Interactions among vegetable-infesting aphids, the fungal pathogen Metarhizium anisopliae (Ascomycota: Hypocreales) and the predatory coccinellid Cheilomenes lunata (Coleoptera: Coccinellidae)

References

• Adisu, B., & Freier, B. (2003). The potential of biocontrol agents for the control of Diuraphis noxia (Homoptera: Aphididae) in spring barley in the central highlands of Ethiopia. Biological Agriculture & Horticulture, 21, 35–51. doi: 10.1080/01448765.2003.9755248
   Web of Science ®Google Scholar
• Alma, C. R., Gillespie, D. R., Roitberg, B. D., & Goettel, M. S. (2010). Threat of infection and threat-avoidance behavior in the predator Dicyphus hesperus feeding on whitefly nymphs infected with an entomopathogen. Journal of Insect Behavior, 23, 90–99. doi: 10.1007/s10905-009-9198-8
   Web of Science ®Google Scholar
• Barron, A., & Wilson, K. (1998). Overwintering survival in the seven spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae). European Journal of Entomology, 95, 639–642.
   Web of Science ®Google Scholar
• Bayissa, H. W., Ekesi, S., Mohamed, S. A., Kaaya, G. P., Wagacha, J. M., Hanna, R., … Maniania, N. K. (2015). Broad-based virulence of entomopathogenic fungi against aphid pests of crucifers and okra. Manuscript submitted for publication.
   Google Scholar
• Bidochka, M. J., & Small, C. S. (2005). Phylogeography of Metarhizium, an insect pathogenic fungus. In F. E. Vega, & M. Blackwell (Eds.), Insect-fungal associations: Ecology and evolution (pp. 28–50). New York, NY: Oxford University Press.
   Google Scholar
• de Bon, H., Huat, J., Parrot, L., Sinzogan, A., Martin, T., Malézieux, E., … Vayssières, J.-F. (2014). Pesticide risks from fruit and vegetable pest management by small farmers in sub-Saharan Africa. A review. Agronomy for Sustainable Development, 34, 723–736. doi: 10.1007/s13593-014-0216-7
   Web of Science ®Google Scholar
• Brown, H. (1972). Predacious behaviour of four species of Coccinellidae (Coleoptera) associated with the wheat aphid, Schizaphis graminum (Rondani), in South Africa. Transactions of the Royal Entomological Society of London, 124, 21–36. doi: 10.1111/j.1365-2311.1972.tb00357.x
   Google Scholar
• Burgerjon, A. (1956). Pulvérisation et poudrage au laboratoire par des préparations pathogènes insecticides. Annals of Epiphytology, 4, 677–688.
   Google Scholar
• Carletto, J., Martin, T., Vanlerberghe-Masutti, F., & Bŕevault, T. (2010). Insecticide resistance traits differ among and within host races in Aphis gossypii. Pest Management Science, 66, 301–307. doi: 10.1002/ps.1874
   PubMed Web of Science ®Google Scholar
• Ceryngier, P., & Hodek, I. (1996). Enemies of Coccinellidae. In I. Hodek & A. Honek (Eds.), Ecology of Coccinellidae (pp. 319–350). Dordrecht: Kluwer Academic.
   Google Scholar
• Dixon, A., Hemptinne, J.-L., & Kindlmann, P. (1997). Effectiveness of ladybirds as biological control agents: Patterns and processes. Entomophaga, 42, 71–83. doi: 10.1007/BF02769882
   Google Scholar
• Ekesi, S., Maniania, N., Ampong-Nyarko, K., & Onu, I. (1999). Effect of intercropping cowpea with maize on the performance of Metarhizium anisopliae against Megalurothrips sjostedti (Thysanoptera: Thripidae) and predators. Environmental Entomology, 28, 1154–1161. doi: 10.1093/ee/28.6.1154
   Web of Science ®Google Scholar
• Ekesi, S., Shah, P., Clark, S., & Pell, J. (2005). Conservation biological control with the fungal pathogen Pandora neoaphidis: Implications of aphid species, host plant and predator foraging. Agricultural and Forest Entomology, 7, 21–30. doi: 10.1111/j.1461-9555.2005.00239.x
   Web of Science ®Google Scholar
• de Faria, M. R., & Wraight, S. P. (2007). Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43, 237–256. doi: 10.1016/j.biocontrol.2007.08.001
   Web of Science ®Google Scholar
• Ginsberg, H. S., Lebrun, R. A., Heyer, K., & Zhioua, E. (2002). Potential nontarget effects of Metarhizium anisopliae (Deuteromycetes) used for biological control of ticks (Acari: Ixodidae). Environmental Entomology, 31, 1191–1196. doi: 10.1603/0046-225X-31.6.1191
   Web of Science ®Google Scholar
• Goettel, M. S., Poprawski, J. D., Vandenberg, J., Li, Z., & Roberts, D. W. (1990). Safety to nontarget invertebrates of fungal biocontrol agents. In M. Laird, L. A. Lacey, & E. W. Davidson (Eds.), Safety of microbial insecticides (pp. 209–231). Boca Raton, FL: CRC.
