Exotic Aphid Control with Pathogens

  • Charlotte Nielsen
  • Stephen P. Wraight
Part of the Progress in Biological Control book series (PIBC, volume 6)

Abstract

Exotic aphids are invading ecosystems worldwide. The principal factors favoring establishment of these invasive pests are their small size, parthenogenetic reproduction, short generation time, ability for long distance dispersal by winged morphs, and their explosive population dynamics. Attention has mainly been focused on invasive aphid pests of economic importance to agriculture, horticulture, and forestry. More recently, however, concerns have also concentrated on potential impacts of aphids on biodiversity, especially with respect to endangered native plants. Fungi are the most prevalent pathogens of aphids, and consequently fungi have been studied and used for biological control of invasive aphid species. Entomopathogenic fungi with high epizootic potential have been used in classical biological control programs, fungi have been mass produced and used for augmentation biological control (both inoculative and inundative), and crop and pest management practices have been modified to preserve/promote activity of naturally occurring fungi in conservation biological control programs. In this chapter we will review the various strategies that have been developed for control of invasive aphid species.

Keywords

Europe Straw Alginate Excavation Argentina 

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References

  1. Andersen US, Córdova JPP, Nielsen UB, Olsen CS, Nielsen C, Sørensen M, Koolmann J (2008) Conservation through utilisation: a case study of the vulnerable Abies guatemalensis in Guatemala. Oryx 42: 206–213CrossRefGoogle Scholar
  2. Austarå Ø, Carter C, Eilenberg J, Halldórsson G, Harding S (1997) Natural enemies of the green spruce aphid in spruce plantations in maritime North West Europe. Búvísindi 11: 113–124Google Scholar
  3. Bałazy S (1993) Flora of Poland. Polska Akademia Nauk, Kraków, PolandGoogle Scholar
  4. Blackman RL, Eastop VF (1994) Aphids on the world’s trees: An identification and information guide. CAB International, Wallingford, UKGoogle Scholar
  5. Blackman RL, Eastop VF (2000) Aphids on the world’s crops: An identification and information guide. John Wiley & Sons, New YorkGoogle Scholar
  6. Brobyn P, Wilding N (1977) Invasive and developmental processes of Entomophothora species infecting aphids. Trans Br Mycol Soc 69:349–366Google Scholar
  7. Cameron PJ, Milner RJ (1981) Incidence of Entomophthora spp. in sympatric populations of Acyrthosiphon kondoi and Acyrthosiphon pisum. NZ J Zool 8:441–446Google Scholar
  8. Carruthers RI, Hural K (1990) Fungi as naturally occurring entomopathogens. In Baker R, Dunn P (eds) New directions in biological control. UCLA Symp Molec Cell Biol 112: 115–138Google Scholar
  9. Carruthers RI, Sawyer AJ, Hural K (1991) Use of fungal pathogens for biological control of insect pests. In: Rice BJ (ed) Sustainable agriculture research and education in the field. National Academy Press, Washington, DC, USA. pp 336–372Google Scholar
  10. Carter CI, Halldórsson G (1998) Origin and background to the green spruce aphid in Europe. In: Day KR, Halldórsson G, Harding S, Straw NA (eds) The Green Spruce Aphid in WesternEurope; ecology, status, impacts and prospects for management. Forestry Commission, Technical paper 24:1–14Google Scholar
  11. Dean GJ, Wilding N (1973) Infection of cereal aphids by the fungus Entomophthora. Ann Appl Biol 74:133–138CrossRefGoogle Scholar
