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Underestimated species diversity and hidden habitat preference in Moina (Crustacea, Cladocera) revealed by integrative taxonomy

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Abstract

In Japan, farm ponds retain water throughout the year while rice fields are continuously inundated for no more than 2 months, usually from spring to early summer. Although the zooplankton fauna in artificial water bodies would be expected to vary according to differences in inundation periods, scientific confirmation of this relation is largely lacking. Due to its ubiquity, the cladoceran Moina is a suitable target for studying habitat-related differences in the planktonic fauna, but its taxonomy remains unresolved, making morphological identifications potentially uncertain. We thus applied integrative taxonomy with both morphological and genetic evaluations for reliable species delimitation to Moina samples collected primarily in Japan (with smaller collections from Taiwan). This approach increased the alpha diversity of Moina species in Japan from three (in previous studies) to seven. It also revealed different habitat preferences among Moina species, with the smaller species being distributed mostly in farm ponds (followed by natural lakes), and the larger species mostly in rice fields. We argue that the phenological match/mismatch with inundation period of rice fields was a major factor for this strong trend of spatial species turnover, with differing degrees of fish predation pressure among the habitat types being another factor.

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References

  • Ali, A. B., 1990. Seasonal dynamics of microcrustacean and rotifer communities in Malaysian rice fields used for rice-fish farming. Hydrobiologia 206: 139–148.

    Google Scholar 

  • Alonso, M., A. N. Neretina, L.-O. Sanoamuang, N. Saengphan & A. A. Kotov, 2019. A new species of Moina Baird, 1850 (Cladocera: Moinidae) from Thailand. Zootaxa 4554: 199–218.

    PubMed  Google Scholar 

  • Ban, S., W. Makino, H. Sakano, H. Haruna & H. Ueda, 2013. Annual variation in biomass and the community structure of crustacean zooplankton over 5 years in Lake Toya, Japan. Limnology 14: 59–70.

    Google Scholar 

  • Bekker, E. I., D. P. Karabanov, Y. R. Galimov & A. A. Kotov, 2016. DNA barcoding reveals high cryptic diversity in the North Eurasian Moina species (Crustacea: Cladocera). PLoS ONE 11: e0161737.

    PubMed  PubMed Central  Google Scholar 

  • Belyaeva, M. & D. J. Taylor, 2009. Cryptic species within the Chydorus sphaericus species complex (Crustacea: Cladocera) revealed by molecular markers and sexual stage morphology. Molecular Phylogenetics and Evolution 50: 534–546.

    CAS  PubMed  Google Scholar 

  • Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and the composition of the plankton. Science 150: 28–35.

    CAS  PubMed  Google Scholar 

  • Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.

    CAS  PubMed  Google Scholar 

  • Collen, B., F. Whitton, E. E. Dyer, J. E. Baillie, N. Cumberlidge, W. R. Darwall, C. Pollock, N. I. Richman, A. Soulsby & M. Böhm, 2014. Global freshwater species congruence. Global Ecology and Biogeography 23: 40–51.

    PubMed  Google Scholar 

  • Collins, R. A. & R. H. Cruickshank, 2013. The seven deadly sins of DNA barcoding. Molecular Ecology Resources 13: 969–975.

    CAS  PubMed  Google Scholar 

  • Crease, T. J. & D. J. Taylor, 1998. The origin and evolution of variable-region helices in V4 and V7 of the small-subunit ribosomal RNA of Branchiopod crustaceans. Molecular Biology and Evolution 15: 1430–1446.

    CAS  PubMed  Google Scholar 

  • deWaard, J. R., V. Sacherova, M. E. A. Cristescu, E. A. Remigio, T. J. Crease & P. D. N. Hebert, 2006. Probing the relationships of the branchiopoid crustaceans. Molecular Phylogenetics and Evolution 39: 491–502.

