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Journal of Pest Science

, Volume 92, Issue 3, pp 1017–1026 | Cite as

Field margins provide a refuge for pest genes beneficial to resistance management

  • James L. MainoEmail author
  • Michael Renton
  • Ary A. Hoffmann
  • Paul A. Umina
Original Paper

Abstract

Fencelines and field margins in broad-acre cropping systems are commonly a refuge for weeds, diseases and invertebrates because they avoid many cropping and pest management regimes applied inside fields. As such, fenceline refuges are often managed separately with the goal to reduce pest reinfestation of fields from the margins. However, the implications of these pest control strategies are poorly understood in terms of their impact on pest genes beneficial to pesticide resistance management. Fenceline management, such as selectively reducing pest populations through insecticides, or non-selectively modifying habitat quality by removing host weeds with herbicides, might increase or decrease resistance evolution rates. Indeed, the potential to perform selective and non-selective control of pests separates management of field margins from structured in-field susceptible refuges (e.g. Bt crops). Here, a simulation approach was used to explore the effect of different fenceline management strategies, cropping characteristics and pest genetics on resistance evolution. The analysis was applied to a major crop pest, the mite Halotydeus destructor, for which fenceline treatments of herbicides and insecticides may be applied. Spraying fencelines with an insecticide decreased reinfestation and the overall abundance of mites, compared with not applying insecticides to fencelines. However, in all scenarios tested, resistance evolution was delayed by leaving fenceline refuges unsprayed with insecticides or herbicides. Just as field margins may provide a reservoir for invertebrates beneficial to pest management (e.g. predators and parasitoids), they may also serve as an important refuge for genes beneficial to resistance management.

Keywords

Integrated pest management Insecticide Pesticide Resistance Evolution Dispersal Acari Spatially explicit 

Notes

Acknowledgements

The authors acknowledge Owain Edwards for discussion during the conception of this study and Elia Pirtle for assistance with figure design. This work was supported by funding from the Grains and Research Development Corporation.

Funding

This study was supported by funding from the Grains Research and Development Corporation (UM00049, UM00057).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10340_2019_1106_MOESM1_ESM.docx (192 kb)
Supplementary material 1 (DOCX 191 kb)

