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Predator-driven biotic resistance and propagule pressure regulate the invasive apple snail Pomacea canaliculata in Japan

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Abstract

Species richness in local communities has been considered an important factor determining the success of invasion by exotic species (the biotic resistance hypothesis). However, the detailed mechanisms, especially the role of predator communities, are not well understood. We studied biotic resistance to an invasive freshwater snail, Pomacea canaliculata, at 31 sites in an urban river basin (the Yamatogawa) in western Japan. First, we studied the relationship between the richness of local animal species and the abundance of P. canaliculata, demonstrating a negative relationship, which suggests that the intensity of biotic resistance regulates local snail populations. This pattern was due to the richness of native predator communities rather than that of introduced species or non-predators (mainly competitors of the apple snail). Local snail abundance was also affected by immigration of snails from nearby rice fields (i.e. propagule pressure), where few predators occur. Second, we assessed short-term predation pressure on the snail by means of a tethering experiment. Predation pressure was positively correlated with the number of individual predators and negatively correlated with snail abundance. The introduced crayfish Procambarus clarkii was responsible for the variance in predation pressure. These results indicate that the predator community, composed of both native and introduced species, is responsible for resistance to a novel invader even in a polluted urban river.

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References

  • Altieri AH, van Wesenbeeck BK, Bertness MD, Silliman BR (2010) Facilitation cascade drives positive relationship between native biodiversity and invasion success. Ecology 91:1269–1275

    Article  PubMed  Google Scholar 

  • Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156

    Google Scholar 

  • Byers JE, Noonburg EG (2003) Scale dependent effects of biotic resistance to biological invasion. Ecology 84:1428–1433

    Article  Google Scholar 

  • Carlsson NOL, Brönmark C, Hansson L-A (2004) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580

    Article  Google Scholar 

  • Carlsson NOL, Sarnelle O, Strayer DL (2009) Native predators and exotic prey -an acquired taste? Front Ecol Environ 7:525–532

    Article  Google Scholar 

  • Carlsson NOL, Jeschke JM, Holmqvist N, Kindberg J (2010) Long-term data on invaders: when the fox is away, the mink will play. Biol Invas 12:633–641

    Article  Google Scholar 

  • Correia AM, Bandeira N, Anastacio PM (2005) Predator-prey interactions of Procambarus clarkii with aquatic macroinvertebrates in single and multiple prey systems. Acta Oecol 28:337–343

    Article  Google Scholar 

  • Cowie RH (2002) Apple snails as agricultural pests: their biology, impacts and management. In: Barker GM (ed) Molluscs as crop pests. CABI Publishing, Wallingford, pp 145–192

    Chapter  Google Scholar 

  • D’Antonio C, Levine J, Thomsen M (2001) Ecosystem resistance to invasion and the role of propagule supply: a California perspective. J Mediterran Ecol 2:233–245

    Google Scholar 

  • deRivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376

    Article  Google Scholar 

  • Dumont CP, Gaymer CF, Thiel M (2011) Predation contributes to invasion resistance of benthic communities against the non-indigenous tunicate Ciona intestinalis. Biol Invas 13:2023–2034

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasion by animals and plants. Methuen Press, London

    Google Scholar 

  • Fang L, Wong PK, Lin L, Lan C, Qiu J-W (2010) Impact of invasive apple snails in Hong Kong on wetland macrophytes, nutrients, phytoplankton and filamentous algae. Freshw Biol 55:1191–1204

    Article  CAS  Google Scholar 

  • Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Von Holle B (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17

    Article  PubMed  CAS  Google Scholar 

  • Harvey BC, White JL, Nakamoto RJ (2004) An emergent multiple predator effect may enhance biotic resistance in a stream fish assemblage. Ecology 85:127–133

    Article  Google Scholar 

  • Hayes KA, Joshi RC, Thiengo SC, Cowie RH (2008) Out of South America: multiple origins of non-native apple snails in Asia. Divers Dist 14:701–712

    Article  Google Scholar 

  • Hunt CE, Yamada SB (2003) Biotic resistance experienced by an invasive crustacean in a temperate estuary. Biol Invas 5:33–43

    Article  Google Scholar 

  • Ichinose K, Wada T, Yusa Y, Kubota T (2000) Influence of habitat differences brought about by environmental changes on the densities of adults and eggs of Pomacea canaliculata. Kyushu Pl Prot Res 46:78–84 (in Japanese with English abstract)

    Article  Google Scholar 

  • Jiang L, Morin PJ (2004) Productivity gradients cause positive diversity-invasibility relationships in microbial communities. Ecol Lett 7:1047–1057

    Article  Google Scholar 

  • Joshi RC, Sebastian LS (2006) Global advances in ecology and management of golden apple snails. Philippine Rice Res Inst, Nueva Ecija, Philippines

    Google Scholar 

  • Kwong KL, Wong PK, Lau SSS, Qiu JW (2008) Determinants of the distribution of apple snails in Hong Kong two decades after their initial invasion. Malacologia 50:293–302

    Article  Google Scholar 

  • Lake PS, O’Dowd DJ (1991) Red crabs in rain forest, Christmas Island: biotic resistance to invasion by an exotic snail. Oikos 62:25–29

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Leprieur F, Beauchard O, Blanchet S, Oberdorff T, Brosse S (2008) Fish invasions in the world’s river systems: when natural processes are blurred by human activities. PLoS Biol 6:404–410

    CAS  Google Scholar 

  • Levine JM (2000) Species diversity and biological invasions: relating local process to community pattern. Science 288:852–854