   Google Scholar
• Gomez, K. A., & Gomez, A. A. (1984). Statistical procedures for agricultural research. New York: John Wiley & Sons.
   Google Scholar
• Iperti, G. (1966). Protection of coccinellids against mycosis. In I. Hodek (Ed.), Ecology of aphidophagous insects (pp. 189–190). The Hague: Junk.
   Google Scholar
• Jandricic, S., Filotas, M., Sanderson, J., & Wraight, S. (2014). Pathogenicity of conidia-based preparations of entomopathogenic fungi against the greenhouse pest aphids Myzus persicae, Aphis gossypii, and Aulacorthum solani (Hemiptera: Aphididae). Journal of Invertebrate Pathology, 118, 34–46. doi: 10.1016/j.jip.2014.02.003
   PubMed Web of Science ®Google Scholar
• Jaronski, S. T., Goettel, M. S., & Lomer, C. J. (2003). Regulatory requirements for ecotoxicological assessments of microbial insecticides – how relevant are they? In H. M. T. Hokkanen & A. E. Hajek (Eds.), Environmental impacts of microbial insecticides (pp. 237–260). Dordrecht: Kluwer Academic.
   Google Scholar
• Jaronski, S. T., Lord, J., Rosinska, J., Bradley, C., Hoelmer, K., Simmons, G., … Antilla, L. (1998, November 9–12). Effect of a Beauveria bassiana-based mycoinsecticide on beneficial insects under field conditions. Brighton Crop Protection Conference: Pests & Diseases, Proceedings of an International Conference, Brighton.
   Google Scholar
• Kabaluk, J. T., Svircev, A. M., Goettel, M. S., & Woo, S. G. (2010). The use and regulation of microbial pesticides in representative jurisdictions worldwide. Retrieved from http://www.iobcglobal.org/publications.html#microbial_regulat-ion_book.
   Google Scholar
• Koo, H.-N., An, J.-J., Park, S.-E., & Ju-Il Kim, G.-H. K. (2014). Regional susceptibilities to 12 insecticides of melon and cotton aphid, Aphis gossypii (Hemiptera: Aphididae) and a point mutation associated with imidacloprid resistance. Crop Protection, 55, 91–97. doi: 10.1016/j.cropro.2013.09.010
   Web of Science ®Google Scholar
• Maniania, N., Sithanantham, S., Ekesi, S., Ampong-Nyarko, K., Baumgärtner, J., Löhr, B., & Matoka, C. (2003). A field trial of the entomogenous fungus Metarhizium anisopliae for control of onion thrips, Thrips tabaci. Crop Protection, 22, 553–559. doi: 10.1016/S0261-2194(02)00221-1
   Web of Science ®Google Scholar
• Meyling, N. V., & Pell, J. K. (2006). Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecological Entomology, 31, 162–171. doi: 10.1111/j.0307-6946.2006.00781.x
   Web of Science ®Google Scholar
• Nderitu, J. H., Kasina, J. M., Kimenju, J. W., & Malenge, F. (2008). Evaluation of synthetic and neem-based insecticides for managing aphids on okra (Malvaceae) in Eastern Kenya. Journal of Entomology, 5, 207–212. doi: 10.3923/je.2008.207.212
   Google Scholar
• Ntow, W., Gijzen, H., Kelderman, P., & Drechsel, P. (2006). Farmer perceptions and pesticide use practices in vegetable production in Ghana. Pest Management Science, 62, 356–365. doi: 10.1002/ps.1178
   PubMed Web of Science ®Google Scholar
• Ofuya, T. I. (1995). Colonization and control of Aphis craccivora Koch (Homoptera: Aphididae) by coccinellid predators in some resistant and susceptible cowpea varieties in Nigeria. Crop Protection, 14, 47–50. doi: 10.1016/0261-2194(95)91111-R
   Web of Science ®Google Scholar
• Ojiewo, C. O., Tenkouano, A., & Yang, R. (2010). The role of AVRDC-The world vegetable centre in vegetable value chains. African Journal of Horticultural Science, 3, 1–23.
   Google Scholar
• Ormond, E. L., Thomas, A. P. M., Pell, J. K., & Roy, H. E. (2006). Overwintering ecology of Coccinella septempunctata, Beauveria bassiana and Dinocampus coccinellae. IOBC wprs Bulletin, 29, 85–88.