References

  1. Alstad DN, Andow DA (1995) Managing the evolution of insect resistance to transgenic plants. Science 80-(268):1894–1896.  https://doi.org/10.1126/science.268.5219.1894 CrossRefGoogle Scholar
  2. Bates SL, Zhao J-Z, Roush RT, Shelton AM (2005) Insect resistance management in GM crops: past, present and future. Nat Biotechnol 23:57CrossRefGoogle Scholar
  3. Bourguet D, Desquilbet M, Lemarié S (2005) Regulating insect resistance management: the case of non-Bt corn refuges in the US. J Environ Manage 76:210–220.  https://doi.org/10.1016/j.jenvman.2005.01.019 CrossRefGoogle Scholar
  4. Capinha C, Essl F, Seebens H et al (2015) The dispersal of alien species redefines biogeography in the anthropocene. Science 80-(348):1248–1251.  https://doi.org/10.1126/science.aaa8913 CrossRefGoogle Scholar
  5. Caprio M (1998) Evaluating resistance management strategies for multiple toxins in the presence of external refuges. J Econ Entomol 91:1021–1031.  https://doi.org/10.1093/jee/91.5.1021 CrossRefGoogle Scholar
  6. Caprio MA, Tabashnik BE (1992) Gene flow accelerates local adaptation among finite populations: simulating the evolution of insecticide resistance. J Econ Entomol 85:611–620.  https://doi.org/10.1093/jee/85.3.611 CrossRefGoogle Scholar
  7. Cheng X, Umina PA, Hoffmann AA (2018) Influence of previous host plants on the reproductive success of a polyphagous mite pest, Halotydeus destructor (Trombidiformes: Penthaleidae). J Econ Entomol 111:680–688.  https://doi.org/10.1093/jee/tox368 CrossRefGoogle Scholar
  8. Comins HN (1977a) The development of insecticide resistance in the presence of migration. J Theor Biol 64:177–197.  https://doi.org/10.1016/0022-5193(77)90119-9 CrossRefGoogle Scholar
  9. Comins HN (1977b) The management of pesticide resistance. J Theor Biol 65:399–420CrossRefGoogle Scholar
  10. DeAngelis DL, Rose KA (1992) Which individual-based approach is most appropriate for a given problem. In: Individual-based models and approaches in ecology: populations, communities and ecosystems, pp 67–87Google Scholar
  11. Edwards OR, Walsh TK, Metcalfe S, Tay WT, Hoffmann AA, Mangano P, Lord A, Micic S, Umina PA (2018) A genomic approach to identify and monitor a novel pyrethroid resistance mutation in the redlegged earth mite. Halotydeus destructor. Pestic Biochem Physiol 144:83–90.  https://doi.org/10.1016/j.pestbp.2017.12.002 CrossRefGoogle Scholar
  12. Frank T (1998) The role of different slug species in damage to oilseed rape bordering on sown wildflower strips. Ann Appl Biol 133:483–493.  https://doi.org/10.1111/j.1744-7348.1998.tb05845.x CrossRefGoogle Scholar
  13. Gardiner MM, Neal MEO (2009) Landscape diversity enhances biological control of an introduced crop pest in the North-Central USA. Ecol Appl 19:143–154CrossRefGoogle Scholar
  14. Georghiou GP, Taylor CE (1977) Operational influences in the evolution of insecticide resistance. J Econ Entomol 70:653–658CrossRefGoogle Scholar
  15. Gould F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol 43:701–726CrossRefGoogle Scholar
  16. Gower JMC, Hoffmann AA, Weeks AR (2008) Effectiveness of spring spraying targeting diapause egg production for controlling redlegged earth mites and other pests in pasture. Aust J Exp Agric 48:1118–1125.  https://doi.org/10.1071/EA07048 CrossRefGoogle Scholar
  17. Hackett SC, Bonsall MB (2016) Type of fitness cost influences the rate of evolution of resistance to transgenic Bt crops. J Appl Ecol 53:1391–1401CrossRefGoogle Scholar
  18. Hatt S, Uyttenbroeck R, Lopes T et al (2018) Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (Brassica napus) crops. Arthropod Plant Interact 12:787–797.  https://doi.org/10.1007/s11829-017-9567-8 CrossRefGoogle Scholar
  19. Herrmann F, Westphal C, Moritz RFA, Steffan-Dewenter I (2007) Genetic diversity and mass resources promote colony size and forager densities of a social bee (Bombus pascuorum) in agricultural landscapes. Mol Ecol 16:1167–1178.  https://doi.org/10.1111/j.1365-294X.2007.03226.x CrossRefGoogle Scholar
  20. Huang F, Andow DA, Buschman LL (2011) Success of the high-dose/refuge resistance management strategy after 15 years of Bt crop use in North America. Entomol Exp Appl 140:1–16CrossRefGoogle Scholar
