1932

Abstract

Development of resistance in major grain insect pest species to the key fumigant phosphine (hydrogen phosphide) across the globe has put the viability and sustainability of phosphine in jeopardy. The resistance problem has been aggravated over the past two decades, due mostly to the lack of suitable alternatives matching the major attributes of phosphine, including its low price, ease of application, proven effectiveness against a broad pest spectrum, compatibility with most storage conditions, and international acceptance as a residue-free treatment. In this review, we critically analyze the published literature in the area of phosphine resistance with special emphasis on the methods available for detection of resistance, the genetic basis of resistance development, key management strategies, and research gaps that need to be addressed.

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2020-01-07
2024-10-12
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Literature Cited

  1. 1. 
    Acda MA. 2000. Phosphine resistance inRhyzopertha dominica(F.) (Coleoptera: Bostrychidae) from the Philippines MS Thesis, Univ. Queensland Brisbane, Aust:.
    [Google Scholar]
  2. 2. 
    Afful E. 2018. Resistance ofRhyzopertha dominica(Coleoptera: Bostrichidae) to phosphine fumigation; geographic variation, high dose treatments and rapid assay assessment PhD Thesis, Kansas State Univ Manhattan: http://hdl.handle.net/2097/39245
    [Google Scholar]
  3. 3. 
    Afful E, Elliott B, Nayak MK, Phillips TW 2018. Phosphine resistance in North American field populations of the lesser grain borer, Rhyzoperthadominica (F.) (Coleoptera: Bostrichidae). J. Econ. Entomol. 111:463–69First extensive survey showing widespread development of phosphine resistance in North America.
    [Google Scholar]
  4. 4. 
    Agrafioti P, Athanassiou CG, Nayak MK 2019. Detection of phosphine resistance in major stored-product insects in Greece and evaluation of a field resistance test kit. J. Stored Prod. Res. 82:40–47First comprehensive phosphine resistance monitoring report from Europe in four decades.
    [Google Scholar]
  5. 5. 
    Ahmedani MS, Shaheen N, Ahmedani MY, Aslam M 2007. Status of phosphine resistance in khapra beetle, Trogodermagranarium (Everts) strains collected from remote villages of Rawalpindi District. Pak. Entomol. 29:95–102
    [Google Scholar]
  6. 6. 
    Athanassiou CG, Phillips TW, Wakil W 2019. Biology and control of the khapra beetle, Trogodermagranarium, a major quarantine threat to global food security. Annu. Rev. Entomol. 64:131–48
    [Google Scholar]
  7. 7. 
    Athie I, Gomes RAR, Bolonhezi S, Valentini SRT, de Castro MFPM 1998. Effects of carbon dioxide and phosphine mixtures on resistant populations of stored-grain insects. J. Stored Prod. Res. 34:27–32
    [Google Scholar]
  8. 8. 
    Aulicky R, Stejskal V. 2015. Efficacy and limitations of phosphine “spot fumigation” against five Coleoptera species of stored product pests in wheat in a grain store: short note. Plant Protect. Sci. 51:33–38
    [Google Scholar]
  9. 9. 
    Aulicky R, Stejskal V, Frydova B 2019. Field validation of phosphine efficacy on the first recorded resistant strains of Sitophilusgranarius and Triboliumcastaneum from Czech Republic. J. Stored Prod. Res. 81:107–13
    [Google Scholar]
  10. 10. 
    Aulicky R, Stejskal V, Frydova B, Athanassiou CG 2015. Susceptibility of two strains of the confused flour beetle (Coleoptera: Tenebrionidae) following phosphine structural mill fumigation: effects of concentration, temperature, and flour deposits. J. Econ. Entomol. 108:62823–30
    [Google Scholar]
  11. 11. 
    Bell CH, Savvidou N, Mills KA, Bradberry S, Barlow ML 1994. A same day test for detecting resistance to phosphine. Proceedings of the 6th International Working Conference on Stored Product Protection E Highley, EJ Wright, HJ Banks, BR Champ 41–44 Wallingford, UK: CAB Int.
    [Google Scholar]
  12. 12. 
    Bell CH, Wilson SM. 1995. Phosphine tolerance and resistance in Trogodermagranarium Everts (Coleoptera: Dermestidae). J. Stored Prod. Res. 31:199–205
    [Google Scholar]
  13. 13. 
    Bengston M, Collins PJ, Daglish GJ, Hallman VL, Kopittke RA, Pavic H 1999. Inheritance of phosphine resistance in Triboliumcastaneum (Coleoptera: Tenebrionidae). J. Econ. Entomol. 92:17–20
    [Google Scholar]
  14. 14. 
