Are neonicotinoid insecticides driving declines of widespread butterflies?

PeerJ

Volumn 2015, Issue 11, 2015, Pages

  Gilburn, Andre S ^a   Bunnefeld, Nils ^a   McVean Wilson, John ^a   Botham, Marc S ^b   Brereton, Tom M ^c   Fox, Richard ^c   Goulson, Dave ^d  

^a UNIVERSITY OF STIRLING   (United Kingdom)

^b Biological Records Centre   (United Kingdom)

^c BUTTERFLY CONSERVATION   (United Kingdom)

^d UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Agricultural intensification; Butterfly; Climate; Neonicotinoids; Pesticides; Species declines

Indexed keywords

NEONICOTINOID; RAIN;

AGRICULTURAL LAND; ARTICLE; BIODIVERSITY; BUTTERFLY; CLIMATE CHANGE; HABITAT; NONHUMAN; PIERIS BRASSICAE; PIERIS RAPAE; SPRING; SUMMER; TEMPERATURE;

EID: 84949671205     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.1402     Document Type: Article

References (41)

1. Baskaran S, Kookana RS, Naidu R. 1999. Degradation of bifenthrin, chlorpyrifos and imidacloprid in soil and bedding materials at termiticidal application rates. Pesticide Science 55:1222-1228 DOI 10.1002/(SICI)1096-9063(199912)55:12¡1222::AID-PS83¿3.0.CO;2-7.
2. Batary P, Dicks LV, Kleijn D, Sutherland WJ. 2015. The role of agri-environment schemes in conservation and environmental management. Conservation Biology 29:1006-1016 DOI 10.1111/cobi.12536.
3. Blacquiére T, Smagghe G, Van Gestel CAM,Mommaerts V. 2012. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973-992 DOI 10.1007/s10646-012-0863-x.
4. Bonmatin J-M, Giorio C, Girolami V, Goulson D, Kreutzweiser D, Krupke C, Liess M, Long E, Marzaro M,Mitchell E, Noome D, Simon-Delso N, Tapparo A. 2015. Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research 22:35-67 DOI 10.1007/s11356-014-3332-7.
5. Brereton TM, Roy DB,Middlebrook I, Botham M,Warren M. 2011. The development of butterfly indicators in the United Kingdom and assessments in 2010. Journal of Insect Conservation 15:139-151 DOI 10.1007/s10841-010-9333-z.
6. Byrne FJ, Toscano NC. 2006. Uptake and persistence of imidacloprid in grapevines treated by chemigation. Crop Protection 85:831-834 DOI 10.1016/j.cropro.2005.11.004.
7. Castle SJ, Byrne FJ, Bi JL, Toscano NC. 2005. Spatial and temporal distribution of imidacloprid and thiamethoxam in citrus and impact on Homalodisca coagulata populations. Pest Management Science 64:75-84 DOI 10.1002/ps.949.
8. Cresswell JE. 2011. A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149-157 DOI 10.1007/s10646-010-0566-0.
9. Cutler GC, Scott-Dupree CD. 2007. Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. Journal of Economic Entomology 100:765-772 DOI 10.1603/0022-0493(2007)100[765:ETCSCH]2.0.CO;2.
10. De Cant J, Barrett M. 2010. Environmental fate and ecological risk assessment for the registration of clothianidin for use as a seed treatment on mustard seed (oilseed and condiment) and cotton. United States Environmental Protection Agency Report.
11. Defra. 2014. Pesticide usage statistics. Available at https://secure.fera.defra.gov.uk/pusstats/ (accessed June 2014).
12. Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F, Gargiulo G, Pennachio F. 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences of the United States of America 110:18466-18471 DOI 10.1073/pnas.1314923110.
13. Dias PC. 1996. Sources and sinks in population biology. Trends in Ecology and Evolution 12:326-330 DOI 10.1016/0169-5347(96)10037-9.
14. Donald PF, Green RE, Heath MF. 2001. Agricultural intensification and the collapse of Europe's farmland bird populations. Proceedings of the Royal Society B 268:25-29 DOI 10.1098/rspb.2000.1325.
15. Elbert A, Haas M, Springer B, Thielert W, Nauen R. 2008. Applied aspects of neonicotinoid uses in crop protection. Pest Management Science 64:1099-1105 DOI 10.1002/ps.1616.
16. Fox R, Brereton TM, Asher J, Botham MS,Middlebrook I, Roy DB,Warren MS. 2011. The State of the UK's Butterflies 2011. Butterfly Conservation and the Centre for Ecology & Hydrology, Wareham, Dorset. Available at https://butterfly-conservation.org/files/soukb2011.pdf (accessed January 2015).
17. Gelman A, Hill J. 2007. Data analysis using regression and multilevel/hierarchical models. Cambridge: Cambridge University Press.
18. Gibbs KE,Mackey RL, Currie DJ. 2009. Human landuse, agriculture, pesticides and losses of imperiled species. Diversity and Distributions 15:242-253 DOI 10.1111/j.1472-4642.2008.00543.x.
19. Gill RJ, Ramos-Rodriguez O, Raine NE. 2012. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105-108 DOI 10.1038/nature11585.
