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Landscape ecology and expanding range of biocontrol agent taxa enhance prospects for diamondback moth management. A review

  • Geoff M. Gurr
  • Olivia L. Reynolds
  • Anne C. Johnson
  • Nicolas Desneux
  • Myron P. Zalucki
  • Michael J. Furlong
  • Zhenyu Li
  • Komivi S. Akutse
  • Junhui Chen
  • Xiwu Gao
  • Minsheng You
Review Article
Part of the following topical collections:
  1. Pest control

Abstract

Diamondback moth (Plutella xylostella) is a globally significant pest of Brassicaceae crops that has attracted enormous research investment. It is typical of many agricultural pests, with insecticides remaining the most common method of control, despite frequent cases of resistance in pest populations and the potential for other management options such as natural enemies to provide suppression. Here we review scope to make better use of neglected natural enemy taxa and integrate recent work on landscape ecology to identify opportunities for more effective pest suppression. Our main findings are as follows: (1) relatively neglected taxa of natural enemies, especially predators and entomopathogens, are now attracting growing levels of research interest, although parasitoids remain most frequently used and researched; (2) knowledge of the spatio-temporal dynamics of populations at the landscape scale have advanced rapidly in the last decade; (3) ecological insights open new possibilities for exploiting spatial heterogeneity at scales larger than individual fields and even farms that influence pests and their natural enemies; (4) there is evidence for landscapes that selectively favor particular guilds and this knowledge could be developed to favor targeted natural enemies over pests in focal crops; and (5) landscape-scale effects can even over-ride field-scale management practices. The significance of these advances is that future management of diamondback moth and similar pests will benefit from a move away from reliance on the use of particular species of biological control agents, especially exotic parasitoids, and strategies that depend on use of broad-spectrum insecticides. Together with this move, we call for greater use of area-wide management that exploits the potential of landscapes to promote diverse assemblages of natural enemy species.

Keywords

Plutella xylostella Conservation biological control Habitat management Donor habitat Landscape connectivity Area-wide management Bacillus thuringiensis Entomopathogen Predator Parasitoid 

Notes

Acknowledgements

We acknowledge the input of David Perovic & Sagrario Gamez-Virues in the early stages of planning this review.

Funding information

This project was supported by the National Natural Science Foundation of China (No. 31230061 and No. 31320103922). GMG was supported by the National Thousand Talents Fellowship, the Advanced Talents of SAEFA in China and a Graham Centre Research Fellowship. ND was supported by the project EUCLID (H2020-SFS-2014, grant number: 633999). OLR was supported by a Jinshan Scholar Fellowship at Fujian Agriculture and Forestry University (FAFU), China. KSA was supported as a postdoctoral fellow by the National Thousand Talents Fellowship at FAFU, China. Grants CS2/1998/089, HORT/2002/062, HORT/2004/063 and HORT/2010/090 from the Australian Centre for International Agricultural Research (ACIAR) have supported diamondback moth research by MJF and MPZ in China, Democratic Republic of Korea, Fiji, Samoa and Tonga.

