The occurrence of entomopathogenic fungi in apple orchards and their biocontrol potential against Eriosoma lanigerum
DOI:
https://doi.org/10.17159/2254-8854/20232/a13728Keywords:
Biological control, pathogenicity, woolly apple aphid, Metarhizium, BeauveriaAbstract
Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae), woolly apple aphid (WAA) is an important pest on apples globally and a key pest of apple production in South Africa. The aphid has developed some level of resistance against several chemical insecticides. Entomopathogenic fungi (EPF) have been identified as promising biological control agents against a wide array of insect pests. The main aim of this study was to conduct a survey in local apple orchards in the Western Cape province for EPF and to use isolates to test the susceptibility of WAA under optimum laboratory conditions. Soil samples were collected from apple orchards and EPF, baited and isolated using larvae of Galleria mellonella and Tenebrio molitor. Six EPF species: Beauveria bassiana, Cordyceps fumosorosea, Metarhizium brunneum, M. pinghaense, M. robertsii and Purpureocillium lilacinum were identified from the soil samples. The results from bioassays showed that Metarhizium robertsii and M. pinghaense isolates were the most effective with an average percentage mortality of > 90%. Metarhizium brunneum also proved to be effective when used against the insect with an average percentage mortality of > 80%, while B. bassiana and C. fumosorosea were the least effective with average percentage mortality of 52% and 48%, respectively. The LT50 and LT90 of M. robertsii (2.12; 4.19) and M. pinghaense (2.05; 4.45) showed to require similar mortality time in days of E. lanigerum. The results obtained in the study have provided an insight into the diversity of EPF species across apple orchards of the Western Cape and shown the efficacy of the Metarhizium isolates as potential biological control agents of the WAA.
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Abaajeh AR, Nchu F. 2015. Isolation and pathogenicity of some South African entomopathogenic fungi (Ascomycota) against eggs and larvae of Cydia pomonella (Lepidoptera: Tortricidae). Biocontrol Science and Technology 25(7): 828–842. https://doi.org/10.1080/09583157.2015.1019831
Abu-Romman S, Ateyyat M. 2014. Phenotypic and molecular screening of apple genotypes to woolly apple aphid resistance. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 42(1): 99–103. https://doi.org/10.15835/nbha4219460
Asensio L, Carbonell T, López-Jiménez JA, Lopez-Llorca LV. 2003. Entomopathogenic fungi in soils from Alicante province [Spain]. Spanish Journal of Agricultural Research 1(3): 37–45. https://doi.org/10.5424/sjar/2003013-33
Beers EH, Suckling DM, Prokopy RJ, Avilla J. 2003. Ecology and management of apple arthropod pests. In: Ferree D, editor. Apples: Botany, Production and Uses. Wallingford, UK: CABI. p. 489–519. https://doi.org/10.1079/9780851995922.0489
Bhatia V, Uniyal PL, Bhattacharya R. 2011. Aphid resistance in Brassica crops: challenges, biotechnological progress and emerging possibilities. Biotechnology Advances 29(6):879–888. https://doi.org/10.1016/j.biotechadv.2011.07.005
Blackman RL, Eastop VF. 2000. Aphids on the world’s crops: An identification and information guide. New York, USA:Wiley.
Brown MW, Schmitt JJ. 1990. Growth reduction in non-bearing apple trees by woolly apple aphids (Homoptera: Aphididae) on roots. Journal of Economic Entomology 83(4): 1526–1530. https://doi.org/10.1093/jee/83.4.1526
Brown MW, Schmitt JJ, Ranger S, Hogmire HW. 1995. Yield reduction in apple by edaphic woolly apple aphid (Homoptera: Aphididae) populations. Journal of Economic Entomology 88(1): 127–133. https://doi.org/10.1093/jee/88.1.127
Castillo Lopez D, Zhu-Salzman K, Ek-Ramos MJ, Sword GA. 2014. The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS One 9(8): e103891. https://doi.org/10.1371/journal.pone.0103891
Chandler D, Hay D, Reid AP. 1997. Sampling and occurrence of entomopathogenic fungi and nematodes in UK soils. Applied Soil Ecology 5(2): 133–141. https://doi.org/10.1016/S0929-1393(96)00144-8
Chase AR, Osborne LS, Ferguson VM. 1986. Selective isolation of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae from an artificial potting medium. Florida Entomology 69(2): 285–292. https://doi.org/10.2307/3494930
Christians GE. 2003. Identification of molecular markers linked to woolly apple aphid (Eriosoma lanigerum) (Hausmann) resistance in apple. Ph.D. dissertation, Stellenbosch University, Stellenbosch, South Africa.