20. Girolami V,Marzaro M, Vivan L,Mazzon L, Giorio C,Marton D, Tapparo A. 2013. Aerial powdering of bees inside mobile cages and the extent of neonicotinoid cloud surrounding corn drillers. Journal of Applied Entomology 137:35-44 DOI 10.1111/j.1439-0418.2012.01718.x.
21. Godfray HCJ, Blacquiere T, Field LM, Hails RS, Petrokofsky G, Potts SG, Raine NE, Vanbergen AJ,McLean AR. 2014. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B 281:20140558 DOI 10.1098/rspb.2014.0558.
22. Goulson D. 2013. An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology 50:977-987 DOI 10.1111/1365-2664.12111.
23. Goulson D. 2014. Pesticides linked to bird declines. Nature 511:295-296 DOI 10.1038/nature13642.
24. Hallmann CA, Foppen RPB, Van Turnhout CAM, De Kroon H, Jongejans E. 2014. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511:341-343 DOI 10.1038/nature13531.
25. Henry M, Beguin M, Requier F, Rollin O, Odoux JF, Aupinel P, Aptel J, Tchamitchian S, Decourtye A. 2012. A common pesticide decreases foraging success and survival in honey bees. Science 336:348-350 DOI 10.1126/science.1215039.
26. JNCC. 2015. Expenditure on UK and international biodiversity. Available at http://jncc.defra.gov. uk/page-4251 (accessed May 2015).
27. Kleijn D, Kohler F, Baldi A, Batary P, Concepcíon ED, Clough Y, Diaz M, Gabriel D, Holzschuh A, Knop E, Kovacs A,Marshall EJP, Tscharntke T, Verhulst J. 2009. On the relationship between farmland biodiversity and land-use intensity in Europe. Proceedings of the Royal Society B 276:903-909 DOI 10.1098/rspb.2008.1509.
28. Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K. 2012. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7:e29268 DOI 10.1371/journal.pone.0029268.
29. Met Office. 2014. UK climate datasets. Available at http://www.metoffice.gov.uk/climate/uk/datasets/ (accessed June 2014).
30. Oliver JB, Fare DC, Youssef N, Scholl SS, Reding ME, Ranger CM,Moyseenko JJ, Halcomb MA. 2010. Evaluation of a single application of neonicotinoid and multi-application contact insecticides for flatheaded borer management in field grown red maple cultivars. Journal of Environmental Horticulture 28:135-149.
31. Oliver TH, Hill JK, Thomas CD, Brereton T, Roy DB. 2009. Changes in habitat specificity of species at their climatic range boundaries. Ecology Letters 12:1091-1102 DOI 10.1111/j.1461-0248.2009.01367.x.
32. Pilling E, Campbell P, Coulson M, Ruddle N, Tornier I. 2013. A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS ONE 8:e77193-e77193 DOI 10.1371/journal.pone.0077193.
33. Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M,McField M,Morrissey CA, Noome DA, Settele J, Simon-Delso N, Stark JD, Van der Sluijs JP, Van Dyck H,Wiemers M. 2015. Effects of neonicotinoids and fipronil on non-target invertebrates. Environmental Science and Pollution Research 22:68-102 DOI 10.1007/s11356-014-3471-x.
34. R Development Core Team. 2015. R: a language and environment for statistical computing. Vienna: The R Foundation for Statistical Computing. Available at http://www.r-project.org/ (accessed July 2015).
35. Roy DB, Rothery P,Moss D, Pollard E, Thomas JA. 2001. Butterfly numbers and weather: predicting historical trends in abundance and the future effects of climate change. Journal of Animal Ecology 70:201-217 DOI 10.1046/j.1365-2656.2001.00480.x.
36. Rundlöf M, Andersson GKS, Bommarco R, Fries I, HederstromV, Jonsson O, Klatt BK, Pedersen TR, Yourstone J, Smith HG. 2015. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521:77-80 DOI 10.1038/nature14420.
37. Stewart SD, Lorenz GM, Catchot AL, Gore J, Cook D, Skinner J,Mueller TC, Johnson DR, Zawislak J, Barber J. 2014. Potential exposure of pollinators to neonicotinoid insecticides from the use of insecticide seed treatments in the mid-southern United States. Environtal Science and Technology 48:9762-9769 DOI 10.1021/es501657w.
38. Sur R, Storl A. 2003. Uptake, translocation and metabolism of imidacloprid in plants. Bulletin of Insectology 56:35-40.
39. Van Dyck H, Van Strien AJ,Maes D, Van Swaay CAM. 2009. Declines in common, widespread butterflies in a landscape under intense human use. Conservation Biology 23:957-965 DOI 10.1111/j.1523-1739.2009.01175.x.
40. Warren MS, Hill JK, Thomas JA, Asher J, Fox R, Huntley B, Roy DB, Telfer MG, Jeffcoate S, Harding P, Jeffcoate G,Willis SG, Greatorex-Davies JN,Moss D, Thomas CD. 2001. Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414:65-69 DOI 10.1038/35102054.
41. Whitehorn PR, O'Connor S,Wackers FL, Goulson D. 2012. Neonicotinoid pesticides reduces bumble bee colony growth and queen production. Science 336:351-352 DOI 10.1126/science.1215025.