Effects of a herbicide on paddy predatory insects depend on their microhabitat use and an insecticide application.
Odonata
agroecosystem
biotic interactions
ecotoxicology
fipronil
functional traits
indirect effects of pesticides
mesocosms
pentoxazone
pesticide mixture effects
Journal
Ecological applications : a publication of the Ecological Society of America
ISSN: 1051-0761
Titre abrégé: Ecol Appl
Pays: United States
ID NLM: 9889808
Informations de publication
Date de publication:
09 2019
09 2019
Historique:
received:
23
12
2018
revised:
01
04
2019
accepted:
30
04
2019
pubmed:
8
6
2019
medline:
12
10
2019
entrez:
8
6
2019
Statut:
ppublish
Résumé
Indirect effects of agrochemicals on organisms via biotic interactions are less studied than direct chemical toxicity despite their potential relevance in agricultural landscapes. In particular, the role of species traits in characterizing indirect effects of pesticides has been largely overlooked. Moreover, it is still unclear whether such indirect effects on organisms are prevalent even when the organisms are exposed to direct toxicity. We conducted a mesocosm experiment to examine indirect effects of a herbicide (pentoxazone) on aquatic predatory insects of rice paddies. Because the herbicide selectively controls photosynthetic organisms, we assumed that the effects of the herbicide on predatory insects would be indirect. We hypothesized that phytophilous predators such as some Odonata larvae, which cling to aquatic macrophytes, would be more subject to negative indirect effects of the herbicide through a decrease in abundance of aquatic macrophytes than benthic, nektonic, and neustonic predators. Also, we crossed-applied an insecticide (fipronil) with herbicide application to examine whether the indirect effects of the herbicide on the assembling predators act additively with direct adverse effects of the insecticide. The herbicide application did not decrease the abundance of phytoplankton constitutively, and there were no clear negative impacts of the herbicide on zooplankton and prey insects (detritivores and herbivores). However, the abundance of aquatic macrophytes was significantly decreased by the herbicide application. Although indirect effects of the herbicide were not so strong on most predators, their magnitude and sign differed markedly among predator species. In particular, the abundance of phytophilous predators was more likely to decrease than that of benthic, nektonic, and neustonic predators when the herbicide was applied. However, these indirect effects of the herbicide could not be detected when the insecticide was also applied, seemingly due to fipronil's high lethal toxicity. Our study highlights the importance of species traits such as microhabitat use, which characterize biotic interactions, for predicting indirect effects of agrochemicals. Given that indirect effects of the chemicals vary in response to species traits and direct toxicity of other chemicals, efforts to explain this variation are needed to predict the realistic risks of indirect effects of agrochemicals in nature.
Substances chimiques
Herbicides
0
Insecticides
0
Water Pollutants, Chemical
0
Banques de données
GENBANK
['SMZ1500']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e01945Subventions
Organisme : Environment Research and Technology Development Fund (ERTDF)
ID : FY2017 (4-1701)
Pays : International
Organisme : Ministry of the Environment
Pays : International
Informations de copyright
© 2019 by the Ecological Society of America.
Références
Altenburger, R., T. Backhaus, W. Boedeker, M. Faust, and M. Scholze. 2013. Simplifying complexity: mixture toxicity assessment in the last 20 years. Environmental Toxicology and Chemistry 32:1685-1687.
Bambaradeniya, C. N. B., J. P. Edirisinghe, D. N. De Silva, C. V. S. Gunatilleke, K. B. Ranawana, and S. Wijekoon. 2004. Biodiversity associated with an irrigated rice agro-ecosystem in Sri Lanka. Biodiversity and Conservation 13:1715-1753.
Braun-Blanquet, J. 1964. Pflanzensoziologie. Third edition. Springer-Verlag, Vienna, Austria.
Brock, T. C. M., J. Lahr, and P. J. Van den Brink. 2000a. Ecological risks of pesticides in freshwater ecosystems Part 1: Herbicides. Alterra-Report 088.
