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Wednesday, 2 December 2020

Misgurnus bipartitus: An invasive Weatherfish found in Austria.

Throughout the world, there is an increasing number of alien species, sometimes with negative effects on indigenous taxa. This is also true for Weatherfish of the family Cobitidae. Eschmeyer’s Catalogue of Fishes lists seven species of Misgurnus and one species of Paramisgurnus, mostly known from East Asia. Misgurnus fossilis is the only Weatherfish native to Europe. It is a species of special national and European conservation concern and mainly threatened by the loss of suitable habitats. Negative impacts on European Weatherfish populations may further arise by the spread of allochthonous Weatherfish due to potential interspecific competition, but also by potential hybridisation. Hybridisation has been documented in natural populations of Paramisgurnus dabryanus and Misgurnus anguillicaudatus. Hence, identifying potentially invasive alien Weatherfish and taking actions against their further spread might be crucial to the long-term survival of the indigenous species.

Weatherfish were initially farmed for the food industry in Asia. Subsequently the aquarium trade of ornamental pond Fish has fueled their global spread and concordantly reports of alien Weatherfish have been ever increasing. Today, populations of Asian Weatherfish are known from Australia, North America, South America and Asia outside of their natural range. From Europe, Misgurnus anguillicaudatus, the Oriental Weatherfish has been reported from Italy, Spain, Germany, and the Netherlands. Furthermore, two studies in the last decade have confirmed Paramisgurnus dabryanus, from Switzerland and Germany, respectively.

In a paper published in the journal BioInvasions Records on 30 March 2020, Lukas Zangl of the Institute of Biology at the University of Graz, and the Studienzentrum Naturkunde at the Universalmuseum Joanneum, Michael Jung of the Eberstaller Zauner Büros, Wolfgang Gessl and Stephan Koblmüller, also of the Institute of Biology at the University of Graz, and Clemens Ratschan, also of the Eberstaller Zauner Büros, report the first record of an alien Misgurnus species in Austria.

Based on morphology, DNA barcodes (part of the mitochondrial cytochrome oxidase subunit 1 gene) and sequences of the nuclear recombination activating gene 1 Zangl et al. have to identified the Fish to the species level and relate it to recent findings of alien Weatherfish species in Germany. Furthermore, they discuss difficulties in the correct species identification of alien Weatherfish species, even when DNA sequence data are available, as systematics and taxonomy, especially of the genera Misgurnus and Paramisgurnus, are still not fully resolved.

On 18 October 2018 two strange Cobitid individuals (both with a total length of 125 mm) were caught in the central area of the impoundment of the Egglfing-Obernberg power plant in Upper Austria, at the River Inn during an electrofishing survey. Specimens from the river Inn were determined morphologically, sampled, fixed in formalin and deposited at the Biologiezentrum Linz

 
(A), (B) Pictures of the two Misgurnus bipartitus caught in the Inn impoundment lake close to the German border. (C) Bird’s eye view picture of the impoundment lake at the Egglfing-Obernberg power plant and a map of Central Europe showing the sampling site close to the German border. Zangl et al. (2020).

Based on characters given in the a by Russuiab ichthyologist Ekaterina Vasil'eva (caudal peduncle depth 2.4–2.5 times in caudal peduncle length vs. 1.3–1.8 times in Misgurnus anguillicaudatus, maximum body depth 8.2–8.6 times in standard length vs. less than 7.5 times in Misgurnus anguillicaudatus) Zangl et al.'s specimens from the Inn were identified as Misgurnus bipartitus. Phylogenetic analysis of 612 base pairs of the mitochondrial cytochrome oxidase subunit 1 gene also grouped the alien Austrian Misgurnus with Misgurnus bipartitus. Interestingly, the Austrian Fish and Misgurnus bipartitus share their haplotype with German Fish previously identified as Misgurnus anguillicaudatus (KX865082, KX865083, KX865084) collected 145 km further upstream in an oxbow of the Inn in Germany. Consistent with previous studies, the genus Misgurnus was found to be paraphyletic. Phylogenetic relationships based on 658 base pairs of the nuclear recombination activating gene 1 mirrored the results of the mitochondrial cytochrome oxidase subunit 1 gene data, although node support was generally lower in the nuclear trees. In the recombination activating gene 1 tree, the Austrian Fish grouped with a Misgurnus sp. 2 from Korea and a single Misgurnu mohoity from Russia. All other Misgurnu mohoity from their native range form a distinct clade, sister to that including the Austrian samples, albeit with limited bootstrap support. It is noteworthy though, that no ecombination activating gene 1 sequences of alleged Misgurnus bipartitus were available to be included in Zangl et al.'s analysis. The maximum intraspecific genetic distance, based on uncorrected p-distances of the cytochrome oxidase subunit 1 gene, varied from 0% within Misgurnus bipartitus to 3.6% within Misgurnu mohoity. The minimum interspecific distance was 9% between Misgurnus anguillicaudatus and Misgurnus bipartitus.

