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.
Similar content being viewed by others
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
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
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
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
Correia AM (2003) Food choice by the introduced crayfish Procambarus clarkii. Ann Zool Fennici 40:517–528
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)
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
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
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
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
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
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
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
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)
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
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)
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)
Kruskal JB (1964) Multidimentional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27
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
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
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
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
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
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
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)
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)
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
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)
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
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)
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)
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
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)
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
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
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
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
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
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)
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-021-02700-7