  12. Dedryver CA (1979) Déclenchement en serre d’une epizootie à Entomophthora fresenii Nowak. sur Aphis fabae Scop. par introduction d’inoculum et régulation de l’humidite relative. Entomophaga 24:443–453CrossRefGoogle Scholar
  13. Dedryver CA (1983) Field pathogenesis of three species of Entomophthorales of cereal aphids in Western France. In: Cavalloro R (ed) Aphid antagonists. Commission of the European Communities, Rotterdam. pp 11–19Google Scholar
  14. Dixon AFG (1987) Parthenogenetic reproduction and rate of increase in aphids. In: Minks AK, Harrewijn P (eds) Aphids their biology, natural enemies and control, Vol. 2A. Elsevier, Amsterdam, The Netherland. pp 269–286Google Scholar
  15. Dixon AFG (1998) Aphid ecology. An optimization approach. 2nd edition. Chapman & Hall, London, UKGoogle Scholar
  16. Eilenberg J, Hajek AE, Lomer C (2001) Suggestions for unifying the terminology in biological control. BioControl 46:387–400CrossRefGoogle Scholar
  17. Faria MR de, Wraight SP (2007) Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256CrossRefGoogle Scholar
  18. Feng MG, Johnson JB, Kish LP (1990) Survey of entomopathogenic fungi naturally infecting cereal aphids (Homoptera: Aphididae) of irrigated grain crops Southwestern Idaho. Environ Entomol 19:1535–1542Google Scholar
  19. Feng MG, Johnson JB, Halbert SE (1991) Natural control of cereal aphids (Homoptera: Aphididae) by entomopathogenic fungi (Zygomycetes: Entomophthorales) and parasitoids (Hymenoptera: Braconidae and Encyrtidae) on irrigated spring wheat in Southwestern Idaho. Environ Entomol 20:1699–1710Google Scholar
  20. Feng MG, Nowierski RM, Johnson JB, Poprawski TJ (1992) Epizootics caused by entomophthoralean fungi (Zygomycetes, Entomophthorales) in populations of cereal aphids (Hom., Aphididae) in irrigated small grains in southwestern Idaho, USA. J Appl Entomol 113:376–390Google Scholar
  21. Galaini-Wraight S, Wraight SP, Carruthers RI, Magalhães BP, Roberts DW (1991) Description of a Zoophthora radicans (Zygomycetes: Entomophthoraceae) epizootic in a population of Empoasca kraemeri (Homoptera: Cicadellidae) on beans in Central Brazil. J Invertebr Pathol 58:311–326CrossRefGoogle Scholar
  22. Glare TR, Chilvers GA, Milner RJ (1985) Capilliconidia as infective spores in Zoophthora phalloides. Trans Br Mycol Soc 85:463–470CrossRefGoogle Scholar
  23. Hajek AE (1997) Ecology of terrestrial fungal entomopathogens. Adv Micr Ecol 15:193–249Google Scholar
  24. Hajek AE, St. Leger RJ (1994) Interactions between fungal pathogens and insect hosts. Ann Review Entomol 39:293–322CrossRefGoogle Scholar
  25. Hall RA (1981) The fungus Verticillium lecanii as a microbial insecticide against aphids and scales. In: Burges HD (ed) Microbial control of pests and plant diseases. Academic Press, New York. pp 483–498Google Scholar
  26. Hatting JL, Humber RA, Poprawski TJ, Miller RM (1999) A survey of fungal pathogens of aphids from South Africa, with special reference to cereal aphids. Biol Control 16:1–12CrossRefGoogle Scholar
  27. Hatting JL, Poprawski TJ, Miller RM (2000) Prevalences of fungal pathogens and other natural enemies of cereal aphids (Homoptera: Aphididae) in wheat under dryland and irrigated conditions in South Africa. BioControl 45:179–199CrossRefGoogle Scholar
  28. Hatting JL, Wraight SP, Miller RM (2004) Efficacy of Beauveria bassiana (Hyphomycetes) for control of Russian wheat aphid (Homoptera: Aphididae) on resistant wheat under field conditions. Biocon Sci Technol 14:459–473CrossRefGoogle Scholar
  29. Heie OE (1980) The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. I.General part. Fauna Entomologica Scandinavica, Vol. 9. Scandinavian Science Press, Klampenborg, DenmarkGoogle Scholar
