Identification of a rosette-like agent as Sphaerothecum destruens, a multi-host fish pathogen

A recent threat to European fish diversity was attributed to an infectious pathogen, a rosette-like intracellular parasite carried by invasive cyprinids. Here we show that the emerging rosette-like agent is Sphaerothecum destruens, originally found to be responsible for disease outbreaks in salmon in the United States. Sequencing of the ribosomal internal transcribed spacer (ITS) DNA highlights some level of geographical isolation. Unlike the situation in the United States, its occurrence in invasive fishes presents a risk of spread from wild invasive populations to sympatric populations of susceptible native fish and as such represents a risk for fisheries, as movement of fish for stocking purposes is common practice.     

Invasion of the Hawaiian Islands by a parasite infecting imperiled stream fishes

Points of origin and pathways of spread are often poorly understood for introduced parasites that drive disease emergence in imperiled native species. Co‐introduction of parasites with non‐native hosts is of particular concern in remote areas like the Hawaiian Islands, where the introduced nematode Camallanus cotti has become the most prevalent parasite of at‐risk native stream fishes. In this study, we evaluated the prevailing hypothesis that C. cotti entered the Hawaiian Islands with poeciliid fishes from the Americas, and spread by translocation of poeciliid hosts across the archipelago for mosquito control. We also considered the alternative hypothesis of multiple independent co‐introductions with host fishes originating from Asia. We inferred conduits of introduction and spread of C. cotti across the archipelago from geographic patterns of mtDNA sequence variation and allelic variation across 11 newly developed microsatellite markers. The distribution of haplotypes suggests that C. cotti spread across the archipelago following an initial introduction on O'ahu. Approximate Bayesian Computation modeling and allelic variation also indicate that O'ahu is the most likely location of introduction, from which C. cotti dispersed to Maui followed by spread to the other islands in the archipelago. Evidence of significant genetic structure across islands indicates that contemporary dispersal is limited. Our findings parallel historical records of non‐native poeciliid introductions and suggest that remediating invasion hotspots could reduce the risk of infection in native stream fishes, which illustrates how inferences on parasite co‐introductions can improve conservation efforts by guiding responses to emerging infectious disease in species of concern.     

Do trophic subsidies affect the outcome of introductions of a non‐native freshwater fish?

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Non-native aquatic animals introductions have driven disease emergence in Europe

In this paper it is argued, using examples of disease emergence in aquatic animals in Europe, that the introduction of non-native species drives disease emergence by both extending the geographic range of parasites and pathogens and facilitating host-switching. Enteric red mouth disease and infectious haematopoietic necrosis of salmonids have extended their geographic range from North America to Europe with the import of live fish (Pimephales promelas) and rainbow trout eggs, respectively. Host-switching results in disease emergence when previously unidentified commensal organisms or known pathogen switch to new naïve hosts. The most serious endemic diseases of wild aquatic animals in Europe in recent years can be traced to the introduction of non-native species. Across Europe dramatic populations declines have occurred in native crayfish (e.g. Astacus astacus), oysters (Ostrea edulis) and eels (Anguilla anguilla), all which can be attributed, in varying degrees, to diseases (crayfish plague, Bonamia ostreae and Anguillicoloides crassus, respectively) introduced with non-native species. The severe adverse effects at a population level can be attributed to the lack of immunity in the new hosts. The impact of parasites more recently introduced to Europe, Sphaerothecum destruens (the rosette agent), and Batrachochytrium dendrobatidis, have yet to be fully determined. Both are generalists, with wide host ranges, and may present serious threats to native species. Aquaculture is the key driver for the introduction of non-native species. Most farming systems allow pathogen exchange between farmed and wild populations which underpins host-switching. Subsequently movements of animals between farms may result in the spread of newly emerged diseases. The introduction of non-native aquatic animals drives disease emergence, thus the ex-ante assessment of these hazards is severely limited. Generic risk mitigation measures (e.g. movement of disinfected eggs in place of live animals) and improved methods for rapid detection of new diseases are vital.     

