Potts, S. G. et al. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010).
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).
Ollerton, J. Pollinator diversity: Distribution, ecological function, and conservation. Ann. Rev. Ecol. Evol. Syst. 48, 353–376 (2017).
Botías, C. et al. Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environ. Sci. Technol. 49, 12731–12740 (2015).
Botías, C., David, A., Hill, E. M. & Goulson, D. Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects. Sci. Tot. Environ. 566, 269–278 (2016).
Long, E. Y. & Krupke, C. H. Non-cultivated plants present a season-long route of pesticide exposure for honey bees. Nat. Commun. 7, 11629 (2016).
Mogren, C. L. & Lundgren, J. G. Neonicotinoid-contaminated pollinator strips adjacent to cropland reduce honey bee nutritional status. Sci. Rep. 6, 29608 (2016).
Tsvetkov, N. et al. Chronic exposure to neonicotinoids reduces honey-bee health near corn crops. Science 356, 1395–1397 (2017).
Wood, T. J., Kaplan, I., Zhang, Y. & Szendrei, Z. Honeybee dietary neonicotinoid exposure is associated with pollen collection from agricultural weeds. Proc. R. Soc. B 286, 20190989 (2019).
Douglas, M. R. & Tooker, J. F. Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in US field crops. Environ. Sci. Technol. 49, 5088–5097 (2015).
DiBartolomeis, M., Kegley, S., Mineau, P., Radford, R. & Klein, K. An assessment of acute insecticide toxicity loading (AITL) of chemical pesticides used on agricultural land in the United States. PLoS One 14, e0220029 (2019).
Douglas, M. R., Sponsler, D. B., Lonsdorf, E. V. & Grozinger, C. M. County-level analysis reveals a rapidly shifting landscape of insecticide hazard to honey bees (Apis mellifera) on US farmland. Sci. Rep. 10, 797 (2020).
Gilburn, A. S. et al. Are neonicotinoid insecticides driving declines of widespread butterflies?. PeerJ 3, e1402 (2015).
Forister, M. L. et al. Increasing neonicotinoid use and the declining butterfly fauna of lowland California. Biol. Lett. 12, 20160475 (2016).
Wepprich, T., Adrion, J. R., Ries, L., Wiedmann, J. & Haddad, N. M. Butterfly abundance declines over 20 years of systematic monitoring in Ohio, USA. PLoS One 14, e0216270 (2019).
Braak, N., Neve, R., Jones, A. K., Gibbs, M. & Breuker, C. J. The effects of insecticides on butterflies: A review. Environ. Pollut. 242, 507–518 (2018).
Mulé, R., Sabella, G., Robba, L. & Manachini, B. Systematic review of the effects of chemical insecticides on four common butterfly families. Front. Environ. Sci. 5, 32 (2017).
Russell, C. & Schultz, C. B. Effects of grass-specific herbicides on butterflies: An experimental investigation to advance conservation efforts. J. Insect Conserv. 14, 53–63 (2009).
Bohnenblust, E., Egan, J. F., Mortensen, D. & Tooker, J. Direct and indirect effects of the synthetic-auxin herbicide dicamba on two lepidopteran species. Environ. Entomol. 42, 586–594 (2013).
Hahn, M., Geisthardt, M. & Bruhl, C. A. Effects of herbicide-treated host plants on the development of Mamestra brassicae L. caterpillars. Environ. Toxicol. Chem. 33, 2633–2638 (2014).
Stark, J. D., Chen, X. D. & Johnson, C. Effects of herbicides on Behr’s Metalmark butterfly, a surrogate species for the endangered butterfly, Lange’s Metalmark. Environ. Pollut. 164, 24–27 (2012).
Eliyahu, D., Applebaum, S. W. & Rafaeli, A. Moth sex-pheromone biosynthesis is inhibited by the herbicide diclofop. Pestic. Biochem. Physiol. 77, 75–81 (2003).