  21. Ives AR, Andow DA (2002) Evolution of resistance to Bt crops: directional selection in structured environments. Ecol Lett 5:792–801CrossRefGoogle Scholar
  22. Jones RAC, McKirdy SJ, Shivas RG (1990) Occurrence of barley yellow dwarf viruses in over-summering grasses and cereal crops in Western Australia. Australas Plant Pathol 19:90–96.  https://doi.org/10.1071/APP9900090 CrossRefGoogle Scholar
  23. Karp DS, Chaplin-Kramer R, Meehan TD et al (2018) Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc Natl Acad Sci 115:E7863–E7870.  https://doi.org/10.1073/pnas.1800042115 CrossRefGoogle Scholar
  24. Lee JC, Menalled FD, Landis DA (2001) Refuge habitats modify impact of insecticide disturbance on carabid beetle communities. J Appl Ecol 38:472–483.  https://doi.org/10.1046/j.1365-2664.2001.00602.x CrossRefGoogle Scholar
  25. Maclennan KE, McDonald G, Ward SA (1998) Soil microflora as hosts of redlegged earth mite (Halotydeus destructor). Entomol Exp Appl 86:319–323.  https://doi.org/10.1023/A:1003128318616 CrossRefGoogle Scholar
  26. Maino JL, Binns M, Umina P (2018a) No longer a west-side story—pesticide resistance discovered in the eastern range of a major Australian crop pest, Halotydeus destructor (Acari: Penthaleidae). Crop Pasture Sci 69:216–221.  https://doi.org/10.1071/CP17327 CrossRefGoogle Scholar
  27. Maino JL, Umina PA, Hoffmann AA (2018b) Climate contributes to the evolution of pesticide resistance. Glob Ecol Biogeogr 27:223–232.  https://doi.org/10.1111/geb.12692 CrossRefGoogle Scholar
  28. Marshall EJP, Moonen AC (2002) Field margins in northern Europe: integrating agricultural, environmental and biodiversity functions. Agric Ecosyst Environ 89:5–21.  https://doi.org/10.1016/S0167-8809(01)00315-2 CrossRefGoogle Scholar
  29. Micic S, Lord A (2018) Prevent redlegged earth mite resistance. In: Department of Primary Industries and Regional Development’s Agriculture and Food. https://www.agric.wa.gov.au/mites-spiders/prevent-redlegged-earth-mite-resistance. Accessed 5 Aug 2018
  30. Onstad DW, Gould F (1998) Modeling the dynamics of adaptation to transgenic maize by European Corn Borer (Lepidoptera: Pyralidae). J Econ Entomol 91:585–593.  https://doi.org/10.1093/jee/91.3.585 CrossRefGoogle Scholar
  31. Renton M (2013) Shifting focus from the population to the individual as a way forward in understanding, predicting and managing the complexities of evolution of resistance to pesticides. Pest Manag Sci 69:171–175.  https://doi.org/10.1002/ps.3341 CrossRefGoogle Scholar
  32. Renton M, Busi R, Neve P et al (2014) Herbicide resistance modelling: past, present and future. Pest Manag Sci 70:1394–1404.  https://doi.org/10.1002/ps.3773 CrossRefGoogle Scholar
  33. Ridsdill-Smith TJ (1997) Biology and control of Halotydeus destructor (Tucker) (Acarina: Penthaleidae): a review. Exp Appl Acarol 21:195–224CrossRefGoogle Scholar
  34. Ridsdill-Smith TJ, Annells AJ (1997) Seasonal occurrence and abundance of redlegged earth mite Halotydeus destructor (Acari: Penthaleidae) in annual pastures of southwestern Australia. Bull Entomol Res 87:413CrossRefGoogle Scholar
  35. Roush RT (1998) Two–toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Philos Trans R Soc Lond B Biol Sci 353:1777–1786CrossRefGoogle Scholar
  36. Roush RT, McKenzie JA (1987) Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361–380CrossRefGoogle Scholar
  37. Roush RT, Tabashnik BE (1990) Pesticide resistance in arthropods. Springer, BerlinGoogle Scholar
  38. Shirk AJ, Wallin DO, Cushman SA et al (2010) Inferring landscape effects on gene flow: a new model selection framework. Mol Ecol 19:3603–3619.  https://doi.org/10.1111/j.1365-294X.2010.04745.x CrossRefGoogle Scholar
  39. Skellern MP, Cook SM (2018) Prospects for improved off-crop habitat management for pollen beetle control in oilseed rape. Arthropod Plant Interact 12:849–866.  https://doi.org/10.1007/s11829-018-9598-9 CrossRefGoogle Scholar
  40. Somerville GJ, Powles SB, Walsh MJ, Renton M (2017) How do spatial heterogeneity and dispersal in weed population models affect predictions of herbicide resistance evolution? Ecol Model 362:37–53.  https://doi.org/10.1016/j.ecolmodel.2017.08.002 CrossRefGoogle Scholar