    CAS  PubMed  Google Scholar 

  • Elías-Gutiérrez, M., F. M. Jerónimo, N. V. Ivanova, M. Valdez-Moreno & P. D. N. Hebert, 2008. DNA barcodes for Cladocera and Copepoda from Mexico and Guatemala, highlights and new discoveries. Zootaxa 1839: 1–42.

    Google Scholar 

  • Elías-Gutiérrez, M., M. Valdez-Moreno, J. Topan, M. R. Young & J. A. Cohuo-Colli, 2018. Improved protocols to accelerate the assembly of DNA barcode reference libraries for freshwater zooplankton. Ecology and Evolution 8: 3002–3018.

    PubMed  PubMed Central  Google Scholar 

  • Elías-Gutiérrez, M., P. J. J. Juračka, L. Montoliu-Elena, M. R. Miracle, A. Petrusek & V. Kořínek, 2019. Who is Moina micrura? Redescription of one of the most confusing cladocerans from terra typica, based on integrative taxonomy. Limnetica 38: 227–252.

    Google Scholar 

  • Gliwicz, Z. M., 1990. Food thresholds and body size in cladocerans. Nature 343: 638–640.

    Google Scholar 

  • Goulden, C. E., 1968. The systematics and evolution of the Moinidae. Transactions of the American Philosophical Society Philadelphia 58: 1–101.

    Google Scholar 

  • Hayasaka, D., T. Korenaga, K. Suzuki, F. Sánchez-Bayo & K. Goka, 2012. Differences in susceptibility of five cladoceran species to two systemic insecticides, imidacloprid and fipronil. Ecotoxicology 21: 421–427.

    CAS  PubMed  Google Scholar 

  • Hayasaka, D., K. Suzuki, T. Nomura, M. Nishiyama, T. Nagai, F. Sánchez-Bayo & K. Goka, 2013. Comparison of acute toxicity of two neonicotinoid insecticides, imidacloprid and clothianidin, to five cladoceran species. Journal of Pesticide Science 38: 44–47.

    CAS  Google Scholar 

  • Hayashi, N., T. Ohuchi & N. Miyata, 2009. Planktonic biota occurring in rice fields in Japan. Journal of the Natural History Museum and Institute, Chiba 10: 71–79 (in Japanese with English abstract).

    Google Scholar 

  • Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. deWaaard, 2003a. Biological identifications through DNA barcodes. Proceedings of the Royal Society London B 270: 313–321.

    CAS  Google Scholar 

  • Hebert, P. D. N., S. Ratnasingham & J. R. deWaard, 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society London B 270(Suppl 1): S96–S99.

    CAS  Google Scholar 

  • Hidaka, K., 1998. Biodiversity conservation and environmentally regenerated farming system in rice paddy fields. Japanese Journal of Ecology 48: 167–178 (in Japanese with English title).

    Google Scholar 

  • Hudec, I., 1990. Moina weismanni Ishikawa, 1896 (Cladocera, Moinidae) in Central Europe. Hydrobiologia 190: 33–42.

    Google Scholar 

  • Ishikawa, C., 1896. Phyllopoda crustacean of Japan. Zoological Magazine, Tokyo 8: 1–6.

    Google Scholar 

  • Jeong, H., A. A. Kotov & W. Lee, 2014. Checklist of the freshwater Cladocera (Crustacea: Branchiopoda) of South Korea. Proceedings of the Biological Society of Washington 127: 216–228.

    Google Scholar 

  • Johnson, M., I. Zaretskaya, Y. Raytselis, Y. Merezhuk, S. McGinnis & T. L. Madden, 2008. NCBI BLAST: a better web interface. Nucleic Acids Research 36(suppl 2): W5–W9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kadono, Y., 1994. Aquatic Plants of Japan. Bun-ichi sogo shuppan, Tokyo (in Japanese).

    Google Scholar 

  • Kadono, Y. & M. Yuma, 1995. The Nature of Wetlands in Japan. Hoikusha, Osaka (in Japanese).

