Negative effects of pesticides on wild bee communities can be buffered by landscape context

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1809, 2015, Pages

  Park, Mia G ^a,b   Blitzer, E J ^a,c   Gibbs, Jason ^a,d   Losey, John E ^a   Danforth, Bryan N ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF NORTH DAKOTA   (United States)

^c Carroll College   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Agroecosystem; Apple; Native bees; Orchards; Pest management

Indexed keywords

ABUNDANCE; AGRICULTURAL ECOSYSTEM; BEE; LANDSCAPE STRUCTURE; NATIVE SPECIES; ORCHARD; PESTICIDE APPLICATION; POLLINATOR; POLLUTION EFFECT; SPECIES RICHNESS; TOLERANCE; WILD POPULATION;

APOIDEA; MALUS X DOMESTICA;

INSECTICIDE;

AGRICULTURE; ANIMAL; BEE; BIOTA; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MALUS; NEW YORK; POLLINATION;

AGRICULTURE; ANIMALS; BEES; BIOTA; INSECTICIDES; MALUS; NEW YORK; POLLINATION;

EID: 84931292258     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.0299     Document Type: Article

References (72)

1. Klein A-M, Vaissiére BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T. 2007 Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313. (doi:10.1098/rspb.2006.3721)
2. Eilers EJ, Kremen C, Greenleaf SS, Garber AK, Klein A-M. 2011 Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS ONE 6, e21363. (doi:10.1371/journal.pone.0021363)
3. Ascher JS, Pickering J. 2015 Discover life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). [Updated 2015 Mar 9; cited 2015 May 18]. See: http://www.discoverlife.org/mp/20q?/guide=Apoidea species.
4. National Research Council. 2007 Status of pollinators in North America. Washington, DC: The National Academies Press.
5. Oldroyd BP. 2007 What’s killing American honey bees? PLoS Biol. 5, e168. (doi:10.1371/journal.pbio.0050168)
6. van Engelsdorp D et al. 2009 Colony collapse disorder: a descriptive study. PLoS ONE 4, e6481. (doi:10.1371/journal.pone.0006481)
7. Winfree R. 2008 Pollinator-dependent crops: an increasingly risky business. Curr. Biol. 18, 968–969. (doi:10.1016/j.cub.2008.09.010)
8. Garibaldi LA et al. 2013 Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611. (doi:10.1126/science.1230200)
9. Tylianakis JM. 2013 The global plight of pollinators. Science 339, 1532–1533. (doi:10.1126/science.1235464)
10. Kremen K, Williams NM, Bugg R, Fay J, Thorp RW. 2004 The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecol. Lett. 7, 1109–1119. (doi:10.1111/j.1461-0248.2004.00662.x)
11. Garibaldi LA et al. 2011 Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett. 14, 1062–1072. (doi:10.1111/j.1461-0248.2011.01669.x)
12. Klein A-M. 2009 Nearby rainforest promotes coffee pollination by increasing spatio-temporal stability in bee species richness. For. Ecol. Manag. 258, 1838–1845. (doi:10.1016/j.foreco.2009.05.005)
13. Meehan TD, Werling BP, Landis DA, Gratton C. 2011 Agricultural landscape simplification and insecticide use in the Midwestern United States. Proc. Natl Acad. Sci. USA 108, 11 500–11 505. (doi:10.1073/pnas.1100751108)
14. Kremen C et al. 2007 Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol. Lett. 10, 299–314. (doi:10.1111/j.1461-0248.2007.01018.x)
15. Ricketts TH et al. 2008 Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11, 499–515. (doi:10.1111/j.1461-0248.2008.01157.x)
16. Winfree R, Aguilar R, Vázquez DP, LeBuhn G, Aizen MA. 2009 A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076. (doi:10.1890/08-1245.1)
17. Viana BF, Boscolo D, Mariano Neto E, Lopes L, Lopes A, Fereira P, Pigozzo CM, Primo L. 2012 How well do we understand landscape effects on pollinators and pollination services? J. Pollinat. Ecol. 7, 31–41.
18. Kennedy CM et al. 2013 A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599. (doi:10.1111/ele.12082)
19. Kevan P. 1975 Forest application of the insecticide fenitrothion and its effect on wild bee pollinators (Hymenoptera: Apoidea) of lowbush blueberries (Vaccinium SPP.) in Southern New Brunswick, Canada. Biol. Conserv. 7, 301–309. (doi:10.1016/0006-3207(75)90045-2)
20. Desneux N, Decourtye A, Delpuech J-M. 2007 The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106. (doi:10.1146/annurev.ento.52.110405.091440)
21. Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G. 2010 Risk assessment for side effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19, 207–215. (doi:10.1007/s10646-009-0406-2)
