Abstract
Invasive species prevention involves avoiding two aspects: introduction and secondary spread. The latter is essential in places that can become hubs for spreading invasive species. Lake Biwa, the largest lake in Japan, is an important area for biodiversity and fisheries. However, several invasive fish and crustaceans were established in the lake last century. One of the conservation problems in the Lake Biwa region is the unresolved suspicion that the native freshwater shrimp Neocaridina denticulata have been replaced with alien Neocaridina species. To verify whether exotic species have replaced the native Neocaridina population in this region, we estimated the population structure of Neocaridina spp., collected from 19 sites in and around Lake Biwa, based on genome-wide SNPs and mitochondrial DNA. The three detected genetic clusters were characterized by quantitative analysis of multiple morphological traits. Two clusters were identified as non-native N. davidi and the other as native N. denticulata. However, species discrimination based solely on morphological analysis was difficult, highlighting the importance of genetic analysis. We rediscovered the native populations in the region for the first time in a century; however, in 11 sites, the invasive species were dominant. These findings suggest that the native populations are in a critical situation. Furthermore, fishery resource stocking throughout Japan from Lake Biwa can cause the secondary spread of the invasive shrimps from the lake, acting as a hub, to other parts of the country.
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References
Aino S, Yodo T, Yoshioka M (2015) Changes in the composition of stock origin and standard length of ayu Plecoglossus altivelis altivelis during the Tomozuri angling season in the Nagara River, central Japan. Fish Sci 81:37–42. https://doi.org/10.1007/s12562-014-0822-y
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. https://doi.org/10.1101/gr.094052.109
Anisimova M, Gil M, Dufayard J-F, Dessimoz C, Gascuel O (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 60:685–699. https://doi.org/10.1093/sysbio/syr041
Annandale N (1922) The macroscopic fauna of Lake Biwa. Annot Zool Jap 10:127–153
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bouvier EL (1904) Crevettes de la famille des Atyidés: espèces qui font partie des collections du Muséum d’Histoire Naturelle. Bull Mus Nat Hist Nat 10:129–138 ([In French])
Cai Y (1996) A revision of the genus Neocaridina (Crustacea: Decapoda: Atyidae). Acta Zootaxonomica Sin 21:129–160
Cai Y, Shokita S (2006) Atyid shrimps (Crustacea: Decapoda: Caridea) of the Ryukyu Islands, southern Japan, with descriptions of two new species. J Nat Hist 40:2123–2172. https://doi.org/10.1080/00222930601084049
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Chen Q-H, Chen W-J, Zheng X-Z, Guo Z-L (2020) Two freshwater shrimp species of the genus caridina (decapoda, caridea, atyidae) from Dawanshan Island, Guangdong, China, with the description of a new species. Zookeys 923:15–32. https://doi.org/10.3897/zookeys.923.48593
Dlugosch KM, Alice Cang F, Barker BS, Andonian K, Swope SM, Rieseberg LH (2015) Evolution of invasiveness through increased resource use in a vacant niche. Nat Plants 1:15066. https://doi.org/10.1038/nplants.2015.66
Folmer O, Black M, Hoeh W, Lutz RVR (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299. https://doi.org/10.1371/journal.pone.0013102
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks
Fujino T, Shokita S (1975) Report on some new atyid shrimps (crustacea, decapoda, caridea) from the Ryukyu Islands. Bull Sci & Eng Div Univ Ryukyus (math & Nat Sci) 18:93–113
Fujioka Y (2012) Utilization of young ayu fish. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, Dordrecht, p 355
Fujioka Y, Maehata M (2012) Recent Changes in the Lake Biwa Fisheries. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, Dordrecht, pp 313–316
Fujita T, Nishino M, Hosoya K (2008) The original scenery of the “Naiko” lagoons around Lake Biwa inferred by fish specimen survey. Jap J Ichthyol 55:73–93. https://doi.org/10.11369/jji1950.55.77
