Invasive Chinese pond mussel <i>Sinanodonta woodiana</i> threatens native mussel reproduction by inducing cross‐resistance of host fish

Donrovich, Seth W.; Douda, Karel; Plechingerová, Věra; Rylková, Kateřina; Horký, Pavel; Slavík, Ondřej; Liu, Huanzhang; Reichard, Martin; Lopes‐Lima, Manuel; Sousa, Ronaldo

doi:10.1002/aqc.2759

Cited by 52 publications

(41 citation statements)

References 55 publications

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“…Both innate and acquired host immunity was identified by previous studies to be involved in the protection of fish against glochidia of freshwater mussels (Bauer, ; Dodd, Barnhart, Rogers‐Lowery, Fobian, & Dimock, ; Rogers‐Lowery, Dimock, & Kuhn, ), including S. woodiana (Donrovich et al., ). In this study, we were not able to separate the roles of innate and acquired immunity in bitterling fish resistance because we used wild‐caught individuals for which we cannot exclude potential previous contact with glochidia.…”

Section: Discussionmentioning

confidence: 97%

The role of local adaptation in shaping fish‐mussel coevolution

Douda

Liu

et al. 2017

Freshwater Biology

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Abstract1. The survival of affiliate (dependent) species in a changing environment is determined by the interactions between the affiliate species and their available hosts.However, the patterns of spatial and temporal changes in host compatibility are often unknown despite host shifts having direct impact on the persistence of local populations. Bivalves of the order Unionida (freshwater mussels) are a functionally important but declining group of affiliate species, which are dependent on freshwater fish to host their parasitic larvae. The role of local adaptations and host fish resistance in shaping freshwater mussel host relationships remains poorly understood. 2.We used an invasive East Asian unionid bivalve, Sinanodonta woodiana, and its potential host fishes to study the mechanisms shaping fish-mussel coevolution using a combination of laboratory cross-exposure methods and field-collected data. We tested whether generalist host use of S. woodiana is pertinent to native host species, with special attention to bitterling fishes (Cyprinidae: Acheilognathinae) that are characterised by a mutual association with freshwater mussels. We also tested whether the pattern of the parasite-host association varies temporally (between areas of ancient and recent sympatry) and spatially (at a sub-basin level in its native range). 3.Results revealed the ability of S. woodiana to widely exploit non-bitterling host fishes at a global scale. In contrast, the ability of S. woodiana to exploit closely associated bitterling fishes was low in its native range (with ancient sympatry). In areas of recent sympatry (non-native S. woodiana range in Europe), S. woodiana glochidia were demonstrated to readily parasitise local, evolutionarily naive bitterling species at high density. 4.The results of a population-level experiment with three native populations of S. woodiana and rose bitterling, Rhodeus ocellatus, from various sub-basins of the River Yangtze confirmed that mussel populations vary in their compatibility with particular host populations. However, there was no evidence of population-specific adaptive coevolution.5. This study provides the first evidence for a role of fish counter-adaptations against freshwater mussel glochidia, and documents the importance of population-level variation in shaping compatibility between glochidia and their host

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Section: Discussionmentioning

confidence: 97%

The role of local adaptation in shaping fish‐mussel coevolution

Douda

Liu

et al. 2017

Freshwater Biology

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“…Given its generalist exploitation of fish hosts, S. woodiana could potentially decrease the accessibility of fish hosts to native unionid species. Individual fish hosts respond to glochidia parasitism by a partial immunization and cross‐resistance after parasitism by S. woodiana glochidia, which has the effect of decreasing recruitment of native European mussels (Donrovich et al., ). Unionid mussels are also hosts to a group of parasitic cyprinid fishes, the bitterling (Acheilognathinae).…”

Section: Discussionmentioning

confidence: 99%

“…Second, a population in a large Siberian river, the Yenisei, has been discovered recently and is limited to a thermally polluted outlet from a power station (Bespalaya et al, 2017). Third, populations from North America were first recorded in 2010 in New Jersey (Bogan et al, 2011), well after the expansion of S. woodiana in Europe (Lajtner & Crnčan, 2011 parasitism by a partial immunization and cross-resistance after parasitism by S. woodiana glochidia, which has the effect of decreasing recruitment of native European mussels (Donrovich et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Modelling the invasion history of Sinanodonta woodiana in Europe: Tracking the routes of a sedentary aquatic invader with mobile parasitic larvae