    Benhalima H, Chaudhry MQ, Mills KA, Price NR 2004. Phosphine resistance in stored-product insects collected from various grain storage facilities in Morocco. J. Stored Prod. Res. 40:241–49
    [Google Scholar]
  15. 15. 
    Bond EJ. 1984. Manual of fumigation for insect control Plant Prod. Protect. Pap. 54, Food Agric. Org U.N., Rome:
    [Google Scholar]
  16. 16. 
    Boyer S, Zhang H, Lempérière G 2012. A review of control methods and resistance mechanisms in stored-product insects. Bull. Entomol. Res. 102:213–29
    [Google Scholar]
  17. 17. 
    Cao Y, Son Y, Sun GY 2003. A survey of psocid species infesting stored grain in China and resistance to phosphine in field populations of Liposcelisentomophila (Enderlein) (Psocoptera: Liposcelididae). Proceedings of the 8th International Working Conference on Stored Product Protection PF Credland, DM Armitage, CH Bell, PM Cogan, E Highley 662–67 Wallingford, UK: CAB Int.
    [Google Scholar]
  18. 18. 
    Cato AJ. 2015. Phosphine resistance in North American Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) MS Thesis, Kansas State Univ Manhattan: http://hdl.handle.net/2097/20337
    [Google Scholar]
  19. 19. 
    Cato AJ, Elliott B, Nayak MK, Phillips TW 2017. Geographic variation in phosphine resistance among North American populations of the red flour beetle (Coleoptera: Tenebrionidae). J. Econ. Entomol. 110:1359–65
    [Google Scholar]
  20. 20. 
    Chadda IC. 2016. Fumigation with phosphine: a perspective. Indian J. Entomol. 78:39–45
    [Google Scholar]
  21. 21. 
    Champ BR, Dyte CE. 1976. Report on the FAO global survey of pesticide susceptibility of stored grain pests Rep. 5, Plant Protect. Prod. Serv., Food Agric. Org U.N., Rome:First survey of phosphine resistance in major stored product pests across six continents.
    [Google Scholar]
  22. 22. 
    Chaudhry MQ. 1997. A review of the mechanisms involved in the action of phosphine as an insecticide and phosphine resistance in stored-products insects. Pestic. Sci. 49:213–28
    [Google Scholar]
  23. 23. 
    Chen Z, Schlipalius D, Opit G, Subramanyam B, Phillips TW 2015. Diagnostic molecular markers for phosphine resistance in US populations of Triboliumcastaneum and Rhyzoperthadominica. PLOS ONE 10:3e0121343First US study using a PCR diagnostic for strong resistance gene in Tribolium castaneum field populations.
    [Google Scholar]
  24. 24. 
    Collins PJ. 2009. Strategy to manage resistance to phosphine in the Australian grain industry Rep. CRC70096, Natl. Work. Party Grain Protect., Coop. Res. Cent. Natl. Plant Biosecur. Proj Bruce, Aust. https://www.graintrade.org.au/sites/default/files/file/NWPGP/Phosphine%20Resistance%20Strategy.pdf
    [Google Scholar]
  25. 25. 
    Collins PJ, Daglish GJ, Bengston M, Lambkin TM, Pavic H 2002. Genetics of phosphine resistance in Rhyzoperthadominica (Coleoptera: Bostrichidae). J. Econ. Entomol. 95:4862–69First characterization of two levels (weak and strong) of phosphine resistance in a stored product pest.
    [Google Scholar]
  26. 26. 
    Collins PJ, Daglish GJ, Pavic H, Kopittke KA 2005. Response of mixed-age cultures of phosphine-resistant and susceptible strains of the lesser grain borer, Rhyzoperthadominica, to phosphine at a range of concentrations and exposure periods. J. Stored Prod. Res. 41:373–85
    [Google Scholar]
  27. 27. 
    Collins PJ, Falk MG, Nayak MK, Emery RN, Holloway JC 2017. Monitoring resistance to phosphine in the lesser grain borer, Rhyzoperthadominica, in Australia: a national analysis of trends, storage types and geography in relation to resistance detections. J. Stored Prod. Res 70:25–36
    [Google Scholar]
  28. 28. 
    Daglish GJ. 2004. Effect of exposure period on degree of dominance of phosphine resistance in adults of Rhyzoperthadominica (Coleoptera: Bostrychidae) and Sitophilusoryzae (Coleoptera: Curculionidae). Pest Manag. Sci. 60:822–26
    [Google Scholar]
  29. 29. 
    Daglish GJ, Collins PJ. 1999. Improving the relevance of assays for phosphine resistance. Proceedings of the 7th International Working Conference on Stored Product Protection Z Jin, Q Liang, Y Liang, X Tan, L Guan 584–93 Wallingford, UK: CAB Int.
    [Google Scholar]
  30. 30. 
