Korean Journal of Environment and Ecology (한국환경생태학회지)

Korean Society of Environment and Ecology (한국환경생태학회)
권호 표지
DOI QR코드

DOI QR Code

Distribution Status of Invasive Alien Species (Procambarus clarkii (Girard, 1852)) Using Biomonitoring with Environmental DNA in South Korea

생물모니터링 및 환경유전자(eDNA)를 이용한 침입외래종 미국가재(Procambarus clarkii)의 한국분포 현황

  • Received : 2022.02.25
  • Accepted : 2022.06.23
  • Published : 2022.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

Biomonitoring of an invasive alien crayfish species, Procambarus clarkii (Girard, 1852), was performed from February to October 2021, along with environmental DNA analysis, at five locations including Wanju-gun, Hampyeong-gun, Naju-si, Gurye-gun, and Cheongju-si. For the investigation, an umbrella-shaped trap for adults and a hand net for young crayfish were used, and 8 to 10L of freshwater was collected for eDNA analysis. The current status and past distributional records of crayfish in Korea were analyzed along with benthic macroinvertebrates at each survey site. As a result of the investigation, a total of 122 individuals were identified, and Hampyeong-gun recorded the largest number of populations with 59 individuals (48.36%) and the highest environmental DNA (eDNA). The frequency of appearance of P. clarkii was highest in May. The ratio of females to males was 21:5, and the body size was 72.2±21.1mm for female, 80.5±15.6mm for male, and 25.3±9.8mm for young crayfish. P. clarkii introduced into Korea is mainly spreading in the southwest region and it has not been observed in Seoul where there had been a record of appearance in the past. No external symbiosis (Branchiobdellida) of P. clarkii has been identified, and P. clarkii that has appeared in Korea was presumed to be imported from Japan. There are more than eight kinds of exotic crayfish distributed in Korea, and among them, the marbled crayfish (P. virginalis) was identified as a harmful species to the ecosystem of Korea by the Ministry of Environment in 2021. The identified species of benthic macroinvertebrates inhabiting the survey area where P. clarkii has appeared were 69 belonging to 39 families, 15 orders, five classes, and three phyla. Among them, Odonata were the most abundant (16 spp.; 24.62%), followed by Coleoptera (11 spp.; 16.92%) and Hemiptera (11 spp.; 16.92%). In the survey area, one Korean endemic species (Rhoenanthus coreanus), one species (Helophorus auriculatus) classified as Near Threatened (NT) on the Korean Red List, and six species of Crustaceans appeared. In the functional feeding group, the predators appeared predominantly while in habitat oriented group, the climbers appeared to be abundant. It was confirmed that P. clarkii in the survey area prefers an area rich in aquatic vegetation with waterside vegetation, and has high resistance to turbid water quality. The omnivore invader P. clarkii is expected to maintain a competitive relationship with carnivorous benthic macroinvertebrates that are predominant in the same species, and is expected to continue to generate ecosystem disturbance along the food chains.

국내 침입외래종 미국가재(Procambarus clarkii)의 생물모니터링을 환경유전자 분석과 함께 2021년 2월부터 10월까지 완주군, 함평군, 나주시, 구례군 청주시, 5지점에서 수행하였다. 조사방법은 우산형통발과 둥근뜰채를 이용하였으며, eDNA 분석을 위해 8~10 L의 물을 채수하였다. 조사지 내의 동소종인 저서성 대형무척추동물과 함께 과거 분포기록 및 국내 가재류 유통 현황도 분석하였다. 조사결과 미국가재는 총 122개체가 확인되었으며, 함평군에서 59개체(48.36%)로 가장 많은 개체수와 높은 환경유전자(eDNA)가 검출되었고 계절상 5월달에 출현 빈도가 가장 높았다. 암컷과 수컷의 비율은 21:5로 암컷이 우세하였으며, 크기는 암컷이 72.2±21.1 mm, 수컷이 80.5±15.6 mm, 어린개체가 25.3±9.8 mm이었다. 국내에 유입된 미국가재는 남서쪽 지역을 중심으로 확산되고 있는 것으로 파악되었으며, 과거에 출현 기록이 있는 서울지역에서는 확인되지 않았다. 미국가재에 외부공생하는 끈거머리지렁이류는 확인되지 않았으며, 국내의 출현한 미국가재는 일본에서부터 수입된 개체로 추정되었다. 국내에서 유통되고 있는 외래 가재류는 8종 이상이었으며, 이중 마블가재(Procambarus virginalis)는 2021년에 환경부에서 유입주의 생물로 지정된 종으로 파악되었다. 미국가재 조사지역 일대에 서식하는 저서성 대형무척추동물은 총 3문 5강 39과 69종이 출현하였으며, 잠자리목이 24.62%, 딱정벌레목과 노린재목이 각각 16.92%로 우세하게 나타났다. 이 중 한반도고유종 1종, 적색목록 범주의 준위협(NT)으로 구분되는 1종, 갑각류는 총 6종이 출현하였다. 섭식기능군에서는 잡아먹는무리가 서식기능군에서는 기어오르는무리가 전체적으로 우세하여 출현하였다. 조사지역 내의 미국가재는 수초와 수변부 식생이 풍부한 지역을 선호하며, 수질이 탁한 곳에서도 내성이 강한 것으로 분석되었다. 잡식성인 미국가재는 동소종에서 우세하게 출현하는 육식성 저서생물과 상호 경쟁관계를 유지할 것으로 보이며, 먹이사슬에 따른 생태계 교란이 지속적으로 일어날 것으로 판단된다.

