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Comparison of the community composition of aquatic insects between wetlands with and without the presence of Procambarus clarkii: a case study from Japanese wetlands

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Abstract

The red swamp crayfish Procambarus clarkii (Cambaridae) has been introduced globally and has caused enormous biodiversity losses in freshwater ecosystems. Recently, this invasive species has been acknowledged as factor causing the decline of aquatic insect populations (Odonata, Hemiptera, and Coleoptera) in Japan. Although the negative impacts of P. clarkii on aquatic insect communities have been validated by observational studies and laboratory experiments, field studies have not yet been performed. In this study, we investigated whether the presence of P. clarkii was a significant factor influencing the community composition of aquatic insects and identified vulnerable taxa by comparing the aquatic insect communities in wetlands invaded by P. clarkii and uninvaded wetlands. We recorded a total of 52 species and 2721 individuals: 50 species and 2405 individuals in non-invaded wetlands, and 23 species and 316 individuals in invaded wetlands. This indicates that the aquatic insect diversity of non-invaded wetlands was higher than that of invaded wetlands. The composition of aquatic insect communities differed between the invaded and non-invaded wetlands. The effect of P. clarkii on aquatic insects differed according to their habit-related traits: species that utilize on the water surface and float near the water surface was less vulnerable than those that utilize aquatic plants as food, oviposition substrates, and perches and hide in the bottom substrate. The eradication of P. clarkii at the early stages of invasion, as well as the prevention of its spread in invaded ecosystems is essential to prevent negative impacts on aquatic insects.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Bilton DT, Mcabendroth L, Bedford A, Ramsay PM (2006) How wide to cast the net? Cross-taxon congruence of species richness, community similarity and indicator taxa in ponds. Freshw Biol 51:578–590. https://doi.org/10.1111/j.1365-2427.2006.01505.x

    Article  Google Scholar 

  • Briers RA, Biggs J (2003) Indicator taxa for the conservation of pond invertebrate diversity. 330:323–330. doi: https://doi.org/10.1002/aqc.576

  • Bucciarelli GM, Suh D, Lamb AD et al (2018) Assessing effects of non-native crayfish on mosquito survival. Conserv Biol 33:122–131. https://doi.org/10.1111/cobi.13198

    Article  PubMed  Google Scholar 

  • Carreira BM, Segurado P, Laurila A, Rebelo R (2017) Can heat waves change the trophic role of the world’s most invasive crayfish? Diet shifts in Procambarus clarkii. PLoS ONE 12:1–15

    Article  Google Scholar 

  • Chucholl C (2013) Feeding ecology and ecological impact of an alien “warm-water” omnivore in cold lakes. Limnologica 43:219–229. https://doi.org/10.1016/j.limno.2012.10.001

    Article  Google Scholar 

  • Correia AM (2003) Food choice by the introduced crayfish Procambarus clarkii. Ann Zool Fennici 40:517–528

    Google Scholar 

  • Doi H, Murakami H (2011) Similarity indices, ordination, and community analysis tests using the software R. Jpn J Ecol 61:3–20 (in Japanese with English summary)

    Google Scholar 

  • Dormann CF, Elith J, Bacher S et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography (cop) 36:27–46. https://doi.org/10.1111/j.1600-0587.2012.07348.x

    Article  Google Scholar 

  • Foster GN, Bilton DT (2014) Chapter 10: the conservation of predaceous diving beetles: knowns, unknowns and ancedotes. In: Yee DA (ed) Ecology, systematics, and the natural history of predaceous diving beetles (Coleoptera: Dytiscidae). Springer, New York, pp 437–462

    Google Scholar 

  • Fox J, Weisberg S, Price B, et al (2020) Package ‘car.’ https://cran.r-project.org/web/packages/car/car.pdf. Accessed 21 Mar 2021