Srivastava, K., Sharma, S., Sharma, D. & Kumar, R. Effect of fungicides on growth and development of Spodoptera litura. Int. J. Life Sci. Sci. Res. 3, 905–908 (2017).
Nicodemo, D. et al. Pyraclostrobin impairs energetic mitochondrial metabolism and productive performance of silkworm (Lepidoptera: Bombycidae) caterpillars. J. Econ. Entomol. 111, 1369 (2018).
Pilling, E. D. & Jepson, P. C. Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic. Sci. 39, 293–297 (1993).
Pilling, E. D., Bromley-Challenor, K. A. C., Walker, C. H. & Jepson, P. C. Mechanism of synergism between the pyrethroid insecticide λ-cyhalothrin and the imidazole fungicide prochloraz, in the honeybee (Apis mellifera L). Pestic. Biochem. Physiol. 51, 1–11 (1995).
Johnson, R. M., Ellis, M. D., Mullin, C. A. & Frazier, M. Pesticides and honey bee toxicity—USA. Apidologie 41, 312–331 (2010).
Wade, A., Lin, C. H., Kurkul, C., Regan, E. & Johnson, R. M. Combined toxicity of insecticides and fungicides applied to California almond orchards to honey bee larvae and adults. Insects 10, 20 (2019).
Lichtenstein, E. P., Liang, T. T. & Anderegg, B. N. Synergism of insecticides by herbicides. Science 181, 847–849 (1973).
James, D. G. 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 (2019).
Sinha, S. N., Lakhani, K. H. & Davis, B. N. K. Studies on the toxicity of insecticidal drift to the first instar larvae of the large white butterfly Pieris brassicae (Lepidoptera: Pieridae). Ann. Appl. Biol. 116, 27–41 (1990).
Davis, B. N. K., Lakhani, K. H. & Yates, T. J. The hazards of insecticides to butterflies of field margins. Agric. Ecosyst. Environ. 36, 151–161 (1991).
Çilgi, T. & Jepson, P. C. The risks posed by deltamethrin drift to hedgerow butterflies. Environ. Pollut. 87, 1–9 (1995).
Whitehorn, P. R., Norville, G., Gilburn, A. & Goulson, D. Larval exposure to the neonicotinoid imidacloprid impacts adult size in the farmland butterfly Pieris brassicae. PeerJ 6, e4772 (2018).
Agrawal, A. A. & Inamine, H. Mechanisms behind the monarch’s decline. Science 360, 1294–1296 (2018).
Belsky, J. & Joshi, N. K. Assessing role of major drivers in recent decline of monarch butterfly population in North America. Front. Environ. Sci. 6, 86 (2018).
Malcolm, S. B. Anthropogenic impacts on mortality and population viability of the monarch butterfly. Ann. Rev. Entomol. 63, 277–302 (2018).
Hartzler, R. G. Reduction in common milkweed (Asclepias syriaca) occurrence in Iowa cropland from 1999 to 2009. Crop Prot. 29, 1542–1544 (2010).
Pleasants, J. M. & Oberhauser, K. S. Milkweed loss in agricultural fields because of herbicide use: Effect on the monarch butterfly population. Insect Conserv. Div. 6, 135–144 (2013).
Thogmartin, W. E. et al. Monarch butterfly population decline in North America: Identifying the threatening processes. R. Soc. Open. Sci. 4, 170760 (2017).
Thogmartin, W. E. et al. Restoring monarch butterfly habitat in the Midwestern US: ‘all hands on deck’. Environ. Res. Lett. 12, 074005 (2017).
Saunders, S. P., Ries, L., Oberhauser, K. S., Thogmartin, W. E. & Zipkin, E. F. Local and cross-seasonal associations of climate and land use with abundance of monarch butterflies Danaus plexippus. Ecography 41, 278–290 (2018).
Stenoien, C. et al. Monarchs in decline: A collateral landscape-level effect of modern agriculture. Insect Sci. 25, 528–541 (2018).