    Daglish GJ, Collins PJ, Pavic H, Kopittke KA 2002. Effects of time and concentration on mortality of phosphine-resistant Sitophilusoryzae (L.) fumigated with phosphine. Pest Manag. Sci. 58:1015–21First quantification of time and concentration effects on phosphine efficacy against resistant pest populations.
    [Google Scholar]
  31. 31. 
    Daglish GJ, Nayak MK, Pavic H 2014. Phosphine resistance in Sitophilusoryzae (L.) from eastern Australia: inheritance, fitness and prevalence. J. Stored Prod. Res. 59:237–44
    [Google Scholar]
  32. 32. 
    Daglish GJ, Nayak MK, Pavic H, Smith LW 2015. Prevalence and potential fitness cost of weak phosphine resistance in Triboliumcastaneum (Herbst) in eastern Australia. J. Stored Prod. Res. 61:54–58
    [Google Scholar]
  33. 33. 
    Daglish GJ, Ridley AW, Reid R, Walter GH 2017. Testing the consistency of spatio-temporal patterns of flight activity in the stored grain beetles Triboliumcastaneum (Herbst) and Rhyzoperthadominica (F.). J. Stored Prod. Res. 72:68–74
    [Google Scholar]
  34. 34. 
    Edde PA, Phillips TW, Nansen C, Payton ME 2006. Flight activity of the lesser grain borer, Rhyzoperthadominica F. (Coleoptera: Bostrichidae), in relation to weather. Environ. Entomol. 35:616–24
    [Google Scholar]
  35. 35. 
    Emery RN, Nayak MK, Holloway JC 2011. Lessons learned from phosphine resistance monitoring in Australia. Stewart Postharvest Rev7(3):spr.2011.3.6
    [Google Scholar]
  36. 36. 
    FAO 1975. Recommended methods for the detection and measurement of resistance of agricultural pests to pesticides: tentative method for adults of some major species of stored cereals with methyl bromide and phosphine—FAO Method No 16. FAO Plant Prot. Bull. 23:12–25First bioassay method to detect phosphine resistance in major stored product pests.
    [Google Scholar]
  37. 37. 
    Farm Futures 2007. Egypt rejects wheat shipment. Farm Futures June 12. http://www.farmfutures.com/story-egypt-rejects-wheat-shipment-17-27041
    [Google Scholar]
  38. 38. 
    Finney DJ. 1971. Probit Analysis Cambridge, UK: Cambridge Univ. Press3rd ed.
    [Google Scholar]
  39. 39. 
    Gautam SG, Opit GP, Hosoda E 2016. Phosphine resistance in adult and immature life stages of Triboliumcastaneum (Coleoptera: Tenebrionidae) and Plodiainterpunctella (Lepidoptera: Pyralidae) populations in California. J. Econ. Entomol. 109:2525–33
    [Google Scholar]
  40. 40. 
    Gengembre M. 1783. Mémoire sur un nouveau gas obtenu, par l'action des substances alkalines, sur le phosphore de Kunckel. Mém. Math. Phys. 10:651–58
    [Google Scholar]
  41. 41. 
    GRDC 2014. Pressure testing sealable silos Grain Storage Fact Sheet, Grain Res. Dev. Corp Kingston, Aust: http://storedgrain.com.au/pressure-testing/
    [Google Scholar]
  42. 42. 
    GRDC 2017. Grain Research and Development Corporation updates: economics of on-farm grain storage: a grains industry guide Rep., Grain Res. Dev. Corp Canberra, Aust: https://grdc.com.au/resources-and-publications/all-publications/publications/2013/09/economics-of-onfarm-grain-storage
    [Google Scholar]
  43. 43. 
    GTA 2019. GTA Trading Standards 2019/20: wheat and barley Rep., Grain Trade Aust. Sydney: http://www.graintrade.org.au/commodity_standards
    [Google Scholar]
  44. 44. 
    Hagstrum DW, Phillips TW, Cuperus G 2012. Stored Product Protection DW Hagstrum, TW Phillips, G Cuperus 1–5 Manhattan, KS: Kansas State Univ.
    [Google Scholar]
  45. 45. 
    Holloway JC, Falk MG, Emery RN, Collins PJ, Nayak MK 2016. Resistance to phosphine in Sitophilusoryzae in Australia: a national analysis of trends and frequencies over time and geographic spread. J. Stored Prod. Res. 69:129–37
    [Google Scholar]
  46. 46. 
    Holloway JC, Mayer DG, Daglish GJ 2018. Flight activity of Cryptolestesferrugineus in southern New South Wales, Australia. J. Pest Sci. 91:1353–62
    [Google Scholar]
  47. 47. 
