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Invasion, dispersion, population persistence and ecological impacts of a freshwater mussel (Limnoperna fortunei) in the Honshu Island of Japan

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Abstract

The freshwater mussels Limnoperna and Dreissena require the low advective flow conditions of large continental rivers so their larvae can develop sufficiently to settle before reaching the ocean in order to maintain their populations. However, these species have also invaded some island rivers with high advective flows. We integrated data for the invasion, distribution, genetic composition and ecological impacts of L. fortunei on the Honshu Island of Japan. Invasion route and mechanisms of dispersion and population persistence are detailed in non-continental rivers. The initial invasion and several of the dispersions of L. fortunei were closely related to the food culture of consuming freshwater clams in Japan. Other dispersions were most likely affected by headrace channels. Thus, population persistence depends on anthropogenic lentic environments such as reservoirs and channel networks as a nursing habitat for L. fortunei larvae. L. fortunei was often abundant near artificial habitats and less abundant in the lower segments of rivers. We also contrast the invasion processes of freshwater mussels in continental and non-continental rivers.

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References

  • Akamatsu F, Toda H, Okino T (2004) Food source of riparian spiders analyzed by using stable isotope ratios. Ecol Res 19:655–662

    Article  Google Scholar 

  • Akehoshi Y (2011) Study of ecological features and prevention of damage of Limnoperna fortunei in the irrigation institution. Rep Yahagi Riv Ins 15:55–63 (in Japanese)

    Google Scholar 

  • Aldridge DC (2010) Dreissena polymorpha in Great Britain: history of spread, impacts and control. In: The zebra mussel in Europe pp 79–91

  • Arianoutsou M, Bazos I, Delipetrou P, Kokkoris Y (2010) The alien flora of Greece: taxonomy, life traits and habitat preferences. Biol Invasions 12:3525–3549

    Article  Google Scholar 

  • Barnard C, Frenette JJ, Vincent WF (2003) Planktonic invaders of the St. Lawrence estuarine transition zone: environmental factors controlling the distribution of zebra mussel veligers. Can J Fish Aquat Sci 60:1245–1257

    Article  Google Scholar 

  • Belz CE, Darrigran G, Netto OSM et al (2012) Analysis of four dispersion vectors in inland waters: the case of the invading bivalves in South America. J Shellfish Res 31:777–784

    Article  Google Scholar 

  • Bidwell JR (2010) Range expansion of Dreissena polymorpha: a review of major dispersal vectors in Europe and North America. In: van der Velde G, Rajagopal S, de Vaate Bij A (eds) The zebra mussel in Europe. Margaraf Publishers, Leiden, pp 69–78

    Google Scholar 

  • Blackburn TM, Pyšek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339

    Article  PubMed  Google Scholar 

  • Bobeldyk AM, Bossenbroek JM, Evans-White MA et al (2005) Secondary spread of zebra mussel (Dreissena polymorpha) in coupled lake-stream systems. Ecoscience 15:339–346

    Article  Google Scholar 

  • Boltovskoy D, Correa N, Cataldo D, Sylvester F (2006) Dispersion and ecological impact of the invasive freshwater bivalve Limnoperna fortunei in the Rio de la Plata watershed and beyond. Biol Invasions 8:947–963

    Article  Google Scholar 

  • Boltovskoy D, Karatayev A, Burlakova L et al (2009) Significant ecosystem-wide effects of the swiftly spreading invasive freshwater bivalve Limnoperna fortunei. Hydrobiologia 636:271–284

    Article  Google Scholar 

  • Buchan LAJ, Padilla DK (1999) Estimating the probability of long-distance overland dispersal of invading aquatic species. Ecol Appl 9:254–265

    Article  Google Scholar 

  • Caraco NF, Cole JJ, Raymond PA et al (1997) Zebra mussel invasion in a large, turbid river: phytoplankton response to increased grazing. Ecology 78:588–602

    Article  Google Scholar 

  • Darrigran G (2002) Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biol Invasions 4:145–156