   Google Scholar
• Pell, J., Pluke, R., Clark, S., Kenward, M., & Alderson, P. (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). Journal of Invertebrate Pathology, 69, 261–268. doi: 10.1006/jipa.1996.4651
   Web of Science ®Google Scholar
• Pell, J., & Vandenberg, J. (2002). Interactions among the aphid Diuraphis noxia, the entomopathogenic fungus Paecilomyces fumosoroseus and the coccinellid Hippodamia convergens. Biocontrol Science and Technology, 12, 217–224. doi: 10.1080/09583150120124478
   Web of Science ®Google Scholar
• Pourian, H.-R., Talaei-Hassanloui, R., Kosari, A., & Ashouri, A. (2011). Effects of Metarhizium anisopliae on searching, feeding and predation by Orius albidipennis (Hem., Anthocoridae) on Thrips tabaci (Thy., Thripidae) larvae. Biocontrol Science and Technology, 21, 15–21. doi: 10.1080/09583157.2010.517603
   Web of Science ®Google Scholar
• R Development Core Team. (2011). R: A language and environment for statistical computing. Retrieved from http://www.R-project.org/
   Google Scholar
• Roy, H. E., Baverstock, J., Ware, R. L., Clark, S. J., Majerus, M. E. N., Baverstock, K. E., & Pell, J. K. (2008). Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecological Entomology, 33, 175–182. doi: 10.1111/j.1365-2311.2007.00954.x
   Web of Science ®Google Scholar
• Roy, H. E., & Cottrell, T. E. (2008). Forgotten natural enemies: Interactions between coccinellids and insect-parasitic fungi. European Journal of Entomology, 105, 391–398. doi: 10.14411/eje.2008.049
   Web of Science ®Google Scholar
• Roy, H. E., & Pell, J. K. (2000). Interactions between entomopathogenic fungi and other natural enemies: Implications for biological control. Biocontrol Science & Technology, 10, 737–752. doi: 10.1080/09583150020011708
   Web of Science ®Google Scholar
• Roy, H. E., Pell, J. K., & Alderson, P. G. (2003). Effect of spatial heterogeneity on the role of Coccinella septempunctata as an intra-guild predator of the aphid pathogen Pandora neoaphidis. Journal of Invertebrate Pathology, 82, 85–95. doi: 10.1016/S0022-2011(02)00201-X
   PubMed Web of Science ®Google Scholar
• Roy, H. E., Pell, J. K., Clark, S., & Alderson, P. G. (1998). Implications of predator foraging on aphid pathogen dynamics. Journal of Invertebrate Pathology, 71, 236–247. doi: 10.1006/jipa.1997.4736
   PubMed Web of Science ®Google Scholar
• Sæthre, M-G., Godonou, I., Hofsvang, T., Tepa-Yotto, G., & James, B. (2011). Aphids and their natural enemies in vegetable agroecosystems in Benin. International Journal of Tropical Insect Science, 31, 103–117. doi: 10.1017/S1742758411000191
   Google Scholar
• Shackleton, C. M., Pasquini, M. W., & Drescher, A. W. (2009). African indigenous vegetables in urban agriculture. London: Earthscan.
   Google Scholar
• Sithanantham, S., Ampong-Nyarko, K., Seshu-Reddy, K., Ampong-Nyarko, K., Varla, A., Maniania, N., … Lako, G. (1997). IPM for export vegetables. Nairobi: ICIPE Science Press.
   Google Scholar
• Smith, F. I., & Eyzaguirre, P. (2007). African leafy vegetables: Their role in the World Health Organization's global fruit and vegetables initiative. African Journal of Food Agriculture Nutrition and Development, 7, 1–17.
   Google Scholar
• Vandenburg, J. D., Ramos, M., & Altre, J. A. (1998). Dose–response and age- and temperature-related susceptibility of the diamondback moth (Lepidoptera: Plutellidae) to two isolates of Beauveria bassiana (Hyphomycetes: Moniliaceae). Environmental Entomology, 27, 1017–1021. doi: 10.1093/ee/27.4.1017
   Web of Science ®Google Scholar
• Veen, K. (1968). Recherches sur la maladie due à Metarrhizium anisopliae chez le criquet pèlerin (Vol. 68, pp. 1–77). Mededelingen Landbouwhogeschool: Wageningen.
   Google Scholar
• Wells, P. M., Baverstock, J., Majerus, M. E. N., Jiggins, F. M., Roy, H. E., & Pell, J. K. (2011). The effect of the coccinellid Harmonia axyridis on transmission and dispersal of the fungal pathogen Pandora neoaphidis. European Journal Entomology, 108, 87–90. doi: 10.14411/eje.2011.011
   Web of Science ®Google Scholar
• Williamson, S., Ball, A., & Pretty, J. (2008). Trends in pesticide use and drivers for safer pest management in four African countries. Crop Protection, 27, 1327–1334. doi: 10.1016/j.cropro.2008.04.006
   Web of Science ®Google Scholar
• Woin, N., Volkmar, C., & Ghogomu, T. (2006). Numerical response of predatory ladybirds (Coccinellidae) to aphid outbreaks and their diversity in major rice ecosystems of Cameroon. Archives of Phytopathology and Plant Protection, 39, 189–196. doi: 10.1080/03235400400027366
   Google Scholar
• Zimmermann, G. (2007). Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Science and Technology, 17, 879–920. doi: 10.1080/09583150701593963
   Web of Science ®Google Scholar