Infection of insects and persistence of Metarhizium (Hypocreales: Clavicipitaceae) species on apple bark
DOI:
https://doi.org/10.17159/2254-8854/2023/a13944Keywords:
Codling moth, woolly apple aphid, biological control, Metarhizium brunneum, Metarhizium pinghaense, conidiaAbstract
Entomopathogenic fungi (EPF) are cosmopolitan soil borne pathogens that cause epizootics in various insect
orders. EPF isolates of Metarhizium brunneum and M. pinghaense have shown the potential for use as biological
agents of important agricultural insect pests. The aim of the current study was to test for the persistence of
M. brunneum and M. pinghaense on apple bark over a period of three weeks, under laboratory conditions. Apple
bark was sprayed with conidial suspensions of both fungi, at a standard infective conidial concentration of
107 conidia/ml. The persistence, or survival, of the conidia on apple bark was measured using codling moth
larvae (CM) (Cydia pomonella) and females of woolly apple aphid (WAA) (Eriosoma lanigerum) as indicator
species. The results showed that conidia of M. pinghaense can induce mortality of insect pests through contact
with an EPF-treated substrate, with mortality of 39% to 82% for WAA over a period of 10 days post application,
and with mortality of 3% to 68% for CM over a period of 7 days, after application to apple bark. Further
evaluation showed that the conidia of M. pinghaense persisted longer on apple bark, up to 63%, than did
M. brunneum, up to 11%, three weeks post application of the conidial suspensions. The study provides insights
into the potential persistence of fungal isolates on apple bark over time post application. Further evaluation of
the persistence of the isolates on apple bark under both glasshouse and field conditions should be conducted.
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References
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
Bidochka MJ, Kasperski JE, Wild GA. 1998. Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Canadian Journal of Botany 76(7): 1198–1204. https://doi.org/10.1139/b98-115
Blomefield T. 1994. Codling moth resistance: is it here, and how do we manage it? Deciduous Fruit Grower 44(4): 130–132.
Charnley AK, St Leger R. 1991. The role of cuticle-degrading enzymes in fungal pathogenesis in insects. In: Cole GT, Hoch HC, editors. The Fungal Spore and Disease Initiation in Plants and Animals. New York: Springer US; p. 267–286.
Chase AR, Osborne LS, Ferguson VM. 1986. Selective isolation of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae from an artificial potting medium. Florida Entomologist 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. PhD dissertation, Stellenbosch University, Stellenbosch.
Coombes CA. 2012. Entomopathogenic fungi for control of soil-borne life stages of false codling moth, Thaumatotibia leucotreta (Meyrick) (1912) (Lepidoptera: Tortricidae). MSc dissertation, Rhodes University, Grahamstown.
Coombes CA, Hill MP, Moore SD, Dames JF, Fullard T. 2013. Persistence and virulence of promising entomopathogenic fungal isolates for use in citrus orchards in South Africa. Biocontrol Science and Technology 23(9): 1053–1066. https://doi.org/10.1080/09583157.2013.819489
Cossentine JE, Judd GJR, Bissett JD, Lacey LA. 2010. Susceptibility of apple clearwing moth larvae, Synanthedon myopaeformis (Lepidoptera: Sesiidae) to Beauveria bassiana and Metarhizium brunneum. Biocontrol Science and Technology 20(7): 703–707. https://doi.org/10.1080/09583151003690390
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
Dardeau F, Deprost E, Laurans F, Lainé V, Lieutier F, Sallé A. 2014. Resistant poplar genotypes inhibit pseudogall formation by the woolly poplar aphid, Phloeomyzus passerinii Sign. Trees. 28(4): 1007–1019. https://doi.org/10.1007/s00468-014-1014-1
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.2007.08001
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): 539–553. https://doi.org/10.1016/j.crvi.2010.03.009
Ekesi S, Maniania NK, Lux SA. 2002. Mortality in three African 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
Gilbert LI, Gill SS. 2010. Insect control: biological and synthetic agents. London: Academic Press.
Goble TA. 2009. Investigation of entomopathogenic fungi for control of false codling moth, Thaumatotibia leucotreta, Mediterranean fruit fly, Ceratitis capitata and Natal fruit fly, C. rosa in South African citrus. PhD dissertation, Rhodes University, Grahamstown.
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. 2001. The biology and management of aerial populations of woolly apple aphid, Eriosoma lanigerum (Hausmann) (Homoptera: Aphididae). PhD dissertation, Stellenbosch University, Stellenbosch.
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 Edition. Academic Press. London: Academic Press; p. 189–253.
Inglis GD, Goettel MS, Johnson DL. 1993. Persistence of the entomopathogenic fungus, Beauveria bassiana, on phylloplanes of crested wheatgrass and alfalfa. Biological Control. 3(4): 258–270. https://doi.org/10.1006/bcon.1993.1035
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: CAB International; p. 23–69.
Inyang EN, McCartney HA, Oyejola B, Ibrahim L, Archer SA. 2000. Effect of formulation, application and rain on the persistence of the entomogenous fungus Metarhizium anisopliae on oilseed rape. Mycological Research. 104(6): 653–661.
