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Developmental and reproductive effects of clothianidin exposure in monarch butterflies (Lepidoptera: Nymphalidae)

Published online by Cambridge University Press:  16 March 2021

Alana A.E. Wilcox*
Affiliation:
1Department of Integrative Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada
Amy E.M. Newman
Affiliation:
1Department of Integrative Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada
D. Ryan Norris
Affiliation:
1Department of Integrative Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada 2Nature Conservancy of Canada, 245 Eglington Avenue East, Toronto, Ontario, M4P 3J1, Canada
*
*Corresponding author. Email: [email protected]

Abstract

Neonicotinoid insecticides are used to reduce crop damage caused by insect pests, but sublethal levels could affect development and reproduction in nontarget insects, such as monarch butterflies (Danaus plexippus) (Lepidoptera: Nymphalidae). To investigate the impact of field-realistic concentrations of the neonicotinoid clothianidin on monarch butterflies, we grew swamp milkweed (Asclepias incarnata) (Apocynaceae) in either low (15 ng/g of soil) or high (25 ng/g of soil) levels of clothianidin, or in a control (0 ng/g), then raised monarchs on the milkweed. Morphological traits of monarch caterpillars were measured during development and, once they eclosed, were mated as adults to quantify egg size and mass and the number of eggs laid. Although the effects of the treatment had complex effects on caterpillar length, width and volume of late-instar caterpillars were negatively affected. Fifth-instar caterpillars from the high-dose insecticide treatment had lower mass than other groups. Adult monarch butterflies raised on treated milkweed were larger than controls, but clothianidin exposure did not affect the number of eggs laid or egg size. Although the magnitude of the effect depends on clothianidin concentration, our results suggest that exposure to clothianidin during early life can impact monarch caterpillar development but is unlikely to reduce female reproductive output.

Type
Research Papers
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada.