    Hori M, Kasaishi Y. 2005. Development of the new assay method for quickly evaluating phosphine resistance of the cigarette beetle, Lasiodermaserricorne (Fabricius) (Coleoptera: Anobiidae), based on the knockdown of the adult beetles. Appl. Entomol. Zool. 40:99–104
    [Google Scholar]
  48. 48. 
    Hsu CH, Chi BC, Liu MY, Li JH, Chen CJ, Chen RY 2002. Phosphine induced oxidative damage in rats: role of glutathione. Toxicology 179:1–8
    [Google Scholar]
  49. 49. 
    Jagadeesan R, Collins PJ, Daglish GJ, Ebert PR, Schlipalius DI 2012. Phosphine resistance in the rust red flour beetle, Triboliumcastaneum (Herbst) (Coleoptera: Tenebrionidae): inheritance, gene interactions and fitness costs. PLOS ONE 7:2e31582
    [Google Scholar]
  50. 50. 
    Jagadeesan R, Collins PJ, Nayak MK, Schlipalius DI, Ebert PR 2016. Genetic characterization of field-evolved resistance to phosphine in the rusty grain beetle, Cryptolestesferrugineus (Laemophloeidae: Coleoptera). Pest Biochem. Physiol. 127:67–75
    [Google Scholar]
  51. 51. 
    Jagadeesan R, Fotheringham A, Ebert PR, Schlipalius DI 2013. Rapid genome wide mapping of phosphine resistance loci by a simple regional averaging analysis in the red flour beetle, Triboliumcastaneum. BMC Genom. 14:650–62
    [Google Scholar]
  52. 52. 
    Jagadeesan R, Nayak MK. 2017. Phosphine resistance does not confer cross-resistance to sulfuryl fluoride in four major stored grain insect pests. Pest Manag. Sci. 73:1391–401
    [Google Scholar]
  53. 53. 
    Jagadeesan R, Nayak MK, Pavic H, Chandra K, Collins PJ 2015. Susceptibility to sulfuryl fluoride and lack of cross-resistance to phosphine in developmental stages of the red flour beetle, Triboliumcastaneum (Coleoptera: Tenebrionidae). Pest Manag. Sci. 71:1379–86First-time determination of lack of cross-resistance to sulfuryl fluoride in phosphine-resistant pests.
    [Google Scholar]
  54. 54. 
    Jagadeesan R, Singarayan VT, Ebert PR, Nayak MK 2018. Potential of co-fumigation with phosphine (PH3) and sulfuryl fluoride (SO2F2) for the management of strongly phosphine-resistant insect pests of stored grain. J. Econ. Entomol. 111:2956–65
    [Google Scholar]
  55. 55. 
    Kashi KP. 1981. Toxicity of phosphine to five species of store-product insects in atmospheres of air and nitrogen. Pestic. Sci. 12:116–22
    [Google Scholar]
  56. 56. 
    Kaur R, Daniels E, Nayak MK, Ebert PR, Schlipalius DI 2013. Determining changes in the distribution and abundance of a Rhyzoperthadominica phosphine resistance allele in farm grain storages using a DNA marker. Pest Manag. Sci. 69:685–88
    [Google Scholar]
  57. 57. 
    Kaur R, Nayak MK. 2015. Developing effective fumigation protocols to manage strongly phosphine-resistant Cryptolestesferrugineus (Stephens) (Coleoptera: Laemophloeidae). Pest Manag. Sci. 71:1297–302
    [Google Scholar]
  58. 58. 
    Kaur R, Schlipalius DI, Collins PJ, Swain AJ, Ebert PR 2012. Inheritance and relative dominance, expressed as toxicity response and delayed development, of phosphine resistance in immature stages of Rhyzoperthadominica (F.) (Coleoptera: Bostrichidae). J. Stored Prod. Res. 51:74–80
    [Google Scholar]
  59. 59. 
    Kaur R, Subbarayalu M, Jagadeesan R, Daglish GJ, Nayak MK et al. 2015. Phosphine resistance in India is characterised by a dihydrolipamide dehydrogenase variant that is otherwise unobserved in eukaryotes. Heredity 115:188–94
    [Google Scholar]
  60. 60. 
    Koçak E, Schlipalius D, Kaur R, Tuck A, Ebert P et al. 2015. Determining phosphine resistance in rust red flour beetle, Triboliumcastaneum (Herbst.) (Coleoptera: Tenebrionidae) populations from Turkey. Türk. Entomol. Derg. 39:129–36
    [Google Scholar]
  61. 61. 
    Konemann CE, Hubhachen Z, Opit GP, Gautam S, Bajracharya NS 2017. Phosphine resistance in Cryptolestesferrugineus (Coleoptera: Laemophloeidae) collected from grain storage facilities in Oklahoma, USA. J. Econ. Entomol. 110:1377–83
    [Google Scholar]
  62. 62. 