Keywords

Acknowledgement

본 논문은 환경부의 재원으로 국립생태원의 지원을 받아 수행하였습니다(과제번호 NIE-법정연구-2022-09)

References

  1. Alcorlo, P. and A. Baltanas(2013) The trophic ecology of the red swamp crayfish (Procambarus clarkii) in Mediterranean aquatic ecosystems: A stable isotope study. Limnetica 32(1): 121-138.
  2. Bustin, S.A., V. Benes, J.A. Garson, J. Hellemans, J. Huggett, M. Kubista, R. Mueller, T. Nolan, M.W. Pfaffl, G.L. Shipley and J. Vandesompele(2009) The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55(4): 611-622. https://doi.org/10.1373/clinchem.2008.112797
  3. Choi, J.Y., S.K. Kim, J.C. Kim and J.H. Yun(2021) Invasion and Dispersion of the Exotic Species Procambarus clarkii (Decapoda Cambaridae) in Yeongsan River Basin, South Korea. Animals 11: 3489. https://doi.org/10.3390/ani11123489
  4. Correia, A.M. and O. Ferreira(1995) Burrowing behavior of the introduced red swamp crayfish Procambarus clarkii (Decapoda: Cambaridae) in Portufal. Journal of Crustacean Biology 15(2): 248-257. https://doi.org/10.2307/1548953
  5. Correia, A.M. and P.M. Anastacio(2008) Shifts in aquatic macroinvertebrate biodiversity associated with the presence and size of an alien crayfish. Ecological Research 23: 729-734. https://doi.org/10.1007/s11284-007-0433-5
  6. Correia, A.M.(2002) Niche breadth and trophic diversity: Feeding behaviour of the red swamp crayfish (Procambarus clarkii) towards environmental availability of aquatic macroinvertebrates in a rice field (Portugal). Acta Oecologia 23: 421-429. https://doi.org/10.1016/S1146-609X(02)01166-9
  7. Delsinne, T., R.M. Lafontaine, R.C. Beudels and H. Robert(2013) Risk analysis of the Louisiana Crayfish Procambarus clarkii (Girard, 1852).-Risk analysis report of non-native organisms in Belgium from the Royal Belgian Institute of Natural Sciences for the Federal Public Service Health, Food Chain Safety and Environment, 63pp.
  8. Geiger, W., P. Alcorlo, A. Baltanas and C. Montes(2005) Impact of an introduced Crustacean on the trophic webs of Mediterranean wetlands. Biological Invasions 7: 49-73. https://doi.org/10.1007/s10530-004-9635-8
  9. Gelder, S.R. and A. Ohtaka(2000) Description of a new species and a redescription of Cirrodrilus aomorensis (Yamaguchi, 1934) with a detailed distribution of the branchiobdellidans (Annelida: Clitellata) in northern Honshu, Japan. Proceedings of Biological Society of Washington 113(3): 633-643.
  10. Gherardi, F. and S. Barbaresi(2000) Invasive crayfish: Activity patterns of Procambarus clarkii in the rice fields of the Lower Guadalquivir (Spain). Archiv fur Hydrobiologie 150: 153-168. https://doi.org/10.1127/archiv-hydrobiol/150/2000/153
  11. Haubrock, P.J., A.F. Inghilesi, G. Mazza, M. Bendoni, L. Solari and E. Tricarico(2019) Burrowing activity of Procambarus clarkii on levees: Analysing behaviour and burrow structure. Wetlands Ecol Manage 27: 497-511. https://doi.org/10.1007/s11273-019-09674-3
  12. Hobbs, H.H.III, J.P. Pass and J.V. Huner(1989) A review of global crayfish introductions with particular emphasis on two North American species (Decapoda, Cambaridae). Crustaceana 56: 299-316. https://doi.org/10.1163/156854089X00275