Towards the successful control of the invasive <Emphasis Type="Italic">Pseudorasbora parva</Emphasis> in the UK

The aim of this paper is to detail a control programme of the invasive Asian cyprinid fish Pseudorasbora parva in the UK that was initiated in March 2005. Described as Europe’s most invasive fish, P. parva presents a risk to native fishes through the transmission of a novel pathogen and undesirable impacts arising from processes including increased inter-specific competition. Populations have been recorded in 32 UK waters since their first recording outside of aquaculture in 1996; the majority are lakes <5 ha used for recreational angling in England. The aims of the control programme were to develop a basic evaluation framework that assesses populations by risk (high, medium and low), determine commensurate management actions according to that risk and then execute those actions. For populations assessed as ‘high-risk’, for example those that could result in P. parva dispersal into a river catchment, eradication was determined as the commensurate management action and six operations have since been completed, principally using rotenone, and all have been successful to date. For P. parva populations in sites evaluated as lower risk, techniques such as biomanipulation were determined as more appropriate actions and have been used to successfully reduce their abundance by >99%. To date, the total direct cost of this programme of sustained and on-going P. parva control is approximately ￡190,000.     

Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host

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Laboratory and field validation of a simple method for detecting four species of non‐native freshwater fish using eDNA

This paper presents the first phase in the development and validation of a simple and reliable environmental (e)DNA method using conventional PCR to detect four species of non‐native freshwater fish: pumpkinseed Lepomis gibbosus, sunbleak Leucaspius delineatus, fathead minnow Pimephales promelas and topmouth gudgeon Pseudorasbora parva. The efficacy of the approach was demonstrated in indoor tank (44 l) trials in which all four species were detected within 24 h. Validation was through two field trials, in which L. gibbosus was detected 6–12 h after its introduction into outdoor experimental ponds and P. parva was successfully detected in disused fish rearing ponds where the species was known to exist. Thus, the filtration of small (30 ml) volumes of pond water was sufficient to capture fish eDNA and the approach emphasised the importance of taking multiple water samples of sufficient spatial coverage for detecting species of random or patchy distribution.     

Trophic interactions and consequent impacts of the invasive fish Pseudorasbora parva in a native aquatic foodweb: a field investigation in the UK

Introduction of the invasive Asian cyprinid fish Pseudorasbora parva into a 0.3 ha pond in England with a fish assemblage that included Cyprinus carpio, Rutilus rutilus and Scardinius erythrophthalmus resulted in their establishment of a numerically dominant population in only 2 years; density estimates exceeded 60 ind. m^?2 and they comprised >99% of fish present. Stable isotope analysis (SIA) revealed significant trophic overlap between P. parva, R. rutilus and C. carpio, a shift associated with significantly depressed somatic growth in R. rutilus. Despite these changes, fish community composition remained similar between the ponds. Comparison with SIA values collected from an adjacent pond free of P. parva revealed a simplified food web in P. parva presence, but with an apparent trophic position shift for several fishes, including S. erythrophthalmus which appeared to assimilate energy at a higher trophic level, probably through P. parva consumption. The marked isotopic shifts shown in all taxa in the P. parva invaded pond (¹³C-enriched, ¹⁵N depleted) were indicative of a shift to a cyanobacteria-dominated phytoplankton community. These findings provide an increased understanding of the ecological consequences of the ongoing P. parva invasion of European freshwater ecosystems.     

The distribution of an invasive fish species is highly affected by the presence of native fish species: evidence based on species distribution modelling

Topmouth gudgeon (Pseudorasbora parva) is one of the most invasive aquatic fish species in Europe and causes adverse effects to ecosystem structure and functioning. Knowledge and understanding of the species’ interactions with the environment and with native fish are important to stop and prevent the further spread of the species. Creating species distribution models is a useful technique to determine which factors influence the occurrence and abundance of a species. We applied three different modelling techniques: general additive models, random forests and fuzzy habitat suitability modelling (FHSM) to assess the habitat suitability of topmouth gudgeon. The former two techniques indicated that the abundance of native fish (i.e. biotic variables) was more important than environmental variables when determining the abundance of topmouth gudgeon in Flanders (Belgium). Bitterling (Rhodeus amarus), stone loach (Barbatula barbatula), three-spined stickleback (Gasterosteus aculeatus) and predator abundance were selected as the most important biotic variables and implemented in the FHSM to investigate species interactions. Depending on the preferred food source and spawning behaviour, either coexistence or interspecific competition can occur with bitterling, stone loach and three-spined stickleback. In contrast, the presence of predators clearly had a top down effect on topmouth gudgeon abundance. These findings could be applied as a biological control measure and implemented in conservation strategies in order to reduce the abundance of earlier established populations of topmouth gudgeon.     

