Scarab beetles (Coleoptera: Scarabaeidae) as economically important pests and the possibility of using entomopathogenic fungi for their control

Authors

  • Eva PRAPROTNIK Kmetijski inštitut Slovenije, Ljubljana, Slovenija
  • Jaka RAZINGER Kmetijski inštitut Slovenije, Ljubljana, Slovenija
  • Stanislav TRDAN Univerza v Ljubljani, Biotehniška fakulteta, Oddelek za agronomijo, Ljubljana, Slovenija

DOI:

https://doi.org/10.14720/aas.2022.118.1.2476

Keywords:

Scarabaeidae, scarab beetles, white grubs, entomopathogenic fungi, biological control

Abstract

Scarab beetles (Coleoptera: Scarabaeidae) are a cosmopolitan group of beetles found on all continents except Antarctica. Because of their size, vibrant colors, and above all their role in the ecosystem, they are one of the most recognizable and studied taxons of beetles. Most larvae and adult beetles of species belonging to subfamilies Melolonthinae, Rutelinae, Dynastinae and Cetoniinae feed on plant organs such as roots, leaves, flowers and young fruits and are thus considered to be species of economic importance. In this article we describe some of the most economically important species of scarabs, including their most common host plants. Because the use of chemical insecticides to control scarabs is often limited, the implementation of entomopathogenic fungi as biological control agents is an appropriate alternative based on the rational use of microorganisms to maintain an environmentally balanced level of the pest population. Representatives of the genera Beauveria and Metarhizium are the most commonly used entomopathogenic fungi to control larvae (white grubs) of scarab beetles. Biological control by entomopathogenic fungi has shown to be effective in some cases, however host range is often species-specific. Therefore, in order to effectively use the entomopathogens against scarab beetles, one needs to identify target species in grub-infested area and consequently select strains that are capable of overcoming the host’s defences.

References

Bai, M., Li, S., Lu, Y., Yang, H., Tong, Y., & Yang, X. (2015). Mandible evolution in the Scarabaeinae (Coleoptera: Scarabaeidae) and adaptations to coprophagous habits. Frontiers in Zoology, 12(1), 1–10. https://doi.org/10.1186/s12983-015-0123-z

Bernays, E. A., & Chapman, R. F. (1994). Chemicals in plants. In E. A. Bernays & R. F. Chapman (Eds.), Host-plant selection by phytophagous insects (pp. 22–23). New York: Chapman and Hall. https://doi.org/10.1007/b102508

Berón, C. M., & Diaz, B. M. (2005). Pathogenicity of hyphomycetous fungi against Cyclocephala signaticollis. BioControl, 50(1), 143–150. https://doi.org/10.1007/s10526-004-0586-x

Bouchard, P., Bousquet, Y., Davies, A. E., Alonso-Zarazaga, M. A., Lawrence, J. F., Lyal, C. H. C., … Smith, A. B. T. (2011). Family-group names in Coleoptera (Insecta). ZooKeys, 88, 1–972. https://doi.org/10.3897/zookeys.88.807

Bragard, C., Dehnen-Schmutz, K., Di Serio, F., Gonthier, P., Jacques, M. A., Jaques Miret, J. A., … MacLeod, A. (2018). Pest categorisation of Popil-lia japonica. EFSA Journal, 16(11). https://doi.org/10.2903/j.efsa.2018.5438

Brunner-Mendoza, C., Reyes-Montes, M. del R., Moonjely, S., Bidochka, M. J., & Toriello, C. (2019). A review on the genus Metarhizium as an en-tomopathogenic microbial biocontrol agent with emphasis on its use and utility in Mexico. Biocontrol Science and Technology, 29(1), 83–102. https://doi.org/10.1080/09583157.2018.1531111

Bullard, G., Pulsford, D., & Rath, A. C. (1993). BioGreen - A new Metarhizium anisopliae product for the control of pasture scarabs in Australia. In Society for Invertebrate Pathology XXVl Annual Meeting, Program and Abstracts (pp. 1–6). Asheville.

Burkhardt, C. C. (1955). Preliminary studies on control of white grubs in wheat. Journal of the Kansas Entomological Society, 28(2), 60–63.