  • Gherardi F, Acquistapace P (2007) Invasive crayfish in Europe: the impact of Procambarus clarkii on the littoral community of a Mediterranean lake. Freshw Biol 52:1249–1259. https://doi.org/10.1111/j.1365-2427.2007.01760.x

    Article  Google Scholar 

  • Gioria M (2014) Chapter 7 Habitats. In: Yee DA (ed) Ecology, systematics, and the natural history of predaceous diving beetles (Coleoptera: Dytiscidae). Springer, New York, pp 307–362

    Google Scholar 

  • Guillermo-Ferreira R, Del-Claro K (2011) Oviposition site selection in Oxyagrion microstigma Selys, 1876 (Odonata: Coenagrionidae) is related to aquatic vegetation structure. Int J Odonatol 14:275–279. https://doi.org/10.1080/13887890.2011.621109

    Article  Google Scholar 

  • Hayashi M, Miyamoto S (2018) Hemiptera. In: Aquatic insects of Japan: manual with keys and illustrations the second edition. Tokai University Press, Kanagawa, pp 329–427 (in Japanese)

  • Hayashi M, Nakajima J, Ishida K et al (2020) Species diversity of aquatic Hemiptera and Coleoptera in Japan. Jpn J Syst Entomol 26:191–200

    Google Scholar 

  • He M, Liu F, Wang F (2021) Quantitative analysis of density dependent resource utilization, cannibalism, and competition of the red swamp crayfish (Procambarus clarkii) in rice-crayfish cocultures without supplementary food. Aquaculture 2(543):736966

    Article  Google Scholar 

  • Hirai N, Morioka T, Ishii M (2020) Species diversity of Odonata in Nakaikemi Marsh, Fukui Prefecture, Japan. Jpn J Environ Entomol Zool 31:1–12 (in Japanese with English summary)

    Google Scholar 

  • Ibrahim AM, Khalil MT, Mobarak MF (1995) On the feeding behaviour of the exotic crayfish Procambarus clarkii in Egypt and its prospects in the biological control of local vector snails. J Union Arab Biol 4:321–340

    Google Scholar 

  • Ichikawa N, Ohba S (2015) Aquatic insects in paddy fields and ponds in western Hyogo Prefecture, Japan, where Kirkaldyia deyrolli and Cybister chinensis breed. Jpn J Environ Entomol Zool 26:89–93 (in Japanese with English summary)

    Google Scholar 

  • Karube H, Kitano T (2016) The crisis of aquatic insects in Amami Islands: Loss and degradation of wetland environment and impact of invasive alien species. In: Natural history of Amami Islands: Biodiversity in subtropical islands. Tokai University Press, Kanagawa, p 388 (in Japanese)

  • Kawai T, Tanida K (2018) Aquatic insects of Japan: manual with keys and illustrations The, 2nd edn. Tokai University Press, Kanagawa (in Japanese)

    Google Scholar 

  • Kruskal JB (1964) Multidimentional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27

    Article  Google Scholar 

  • Larson ER, Twardochleb LA, Olden JD (2017) Comparison of trophic function between the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii. Limnology 18:275–286. https://doi.org/10.1007/s10201-016-0505-8

    Article  CAS  Google Scholar 

  • Loureiro TG, Anastácio PM, de Bueno SL, S, et al (2019) Food matters: trophodynamics and the role of diet in the invasion success of Procambarus clarkii in an Atlantic Forest conservation area. Limnologica 79:125717. https://doi.org/10.1016/j.limno.2019.125717

    Article  Google Scholar 

  • Loureiro TG, Anastácio PMSG, Araujo PB et al (2015) Red swamp crayfish: biology, ecology and invasion - an overview. Nauplius 23:1–19. https://doi.org/10.1590/s0104-64972014002214

    Article  Google Scholar 

  • Lüdecke D, Makowski D, Waggoner P, et al (2021) Package ‘performance.’ https://cran.r-project.org/web/packages/performance/performance.pdf. Accessed 21 Mar 2021