  13. Invasive Alien Species Research Team(2021) Monitoring of Invasive Alien Species Designated by the Act on the Conservation and Use of Biological Diversity. National Institute of Environmental Research, Incheon, Korea, 348pp. (in Korean)
  14. Jung, J.H., M.S. Kim, D.H. Ahn and G.S. Min(2009) Growth Rate, Sex Ratio, Age Structure and Mating Period of Korean Crayfish Cambaroides similis Natural Population. Journal of Aquaculture 22(1): 16-22. (in Korean with English abstract)
  15. Jung, K.S.(2011) Odonata Larvae of Korea. Nature and Ecology, Seoul, 399pp. (in Korean)
  16. Jung, S.W., Y.C. Cho and H.G. Lee(2017) Community Characteristics and Biological Quality Assessment on Benthic Macroinvertebrates of Bongseonsa Stream in Gwangneung Forest, South Korea. Korean Journal of Environmental Ecology 31(6): 508-519. (in Korean with English abstract) https://doi.org/10.13047/KJEE.2017.31.6.508
  17. Kawai, T. and Y. Kobayashi(2006) Origin and current distribution of the alien Crayfish, Procambarus clarkii (Girard, 1852) in Japan. Crustaceana 78(9): 1143-1149. https://doi.org/10.1163/156854005775361034
  18. Kawai, T.(2017) A Review of the Spread of Procambaus clarkii across Japan and its Morphological Observations. Freshwater Crayfish 23(1): 41-53. https://doi.org/10.5869/fc.2017.v23-1.41
  19. Kawai, T., H. Chokki, JCC(Japan Crayfish Club), K. Nakata, T. Kobayashi and K. Arai(2003) Introduction and distribution of Procambarus clarkii in Japan. Journal of Natural Histroy of Aomori 8: 1-8. (in Japanese)
  20. Kim, J.M., J.H. Kil, W.M. Kim, J.H. Seo, H.C. Shin, W.H. Kim, J.Y. Ban, U.G. Kim, J.Y. Lee, G.S. Go, S.H. Park and H.S. Oh(2006) A Study of Detailed Survey on Invasive Alien Species in Korea and Designation of Invasive Alien Species in Foreign Countries. National Institute of Environmental Research, Incheon, Korea, 408pp. (in Korean with English abstract)
  21. Kim, M.C., S.P. Chun and J.K. Lee(2013) Invertebrates in Korean Freshwater Ecosystems. Geobook, Seoul, 483pp. (in Korean)
  22. Kim, S.H., H.J. Baek and G.B. Yang(2019) Report on Settlement of Alien Species Red Swamp Crawfish (Procambarus clarkii) in Korea. Korean Journal of Ecology and Environment 52(4): 333-339. (in Korean with English abstract) https://doi.org/10.11614/KSL.2019.52.4.333
  23. Kim, S.H., H.J. Baek, G.B. Yang, S.J. Kwon, Y.C. Jeon, S.P. Cheon, H.Y. Kwon, Y.J. Kwon, S.M. Jeong, D.H. Ahn, J.G. Kim, H.S. Shin, M.G. Oh, S.W. Jung and C.W. Park(2019) Survey of American Freshwater Crayfish Distribution in Korea Water System. National Institute of Ecology, Seocheon, Korea, 38pp. (in Korean with English abstract)
  24. King, A.C., R. Krieg, A. Weston and A.K. Zenker(2022) Using eDNA to simultaneously detect the distribution of native and invasive crayfish within an entire country. Journal of Environmental Management 302: 113929.
  25. Kwak, I.S., Y.S. Park and K.H. Chang(2021) Application and Utilization of Environmental DNA Technology for Biodiversity in Water Ecosystems. Korean Journal of Ecology and Environment 54(3): 151-155. (in Korean with English abstract) https://doi.org/10.11614/KSL.2021.54.3.151
  26. Kwon, O.K.(1990) Illustrated encyclopedia of fauna & flora of Korea vol.32 Mollusca(I). Ministry of Education Republic of Korea, 446pp. (in Korean)