Brock, T. C. M., R. P. A. van Wijngaarden, and G. J. van Geest. 2000b. Ecological risks of pesticides in freshwater ecosystems Part 2: Insecticides. Alterra-Report 089.
Clements, W. H., and J. R. Rohr. 2009. Community responses to contaminants: using basic ecological principles to predict ecotoxicological effects. Environmental Toxicology and Chemistry 28:1789-1800.
Crumrine, P. W. 2005. Size structure and substitutability in an odonate intraguild predation system. Oecologia 145:132-139.
Fleeger, J. W., K. R. Carman, and R. M. Nisbet. 2003. Indirect effects of contaminants in aquatic ecosystems. Science of the Total Environment 317:207-233.
Gant, D. B., A. E. Chalmers, M. A. Wolff, H. B. Hoffman, and D. F. Bushey. 1998. Fipronil: action at the GABA receptor. Pages 147-156 in R. J. Kuhr and N. Motoyama, editors. Pesticides and the future. IOS Press, Amsterdam, The Netherlands.
Gunasekara, A. S., T. Truong, K. S. Goh, F. Spurlock, and R. S. Tjeerdema. 2007. Environmental fate and toxicology of fipronil. Journal of Pesticide Science 32:189-199.
Halstead, N. T., T. A. McMahon, S. A. Johnson, T. R. Raffel, J. M. Romansic, P. W. Crumrine, and J. R. Rohr. 2014. Community ecology theory predicts the effects of agrochemical mixtures on aquatic biodiversity and ecosystem properties. Ecology Letters 17:932-941.
Hayasaka, D., T. Korenaga, F. Sánchez-Bayo, and K. Goka. 2012a. Differences in ecological impacts of systemic insecticides with different physicochemical properties on biocenosis of experimental paddy fields. Ecotoxicology 21:191-201.
Hayasaka, D., T. Korenaga, K. Suzuki, F. Saito, F. Sánchez-Bayo, and K. Goka. 2012b. Cumulative ecological impacts of two successive annual treatments of imidacloprid and fipronil on aquatic communities of paddy mesocosms. Ecotoxicology and Environmental Safety 80:355-362.
Hirai, K., T. Yano, S. Ugai, T. Yoshimura, and M. Hori. 2001. Development of a herbicide, pentoxazone. Journal of Pesticide Science 26:194-202 [in Japanese].
Japan Plant Protection Association (JPPA). 2011. Pesticide handbook 2011. Japan Plant Protection Association, Tokyo, Japan [in Japanese].
Jinguji, H., D. Q. Thuyet, T. Uéda, and H. Watanabe. 2013. Effect of imidacloprid and fipronil pesticide application on Sympetrum infuscatum (Libellulidae: Odonata) larvae and adults. Paddy and Water Environment 11:277-284.
Kasai, F., and T. Hanazato. 1995. Effects of the triazine herbicide, simetryn, on freshwater plankton communities in experimental ponds. Environmental Pollution 89:197-202.
Kasai, A., T. I. Hayashi, H. Ohnishi, K. Suzuki, D. Hayasaka, and K. Goka. 2016. Fipronil application on rice paddy fields reduces densities of common skimmer and scarlet skimmer. Scientific Reports 6:23055.
Katoh, K., S. Sakai, and T. Takahashi. 2009. Factors maintaining species diversity in satoyama, a traditional agricultural landscape of Japan. Biological Conservation 142:1930-1936.
Klecka, J., and D. S. Boukal. 2014. The effect of habitat structure on prey mortality depends on predator and prey microhabitat use. Oecologia 176:183-191.
Kobashi, K., T. Harada, Y. Adachi, M. Mori, M. Ihara, and D. Hayasaka. 2017. Comparative ecotoxicity of imidacloprid and dinotefuran to aquatic insects in rice mesocosms. Ecotoxicology and Environmental Safety 138:122-129.
Leipelt, K. G., F. Suhling, and S. N. Gorb. 2010. Ontogenetic shifts in functional morphology of dragonfly legs (Odonata: Anisoptera). Zoology 113:317-325.