    Ling Z. 1999. Development and countermeasures of resistance in stored grain insects in Guangdong of China. Proceedings of the 7th International Working Conference on Stored Product Protection Z Jin, Q Liang, Y Liang, X Tan, L Guan 642–47 Wallingford, UK: CAB Int.
    [Google Scholar]
  63. 63. 
    Lorini I, Collins PJ, Daglish GJ, Nayak MK, Pavic H 2007. Detection and characterisation of strong resistance to phosphine in Brazilian Rhyzoperthadominica (F.) (Coleoptera: Bostrychidae). Pest Manag. Sci. 63:358–64
    [Google Scholar]
  64. 64. 
    Malekpour R, Rafter MA, Daglish GJ, Walter GH 2018. The movement abilities and resource location behaviour of Triboliumcastaneum: phosphine resistance and its genetic influences. J. Pest Sci. 91:739–49
    [Google Scholar]
  65. 65. 
    Manivannan S, Koshy GE, Patil SA 2016. Response of phosphine-resistant mixed-age cultures of lesser grain borer, Rhyzoperthadominica (F.) to different phosphine-carbon dioxide mixtures. J. Stored Prod. Res. 69:175–78
    [Google Scholar]
  66. 66. 
    Mau YS, Collins PJ, Daglish GJ, Nayak MK, Ebert PR 2012. The rph2 gene is responsible for high level resistance to phosphine in independent field isolates of Rhyzoperthadominica. PLOS ONE 7:3e34027
    [Google Scholar]
  67. 67. 
    Mau YS, Collins PJ, Daglish GJ, Nayak MK, Pavic H, Ebert PR 2012. The rph1 gene is a common contributor to the evolution of phosphine resistance in independent field isolates of Rhyzoperthadominica. PLOS ONE 7:2e31541
    [Google Scholar]
  68. 68. 
    McCulloch GA, Mohankumar S, Subramanian S, Sonai Rajan T, Rahul C et al. 2019. Contrasting patterns of phylogeographic structuring in two key beetle pests of stored grain in India and Australia. J. Pest Sci. 92:1249–59
    [Google Scholar]
  69. 69. 
    Mills KA. 1983. Resistance to the fumigant hydrogen phosphide in some stored product species associated with repeated inadequate treatments. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 4:98–101
    [Google Scholar]
  70. 70. 
    Mills KA, Athie I. 1999. The development of a same day test for the detection of resistance to phosphine in Sitophilusoryzae (L.) and Oryzaephilussurinamensis (L.) and findings on the genetics of the resistance related to a strategy to prevent its increase. Proceedings of the 7th International Working Conference on Stored Product Protection Z Jin, Q Liang, Y Liang, X Tan, L Guan 594–602 Wallingford, UK: CAB Int.
    [Google Scholar]
  71. 71. 
    Myers SW, Hagstrum DW. 2012. Quarantine. Stored Product Protection DW Hagstrum, TW Phillips, G Cuperus 297–304 Manhattan, KS: Kansas State Univ.
    [Google Scholar]
  72. 72. 
    Nayak MK, Collins PJ. 2008. Influence of temperature and humidity on toxicity of phosphine against strongly resistant Liposcelisbostrychophila Badonnel (Psocoptera: Liposcelididae), a cosmopolitan pest of stored commodities. Pest Manag. Sci. 64:971–76
    [Google Scholar]
  73. 73. 
    Nayak MK, Collins PJ, Holloway JC, Emery RN, Pavic H, Bartlet J 2013. Strong resistance to phosphine in the rusty grain beetle, Cryptolestesferrugineus (Stephens) (Coleoptera: Laemophloeidae): its characterisation, a rapid assay for diagnosis and its distribution in Australia. Pest Manag. Sci. 69:48–53First characterization of resistance in Cryptolestesferrugineus, the strongest ever recorded for stored product pests.
    [Google Scholar]
  74. 74. 
    Nayak MK, Collins PJ, Pavic H, Kopittke RA 2003. Inhibition of egg development by phosphine in the cosmopolitan pest of stored products Liposcelisbostrychophila (Psocoptera: Liposcelididae). Pest Manag. Sci. 59:1191–96
    [Google Scholar]
  75. 75. 
    Nayak MK, Collins PJ, Throne JE, Wang JJ 2014. Biology and management of psocids infesting stored products. Annu. Rev. Entomol. 59:279–97
    [Google Scholar]
  76. 76. 
    Nayak MK, Daglish GJ, Phillips TW 2015. Managing resistance to chemical treatments in stored products pests. Stewart Postharvest Rev11(1):spr.2015.1.3
    [Google Scholar]
  77. 77. 