Cross JV, Solomon MG, Babandreier D, Blommers L, Easterbrook MA, Jay CN, Jenser G, Jolly RL, Kuhlmann U, Lilley R, et al. 1999b. Biocontrol of pests of apples and pears in northern and central Europe: parasitoids. Biocontrol Science and Technology 9(3): 277–314. https://doi.org/10.1080/09583159929569
Cross JV, Solomon MG, Chandler D, Jarrett P, Richardson PN, Winstanley D, Bathon H, Huber J, Keller B, Langenbruch GA, et al. 1999a. Biocontrol of pests of apples and pears in northern and central Europe: 1. Microbial agents and nematodes. Biocontrol Science and Technology 9(2): 125–149. https://doi.org/10.1080/09583159929721
Damavandian MR, Pringle KL. 2002. Development of a system for sampling population levels of subterranean Eriosoma lanigerum (Homoptera: Aphididae) in apple orchards. African Entomology 10(2): 341–344.
Damavandian MR, Pringle KL. 2007. The field biology of subterranean populations of the woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae), in South African apple orchards. African Entomology 15(2): 287–294. https://doi.org/10.4001/1021-3589-15.2.287
Damavandian MR. 2000. Biology of subterranean populations of woolly apple aphid, Eriosoma lanigerum (Hausmann) (Homoptera: Aphididae), in apple orchards. Ph.D dissertation, Stellenbosch University, Stellenbosch, South Africa.
De Faria MR, Wraight SP. 2007. Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biological Control 43(3): 237–256. https://doi.org/10.1016/j.biocontrol.2007.08.001
Dedryver CA, Le Ralec A, Fabre F. 2010. The conflicting relationships between aphids and men: a review of aphid damage and control strategies. Comptes Rendus Biologies 333(6–7): 539–553. https://doi.org/10.1016/j.crvi.2010.03.009
Ekesi S, Maniania N, Lux S. 2002. Mortality in three tephritid fruit fly puparia and adults caused by the entomopathogenic fungi, Metarhizium anisopliae and Beauveria bassiana. Biocontrol Science and Technology 12(1): 7–17. https://doi.org/10.1080/09583150120093077
Erler F, Pradier T, Aciloglu B. 2014. Field evaluation of an entomopathogenic fungus, Metarhizium brunneum strain F52, against pear psylla, Cacopsylla pyri. Pest Management Science 70(3): 496–501. https://doi.org/10.1002/ps.3603
Gillespie AT, Moorhouse ER. 1989. The use of fungi to control pests of agricultural and horticultural importance. In: Whipps JM, Lumsden RD, editors. Biotechnology of Fungi for Improving Plant Growth. Cambridge, UK: University of Cambridge; p. 55–84.
Goble TA, Dames JF, Hill MP, Moore SD. 2010. The effects of farming system, habitat type and bait type on the isolation of entomopathogenic fungi from citrus soils in the Eastern Cape Province, South Africa. BioControl 55(3): 399–412. https://doi.org/10.1007/s10526-009-9259-0
Gontijo LM. 2011. Integrated biological control of woolly apple aphid in Washington State. Ph.D. dissertation. Washington State University, Pullman, WA, USA.
Gresham SDM. 2013. Ecological and logistical considerations toward introducing Heringia calcarata to New Zealand. Ph.D. dissertation. Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.
Harris, S.A., Robinson, J.P. & Juniper, B.E. 2002. Genetic clues to the origin of the apple. Trends in Genetics 18(8): 426–430. https://doi.org/10.1016/S0168-9525(02)02689-6.
Hatting JL, Moore SD, Malan AP. 2019. Microbial control of phytophagous invertebrate pests in South Africa: current status and future prospects. Journal of Invertebrate Pathology 165: 54–66. https://doi.org/10.1016/j.jip.2018.02.004.
Heunis JM, Pringle KL. 2003. The susceptibility of Aphelinus mali (Haldeman), a parasitoid of Eriosoma lanigerum (Hausmann), to pesticides used in apple orchards in the Elgin area, Western Cape province, South Africa. African Entomology 11(1): 91–95.
Heunis JM, Pringle KL. 2006. Field biology of woolly apple aphid, Eriosoma lanigerum (Hausmann), and its natural enemy, Aphelinus mali (Haldeman), in apple orchards in the Western Cape province. African Entomology 14(1): 77–86.