References

  1. Abrams PA, Matsuda H (1996) Positive indirect effects between prey species that share predators. Ecology 77(2):610–616.  https://doi.org/10.2307/2265634 Google Scholar
  2. Adamson D, Zalucki MP, Furlong MJ (2014) Pesticides and integrated pest management practice, practicality and policy in Australia. In: Peshin R, Pimentel D (eds) Integrated pest management: experiences with implementation, global overview, Vol.4. Springer Netherlands, Dordrecht, pp 387–411. doi: https://doi.org/10.1007/978-94-007-7802-3_16
  3. Ankersmit G (1953) DDT-resistance in Plutella maculipennis (Curt.)(Lep.) in Java. Bull Entomol Res 44(03):421–425.  https://doi.org/10.1017/S0007485300025530 Google Scholar
  4. Barbosa P, Krischik VA, Jones CG (1991) Microbial mediation of plant-herbivore interactions. John Wiley & Sons, New YorkGoogle Scholar
  5. Bentur JS, Viraktamath BC (2008) Rice planthoppers strike back. Curr Sci 95(4):441–443Google Scholar
  6. Bidochka MJ, Kamp AM, Lavender TM, Dekoning J, De Croos JNA (2001) Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species? Appl Environ Microbiol 67(3):1335–1342.  https://doi.org/10.1128/aem.67.3.1335-1342.2001 PubMedPubMedCentralGoogle Scholar
  7. Blumthaler M, Ambach W, Silbernagl R, Staehelin J (1994) Erythemal UV-B irradiance (Robertson-Berger sunburn meter data) under ozone deficiencies in winter/spring 1993. Photochem Photobiol 59(6):657–659.  https://doi.org/10.1111/j.1751-1097.1994.tb09672.x Google Scholar
  8. Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55(3):433–440.  https://doi.org/10.1007/s10144-013-0371-8 Google Scholar
  9. Bradshaw CJA, Leroy B, Bellard C, Roiz D, Albert C, Fournier A, Barbet-Massin M, Salles J-M, Simard F, Courchamp F (2016) Massive yet grossly underestimated global costs of invasive insects. Nat Commun 7:12986.  https://doi.org/10.1038/ncomms12986 PubMedPubMedCentralGoogle Scholar
  10. Braga GUL, Flint SD, Messias CL, Anderson AJ, Roberts DW (2001) Effect of UV-B on conidia and germlings of the entomopathogenic hyphomycete Metarhizium anisopliae. Mycol Res 105(7):874–882.  https://doi.org/10.1017/S0953756201004270 Google Scholar
  11. Brown J, Frohlich D, Rosell R (1995) The sweetpotato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annu Rev Entomol 40(1):511–534.  https://doi.org/10.1146/annurev.en.40.010195.002455 Google Scholar
  12. Burges HD, Thomson EM, Latchford RA (1976) Importance of spores and δ-endotoxin protein crystals of Bacillus thuringiensis in Galleria mellonella. J Invertebr Pathol 27(1):87–94.  https://doi.org/10.1016/0022-2011(76)90032-X Google Scholar
  13. Campbell JF, Lewis E, Yoder F, Gaugler R (1995) Entomopathogenic nematode (Heterorhabditidae and Steinernematidae) seasonal population dynamics and impact on insect populations in turfgrass. Biol Control 5(4):598–606.  https://doi.org/10.1006/bcon.1995.1071 Google Scholar
  14. Campbell JF, Orza G, Yoder F, Lewis E, Gaugler R (1998) Spatial and temporal distribution of endemic and released entomopathogenic nematode populations in turfgrass. Entomologia Experimentalis et Applicata 86(1):1–11.  https://doi.org/10.1046/j.1570-7458.1998.00260.x Google Scholar
  15. Casey C, Newman JP, Robb KL, Tjosvold SA, MacDonald JD, Parrella MP (2007) IPM program successful in California greenhouse cut roses. Calif Agric 61(2):71–78.  https://doi.org/10.3733/ca.v061n02p71 Google Scholar
  16. Chailleux A, Mohl E, Teixeira-Alves M, Messelink G, Desneux N (2014) Natural enemy-mediated indirect interactions among prey species: potential for enhancing biocontrol services in agroecosystems. Pest Manag Sci 70:1769–1779.  https://doi.org/10.1002/ps.3916 PubMedGoogle Scholar
  17. Chapman JW, Reynolds DR, Smith AD, Riley JR, Pedgley DE, Woiwod IP (2002) High-altitude migration of the diamondback moth Plutella xylostella to the U.K.: a study using radar, aerial netting, and ground trapping. Ecol Entomol 27(6):641–650.  https://doi.org/10.1046/j.1365-2311.2002.00472.x Google Scholar
  18. Cherry AJ, Mercadier G, Meikle W, Castelo-Branco M, Schroer S (2004) The role of entomopathogens in DBM biological control. In: Kirk AA, Bordat D (eds) Improving biocontrol of Plutella xylostella: Proceedings of the International Symposium, Montpellier, France, 21–24 October, 2002. CIRAD, pp 51–70Google Scholar
  19. Crickmore N (2006) Beyond the spore—past and future developments of Bacillus thuringiensis as a biopesticide. J Appl Microbiol 101(3):616–619.  https://doi.org/10.1111/j.1365-2672.2006.02936.x PubMedGoogle Scholar
  20. Denno RF, Finke DL (2006) Multiple predator interactions and food-web connectance: implications for biological control. In: Brodeur J, Boivin G (eds) Trophic and guild in biological interactions control. Springer, Berlin, pp 45–70Google Scholar
  21. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52(1):81–106.  https://doi.org/10.1146/annurev.ento.52.110405.091440 PubMedGoogle Scholar
  22. Dosdall L, Mason P, Olfert O, Kaminski L, Keddie B (2004) The origins of infestations of diamondback moth, Plutella xylostella (L.), in canola in western Canada. In: Endersby N, Ridland PM (eds) The management of diamondback moth and other crucifer pests: Proceedings of the IV International workshop. The Regional Inst., Melbourne, pp 26–29Google Scholar
  23. Downes S, Kriticos D, Parry H, Paull C, Schellhorn N, Zalucki MP (2017) A perspective on management of Helicoverpa armigera: transgenic Bt cotton, IPM, and landscapes. Pest Manag Sci 73(3):485–492.  https://doi.org/10.1002/ps.4461 PubMedGoogle Scholar
  24. Duarte RT, Gonçalves KC, Espinosa DJL, Moreira LF, De Bortoli SA, Humber RA, Polanczyk RA (2016) Potential of entomopathogenic fungi as biological control agents of diamondback moth (Lepidoptera: Plutellidae) and compatibility with chemical insecticides. J Econ Entomol 109(2):594–601.  https://doi.org/10.1093/jee/tow008 PubMedGoogle Scholar
  25. Efron D, Nestel D, Glazer I (2001) Spatial analysis of entomopathogenic nematodes and insect hosts in a citrus grove in a semi-arid region in Israel. Environ Entomol 30(2):254–261.  https://doi.org/10.1603/0046-225X-30.2.254 Google Scholar
