群落生态的影响。我们在两年内从弗吉尼亚州和华盛顿特区的六个淡水种群中收集了蜗牛。我们解剖了蜗牛以确定共生体的多样性。鉴于在非土著人群中检测到的全球性、共同的寄生虫逃逸特征（例如，Blakeslee 等人， 2013 年；Keller 等人， 2009 年；Torchin 等人， 2003 年）)，我们预测神秘蜗牛的同伴会更少，被更少的类群寄生，并且总体上比同时出现的本土蜗牛感染率更低。除了吸虫寄生虫，我们还注意到蜗牛中的其他共生类群，包括纤毛虫、线虫和寡毛类。此外，我们对先前在田间调查中发现的蜗牛物种中发现的吸虫寄生虫进行了文献综述。我们的研究首次汇编了土著和非土著范围内神秘蜗牛中已知的共生体，并首次比较了北美神秘蜗牛和同时发生的土著蜗牛中吸虫寄生虫的流行和多样性。
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