Krischik, V., Rogers, M., Gupta, G. & Varshney, A. Soil-applied imidacloprid translocates to ornamental flowers and reduces survival of adult Coleomegilla maculata, Harmonia axyridis, and Hippodamia convergens lady beetles, and larval Danaus plexippus and Vanessa cardui butterflies. PLoS One 10, e0119133 (2015).
Krishnan, N. et al. Assessing field-scale risks of foliar insecticide applications to monarch butterfly (Danaus plexippus) larvae. Environ. Toxicol. Chem. 39, 923–941 (2020).
Pecenka, J. R. & Lundgren, J. G. Non-target effects of clothianidin on monarch butterflies. Sci. Nat. 102, 19 (2015).
Bargar, T. A., Hladik, M. L. & Daniels, J. C. Uptake and toxicity of clothianidin to monarch butterflies from milkweed consumption. PeerJ 8, e8669 (2020).
Hartzler, R. G. & Buhler, D. D. Occurrence of common milkweed (Asclepias syriaca) in cropland and adjacent areas. Crop Prot. 19, 363–366 (2000).
Zaya, D. N., Pearse, I. S. & Spyreas, G. Long-term trends in midwestern milkweed abundances and their relevance to monarch butterfly declines. Bioscience 67, 343–356 (2017).
Agrawal, A. A. & Fishbein, M. Plant defense syndromes. Ecology 87, S132–S149 (2006).
Lefevre, T., Oliver, L., Hunter, M. D. & de Roode, J. C. Evidence for trans-generational medication in nature. Ecol. Lett. 13, 1485–1493 (2010).
Olaya-Arenas, P. & Kaplan, I. Quantifying pesticide exposure risk for monarch caterpillars on milkweeds bordering agricultural land. Front. Ecol. Evol. 7, 223 (2019).
Olaya-Arenas, P., Scharf, M. E. & Kaplan, I. Do pollinators prefer pesticide-free plants? An experimental test with monarchs and milkweeds. J. Appl. Ecol. 20, 20 (2020).
Bauerfeind, S. S., Fischer, K., Hartstein, S., Janowitz, S. & Martin-Creuzburg, D. Effects of adult nutrition on female reproduction in a fruit-feeding butterfly: The role of fruit decay and dietary lipids. J. Insect Physiol. 53, 964–973 (2017).
Geister, T. L., Lorenz, M. W., Hoffmann, K. H. & Fischer, K. Adult nutrition and butterfly fitness: Effects of diet quality on reproductive output, egg composition, and egg hatching success. Front. Zool. 5, 10 (2008).
Van Hook, T., Williams, E. H., Brower, L. P., Borkin, S. & Hein, J. A standardized protocol for ruler-based measurement of wing length in monarch butterflies, Danaus plexippus L. (Nymphalidae, Danainae). Trop. Lep. Res. 22, 42–52 (2012).
Davis, A. K. & Holden, M. T. Measuring intraspecific variation in flight-related morphology of monarch butterflies (Danaus plexippus): Which sex has the best flying gear?. J. Insects 20, 591705 (2015).
García-Barros, E. Multivariate indices as estimates of dry body weight for comparative study of body size in Lepidoptera. Nota Lepi. 38, 59–74 (2015).
Wiesweg, M. Survival Analysis: High-Level Interface for Survival Analysis and Associated Plots. R Package Version 0.1.1. (2019). https://CRAN.R-project.org/package=survivalAnalysis.
Wickham, et al. Welcome to the tidyverse. J. Open Source Softw. 4, 1686 (2019).
Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plots. R Package Version 0.2.5. (2020). https://CRAN.R-project.org/package=ggpubr.
Kassambara, A. Rstatix: Pipe-Friendly Framework for Basic Statistical Tests. R package version 0.4.0. (2020). https://CRAN.R-project.org/package=rstatix.
Fox, J. & Weisberg, S. An R Companion to Applied Regression 3rd edn. (Sage, Thousand Oaks, 2019).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, New York, 2016).