  30. Heimpel GE, Ragsdale DW, Venette R, Hopper KR, O’Neil RJ, Rutledge CE, Wu Z (2004) Prospects for importation biological control of the soybean aphid: Anticipating potential costs and benefits. Ann Entomol Soc Am 97:249–258CrossRefGoogle Scholar
  31. Heimpel GE, Shelly TE (2004) The soybean aphid: A review of its biology and management. Ann Entomol Soc Am 97:203CrossRefGoogle Scholar
  32. Humber RA (1989) Synopsis of a revised classification for Entomophthorales (Zygomycotina). Mycotaxon 34:441–460Google Scholar
  33. Humber RA (1992) Collection of entomopathogenic fungal cultures: Catalog of strains. US Dept of Agriculture, Agricultural Research Service, ARS-110. 177ppGoogle Scholar
  34. Humber RA (1997) Fungi: Identification. In: Lacey, L (ed) Manual of techniques in insect pathology. Academic Press, San Diego, USA. pp 153–186CrossRefGoogle Scholar
  35. Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of Hyphomycetous fungi for managing insect pests. In: Butt T, Jackson C, Magan N (eds) Fungal biocontrol agents: Progress, problems and potential. Kluwer, Dordrecht, Netherlands. pp 23–69Google Scholar
  36. Keller S (2006) Entomophthorales attacking aphids with a description of two new species. Sydowia 58:38–74Google Scholar
  37. Keller S, Duelli P (1998) Aphidophaga and the case for nature protection and biotype conservation. In: Niemczuk E, Dixon AFG (eds) Ecology and effectiveness of Aphidophaga. SPB Academic Publishing, The Hargue, The Netherlands. pp 95–97Google Scholar
  38. Keller S, Suter H (1980) Epizootiologische Untersuchungen über das Entomophthora – Auftreten bei feldbaulich wichtigen Blattlausarten. Acta Æcologica 1:63–81Google Scholar
  39. Klingen I, Eilenberg J, Meadow R (2002) Effects of farming system, field margins and bait insect on the occurrence of insect pathogenic fungi in soils. Agric Ecosyst Environ 91:191–198CrossRefGoogle Scholar
  40. Knudsen GR, Schotzko DJ (1999) Spatial simulation of epizootics caused by Beauveria bassiana in Russian wheat aphid populations. Biol Control 16:318–326CrossRefGoogle Scholar
  41. Knudsen GR, Wang ZG (1998) Microbial control of the Russian wheat aphid (Homoptera: Aphididae) with the entomopathogen Beauveria bassiana. In: Quisenberry SS, Peairs FB (eds) Response model for an introduced pest – The Russian wheat aphid. Entomological Society of America, Lanham, MD. pp 209–233Google Scholar
  42. Knudsen GR, Johnson JB, Eschen DJ (1990) Alginate pellet formulation of a Beauveria bassiana (Fungi: Hyphomycetes) isolate pathogenic to cereal aphids. J Econ Entomol 83:2225–2228Google Scholar
  43. Knudsen GR, Eschen DJ, Dandurand LM, Wang ZG (1991) Methods to enhance growth and sporulation of pelletized biocontrol fungi. Appl Environ Microbiol 57:2864–2867PubMedGoogle Scholar
  44. Knudsen GR, Schotzko DJ, Krag CR (1994) Fungal entomopathogen effect on numbers and spatial patterns of the Russian wheat aphid (Homoptera: Aphididae) on preferred and nonpreferred host plants. Environ Entomol 23:1558–1567Google Scholar
  45. Latteur G, Godefroid J (1983) Trial of field treatments against cereal aphids with mycelium of Erynia neoaphidis (Entomophthorales) produced in vitro In: Cavalloro R (ed) Aphid antagonists. AA Balkema, Rotterdam, The Netherlands. pp 2–10Google Scholar
  46. Latgé JP, Papierok B (1988) Aphid pathogens. In: Minks AK, Harrewijn P (eds) Aphids their biology, natural enemies and control, Vol 2B. Elsevier, Amsterdam, Netherlands.pp 323–335Google Scholar