    Article  Google Scholar 

  • Darrigran G, Damborenea C (2011) Ecosystem engineering impact of Limnoperna fortunei in South America. Zool Sci 28:1–7

    Article  PubMed  Google Scholar 

  • Endo N, Sato K, Nogata Y (2009) Molecular based method for the detection and quantification of larvae of the golden mussel Limnoperna fortunei using real-time PCR. Plankton Benthos Res 4:125–128

    Article  Google Scholar 

  • Fukumoto H, Oguri Y, Osawa H et al (2010) Distributions of invasive species Limnoperna fortunei and its management in lower tone river. Proceedings of 14th Japanese society of ecology and civil engineering, pp 229–232 (in Japanese)

  • Hamada M (2010) History of invasion and present status of the golden mussel Limnoperna fortunei in Central Japan. Sessile Org 27:7–16 (in Japanese)

    Google Scholar 

  • Havel JE, Lee CE, Vander Zanden MJ (2005) Do reservoirs facilitate invasions into landscapes? Bioscience 55:518–525

    Article  Google Scholar 

  • Horvath TG, Lamberti GA (1999) Mortality of zebra mussel, Dreissena polymorpha, veligers during downstream transport. Freshw Biol 42:69–76

    Article  Google Scholar 

  • Horvath TG, Lamberti GA, Lodge DM, Perry WL (1996) Zebra mussel dispersal in lake-stream systems: source-sink dynamics? J N Am Benthol Soc 15:564–575

    Article  Google Scholar 

  • Ito K (2010) Spatial distribution and expansion process of the golden mussel Limnoperna fortunei in Kanto Region, Japan. Sessile Org 27:17–23 (in Japanese)

    Google Scholar 

  • Ito K (2011) Spatial distribution and status of the golden mussel, Limnoperna fortunei in Kanto region, Japan. Rep Yahagi Riv Ins 15:91–96 (in Japanese)

    Google Scholar 

  • Karatayev AY, Padilla DK, Minchin D, Boltovskoy D, Burlakova LE (2007) Changes in global economics and trade: the potential spread of exotic freshwater bivalves. Biol Invasions 9:161–180

    Article  Google Scholar 

  • Katayama M, Shimizu R, Matsumoto H (2005) The first record of Limnoperna fortunei (Bivalvia, Mytilidae) in Gunma. Field Biol 14:35–40 (in Japanese)

    Google Scholar 

  • Kato C, Iwata T, Nakano S et al (2003) Dynamics of aquatic insect flux affects distribution of riparian web-building spiders. Oikos 103:113–120

    Article  Google Scholar 

  • Kimura T (1994) The earliest record of Limnoperna fortunei (Dunker) from Japan. Chiribotan 25:34–35 (in Japanese)

    Google Scholar 

  • Kimura T, Inoue A, Kimura S et al (2011) Spatial distribution of an exotic mussel, Limnoperna fortunei, in Lake Biwa and connected waters in western Japan. Sessile Org 28:9–18 (in Japanese)

    Article  Google Scholar 

  • Kinzelbach R (1992) The main features of the phylogeny and dispersal of the zebra mussel Dreissena polymorpha. Limnologie aktuell 4:5–17

    Google Scholar 

  • Kraft CE, Sullivan PJ, Karatayev AY et al (2002) Landscape patterns of an aquatic invader: assessing dispersal extent from spatial distributions. Ecol Appl 12:749–759

    Article  Google Scholar 

  • Ling SD, Johnson CR, Mundy CN et al (2012) Hotspots of exotic free-spawning sex: man-made environment facilitates success of an invasive seastar. J Appl Ecol 49:733–741

    Article  Google Scholar 

  • Lozano SJ, Scharold JV, Nalepa TF (2001) Recent declines in benthic macroinvertebrate densities in Lake Ontario. Can J Fish Aquat Sci 58:519–529

    Article  Google Scholar 

  • Lucy FE, Minchin D, Boelens R (2008) From lakes to rivers: downstream larval distribution of Dreissena polymorpha in Irish river basins. Aquat Invasions 3:297–304

