Infection of insects and persistence of Metarhizium (Hypocreales: Clavicipitaceae) species on apple bark




Codling moth, woolly apple aphid, biological control, Metarhizium brunneum, Metarhizium pinghaense, conidia


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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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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

TIBCO Software Inc. 2018. STATISTICA (data analysis software system), version 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.

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.

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.




How to Cite

Mathulwe LL, Malan AP, Stokwe NF. Infection of insects and persistence of Metarhizium (Hypocreales: Clavicipitaceae) species on apple bark. Afr. Entomol. [Internet]. 2023 Feb. 10 [cited 2023 Mar. 23];31. Available from: