Effects of the entomopathogenic fungus, Lecanicillium longisporum on survival and population growth parameters of the cabbage aphid, Brevicoryne brassicae (Hemiptera: Aphididae) under laboratory conditions

Document Type : Paper, English

Authors

Department of Plant Protection, Faculty of Agriculture, Urmia University

Abstract

This study was carried out to determine the effects of the entomopathogenic fungus, Lecanicillium longisporum Zimmermann Strain LRC 190, on survival and population growth parameters of the cabbage aphid, Brevicoryne brassicae (L.) treated by using different conidial concentrations (1×103, 1×104, 1×105, 1×106, and 1×107 conidia/ml). Experiments were conducted at 23±1oC temperature, 60±5 %RH and a photoperiod of 16: 8 h. (L: D) on cabbage seedlings, Brassica oleracea var. capitata under laboratory conditions. Based on the results the longevity of the aphid adults was significantly different based on conidial concentrations of L. longisporum (Petch) Zare and Gams. The shortest longevity of the cabbage aphid adults was 10.70±1.59 days when treated with 1×107 conidia/ml, compared to 22.65±0.94 days in control treatment. The LC50 value was 1.82×106 conidia/ml 7 days after inoculation. Net rate of reproduction (R0), intrinsic rate of increase (rm) and finite rate of increase (λ) were significantly reduced in treated aphids compared to control treatment. There was no significant difference among mean generation times (T) in populations treated with 1×105, 1×106, 1×107 conidia/ml (P>0.05). Fungal infection was detectedin lower rm values and prolonged doubling time (DT) in treated females (3.492 days at the concentration of 1×107 conidia/ml), compared to the control (2.652 days). Considering higher concentrations of L. longisporum can effectively reduce the cabbage aphid longevity, reproduction and population growth under laboratory conditions, it seems that the fungus has ability for biological control of the cabbage aphid.