    Nayak MK, Falk MG, Emery RN, Collins PJ, Holloway JC 2017. An analysis of trends, frequencies and factors influencing the development of resistance to phosphine in the red flour beetle Triboliumcastaneum (Herbst) in Australia. J. Stored Prod. Res. 72:35–48
    [Google Scholar]
  78. 78. 
    Nayak MK, Jagadeesan R, Kaur R, Daglish GJ, Reid R, Pavic H et al. 2016. Use of sulfuryl fluoride in the management of strongly phosphine resistant insect pest populations in bulk grain storages in Australia. Indian J. Entomol. 78:100–8
    [Google Scholar]
  79. 79. 
    Nayak MK, Kaur R, Jagadeesan R, Pavic H, Phillips TW, Daglish GJ 2019. Development of a quick knock down test for diagnosing resistance to phosphine in rice weevil, Sitophilusoryzae, a major pest of stored products. J. Econ. Entomol. 112:1975–82
    [Google Scholar]
  80. 80. 
    Nguyen TT, Collins PJ, Duong TM, Schlipalius DI, Ebert PR 2016. Genetic conservation of phosphine resistance in the rice weevil Sitophilusoryzae (L.). J. Hered. 107:228–37
    [Google Scholar]
  81. 81. 
    Nguyen TT, Collins PJ, Ebert PR 2015. Inheritance and characterization of strong resistance to phosphine in Sitophilusoryzae (L.). PLOS ONE 10:4e0124335
    [Google Scholar]
  82. 82. 
    Nopsa JFH, Daglish GJ, Hagstrum DW, Leslie JF, Phillips TW et al. 2015. Ecological networks in stored grain: identifying key nodes for emerging pests and mycotoxins in postharvest networks. Bioscience 65:985–1002
    [Google Scholar]
  83. 83. 
    Opit GP, Phillips TW, Aikins MJ, Hasan MM 2012. Phosphine resistance in Triboliumcastaneum and Rhyzoperthadominica from stored wheat in Oklahoma. J. Econ. Entomol. 105:1107–14
    [Google Scholar]
  84. 84. 
    Opit GP, Thoms E, Phillips TW, Payton ME 2016. Effectiveness of sulfuryl fluoride fumigation for the control of phosphine-resistant grain insects infesting stored wheat. J. Econ. Entomol. 109:2930–41
    [Google Scholar]
  85. 85. 
    Perez-Mendoza J, Flinn PW, Campbell JF, Hagstrum DW, Throne JE 2004. Detection of stored-grain insect infestation in wheat transported in railroad hopper-cars. J. Econ. Entomol. 97:1474–83
    [Google Scholar]
  86. 86. 
    Pike V. 1994. Laboratory assessment of the efficacy of phosphine and methyl bromide fumigation against all life stages of Liposcelisentomophilus (Enderlein). Crop Protect. 13:141–45
    [Google Scholar]
  87. 87. 
    Pimentel MAG, Faroni LRD'A, da Silva FH, Batista MD, Guedes RNC 2010. Spread of phosphine resistance among Brazilian populations of three species of stored product insects. Neotrop. Entomol. 39:1101–7
    [Google Scholar]
  88. 88. 
    Pimentel MAG, Faroni LRD'A, Guedes RNC, Sousa AH, Tótola MR 2009. Phosphine resistance in Brazilian populations of Sitophiluszeamais Motschulsky (Coleoptera: Curculionidae). J. Stored Prod. Res. 45:71–74
    [Google Scholar]
  89. 89. 
    Pimentel MAG, Faroni LRD'A, Tótola MR, Guedes RNC 2007. Phosphine resistance, respiration rate and fitness consequences in stored-product insects. Pest Manag. Sci. 63:876–81
    [Google Scholar]
  90. 90. 
    Plumier BM, Schramm M, Maier DE 2018. Developing and verifying a fumigant loss model for bulk stored grain to predict phosphine concentrations by taking into account fumigant leakage and sorption. J. Stored Prod. Res. 77:197–204
    [Google Scholar]
  91. 91. 
    Rafter MA, McCulloch GA, Daglish GJ, Gurdasani K, Walter GH 2018. Polyandry, genetic diversity and fecundity of emigrating beetles: understanding new foci of infestation and selection. J. Pest Sci. 91:287–98
    [Google Scholar]
  92. 92. 
    Rajan TS, Muralitharan V, Daglish GJ, Mohankumar S, Rafter MA et al. 2018. Flight of three major insect pests of stored grain in the monsoonal tropics of India, by latitude, season and habitat. J. Stored Prod. Res. 76:43–50
    [Google Scholar]
  93. 93. 