 
Maximum Likelihood phylograms based on 612 base pairs of the mitochondrial cytochrome oxidase subunit 1 gene. Node labels indicate bootstrap support values (1000 bootstrap replicates; only values greater than 85 are shown). Samples in bold were obtained and sequenced in this study. Numbers in parentheses represent GenBank accession numbers. Zangl et al. (2020).

Zangl et al. present the first record of an alien Misgurnus species for Austria. Phylogenetic analysis of the mitochondrial cytochrome oxidase subunit 1 gene clearly clustered the two specimens caught in the Inn impoundment with other previously published cytochrome oxidase subunit 1 sequences of Misgurnus bipartitus. This particular clade also contains three sequences of specimens likely misidentified as Misgurnus anguillicaudatus from further upstream the Inn in Germany, which share the exact same haplotype with the Austrian samples and all Misgurnus bipartitus included in our dataset. In theory, ancient hybridisation could explain this finding, as hybridisation is known to occur between Misgurnus species as well as between Misgurnus and Paramisgurnus. On the other hand, the study which genetically identified the German specimens did not include any sequence of Misgurnu mohoity and Misgurnus bipartitus. Unfortunately, the systematic background of the genera Misgurnus and Paramisgurnus is still not fully resolved. Anabel Perdices, Victor Vasil’ev , and Ekaterina Vasil'eva, for example, suggested synonymy of Misgurnus bipartitus and Misgurnu mohoity based on DNA sequence data of the mitochondrial cytochrome b and the nuclear recombination activating gene 1 genes, a view concordant with Ekaterina Vasil'eva morphological study. However, other studies have granted species level to Misgurnus bipartitus as well, based on clear divergence in DNA sequence data of the mitochondrial cytochrome oxidase subunit 1 gene and morphology. Zangl et al. follow these studies and treat Misgurnus bipartitus as a valid and distinct species. Thus, based on our data we strongly argue that the three specimens found in the German stretches of the Inn river and the two specimens found on the Austrian side do belong to Misgurnus bipartitus, the northern Weatherfish and so might several other findings of alien Loaches in Germany determined as Misgurnus anguillicaudatus down to 46 km upstream of the recent finding, be as well. These findings are also corroborated by nuclear recombination activating gene 1 data, which group the Austrian samples not with Misgurnus anguillicaudatus, but with a distinct lineage within M. mohoity (but note, no recombination activating gene 1 data are available for morphologically identified Misgurnu mohoity).

 
Maximum Likelihood phylograms based on 658 base pairs of the nuclear recombination activating gene 1. Node labels indicate bootstrap support values (1000 bootstrap replicates; only values greater than 85 are shown). Samples in bold were obtained and sequenced in this study. Numbers in parentheses represent GenBank accession numbers. Zangl et al. (2020).

The close genetic relationship of German and Austrian alien Misgurnus from the Inn, however, further indicates a downstream range expansion of at least 145 km, which is also supported by several more recent catches of alien Misgurnus along the German stretch of the Inn downstream the site of first record. Thus, alien Misgurnus seem to use the main stem of the Alpine river Inn with low water temperatures and high turbidity at least as a dispersal corridor. Systematic uncertainties as well as scarce available ecological data on these species further complicate the prediction of the invasive potential, prime habitats and possible conflicts with native biota.

Despite the above-mentioned challenges, Zangl et al. agree that DNA barcoding, and even more so eDNA metabarcoding or the application of diagnostic primers for detecting alien species in eDNA samples helps to detect and identify non-native Misgurnus/Paramisgurnus species, which might be a threat to the autochthonous Misgurnus species. Confronted with a new alien species, facing potential interspecific competition and/or genetic dilution through hybridisation, protection and conservation of Misgurnus fossilis should be enforced. Furthermore, appropriate regulations on the trade of ornamental Fish should be considered in order to reduce the risk of unintentional spread of alien species that could become invasive and threaten the native biodiversity.

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