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Arrived to the USA Via 1 Invasive Fish Misgurnus Anguillicaudat

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Arrived to the USA Via 1 Invasive Fish Misgurnus Anguillicaudat Manuscript Click here to access/download;Manuscript;Reyda et al after 2nd review.pdf Click here to view linked References 1 Global parasite trafficking: Asian Gyrodactylus (Monogenea) arrived to the U.S.A. via 1 2 2 invasive fish Misgurnus anguillicaudatus as a threat to amphibians 3 4 5 3 6 7 4 Florian B. Reyda 1 8 9 10 11 5 [email protected] 12 13 14 6 Scott M. Wells 2 15 16 17 18 7 Alexey V. Ermolenko 3 19 20 21 8 Marek S. Ziętara 4 22 23 24 25 9 Jaakko I. Lumme 5 26 27 2810 1. Biology Department and Biological Field Station, State University of New York at 29 30 3111 Oneonta, College at Oneonta, Oneonta, NY, U.S.A.; 32 3312 2. New York State State Department of Environmental Conservation, Region 4 Bureau of 34 3513 Fisheries Stamford, NY, U.S.A.; 36 37 3814 3. Institute of Biology and Soil Science 159, Prospekt Stoletiya, 690022 Vladivostok, Russia; 39 4015 4. Department of Molecular Evolution, Faculty of Biology, University of Gdańsk, Wita 41 42 4316 Stwosza St., 59, PL-80-308 Gdańsk, Poland; 44 4517 5. Ecology and Genetics , University of Oulu, Oulu, Finland. 46 47 4818 Short title: Intercontinental transfer of parasites by invasive fish 49 50 5119 Running head/short title: Parasite transfer by invasive fish 52 53 5420 Keywords: Intercontinental parasite dispersal, molecular systematics, aquatic invasive species, 55 5621 chytrid fungus. 57 5822 59 60 61 62 63 64 1 65 23 Abstract 1 224 A monogenean flatworm Gyrodactylus jennyae Paetow, Cone, Huyse, McLaughlin & 3 4 525 Marcogliese, 2009 was previously described as a pathogen on bullfrog Lithobates 6 726 catesbeianus Shaw, 1802, in a Canadian captive population originating in Missouri, U.S.A. 8 9 1027 The ITS barcoding of G. jennyae showed relatedness to Asian Gyrodactylus macracanthus 11 1228 Hukuda 1940, a parasite of the Asian loach Misgurnus anguillicaudatus Cantor, 1842. The 13 1429 resulting suggestion that the globally invasive pet-trade of fish may be a mechanism for 15 16 1730 arrival of Gyrodactylus species to North America provided the framework for the current 18 1931 study. The present study was undertaken following the discovery of two other species of 20 21 2232 Gyrodactylus in a population of illegally introduced M. anguillicaudatus in New York State. 23 2433 Here the invasion hypothesis was tested via DNA sequencing of the ITS of the two 25 26 2734 Gyrodactylus species obtained from M. anguillicaudatus from New York, termed 28 2935 Gyrodactylus sp. A and Gyrodactylus sp. B. Both Gyrodactylus sp. A and Gyrodactylus sp. B 30 3136 were closely related to G. jennyae and G. macracanthus, and all belong to a molecularly well- 32 33 3437 supported monophyletic Asian freshwater group. In conclusion, this invasive fish has 35 3638 trafficked at least three parasite species to the U.S.A., one of them also found on frog. This 37 38 3939 route from the Asian wetlands to other continents is similar to that of amphibian chytrid fungi 40 4140 of genus Batrachochytrium Longcore, Pessier & Nichols, 1999. 42 43 4441 45 4642 Keywords 47 48 4943 Intercontinental parasite dispersal 50 5144 Molecular systematics 52 5345 Aquatic invasive species 54 55 5646 Chytrid fungus 57 5847 59 60 61 62 63 64 2 65 48 Introduction 1 2 349 Introduced and invasive species are increasingly recognized as a threat to local ecosystems. 4 550 The interactions of the invaders and the native populations are often simplified as resource 6 7 851 competition of the organisms at the same trophic level. Perhaps biological invasions are more 9 1052 complicated, and the harmful effects caused by new intruders surpass simple competition. 11 1253 Introduced organisms may shed their native parasites and diseases and gain a competitive 13 14 1554 advantage (Enemy release hypothesis, Torchin et al. 2003) in new ecosystems. The invaders 16 1755 may also introduce diseases which are new to the target ecosystem, and therefore harm the 18 19 2056 native populations of interacting species (Verneau et al. 2011). Disturbed ecosystems may in 21 2257 turn spread pathogens to humans and livestock and increase the number of zoonoses (EIDs or 23 24 2558 emerging infectious diseases; Daszak et al. 2000). One drastic example of harmful invasion in 26 2759 line with the focus of this paper was the transport of Baltic strains of Atlantic salmon (Salmo 28 2960 salar L.) to Norway. With clinically healthy (tolerant) Baltic fish, the monogenean flatworm 30 31 3261 parasite Gyrodactylus salaris Malmberg, 1957 arrived in Norway in 1975 and destroyed 45 33 3462 Atlantic salmon river populations in just a few decades (Johnsen and Jensen 1991; Bakke et 35 36 3763 al. 2002, 2007). In contrast, the long-isolated Baltic salmon (Lumme et al. 2015) is tolerant 38 3964 and co-adapted with G. salaris, so that the spatially and genetically differentiated host- 40 41 4265 parasite combinations remain stable despite the physical mobility (Lumme et al. 2016a). The 43 4466 parasite introduced to the susceptible Atlantic salmon populations spread rapidly, with fatal 45 46 4767 consequences. 