22. Henry M, Béguin M, Requier F, Rollin O, Odoux J-F, 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:w10.1126/science.1215039)
23. Whitehorn PR, O’Connor S, Wackers FL, Goulson D. 2012 Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352. (doi:10.1126/science.1215025)
24. Pettis JS, Lichtenberg EM, Andree M, Stitzinger J, Rose R, vanEngelsdorp D. 2013 Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8, e70182. (doi:10.1371/journal.pone.0070182)
25. Ladurner E, Bosch J, Kemp WP, Maini S. 2005 Assessing delayed and acute toxicity of five formulated fungicides to Osmia lignaria Say and Apis mellifera. Apidologie 36, 449–460. (doi:10.1051/apido:2005032)
26. Alston DG, Tepedino VJ, Bradley BA, Toler TR, Griswold TL, Messinger SM. 2007 Effects of the insecticide phosmet on solitary bee foraging and nesting in orchards of Capitol Reef National Park, Utah. Environ. Entomol. 36, 811–816. (doi:10.1093/ee/36.4.811)
27. Sandrock C, Tanadini LG, Pettis JS, Biesmeijer JC, Potts SG, Neumann P. 2014 Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agric. For. Entomol. 16, 119–128. (doi:10.1111/afe.12041)
28. Brittain C, Potts SG. 2011 The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl. Ecol. 12, 321–331. (doi:10.1016/j.baae.2010.12.004)
29. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS. 2010 High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5, e9754. (doi:10.1371/journal.pone.0009754)
30. USDA National Agricultural Statistics Service. 2014 Census of Agriculture 2012. USDA-NASS, Washington, DC. Available at http://www.agcensus.usda.gov/Publications/2012/
31. Greenleaf SS, Williams NM, Winfree R, Kremen C. 2007 Bee foraging ranges and their relationship to body size. Oecologia 153, 589–596. (doi:10.1007/s00442-007-0752-9)
32. Zurbuchen A, Landert L, Klaiber J, Müller A, Hein S, Dorn S. 2010 Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol. Conserv. 143, 669–676. (doi:10.1016/j.biocon.2009.12.003)
33. ESRI. 2011 ArcGIS Desktop: Release 10 Redlands, CA: Environmental Systems Research Institute. Available at http://www.esri.com/software/arcgis/arcgis-for-desktop.
34. USDA National Agricultural Statistics Service Cropland Data Layer. 2010 Published crop-specific data layer [Online]. USDA-NASS, Washington, DC. Available at http://nassgeodata.gmu.edu/CropScape/.
35. USDA Farm Service Agencies Aerial Photography Field Offices Digital Ortho County Mosaic. 2011 1:12,000. USDA-FSA-APFO, Salt Lake City, UT. Available at http://datagateway.nrcs.usda.gov/.
36. Kovach J, Petzoldt C, Degnil J, Tette J. 1992 A method to measure the environmental impact of pesticides. New Yorks Food Life Sci. Bull. 139, 1–8.
37. Greitens TJ, Day E. 2007 An alternative way to evaluate the environmental effects of integrated pest management: pesticide risk indicators. Renew. Agric. Food Syst. 22, 213–222. (doi:10.1017/S1742170507001755)
38. Morse R. 1989 Bee poisoning. In New York State Pesticide Recommendation, 1989 edition, pp. 28–30 Ithaca, NY: The Chemicals-Pesticides Program, Cornell University.
39. Ciarlo TJ, Mullin CA, Frazier JL, Schmehl DR. 2012 Learning impairment in honey bees caused by agricultural spray adjuvants. PLoS ONE 7, e40848. (doi:10.1371/journal.pone.0040848)
40. Herrera CM. 1988 Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biol. J. Linn. Soc. 35, 95–125. (doi:10.1111/j.1095-8312.1988.tb00461.x)
41. Zuur AF. 2009 Mixed effects models and extensions in ecology with R. New York, NY: Springer.
42. Dushoff J, Caldwell B, Mohler CL. 1994 Evaluating the environmental effect of pesticides: a critique of the environmental impact quotient. Am. Entomol. 40, 180–184. (doi:10.1093/ae/40.3.180)
43. Van der Werf HMG. 1996 Assessing the impact of pesticides on the environment. Agric. Ecosyst. Environ. 60, 81–96. (doi:10.1016/S0167-8809(96)01096-1)
44. Bolker BM et al. 2013. Strategies for fitting nonlinear ecological models in R, AD model builder, and BUGS. Methods Ecol. Evol. 4, 501–512. (doi:10.1111/2041-210X.12044)
45. Fortin M-J, Dale MRT. 2005 Spatial analysis: a guide for ecologists. Cambridge, UK: Cambridge University Press.
46. Kutner MH, Nachtsheim CJ, Neter J. 2004 Applied linear regression models, 4th edn. New York, NY: McGraw-Hill Irwin.
47. R Core Team. 2014 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
48. Pinheiro J, Bates D, Sarkar D, R Core Team. 2014 NLME: linear and nonlinear mixed effects models. R package version 3.1–117. See http://CRAN.Rproject.org/package=nlme.