Calcetas, O. A., Adorada, J. L., Adorada, J. R., Caoili, B. L., Rosales, A. M., & Dimapilis, E. F. (2021). New records of scarab insect pests of cacao (Theobroma cacao L .) in the Philippines. Philippine Journal of Science, 150(5), 1197–1206.

Carlson, D. C. (1991). Order Coleoptera. Lucanidae, Passalidae, Scarabaeidae (Scarabaeoidea). In F. W. Stehr (Ed.), Immature insects, Volume 2 (pp. 372–384). Iowa: Kendall/Hunt Publishing.

Carne, P. B., Greaves, R. T. G., & McInnes, R. S. (1974). Insect damage to plantation‐grown eucalypts in North Coastal New South Wales, with particular reference to Christmas beetles (Coleoptera: Scarabaeidae). Australian Journal of Entomology, 13(3), 189–206. https://doi.org/10.1111/j.1440-6055.1974.tb02173.x

Chandel, R. S., Chandla, V. K., Verma, K. S., & Pathania, M. (2013). Insect Pests of Potato in India: Biology and Management. In P. Giordanengo, C. Vincent, & A. Alyokhin (Eds.), Insect Pests of Potato Global Perspectives on Biology and Management (pp. 227–245). Academic Press. https://doi.org/10.1016/B978-0-12-386895-4.00008-9

Chandel, R. S., Pathania, M., Verma, K. S., Bhatacharyya, B., Vashisth, S., & Kumar, V. (2015). The ecology and control of potato whitegrubs of India. Potato Research, 58(2), 147–164. https://doi.org/10.1007/s11540-015-9295-3

Ciss, M., Bassène, M. D., Seck, M. T., Mbaye, A. G., Sall, B., Fall, A. G., … Bouyer, J. (2019). Environmental impact of tsetse eradication in Senegal. Scientific Reports, 9(1), 1–9. https://doi.org/10.1038/s41598-019-56919-5

Cock, M. J. W., & Allard, G. B. (2013). Observations on white grubs affecting sugar cane at the Juba Sugar project, south-western Somalia, in the 1980s, and implications for their management. Insects, 4(2), 241–272. https://doi.org/10.3390/insects4020241

De Goffau, L. J. W. (1996). Population development and dispersal of Melolontha and other Scarabaeidae in the Netherlands during the past 10 years. IOBC/WPRS Bulletin, 19, 9–14.

Dolci, P., Guglielmo, F., Secchi, F., & Ozino, O. I. (2006). Persistence and efficacy of Beauveria brongniartii strains applied as biocontrol agents against Melolontha melolontha in the valley of Aosta (northwest Italy). Journal of Applied Microbiology, 100(5), 1063–1072. https://doi.org/10.1111/j.1365-2672.2006.02808.x

Dworecka-Kaszak, B. (2014). Cordyceps fungi as natural killers, new hopes for medicine and biological control factors. Annals of Parasitology, 60(3), 151–158.

Eberle, J., Myburgh, R., & Ahrens, D. (2014). The evolution of morphospace in phytophagous scarab chafers: No competition - No divergence? PLoS ONE, 9(5). https://doi.org/10.1371/journal.pone.0098536

Enkerli, J., Widmer, F., & Keller, S. (2004). Long-term field persistence of Beauveria brongniartii strains applied as biocontrol agents against Euro-pean cockchafer larvae in Switzerland. Biological Control, 29(1), 115–123. https://doi.org/10.1016/S1049-9644(03)00131-2

Erler, F., & Ates, A. O. (2015). Potential of two entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae (Coleoptera: Scarabaei-dae), as biological control agents against the june beetle. Journal of Insect Science, 15(1), 1–6. https://doi.org/10.1093/jisesa/iev029

Fătu, A., Dinu, M. M., & Andrei, A. M. (2018). Susceptibility of some Melolonthinae scarab species to entomopathogenic fungus Beauveria brongni-artii (Sacc.) Petch and Metarhizium anisopliae (Metsch.). Scientific Bulletin. Series F. Biotechnologies, 22, 42–49.

Ferron, P. (1978). Biological control of insect pests by entomogenous fungi. Annual Review Of Entomology, 23(1), 409–442. https://doi.org/10.1146/annurev.en.23.010178.002205

Fleming, W. E. (1972). Biology of the Japanese Beetle. Washington, DC.: USDA Technical Bulletin 1449.