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Footnotes

Subject editor: David Siaussat

References

Ahmad, S., Ansari, M.S., and Ahmand, N. 2013. Acute toxicity and sublethal effects of the neonicotinoid imidacloprid on the fitness of Helicoverpa armigera (Lepidoptera: Noctuidae). International Journal of Tropical Insect Science, 33: 264275. https://doi.org/10.1017/S1742758413000246.CrossRefGoogle Scholar
Altizer, S.M. and Oberhauser, K.S. 1999. Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). Journal of Invertebrate Pathology, 74: 7688. https://doi.org/10.1006/jipa.1999.4853.CrossRefGoogle Scholar
Arce, A.N., Rodrigues, A.R., Yu, J., Colgan, T.J., Wurm, Y., and Gill, R.J. 2018. Foraging bumblebees acquire a preference for neonicotinoid-treated food with prolonged exposure. Proceedings of the Royal Society B, 285: 20180655. https://doi.org/10.1098/rspb.2018.0655.CrossRefGoogle ScholarPubMed
Ayyanath, M.M., Cutler, G.C., Scott-Dupree, C.D., Prithivirai, B., Kandasamy, S., and Prithivirai, K. 2014. Gene expression during imidacloprid-induced hormesis in green peach aphid. Dose-Response, 12: 480497. https://doi.org/10.2203/dose-response.13-057.CrossRefGoogle ScholarPubMed
Baron, G.L., Raine, N.E., and Brown, M.J.F. 2017. General and species-specific impacts of a neonicotinoid insecticide on the ovary development and feeding of wild bumblebee queens. Proceedings of the Royal Society B, 284: 20170123. https://doi.org/10.1098/rspb.2017.0123.CrossRefGoogle ScholarPubMed
Bass, C., Denholm, I., Williamson, M.S., and Nauen, R. 2015. The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121: 7887. https://doi.org/10.1016/j.pestbp.2015.04.004.CrossRefGoogle ScholarPubMed
Boguski, T.K. 2006. Understanding units of measurement [online]. Available from https://cfpub.epa.gov/ncer_abstracts/index.cfm/fuseaction/display.files/fileid/14285 [accessed 26 May 2019].Google Scholar
Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, H.M.H., and White, J.S. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution, 24: 127135. https://doi.org/10.1016/j.tree.2008.10.008.CrossRefGoogle ScholarPubMed
Bonmatin, J.M., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D.P., Krupke, C., et al. 2015. Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research, 22: 3567. https://doi.org/10.1007/s11356-014-3332-7.CrossRefGoogle ScholarPubMed
Burnham, K.P. and Anderson, D.R. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media, Berlin, Germany.Google Scholar
Canadian Food Inspection Agency. 2008. Determination of pesticides in infant foods using liquid chromatography electrospray ionization mass spectrometry (LC/ESI-MS/MS). CFIA method PMR-006-V1.0 (effective April 1, 2008). In Pesticides multiresidues analytical methods manual. Volume 7. Pp.1–25.Google Scholar
Chamberlain, K., Tench, A.J., Williams, R.H., and Bromilow, R.H. 1995. Phloem translocation of pyridinecarboxylic acids and related imidazolinone herbicides in Ricinus communis . Pesticide Science, 45: 6975. https://doi.org/10.1002/ps.2780450110.CrossRefGoogle Scholar
Chan, D.S.W., Prosser, R.S., Rodríguez-Gill, J.L., and Raine, N.E. 2019. Assessment of risk to hoary squash bees (Peponapis pruinosa) and other ground-nesting bees from systemic insecticides in agricultural soil. Scientific Reports, 9: 11870. https://doi.org/10.1038/s41598-019-47805-1.CrossRefGoogle Scholar
Craddock, H.A., Huang, D., Turner, P.C., Quirós-Alcalá, L., and Payne-Sturges, D.C. 2019. Trends in neonicotinoid pesticide residues in food and water in the United States, 1999–2015. Environmental Health, 18: 7. https://doi.org/10.1186/s12940-018-0441-7.CrossRefGoogle ScholarPubMed
Cresswell, J.E., Robert, F.X., Florance, H., and Smirnoff, N. 2014. Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Management Science, 70: 332337. https://doi.org/10.1002/ps.3569.CrossRefGoogle Scholar
Decant, J. 2010. Clothianidin registration of Prosper T400 seed treatment on mustard seed (oilseed and condiment) and Poncho/Votivo seed treatment on cotton. United States Environmental Protection Agency, Washington, D.C., United States of America.Google Scholar
Douglas, M.R. and Tooker, J.F. 2015. Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in U.S. field crops. Environmental Science & Technology, 49: 50885097. https://doi.org/10.1021/es506141g.CrossRefGoogle ScholarPubMed
Flockhart, D.T.T., Martin, T.G., and Norris, D.R. 2012. Experimental examination of intraspecific density-dependent competition during the breeding period in monarch butterflies (Danaus plexippus). PLOS One, 7: e45080. https://doi.org/10.1371/journal.pone.0045080.CrossRefGoogle Scholar