Lenth, R. V. 2016. Least-squares means: the R package lsmeans. Journal of Statistical Software 69:1-33.
Liess, M., and M. Beketov. 2011. Traits and stress: keys to identify community effects of low levels of toxicants in test systems. Ecotoxicology 20:1328-1340.
Liess, M., and P. C. von der Ohe. 2005. Analyzing effects of pesticides on invertebrate communities in streams. Environmental Toxicology and Chemistry 24:954.
Maezono, Y., and T. Miyashita. 2004. Impact of exotic fish removal on native communities in farm ponds. Ecological Research 19:263-267.
Moretti, M., et al. 2017. Handbook of protocols for standardized measurement of terrestrial invertebrate functional traits. Functional Ecology 31:558-567.
Nagai, T., S. Ishihara, A. Yokoyama, and T. Iwafune. 2011. Effects of four rice paddy herbicides on algal cell viability and the relationship with population recovery. Environmental Toxicology and Chemistry 30:1898-1905.
Nakanishi, K., H. Yokomizo, and T. I. Hayashi. 2018. Were the sharp declines of dragonfly populations in the 1990s in Japan caused by fipronil and imidacloprid? An analysis of Hill's causality for the case of Sympetrum frequens. Environmental Science and Pollution Research 25:35352-35364.
Paine, R. T. 1992. Food-web analysis through field measurement of per capita interaction strength. Nature 355:73-75.
Peguero, G., H. C. Muller-Landau, P. A. Jansen, and S. J. Wright. 2017. Cascading effects of defaunation on the coexistence of two specialized insect seed predators. Journal of Animal Ecology 86:136-146.
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, R Core Team. 2017. nlme: linear and nonlinear mixed effects models. R package version 3.1-131. https://CRAN.R-project.org/package=nlme
R Core Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/
Relyea, R. A. 2009. A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363-376.
Relyea, R. A., and J. Hoverman. 2006. Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecology Letters 9:1157-1171.
Remsburg, A. J., and M. G. Turner. 2009. Aquatic and terrestrial drivers of dragonfly (Odonata) assemblages within and among north-temperate lakes. Journal of the North American Benthological Society 28:44-56.
Rodriguez-Cabal, M. A., M. N. Barrios-Garcia, G. C. Amico, M. A. Aizen, and N. J. Sanders. 2013. Node-by-node disassembly of a mutualistic interaction web driven by species introductions. Proceedings of the National Academy of Sciences USA 110:16503-16507.
Rohr, J. R., and P. W. Crumrine. 2005. Effects of an herbicide and an insecticide on pond community structure and processes. Ecological Applications 15:1135-1147.
Rohr, J. R., J. L. Kerby, and A. Sih. 2006. Community ecology as a framework for predicting contaminant effects. Trends in Ecology and Evolution 21:606-613.
Rubach, M. N., R. Ashauer, D. B. Buchwalter, H. J. De Lange, M. Hamer, T. G. Preuss, K. Töpke, and S. J. Maund. 2011. Framework for traits-based assessment in ecotoxicology. Integrated Environmental Assessment and Management 7:172-186.
Simon-Delso, N., et al. 2015. Systemic insecticides (Neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environmental Science and Pollution Research 22:5-34.
Sugimura, M., S. Ishida, K. Kojima, K. Ishida, and T. Aoki. 1999. Dragonflies of the Japanese archipelago in color. Hokkaido University Press, Sapporo, Japan [in Japanese].
Tylianakis, J. M., R. K. Didham, J. Bascompte, and D. A. Wardle. 2008. Global change and species interactions in terrestrial ecosystems. Ecology Letters 11:1351-1363.
Van den Brink, P. J., D. J. Baird, H. J. Baveco, and A. Focks. 2013. The use of traits-based approaches and eco(toxico)logical models to advance the ecological risk assessment framework for chemicals. Integrated Environmental Assessment and Management 9:e47-e57.
Washitani, I. 2001. Traditional sustainable ecosystem “SATOYAMA” and biodiversity crisis in Japan: Conservation Ecological Perspective. Global Environmental Research 5:119-133.