49. Fournier D, Skaug H, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J. 2012 AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim. Methods Softw. 27, 233–249. (doi:10.1080/10556788.2011.597854)
50. Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A. 2014 Generalized linear mixed models using AD model builder. R package version 0.8.0. See http://r-forge.r-project.org/projects/glmmadmb.
51. Kremen C, Williams NM, Thorp RW. 2002 Crop pollination from native bees at risk from agricultural intensification. Proc. Natl Acad. Sci. USA 99, 16 812–16 816. (doi:10.1073/pnas.262413599)
52. Deguines N, Jono C, Baude M, Henry M, Julliard R, Fontaine C. 2014 Large-scale trade-off between agricultural intensification and crop pollination services. Front. Ecol. Environ. 12, 212–217. (doi:10.1890/130054)
53. Watson JC, Wolf AT, Ascher JS. 2011 Forested landscapes promote richness and abundance of native bees (Hymenoptera: Apoidea: Anthophila) in Wisconsin apple orchards. Environ. Entomol. 40, 621–632. (doi:10.1603/EN10231)
54. Tscharntke T et al. 2012 Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol. Rev. 87, 661–685. (doi:10.1111/j.1469-185X.2011.00216.x)
55. Tuell JK, Isaacs R. 2010 Community and speciesspecific responses of wild bees to insect pest control programs applied to a pollinator-dependent crop. J. Econ. Entomol. 103, 668–675. (doi:10.1603/EC09314)
56. Pilling ED, Jepson PC. 1993 Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic. Sci. 39, 293–297. (doi:10.1002/ps.2780390407)
57. Sanchez-Bayo F, Goka K. 2014 Pesticide residues and bees—a risk assessment. PLoS ONE 9, e94482. (doi:10.1371/journal.pone.0094482)
58. Johansen CA, Mayer DF, Eves JD, Kiuos CW. 1983 Pesticides and bees. Environ. Entomol. 12, 1513–1518. (doi:10.1093/ee/12.5.1513)
59. Brittain C, Vinghi M, Bommarco R, Settele J, Potts S. 2010 Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl. Ecol. 11, 106–115. (doi:10.1016/j.baae.2009.11.007)
60. Mayer DF, Lunden JD. 1986 Toxicity of fungicides and an acaricide to honey bees (Hymenoptera: Apidae) and their effects on bee foraging behavior and pollen viability on blooming apples and pears. Environ. Entomol. 15, 1047–1049. (doi:10.1093/ee/15.5.1047)
61. Bartomeus I, Park MG, Gibbs J, Danforth BN, Lakso AN, Winfree R. 2013 Biodiversity ensures plant– pollinator phenological synchrony against climate change. Ecol. Lett. 16, 1331–1338. (doi:10.1111/ele.12170)
62. Yoder JA, Jajack AJ, Rosselot AE, Smith TJ, Yerke MC, Sammataro D. 2013 Fungicide contamination reduces beneficial fungi in bee bread based on an area-wide field study in honey bee, Apis mellifera, colonies. J. Toxicol. Environ. Health A 76, 587–600. (doi:10.1080/15287394.2013.798846)
63. Fischer D, Moriarty T. 2014 Pesticide risk assessment for pollinators. Ames, IA: Wiley-Blackwell.
64. Biddinger DJ, Robertson JL, Mullin C, Frazier J, Ashcraft SA, Rajotte EG, Joshi NK, Vaughn M. 2013 Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS ONE 8, e72587. (doi:10.1371/journal.pone.0072587)
65. Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG. 2010 Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 143, 2280–2291. (doi:10.1016/j.biocon.2010.03.024)
66. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, Suchail S, Brunet JL, Alaux C. 2013 Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS ONE 8, e72016. (doi:10.1371/journal.pone.0072016)
67. Chaplin-Kramer R, O’Rourke ME, Blitzer EJ, Kremen C. 2011 A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecol. Lett. 14, 922–932. (doi:10.1111/j.1461-0248.2011.01642.x)
68. Landis DA, Wratten SD, Gurr GM. 2000 Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45, 175–201. (doi:10.1146/annurev.ento.45.1.175)
69. Obrycki JJ, Kring TJ. 1998 Predaceous Coccinellidae in biological control. Annu. Rev. Entomol. 43, 295–321. (doi:10.1146/annurev.ento.43.1.295)
70. Holzschuh A, Steffan-Dewenter I, Kleijn D, Tscharntke T. 2007 Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context. J. Appl. Ecol. 44, 41–49. (doi:10.1111/j.1365-2664.2006.01259.x)
71. Westphal C, Steffan-Dewenter I, Tscharntke T. 2003 Mass flowering crops enhance pollinator densities at a landscape scale. Ecol. Lett. 6, 961–965. (doi:10.1046/j.1461-0248.2003.00523.x)
72. Carvalheiro LG, Seymour CL, Nicolson SW, Veldtman R. 2012 Creating patches of native flowers facilitates crop pollination in large agricultural fields: mango as a case study. J. Appl. Ecol. 49, 1373–1383. (doi:10.1111/j.1365-2664.2012.02217.x)