Jaques RP. 1983. The potential of pathogens for pest control. Agriculture, Ecosystems & Environment. 10(2): 101–126.
Kirubakaran SA, Abdel-Megeed A, Senthil-Nathan S. 2018. Virulence of selected indigenous Metarhizium pingshaense (Ascomycota: Hypocreales) isolates against the rice leaf folder, Cnaphalocrocis medinalis (Guenèe) (Lepidoptera: Pyralidae). Physiological and Molecular Plant Pathology. 101: 105–115. https://doi.org/10.1016/j.pmpp.2017.06.004
Mathulwe LL, Malan AP, Stokwe NF. 2021. Laboratory screening of entomopathogenic fungi and nematodes for pathogenicity against the obscure mealybug, Pseudococcus viburni (Hemiptera: Pseudococcidae). Biocontrol Science and Technology. 32(4): 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: 145–155. https://doi.org/10.1016/j.biocontrol.2007.07.007
Odendaal D, Addison MF, Malan AP. 2015. Control of codling moth (Cydia pomonella) (Lepidoptera: Tortricidae) in South Africa with special emphasis on using entomopathogenic nematodes. African Entomology. 23(2): 259–274.
Odendaal D, Addison MF, Malan AP. 2016. Control of diapausing codling moth, Cydia pomonella (Lepidoptera: Tortricidae) in wooden fruit bins, using entomopathogenic nematodes (Heterorhabditidae and Steinernematidae). Biocontrol Science and Technology. 26(11): 1504–1515. https://doi.org/10.1080/09583157.2016.1217393
Pajač I, Pejič I, Barić B. 2011. Codling moth, Cydia pomonella (Lepidoptera: Tortricidae) –major pest in apple production: an overview of its biology, resistance, genetic structure and control strategies. Agriculturae Conspectus Scientificus. 76(2): 87–92.
Pringle KL, Eyles DK, Brown L. 2003. Trends in codling moth activity in apple orchards under mating disruption using pheromones in the Elgin area, Western Cape Province, South Africa. African Entomology. 11(1): 65–75.
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
Riedl H, Blomefield TL, Giliomee JH. 1998. A century of codling moth control in South Africa: II. Current and future status of codling moth management. Journal of the Southern African Society for Horticultural Sciences. 8: 32–54.
Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK. 2006. Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology. 51: 331–357. https://doi.org/10.1146/annurev.ento.51.110104.150941
Sandanayaka WRM, Hale CN. 2003. Electronically monitored stylet penetration pathway of woolly apple aphid, Eriosoma lanigerum (Homoptera: Aphididae), on apple (Malus domestica). New Zealand Journal of Crop and Horticultural Science. 31(2): 107–113.
Sandanayaka WRM, Bus VGM, Connolly P, Newcomb R. 2003. Characteristics associated with woolly apple aphid Eriosoma lanigerum, resistance of three apple rootstocks. Entomologia Experimentalis et Applicata. 109(1): 63–72.
Shah PA, Pell JK. 2003. Entomopathogenic fungi as biological control agents. Applied Microbiology and Biotechnology. 61(5): 413–423. https://doi.org/10.1007/s00253-03-1240-8
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
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). PhD dissertation, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.
St Leger RJ, Frank DC, Roberts DW, Staples RC. 1992. Molecular cloning and regulatory analysis of the cuticle‐degrading‐protease structural gene from the entomopathogenic fungus Metarhizium anisopliae. European Journal of Biochemistry. 204(3): 991–1001. https://doi.org/10.1111/j.1432-1033.1992.tb16721.x
St Leger RJ, Joshi L, Bidochka MJ, Roberts DW. 1996. Construction of an improved mycoinsecticide overexpressing a toxic protease. Proceedings of the National Academy of Sciences. 93(13): 6349–6354. https://doi.org/10.1073/pnas.93.13.6349
TIBCO Software Inc. 2018. STATISTICA (data analysis software system), version 13.5.0.17. TIBCO Software Inc., Palo Alto, CA, USA.
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Pell JK. 2009. Fungal entomopathogens: new insights on their ecology. Fungal Ecology. 2(4): 149–159. https://doi.org/10.1016/j.funeco.2009.05.001
Vreysen MJB, Carpenter JE, Marec F. 2010. Improvement of the sterile insect technique for codling moth Cydia pomonella (Linnaeus) (Lepidoptera Tortricidae) to facilitate expansion of field application. Journal of Applied Entomology. 134(3): 165–181. https://doi.org/10.1111/j.1439-0418.2009.01430.x
Wraight SP, Carruthers RI, Jaronski ST, Bradley CA, Garza CJ, Galaini-Wraight S. 2000. Evaluation of the entomopathogenic fungi Beauveria bassiana and Paecilomyces fumosoroseus for microbial control of the silverleaf whitefly, Bemisia argentifolii. Biological Control. 17(3): 203–217. https://doi.org/10.1006/bcon.1999.0799
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