Inglis GD, Enkerli J, Goettel MS. 2012. Laboratory techniques used for entomopathogenic fungi: Hypocreales. In: Lacey LA, editor. Manual of Techniques in Invertebrate Pathology. 2nd ed. Cambridge, MA, USA: Academic Press. p. 189–253. https://doi.org/10.1016/B978-0-12-386899-2.00007-5
Inglis GD, Goettel MS, Butt TM, Strasser H. 2001. Use of hyphomycetous fungi for managing insect pests. In: Butt TM, Jackson C, Magan N, editors. Fungi as Biocontrol Agents: Progress, Problems and Potential. Wallingford, UK: CAB International. p. 23–69. https://doi.org/10.1079/9780851993560.0023
Kirubakaran SA, Abdel-Megeed A, Senthil-Nathan S. 2018. Virulence of selected indigenous Metarhizium pingshaense (Ascomycota: Hypocreales) isolates against the rice leaffolder, Cnaphalocrocis medinalis (Guenèe) (Lepidoptera: Pyralidae). Physiological and Molecular Plant Pathology 101: 105–115. https://doi.org/10.1016/j.pmpp.2017.06.004
Krassilstschik J. 1888. Industrial production of entomopathogens for the destruction of harmful insects. Bulletin Scientifique de la France et de la Belgique 19: 461–472.
Lacey LA, Solter LF. 2012. Initial handling and diagnosis of diseased invertebrates. In: Manual of Techniques in Invertebrate Pathology. 2nd ed. p. 1–14. Cambridge, MA, USA: Academic Press. https://doi.org/10.1016/B978-0-12-386899-2.00001-4
Lordan J, Alegre S, Gatius F, Sarasúa MJ, Alins G. 2015. Woolly apple aphid Eriosoma lanigerum Hausmann ecology and its relationship with climatic variables and natural enemies in Mediterranean areas. Bulletin of Entomological Research 105(01): 60–69. https://doi.org/10.1017/S0007485314000753.
Mathulwe LL, Malan AP, Stokwe NF. 2022. Laboratory screening of entomopathogenic fungi and nematodes for pathogenicity against the obscure mealybug, Pseudococcus viburni (Hemiptera: Pseudococcidae). Biocontrol Science and Technology 32: 397–417. https://doi.org/10.1080/09583157.2021.2010653
Meyling NV, Eilenberg J. 2007. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biological Control 43(2): 145–155. https://doi.org/10.1016/j.biocontrol.2007.07.007
Meyling NV. 2007. Methods for Isolation of Entomopathogenic Fungi from the Soil Environment – Laboratory Manual. Denmark: University of Copenhagen.
Mols PJM, Boers JM. 2001. Comparison of a Canadian and a Dutch strain of the parasitoid Aphelinus mali (Hald) (Hym. Aphelinidae) for control of woolly apple aphid Erisoma lanigerum (Haussmann) (Hom. Aphididae) in the Netherlands: a simulation approach. Journal of Applied Entomology 125(5): 255–262. https://doi.org/10.1046/j.1439-0418.2001.00543.x.
Moss R, Jackson RR, Pollard SD. 2006. Mask of wax: secretions of wax conceal aphids from detection by spider’s eyes. New Zealand Journal of Zoology. 33(3): 215–220. https://doi.org/10.1080/03014223.2006.9518448.
Nicholas AH. 2000. The pest status and management of woolly aphid in an Australian apple orchard IPM program. Ph.D. dissertation, University of Western Sydney, Sydney, Australia.
Nicholas AH, Spooner-Hart RN, Vickers RA. 2005. Abundance and natural control of the woolly aphid Eriosoma lanigerum in an Australian apple orchard IPM program. BioControl 50(2): 271–291. https://doi.org/10.1007/s10526-004-0334-2
Pringle KL. 1998. The use of imidacloprid as a soil treatment for the control of Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae).Journal of the Southern African Society for Horticultural Sciences 8: 55–56.
Pringle KL, Giliomee JH, Addison MF. 1994. Vamidothion tolerance in a strain of the woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae). African Entomology 2(2): 123–125.
Pu XY, Feng MG, Shi CH. 2005. Impact of three application methods on the field efficacy of a Beauveria bassiana based mycoinsecticide against the false-eye leafhopper, Empoasca vitis (Homoptera: Cicadellidae) in the tea canopy. Crop Protection 24(2): 167–175. https://doi.org/10.1016/j.cropro.2004.07.006.