  26. Ekesi S, Shah PA, Clark SJ, Pell JK (2005) Conservation biological control with the fungal pathogen Pandora neoaphidis: implications of aphid species, host plant and predator foraging. Agric For Entomol 7(1):21–30.  https://doi.org/10.1111/j.1461-9555.2005.00239.x Google Scholar
  27. Feng X, Li ZY, Wu QJ, Chen AD, Wu YD, Hou YM, He YR, Li JH, Xie SH, Zhang JM, Fu W (2011) Research progress of the resistance management and sustainable control of diamondback moth (Plutella xylostella) in China. Chin J Appl Entomol 48(2):247–253Google Scholar
  28. Fernández-Bravo M, Garrido-Jurado I, Valverde-García P, Enkerli J, Quesada-Moraga E (2016) Responses to abiotic environmental stresses among phylloplane and soil isolates of Beauveria bassiana from two holm oak ecosystems. J Invertebr Pathol 141(Supplement C):6–17.  https://doi.org/10.1016/j.jip.2016.09.007 PubMedGoogle Scholar
  29. Fox LR, Eisenbach J (1992) Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia 89(4):574–579.  https://doi.org/10.1007/bf00317166 PubMedGoogle Scholar
  30. Furlong MJ, Ju KH, Su PW, Chol JK, Il RC, Zalucki MP (2008a) Integration of endemic natural enemies and Bacillus thuringiensis to manage insect pests of Brassica crops in North Korea. Agric Ecosyst Environ 125(1):223–238.  https://doi.org/10.1016/j.agee.2008.01.003 Google Scholar
  31. Furlong MJ, Pell JK (1997) The influence of environmental factors on the persistence of Zoophthora radicans conidia. J Invertebr Pathol 69(3):223–233.  https://doi.org/10.1006/jipa.1996.4649 Google Scholar
  32. Furlong MJ, Pell JK (2001) Horizontal transmission of entomopathogenic fungi by the diamondback moth. Biol Control 22(3):288–299.  https://doi.org/10.1006/bcon.2001.0981 Google Scholar
  33. Furlong MJ, Pell JK, Choo OP, Rahman SA (1995) Field and laboratory evaluation of a sex pheromone trap for the autodissemination of the fungal entomopathogen Zoophthora radicans (Entomophthorales) by the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Bull Entomol Res 85(03):331–337.  https://doi.org/10.1017/S0007485300036051 Google Scholar
  34. Furlong MJ, Rowley DL, Murtiningsih R, Greenstone MH (2014) Combining ecological methods and molecular gut-content analysis to investigate predation of a lepidopteran pest complex of Brassica crops. Entomologia Experimentalis et Applicata 153(2):128–141.  https://doi.org/10.1111/eea.12231 Google Scholar
  35. Furlong MJ, Shi Z-H, Liu S-S, Zalucki MP (2004a) Evaluation of the impact of natural enemies on Plutella xylostella L. (Lepidoptera: Yponomeutidae) populations on commercial Brassica farms. Agric For Entomol 6(4):311–322.  https://doi.org/10.1111/j.1461-9555.2004.00228.x Google Scholar
  36. Furlong MJ, Spafford H, Ridland PM, Endersby NM, Edwards OR, Baker GJ, Keller MA, Paull CA (2008b) Ecology of diamondback moth in Australian canola: landscape perspectives and the implications for management. Aust J Exp Agric 48(12):1494–1505.  https://doi.org/10.1071/Ea07413 Google Scholar
  37. Furlong MJ, Wright DJ, Dosdall LM (2013) Diamondback moth ecology and management: problems, progress, and prospects. Annu Rev Entomol 58:517–541.  https://doi.org/10.1146/annurev-ento-120811-153605 PubMedGoogle Scholar
  38. Furlong MJ, Zalucki MP (2010) Exploiting predators for pest management: the need for sound ecological assessment. Entomologia Experimentalis et Applicata 135(3):225–236.  https://doi.org/10.1111/j.1570-7458.2010.00988.x Google Scholar
  39. Furlong MJ, Zu-Hua S, Yin-Quan L, Shi-Jian G, Yao-Bin L, Shu-Sheng L, Zalucki MP (2004b) Experimental analysis of the influence of pest management practice on the efficacy of an endemic arthropod natural enemy complex of the diamondback moth. J Econ Entomol 97(6):1814–1827.  https://doi.org/10.1603/0022-0493-97.6.1814 PubMedGoogle Scholar
  40. Fuxa JR (1998) Environmental manipulation for microbial control of insects. In: Barbosa P (ed) Conservation biological control. Academic Press, San Diego, USA, pp 255–268Google Scholar
  41. Gabriel D, Sait SM, Hodgson JA, Schmutz U, Kunin WE, Benton TG (2010) Scale matters: the impact of organic farming on biodiversity at different spatial scales. Ecol Lett 13(7):858–869.  https://doi.org/10.1111/j.1461-0248.2010.01481.x PubMedGoogle Scholar
  42. Gamez-Virues S, Perovic DJ, Gossner MM, Borschig C, Bluthgen N, de Jong H, Simons NK, Klein AM, Krauss J, Maier G, Scherber C, Steckel J, Rothenwohrer C, Steffan-Dewenter I, Weiner CN, Weisser W, Werner M, Tscharntke T, Westphal C (2015) Landscape simplification filters species traits and drives biotic homogenization. Nat Commun 6:8568.  https://doi.org/10.1038/ncomms9568 PubMedPubMedCentralGoogle Scholar
  43. Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9(11):791–802.  https://doi.org/10.1038/nrmicro2649 PubMedGoogle Scholar
  44. Gao X, Yang J, Xu B, Yang F, Wu Q (2016) Insecticide resistance in diamondback moth populations in Beijing and Hebei. Chin J Appl Environ Biol 53:279–284Google Scholar
  45. Geertsema W, Rossing WAH, Landis DA, Bianchi FJJA, van Rijn PCJ, Schaminée JHJ, Tscharntke T, van der Werf W (2016) Actionable knowledge for ecological intensification of agriculture. Front Ecol Environ 14(4):209–216.  https://doi.org/10.1002/fee.1258 Google Scholar
  46. Gillespie MA, Gurr GM, Wratten SD (2016) Beyond nectar provision: the other resource requirements of parasitoid biological control agents. Entomologia Experimentalis et Applicata 159:1–15.  https://doi.org/10.1111/eea.12424 Google Scholar
  47. Glazer I, Kozodoi E, Salame L, Nestel D (1996) Spatial and temporal occurrence of natural populations of Heterorhabditis spp. (Nematoda: Rhabditida) in a semiarid region. Biol Control 6(1):130–136.  https://doi.org/10.1006/bcon.1996.0016 Google Scholar
  48. Godfray HCJ (2011) Ecology, food and biodiversity. Science 333(6047):1231–1232.  https://doi.org/10.1126/science.1211815 PubMedGoogle Scholar
  49. Gonçalves F, Carlos C, Aranha J, Torres L (2017) Does habitat heterogeneity affect the diversity of epigaeic arthropods in vineyards? Agric Forest Entomol:n/a-n/a doi: https://doi.org/10.1111/afe.12270