Genetic variation of the mtDNA <Emphasis Type="Italic">cyt b</Emphasis> locus in topmouth gudgeon introduced into water bodies in the northern part of the Black Sea region

The up-to-date phylogeographical distribution of the topmouth gudgeon Pseudorasbora parva Temminck et Schlegel 1846 in water bodies of the Northern Black Sea region is considered. Genetic variation of mtDNA cyt b gene is analyzed. It is established that topmouth gudgeon penetrated and spread in the basins of the Dnieper and Don rivers and in water bodies of Crimea from the secondary center of its dispersion— water bodies of Central Europe. It is demonstrated that haplotypes of topmouth gudgeon in the Danube delta are the most homologous to the haplotypes in the native range of the species in China. A considerable decrease in the level of genetic variation in the populations in the Black Sea region is reported.     

Slipping through the Cracks: The Taxonomic Impediment Conceals the Origin and Dispersal of Haminoea japonica,an Invasive Species with Impacts to Human Health

Haminoea japonica is a species of opisthobranch sea slug native to Japan and Korea. Non-native populations have spread unnoticed for decades due to difficulties in the taxonomy of Haminoea species. Haminoea japonica is associated with a schistosome parasite in San Francisco Bay, thus further spread could have consequence to human health and economies. Anecdotal evidence suggests that H. japonica has displaced native species of Haminoea in North America and Europe, becoming locally dominant in estuaries and coastal lagoons. In this paper we study the population genetics of native and non-native populations of H. japonica based on mt-DNA data including newly discovered populations in Italy and France. The conclusions of this study further corroborate a Northeastern Japan origin for the non-native populations and suggest possible independent introductions into North America and Europe. Additionally, the data obtained revealed possible secondary introductions within Japan. Although non-native populations have experienced severe genetic bottlenecks they have colonized different regions with a broad range of water temperatures and other environmental conditions. The environmental tolerance of this species, along with its ability to become dominant in invaded areas and its association with a schistosome parasite, suggest H. japonica could be a dangerous invasive species.     

Piscivorous fishes diet dominated by the Asian cyprinid invader,topmouth gudgeon (<Emphasis Type="Italic">Pseudorasbora parva</Emphasis>)

Predation on the non-native cyprinid, Pseudorasbora parva, was reported during an annual study in a small connecting canal about 40 km south of Brno, Czech Republic. Two cyprinid fish species (Pseudorasbora parva, Rutilus rutilus) were identified in the diet of 23 piscivores belonging to three native fishes (Perca fluviatilis, Sander lucioperca, Esox lucius). The relative abundance of prey fishes changed seasonally and was dominated by the topmouth gudgeon in spring. Thereafter roach incidence continuously increased. In contrast, topmouth gudgeon was found to be a more sized-available prey and was the most dominant prey species in the diet of all piscivorous fishes during the whole season. Strong piscivory towards this alien might be beneficial for its eradication or control to support ecological integrity in natural and modified seminatural habitats.     