Kassambara, A. ggcorrplot: Visualization of a Correlation Matrix Using ‘ggplot2’. R Package Version 0.1.3. (2019) https://CRAN.R-project.org/package=ggcorrplot.
Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).
Schaarschmidt, F. & Gerhard, D. pairwiseCI: Confidence Intervals for Two-Sample Comparisons. R Package Version 0.1-27. (2019) https://CRAN.R-project.org/package=pairwiseCI.
Thompson, H. M., Fryday, S. L., Harkin, S. & Milner, S. Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie 45, 545–553 (2014).
Tadei, R. et al. Late effect of larval co-exposure to the insecticide clothianidin and fungicide pyraclostrobin in Africanized Apis mellifera. Sci. Rep. 9, 3277 (2019).
Després, L., David, J. P. & Gallet, C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22, 298–307 (2007).
Jones, P. L., Petschenka, G., Flacht, L. & Agrawal, A. A. Cardenolide intake, sequestration, and excretion by the monarch butterfly along gradients of plant toxicity and larval ontogeny. J. Chem. Ecol. 45, 264–277 (2019).
Karageorgi, M. et al. Genome editing retraces the evolution of toxin resistance in the monarch butterfly. Nature 574, 409–412 (2019).
Hardy, N. B., Peterson, D. A., Ross, L. & Rosenheim, J. A. Does a plant-eating insect’s diet govern the evolution of insecticide resistance? Comparative tests of the pre-adaptation hypothesis. Evol. Appl. 11, 739–747 (2018).
Basley, K. & Goulson, D. Effects of field-relevant concentrations of clothianidin on larval development of the butterfly Polyommatus icarus (Lepidoptera, Lycaenidae). Environ. Sci. Technol. 52, 3990–3996 (2018).
Halsch, C. et al. Pesticide contamination of milkweeds across the agricultural, urban, and open spaces of low elevation Northern California. Front. Ecol. Evol. 8, 162 (2020).
Altizer, S. & Davis, A. K. Populations of monarch butterflies with different migratory behaviors show divergence in wing morphology. Evolution 64, 1018–1028 (2010).
Dockx, C. Directional and stabilizing selection on wing size and shape in migrant and resident monarch butterflies, Danaus plexippus (L.). Cuba. Biol. J. Linn. Soc. 92, 605–616 (2007).
Satterfield, D. A. & Davis, A. K. Variation in wing characteristics of monarch butterflies during migration: Earlier migrants have redder and more elongated wings. Anim. Migr. 2, 1–7 (2014).
Freedman, M. G. & Dingle, H. Wing morphology in migratory North American monarchs: Characterizing sources of variation and understanding changes through time. Anim. Migr. 5, 61–73 (2018).
Inamine, H., Ellner, S. P., Springer, J. P. & Agrawal, A. A. Linking the continental migratory cycle of the monarch butterfly to understand its population decline. Oikos 125, 1081–1091 (2016).
Nylin, S. & Gotthard, K. Plasticity in life-history traits. Ann. Rev. Entomol. 43, 63–83 (1998).
Awmack, C. S. & Leather, S. R. Host plant quality and fecundity in herbivorous insects. Ann. Rev. Entomol. 47, 817–844 (2002).
Jervis, M. A., Boggs, C. L. & Ferns, P. N. Egg maturation strategy and its associated trade-offs: A synthesis focusing on Lepidoptera. Ecol. Entomol. 30, 359–375 (2005).
Oberhauser, K. S. Fecundity, lifespan and egg mass in butterflies: Effects of male-derived nutrients and female size. Funct. Ecol. 11, 166–175 (1997).
Main, A. R., Webb, E. B., Goyne, K. W. & Mengel, D. Neonicotinoid insecticides negatively affect performance measures of non-target terrestrial arthropods: A meta-analysis. Ecol. Appl. 28, 1232–1244 (2018).
Source: Ecology - nature.com