  50. Gossner MM, Lewinsohn TM, Kahl T, Grassein F, Boch S, Prati D, Birkhofer K, Renner SC, Sikorski J, Wubet T, Arndt H, Baumgartner V, Blaser S, Blüthgen N, Börschig C, Buscot F, Diekötter T, Jorge LR, Jung K, Keyel AC, Klein A-M, Klemmer S, Krauss J, Lange M, Müller J, Overmann J, Pašalić E, Penone C, Perović DJ, Purschke O, Schall P, Socher SA, Sonnemann I, Tschapka M, Tscharntke T, Türke M, Venter PC, Weiner CN, Werner M, Wolters V, Wurst S, Westphal C, Fischer M, Weisser WW, Allan E (2016) Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540(7632):266–269.  https://doi.org/10.1038/nature20575 PubMedGoogle Scholar
  51. Grzywacz D, Parnell D, Kibata G, Oduor G, Ogutu W, Miano D, Winstanley D (2004) The development of endemic baculoviruses of Plutella xylostella (diamondback moth, DBM) for control of DBM in East Africa. In: Endersby NM (ed) The management of diamondback moth and other crucifer pests: Proceedings of the Fourth International Workshop, Melbourne, Australia, 26-29 November 2001 2004. International Diamondback Moth Working Group, pp 197–206Google Scholar
  52. Grzywacz D, Rossbach A, Rauf A, Russell D, Srinivasan R, Shelton A (2010) Current control methods for diamondback moth and other brassica insect pests and the prospects for improved management with lepidopteran-resistant Bt vegetable brassicas in Asia and Africa. Crop Prot 29(1):68–79.  https://doi.org/10.1016/j.cropro.2009.08.009 Google Scholar
  53. Gurr GM, Lu Z, Zheng X, Xu H, Zhu P, Chen G, Yao X, Cheng J, Zhu Z, Catindig JL, Villareal S, Van Chien H, Cuong LQ, Channoo C, Chengwattana N, Lan LP, Hai LH, Chaiwong J, Nicol HI, Perovic DJ, Wratten SD, Heong KL (2016) Multi-country evidence that crop diversification promotes ecological intensification of agriculture. Nature Plants 2:16014.  https://doi.org/10.1038/nplants.2016.14 PubMedGoogle Scholar
  54. Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62(1):91–109.  https://doi.org/10.1146/annurev-ento-031616-035050 PubMedGoogle Scholar
  55. Halaj J, Wise DH (2001) Terrestrial trophic cascades: how much do they trickle? Am Nat 157(3):262–281.  https://doi.org/10.1086/319190 PubMedGoogle Scholar
  56. Heimoana V, Pilkington LJ, Raman A, Mitchell A, Nicol HI, Johnson AC, Gurr GM (2017) Integrating spatially explicit molecular and ecological methods to explore the significance of non-crop vegetation to predators of brassica pests. Agric Ecosyst Environ 239:12–19.  https://doi.org/10.1016/j.agee.2017.01.008 Google Scholar
  57. Hendrichs J, Kenmore P, Robinson AS, Vreysen MJB (2007) Area-wide integrated pest management (AW-IPM): principles, practice and prospects. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Netherlands, Dordrecht, pp 3–33.  https://doi.org/10.1007/978-1-4020-6059-5_1 Google Scholar
  58. Holland JM, Douma JC, Crowley L, James L, Kor L, Stevenson DRW, Smith BM (2017) Semi-natural habitats support biological control, pollination and soil conservation in Europe. A review. Agron Sustain Dev 37(4).  https://doi.org/10.1007/s13593-017-0434-x
  59. Holt R, Lawton J (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25(1):495–520.  https://doi.org/10.1146/annurev.es.25.110194.002431 Google Scholar
  60. Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12(2):197–229.  https://doi.org/10.1016/0040-5809(77)90042-9 PubMedGoogle Scholar
  61. Huang NX, Enkegaard A, Osborne LS, Ramakers PMJ, Messelink GJ, Pijnakker J, Murphy G (2011) The banker plant method in biological control. Crit Rev Plant Sci 30(3):259–278.  https://doi.org/10.1080/07352689.2011.572055 Google Scholar
  62. Hummel RL, Walgenbach JF, Barbercheck ME, Kennedy GG, Hoyt GD, Arellano C (2002) Effects of production practices on soil-borne entomopathogens in western North Carolina vegetable systems. Environ Entomol 31(1):84–91.  https://doi.org/10.1603/0046-225X-31.1.84 Google Scholar
  63. Inglis G, Goettel M, Butt T, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Butt T, Jackson C, Magan N (eds) Fungi as biocontrol agents. CAB International, Wallingford, UK, pp 23–69Google Scholar
  64. Jaronski ST (2007) Soil ecology of the entomopathogenic ascomycetes: a critical examination of what we (think) we know. In: Ekesi S, Maniania NK (eds) Use of entomopathogenic fungi in biological Pest management. Research SignPosts, Trivandrum, India, pp 91–144Google Scholar
  65. Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. BioControl 55(1):159–185.  https://doi.org/10.1007/s10526-009-9248-3 Google Scholar
  66. Jervis MA, Kidd N (1996) Insect natural enemies. Chapman Hall Australia, MelbourneGoogle Scholar
  67. Keller S, Kessler P, Schweizer C (2003) Distribution of insect pathogenic soil fungi in Switzerland with special reference to Beauveria brongniartii and Metharhizium anisopliae. BioControl 48(3):307–319.  https://doi.org/10.1023/a:1023646207455 Google Scholar
  68. Kirk A, Mercadier G, Bordat D, Delvare G, Pichon A, Arvanitakis L, Goudégnon A, Rincon C (2004) Variability in Plutella and its natural enemies: implications for biological control. In: Endersby N (ed) The management of diamondback moths and other crucifer pests: Proceedings of the Fourth International Workshop, Melbourne, Australia, 26-29 November, 2001 2004. Australian Entomological Society, pp 71–77Google Scholar
  69. Klassen W (2005) Area-wide integrated pest management and the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Netherlands, Dordrecht, pp 39–68.  https://doi.org/10.1007/1-4020-4051-2_2 Google Scholar
  70. Klein RM (1978) Plants and near-ultraviolet radiation. Bot Rev 44(1):1–127.  https://doi.org/10.1007/bf02860853 Google Scholar
  71. Koss AM, Chang GC, Snyder WE (2004) Predation of green peach aphids by generalist predators in the presence of alternative, Colorado potato beetle egg prey. Biol Control 31(2):237–244.  https://doi.org/10.1016/j.biocontrol.2004.04.006 Google Scholar
  72. Lacey LA, Frutos R, Kaya HK, Vail P (2001) Insect pathogens as biological control agents: do they have a future? Biol Control 21(3):230–248.  https://doi.org/10.1006/bcon.2001.0938 Google Scholar
  73. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201.  https://doi.org/10.1146/annurev.ento.45.1.175 PubMedGoogle Scholar
  74. Lawrence JL, Hoy CW, Grewal PS (2006) Spatial and temporal distribution of endemic entomopathogenic nematodes in a heterogeneous vegetable production landscape. Biol Control 37(3):247–255.  https://doi.org/10.1016/j.biocontrol.2006.02.002 Google Scholar