48 4968 Gurevitch and Padilla (2004) asked whether species invasions are a major cause of 50 5169 extinctions, and claimed that data supporting this widely-accepted view often are anecdotal, 52 53 5470 speculative, and based on limited observation. A problem common with such observations 55 5671 about "change" is that many global changes occur in the same time axis and are temporally 57 58 5972 associated. This leads to skepticism against invoking explanations of "change". Pimentel et al. 60 61 62 63 64 3 65 73 (2005) estimated that there are 50,000 foreign plant or animal species in the United States 1 274 alone, and that 42% of endemic species are endangered or threatened because of aliens. The 3 4 575 authors concluded that the total economic damages and losses caused by invasive species add 6 776 up to an estimated $120 billion per year in the U.S.A. alone. 8 9 1077 This study maps a complex case of an introduced and rapidly spreading Asian fish in 11 1278 North America, accompanied by East Asian parasites. The starting point of this narrative was 13 1479 as follows. A monogenean flatworm species Gyrodactylus jennyae Paetow, Cone, Huyse, 15 16 1780 McLaughlin and Marcogliese 2009 was described as a new pathogenic parasite on the 18 1981 American bullfrog Lithobates catesbeianus Shaw, 1802 in North America. The bullfrog itself 20 21 2282 is widely trafficked (Mata-López et al. 2010). Paetow et al. (2013) also demonstrated that G. 23 2483 jennyae infection increased the mortality of the tadpoles associated with fungal disease 25 26 2784 Batrachochytrium dendrobatidis Longcore, Pessier & Nichols, 1999, making matters worse. 28 2985 This fungal disease is considered one of the main reasons for the contemporary decline of 30 3186 global amphibian populations (Collins and Crump 2009). The question was raised about the 32 33 3487 origin of this newly described Gyrodactylus species, which are monogenean ectoparasites of 35 3688 fish, seldom found on amphibians. Records on amphibians were reviewed in Paetow et al. 37 38 3989 2009. 40 4190 Fortunately, the formal description of G. jennyae was accompanied with the DNA 42 43 4491 sequence of complete ribosomal Internal Transcribed Spacer segments (ITS1-5.8S rDNA– 45 4692 ITS2), hereafter ITS. This fragment of DNA is the most popular in Gyrodactylus studies (e.g., 47 48 4993 Paetow et al. 2009), and consequently the most useful DNA segment for “barcoding” in the 50 5194 genus (Mendoza-Palmero et al., 2019). The parasites of genus Gyrodactylus are very small 52 5395 (<0.5 mm), living on the surface or gills of the fish, and most often clinically more or less 54 55 5696 asymptomatic. In fact, they are seldom detected without targeted search. Emphasis of research 57 5897 has been on fish farms, especially those of salmonids (Paladini 2012). A minimum number of 59 60 61 62 63 64 4 65 98 Gyrodactylus species diversity has been estimated at 20,000 (Bakke et al. 2002), with some 1 299 417 formally described (Harris et al. 2004), and only 200 barcoded by ITS. 3 4 1005 Paetow et al. (2009) conducted a BLAST search of G. jennyae among the published 6 1017 ITS sequences of Gyrodactylus spp., and confirmed closest matches of ITS1 and ITS2 8 9 10102 segments to species of the nominal subgenus G. (Gyrodactylus) which are mainly Eurasian 11 12103 parasites on cyprinids. The genetic distance of G. jennyae to G. neili LeBlanc, Hansen, Burt 13 14 104 & Cone 2006, a North American member of the subgenus G. (Gyrodactylus) is dK2P = 0.320. 15 16 17105 However, in a small unpublished collection of ITS sequences from Far East Asia maintained 18 19 106 by the authors, a much closer match dK2P = 0.085 was found between G. jennyae and G. 20 21 22107 macracanthus Hukuda, 1940, described in the Han River system, Korea. G. macracanthus is a 23 24108 parasite of the Asian pond loach (Misgurnus anguillicaudatus Cantor, 1842). 25 26 27109 Because M. anguillicaudatus is an invasive freshwater species trafficked by the 28 29110 aquarium pet trade (Chang et al. 2009) with established non-native populations in Australia, 30 31111 North and South America, and Europe (Belle et al. 2017 and references therein), we 32 33 34112 hypothesized that it might be a mechanism for transport of East Asian parasites to North 35 36113 America. A focused search was conducted in New York State (Wells 2014). 37 38 39114 40 41115 Methods 42 43 44116 The Far East and U.S.A.
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