García-Barros, E. 2000. Body size, egg size, and their interspecific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidea, Hesperioidea). Biological Journal of the Linnean Society, 70: 251284. https://doi.org/10.1111/j.1095-8312.2000.tb00210.x.CrossRefGoogle Scholar
Goehring, L. and Oberhauser, K.S. 2002. Effects of photoperiod, temperature, and host plant age on induction of reproductive diapauses and development time in Danaus plexippus . Ecological Entomology, 27: 674685. https://doi.org/10.1046/j.1365-2311.2002.00454.x.CrossRefGoogle Scholar
Goulson, D. 2013. Review: an overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology, 50: 977987. https://doi.org/10.1111/1365-2664.12111.CrossRefGoogle Scholar
James, D.G. 2019. A neonicotinoid insecticide at a rate found in nectar reduces longevity but not oogenesis in monarch butterflies, Danaus plexippus (L.). (Lepidoptera: Nymphalidae). Insects, 10: 276. https://doi.org/10.3390/insects10090276.CrossRefGoogle Scholar
Kessler, S.C., Tiedeken, E.J., Simcock, K.L., Derveau, S., Mitchell, J., Softley, S., et al. 2015. Bees prefer foods containing neonicotinoid pesticides. Nature, 521: 7476. https://doi.org/10.1038/nature14414.CrossRefGoogle ScholarPubMed
Kobiela, M.E. and Snell-Rood, E.C. 2020. Genetic variation influences tolerance to a neonicotinoid insecticide in three butterfly species. Environmental Toxicology and Chemistry, 39: 22282236. https://doi.org/10.1002/etc.4845.CrossRefGoogle Scholar
Laycock, I., Cotterell, K.C., Wheller, T.A., and Cresswell, J.E. 2014. Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees. Ecotoxicology and Environmental Safety, 100: 153158. https://doi.org/10.1016/j.ecoenv.2013.10.027.CrossRefGoogle ScholarPubMed
Laycock, I., Lenthall, K.M., Barratt, A.T., and Cresswell, J.E. 2012. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Exotoxicology, 21: 19371945. https://doi.org/10.1007/s10646-012-0927-y.CrossRefGoogle Scholar
Lin, H., Slate, D.J., Paetsch, C.R., Dorfmann, A.L., and Trimmer, B.A. 2011. Scaling of caterpillar body properties and its biomechanical implications for the use of a hydrostatic skeleton. Journal of Experimental Biology, 214: 11941204. https://doi.org/10.1242/jeb.051029.CrossRefGoogle ScholarPubMed
Manjon, C., Troczka, B.J., Zaworra, M., Beadle, K., Randall, E., Hertlein, G., et al. 2018. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Current Biology, 28: 11371143. https://doi.org/10.1016/j.cub.2018.02.045.CrossRefGoogle ScholarPubMed
Merck, Manuals. 2015. Ectoparasiticides used in small animals: pharmacology (veterinary manual) [online]. Available from http://www.msdvetmanual.com/pharmacology/ectoparasiticides/ectoparasiticides-used-in-small-animals [accessed 21 May 2019].Google Scholar
Miller, W.E. 1977. Wing measure as a size index in Lepidoptera: the family Olethreutidae. Annals of the Entomological Society of America, 70: 253256. https://doi.org/10.1093/aesa/70.2.253.CrossRefGoogle Scholar
Miller, W.E. 1991. Body size in North American Lepidoptera as a related to geography. Journal of the Lepidopterists’ Society, 45: 158168.Google Scholar
Mörtl, M., Kereki, O., Daryas, B., Kláyik, S., Vehovszky, Á., Gyri, J., and Székács, A. 2016. Study on soil mobility of two neonicotinoid insecticides. Journal of Chemistry, 2016: 4546584. http://dx.doi.org/10.1155/2016/4546584.CrossRefGoogle Scholar
Oberhauser, K.S. 1988. Male monarch butterfly spermatophore mass and mating strategies. Animal Behaviour, 36: 13841388. https://doi.org/ 10.1016/S0003-3472(88)80208-2.CrossRefGoogle Scholar
Oberhauser, K.S. 1997. Fecundity, lifespan and egg mass in butterflies: effects of male-derived nutrients and female size. Functional Ecology, 11: 166175. https://doi.org/10.1046/j.1365-2435.1997.00074.x CrossRefGoogle Scholar
Oberhauser, K.S. 2004. Overview of monarch breeding biology. In The monarch butterfly: biology and conservation. Edited by K.S. Oberhauser and M.J. Solensky. Cornell Press, New York, New York, United States of America. Pp. 37.Google Scholar
Olaya-Arenas, P., Hauri, K., Scharf, M.E., and Kaplan, I. 2020. Larval pesticide exposure impacts monarch butterfly performance. Scientific Reports, 10: 14490. https://doi.org/10.1038/s41598-020-71211-7.CrossRefGoogle ScholarPubMed
Olaya-Arenas, P. and Kaplan, I. 2019. Quantifying pesticide exposure risk for monarch caterpillars on milkweeds bordering agricultural land. Frontiers in Ecology and Evolution, 7: 116. https://doi.org/10.3389/fevo.2019.00223.CrossRefGoogle Scholar
Pecenka, J. and Lundgren, J. 2015. Non-target effects of clothianidin on monarch butterflies. Science of Nature, 102: 19. https://doi.org/10.1007/s00114-015-1270-y.CrossRefGoogle ScholarPubMed