  75. Li Y, Weldegergis BT, Chamontri S, Dicke M, Gols R (2017) Does aphid infestation interfere with indirect plant defense against lepidopteran caterpillars in wild cabbage? J Chem Ecol 43(5):493–505.  https://doi.org/10.1007/s10886-017-0842-z PubMedPubMedCentralGoogle Scholar
  76. Li Z, Feng X, Liu S-S, You M, Furlong MJ (2016a) Biology, ecology, and management of the diamondback moth in China. Annu Rev Entomol 61:277–296.  https://doi.org/10.1146/annurev-ento-010715-023622 PubMedGoogle Scholar
  77. Li Z, Zalucki MP, Yonow T, Kriticos DJ, Bao H, Chen H, Hu Z, Feng X, Furlong MJ (2016b) Population dynamics and management of diamondback moth (Plutella xylostella) in China: the relative contributions of climate, natural enemies and cropping patterns. Bull Entomol Res 106(2):197–214.  https://doi.org/10.1017/S0007485315001017 PubMedGoogle Scholar
  78. Liu S, Shi Z, Furlong MJ, Zalucki M (2005) Conservation and enhancement of biological control helps to improve sustainable production of Brassica vegetables in China and Australia. In: Hoddle MS (ed) Second International Symposium on Biological Control of Arthropods, Davos, Switzerland, 2005. pp 254–266Google Scholar
  79. Liu Y-Q, Shi Z-H, Zalucki MP, Liu S-S (2014) Conservation biological control and IPM practices in Brassica vegetable crops in China. Biol Control 68(0):37–46.  https://doi.org/10.1016/j.biocontrol.2013.06.008 Google Scholar
  80. Lu ZX, Zhu PY, Gurr GM, Zheng XS, Read DMY, Heong KL, Yang YJ, Xu HX (2014) Mechanisms for flowering plants to benefit arthropod natural enemies of insect pests: prospects for enhanced use in agriculture. Insect Sci 21(1):1–12.  https://doi.org/10.1111/1744-7917.12000 PubMedGoogle Scholar
  81. Macfadyen S, Hopkinson J, Parry H, Neave MJ, Bianchi FJJA, Zalucki MP, Schellhorn NA (2015) Early-season movement dynamics of phytophagous pest and natural enemies across a native vegetation-crop ecotone. Agric Ecosyst Environ 200:110–118.  https://doi.org/10.1016/j.agee.2014.11.012 Google Scholar
  82. Marshall EJP (2002) Introducing field margin ecology in Europe. Agric Ecosyst Environ 89(1):1–4.  https://doi.org/10.1016/S0167-8809(01)00314-0 Google Scholar
  83. Mason JM, Matthews GA, Wright DJ (1999) Evaluation of spinning disc technology for the application of entomopathogenic nematodes against a foliar pest. J Invertebr Pathol 73(3):282–288.  https://doi.org/10.1006/jipa.1998.4832 PubMedGoogle Scholar
  84. Mason JM, Wright DJ (1997) Potential for the control of Plutella xylostella larvae with entomopathogenic nematodes. J Invertebr Pathol 70(3):234–242.  https://doi.org/10.1006/jipa.1997.4695 Google Scholar
  85. Meyling NV, Eilenberg J (2006) Isolation and characterisation of Beauveria bassiana isolates from phylloplanes of hedgerow vegetation. Mycol Res 110(2):188–195.  https://doi.org/10.1016/j.mycres.2005.09.008 PubMedGoogle Scholar
  86. Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43(2):145–155.  https://doi.org/10.1016/j.biocontrol.2007.07.007 Google Scholar
  87. Meyling NV, Hajek AE (2010) Principles from community and metapopulation ecology: application to fungal entomopathogens. BioControl 55(1):39–54.  https://doi.org/10.1007/s10526-009-9246-5 Google Scholar
  88. Meyling NV, Lübeck M, Buckley EP, Eilenberg J, Rehner SA (2009) Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Mol Ecol 18(6):1282–1293.  https://doi.org/10.1111/j.1365-294X.2009.04095.x PubMedGoogle Scholar
  89. Mo J, Baker G, Keller M, Roush R (2003) Local dispersal of the diamondback moth (Plutella xylostella (L.)) (Lepidoptera: Plutellidae). Environ Entomol 32(1):71–79Google Scholar
  90. Mori AS, Furukawa T, Sasaki T (2013) Response diversity determines the resilience of ecosystems to environmental change. Biol Rev 88(2):349–364.  https://doi.org/10.1111/brv.12004 PubMedGoogle Scholar
  91. Mouttet R, Bearez P, Thomas C, Desneux N (2011) Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLoS One 6(5):e18840.  https://doi.org/10.1371/journal.pone.0018840 PubMedPubMedCentralGoogle Scholar
  92. Mouttet R, Kaplan I, Bearez P, Amiens-Desneux E, Desneux N (2013) Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites. Oecologia 173(4):1379–1386.  https://doi.org/10.1007/s00442-013-2716-6 PubMedGoogle Scholar
  93. Muckenfuss A, Shepard B, Ferrer E (1992) Natural mortality of diamondback moth in coastal South Carolina. In: Talekar NS (ed) Diamondback moth and other crucifer pests: proceedings of the second international workshop, Tainan, Taiwan, 10–14 December 1990. Asian Vegetable Research and Development Center, pp 10–14Google Scholar
  94. Niu Y-Q, Sun Y-X, Liu T-X (2014) Development and reproductive potential of diamondback moth (Lepidoptera: Plutellidae) on selected wild crucifer species. Environ Entomol 43(1):69–74.  https://doi.org/10.1603/EN13206 PubMedGoogle Scholar
  95. Östman Ö, Ives AR (2003) Scale-dependent indirect interactions between two prey species through a shared predator. Oikos 102(3):505–514.  https://doi.org/10.1034/j.1600-0706.2003.12422.x Google Scholar
  96. Paredes D, Cayuela L, Gurr GM, Campos M (2015) Is ground cover vegetation an effective biological control enhancement strategy against olive pests? PLoS One 10(2):e0117265.  https://doi.org/10.1371/journal.pone.0117265 PubMedPubMedCentralGoogle Scholar
  97. Parolin P, Bresch C, Poncet C, Desneux N (2012) Functional characteristics of secondary plants for increased pest management. Int J Pest Manag 58(4):369–377.  https://doi.org/10.1080/09670874.2012.734869 Google Scholar
  98. Pell J, Eilenberg J, Hajek A, Steinkraus D (2001) Biology, ecology and pest management potential of Entomophthorales. In: Butt T, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential CABI International, Wallingford, pp 71–154Google Scholar
  99. Pell JK, Hannam JJ, Steinkraus DC (2010) Conservation biological control using fungal entomopathogens. BioControl 55(1):187–198.  https://doi.org/10.1007/s10526-009-9245-6 Google Scholar
  100. Perović DJ, Gámez-Virués S, Landis DA, Wäckers F, Gurr GM, Wratten SD, You M-S, Desneux N (2018) Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales. Biol Rev 93(1):306–321.  https://doi.org/10.1111/brv.12346 PubMedGoogle Scholar