    Article  PubMed  CAS  Google Scholar 

  • Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15–26

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trend Ecol Evol 20:223–228

    Article  Google Scholar 

  • Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536

    Article  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species, updated and reprinted version: November 2004. The World Conservation Union (IUCN). Auckland. http://www.issg.org/publications.htm#worst100. Accessed 29 April 2011

  • Maezono Y, Miyashita T (2004) Impact of exotic fish removal on native communities in farm ponds. Ecol Res 19:263–267

    Article  Google Scholar 

  • Martín PR, Estebenet AL, Cazzaniga NJ (2001) Factors affecting the distribution of Pomacea canaliculata (Gastropoda: Ampullariidae) along its southernmost natural limit. Malacologia 43:13–23

    Google Scholar 

  • Ministry of Land, Infrastructure, Transport and Tourism of Japan (2010) Water quality of the major rivers of Japan, 2009. http://www.mlit.go.jp/river/toukei_chousa/kankyo/kankyou/suisitu/index.html. Accessed 29 April 2011 (in Japanese)

  • Osaka Museum of Natural History (2007) Yamatogawa no shizen. Tokai University Press, Kanagawa, Japan (in Japanese)

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute (2008) JMP version 8.0. SAS Institute, Cary

    Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invas 1:21–32

    Article  Google Scholar 

  • Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579

    Article  PubMed  CAS  Google Scholar 

  • Stohlgren TJ, Jarnevich C, Chong GW, Evengelista PH (2006) Scale and plant invasions: a theory of biotic acceptance. Preslia 78:405–426

    Google Scholar 

  • Sugiura N (1978) Further analysts of the data by akaike’ s information criterion and the finite corrections. Comm Stat Theor Meth 7:13–26

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  PubMed  CAS  Google Scholar 

  • Urban MC, Skelly DK, Burchsted D, Price W, Lowry S (2006) Stream communities across a rural-urban landscape gradient. Divers Dist 12:337–350

    Article  Google Scholar 

  • Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218

    Article  Google Scholar 

  • Wada T, Matsukura K, Yoshida K, Yamanishi Y, Yusa Y (2009) Apple snails Pomacea canaliculata escaping from a paddy field into an irrigation canal in South Japan. Kyushu Pl Prot Res 55:93–98 (in Japanese with English abstract)

    Article  Google Scholar 

  • Yonekura R, Kita M, Yuma M (2004) Species diversity in native fish community in Japan: comparison between non-invaded and invaded ponds by exotic fish. Ichthyol Res 51:176–179

    Article  Google Scholar 

  • Yoshida K, Hoshikawa K, Wada T, Yusa Y (2009) Life cycle of the apple snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) inhabiting Japanese paddy fields. Appl Entomol Zool 44:465–474

    Article  Google Scholar 

  • Yoshie H, Yusa Y (2008) Effects of predation on the exotic freshwater snail Pomacea canaliculata (Caenogastropoda: Ampullariidae) by the indigenous turtle Chinemys reevesii (Testudines: Geoemydidae). Appl Entomol Zool 43:475–482

    Article  Google Scholar 

  • Yoshie H, Yusa Y (2011) Indirect interactions in a rice ecosystem: density dependence and the interplay between consumptive and non-consumptive effects of predators. Freshw Biol 56:302–310

    Article  Google Scholar 

  • Yusa Y (2006) Predators of the introduced apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae): their effectiveness and utilization in biological control. In: Joshi RC, Sebastian LS (eds) Global advances in ecology and management of golden apple snails. Philippine Rice Res Inst, Nueva Ecija, Philippines, pp 345–361

    Google Scholar 

  • Yusa Y, Kai S, Ando S, Shiozaki N, Wada T (2001) Predatory potential of the common carp, Cyprinus carpio L., on the apple snail, Pomacea canaliculata (Lamarck), in the field. Kyushu Pl Prot Res 47:69–72 (in Japanese with English abstract)

    Article  Google Scholar 

  • Yusa Y, Sugiura N, Wada T (2006) Predatory potential of freshwater animals on an invasive agricultural pest, the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae) in southern Japan. Biol Invas 8:137–147

    Article  Google Scholar 

Download references

Acknowledgments

We thank Drs. Keiji Wada, Hiroaki Sato, Hisao Ishii, Kenji Hamazaki, and two anonymous reviewers for their valuable comments. We also thank members of the Laboratory of Population and Community Ecology at Nara Women’s University for discussion and assistance.

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Author notes

  1. Yoko Yamanishi

    Present address: Idea Consultants, 2-2-2 Hayabuchi, Tsuzuki, Yokohama, 224-0025, Japan

Authors and Affiliations

  1. Faculty of Science, Nara Women’s University, Kitauoya-nishi, Nara, 630-8506, Japan

    Yoko Yamanishi & Yoichi Yusa

  2. National Agricultural Research Center for Kyushu-Okinawa Region, Suya 2421, Koshi, 861-1192, Japan

    Kazuhiro Yoshida

  3. Toyohashi University of Technology, 1-1 Hibarigaoka, Tempaku, Toyohashi, Aichi, 441-8580, Japan

    Noriomi Fujimori

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  1. Yoko Yamanishi
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  2. Kazuhiro Yoshida
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  4. Yoichi Yusa
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Correspondence to Yoichi Yusa.

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Yamanishi, Y., Yoshida, K., Fujimori, N. et al. Predator-driven biotic resistance and propagule pressure regulate the invasive apple snail Pomacea canaliculata in Japan. Biol Invasions 14, 1343–1352 (2012). https://doi.org/10.1007/s10530-011-0158-9

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