DOI QR코드

DOI QR Code

Identifying Potential Food Source through DNA Barcoding Analysis of Feces from Invasive Slug, Limax maximus (Linnaeus 1758) (Gastropoda: Pulmonata), in Republic of Korea

  • Received : 2024.07.05
  • Accepted : 2024.07.25
  • Published : 2024.08.01

Abstract

Unintentional dispersal of organisms has explosively increased due to expansion of human activities. Among introduced organisms, some organisms are categorized as invasive species because of their effects on environmental risk, economic loss, and human health. In 2023, a leopard slug (Limax maximus) was reported in Suwon, Republic of Korea. This slug was designated as a potential invasive species because a wide range of plant species were identified as food sources for this slug in its original habitats. However, it is difficult to investigate the ecological risk of this newly introduced slug in Republic of Korea. Therefore, the potential ecological risk from this newly introduced slug was estimated by meta-genome analyses of its feces. Through meta-genome analyses, 22 Families, 28 Genera, and 26 Species of land plants were identified. Among these 26 identified plant species, six economically important crops - squash (Cucurbita maxima), tomato (Solanum lycopersicum), potato (Solanum tuberosum), cowpea (Vigna unguiculata), rice (Oryza sativa), and oriental melon (Cucumis melo) - were identified. Therefore, leopard slugs potentially could cause economic losses in Republic of Korea. Further study is required to build a control strategy against leopard slugs.

Keywords

Acknowledgement

This work was supported by a grant of "Nationwide Survey of Non-native species in Republic of Korea (NIE-A-2024-12)" funded by the National Institute of Ecology, Republic of Korea.