  101. Perović DJ, Gurr GM, Raman A, Nicol HI (2010) Effect of landscape composition and arrangement on biological control agents in a simplified agricultural system: a cost-distance approach. Biol Control 52(3):263–270.  https://doi.org/10.1016/j.biocontrol.2009.09.014 Google Scholar
  102. Perring TM (2001) The Bemisia tabaci species complex. Crop Prot 20(9):725–737.  https://doi.org/10.1016/S0261-2194(01)00109-0 Google Scholar
  103. Philips CR, Fu Z, Kuhar TP, Shelton AM, Cordero RJ (2014) Natural history, ecology, and management of diamondback moth (Lepidoptera: Plutellidae), with emphasis on the United States. J Integr Pest Manag 5(3):D1–D11.  https://doi.org/10.1603/IPM14012 Google Scholar
  104. Poelman EH, Zheng S-J, Zhang Z, Heemskerk NM, Cortesero A-M, Dicke M (2011) Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proce Nat Acad Sci USA 108(49):19647–19652.  https://doi.org/10.1073/pnas.1110748108 Google Scholar
  105. Raps A, Vidal S (1998) Indirect effects of an unspecialized endophytic fungus on specialized plant—herbivorous insect interactions. Oecologia 114(4):541–547.  https://doi.org/10.1007/s004420050478 PubMedGoogle Scholar
  106. Ratnasinghe G, Hague N (1998) The invasion, development and reproduction of Steinernema carpocapsae (Rhabditida: Steinernematidae) in the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Nematropica 28(1):1–6Google Scholar
  107. Roberts DW, Campbell AS (1977) Stability of entomopathogenic fungi. Misc Publ Entomol Soc Am 10:19–76Google Scholar
  108. Saqib HS, You M, Gurr GM (2017) Multivariate ordination identifies vegetation types associated with spider conservation in brassica crops. PeerJ Preprints 5:e3003v3001.  https://doi.org/10.7287/peerj.preprints.3003v1 Google Scholar
  109. Sarfraz M, Keddie AB, Dosdall LM (2007) Biological control of the diamondback moth, Plutella xylostella: a review. Biocontrol Sci Tech 15(8):763–789.  https://doi.org/10.1080/09583150500136956 Google Scholar
  110. Sarfraz M, Keddie BA (2005) Conserving the efficacy of insecticides against Plutella xylostella (L.) (Lep., Plutellidae). J Appl Entomol 129(3):149–157.  https://doi.org/10.1111/j.1439-0418.2005.00930.x Google Scholar
  111. Schellhorn NA, Macfadyen S, Bianchi FJJA, Williams DG, Zalucki MP (2008) Managing ecosystem services in broadacre landscapes: what are the appropriate spatial scales? Aust J Exp Agric 48(12):1549–1559.  https://doi.org/10.1071/EA08112 Google Scholar
  112. Schmidt MH, Roschewitz I, Thies C, Tscharntke T (2005) Differential effects of landscape and management on diversity and density of ground-dwelling farmland spiders. J Appl Ecol 42(2):281–287.  https://doi.org/10.1111/j.1365-2664.2005.01014.x Google Scholar
  113. Schneider S, Widmer F, Jacot K, Kölliker R, Enkerli J (2012) Spatial distribution of Metarhizium clade 1 in agricultural landscapes with arable land and different semi-natural habitats. Appl Soil Ecol 52(Supplement C):20–28.  https://doi.org/10.1016/j.apsoil.2011.10.007 Google Scholar
  114. Schroer S, Ehlers RU (2005) Foliar application of the entomopathogenic nematode Steinernema carpocapsae for biological control of diamondback moth larvae (Plutella xylostella). Biol Control 33(1):81–86.  https://doi.org/10.1016/j.biocontrol.2004.12.009 Google Scholar
  115. Shah P, Pell J (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61(5–6):413–423.  https://doi.org/10.1007/s00253-003-1240-8 PubMedGoogle Scholar
  116. Shelton A (2004) Management of the diamondback moth: déjà vu all over again In: Endersby NM, Ridland P (eds) The management of diamondback moth and other crucifer pests: Proceedings of the 4th International Workshop, Melbourne, Australia, 26–29 November, 2001. The Regional Institute Ltd, pp 3–8Google Scholar
  117. Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI (2011a) Insect attraction to synthetic herbivore-induced plant volatile-treated field crops. Agric For Entomol 13(1):45–57.  https://doi.org/10.1111/j.1461-9563.2010.00496.x Google Scholar
  118. Simpson M, Gurr GM, Simmons AT, Wratten SD, James DG, Leeson G, Nicol HI, Orre-Gordon GUS (2011b) Attract and reward: combining chemical ecology and habitat manipulation to enhance biological control in field crops. J Appl Ecol 48(3):580–590.  https://doi.org/10.1111/j.1365-2664.2010.01946.x Google Scholar
  119. Stavely F, Pell J, Chapman B, Glare T, Yeo H, Suckling D, Walter M (2004) Insect pathogens for biological control of the diamondback moth with particular emphasis on the fungus Zoophthora radicans in New Zealand. In: Endersby N (ed) The management of diamondback moths and other crucifer pests: Proceedings of the Fourth International Workshop, Melbourne, Australia, 26-29 November, 2001 2004. Australian Entomological Society, pp 285–288Google Scholar
  120. Sun X, Peng H-Y (2007) Recent advances in biological control of pest insects by using viruses in China. Virol Sin 22(2):158–162.  https://doi.org/10.1007/s12250-007-0017-0 Google Scholar
  121. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47(1):561–594.  https://doi.org/10.1146/annurev.ento.47.091201.145240 PubMedGoogle Scholar
  122. Tabashnik BE, Cushing NL, Johnson MW (1987) Diamondback moth (Lepidoptera: Plutellidae) resistance to insecticides in Hawaii: intra-island variation and cross-resistance. J Econ Entomol 80(6):1091–1099.  https://doi.org/10.1093/jee/80.6.1091 Google Scholar
  123. Tack AJM, Gripenberg S, Roslin T (2011) Can we predict indirect interactions from quantitative food webs?—an experimental approach. J Anim Ecol 80(1):108–118.  https://doi.org/10.1111/j.1365-2656.2010.01744.x PubMedGoogle Scholar
  124. Talekar N, Shelton A (1993) Biology, ecology, and management of the diamondback moth. Annu Rev Entomol 38(1):275–301.  https://doi.org/10.1146/annurev.en.38.010193.001423 Google Scholar
  125. Tkaczuk C, Król A, Majchrowska-Safaryan A, Nicewicz Ł (2014) The occurrence of entomopathogenic fungi in soils from fields cultivated in a conventional and organic system. J Ecol Eng 15(4):137–144.  https://doi.org/10.12911/22998993.1125468 Google Scholar
  126. Tkaczuk C, Krzyczkowski T, Wegensteiner R (2012) The occurrence of entomopathogenic fungi in soils from mid-field woodlots and adjacent small-scale arable fields. Acta Mycol 47(2):191–202Google Scholar