  • Maezono Y, Miyashita T (2004) Impact of exotic fish removal on native communities in farm ponds. Ecol Res 19:263–267. https://doi.org/10.1111/j.1440-1703.2004.00634.x

    Article  Google Scholar 

  • Magnusson A, Nielsen A, Berg C, Kristensen K (2020) Package “glmmTMB.” https://cran.r-project.org/web/packages/glmmTMB/glmmTMB.pdf. Accessed 24 Feb 2021

  • Martins EP, Diniz-Filho JAF, Housworth EA (2002) Adaptive constraints and the phylogenetic comparative method: a computer simulation test. Evolution (n y) 56:1–13. https://doi.org/10.1111/j.0014-3820.2002.tb00844.x

    Article  Google Scholar 

  • Matsuzaki SS, Usio N, Takamura N, Washitani I (2009) Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia 158:673–686. https://doi.org/10.1007/s00442-008-1180-1

    Article  PubMed  Google Scholar 

  • Merritt RW, Cummins KW (1996) An introduction to the aquatic insects of North America, 3rd editio. Kendall/Hunt Pub. Co, Dubuque

  • Ministry of the Environment of Japan (2020a) List of regulated living organisms under the invasive alien species act [Animal Kingdom]. https://www.env.go.jp/nature/intro/2outline/files/siteisyu_list_e.pdf. Accessed 14 Feb 2021

  • Ministry of the Environment of Japan (2020b) Red List of Japan. https://www.env.go.jp/press/files/jp/114457.pdf. Accessed 31 Jan 2021

  • Mitamura T, Hirasawa K, Yoshii S (2017) The handbook of Japanese aquatic insect volume 1: Coleoptera. Bun-ichi Sogo Shuppan, Toyo (in Japanese)

  • Mori M, Kitayama A (2002) Dytiscoidea of Japan. Bun-ichi Sogo Shuppan, Tokyo (in Japanese)

  • Muzón J, Ramos LS, Palacio A del (2019) Urban Aquatic Insects. In: Del-claro K, Guillermo R (eds) Aquatic Insects Behavior and Ecology. Springer Nature Switzerland AG, Cham, pp 349–364

  • Nakajima J, Hayashi M, Ishida K, et al (2020) Aquatic Coleoptera and Hemiptera of Japan. Bun-ichi Sogo Shuppan, Tokyo (in Japanese)

  • National Institute for Environmental Studies (2021) Procambarus clarkii. http://www.nies.go.jp/biodiversity/invasive/DB/detail/70320e.html. Accessed 25 Mar 2021

  • Nishihara S (2016) Critical situation of aquatic insects and practice for conservation. Nat Insects 51:2–4 (in Japanese)

    Google Scholar 

  • Nishihara S, Karube H (2010) Exclusion methods of invasive alien species in wetlands. In: Washitani I, Miyashita T, Nishihiro J, Kadoya T (eds) Methods in Conservation Ecology. University of Tokyo Press, Tokyo, pp 179–200 (in Japanese)

    Google Scholar 

  • Nishijima S, Nishikawa C, Miyashita T (2017) Habitat modification by invasive crayfish can facilitate its growth through enhanced food accessibility. BMC Ecol 17:1–9. https://doi.org/10.1186/s12898-017-0147-7

    Article  Google Scholar 

  • Ohba S (2011a) Ecological studies in lentic aquatic insects including rare species: consideration of their conservations and applied aspects from the predator-prey relationship. Jpn J Environ Entomol Zool 22:39–48 (in Japanese with English summary)

    Google Scholar 

  • Ohba S (2011b) Impact of the invasive crayfish Procambarus clarkii on the giant water bug Kirkadlia deyrolli (Hemiptera) in rice ecosystems. Jpn J Environ Entomol Zool 22:93–98

    Google Scholar 

  • Ohba S, Ichikawa N (2016) Crayfish, Procambarus clarkii is not suitable for dietary items of giant water bug, Kirkaldyia deyrolli. Rostria 59:28–30 (in Japanese with English summary)