    Article  Google Scholar 

  • Mackie GL, Claudi R (2010) Monitoring and control of macrofouling Mollusks in fresh water systems. CRC Press, Florida

    Google Scholar 

  • Magara Y, Matsui Y, Goto Y, Yuasa A (2001) Invasion of the non-indigenous nuisance mussel, Limnoperna fortunei, into water supply facilities in Japan. J Water Supp 50:113–124

    Google Scholar 

  • Masuda O, Uchiyama R (2009) Encyclopedia of freshwater mollusks in Japan, part II. PISCES Publishers, Kanagawa (in Japanese)

  • Matsuda M, Uenish M (1992) A newly introduced mussel, Limnoperna lacustris (Martens) in Lake Biwa, Shiga prefecture, Japan (Mollusca; Mytilidae) Ann Rep Biwako-Bunkakan 10: 45. (in Japanese)

  • Matsuoka K, Nishi H (2010) Invasive alien species, Limnoperna fortunei discovered from the River Ure-gawa, Shinshiro City, Japan. Sci Rep Toyohashi Mus Nat Hist 20:1–4 (in Japanese)

    Google Scholar 

  • MC (1996) The distributions of the Limnoperna fortunei and Xenostrobus secures in the Kiso, Nagara and Ibi rivers. Report of the Chubu Regional Construction Bureau, Ministry of Construction, Dec. 1996 (in Japanese)

  • McMahon RF (1999) Invasive characteristics of the freshwater bivalve Corbicula fluminea. In: Claudi R, Leach JH (eds) Nonindigenous Freshwater Organisms Vectors, Biology, and Impacts. CRC Press, Florida, pp 315–343

    Google Scholar 

  • Minchin D, Moriarty C (1998) Distribution of the zebra mussel Dreissena polymorpha (Pallas, 1771) in Ireland, 1997. Ir Nat J 26:38–42

    Google Scholar 

  • MLIT (2006) Invasive alien species, Limnoperna fortunei discovered from Shin-Toyone dam (Tenryu river system). Rep National Census 2004 (Reservoir ver.), II-29 (in Japanese)

  • MLIT (2010) The distributions of the invaded macroinvertebrates, Limnoperna fortunei, Xenostrobus secures, Procambarus clarkia, Pacifastacus leniusculus and Pomacea canaliculata in Japan. (in Japanese) http://mizukoku.nilim.go.jp/ksnkankyo/mizukokuweb/download/pdf/gaiyo/h22/26_chumoku.pdf

  • MOF (2012) Trade Statistics of Japan. http://www.customs.go.jp/toukei/info/

  • Motoki M, Kume K, Nakajima I et al (2007) Distribution of freshwater mussel, Corbicula and aquatic plants in the irrigational canals in Kumagaya City, Saitama Prefecture. Chikyu-kannkyo-kennkyu 9:51–56 (in Japanese)

    Google Scholar 

  • Murakami T, Isaji C, Kuroda N et al (1992) Potamoplanktonic diatoms in the Nagara river; flora, population dynamics and influences on water quality. Jap J Limnol 53:1–12

    Article  CAS  Google Scholar 

  • Naka S (2008) Record of Limnoperna fortunei in the Sawachi River. Nat Hist Mie 76:5 (in Japanese)

    Google Scholar 

  • Nakai K (1995) Invasion of Limnoperna fortunei into water intake facilities of the three rivers, Kiso River. Nagara River and Ibi River. Venus 54:89 (in Japanese)

    Google Scholar 

  • Nakai K (2001) Invasion of golden mussel into Japan. In: Kajihara T, Okutani T (eds) Black Inveders. Kouseisha-kouseikaku, Tokyo, pp 71–85 (in Japanese)

    Google Scholar 

  • Nakamura M (2000) The fisheries of clam in Japan. Tatara-shobo, Yonago

    Google Scholar 

  • Nakano D (2013) Biological Invasion of mollusk in Japan. In: Nakamura F (ed) River ecology. Kodan-sha, Tokyo, pp 288–296 (in Japanese)