Perestrelo, R., Silva, P., Porto-Figueira, P., Pereira, J.A.M., Silva, C., Medina, S., and Câmara, J.S. 2019. QuEChERS: fundamentals, relevant improvements, applications and future trends. Analytica Chimica Acta, 1070: 128.CrossRefGoogle ScholarPubMed
Pitman, G.M., Flockhart, D.T.T., and Norris, D.R. 2018. Patterns and causes of oviposition in monarch butterflies: implications for milkweed restoration. Biological Conservation, 217: 5465. https://doi.org/10.1016/j.biocon.2017.10.019.CrossRefGoogle Scholar
R Core Team. 2015a. stats: the R stats package [online]. Available from https://stat.ethz.ch/R-manual/R-devel/library/stats/html/stats-package.html.Google Scholar
R Core Team. 2015b. R: a language and environment for statistical computing [online]. R Foundation for Statistical Computing, Vienna, Austria. Available from https://www.r-project.org/ [accessed 6 September 2019].Google Scholar
Sánchez-Bayo, F., Goka, K., and Hayasaka, D. 2016. Contamination of the aquatic environment with neonicotinoids and its implication for ecosystems. Frontiers in Environmental Science, 4: 71. https://doi.org/10.3389/fenvs.2016.00071.CrossRefGoogle Scholar
Sandrock, C., Tnaadini, L.G., Lorenzo, J.S., Biesmeijer, J.C., Potts, S.G., and Neumann, P. 2014a. Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agricultural and Forest Entomology, 16: 119128. https://doi.org/10.1111/afe.12041.CrossRefGoogle Scholar
Sandrock, C., Tanadini, M., Tanadini, L.G., Fauser-Misslin, A., Potts, S.G., and Neumann, P. 2014b. Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLOS One, 9: e103592. https://doi.org/10.1371/journal.pone.0103592.CrossRefGoogle ScholarPubMed
Schelling, D. and Jones, G. 1996. Analysis of induction of hsc70, hsp82 and juvenile hormone esterase genes by heat shock in Trichoplusia ni . Journal of Insect Physiology, 42: 295301. https://doi.org/10.1016/0022-1910(95)00094-1.CrossRefGoogle Scholar
Simon-Delso, N., Amaral-Rogers, V., Belzunces, L.P., Bonmatin, J.M., Chagnon, M., Downs, C., et al. 2015. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environmental Science and Pollution Research, 22: 534. https://doi.org/10.1007/s11356-014-3470-y.CrossRefGoogle ScholarPubMed
Thogmartin, W.E., López-Hoffman, L., Rohweder, J., Diffendorfer, J., Drum, R., Semmens, D., et al. 2017b. Restoring monarch butterfly habitat in the midwestern US: ‘all hands on deck.’ Environmental Research Letters, 12: 074005. https://doi.org/10.1088/1748-9326/aa7637.CrossRefGoogle Scholar
Thogmartin, W.E., Wiederholt, R., Oberhauser, K., Dunn, R.G., Diffendorfer, J.E., Altizer, S., et al. 2017a. Monarch butterfly population decline in North America: identifying the threatening processes. Royal Society Open Science, 4: 170760. https://doi.org/10.6084/m9.figshare.c.3876100.CrossRefGoogle ScholarPubMed
United States Geological Survey. 2018. Pesticide national synthesis project: estimated annual agricultural pesticide use, pesticide use maps [online]. Available from https://water.usgs.gov/nawqa/pnsp/usage/maps/ [accessed 29 May 2018].Google Scholar
Wang, J. and Daniel, L. 2009. Determination of 142 pesticides in fruit and vegetable based infant foods by liquid chromatography/electrospray ionization–tandem mass spectrometry and estimation of measurement uncertainty. Journal of AOAC International, 92: 279301.CrossRefGoogle ScholarPubMed
Whitehorn, P.R., Norville, G., Gilburn, A., and Goulson, D. 2018. Larval exposure to the neonicotinoid imidacloprid impacts adult size in the farmland butterfly Pieris brassicae . PeerJ, 6: e4772. https://doi.org/10.7717/peerj.4772.CrossRefGoogle ScholarPubMed
Wilcox, A.A.E., Flockhart, D.T.T., Newman, A.E.M., and Norris, D.R. 2019. An evaluation of studies on the potential threats contributing to the decline of Eastern migratory North American monarch butterflies (Danaus plexippus). Frontiers in Ecology & Evolution, 7: 99. https://doi.org/10.3389/fevo.2019.00099.CrossRefGoogle Scholar
Williams, G.R., Troxler, A., Retschnig, G., Roth, K., Yañez, O., Shutler, D., et al. 2015. Neonicotinoid pesticides severely affect honey bee queens. Scientific Reports, 5: 14621. https://doi.org/10.1038/srep14621.CrossRefGoogle ScholarPubMed
Zalucki, M.P. and Rochester, W.A. 2014. Spatial and temporal population dynamics of monarchs down-under: lessons for North America. In The monarch butterfly: biology and conservation. Edited by K.S. Oberhauser and M.J. Solensky. Cornell University Press, New York, New York, United States of America. Pp 219228.Google Scholar
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