Frew, A., Barnett, K., Nielsen, U. N., Riegler, M., & Johnson, S. N. (2016). Belowground ecology of scarabs feeding on grass roots: Current knowledge and future directions for management in Australasia. Frontiers in Plant Science, 7(321). https://doi.org/10.3389/FPLS.2016.00321

Fröschle, M. (1996). Occurrence of the common cockchafer (Melolontha melolontha L.) in the state of Baden-Wüttemberg/Germany. IOBC/WPRS Bulletin, 19, 1–4.

Gibb, T. (2015). Pest Insects. In Contemporary Insect Diagnostics. The Art and Science of Practical Entomology (pp. 153–245). Academic Press. https://doi.org/10.1016/b978-0-12-404623-8.00005-3

Giroux, F., Lavallée, R., Bauce, É., & Guertin, C. (2015). Susceptibility of the Japanese beetle, Popillia japonica (Newman) (Coleoptera: Scarabaei-dae), to entomopathogenic Hypocreales fungi. Phytoprotection, 95(1), 1–6. https://doi.org/10.7202/1028399ar

Goettel, M. S., Poprawski, T. J. Vendenberg, J. D., Li, Z., & Roberts, D. W. (1990). Safety to nontarget invertebrates of fungal biocontrol agents. In M. Laird, L. A. Lacey, & E. M. Davidson (Eds.), Safety of Microbial Insecticides (pp. 210–224). Boca Raton: CRC Press.

Goh, H. H., Willoughby, B., Prestidge, R. A., & Lyons, S. N. (1991). Pathogenicity of Beauveria, Metarhizium, Paecilomyces and Fusarium isolates against early instar grass grub (Costelytra zealandica) larvae. In Proceedings of the 44th New Zealand Weed and Pest Control Conference (pp. 209–211). https://doi.org/10.30843/nzpp.1991.44.10834

Gopal, M., Gupta, A., & Thomas, G. V. (2006). Prospects of using Metarhizium anisopliae to check the breeding of insect pest, Oryctes rhinoceros L. in coconut leaf vermicomposting sites. Bioresource Technology, 97(15), 1801–1806. https://doi.org/10.1016/j.biortech.2005.09.005

Gyawaly, S., Koppenhöfer, A. M., Wu, S., & Kuhar, T. P. (2016). Biology, ecology, and management of masked chafer (Coleoptera: Scarabaeidae) grubs in turfgrass. Journal of Integrated Pest Management, 7(1), 1–11. https://doi.org/10.1093/jipm/pmw002

Hajek, A. E., & St. Leger, R. J. (1994). Interactions between fungal pathogens and insect hosts. Annual Review of Entomology, 39(1), 293–322. https://doi.org/10.1146/annurev.ento.39.1.293

Hann, P., Trska, C., Wechselberger, K. F., Eitzinger, J., & Kromp, B. (2015). Phyllopertha horticola (Coleoptera: Scarabaeidae) larvae in eastern Austrian mountainous grasslands and the associated damage risk related to soil, topography and management. SpringerPlus, 4(1), 1–15. https://doi.org/10.1186/s40064-015-0918-6

Hanski, I., & Cambefort, Y. (1991). Resource partitioning. In I. Hanski & Y. Cambefort (Eds.), Dung Beetle Ecology (pp. 330–350). Princeton: Prince-ton University Press. https://doi.org/10.1515/9781400862092

Heath, J. J., Williams, R. N., & Phelan, P. L. (2002). Aggregation and male attraction to feeding virgin females in Macrodactylus subspinosus (F.) (Coleoptera: Scarabaeidae: Melolonthinae). Environmental Entomology, 31(6), 934–940. https://doi.org/10.1603/0046-225X-31.6.934

Huang, S. W., Zhang, H. Y., Marshall, S., & Jackson, T. A. (2010). The scarab gut: A potential bioreactor for bio-fuel production. Insect Science, 17(3), 175–183. https://doi.org/10.1111/j.1744-7917.2010.01320.x

Ibrahim, R. A. (2017). Laboratory evaluation of entomopathogenic fungi, commercial formulations, against the Rhinoceros beetle, Oryctes aga-memnon arabicus (Coleoptera: Scarabaeidae). Egyptian Journal of Biological Pest Control, 27(1), 49–55.