Fuke Y, Iwasaki T, Sasazuka M, Yamamoto Y (2021) First record of freshwater shrimp Neocaridina denticulata (Crustacea: Decapoda: Atyidae) from Fukue-jima Island, Goto Islands. Japan Cancer 30:63–71. https://doi.org/10.18988/cancer.30.0_63
Furukawa M, Awano K (1969) Record of introductions of aquatic organisms. Bull Shiga Pref Fish Exp Sta 22:245–250
Gallien L, Carboni M (2017) The community ecology of invasive species: where are we and what’s next? Ecography 40:335–352. https://doi.org/10.1111/ecog.02446
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010
De Haan W (1833–1850) Crustacea. In: Von Siebold PF (ed) Fauna Japonica sive Descriptio Animalium, quae in Itinere per Japoniam, jussu et auspiciis superiorum, qui summum in India Batava imperium tenent, suscepto, annis 1823–1830 collegit, notis, observationibus et adumbrationibus illustravit, vii–xvii, i–xxxi, ix–xvi, 1–243, plates A–J, L–Q, 1–55. (In Latin and French) https://doi.org/10.5962/bhl.title.124951
Han C-C, Hsu K-C, Fang L-S, Cheng I-M, Lin H-D (2019) Geographical and temporal origins of Neocaridina species (Decapoda: Caridea: Atyidae) in Taiwan. BMC Genet 20:86. https://doi.org/10.1186/s12863-019-0788-y
Hasegawa M, Ikeda M, Fujimoto Y (2015) Distribution of the exotic freshwater shrimp Neocaridina spp. in Miyagi Prefecture and influence on the habitat of native shrimp Paratya compressa improbisa. Izunuma Uchinuma Wetland Res 9:47–56. https://doi.org/10.20745/izu.9.0_47
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281
Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152. https://doi.org/10.1016/S0006-3207(98)00153-0
Jabłońska A, Mamos T, Gruszka P, Szlauer-Łukaszewska A, Grabowski M (2018) First record and DNA barcodes of the aquarium shrimp, Neocaridina davidi, in Central Europe from thermally polluted River Oder canal. Poland Knowl Manag Aquat Ecosyst 419:14. https://doi.org/10.1051/kmae/2018004
Jaspers C, Huwer B, Antajan E, Hosia A, Hinrichsen HH, Biastoch A, Angel D, Asmus R, Augustin C, Bagheri S, Beggs SE, Balsby TJS, Boersma M, Bonnet D, Christensen JT, Dänhardt A, Delpy F, Falkenhaug T, Finenko G, Fleming NEC, Fuentes V, Galil B, Gittenberger A, Griffin DC, Haslob H, Javidpour J, Kamburska L, Kube S, Langenberg VT, Lehtiniemi M, Lombard F, Malzahn A, Marambio M, Mihneva V, Møller LF, Niermann U, Okyar MI, Özdemir ZB, Pitois S, Reusch TBH, Robbens J, Stefanova K, Thibault D, van der Veer HW, Vansteenbrugge L, van Walraven L, Woźniczka A (2018) Ocean current connectivity propelling the secondary spread of a marine invasive comb jelly across western Eurasia. Glob Ecol Biogeogr 27:814–827. https://doi.org/10.1111/geb.12742
Kakui K, Komai T (2022) First record of Scutariella japonica (Platyhelminthes: Rhabdocoela) from Hokkaido, Japan, and notes on its host shrimp Neocaridina sp. Aff. davidi (Decapoda: Caridea: Atyidae). Aquat Anim. https://doi.org/10.34394/aquaticanimals.2022.0_AA2022-1
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Kamita T (1951) Freshwater shrimps from the Iwami and Izumo Districts of San-in Province, Japan. Bull Shimane Univ (nat Sci) 1:71–82
Kamita T (1953) Supplementary notes on the freshwater shrimps from the Iwami and Izumo Districts of San-in Province, Japan. Bull Shimane Univ (nat Sci) 3:81–93
Kamita T (1970) Studies on the fresh-water shrimps, prawns and crawfishes of Japan (revised and enlarged edition). Sonoyama, Matsue. (In Japanese with English abstract)
Kanao S, Matsuda M (2012) Present status and future conservation of native bitterlings (Cyprinidae) in Lake Biwa, Japan. Jap J Ichthyol 59:75–78. https://doi.org/10.11369/jji.59.75
Kano Y, Adnan MS, Grudpan C, Grudpan J, Magtoon W, Musikasinthorn P, Natori Y, Ottomanski S, Praxaysonbath B, Phongsa K, Rangsiruji A, Shibukawa K, Shimatani Y, So N, Suvarnaraksha A, Thach P, Thanh PN, Tran DD, Utsugi K, Yamashita T (2013) An online database on freshwater fish diversity and distribution in Mainland Southeast Asia. Ichthyol Res 60:293–295. https://doi.org/10.1007/s10228-013-0349-8