    Google Scholar 

  • Kano, Y., Y. Kawaguchi, T. Yamashita & Y. Shimatani, 2010. Distribution of the oriental weatherloach, Misgurnus anguillicaudatus, in paddy fields and its implications for conservation in Sado Island, Japan. Ichthyological Research 57: 180–188.

    Google Scholar 

  • Katayama, N., Y. G. Baba, Y. Kusumoto & K. Tanaka, 2015. A review of post-war changes in rice farming and biodiversity in Japan. Agricultural Systems 132: 73–84.

    Google Scholar 

  • Katoh, K., J. Rozewicki & K. D. Yamada, 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166.

    PubMed  Google Scholar 

  • Kikuchi, E., Y. Takagi & S. Shikano, 2012. Survey of plankton (aquatic microorganisms) communities in rice fields. Res Bull Environ Edu Cent, Miyagi Univ Edu 14: 7–15. (in Japanese).

    Google Scholar 

  • Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120.

    CAS  PubMed  Google Scholar 

  • Korovchinsky, N. M., 2000. Species richness of pelagic Cladocera of large lakes in the eastern hemisphere. Hydrobiologia 434: 41–54.

    Google Scholar 

  • Korovchinsky, N. M., 2009. The genus Leptodora Lillijeborg (Crustacea: Branchiopoida: Cladocera) is not monotypic: description of a new species from the Amur River basin (Far East of Russia). Zootaxa 2120: 39–52.

    Google Scholar 

  • Kotov, A. A., S. Ishida & D. J. Taylor, 2009. Revision of the genus Bosmina Baird, 1845 (Cladocera: Bosminidae), based on evidence from male morphological characters and molecular phylogenies. Zoological Journal of the Linnean Society 156: 1–51.

    Google Scholar 

  • Kreutzer, C. & W. Lampert, 1999. Exploitative competition in differently sized Daphnia species: a mechanistic explanation. Ecology 80: 2348–2357.

    Google Scholar 

  • Kubota, Z., 1961. Ecology of the Japanese loach, Misgurnus anguillicaudatus (Cantor) – II. Food habit. Journal of Shimonoseki University Fisheries 11: 177–195 (in Japanese with English abstract).

    Google Scholar 

  • Kumar, S., G. Stecher, M. Li, C. Knyaz & K. Tamura, 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lakatos, C., J. Urabe & W. Makino, 2015. Cryptic diversity of Japanese Diaphanosoma (Crustacea: Cladocera) revealed by morphological and molecular assessments. Inland Water 5: 253–262.

    Google Scholar 

  • Lampert, W. & U. Sommer, 2007. Limnoecology: The Ecology of Lakes and Streams, 2nd ed. Oxford University Press, Oxford.

    Google Scholar 

  • Lane, S. J. & M. Fujioka, 1998. The impact of changes in irrigation practices on the distribution of foraging egrets and herons (Ardeidae) in the rice fields of central Japan. Biological Conservation 83: 221–230.

    Google Scholar 

  • Lee, C. E. & B. W. Frost, 2002. Morphological stasis in the Eurytemora affinis species complex (Copepoda: Temoridae). Hydrobiologia 480: 111–128.

    CAS  Google Scholar 

  • Leigh, J. W. & D. Bryant, 2015. POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6: 1110–1116.

    Google Scholar 

  • Ma, X., A. Petrusek, J. Wolinska, W. Hu & M. Yin, 2019. Lineage diversity and reproductive modes of the Daphnia pulex group in Chinese lakes and reservoirs. Molecular Phylogenetics and Evolution 130: 424–443.

    PubMed  Google Scholar 

  • Maezono, Y. & T. Miyashita, 2003. Community-level impacts induced by introduced largemouth bass and bluegill in farm ponds in Japan. Biological Conservation 109: 111–121.

    Google Scholar 

  • Maier, G., 1990. Coexistence of the predatory cyclopoids Acanthocyclops robustus (Sars) and Mesocyclops leuckarti (Claus) in a small eutrophic lake. Hydrobiologia 198: 185–203.

    Google Scholar 

  • Makino, W. & A. S. Tanabe, 2009. Extreme population genetic differentiation and secondary contact in the freshwater copepod Acanthodiaptomus pacificus in the Japanese Archipelago. Molecular Ecology 18: 3699–3713.

    CAS  PubMed  Google Scholar 

  • Makino, W., N. Maruoka, M. Nakagawa & N. Takamura, 2017. DNA barcoding of freshwater zooplankton in Lake Kasumigaura, Japan. Ecological Research 32: 481–493.

    CAS  Google Scholar 

  • Makino, W., A. S. Tanabe & J. Urabe, 2018. The fauna of freshwater calanoid copepods in Japan in the early decades of the 21st Century: implications for the assessment and conservation of biodiversity. Limnology and Oceanography 63: 758–772.

    Google Scholar 

  • Margaritora, F. G., I. Ferrari & D. Crosetti, 1987. A Far East Moina, M. weismanni Ishikawa, 1896 found in an Italian ricefield. Hydrobiologia 145: 93–103.

    Google Scholar 

  • Marrone, F., S. Lo Brutto, A. K. Hundsdoerfer & M. Arculeo, 2013. Overlooked cryptic endemism in copepods: systematics and natural history of the calanoid subgenus Occidodiaptomus Borutzky 1991 (Copepoda, Calanoda, Dia-ptomidae). Molecular Phylogenetics and Evolution 66: 190–202.

    PubMed  Google Scholar 

  • Matsuzaki, S. S., K. Suzuki, T. Kadoya, M. Nakagawa & N. Takamura, 2018. Bottom-up linkages between primary production, zooplankton, and fish in a shallow, hypereutrophic lake. Ecology 99: 2025–2036.

    PubMed  Google Scholar 

  • McElrath, T. C., O. F. Boyd & J. V. McHugh, 2016. MonotomidGen – a matrix based interactive key to the New World genera of Monotomidae (Coleoptera, Cucujoidea). ZooKeys 634: 47–55.

    Google Scholar 

  • McTaggart, S. J. & T. J. Crease, 2009. Length variation in 18S rRNA expansion segment 43/e4 of Daphnia obtusa: ancient or recurring polymorphism? Journal of Molecular Evolution 69: 142–149.

    CAS  PubMed  Google Scholar 

  • Mills, S., J. A. Alcántara-Rodríguez, J. Ciros-Pérez, A. Gómez, A. Hagiwara, K. H. Galindo, et al., 2017. Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia 796: 39–58.

    CAS  Google Scholar 

  • Ministry of Agriculture, Forestry and Fisheries of Japan, 2019. http://www.maff.go.jp/j/tokei/kouhyou/sakumotu/sakkyou_kome/index.html#y3. Accessed 18 Sept 2019.

  • Ministry of Foreign Affairs of Japan, 2019. https://www.mofa.go.jp/mofaj/territory/page1w_000011.html. Accessed 19 Sept 2019.

  • Mirabdullayev, I. M., 1998. Moina mukhamedievi n. sp. (Crustacea, Cladocera) from ricefields of Uzbekistan (central Asia). Hydrobiologia 385: 11–16.

    Google Scholar 

  • Mizuno, T. & E. Takahashi (eds), 2000. An illustrated guide to freshwater zooplankton in Japan (in Japanese). Tokai University Press, Tokyo.

    Google Scholar 

  • Montoliu-Elena, L., M. Elías-Gutiérrez & M. Silva-Briano, 2019. Moina macrocopa (Straus, 1820): a species complex of a common Cladocera, highlighted by morphology and DNA barcodes. Limnetica 38: 253–277.

    Google Scholar 

  • Mukai, Y., T. Suzuki, W. Makino, T. Iwabuchi, M. So & J. Urabe, 2014. Ecological impacts of the 2011 Tohoku Earthquake Tsunami on aquatic animals in rice paddies. Limnology 15: 201–211.