Reconciling the biogeography of an invader through recent and historic genetic patterns: the case of topmouth gudgeon <Emphasis Type="Italic">Pseudorasbora parva</Emphasis>

The genetic variability and population structure of introduced species in their native range are potentially important determinants of their invasion success, yet data on native populations are often poorly represented in relevant studies. Consequently, to determine the contribution of genetic structuring in the native range of topmouth gudgeon Pseudorasbora parva to their high invasion success in Europe, we used a dataset comprising of 19 native and 11 non-native populations. A total of 666 samples were analysed at 9 polymorphic microsatellite loci and sequenced for 597 bp of mitochondrial DNA. The analysis revealed three distinct lineages in the native range, of which two haplogroups were prevalent in China (100%), with a general split around the Qinling Mountains. Dating of both haplogroups closely matched past geological events. More recently, its distribution has been influenced by fish movements in aquaculture, resulting in gene flow between previously separated populations in Northern and Southern China. Their phylogeography in Europe indicate as few as two introductions events and two dispersal routes. Microsatellite data revealed native populations had higher genetic diversity than those in the invasive range, a contrast to previous studies on P. parva. This study confirms the importance of extensive sampling in both the native and non-native range of invasive species in evaluating the influence of genetic variability on invasion success.     

Isolation and characterization of polymorphic microsatellite DNA markers in topmouth gudgeon,Pseudorasbora (Teleostei: Cyprinidae)

Due to accidental introductions, the distribution of the east Asian topmouth gudgeon, Pseudorasbora parva, has rapidly expanded over recent years, thereby threatening the endangered Japanese species, P. pumila pumila. Sixteen microsatellite loci were isolated and characterized for P. parva, 14 being highly polymorphic (mean H_E = 0.58, mean number of alleles = 4.4). Successful characterization of 10 of these loci was also achieved for P. pumila pumila. These markers should be useful in future investigation of colonization of P. parva and the development of conservation strategies for P. pumila pumila.     

Length–weight and length–length relationships for nine fish species from Lhasa River Basin,Tibet, China

The present study reports length–weight relationships (LWR) and length–length relationships (LLR) for five native freshwater fish species (Schizopygopsis younghusbandi, Triplophysa orientalis, T. tibetana, T. stewartii and T. stenura) and four introduced freshwater fish species (Pseudorasbora parva, Carassius auratus, Micropercops cinctus and Oryzias latipes) captured in the Lhasa River Basin, Tibet, China. Five of the LWRs are presented for the first time.     

Infection Status of Freshwater Fish with Metacercariae of Clonorchis sinensis in Korea

This study investigated freshwater fish for their current infection status with metacercariae of Clonorchis sinensis in Korea. Twenty-one species of freshwater fish (n = 677) were collected from 34 regions nationwidely from February 2007 to June 2008. They were individually examined by digestion technique. Eight species of freshwater fish from 17 different regions were recognized positive for the metacercariae of C. sinensis. The positive rates (range of metacercariae number per fish) of fish by the species were as follows: 48% (1-1,142) in Pseudorasbora parva, 60% (1-412) in Pungtungia herzi, 15.7% (1-23) in Pseudogobio esocinus, 29% (1-7) in Acheilognathus intermedia, 21% (1-4) in Odontobutis interrupta, 33% (1-6) in Zacco temmincki, 3.6% (1-4) in Zacco platypus, and 26.3% (1) in Hemibarbus labeo. The two species, P. parva and P. herzi, are able to be the index fish for estimation of C. sinensis transmission in a certain locality. Still several species of freshwater fish are briskly transmitting C. sinensis infection in many riverside areas of southern Korea.     

A risk assessment for managing non-native parasites

The spread of non-native parasites with the movement of animals is a primary cause of disease emergence worldwide. Such introductions can threaten native biodiversity, hinder conservation efforts and limit the socio-economic development of natural resources. Evaluating the threats from alien parasites can represent a considerable challenge, due to the limited information that often accompanies their introduction. We present a comprehensive modular risk assessment scheme that supports the management of non-native fish parasites in their pre- and post-introduction phases. This scheme addresses some of the shortcomings of current risk analysis, including the risk management of non-notifiable pathogens and impact assessment of parasites following establishment. An initial procedure for hazard identification promotes a rapid assessment of disease risk and prompt imposition of management measures. This is followed by a longer-term assessment of impact that accommodates available and emerging knowledge on the pathogen and its distribution. Consideration is given to ecological and economic consequences of disease at the host, population and fishery levels. Each module provides an easily interpreted output that underpins management responses, ranging from monitoring parasite distribution to their attempted eradication. A final module ensures clear communication of disease risk to relevant stakeholders, using the other modules as a framework. Outputs of this risk assessment will inform the prioritisation of available resources and provides a scientifically robust foundation on which to base practical and proportionate management measures to protect native environments. The scheme presented here was specifically developed for freshwater fisheries in England and Wales, but may be modified for use globally and for the non-native parasite fauna of other taxa.     