Katayama A, Satou R, Yoshikawa T (2017) Distribution of introduced freshwater shrimp Neocaridina sp. and native shrimp Paratya improvisa in the Tsurimi River in eastern Japan. Nat Envl Sci Res 30:5–12. https://doi.org/10.32280/nesr.30.0_5
Katoh K, Standley DM (2013) MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kawabe K (1965) PCP no gyojyo heno eikyo. Nippon Suisan Gakkaishi 31:732–736
Kemp BA (1918) Zoological results of a tour in the Far East. Crustacea Decapoda and Stomatopoda. Mem Asiat Soc Bengal 6:219–297. https://doi.org/10.1038/133051a0
Kitanishi S, Hayakawa A, Takamura K, Nakajima J, Kawaguchi Y, Onikura N, Mukai T (2016) Phylogeography of Opsariichthys platypus in Japan based on mitochondrial DNA sequences. Ichthyol Res 63:506–518. https://doi.org/10.1007/s10228-016-0522-y
Klotz W, Miesen FW, Hüllen S, Herder F (2013) Two Asian fresh water shrimp species found in a thermally polluted stream system in North Rhine-Westphalia, Germany. Aquat Invasions 8:333–339. https://doi.org/10.3391/ai.2013.8.3.09
Krishnamurthy PK, Francis RA (2012) A critical review on the utility of DNA barcoding in biodiversity conservation. Biodivers Conserv 21:1901–1919. https://doi.org/10.1007/s10531-012-0306-2
Kubo I (1938) On the Japanese atyid shrimps. J Imp Fish Institute 33:67–100
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Levitt-Barmats Y, Yanai Z, Cohen T, Shenkar N (2019) Life-history traits and ecological characteristics of the ornamental shrimp Neocaridina denticulata (De Haan, 1844), recently introduced into the freshwater systems of Israel. Aquat Invasions 14:684–702. https://doi.org/10.3391/ai.2019.14.4.08
Liang XQ (2004) Fauna Sinica. Invertebrata. Vol. 36. Crustacea. Decapoda. Atyidae. Science Press, Beijing, China. (In Chinese with English abstract)
Maehata M (2020) Characteristics of the ichthyofauna of Lake Biwa, with special reference to Its long-term changes. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, Cham, pp 213–217
Matida Y (1968) Deleterious effect of agricultural control chemicals to fresh-water fisheries. Annu Rep Noto Mar Lab 8:59–69
Meirmans PG (2020) GENODIVE version 3.0: easy-to-use software for the analysis of genetic data of diploids and polyploids. Mol Ecol Resour 20:1126–1131. https://doi.org/10.1111/1755-0998.13145
Mesgaran MB, Lewis MA, Ades PK, Donohue K, Ohadi S, Li C, Cousens RD (2016) Hybridization can facilitate species invasions, even without enhancing local adaptation. Proc Natl Acad Sci 113:10210–10214. https://doi.org/10.1073/pnas.1605626113
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Von Haeseler A, Lanfear R, Teeling E (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534. https://doi.org/10.1093/molbev/msaa015
Mitsugi M, Suzuki H (2018) Life history of an invasive freshwater shrimp Neocaridina davidi (Bouvier, 1904), (Decapoda: Caridea: Atyidae) in the Tomoe River, the Boso Peninsula, eastern Japan. Crustac Res 47:9–16. https://doi.org/10.18353/crustacea.47.0_9
Mitsugi M, Hisamoto Y, Suzuki H (2017) An invasive freshwater shrimp of the genus Neocaridina Kubo, 1938 (Decapoda: Caridea: Atyidae) collected from Boso Peninsula, Tateyama City, Chiba Prefecture, eastern Japan. Crustac Res 46:83–94. https://doi.org/10.18353/crustacea.46.0_83
Mitsui S, Ito K, Aikawa T, Chokki H, Sato T, Karube H, Matsumoto R, Senou H (2019) The Aquatic fauna of the water moats of the Odawara Castle Park, Odawara City, Kanagawa Prefecture. Nat Hist Rep Kanagawa 40:75–83. https://doi.org/10.32225/nkpmnh.2019.40_75
Nagai H, Imai H (2021) First record of the invasive alien species Neocardina sp. from Okinawajima Island, central Ryukyus. Japan Bull Biogeogr Soc Japan 76:51–57
Nakai K, Kaneko Y (2020) Non-indigenous species in and around Lake Biwa. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, Cham, pp 299–312
Nakanishi M, Sekino T (1996) Recent drastic changes in Lake Biwa bio-communities, with special attention to exploitation of the littoral zone. GeoJournal 40:63–67. https://doi.org/10.1007/BF00222532