    Rajendran S. 1994. Psocids in food commodities and their control. Pestology 28:14–19
    [Google Scholar]
  94. 94. 
    Rajendran S. 1999. Phosphine resistance in stored grain insect pests in India. Proceedings of the 7th International Working Conference on Stored Product Protection Z Jin, Q Liang, Y Liang, X Tan, L Guan 635–41 Wallingford, UK: CAB Int.
    [Google Scholar]
  95. 95. 
    Rajendran S. 2000. Inhibition of hatching of Triboliumcastaneum by phosphine. J. Stored Prod. Res. 36:101–6
    [Google Scholar]
  96. 96. 
    Rajendran S, Muralidharan N. 2001. Performance of phosphine in fumigation of bagged paddy rice in indoor and outdoor stores. J. Stored Prod. Res. 37:351–58
    [Google Scholar]
  97. 97. 
    Rajendran S, Nayak KR, Anjum SS 2001. The action of phosphine against the eggs of phosphine-resistant and -susceptible strains of Rhyzoperthadominica F. Pest Manag. Sci. 57:422–26
    [Google Scholar]
  98. 98. 
    Rajendran S, Parveen H, Begum K, Ramesh C 2004. Influence of phosphine on hatching of Cryptolestesferrugineus (Coleoptera: Cucujidae), Lasiodermaserricorne (Coleoptera: Anobiidae) and Oryzaephilussurinamensis (Coleoptera: Silvanidae). Pest Manag. Sci. 60:114–18
    [Google Scholar]
  99. 99. 
    Reichmuth C. 1991. A quick test to determine phosphine resistance in stored products research. GASGA Newsl 15:14–15
    [Google Scholar]
  100. 100. 
    Ren YL, O'Brien IG, Whittle GP 1994. Studies on the effect of carbon dioxide in insect treatment with phosphine. Proceedings of the 6th International Working Conference on Stored Product Protection E Highley, EJ Wright, HJ Banks, BR Champ 173–77 Wallingford, UK: CAB Int.
    [Google Scholar]
  101. 101. 
    Ridley AW, Burrill PR, Cook CC, Daglish GJ 2011. Phosphine fumigation of silo bags. J. Stored Prod. Res. 47:349–56
    [Google Scholar]
  102. 102. 
    Ridley AW, Hereward JP, Daglish GJ, Collins PJ, Raghu S, Walter GH 2011. The spatiotemporal dynamics of Triboliumcastaneum (Herbst): adult flight and gene flow. Mol. Ecol. 20:1635–46
    [Google Scholar]
  103. 103. 
    Ridley AW, Hereward JP, Daglish GJ, Raghu S, McCulloch GA, Walter GH 2016. Flight of Rhyzoperthadominica (Coleoptera: Bostrichidae): a spatio-temporal analysis with pheromone trapping and population genetics. J. Econ. Entomol. 109:2561–71
    [Google Scholar]
  104. 104. 
    Saglam O, Edde PA, Phillips TW 2015. Resistance of Lasiodermaserricorne (Coleoptera: Anobiidae) to fumigation with phosphine. J. Econ. Entomol. 108:2489–95
    [Google Scholar]
  105. 105. 
    Schlipalius DI, Chen W, Collins P, Nguyen T, Reilly P, Ebert PR 2008. Gene interactions constrain the course of evolution of phosphine resistance in the lesser grain borer, Rhyzoperthadominica. Heredity 100:506–16
    [Google Scholar]
  106. 106. 
    Schlipalius DI, Cheng Q, Reilly PEB, Collins PJ, Ebert PR 2002. Genetic linkage analysis of the lesser grain borer Rhyzoperthadominica identifies two loci that confer high-level resistance to the fumigant phosphine. Genetics 161:773–82
    [Google Scholar]
  107. 107. 
    Schlipalius DI, Tuck AG, Jagadeesan R, Nguyen T, Kaur R et al. 2018. Variant linkage analysis using de novo transcriptome sequencing identifies a conserved phosphine resistance gene in insects. Genetics 209:281–90
    [Google Scholar]
  108. 108. 
    Schlipalius DI, Tuck AG, Pavic H, Daglish GJ, Nayak MK, Ebert PR 2018. A high-throughput system used to determine frequency and distribution of phosphine resistance across large geographical regions. Pest Manag. Sci. 75:1091–98
    [Google Scholar]
  109. 109. 
    Schlipalius DI, Valmas N, Tuck AG, Jagadeesan R, Ma L et al. 2012. A core metabolic enzyme mediates resistance to phosphine gas. Science 338:807–10Pioneering research that discovered the genes responsible for development of strong resistance to phosphine.
    [Google Scholar]
  110. 110. 