Jackson, T. A. (1999). Factors in the success and failure of microbial control agents for soil dwelling pests. Integrated Pest Management Reviews, 4, 281–285. https://doi.org/10.1023/A:1009697019677

Jackson, T. A., & Klein, M. G. (2006). Scarabs as pests: A continuing problem. The Coleopterists Bulletin, 60(5), 102–119.

https://doi.org/10.1649/0010-065x(2006)60[102:sapacp]2.0.co;2

Jameson, M. L., & Ratcliffe, B. C. (2002). Series Scarabaeiformia Crowson 1960, Superfamily Scarabaeoidea Latreille 1802. In R. Arnett Jr., M. C. Thomas, P. E. Skelley, & F. Howard (Eds.), American Beetles, Volume 2: Polyphaga: Scarabaeoidea through Curculionoidea. Boca Raton: CRC Press.

Jessop, L. (1986). Dung beetles and chafers Coleoptera: Scarabaeoidea. In P. C. Barnard & R. R. Askew (Eds.), Handbooks for the Identification of British Insects Vol. 6, Part 11. London: Royal Entomological Society of London.

Keller, S. (2000). Use of Beauveria brongniartii and its acceptance by farmers. IOBC/WPRS Bulletin, 23, 67–71.

Kessler, P., Enkerli, J., Schweizer, C., & Keller, S. (2004). Survival of Beauveria brongniartii in the soil after application as a biocontrol agent against the European cockchafer Melolontha melolontha. BioControl, 49, 563–581. https://doi.org/10.1023/B:BICO.0000036441.40227.ed

Kim, S., Kim, J. C., Lee, S. J., Lee, M. R., Park, S. E., Li, D., … Kim, J. S. (2020). Soil application of Metarhizium anisopliae JEF-314 granules to control, flower chafer beetle, Protaetia brevitarsis seulensis. Mycobiology, 48(2), 139–147. https://doi.org/10.1080/12298093.2020.1735765

Kornsakulkarn, J., Saepua, S., Veeranondha, S., Rachtawee, P., Isaka, M., & Thongpanchang, C. (2018). Carboline alkaloids and isocoumarins from the wasp pathogenic fungus Ophiocordyceps sphecocephala BCC 2661. Phytochemistry Letters, 27, 134–138. https://doi.org/10.1016/j.phytol.2018.07.020

Łabanowska, B., & Bednarek, H. (2011). Efficacy of Beauveria brongniartii as Melocont in the control of the European cockchafer (Melolontha melolontha). IOBC/WPRS Bulletin, 66, 179–182.

Laengle, T., Pernfuss, B., Seger, C., & Strasser, H. (2005). Field efficacy evaluation of Beauveria brongniartii against Melolontha melolontha in potato cultures. Sydowia, 57(1), 54–66.

Laznik, Ž., & Trdan, S. (2014). Evaluation of different soil parameters and wild boar (Sus scrofa [L.]) grassland damage. Italian Journal of Animal Science, 13(4), 759–765. https://doi.org/10.4081/ijas.2014.3434

Laznik, Ž., & Trdan, S. (2015). Failure of entomopathogens to control white grubs (Coleoptera: Scarabaeidae). Acta Agriculturae Scandinavica Section B: Soil and Plant Science, 65(2), 95–108. https://doi.org/10.1080/09064710.2014.968199

LePelley, R. H., & Goddard, W. H. (1952). On the control by insecticides of Heteronychus consimilis Kolbe (Dynastidae), A serious pest of wheat in Kenya. Bulletin of Entomological Research, 43(2), 403–406. https://doi.org/10.1017/S0007485300040578

Lin, W. J., Lee, Y. I., Liu, S. L., Lin, C. C., Chung, T. Y., & Chou, J. Y. (2020). Evaluating the tradeoffs of a generalist parasitoid fungus, Ophiocordyceps unilateralis, on different sympatric ant hosts. Scientific Reports, 10(1), 1–12. https://doi.org/10.1038/s41598-020-63400-1

Logan, D. P., Robertson, L. N., & Milner, R. J. (2000). Review of the development of Metarhizium anisopliae as a microbial insecticide, BioCaneTM, for the control of greyback canegrub Dermolepida albohirtum (Waterhouse) (Coleoptera: Scarabaeidae) in Queensland sugarcane. IOBC/WPRS Bulletin, 23, 131–137.