  127. Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Ann Rev Entomol 49(1):405–430.  https://doi.org/10.1146/annurev.ento.49.061802.123339 Google Scholar
  128. Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batary P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Frund J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87(3):661–685.  https://doi.org/10.1111/j.1469-185X.2011.00216.x PubMedGoogle Scholar
  129. Vandenberg J, Griggs M, Wraight S, Shelton A (1999) Season-long management of lepidopteran pests of fresh-market cabbage using microbial control agents. Paper presented at the XXXIIth Annual Meeting of the Society for Invertebrate Pathology, Irvine, California, 22–27 August 1999Google Scholar
  130. Vandenberg JD, Shelton AM, Wilsey WT, Ramos M (1998) Assessment of Beauveria bassiana sprays for control of diamondback moth (Lepidoptera: Plutellidae) on crucifers. J Econ Entomol 91(3):624–630.  https://doi.org/10.1093/jee/91.3.624 Google Scholar
  131. Verkerk RHJ, Wright DJ (1996) Multitrophic interactions and management of the diamondback moth: a review. Bull Entomol Res 86(3):205–216.  https://doi.org/10.1017/S0007485300052482 Google Scholar
  132. Verkerk RHJ, Wright DJ (1997) Field-based studies with the diamondback moth tritrophic system in Cameron Highlands of Malaysia: implications for pest management. Int J Pest Manag 43(1):27–33.  https://doi.org/10.1080/096708797228942 Google Scholar
  133. Vickers RA, Furlong MJ, White A, Pell JK (2004) Initiation of fungal epizootics in diamondback moth populations within a large field cage: proof of concept for auto-dissemination. Entomologia Experimentalis et Applicata 111(1):7–17.  https://doi.org/10.1111/j.0013-8703.2004.00140.x Google Scholar
  134. Wäckers FL, Lee JC, Heimpel GE, Winkler K, Wagenaar R (2006) Hymenopteran parasitoids synthesize ‘honeydew-specific’ oligosaccharides. Funct Ecol 20(5):790–798.  https://doi.org/10.1111/j.1365-2435.2006.01158.x Google Scholar
  135. Wade MR, Zalucki MP, Wratten SD, Robinson KA (2008) Conservation biological control of arthropods using artificial food sprays: current status and future challenges. Biol Control 45(2):185–199.  https://doi.org/10.1016/j.biocontrol.2007.10.024 Google Scholar
  136. Wang F, Deng J, Schal C, Lou Y, Zhou G, Ye B, Yin X, Xu Z, Shen L (2016) Non-host plant volatiles disrupt sex pheromone communication in a specialist herbivore. Sci Rep 6:32666.  https://doi.org/10.1038/srep32666 PubMedPubMedCentralGoogle Scholar
  137. Wei S-J, Shi B-C, Gong Y-J, Jin G-H, Chen X-X, Meng X-F (2013) Genetic structure and demographic history reveal migration of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) from the southern to northern regions of China. PLoS One 8(4):e59654.  https://doi.org/10.1371/journal.pone.0059654 PubMedPubMedCentralGoogle Scholar
  138. Westphal C, Vidal S, Horgan FG, Gurr GM, Escalada M, Van Chien H, Tscharntke T, Heong KL, Settele J (2015) Promoting multiple ecosystem services with flower strips and participatory approaches in rice production landscapes. Basic Appl Ecol 16(8):681–689.  https://doi.org/10.1016/j.baae.2015.10.004 Google Scholar
  139. Wielgoss A, Clough Y, Fiala B, Rumede A, Tscharntke T (2012) A minor pest reduces yield losses by a major pest: plant-mediated herbivore interactions in Indonesian cacao. J Appl Ecol 49(2):465–473.  https://doi.org/10.1111/j.1365-2664.2012.02122.x Google Scholar
  140. Wilding N (1986) The pathogens of diamondback moth and their potential for its control-a review. In: Talekar NS, Griggs TD (eds) Diamondback moth management: Proceedings of the First International Workshop, Tainan, Taiwan, 11–15 March 1985. The Asian Vegetable Research and Development Center, pp 219–232Google Scholar
  141. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25(1):443–466.  https://doi.org/10.1146/annurev.es.25.110194.002303 Google Scholar
  142. Wright D, Peters A, Schroder S, Fife J (2005) Application technology. In: Grewal P, Ehlers R, Shapiro-Ilan D (eds) Nematodes as biocontrol agents. CAB International, Wallingford, UK, pp 91–106Google Scholar
  143. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Nat Acad Sci USA 96(4):1463–1468.  https://doi.org/10.1073/pnas.96.4.1463 PubMedPubMedCentralGoogle Scholar
  144. Yang MM, Li ML, an Zhang Y, Wang YZ, Qu LJ, Wang QH, Ding JY (2012) Baculoviruses and insect pests control in China. Afr J Agric Res 6(2):214–218.  https://doi.org/10.5897/AJMR11.1357 Google Scholar
  145. Yeo H, Pell J, Walter M, Boyd-Wilson K, Snelling C, Suckling D (2001) Susceptibility of diamondback moth (Plutella xylostella (L.)) larvae to the entomopathogenic fungus, Zoophthora radicans (Brefeld) Batko. New Zealand. Plant Prot 54:47–50Google Scholar
  146. Zalucki M, Furlong M (2011) Predicting outbreaks of a migratory pest: an analysis of DBM distribution and abundance revisited. In: Srinivasan R, Shelton AM, Collins HL (eds) Proceedings of the 6th International Workshop on Management of the Diamondback Moth and Other Crucifer Insect Pests. Nakhon Pathom, Thailand, pp 8–14Google Scholar
  147. Zalucki MP, Adamson D, Furlong MJ (2009) The future of IPM: whither or wither? Aust J Entomol 48(2):85–96.  https://doi.org/10.1111/j.1440-6055.2009.00690.x Google Scholar
  148. Zalucki MP, Shabbir A, Silva R, Adamson D, Shu-Sheng L, Furlong MJ (2012) Estimating the economic cost of one of the world's major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J Econ Entomol 105(4):1115–1129.  https://doi.org/10.1603/EC12107 PubMedGoogle Scholar
  149. Zhang L (2014) Colonization pattern of crop plants by endophytic fungi. PhD, Georg-August-University Göttingen, GermanyGoogle Scholar
  150. Zhang P-J, Broekgaarden C, Zheng S-J, Snoeren TAL, van Loon JJA, Gols R, Dicke M (2013) Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol 197(4):1291–1299.  https://doi.org/10.1111/nph.12106 PubMedGoogle Scholar
  151. Zhao JZ, Collins HL, Li YX, Mau RFL, Thompson GD, Hertlein M, Andaloro JT, Boykin R, Shelton AM (2006) Monitoring of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad, indoxacarb, and emamectin benzoate. J Econ Entomol 99(1):176–181. https://doi.org/10.1603/0022-0493(2006)099[0176:MODMLP]2.0.CO;2Google Scholar