  27. Kwon, S.J., Y.C. Jun and J.H. Park(2013) Benthic Macroinvertebrates. Nature and Ecology, Seoul, 791pp. (in Korean)
  28. Lee, D.S. and Y.S. Park(2019) Evaluation of Potential Distribution Area of the Red Swamp Crayfish (Procambarus clarkia) in South Korea. Korean Journal of Ecology and Environment 52(4): 340-347. (in Korean with English abstract) https://doi.org/10.11614/KSL.2019.52.4.340
  29. Li, Y., X. Guo, L. Chen, X. Bai, X. Wei, X. Zhou, S. Huang and W. Wang(2015) Inferring invasion history of red swamp crayfish (Procambarus clarkii) in China from mitochondrial control region and nuclear intron sequences. International Journal of Molecular Science 16: 14623-14639. https://doi.org/10.3390/ijms160714623
  30. Loureiro, T.G., P.M.S.G. Anastacio, P.B. Araujo, C. Souty-Grosset and M.P. Almerao(2015) Red swamp crayfish: Biology, ecology and invasion-an overview. Nauplius 23(1): 1-19. https://doi.org/10.1590/S0104-64972014002214
  31. Martin-Torrijos, L., T. Kawai, J. Makkonen, J. Jussila, H. Kokko and J. Dieguez-Uribeondo(2018) Crayfish plague in Japan: A real threat to the endemic Cambaroides japonicus. PLoS ONE 13(4): e0195353. https://doi.org/10.1371/journal.pone.0195353
  32. Mathers, K.L., J.C. White, S. Guareschi, M.J. Hill, J. Heino and R. Chadd(2020) Invasive crayfish alter the long-term functional biodiversity of lotic macroinvertebrate communities. Functional Ecology 34: 2350-2361. https://doi.org/10.1111/1365-2435.13644
  33. Mauvisseau, Q., A. Coignet, C. Delaunay, F. Pinet, D. Bouchon and C. Souty-Grosset(2017) Environmental DNA as an efficient tool for detecting invasive crayfishes in freshwater ponds. Hydrobiologia 805: 163-175.
  34. Mauvisseau, Q., S. Tonges, R. Andriantsoa, F. Lyko and M. Sweet(2019) Early detection of an emerging invasive species: eDNA monitoring of a parthenogenetic crayfish in freshwater systems. Management of Biological Invasions 10(3): 461-472. https://doi.org/10.3391/mbi.2019.10.3.04
  35. McCarthy, J.M., C.L. Hein, J.D. Olden and M.J. Vander Zanden(2006) Coupling long-term studies with meta-analysis to investigate impacts of non-native crayfish on zoobenthic communities. Freshwater Biology 51: 4-235.
  36. Merrit, R.W., K.W. Cummins and M.B. Berg(2008) An Introduction to the Aquatic Insects of North America (4h ed.). Kendall/Hunt Publish. Co. Dubuque, Iowa, 1158pp.
  37. Nystrom, P., C. Bronmark and W. Graneli(1999) Influence of an exotic and a native crayfish species on a littoral benthic community. Oikos 85: 545-553. https://doi.org/10.2307/3546704
  38. Park, C.W., J.W. Kim, Y.J. Cho, J.G. Kim, M.J. Lee and S.H. Kim(2020) Distribution of Invasive Alien Species Red Swamp Crawfish (Procambarus clarkii) in Korea. Korean Journal of Ecology and Environment 53(4): 331-335. (in Korean with English abstract) https://doi.org/10.11614/KSL.2020.53.4.331
  39. Rezinciuc, S., J.V. Sandoval-Sierra, B. Oidtmann and J. DieguezUribeondo(2015) The biology of crayfish plague pathogen Aphanomyces astaci: current answers to most frequent questions, Section 2: Crayfish: New developments. In: T. Kawai, Z. Faulkes and G. Scholtz(eds.), Freshwater Crayfish: A Global Overview. CRC Press, Boca Raton, FL, USA, pp.182-204.