    CAS  Google Scholar 

  • Natsuhara, Y., 2013. Ecosystem services by paddy fields as substitutes of natural wetlands in Japan. Ecological Engineering 53: 97–106.

    Google Scholar 

  • Nature Conservation Bureau of the Environment Agency of Japan, 1995. The 4th National Survey on the Natural Environment, Summary volume: 106 (in Japanese).

  • Nédli, J., L. De Meester, Á. Major, K. Schwenk, I. Szivák & L. Forró, 2014. Salinity and depth as structuring factors of cryptic divergence in Moina brachiata (Crustacea: Cladocera). Fundamental and Applied Limnology 184: 69–85.

    Google Scholar 

  • Ni, Y., X. Ma, W. Hu, D. Blair & M. Yin, 2019. New lineages and old species: lineage diversity and regional distribution of Moina (Crustacea: Cladocera) in China. Molecular Phylogenetics and Evolution 134: 87–98.

    PubMed  Google Scholar 

  • Nishimura, Y., T. Ohtsuka, K. Yoshiyama, D. Nakai, F. Shibahara & M. Maehata, 2011. Cascading effects of larval crucian carp introduction on phytoplankton and microbial communities in a paddy field: top-down and bottom-up controls. Ecological Research 26: 615–626.

    Google Scholar 

  • Nishio, M., K. Edo & Y. Yamazaki, 2017. Paddy management for potential conservation of endangered Itasenpara bitterling via zooplankton abundance. Agriculture, Ecosystems & Environment 247: 166–171.

    Google Scholar 

  • Ohba, S., K. Suzuki, Y. Sakai, J. Shibata & N. Okuda, 2019. Effects of irrigation system alterations on the trophic position of a threatened top predator in rice-field ecosystems. Freshwater Biology 64: 1737–1746.

    Google Scholar 

  • Petrusek, A., 2002. Moina (Crustacea: Anomopoda, Moinidae) in the Czech Republic (a review). Acta Societatis Zoologicae Bohemicae 66: 213–220.

    Google Scholar 

  • Petrusek, A., M. Cerny & E. Audenaert, 2004. Large intercontinental differentiation of Moina micrura (Crustacea: Anomopoda): one less cosmopolitan cladoceran? Hydrobiologia 526: 73–81.

    Google Scholar 

  • Prosser, S., A. Martínez-Arce & M. Elías-Gutiérrez, 2013. A new set of primers for COI amplification from freshwater microcrustaceans. Molecular Ecology Resources 13: 1151–1155.

    CAS  PubMed  Google Scholar 

  • Puillandre, N., A. Lambert, S. Brouillet & G. Achaz, 2012. ABGD, Automated Barcode Gap Discovery for primary species delimitation. Mol Ecol 21: 1864–1877.

    CAS  PubMed  Google Scholar 

  • R Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/. Accessed 20 June 2015.

  • Raupach, M. J. & A. E. Radulovici, 2015. Looking back on a decade of barcoding crustaceans. ZooKeys 539: 53–81.

    Google Scholar 

  • Raupach, M. J., J. J. Astrin, K. Hanning, M. K. Peters, M. Y. Stoeckle & J.-W. Wägele, 2010. Molecular species identification of Central European ground beetles (Coleoptera: Carabidae) using nuclear rDNA expansion segments and DNA barcodes. Frontiers in Zoology 7: 26.

    PubMed  PubMed Central  Google Scholar 

  • Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Daring, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large models space. Systematic Biology 61: 539–542.

    PubMed  PubMed Central  Google Scholar 

  • Rowe, C. L., S. J. Adamowicz & P. D. N. Hebert, 2007. Three new cryptic species of the freshwater zooplankton genus Holopedium (Crustacea: Branchiopoda: Ctenopoda) revealed by genetic methods. Zootaxa 1656: 1–49.