Quesada-Moraga E, Navas-Cortés JA, Maranhao EA, Ortiz-Urquiza A, Santiago-Álvarez C. 2007. Factors affecting the occurrence and distribution of entomopathogenic fungi in natural and cultivated soils. Mycological Research 111(8): 947–966. https://doi.org/10.1016/j.mycres.2007.06.006
Rehner SA, Kepler RM. 2017. Species limits, phylogeography and reproductive mode in the Metarhizium anisopliae complex. Journal of Invertebrate Pathology 148: 60–66. https://doi.org/10.1016/j.jip.2017.05.008
Shahid AA, Rao QA, Bakhsh A, Husnain T. 2012. Entomopathogenic fungi as biological controllers: new insights into their virulence and pathogenicity. Archives of Biological Sciences 64(1)21–42. https://doi.org/10.2298/ABS1201021S
Shi WB, Feng MG. 2004. Lethal effect of Beauveria bassiana, Metarhizium anisopliae, and Paecilomyces fumosoroseus on the eggs of Tetranychus cinnabarinus (Acari: Tetranychidae) with a description of a mite egg bioassay system. Biological Control 30(2):165–173. https://doi.org/10.1016/j.biocontrol.2004.01.017
Short BD. 2003. Inaugural studies of the life history and predator/prey associations of Heringia calcarata (Loew) (Diptera: Syrphidae), a specialist predator of the woolly apple aphid, Eriosoma lanigerum (Hausmann) (Homoptera: Eriosomatidae). Ph.D. dissertation, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.
Smith RG. 1999. Wax glands, wax production and the functional significance of wax use in three aphid species (Homoptera: aphididae). Journal of Natural History 33(4): 513–530. https://doi.org/10.1080/002229399300227
Stoeckli S, Mody K, Gessler C, Patocchi A, Jermini M, Dorn S. 2008. QTL analysis for aphid resistance and growth traits in apple. Tree Genetics & Genomes 4(4): 833–847. https://doi.org/10.1007/s11295-008-0156-y
Stokwe NF. 2016. Efficacy of entomopathogenic nematodes and fungi as biological control agents of woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae) under South African conditions. PhD dissertation, Stellenbosch University, Stellenbosch, South Africa.
Stokwe NF, Malan AP. 2016. Woolly apple aphid, Eriosoma lanigerum (Hausmann), in South Africa: biology and management practices, with focus on the potential use of entomopathogenic nematodes and fungi. African Entomology 24(2): 267–278. https://doi.org/10.4001/003.024.0267
Stokwe NF, Malan AP. 2017. Laboratory bioassays to determine susceptibility of woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae), to entomopathogenic nematodes. African Entomology 25(1): 123–136. https://doi.org/10.4001/003.025.0123
Thwaite WG, Bower CC. 1983. Woolly Aphid. Agfact H4. AE. 3. NSW Agriculture, Orange, Australia.
Tibco Software Inc. 2018. Statistica, version 13.3. https://statistica.io
Timm AAE. 2003. Genetic diversity of root-infesting woolly apple aphid Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae) populations in the Western Cape. Ph.D. dissertation, Stellenbosch University, Stellenbosch, South Africa.
Van Zyl C, Malan AP. 2015. Cost-effective culturing of Galleria mellonella and Tenebrio molitor and entomopathogenic nematode production in various hosts. African Entomology 23(2): 361–375. https://doi.org/10.4001/003.023.0232
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, et al. 2009. Fungal entomopathogens: new insights on their ecology. Fungal Ecology 2(4): 149–159. https://doi.org/10.1016/j.funeco.2009.05.001
Wraight SP, Carruthers R, Bradley CA, Jaronski ST, Lacey LA, Wood P, Galaini-Wraight S. 1998. Pathogenicity of the entomopathogenic fungi Paecilomyces spp. and Beauveria bassiana against the silverleaf whitefly, Bemisia argentifolii. Journal of Invertebrate Pathology 71(3): 217–226. https://doi.org/10.1006/jipa.1997.4734
Zimmermann G. 1986. The Galleria bait method for detection of entomopathogenic fungi in soil. Journal of Applied Entomology 102(1–5): 213–215. https://doi.org/10.1111/j.1439-0418.1986.tb00912.x
Zimmermann G. 2007. Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Science and Technology 17(6): 553–596. https://doi.org/10.1080/09583150701309006
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