Lovett, B., & St. Leger, R. J. (2017). The insect pathogens. Microbiology Spectrum, 5(2), 1–19. https://doi.org/10.1128/microbiolspec.FUNK-0001-2016

Malusá, E., Tartanus, M., Furmanczyk, E. M., & Łabanowska, B. H. (2020). Holistic approach to control Melolontha spp. in organic strawberry plantations. Organic Agriculture, 10, 13–22. https://doi.org/10.1007/s13165-020-00295-2

Maniania, N. K., Ekesi, S., & Dolinski, C. (2017). Entomopathogens Routinely Used in Pest Control Strategies: Orchards in Tropical Climate. In L. A. Lacey (Ed.), Microbial Control of Insect and Mite Pests: From Theory to Practice (pp. 269–282). Academic Press. https://doi.org/10.1016/B978-0-12-803527-6.00018-4

Marchal, M. (1976). Sensibilite a Beauveria brongniartii (Fungi imperfecti, Moniliales) des larves de Melolontha melolontha L. (Col.: Scarabaeidae) parasitees par Pseudomonocystis sp. (Sporozoaire, Eugregarinaria). Comptes Rendus Des Seances de La Societe de Biologie, 170(2), 295–299.

Mariau, D. (2001). Coleoptera. In D. Mariau (Ed.), The Fauna of Oil Palm and Coconut: Insect and Mites Pests and Their Natural Enemies (p. 118). La Librairie du Cirad Montpellier.

Mayerhofer, J., Enkerli, J., Zelger, R., & Strasser, H. (2015). Biological control of the European cockchafer: persistence of Beauveria brongniartii after long-term applications in the Euroregion Tyrol. BioControl, 60(5), 617–629. https://doi.org/10.1007/s10526-015-9671-6

Miah, M. A. H., Biswas, M. M., & Mannan, A. (1986). Effects of some insecticides on white grub control and yield of sugarcane. Tropical Pest Management, 32(4), 338–340. https://doi.org/10.1080/09670878609371089

Mora, M. A. E., Castilho, A. M. C., & Fraga, M. E. (2018). Classification and infection mechanism of entomopathogenic fungi. Arquivos Do Instituto Biológico, 84, 1–10. https://doi.org/10.1590/1808-1657000552015

Moslim, R., Wahid, M. B., Kamarudin, N., Sharma, M., & Ali, S. R. A. (1999). Impact of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) applied by wet and dry inoculum on oil palm rhinoceros beetles, Oryctes rhinoceros (Coleoptera: Scarabaeidae). Journal of Oil Palm Research, II(2), 25–40.

Neuvéglise, C., Brygoo, Y., Vercambre, B., & Riba, G. (1994). Comparative analysis of molecular and biological characteristics of strains of Beauve-ria brongniartii isolated from insects. Mycological Research, 98(3), 322–328. https://doi.org/10.1016/S0953-7562(09)80460-7

Niemczyk, M., Sierpińska, A., Tereba, A., Sokołowski, K., & Przybylski, P. (2019). Natural occurrence of Beauveria spp. in outbreak areas of cockchafers (Melolontha spp.) in forest soils from Poland. BioControl, 64(2), 159–172. https://doi.org/10.1007/s10526-019-09927-3

Oliveira, C. M., & Frizzas, M. R. (2013). Field biology of the beetle Aegopsis bolboceridus in Brazil, with a list of host plants. Journal of Insect Scien-ce, 13(48). https://doi.org/10.1673/031.013.4801

Oliveira, C. M., & Frizzas, M. R. (2021). Root consumption and damage estimates caused by Phyllophaga capillata and Aegopsis bolboceridus (Cole-optera, Melolonthidae) larvae in soybean and maize in central Brazil. Crop Protection, 146, 105651. https://doi.org/10.1016/j.cropro.2021.105651

Pathania, M., & Chandel, R. S. (2017). Life history strategy and behaviour of white grub, Brahmina coriacea (Hope) (Coleoptera: Scarabaeidae: Melolonthinae) an invasive pest of potato and apple agro-ecosystem in northwestern India. Oriental Insects, 51(1), 46–69. https://doi.org/10.1080/00305316.2016.1247756