  47. Leite LG (1991) Estudo de alguns fatores que afetam a epizootia de Zoophthora radicans e utilização do fungo para o controle de Empoasca sp. MS thesis, Univ. São Paulo, Piracicaba, BrazilGoogle Scholar
  48. Losey JA, Waldron JK, Hoebeke ER, Macomber LE, Scott BN (2002) First record of the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in New York. Grt Lks Entomol 35:101–105Google Scholar
  49. Mattson W, Vanhanen H, Veteli T, Sivonen S, Niemela P (2007) Few immigrant phytophagous insects on woody plants in Europe: legacy of the European crucible? Biol Invasions 9:957–974CrossRefGoogle Scholar
  50. McCabe D, Soper RS (1985) Preparation of an entomopathogenic fungal insect control agent. US Patent 4,530,834Google Scholar
  51. Messing RH, Tremblay MN, Mondor EB, Foottit RG, Pike KS (2007) Invasive aphids attack native Hawaiian plants. Biol Invasions 9:601–607CrossRefGoogle Scholar
  52. Milner RJ (1985) Pathogen importantation for biological control – Risk and benefits. In: Gibbs AJ, Meischke HRC (eds) Pest and parasite as migrants. Cambridge University Press, Cambridge, UK. pp 115–121Google Scholar
  53. Milner RJ (1997) Prospects for biopesticides for aphid control. Entomophaga 42:227–239CrossRefGoogle Scholar
  54. Milner RJ, Bourne J (1983) Influence of temperature and duration of leaf wetness on infection of Acyrthosiphon kondoi with Erynia neoaphidis. Ann Appl Biol 102:19–27CrossRefGoogle Scholar
  55. Milner RJ, Lutton GG (1983) Effect of temperature on Zoophthora radicans (Brefeld) Batko: an introduced microbial control agent of the spotted alfalfa aphid, Therioaphis trifolii (Monell) f. maculata. J Aus Entomol Soc 22:167–173CrossRefGoogle Scholar
  56. Milner RJ, Mahon RJ (1985) Strain variation in Zoophthora radicans, a pathogen on a variety of insect hosts in Australia. J Aus Entomol Soc 24:195–198CrossRefGoogle Scholar
  57. Milner RJ, Soper RS (1981) Bioassay of entomophthoralean fungi against the spotted alfalfa aphid Therioaphis trifolii f. maculata. J Invertebr Pathol 37:168–173CrossRefGoogle Scholar
  58. Milner RJ, Teakle RE, Lutton GG, Dare FM (1980) Pathogens (Phycomycetes, Entomophthoraceae) of the blue green aphid Acyrthosiphon kondoi Shinji and other aphids in Australia. Austral J Bot 28:601–619CrossRefGoogle Scholar
  59. Milner RJ, Soper RS, Lutton GG (1982) Field release of an Israeli strain of the fungus Zoophthora radicans (Brefeld) Batko for biological control of Therioaphis trifoli (Monell) f. maculata Spotted alfalfa aphid, pest of leguminous pastures. J Austral Entomol Soc 21:113–118CrossRefGoogle Scholar
  60. Milner RJ, Mahon RJ, Brown WV (1983) A taxonomic study of the Erynia neoaphidis Remaudière and Hennebert (Zygomycetes: Entomophthoraceae) group of insect pathogenic fungi, together with a description of the new species Erynia kondoiensis. Austral J Bot 31:173–188CrossRefGoogle Scholar
  61. Minks AK, Harrewijn P (1988) Aphid pathogens. In: Minks AK, Harrewijn P (eds) Aphids their biology, natural enemies and control, Vol. 2B. Elsevier, Amsterdam, Netherlands. pp V–VIIGoogle Scholar
  62. Missonnier J, Robert Y, Thoizon G (1970) Circonstances épidémiologiques semblant favoriser le développement des mycoses à Entomophthorales chez trios aphides, Aphis fabae Scop. Capitophorus horni Börner et Myzus persicae (Sulz.). Entomophaga 15:169–190CrossRefGoogle Scholar
  63. Nielsen C (2002) Interactions between aphids and entomophthoralean fungi: Characterisation, epizootiology and potential for microbial control. Ph.D. thesis. The Royal Veterinary and Agricultural University, DenmarkGoogle Scholar