References

  1. Barker, G.M. (1979). The introduced slugs of New Zealand (Gastropoda: Pulmonata). New Zealand Journal of Zoology, 6, 411-437. https://doi.org/10.1080/03014223.1979.10428382
  2. Barker, G.M. (1999). Naturalised terrestrial Stylommatophora (Mollusca: Gastropoda). Fauna of New Zealand, 38, 1-254. https://www.landcareresearch.co.nz/publications/fauna-of-new-zealand-series/
  3. Barker, G.M., and McGhie, R.A. (1984). The biology of introduced slugs (Pulmonata) in New Zealand 1. Introduction and notes on Limax maximus. New Zealand Entomologist, 8, 106-111. https://doi.org/10.1080/00779962.1984.9722482
  4. Berg, M.P., Kiers, E.T., Driessen, G., Van Der Heijden, M.A.R.C.E.L., Kooi, B.W., Kuenen, F., et al. (2010). Adapt or disperse: Understanding species persistence in a changing world. Global Change Biology, 16, 587-598. https://doi.org/10.1111/j.1365-2486.2009.02014.x
  5. Bradshaw, C.J., Leroy, B., Bellard, C., Roiz, D., Albert, C., Fournier, A., et al. (2016). Massive yet grossly underestimated global costs of invasive insects. Nature Communications, 7, 12986. https://doi.org/10.1038/ncomms12986 [PMID: 27698460 PMCID: PMC5059451]
  6. Buschmann, H., Keller, M., Porret, N., Dietz, H., and Edwards, P.J. (2005). The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. Functional Ecology, 19, 291-298. https://doi.org/10.1111/j.1365-2435.2005.00960.x
  7. Carlsson, N.O., and Lacoursiere, J.O. (2005). Herbivory on aquatic vascular plants by the introduced golden apple snail (Pomacea canaliculata) in Lao PDR. Biological Invasions, 7, 233-241. https://doi.org/10.1007/s10530-004-0741-4
  8. Choi, S., Sim, C., Kim, H.C., Choi, H.J., and Park, B.K. (2014). Natural infection of Crenosoma vulpis (Nematoda: Crenosomatidae) in an urban Korean dog. Korean Journal of Veterinary Research, 54, 127-129. http://doi.org/10.14405/kjvr.2014.54.2.127
  9. Cook, A., and Radford, D.J. (1988). The comparative ecology of four sympatric limacid slug species in Northern Ireland. Malacologia, 28, 131-146.
  10. Fuehrer, H.P., Morelli, S., Bleicher, J., Brauchart, T., Edler, M., Eisschiel, N., et al. (2020). Detection of Crenosoma spp., Angiostrongylus vasorum and Aelurostrongylus abstrusus in Gastropods in Eastern Austria. Pathogens, 9, 1046. https://doi.org/10.3390/pathogens9121046
  11. Gaitan-Espitia, J.D., Franco, M., Bartheld, J.L., and Nespolo, R.F. (2012). Repeatability of energy metabolism and resistance to dehydration in the invasive slug Limax maximus. Invertebrate Biology, 131, 11-18. https://doi.org/10.1111/j.1744-7410.2011.00255.x
  12. Hasegawa, K., Fukuda, H., and Ishikawa, J. (2009). Discovery of naturalized populations of the introduced slug, Limax maximus in Tsuchiura City, Ibaraki Prefecture, Japar. Chiribotan, 39, 101-105.
  13. Joe, S.M., and Daehler, C.C. (2008). Invasive slugs as underappreciated obstacles to rare plant restoration: Evidence from the Hawaiian Islands. Biological Invasions, 10, 245-255. https://doi.org/10.1007/s10530-007-9126-9
  14. Karlin, E.J., and Bacon, C. (1961). Courtship, mating, and egg-laying behavior in the Limacidae (Mollusca). Transactions of the American Microscopical Society, 80, 399-406. https://doi.org/10.2307/3223598
  15. Kerney, M.P., and Cameron, R.A.D. (1979). A field guide to the land snails of Britain and north-west Europe. Collins.
  16. Kim, H.G., and Lee, D.H. (2019). Review of the biology and ecology of a ragweed leaf beetle, Ophraella communa (Coleoptera: Chrysomelidae), which is a biological control agent of an invasive common ragweed, Ambrosia artemisiifolia (Asterales: Asteraceae). Biocontrol Science and Technology, 29, 185-200. https://doi.org/10.1080/09583157.2018.1540032
  17. Komatsu, W., and Saeki, I. (2022). Feeding habits of the exotic invasive slug Limax maximus: A basis for risk assessment of herbivory on forest and agricultural ecosystems. Management of Biological Invasions, 13(4), 644-658. https://doi.org/10.3391/mbi.2022.13.4.04
  18. Kozlowski, J. (2012). The significance of alien and invasive slug species for plant communities in agrocenoses. Journal of Plant Protection Research, 52, 67-76. https://doi.org/10.2478/v10045-012-0012-9
  19. Lee, J.S., and Min, D.K. (2002). A catalogue of molluscan fauna in Korea. The Korean Journal of Malacology, 18, 93-217.
  20. Li, H., Zhao, R., Pan, Y., Tian, H., and Chen, W. (2024). Insecticidal activity of Ageratina adenophora (Asteraceae) extract against Limax maximus (Mollusca, Limacidae) at different developmental stages and its chemical constituent analysis. PloS One, 19, e0298668. https://doi.org/10.1371/journal.pone.0298668 [PMID: 38625919 PMCID: PMC11020717]
  21. Lu, J., Rincon, N., Wood, D.E., Breitwieser, F.P., Pockrandt, C., Langmead, B., et al. (2022). Metagenome analysis using the Kraken software suite. Nature Protocols, 17, 2815-2839. https://doi.org/10.1038/s41596-022-00738-y [PMID: 36171387 PMCID: PMC9725748]
  22. McDonnell, R., Paine, T., and Gormally, M. (2009). Slugs: a guide to the invasive and native fauna of California. UCANR Publications.
  23. Meyer III, W.M., Ostertag, R., and Cowie, R.H. (2013). Influence of terrestrial molluscs on litter decomposition and nutrient release in a Hawaiian rain forest. Biotropica, 45, 719-727. https://doi.org/10.1111/btp.12057
  24. Nitz, B., Heim, R., Schneppat, U.E., Hyman, I., and Haszprunar, G. (2009). Towards a new standard in slug species descriptions: The case of Limax sarnensis Heim & Nitz n. sp. (Pulmonata: Limacidae) from the Western Central Alps. Journal of Molluscan Studies, 75, 279-294. https://doi.org/10.1093/mollus/eyp030
  25. Park, K., Kim, J., Park, S. G., Mun, C.G., Kim, S.H., Cho, Y., et al. (2024). First report of the leopard slug (Limax maximus), a new alien species in Republic of Korea. Proceedings of the National Institute of Ecology of the Republic of Korea, 5, 50-54. https://doi.org/10.22920/PNIE.2024.5.2.50
  26. Pimentel, D., Zuniga, R., and Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics, 52, 273-288. https://doi.org/10.1016/j.ecolecon.2004.10.002
  27. Roques, A., Rabitsch, W., Rasplus, J.Y., Lopez-Vaamonde, C., Nentwig, W., and Kenis, M. (2009). Alien terrestrial invertebrates of Europe. In Delivering Alien Invasive Species Inventories for Europe (DAISIE) (Eds.), Handbook of alien species in Europe (pp. 63-79). Springer. https://doi.org/10.1007/978-1-4020-8280-1_5
  28. Roth, B., and Sadeghian, P.S. (2006). Checklist of the land snails and slugs of California (p. 81). Santa Barbara Museum of Natural History.
  29. Rowson, B., Anderson, R., Turner, J.A., and Symondson, W.O. (2014). The slugs of Britain and Ireland: Undetected and undescribed species increase a well-studied, economically important fauna by more than 20%. PloS One, 9, e91907. https://doi.org/10.1371/journal.pone.0091907 [PMID: 24740519 PMCID: PMC3989179]
  30. Senanayake, S.N., Pryor, D.S., Walker, J., and Konecny, P. (2003). First report of human angiostrongyliasis acquired in Sydney. Medical Journal of Australia, 179, 430-431. http://doi.org/10.5694/j.1326-5377.2003.tb05623.x [PMID: 14558868]
  31. Sudhaus, W. (2018). Various evolutionary avenues of Nematoda to parasitism in Gastropoda. Soil Organisms, 90, 115-122. http://doi.org/10.25674/1yds-c108
  32. Wang, Q.P., Lai, D.H., Zhu, X.Q., Chen, X.G., and Lun, Z.R. (2008). Human angiostrongyliasis. The Lancet Infectious Diseases, 8, 621-630. http://doi.org/10.1016/S1473-3099(08)70229-9 [PMID: 18922484]