    Google Scholar 

  • Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. PNAS 98:166–170

  • Nakano D, Strayer DL (2014) Biofouling animals in freshwater: biology, impacts and ecosystem engineering. Front Ecol Environ 12:167–175

  • Nakano D, Yamamoto M, Okino T (2005) Ecosystem engineering by larvae of net-spinning stream caddisflies creates a habitat on the upper surface of stones for mayfly nymphs with a low resistance to flows. Freshw Biol 50:1492-1498

  • Nakano D, Kobayashi T, Sakaguchi I (2010) Differences in larval dynamics of golden mussel Limnoperna fortunei between dam reservoirs with and without an aeration system. Landsc Ecol Eng 6:53–60

  • Nakano D, Kobayashi T, Sakaguchi I (2012) Changes in the drift and the settlement of the freshwater mussel Limnoperna fortunei along a headrace channel. Water Sci Tech 65:426–433

  • Nalepa TF, Schloesser DW (1993) Zebra mussel—biology, impacts, and control. Lewis

  • Nalepa TF, Hartson DJ, Fanslow DL et al (1998) Declines in benthic macroinvertebrate populations in southern Lake Michigan, 1980-1993. Can J Fish Aquat Sci 55:2402–2413

    Article  Google Scholar 

  • Nishimura T, Habe T (1987) Contamination of chinese freshwater bivalves in imported freshwater clams. Chiribotan 18:110–111 (in Japanese)

    Google Scholar 

  • Ohtaka A, Narita T, Kamiya T et al (2011) Composition of aquatic invertebrates associated with macrophytes in Lake Tonle Sap, Cambodia. Limnology 12:137–144

    Article  Google Scholar 

  • Pollux BJA, van der Velde G, de Vaate Bij A (2010) A perspective on global spread of Dreissena polymorpha: a review on possibilities and limitations. In: van der Velde G, Rajagopal S, de Vaate Bij A (eds) The zebra mussel in Europe. Backhuys Publishers, Leiden, pp 45–58

  • Rehmann CR, Stoeckel JA, Schneider DW (2003) Effect of turbulence on the mortality of zebra mussel veligers. Can J Zool 81:1063–1069

    Article  Google Scholar 

  • Ricciardi A, Whoriskey FG, Rasmussen JB (1997) The role of the zebra mussel (Dreissena polymorpha) in structuring macroinvertebrate communities on hard substrata. Can J Fish Aquat Sci 54:2596–2608

    Article  Google Scholar 

  • Sakamoto H, Nishi H, Matsuoka K (2013) Records of freshwater fishes, molluscs and sponge from irrigation ponds of Toyohashi City, Aichi Prefecture, central Japan between 2010 and 2011. Sci Rep Toyohashi Mus Nat Hist 23:39–44 (in Japanese)

    Google Scholar 

  • Sakamoto H, Nishi H, Matsuoka K (2014) Records of freshwater fishes, molluscs and sponge from irrigation ponds of Toyohashi City, Aichi Prefecture, central Japan in 2013. Sci Rep Toyohashi Mus Nat Hist 24:25–30 (in Japanese)

    Google Scholar 

  • Shiragane A (2005) Golden mussel, Limnoperna fortunei discovered from Yahagi River. Rio 80(81):4 (in Japanese)

    Google Scholar 

  • Speirs DC, Gurney WSC (2001) Population persistence in rivers and estuaries. Ecology 82:1219–1237

    Article  Google Scholar 

  • Stoeckel JA, Schneider DW, Soeken LA et al (1997) Larval dynamics of a riverine metapopulation: implications for zebra mussel recruitment, dispersal, and control in a large-river system. J N Am Benthol Soc 16:586–601

  • Stoeckel JA, Rehmann CR, Schneider DW et al (2004) Retention and supply of zebra mussel larvae in a large river system: importance of an upstream lake. Freshw Biol 49:919–930

  • Strayer DL (2009) Twenty years of zebra mussels: lessons from the mollusk that made headlines. Front Ecol Environ 7:135–141

    Article  Google Scholar 

  • Strayer DL, Malcom HM (2007) Effects of zebra mussels (Dreissena polymorpha) on native bivalves: the beginning of the end or the end of the beginning? J N Am Benthol Soc 26:111–122