Poprawski, T. J., & Yule, W. N. (1991). Incidence of fungi in natural populations of Phyllophaga spp. and susceptibility of Phyllophaga anxia (LeCon-te) (Col., Scarabaeidae) to Beauveria bassiana and Metarhizium anisopliae (Deuteromycotina). Journal of Applied Entomology, 112, 359–365. https://doi.org/10.1111/j.1439-0418.1991.tb01068.x

Poženel, A. (2007). Izkušnje pri zatiranju poljskega majskega hrošča (Melolontha melolontha L.) na Idrijskem. In Zbornik predavanj in referatov 8. slovenskega posvetovanja o varstvu rastlin (pp. 72–77).

Putnoky-Csicsó, B., Tonk, S., Szabó, A., Márton, Z., Bogdányi, F. T., Tóth, F., … Balog, A. (2020). Effectiveness of the entomopathogenic fungal spe-cies Metarhizium anisopliae strain NCAIM 362 treatments against soil inhabiting Melolontha melolontha larvae in sweet potato (Ipomoea bata-tas L.). Journal of Fungi, 6(116), 1–16. https://doi.org/10.3390/jof6030116

Qu, S., & Wang, S. (2018). Interaction of entomopathogenic fungi with the host immune system. Developmental and Comparative Immunology, 83, 96–103. https://doi.org/10.1016/j.dci.2018.01.010

Radcliffe, E. B., & Lagnaoui, A. (2007). Insect pests in potato. In D. Vreugdenhil (Ed.), Potato Biology and Biotechnology: Advances and Perspectives (pp. 543–567). Elsevier B.V. https://doi.org/10.1016/B978-044451018-1/50067-1

Ranganathaiah, K. G., Veeresh, G. K., & Govindu, H. C. (1973). A new entomogenous fungus on the root grub, Holotricha serrata F. from Mysore. Current Science, 42(12), 432–433.

Ratcliffe, B. C. (2002). A checklist of the Scarabaeoidea (Coleoptera) of Panama. Zootaxa, 32(1), 1–48. https://doi.org/10.11646/zootaxa.32.1.1

Rath, A. C., Koen, T. B., & Rowe, B. A. (1995). Long-term field efficacy of the entomogenous fungus Metarhizium anisopliae against the subterra-nean scarab, Adoryphorus couloni. Biocontrol Science and Technology, 5(4), 439–452. https://doi.org/10.1080/09583159550039639

Reddy, S. G. E. (2020). Lecanicillium spp. for the management of aphids, whiteflies, thrips, scales and mealy bugs: review. In Arthropods. IntechO-pen.

Rehner, S. A. (2005). Phylogenetics of the Insect Pathogenic Genus Beauveria. In F. E. Vega & M. Blackwell (Eds.), Insect-Fungal Associations. Eco-logy and Evolution. New York: Oxford University Press.

Ritcher, P. O. (1966). White grubs and their allies: A study of North American scarabaeoid larvae. Corvallis, Oregon: Oregon State University Press.

Saleem, A. R., & Ibrahim, R. A. (2019). Assessment of the virulence and proteolytic activity of three native entomopathogenic fungi against the larvae of Oryctes agamemnon (Burmeister) (Coleoptera: Scarabaeidae). Egyptian Journal of Biological Pest Control, 29(1), 1–8. https://doi.org/10.1186/s41938-019-0120-1

Sallam, M. N., Mcavoy, C. A., Samson, P. R., & Bull, J. J. (2007). Soil sampling for Metarhizium anisopliae spores in Queensland sugarcane fields. BioControl, 52(4), 491–505. https://doi.org/10.1007/s10526-006-9038-0

Sevim, A., Demir, I., Höfte, M., Humber, R. A., & Demirbag, Z. (2010). Isolation and characterization of entomopathogenic fungi from hazelnut-growing region of Turkey. BioControl, 55(2), 279–297. https://doi.org/10.1007/s10526-009-9235-8

Shanovich, H. N., Dean, A. N., Koch, R. L., & Hodgson, E. W. (2019). Biology and management of Japanese beetle (Coleoptera: Scarabaeidae) in corn and soybean. Journal of Integrated Pest Management, 10(1). https://doi.org/10.1093/jipm/pmz009