    Shi M, Collins PJ, Ridsdill-Smith J, Emery RN, Renton M 2013. Dosage consistency is the key factor in avoiding evolution of resistance to phosphine and population increase in stored-grain pests. J. Stored Prod. Res. 51:23–32
    [Google Scholar]
  111. 111. 
    Sinclair ER, White GG. 1980. Stored product insect pests in combine harvesters on the Darling Downs. Qld. J. Agr. Anim. Sci. 37:93–99
    [Google Scholar]
  112. 112. 
    Sousa AH, Faroni LRD'A, Guedes RNC, Tótola MR, Urruchi WI 2008. Ozone as a management alternative against phosphine-resistant insect pests of stored products. J. Stored Prod. Res. 44:379–85
    [Google Scholar]
  113. 113. 
    Sousa AH, Faroni LRD'A, Pimentel MAG, Guedes RNC 2009. Developmental and population growth rates of phosphine-resistant and -susceptible populations of stored-product insect pests. J. Stored Prod. Res. 45:241–46
    [Google Scholar]
  114. 114. 
    Steuerwald R, Dierks-Lange H, Schmitt S 2006. Rapid bioassay for determining the phosphine tolerance. Proceedings of the 9th International Working Conference on Stored Product Protection I Lorini, B Bacaltchuk, H Beckel, D Deckers, E Sundfeld, JP dos Santos et al.306–11 Wallingford, UK: CAB Int.
    [Google Scholar]
  115. 115. 
    Tahara EB, Barros MH, Oliveira GA, Netto LE, Kowaltowski AJ 2007. Dihydrolipoyl dehydrogenase as a source of reactive oxygen species inhibited by caloric restriction and involved in Saccharomycescerevisiae aging. FASEB J 21:274–83
    [Google Scholar]
  116. 116. 
    Taylor RWD. 1989. Phosphine: a major fumigant at risk. Int. Pest Control 31:10–14
    [Google Scholar]
  117. 117. 
    Taylor RWD. 1991. Resistance to grain fumigants and future prospects for their use. Pestic. Outlook 2:22–24
    [Google Scholar]
  118. 118. 
    Thoms EM, Phillips T. 2004. Fumigation. Handbook of Pest Control S Hedges 1164–216 Mallis, OH: GIE Media. , 9th ed..
    [Google Scholar]
  119. 119. 
    Toon A, Daglish GJ, Ridley AW, Emery RN, Holloway JC, Walter GH 2018. Significant population structure in Australian Cryptolestesferrugineus and interpreting the potential spread of phosphine resistance. J. Stored Prod. Res. 77:219–24
    [Google Scholar]
  120. 120. 
    Tyler PS, Hodges RJ. 2002. Phytosanitary measures against larger grain borer Prostephanustruncatus (Horn) (Coleoptera: Bostrychidae), in international trade. Integr. Pest Manag. Rev. 7:279–89
    [Google Scholar]
  121. 121. 
    UNEP 1994. Montreal Protocol on substances that deplete ozone layer: report of the Methyl Bromide Technical Options Committee, 1995 Assessment Rep., Ozone Secr., U.N. Env. Prog. Nairobi, Kenya:
    [Google Scholar]
  122. 122. 
    Valmas N, Zuryn S, Ebert PR 2008. Mitochondrial uncouplers act synergistically with the fumigant phosphine to disrupt mitochondrial membrane potential and cause cell death. Toxicology 252:33–39
    [Google Scholar]
  123. 123. 
    Venkidusamy M, Jagadeesan R, Nayak MK, Subbarayalu M, Subramanian C, Collins PJ 2018. Relative tolerance and expression of resistance to phosphine in life stages of the rusty grain beetle, Cryptolestesferrugineus. J. Pest Sci. 91:277–86
    [Google Scholar]
  124. 124. 
    Wang D, Collins PJ, Gao X 2006. Optimising indoor phosphine fumigation of paddy rice bag-stacks under sheeting for control of resistant insects. J. Stored Prod. Res. 42:207–17
    [Google Scholar]
  125. 125. 
    Xinyi E, Subramanyam B, Li B 2017. Responses of phosphine susceptible and resistant strains of five stored-product insect species to chlorine dioxide. J. Stored Prod. Res. 72:21–27
    [Google Scholar]
  126. 126. 
    Zettler JL, Cuperus GW. 1990. Pesticide resistance in Triboliumcastaneum (Coleoptera: Tenebrionidae) and Rhyzoperthadominica (Coleoptera: Bostrichidae) in wheat. J. Econ. Entomol. 83:1677–81
    [Google Scholar]
  127. 127. 
    Zuryn S, Kuong J, Ebert PR 2008. Mitochondrial modulation of phosphine toxicity and resistance in Caenorhabditiselegans. Toxicol. Sci 102:1179–86
    [Google Scholar]
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