    Article  Google Scholar 

  • Sugiyama N (2013) Distribution of golden mussel, Limnoperna fortunei, in western Gunma Prefecture (2012). Bull Gunma Mus Nat Hist 17:151–154 (in Japanese)

    Google Scholar 

  • Sunoh N (2006) Records of golden mussel in Lake Kasumigaura. Rep Ibaraki Pref Inland Fish Exp Sta 40:79 (in Japanese)

  • Takao A, Negishi JN, Nunokawa M, Gomi T, Nakahara O (2006) Potential influences of a net-spinning caddisfly (Trichoptera: Stenopsyche marmorata) on stream substratum stability in heterogeneous field environments. J N Am Benthol Soc 25:545–555

    Article  Google Scholar 

  • Tanida K (1995) Habitat creation and modification by stream benthos: Trichoptera as key-species. In: Takemon Y (ed) Ecology of Habitat. Tokyo, Heibon-sha, pp 95–128 (in Japanese)

    Google Scholar 

  • Tominaga A, Goka K, Kimura T et al (2009) Genetic structure of Japanese introduced populations of the Golden Mussel, Limnoperna fortunei, and the estimation of their range expansion process. Biodiversity 10:61–66

    Article  Google Scholar 

  • Uchida S, Shiragane A, Uchida A et al (2007) A mass death after a high abundance of the invasive mussel, Limnoperna fortunei, in the Yahagi River, Honshu, Japan. Rep Yahagi Riv Ins 11:35–46 (in Japanese)

    Google Scholar 

  • van der Velde G, Ragagopal S, de Vaate Bij A (2010) From zebra mussels to quagga mussels: an introduction to the Dreissenidae. In: van der Velde G, Ragagopal S, de Vaate Bij A (eds) The Zebra Mussel in Europe. Backhuys Publishers, Leiden, pp 1–10

  • Xu M, Wang Z, Duan X et al. (2009) Ecological measures of controlling invasion of golden mussel (Limnoperna fortunei) in water transfer systems. Proceedings of 33rd IAHR Congress: Water Engineering for a Sustainable Environment, pp 1609–1616

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Acknowledgments

We thank David L. Strayer, Katsuki Nakai, Yasuyuki Nogata, Rikyu Matsuki and Isamu Sakaguchi for their helpful advice on this study. We appreciate the associate editor and two anonymous reviewers giving critical and helpful comments on an earlier draft of our manuscript.

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Authors and Affiliations

  1. Environmental Science Research Laboratory, Central Research Institute of Electric Power Industry (CRIEPI), 1646 Abiko, Chiba, 270-1194, Japan

    Daisuke Nakano, Noriyuki Endo, Ai Fujinaga & Takuya Kobayashi

  2. Cary Institute of Ecosystem Studies, Millbrook, NY, USA

    Daisuke Nakano

  3. Department of Ecosystem Studies, School of Environmental Science, University of Shiga Prefecture, 2500 Hassaka, Hikone, Shiga, 522-8533, Japan

    Takashi Baba & Misako Urabe

  4. Aqua Restoration Research Center (ARRC), Public Works Research Institute, Kasada-machi, Kawashima, Kakamigahara, Gifu, 501-6021, Japan

    Shigeya Nagayama

  5. Toyota Yahagi River Institute, 2-19 Nishi-machi, Toyota, Aichi, 471-0025, Japan

    Asako Uchida & Akiko Shiragane

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  1. Daisuke Nakano
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  2. Takashi Baba
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  3. Noriyuki Endo
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Correspondence to Daisuke Nakano.

Appendix

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Table 3 List of locations and appeared haplotypes of L. fortunei samples for genetic analysis
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Nakano, D., Baba, T., Endo, N. et al. Invasion, dispersion, population persistence and ecological impacts of a freshwater mussel (Limnoperna fortunei) in the Honshu Island of Japan. Biol Invasions 17, 743–759 (2015). https://doi.org/10.1007/s10530-014-0765-3

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