Naruse T, Shokita S, Cai Y (2006) Neocaridina iriomotensis, a new species of land-locked freshwater shrimp (Crustacea: Decapoda: Atyidae) from Iriomote Island, southern Ryukyu, Japan. Proc Biol Soc Wash 119:25–31. https://doi.org/10.2988/0006-324X(2006)119[25:NIANSO]2.0.CO;2
Nishida K (2016) Longitudinal distributions of native shrimp Paratya improvisa and non-native shrimp Neocaridina spp. in downstream of the Shiroyama Dam, Sagami River basin, Japan. Nat Hist Rep Kanagawa 37:21–24. https://doi.org/10.32225/nkpmnh.2016.37_21
Nishino M (1980) Geographical variations in body size, brood size and egg size of a freshwater shrimp, Palaemon paucidens De Haan, with some discussion on brood habit. Japanese J Limnol 41:185–202
Nishino M (2017) Invasion of alien freshwater shrimps, Neocaridina spp., into Japan and taxonomic problem of the genus. Bull Kansai Organ Nat Conserv 39:21–28
Nishino M (2020a) Biodiversity of Lake Biwa. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, Cham, p 69
Nishino M (2020b) Malacostraca. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, Cham, pp 165–166
Nishino M, Azuma Y, Tatsumi M, Kaneko Y (2020) Ecological changes in the littoral of Lake Biwa and adjacent areas with special reference to water-level control. In: Kawanabe H, Nishino M, Maehata M (eds) Lake Biwa: Interactions between Nature and People. Springer, Cham, pp 261–264
Niwa N (2010) Invasion and dispersion routes of alien alive freshwater shrimps Neocaridina spp. (Caridea, Atyidae) and Palaemonidae spp. (Caridea) imported into Japan. Cancer 19:75–80. https://doi.org/10.18988/cancer.19.0_75
Niwa N, Archdale MV, Matsuoka T, Kawamoto A, Nishiyama H (2014) Microhabitat distribution and behaviour of Branchiobdellidan Holtodrilus truncatus found on the freshwater shrimp Neocaridina spp. from the Sugo River. Japan Cent Eur J Biol 9:80–85. https://doi.org/10.2478/s11535-013-0184-3
Okonechnikov K, Golosova O, Fursov M, Varlamov A, Vaskin Y, Efremov I, German Grehov OG, Kandrov D, Rasputin K, Syabro M, Tleukenov T (2012) Unipro UGENE: A unified bioinformatics toolkit. Bioinformatics 28:1166–1167. https://doi.org/10.1093/bioinformatics/bts091
Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55. https://doi.org/10.1146/annurev-environ-033009-095548
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rochette NC, Rivera-Colón AG, Catchen JM (2019) Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28:4737–4754. https://doi.org/10.1111/mec.15253
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Schneider G, Chicken E, Becvarik R (2021) NSM3: Functions and datasets to accompany Hollander, Wolfe, and Chicken - Nonparametric Statistical Methods, third edition. R package version 1.16. https://CRAN.R-project.org/package=NSM3
Seebens H, Schwartz N, Schupp PJ, Blasius B (2016) Predicting the spread of marine species introduced by global shipping. Proc Natl Acad Sci 113:5646–5651. https://doi.org/10.1073/pnas.1524427113
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176. https://doi.org/10.1016/S0169-5347(02)02495-3
Shih H-T, Cai Y (2007) Two new species of the land-locked freshwater shrimps genus, Neocaridina Kubo, 1938 (Decapoda: Caridea: Atyidae), from Taiwan, with notes on speciation on the Island. Zool Stud 46:680–694
Shih H-T, Cai Y, Niwa N, Nakahara Y (2017) A new species of land-locked freshwater shrimp of the genus Neocaridina (Decapoda: Caridea: Atyidae) from Iki Island, Kyushu, Japan. Zool Stud 56:1–14. https://doi.org/10.6620/ZS.2017.56-30
Shih H-T, Cai Y, Chiu Y-W (2019) Neocaridina fonticulata, a new land-locked freshwater shrimp from Hengchun Peninsula, Taiwan (Decapoda, Caridea, Atyidae). Zookeys 817:11–23. https://doi.org/10.3897/zookeys.817.29332
Suyama Y, Matsuki Y (2015) MIG-seq: An effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Sci Rep 5:16963. https://doi.org/10.1038/srep16963
Suyama Y, Hirota SK, Matsuo A, Tsunamoto Y, Mitsuyuki C, Shimura A, Okano K (2021) Complementary combination of multiplex high-throughput DNA sequencing for molecular phylogeny. Ecol Res 37:171–181. https://doi.org/10.1111/1440-1703.12270
Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hübner S, Heredia SM, Hahn MA, Caseys C, Bock DG, Rieseberg LH (2016) Hybridization and extinction. Evol Appl 9:892–908
Usio N, Azuma N, Larson ER, Abbott CL, Olden JD, Akanuma H, Takamura K, Takamura N (2016) Phylogeographic insights into the invasion history and secondary spread of the signal crayfish in Japan. Ecol Evol 6:5366–5382. https://doi.org/10.1002/ece3.2286
Vander Zanden MJ, Olden JD (2008) A management framework for preventing the secondary spread of aquatic invasive species. Can J Fish Aquat Sci 65:1512–1522. https://doi.org/10.1139/F08-099
Watanabe K (2012) Faunal structure of Japanese freshwater fishes and its artificial disturbance. Environ Biol Fishes 94:533–547. https://doi.org/10.1007/s10641-010-9601-5
Watanabe K, Kano Y, Takahashi H, Mukai T, Kakioka R, Tominaga K (2010) GEDIMAP: a database of genetic diversity for Japanese freshwater fishes. Ichthyol Res 57:107–109. https://doi.org/10.1007/s10228-009-0129-7
Watanabe K, Tabata R, Nakajima J, Kobayakawa M, Matsuda M, Takaku K, Hosoya K, Ohara K, Takagi M, Jang-Liaw NH (2020) Large-scale hybridization of Japanese populations of Hinamoroko, Aphyocypris chinensis, with A. kikuchii introduced from Taiwan. Ichthyol Res 67:361–374. https://doi.org/10.1007/s10228-019-00730-9
Yoshigou H (2011) The occurrence of the alien shrimp (Neocaridina sp.) in the Hiroshima Prefecture, with notes of some fishes in the mixing in transported shrimps from foreigner. J Hiba Soc Nat Hist 239:9–29
Yu Y-Q, Yang W-J, Yang J-S (2014) The complete mitogenome of the Chinese swamp shrimp Neocaridina denticulata sinensis Kemp 1918 (Crustacea: Decapoda: Atyidae). Mitochondrial DNA 25:204–205. https://doi.org/10.3109/19401736.2013.796465
Zhou C, Feng M, Tang Y, Yang C, Meng X, Nie G (2021) Species diversity of freshwater shrimp in Henan Province, China, based on morphological characters and COI mitochondrial gene. Ecol Evol 11:10502–10514. https://doi.org/10.1002/ece3.7855
Acknowledgements
We are grateful to Masaki Asano, Shota Kunimatsu, Eugene Agyeman and Masami Hashiguchi for their cooperation in the fieldwork; Takafumi Nakano for registering the specimens and supporting the research in KUZ; Shoko Matsui for supporting the MIG-seq primer selection process; Yuichi Kano for registering the photographs to the database; Keiichi Kakui and Tomoyuki Komai for letting us use their beautiful illustrations; Katsutoshi Watanabe for giving helpful comments to our manuscript.
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This work was partly supported by Grant-in-Aid for JSPS Research Fellow Grant Number JP19J23130 to Yusuke Fuke.
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All authors contributed to the study conception and design, sampling, morphometry, and manuscript preparation. All statistical analyses were performed by Keisuke Onuki. Primer development and genetic analysis were performed by Yusuke Fuke. All authors read and approved the final manuscript.
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Supplementary file1 (EPS 3031 kb) Supplemental Figure 1 Phylogenetic relationships of the Neocaridina species based on the 596 bp mtDNA COI region. Tree estimation was performed by the maximum likelihood method using IQ-TREE2 based on the HKY+F+I+G4 model. The numbers in each node represent the support values or posterior probability estimated by SH-like approximate likelihood ratio test 1000 times, approximate Bayes test, and the ultrafast bootstrap 1000 times. The bold tip labels represent samples with evidence of identification by morphology in previous studies or this study. The blue tip labels represent haplotypes detected in this study
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Onuki, K., Fuke, Y. Rediscovery of a native freshwater shrimp, Neocaridina denticulata, and expansion of an invasive species in and around Lake Biwa, Japan: genetic and morphological approach. Conserv Genet 23, 967–980 (2022). https://doi.org/10.1007/s10592-022-01467-1
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DOI: https://doi.org/10.1007/s10592-022-01467-1