  64. Nielsen C, Hajek AE (2005) Control of invasive soybean aphid, Aphis glycines (Hemiptera: Aphididae), populations by existing natural enemies in New York State, with emphasis on entomopathogenic fungi. Environ Entomol 34:1036–1047CrossRefGoogle Scholar
  65. Nielsen C, Eilenberg J, Harding S, Oddsdottir E, Halldórsson G (2000) Entomophthoralean fungi infecting the green spruce aphid (Elatobium abietinum) in the north-western part of Europe. IOBC/WPRS Bull 23:131–134Google Scholar
  66. Nielsen C, Eilenberg J, Harding S, Oddsdottir E, Halldórsson G (2001) Geographical distribution and host range of Entomophthorales infecting the green spruce aphid Elatobium abietinum Walker in Iceland. J Invertebr Pathol 78:72–80PubMedCrossRefGoogle Scholar
  67. Nielsen C, Hajek AE, Humber RA, Bresciani J, Eilenberg J (2003) Soil as an environment for winter survival of aphid-pathogenic Entomophthorales. Biol Control 28:92–100CrossRefGoogle Scholar
  68. Nielsen C, Jensen AB, Eilenberg J (2008) Survival of entomophthoralean fungi infecting aphids and higher flies during unfavorable conditions and implications for conservation biological control. In: Ekesi S, Maniania NK (eds) Use of entomopathogenic fungi in biological pest management. Research SignPost, Kerala, India. pp 13–38Google Scholar
  69. Pell JK, Pluke R, Clark SJ, Kenward M, Alderson PG (1997) Interactions between two aphid natural enemies, the entomopathogenic fungus Erynia neoaphidis Remaudière & Hennebert (Zygomycetes: Entomophthorales) and the predatory beetle Coccinella septempunctata L. (Coleoptera: Coccinellidae). J Invertebr Pathol 69:261–268CrossRefGoogle Scholar
  70. Pell J, Steinkraus D, Eilenberg J, Hajek A (2001) Exploring the potential of Entomophthorales in integrated crop management. In: Butt T, Jackson C, Magan N (eds) Fungal biocontrol agents: Progress, problems and potential. Kluwer, Dordrecht, Netherlands. pp 71–167Google Scholar
  71. Poprawski TJ, Wraight SP (1998) Fungal pathogens of Russian wheat aphid (Homoptera: Aphididae). In: Quisenberry SS, Peairs FB (eds) Response model for an introduced pest – The Russian wheat aphid. Entomological Society of America, Lanham, MD. pp 209–233Google Scholar
  72. Ragsdale DW, Voegtlin DJ, O’Neil R J (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208CrossRefGoogle Scholar
  73. Roberts DW, St. Leger RJ (2004) Metarhizium spp., cosmopolitan insect pathogenic fungi: Mycological aspects. Adv Appl Microbiol 54:1–70PubMedCrossRefGoogle Scholar
  74. Roy HE, Pell JK, Clark SJ, Alderson PG (1998) Implications of predator foraging on aphid pathogen dynamics. J Ivertebr Pathol 71:236–247CrossRefGoogle Scholar
  75. Rutledge CE, O’Neil RJ, Fox TB, Landis DA (2004) Soybean aphid predators and their use in integrated pest management. Ann Entomol Soc Am 97:240–248CrossRefGoogle Scholar
  76. Scorsetti AC, Humber RA, Garcia JJ, Lastra CCL (2007) Natural occurrence of entomopathogenic fungi (Zygomycetes: Entomophthorales) of aphid (Hemiptera: Aphididae) pests of horticultural crops in Argentina. BioControl 52:641–655CrossRefGoogle Scholar
  77. Shah PA, Pell JP (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413–423PubMedGoogle Scholar
  78. Shah PA, Aebi M, Tuor U (2000) Infection of Macrosiphum euphorbiae with mycelial preparations of Erynia neoaphidis in a greenhouse trial. Mycol Res 104:645–652CrossRefGoogle Scholar
  79. Sigurdsson V, Halldorsson G, Sigurgeirsson A, Thorsson AT, Anamthawat-Jonsson K (1999) Genetic differentiation of the green spruce aphid (Elatobium abietinum Walker), a recent invader to Iceland. Agri Forest Entomol 1:157–163CrossRefGoogle Scholar