Konečný

Popa

Bartáková

et al. 2018

Evolutionary Applications

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Understanding the invasive potential of species outside their native range is one of the most pressing questions in applied evolutionary and ecological research. Admixture of genotypes of invasive species from multiple sources has been implicated in successful invasions, by generating novel genetic combinations that facilitate rapid adaptation to new environments. Alternatively, adaptive evolution on standing genetic variation, exposed by phenotypic plasticity and selected by genetic accommodation, can facilitate invasion success. We investigated the population genetic structure of an Asian freshwater mussel with a parasitic dispersal stage, Sinanodonta woodiana, which has been present in Europe since 1979 but which has expanded rapidly in the last decade. Data from a mitochondrial marker and nuclear microsatellites have suggested that all European populations of S. woodiana originate from the River Yangtze basin in China. Only a single haplotype was detected in Europe, in contrast to substantial mitochondrial diversity in native Asian populations. Analysis of microsatellite markers indicated intensive gene flow and confirmed a lower genetic diversity of European populations compared to those from the Yangtze basin, though that difference was not large. Using an Approximate Bayesian Modelling approach, we identified two areas as the probable source of the spread of S. woodiana in Europe, which matched historical records for its establishment. Their populations originated from a single colonization event. Our data do not support alternative explanations for the rapid recent spread of S. woodiana; recent arrival of a novel (cold‐tolerant) genotype or continuous propagule pressure. Instead, in situ adaptation, facilitated by repeated admixture, appears to drive the ongoing expansion of S. woodiana. We discuss management consequences of our results.

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“…The chance of a successful encystment is smaller in fish that have been previously infected with glochidia, due to adaptive immune response (Bauer, 1987a;Dodd, Barnhart, Rogers-Lowery, Fobian, & Dimock, 2006). Initiation of the adaptive immune response is a natural process but can be problematic if caused by an invasive mussel species such as Chinese pond mussel (Sinanodonta woodiana, Unionidae) (Donrovich et al, 2017). Young fish hosts are generally the most infested, because they are usually numerous and lack a well-developed immune response.…”

Section: Why Are Fish Important For Freshwater Mussels?mentioning

confidence: 99%

Fish and mussels: Importance of fish for freshwater mussel conservation

Ilarri²,

et al. 2017

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Co‐extinctions are increasingly recognized as one of the major processes leading to the global biodiversity crisis, but there is still limited scientific evidence on the magnitude of potential impacts and causal mechanisms responsible for the decline of affiliate (dependent) species. Freshwater mussels (Bivalvia, Unionida), one of the most threatened faunal groups on Earth, need to pass through a parasitic larval (glochidia) phase using fishes as hosts to complete their life cycle. Here, we provide a synthesis of published evidence on the fish–mussel relationship to explore possible patterns in co‐extinction risk and discuss the main threats affecting this interaction. We retrieved 205 publications until December 2015, most of which were performed in North America, completed under laboratory conditions and were aimed at characterizing the life cycle and/or determining the suitable fish hosts for freshwater mussels. Mussel species were reported to infest between one and 53 fish species, with some fish families (e.g., Cyprinidae and Percidae) being used more often as hosts than others. No relationship was found between the breadth of host use and the extinction risk of freshwater mussels. Very few studies focused on threats affecting the fish–mussel relationship, a knowledge gap that may impair the application of future conservation measures. Here, we identify a variety of threats that may negatively affect fish species, document and discuss the concomitant impacts on freshwater mussels, and suggest directions for future studies.

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Invasive Chinese pond mussel Sinanodonta woodiana threatens native mussel reproduction by inducing cross‐resistance of host fish

Cited by 52 publications

References 55 publications

The role of local adaptation in shaping fish‐mussel coevolution

The role of local adaptation in shaping fish‐mussel coevolution

Modelling the invasion history of Sinanodonta woodiana in Europe: Tracking the routes of a sedentary aquatic invader with mobile parasitic larvae

Fish and mussels: Importance of fish for freshwater mussel conservation

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