    Google Scholar 

  • Saitoh, K., O. Katano & A. Koizumi, 1988. Movement and spawning of several freshwater fishes in temporary waters around paddy fields. Japanese Journal of Ecology 38: 35–47 (in Japanese with English abstract).

    Google Scholar 

  • Simons, J. L., 2013. Prey (Moina macrocopa) population density drives emigration rate of its predator (Trichocorixa verticalis) in a rock-pool metacommunity. Hydrobiologia 715: 19–27.

    Google Scholar 

  • Stefanni, S., D. Stankovic, D. Borme, A. de Olazabal, T. Juretic, A. Pallavicini & V. Tirelli, 2018. Multi-marker metabarcording approach to study mesozooplankton at basin scale. Scientific Reports 8: 12085.

    PubMed  PubMed Central  Google Scholar 

  • Strayer, D. L. & D. Dudgeon, 2010. Freshwater biodiversity conservation: recent progress and future challenges. Journal of the North American Benthological Society 29: 344–358.

    Google Scholar 

  • Taira, M. & K. Hogetsu, 1987. Species composition of phyto- and zoo-plankton communities in fertilized and non-fertilized paddy fields. Japanese Journal of Limnology 48: 77–83 (in Japanese with English abstract).

    Google Scholar 

  • Takamura, N., H. Mikami, H. Mizutani & K. Nagasaki, 1999. Did a drastic change in fish species from kokanee to pond smelt decrease the Secchi disc transparency in the oligotrophic Lake Towada, Japan? Archiv für Hydrobiologie 144: 283–304.

    Google Scholar 

  • Takamura, N., M. Nakagawa & T. Hanazato, 2017. Zooplankton abundance in the pelagic region of Lake Kasumigaura (Japan): monthly data since 1980. Ecological Research 32: 1–1.

    Google Scholar 

  • Tanabe, A. S., 2007. KAKUSAN: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data. Molecular Ecology Resources 7: 962–964.

    CAS  Google Scholar 

  • Tanabe, A. S., S. Nagai, K. Hida, M. Yasuike, A. Fujiwara, Y. Nakamura, Y. Takano & S. Katakura, 2016. Comparative study of the validity of three regions of the18S-rRNA gene for massively parallel sequencing-based monitoring of the planktonic eukaryote community. Molecular Ecology Resources 16: 402–414.

    CAS  PubMed  Google Scholar 

  • Tanaka, S., 1999. Notes on the Cladocera of Japan. 7. Family Moinidae Goulden, 1967. Member of Faculty Education Toyama University 53: 69–78 (in Japanese).

    Google Scholar 

  • Tanaka, M., 2004. The Lakes in Japan II. Nagoya University Press, Nagoya. (in Japanese).

    Google Scholar 

  • Tanaka, M. & N. Makita, 2017. An illustrated guide to Branchiopoda of Japan. Kyoritsu Shuppan Co., Ltd, Tokyo.

    Google Scholar 

  • Tanaka, S., A. Ohtaka & M. Nishino, 2004. Cladoceran fauna in littoral zones and Naikos (attached lakes or lagoons) of Lake Biwa, central Japan. Japanese Journal of Limnology 65: 167–179.

    Google Scholar 

  • Uchida, Y., 2003. Disasters on Irrigation Ponds and Conservation of Regional Environment in Japan. Kaiseisha Press, Otsu. (in Japanese).

    Google Scholar 

  • Usio, N., 2014. Environmentally Friendly Farming in Japan: Introduction. In Usio, N. & T. Miyashita (eds), Social-Ecological Restoration in Paddy-Dominated Landscapes. Springer, Tokyo: 69–86.

    Google Scholar 

  • Usio, N., M. Nakagawa, T. Aoki, S. Higuchi, Y. Kadono, M. Akasaka & N. Takamura, 2017. Effects of land use on trophic status and multi-taxonomic diversity in Japanese farm ponds. Agriculture, Ecosystems & Environment 247: 205–215.