  80. Silvie P, Dedryver CA, Tanguy S (1990) Application expérimentale de mycélium d’Erynia neoaphidis (Zygomycètes: Entomophthorales) dans des populations de pucerons sur laitues en serre mairaîchère: étude du suivi de l’inoculum par charactérisation enzymatiques. Entomophaga 35:375–384CrossRefGoogle Scholar
  81. Sopp PI, Sunderland KD, Coombes DS (1987) Observations on the number of cereal aphids on the soil in relation to aphid density in winter wheat. J Appl Biol 111:53–57CrossRefGoogle Scholar
  82. Steinkraus DC, Hollingsworth RG, Slaymaker PH (1995) Prevalence of Neozygites fresenii (Entomophthorales: Neozygitaceae) on cotton aphids (Homoptera: Aphididae) in Arkansas cotton. Environ Entomol. 24:465–474Google Scholar
  83. Steinkraus DC, Boys GO, Hollingsworth RG, Bacheler JS, Durant JA, Freeman BL, Gaylor MJ, Harris FA, Knutson A, Lentz GL (1996) Multi-state sampling for Neozygites fresenii in cotton. Proc Beltwide Cotton Conf 1996, Memphis, Tenn. pp 888–889Google Scholar
  84. Steinkraus DC, Boys GO, Bagwell RD, Johnson DR, Lorenz GM, Meyers H, Layton MB, O’Leary PF (1998) Expansion of extension-based aphid fungus sampling service to Louisiana and Mississippi. Proc Beltwide Cotton Conf 1998. San Diego, California pp 1239–1242Google Scholar
  85. Steinkraus DC, Boys GO, Rosenheim JA (2002) Classical biological control of Aphis gossypii (Homoptera: Aphididae) with Neozygites fresenii (Entomophthorales: Neozygitaceae) in California cotton. Biol Control 25:297–304CrossRefGoogle Scholar
  86. Tanada Y, Kaya HK (1993) Insect pathology. Academic Press, LondonGoogle Scholar
  87. Teulon DAJ, Stufkens MAW (2002) Biosecurity and aphids in New Zealand. NZ Plant Prot55:12–17Google Scholar
  88. Vandenberg JD, Sandvol LE, Jaronski ST, Jackson MA, Souza EJ, Halbert SE (2001) Efficacy of fungi for control of Russian wheat aphid (Homoptera: Aphididae) in irrigated wheat. Southwestern Entomol 26:73–85Google Scholar
  89. Wilding N (1981a) Pest control by Entomophthorales. In: Burges HD (ed) Microbial control of pest and plant diseases 1970–1980. Academic Press, London. pp 539–554Google Scholar
  90. Wilding, N. (1981b) The effect of introducing aphid pathogenic Entomophthoraceae into field populations of Aphis fabae. Ann Appl Biol 99:11–23CrossRefGoogle Scholar
  91. Wilding N, Mardell SK, Brobyn PJ, Wratten SD, Lomas J (1986) The effect of introducing the aphid-pathogenic fungus Erynia neoaphidis into populations of cereal aphids. Ann Appl Biol 117:683–691CrossRefGoogle Scholar
  92. Wraight SP, Poprawski TJ, Meyer WL, Peairs FB (1993) Natural enemies of Russian wheat aphid (Homoptera, Aphididae) and associated cereal aphid species in spring-planted wheat and barley in Colorado. Environ Entomol 22:1383–1391Google Scholar
  93. Wraight SP, Galaini-Wraight S, Carruthers RI, Roberts DW (2003) Zoophthora radicans (Zygomycetes: Entomophthorales) conidia production from naturally-infected Empoasca kraemeri and dry-formulated mycelium under laboratory and field conditions. Biol Control 28:60–77CrossRefGoogle Scholar
  94. Wu ZS, Schenk-Hamlin D, Zhan WY, Ragsdale DW, Heimpel GE (2004) The soybean aphid in China: A historical review. Ann Entomol Soc Am 97:209–218CrossRefGoogle Scholar
  95. Zimmermann G (1978) Biological control of aphids by entomopathogenic fungi: Present state and prospects. In: Cavalloro R (ed) Aphid antagonists. Balkema, Rotterdam. pp 33–40Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Charlotte Nielsen
    • 1
    • 2
  • Stephen P. Wraight
  1. 1.Department of Entomology Comstock HallCornell UniversityIthacaUSA
  2. 2.Department of EcologyUniversity of Copenhagen Faculty of Life SciencesDenmark

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