Sharma, A., Chandla, V. K., & Thakur, D. R. (2012). Biodiversity and pathogenicity potential of mycoflora associated with Brahmina coriacea in potato fields of North-Western Indian Hills. Journal of Entomology, 9, 319–331. https://doi.org/10.3923/je.2012.319.331

Sharma, L., & Marques, G. (2018). Fusarium, an entomopathogen—a myth or reality? Pathogens, 7(4). https://doi.org/10.3390/pathogens7040093

Shrestha, B., Tanaka, E., Hyun, M. W., Han, J.-G., Kim, C. S., Jo, J. W., … Sung, G.-H. (2016). Coleopteran and lepidopteran hosts of the entomo-pathogenic genus Cordyceps sensu lato. Journal of Mycology, 2016, 1–14. https://doi.org/10.1155/2016/7648219

Sierpińska, A., Popowska-Nowak, E., & Bednarek, A. (2015). Beauveria brongniartii Sacc. (Petch) against Melolontha spp. white grubs in forest nurseries with different soil pH. Folia Forestalia Polonica, Series A, 57(4), 210–217. https://doi.org/10.1515/ffp-2015-0021

Sinha, K. K., Choudhary, A. K., & Kumari, P. (2016). Entomopathogenic Fungi. In Omkar (Ed.), Ecofriendly Pest Management for Food Security (pp. 475–505). Academic Press. https://doi.org/10.1016/B978-0-12-803265-7.00015-4

Sosa-Gómez, D. R., López Lastra, C. C., & Humber, R. A. (2010). An overview of arthropod-associated fungi from Argentina and Brazil. Mycopatho-logia, 170(1), 61–76. https://doi.org/10.1007/s11046-010-9288-3

St. Leger, R. J., Screen, S. E., & Shams-Pirzadeh, B. (2000). Lack of host specialization in Aspergillus flavus. Applied and Environmental Microbiology, 66(1), 320–324. https://doi.org/10.1128/AEM.66.1.320-324.2000

Teetor-Barsch, G. H., & Roberts, D. W. (1983). Entomogenous Fusarium species. Mycopathologia, 84, 3–16. https://doi.org/10.1007/BF00436991

Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S. B., Klaassen, C. H. W., Perrone, G., … Samson, R. A. (2014). Identification and nomenclature of the genus Penicillium. Studies in Mycology, 78(1), 343–371. https://doi.org/10.1016/j.simyco.2014.09.001

Wagenhoff, E., Blum, R., & Delb, H. (2014). Spring phenology of cockchafers, Melolontha spp. (Coleoptera: Scarabaeidae), in forests of south-western Germany: Results of a 3-year survey on adult emergence, swarming flights, and oogenesis from 2009 to 2011. Journal of Forest Scien-ce, 60(4), 154–165. https://doi.org/10.17221/5/2014-jfs

Wightman, J. A., Brier, H. B., & Wright, G. C. (1994). The effect of root damage caused by simulated white grub attack on the growth, yield and water-use of groundnut plants. Plant and Soil, 160(2), 267–275. https://doi.org/10.1007/BF00010152

Williamson, R. C., Brandenburg, R., & Thompson, S. (2004). Turfgrass Insects of the United States: Biology and Management. In Encyclopedia of Entomology (pp. 2372–2403). Dordrecht: Springer Netherlands. https://doi.org/10.1007/0-306-48380-7_4440

Willis, J. H. (1959). Australian species of the fungal genus Cordyceps (Fr.) Link (with critical notes on collection in Australian herbaria). Muelleria, 1, 68–89.

Xu, J., Liu, N., & Zhang, R. (2013). Other Pests - China. In P. Giordanengo, C. Vincent, & A. Alyokhin (Eds.), Insect Pests of Potato Global Perspectives on Biology and Management (pp. 212–217). Academic Press. https://doi.org/10.1016/B978-0-12-386895-4.00007-7

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

Published

4. 04. 2022

Issue

Section

Review Article

How to Cite

PRAPROTNIK, E., RAZINGER, J., & TRDAN, S. (2022). Scarab beetles (Coleoptera: Scarabaeidae) as economically important pests and the possibility of using entomopathogenic fungi for their control. Acta Agriculturae Slovenica, 118(1), 1–10. https://doi.org/10.14720/aas.2022.118.1.2476

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