    Google Scholar 

  • Xiang, X.-F., G.-H. Ji, S.-Z. Chen, G.-L. Yu, L. Xu, B.-P. Han, A. A. Kotov & H. J. Dumont, 2015. Annotated checklist of Chinese Cladocera (Crustacea: Branchiopoda). Part I. Haplopoda, Ctenopoda, Onychopoda and Anomopoda (families Daphniidae, Moinidae, Bosminidae, Ilyocryptidae). Zootaxa 3904: 1–27.

    PubMed  Google Scholar 

  • Yamamoto, A., W. Makino & J. Urabe, 2019. The taxonomic position of Asian Holopedium (Crustacea: Cladocera) confirmed by morphological and genetic analyses. Limnology. https://doi.org/10.1007/s10201-019-00585-z.

    Article  Google Scholar 

  • Yamazaki, M., Y. Hamada, N. Kamimoto, T. Momii, Y. Aiba, N. Yasuda, S. Mizuno, S. Yoshida & M. Kimura, 2003. Changes in the community structure of aquatic organisms after midseason drainage in the floodwater of Japanese paddy fields. Soil Science and Plant Nutrition 49: 125–135.

    Google Scholar 

  • Yamazaki, M., T. Ohtsuka, Y. Kusuoka, M. Maehata, H. Obayashi, K. Imai, F. Shibahara & M. Kimura, 2010. The impact of nigorobuna crucian carp larvae/fry stocking and rice-straw application on the community structure of aquatic organisms in Japanese rice fields. Fisheries Science 76: 207–217.

    CAS  Google Scholar 

  • Yang, J., X. Zhang, Y. Xie, C. Song, Y. Zhang, H. Yu & G. A. Burton, 2017. Zooplankton community profiling in a eutrophic freshwater ecosystem-Lake Tai basin by DNA metabarcoding. Scientific Reports 7: 1773.

    PubMed  PubMed Central  Google Scholar 

  • Yoon, S. M. & W. Kim, 1992. A taxonomic study of genus Moina (Branchiopoida, Cladocera, Moinidae) of Korea. Korean Journal of Systematic Zoology 8: 89–106.

    Google Scholar 

  • Young, H. S., D. J. McCauley, M. Galetti & R. Dirzo, 2016. Patterns, causes, and consequences of Anthropocene defaunation. Annual Review of Ecology and Systematics 47: 333–358.

    Google Scholar 

  • Zaret, T. M., 1980. Predation and Freshwater Communities. Yale University Press, New Haven and London.

    Google Scholar 

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Acknowledgements

We very gratefully acknowledge Seiki Igarashi, Akiyoshi Shinada, Hitoshi Kumagai, Mariko Nagano, Takuya Taira, Sayumi Yamada, Hajime Ohtsuki, Tsubasa Iwabuchi, Toru Koabari, Takeshi Yuhara, Natsumi Maruoka, Ryotaro Ichige, Takehiro Kazama, Megumi Nakagawa, Noriko Takamura, Hajime Yoshino, Fu-Lung Shih, and Osamu Miura for providing us with Moina specimens. Jotaro Urabe developed the source code for R to draw the map of Japan in Fig. 4, for which we are grateful. We also thank the anonymous referees, whose comments significantly improved our manuscript.

Funding

This study was supported by grants from the Japan Society for the Promotion of Science (16770011, 19770010, 23570015, 15H02380, 15K07211, and 18K06407) and the Ministry of the Environment, Japan (the Environment Research and Technology Development Fund, 4-1602), and the Water Resources Environment Technology Center (Nos. 2008-06 and 2018-03) and was performed under the cooperative research program of the Institute of Nature and Environmental Technology, Kanazawa University (Nos. 17030, 18020, and 19034).

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Makino, W., Machida, R.J., Okitsu, J. et al. Underestimated species diversity and hidden habitat preference in Moina (Crustacea, Cladocera) revealed by integrative taxonomy. Hydrobiologia 847, 857–878 (2020). https://doi.org/10.1007/s10750-019-04147-3

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