    Google Scholar 

  • Ohba S, Murakami R, Watanabe R, Jun B (2019) Factors affecting a fauna of aquatic insects in swimming pools of schools in the southern part of Nagasaki, Japan. Jpn J Appl Entomol Zool 63:163–173 (in Japanese with English summary)

    Article  Google Scholar 

  • Ohba S, Takagi M (2010) Predatory ability of adult diving beetles on the Japanese encephalitis vector Culex tritaeniorhynchus. J Am Mosq Control Assoc 26:32–36. https://doi.org/10.2987/09-5946.1

    Article  PubMed  Google Scholar 

  • Ohba S, Tanaka R, Yamamoto K et al (2018) Current status and extermination problems of an exotic crayfish, Procambarus clarkii, in Fukue Island, Nagasaki, Japan. Jpn J Environ Entomol Zool 29:21–26 (in Japanese with English summary)

    Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M et al (2020) Package “vegan.” https://cran.r-project.org/web/packages/vegan/vegan.pdf. Accessed 25 Mar 2021

  • R Core Team (2019) R: a language and environment for statistical computing. In: R Foudation Stat. Comput. Vienna, Austria. https://www.r-project.org/. Accessed 4 Jan 2021

  • Ripley B, Venables B, Bates DM, et al (2021) Package ‘MASS.’ https://cran.r-project.org/web/packages/MASS/MASS.pdf. Accessed 25 Mar 2021

  • Rodríguez CF, Bécares E, Fernández-Aláez M (2003) Shift from clear to turbid phase in Lake Chozas (NW Spain) due to the introduction of American red swamp crayfish (Procambarus clarkii). Hydrobiologia 506–509:421–426

    Article  Google Scholar 

  • Russell A, Lenth V, Buerkner P, et al (2021) Package ‘emmeans.’ https://cran.r-project.org/web/packages/emmeans/emmeans.pdf. Accessed 25 Mar 2021

  • Sánchez-Fernández D, Abellán P, Mellado A et al (2006) Are water beetles good indicators of biodiversity in Mediterranean aquatic ecosystems? The case of the Segura river basin (SE Spain). Biodivers Conserv 15:4507–4520

    Article  Google Scholar 

  • Sigutova H, Sigut M, Dolny A (2015) Intensive fish ponds as ecological traps for dragonflies: an imminent threat to the endangered species Sympetrum depressiusculum (Odonata: Libellulidae). J Insect Conserv 19:961–974

    Article  Google Scholar 

  • Skern M, Zweimüller I, Schiemer F (2010) Aquatic Heteroptera as indicators for terrestrialisation of floodplain habitats. Limnologica 40:241–250. https://doi.org/10.1016/j.limno.2009.09.002

    Article  Google Scholar 

  • Souty-Grosset C, Anastácio PM, Aquiloni L et al (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

    Article  Google Scholar 

  • Takahashi K (2017) Reviving Fish. Kouseisha Kouseikaku, Tokyo (in Japanese)

  • Wakasugi K (2013) Actual situation and measures of paddy field leakage by Procambarus clarkii. Agric Hortic 88:795–806 (in Japanese)

    Google Scholar 

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Acknowledgements

We would like to acknowledge Dr. Noritaka Ichikawa (Himeji Dokkyo University) and Mr. Masao Mieda for allowing us to conduct our research at the study site. We also thank Mrs. Shizuko Yagi and the Sonoda family for providing us with their great field stations. We would like to thank Editage (www.editage.jp) for English language editing.

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Correspondence to Reiya Watanabe.

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Watanabe, R., Ohba, S. Comparison of the community composition of aquatic insects between wetlands with and without the presence of Procambarus clarkii: a case study from Japanese wetlands. Biol Invasions 24, 1033–1047 (2022). https://doi.org/10.1007/s10530-021-02700-7

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