  41. Storer NP (2003) A spatially explicit model simulating western corn rootworm (Coleoptera: Chrysomelidae) adaptation to insect-resistant maize. J Econ Entomol 96:1530–1547CrossRefGoogle Scholar
  42. Storer NP, Peck SL, Gould F et al (2003) Spatial processes in the evolution of resistance in Helicoverpa zea (Lepidoptera: Noctuidae) to Bt transgenic corn and cotton in a mixed agroecosystem: a biology-rich stochastic simulation model. J Econ Entomol 96:156–172.  https://doi.org/10.1603/0022-0493-96.1.156 CrossRefGoogle Scholar
  43. Stratonovitch P, Elias J, Denholm I et al (2014) An individual-based model of the evolution of pesticide resistance in heterogeneous environments: control of Meligethes aeneus population in oilseed rape crops. PLoS ONE 9:1–24.  https://doi.org/10.1371/journal.pone.0115631 CrossRefGoogle Scholar
  44. Sudo M, Takahashi D, Andow DA et al (2018) Optimal management strategy of insecticide resistance under various insect life histories: heterogeneous timing of selection and interpatch dispersal. Evol Appl 11:271–283CrossRefGoogle Scholar
  45. Swinton SM, Lupi F, Robertson GP, Hamilton SK (2007) Ecosystem services and agriculture: cultivating agricultural ecosystems for diverse benefits. Ecol Econ 64:245–252.  https://doi.org/10.1016/j.ecolecon.2007.09.020 CrossRefGoogle Scholar
  46. Tabashnik BE (1990) Modeling and Evaluation of Resistance Management Tactics. In: Roush RT, Tabashnik BE (eds) Pesticide resistance in arthropods. Springer, Boston, pp 153–182CrossRefGoogle Scholar
  47. Tabashnik BE, Gassmann AJ, Crowder DW, Carriére Y (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26:199CrossRefGoogle Scholar
  48. Takahashi D, Yamanaka T, Sudo M, Andow DA (2017) Is a larger refuge always better? Dispersal and dose in pesticide resistance evolution. Evolution (N Y) 71:1494–1503Google Scholar
  49. Umina PA (2007) Pyrethroid resistance discovered in a major agricultural pest in southern Australia: the redlegged earth mite Halotydeus destructor (Acari: Penthaleidae). Pest Manag Sci 63:1185–1190.  https://doi.org/10.1002/ps.1439 CrossRefGoogle Scholar
  50. Umina PA, Hoffmann AA (2004) Plant host associations of Penthaleus species and Halotydeus destructor (Acari: Penthaleidae) and implications for integrated pest management. Exp Appl Acarol 33:1–20.  https://doi.org/10.1023/B:APPA.0000030014.00162.44 CrossRefGoogle Scholar
  51. Umina P, McDonald G (2015) Redlegged earth mite. In: PestNotes South. http://www.cesaraustralia.com/sustainable-agriculture/pestnotes/insect/Redlegged-earth-mite. Accessed 16 Aug 2018
  52. Umina PA, Hoffmann AA, McDonald G, et al (2016) Resistance management strategy for the redlegged earth mite in Australian grains and pastures. Kingston ACT 2604Google Scholar
  53. Umina PA, Lord A, Micic S, Edwards O (2017) Discovery and characterisation of field resistance to organophosphorus chemicals in a major mite pest, Halotydeus destructor. Pest Manag Sci 73:1719–1724.  https://doi.org/10.1002/ps.4520 CrossRefGoogle Scholar
  54. Umina PA, McDonald G, Maino J et al (2018) Escalating insecticide resistance in Australian grain pests: contributing factors, industry trends and management opportunities. Pest Manag Sci.  https://doi.org/10.1002/ps.5285 Google Scholar
  55. Weeks AR, Turelli M, Hoffmann AA (2000) Dispersal patterns of pest earth mites (Acari: Penthaleidae) in pastures and crops. J Econ Entomol 93:1415–1423.  https://doi.org/10.1603/0022-0493-93.5.1415 CrossRefGoogle Scholar
  56. Wilson PJ, Aebischer NJ (1995) The distribution of dicotyledonous arable weeds in relation to distance from the field edge. J Appl Ecol 32:295–310.  https://doi.org/10.2307/2405097 CrossRefGoogle Scholar
  57. Zhao J-Z, Collins HL, Shelton AM (2010) Testing insecticide resistance management strategies: mosaic versus rotations. Pest Manag Sci 66:1101–1105.  https://doi.org/10.1002/ps.1985 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of BioSciencesThe University of MelbourneParkvilleAustralia
  2. 2.cesarParkvilleAustralia
  3. 3.School of Biological Sciences M090The University of Western AustraliaCrawleyAustralia

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