  40. Richman, N.I. et al.(2015) Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea). Philosophical Transactions of the Royal Society B 370: 20140060. https://doi.org/10.1098/rstb.2014.0060
  41. Ro, T.H. and D.J. Chun(2004) Functional feeding group categorization of Korean immature aquatic insects and community stability analysis. The Korean Journal of Limnology 37(2): 137-148. (in Korean with English abstract)
  42. Ro, T.H.(2002) Categorization and Ecological Importance of Functional Feeding Groups as Essential Units in Lotic Ecosystems. Bulletin of the KACN 21: 67-93. (in Korean)
  43. Song, H.R., N.Y. Kim, S.H. Kim, D.E. Kim, D.H. Lee, D.H. Choi, H.J. Lee, H.J. Baek, D.K. Kim, M.J. Kim, T.B. Ryu, Y.C. Kim and S.W. Sim(2018) Investigating Ecological Risk of Alien Species (V). National Institute of Ecology, Seocheon, Korea, 89pp. (in Korean with English abstract)
  44. Souty-Grosset, C., P.M. Anastacio, L. Aquiloni, F. Banha, J. Choquer, C. Chucholl and E. Tricarico(2016) The red swamp crayfish Procambarus clarkii in Europe: Impacts on aquatic ecosystems and human well-being. Limnologica 58: 78-93. https://doi.org/10.1016/j.limno.2016.03.003
  45. Treguier, A., J.M. Paillisson, T. Dejean, A. Valentini, M.A. Schlaepfer and J.M. Roussel(2014) Environmental DNA surveillance for invertebrate species: Advantages and technical limitations to detect invasive crayfish Procambarus clarkii in freshwater ponds. Journal of Applied Ecology 51: 871-879. https://doi.org/10.1111/1365-2664.12262
  46. Usio, N. and C.R. Townsend(2002) Functional significance of crayfish in stream food webs: Roles of omnivory, substrate heterogeneity and sex. Oikos 98: 512-522. https://doi.org/10.1034/j.1600-0706.2002.980316.x
  47. Usio, N. and C.R. Townsend(2004) Roles of crayfish: Consequences of predation and bioturbation for stream invertebrates. Ecology 166: 807-822. https://doi.org/10.1890/02-0618
  48. Yi, S., L. Zhang, Y. Li, L. Shi, J. Chen, W. Wang, L. She and J. He(2020) Genetic diversity and phenotypic variation of the red swamp crayfish, Procambarus clarkii (Girard, 1852) (Decapoda: Astacidea: Astacidae), in China. Journal of Crustacean Biology 1-10.
  49. Yi, S., Y. Li, L. Shi, L. Zhang, Q. Li and J. Chen(2018) Characterization of Population Genetic Structure of red swamp crayfish, Procambarus clarkii, in China. Scientific Reports 8: 5586. https://doi.org/10.1038/s41598-018-23986-z
  50. Yoon, I.B.(1995) Aquatic Insects of Korea. Junghaengsa, Seoul, 262pp. (in Korean)
  51. Yue, G.H., J. Li, Z. Bai, C.M. Wang and F. Feng(2010) Genetic diversity and population structure of the invasive alien red swamp crayfish. Biological Invasions 12: 2697-2706. https://doi.org/10.1007/s10530-009-9675-1
  52. Yusop, M.H.M., S. Mustafa, Y.B.C. Man, A.R. Omar and N.F.K. Mokhtar(2012) Detection of Raw Pork Targeting Porcine-Specific Mitochondrial Cytochrome B Gene by Molecular Beacon Probe Real-Time Polymerase Chain Reaction. Food Analytical Methods 5: 422-429. https://doi.org/10.1007/s12161-011-9260-y
  53. Zhang, Y., J.S. Richardson and J.N. Negishi(2004) Detritus processing, ecosystem engineering and benthic diversity: A test of predator-omnivore interference. Journal of Animal Ecology 73: 756-766. https://doi.org/10.1111/j.0021-8790.2004.00849.x