Overlapping niches between two co-occurring invasive fish: the topmouth gudgeon Pseudorasbora parva and the common bleak Alburnus alburnus

Invasive fish species impact aquatic ecosystems and modify native communities, often leading to a decline in local species. These ecological impacts include the transmission of pathogens, predation, competition as well as hybridization. Two invasive fish species, the common bleak Alburnus alburnus and the topmouth gudgeon Pseudorabora parva, have both been recently found co-occurring in several regions of southern Europe, such as the Italian Arno River. Nonetheless, the trophic relationships among invasive fish species, especially cyprinids, remain poorly understood, and no studies have reported the trophic interaction between these two species. This study compared length–weight relationship and used stomach content and stable isotope analysis of two co-occurring populations in the Arno River to characterize the growth and overlap of potential trophic niches. It also found similar allometric growth in both species, a wider generalist trophic niche for P. parva and a more specialized niche for A. alburnus. A considerable niche overlap was found, suggesting that feeding competition can occur if resources were to be limited. Moreover, the niche of P. parva was more likely to overlap with that of A. alburnus than vice versa, suggesting that P. parva can be considered as a potential over competitor. Nonetheless, the authors found in the overlapping populations no evidence of realized competition, probably avoided through a combination of fine-scale mechanisms. They also highlighted that these two invasive species can co-exist and share resources, at least in an open ecosystem like a river, thus potentially doubling up their trophic impact on local communities.     

Movement and assemblage of fish in an artificial wetland and canal in a paddy fields area,in eastern Japan

This study, carried out in a paddy fields area in eastern Japan, investigated the timing and patterns of fish movement and assemblage in an artificial wetland and canal. The number of Misgurnus anguillicaudatus and Lefua echigonia immigrating and emigrating between the wetland and the canal accounted for 80–90 % of all the sampled fish. M. anguillicaudatus, L. echigonia, Pseudorasbora parva and Rhynchocypris lagowskii were dominant in the wetland. Immigration of mature M. anguillicaudatus and L. echigonia was detected between late winter and spring. The standard length of the two loach species in the wetland was smaller than that in the canal. These results confirm that wetlands play a role in spawning and nursery for the two species of loaches. The standard length of P. parva in the wetland was smaller than in the canal. This suggests that the wetland was a more suitable spawning and nursery area for this fish species than the canal. L. echigonia used the wetland as a spawning and nursery area, but previous studies reported that the loach did not use paddy fields near the wetland. This could be because the paddy fields were irrigated between June and September and this period did not largely overlap with the fish spawning season. Therefore, we conclude that the conservation and restoration of wetlands, where water is present throughout the year, will contribute toward the preservation of the fish population in a paddy fields area.     

Identifying conservation priority ponds of an endangered minnow, <Emphasis Type="Italic">Pseudorasbora pumila</Emphasis>, in the area invaded by <Emphasis Type="Italic">Pseudorasbora parva</Emphasis>

We investigated the occurrence pattern of the pond-living endangered cyprinid, Pseudorasbora pumila, and also compared its habitat characteristics with those of the congeneric invasive species, Pseudorasbora parva, in the contact zone. Comparison of 16 environmental variables among the P. pumila habitats, P. parva habitats, and unoccupied ponds revealed that conductivity was a common limitation factor of distribution of both species. We found that emergent vegetation occupancy along the pond bank was the most important factor determining P. pumila occurrence and that ponds with steep banks may have a low probability of containing P. parva. We constructed a logistic regression model to predict the establishment risk of P. parva in ponds occupied by P. pumila. The model demonstrated that more than half of the ponds exhibited a high establishment risk of P. parva. Principal component analysis using six parameters selected from stepwise logistic regression analysis revealed that seven unoccupied ponds had the potential to sustain P. pumila, suggesting that our study site is capable of supporting more P. pumila populations and expanding the current range.