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© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, duplication, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

Authors and Affiliations

  • Geoff M. Gurr
    • 1
    • 2
    • 3
    • 4
  • Olivia L. Reynolds
    • 2
    • 4
    • 5
  • Anne C. Johnson
    • 4
  • Nicolas Desneux
    • 6
  • Myron P. Zalucki
    • 7
  • Michael J. Furlong
    • 7
  • Zhenyu Li
    • 8
  • Komivi S. Akutse
    • 1
    • 2
    • 3
    • 10
  • Junhui Chen
    • 1
    • 2
    • 3
  • Xiwu Gao
    • 9
  • Minsheng You
    • 1
    • 2
    • 3
  1. 1.State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied EcologyFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Joint International Research Laboratory of Ecological Pest Control, Ministry of EducationFuzhouChina
  3. 3.Fujian-Taiwan Joint Innovation Centre for Ecological Control of Crop PestsFujian Agriculture and Forestry UniversityFuzhouChina
  4. 4.Graham Centre (an alliance between NSW Department of Primary Industries and Charles Sturt University)Wagga WaggaAustralia
  5. 5.NSW Department of Primary IndustriesElizabeth Macarthur Agricultural InstituteMenangleAustralia
  6. 6.INRA (French National Institute for Agricultural Research), CNRS, UMR 1355-7254 Institute Sophia AgrobiotechUniversité Côte d’AzurSophia-AntipolisFrance
  7. 7.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  8. 8.Institute of Plant Protection, Guangdong Academy of Agricultural Sciences and Guangdong Provincial Key Laboratory of High Technology for Plant ProtectionGuangzhouChina
  9. 9.Department of EntomologyChina Agricultural UniversityBeijingChina
  10. 10.International Centre of Insect Physiology and EcologyNairobiKenya

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