Keywords


Alavo, T. B. C., Sermann, H. & Bochow, H. (2002) Virulence of strains of entomopathogenic fungus Verticillium lecanii to aphids strain improvement. Archives of Phytopathology and Plant Protection 34(6), 379-398.
Andrewartha, H. & Birch, L. (1954) The Distribution and Abundance of Animals. University of Chicago Press, Chicago, Illinois.
Ansari, M. A., Vestergaard, S., Tirry, L. & Moensa, M. (2004) Selection of a highly virulent fungal isolates, Metarhizium anisopliae CLO 53, for controlling Hoplia philanthus. Journal of Invertebrate Pathology 85(2), 89-96.
Asi, M. R., Bashir, M. H., Mirza, J. H., Afzal,M. & Imran,S. (2009) In vitro efficacy of entomopathogenic fungi against cabbage aphid, Brevicoryne brassicae L. Pakistan Journal of Entomology 31(1), 43-46.
Askary, H., Carriere, Y., Belanger, R. R. & Brodeur, J. (1998) Pathogenicity of the fungus Verticillium lecanii to aphids and powdery mildew. Bicontrol Science and Technology 8(1), 23-32.
Blackman, R. L. & Eastop, V. F. (2006) Aphids on the World’s Herbaceous Plants and Shrubs. Vol. 1. John Wiley & Sons, West Sussex, England.
Carey, J. R. (1993) Applied Demography for Biologists, with Special Emphasis on Insects. Oxford University Press, Oxford.
Cole, L. C. (1954) The population consequences of life history phenomena. The Quarterly Review of Biology 29, 103-137.
Cooke, R. (1977) The Biology of Symbiotic Fungi. John Willey and Sons, New York.
Copping, L. G. (2004) The Manual of Biocontrol Agents. British Crop Protection Council.
Dixon, A. F. G. (1987) Parthenogenetic reproduction and the rate of increase of aphids. pp. 269-287 in: Minks A. K. & Harrewijn P. (Eds). Aphids: Their Biology, Natural Enemies and Control. Elsevier, Amsterdam, The Netherlands.
Ekesi, S. & Maniania, N. K. (2000) Susceptibility of Megalurothrips sjostedti development stages to Metarhizium anisopliae and the effects of infection on feeding, adult fecundity, egg fertility and longevity. Entomologia Experimentalis et Applicata 94, 229-236.
Ellis, P. R., Pink, D. A. C., Phelps, K., Jukes, P. L., Breeds, S. E. & Pinnegar, A. E. (1998) Evaluation of a core collection of brassica accessions for resistance to Brevicoryne brassicae. Euphytica 103, 149-160.
Emami, S., Safavi, S. A. & Gusta, Y. (2016) Lethal and sublethal effects of Metarhizium anisoplinae on fertility life table parameters of Brevicoryne brassicae in laboratory conditions. Biological Control of Pests and Plant Diseases 5(2), 261-268.
Fadayivata S., Moravvej, Gh. & Karimi J. (2014) Pathogenicity of the fungus Lecanicillium longisporum against Sipha maydis and Metopolophium dirhodum in laboratory conditions. Journal of Plant Protection Research 54(1), 67-73.
Faria, M. R. & Wraight, S. P. (2007) Mycoinsecticides and mycoacarides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control 43, 237-256.
Fazeli-Dinan, M, Talaei-Hassanloui, R. & Goettel, M. (2016) Virulence of the entomopathogenic fungus Lecanicillium longisporum against the greenhouse whitefly, Trialeurodes vaporariorum and its parasitoid Encarsia formosa. International Journal of Pest Management 62(3), 251-260.
Fournier, V. & Brodeur, J. (2000) Dose response susceptibility of pest aphids (Homoptera: Aphididae) and their control on hydroponically grown lettuce with the entomopathogenic fungus Verticillium lecanii, azadirachtin, and insecticidal soap. Environmental Entomology 29, 568-578.
Ganassi, S., Grazioso, P., Moretti, A. & Sabatini, M. A. (2010) Effects of the fungus Lecanicillium lecanii on survival and reproduction of the aphid Schizaphis graminum. BioControl 55(2), 299-312.
Ganassi, S., Moretti, A., Logrieco, A., Bonvicini Pagliai A. M & Sabatini, M. A. (2004) A laboratory study on colonisation of aphids by some filamentous fungi. pp. 299-306 in Simon, J.-C., Dedryver, C. A., Rispe, C., Hulle´, M. (Eds), Aphids in a New Millennium. Proceedings of the VIth International Symposium on Aphids, Versailles, INRA Editions.
Ghaffari, S., Karimi, J., Kamali, Sh. & Moghadam, E. M. (2017) Biocontrol of Planococcus citri (Hemiptera: Pseudococcidae) by Lecanicillium longisporum and Lecanicillium lecanii under laboratory and greenhouse conditions. Journal of Asia Pacific Entomology 20(2), 605-612.
Goettel, S. & Inglis, G. D. (1997) Fungi: Hyphomycetes. pp. 14-19 in: Lacey, L. A. (Ed), Manual of Techniques in Insect Pathology. Academic Press, London.
Goettel, M. S., Koike, M., Kim, J. J., Aiuchi, D., Shinya, R. & Brodeur, J. (2008) Potential of Lecanicillium spp. for management of insects, nematodes and plant diseases. Journal of Invertebrate Pathology 98, 256-261.
Hall, R. A. (1984) Epizootic potential for aphids of different isolates of the fungus Verticillium lecanii. Entomophaga 29, 311-321.
Holder, D. J. & Keyhani, N. O. (2005) Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Applied and Environmental Microbiology 71 (9), 5260-5266.
Isman, M. B. (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annual Review of Entomology 51, 45-66.
Kim, J. J. (2007) Influence of Lecanicillium attenuatum on the development and reproduction of the cotton aphid, Aphis gossypii. BioControl 52(6), 789-799.
Kim, J. J., Goettel, M. S. & Gillespie, D. R. (2007) Potential of Lecanicillium species for dual microbial control of aphids and the cucumber powdery mildew fungus, Sphaerotheca fuliginea. Biological Control 40 (3), 327-332.
Kim, J. J., Goettel, M. S. & Gillespie, D. R. (2008) Evaluation of Lecanicillium longisporum, Vertalec® for simultaneous suppression of cotton aphid, Aphis gossypii, and cucumber powdery mildew, Sphaerotheca fuliginea, on potted cucumbers. Biological Control 45, 404-409.
Kim, J. J., Goettel, M. S. & Gillespie, D. R. (2010) Evaluation of Lecanicillium longisporum, Vertalec® against the cotton aphid, Aphis gossypii, and cucumber powdery mildew, Sphaerotheca fuliginea in a greenhouse environment. Crop Protection 29, 540-544.
Kim, J. J., Lee, M. H., Yoon, C. S., Kim, H. S., Yoo, J. K. & Kim, K. C. (2001) Control of cotton aphid and greenhouse whitefly with a fungal pathogen. pp. 8-15 in Biological control of greenhouse pests. Food and Fertilizer Technology Center Extension Bulletin, 502. Food and Fertilizer Technology Center, Taipei, Taiwan.
Lashkari, M. R., Sahragard, A. & Ghadamyari, M. (2007) Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid, Brevicoryne brassicae on rapeseed, Brassica napus L. Insect Science 14, 207-212.
Liu, H., Skinner, M., Parker, B. L. & Brownbridge, M. (2002) Pathogenicity of Beauveria bassiana, Metarhizium anisopliae (Deuteromycotina: Hyphomycetes), and other Entomopathogenic Fungi against Lygus lineolaris (Hemiptera: Mirridae). Journal of Economic Entomology 95, 675-681.
Maia, A. H. N., Pazianotto, R. A. A., Luiz, A. J. B., Marinho-Prado, J. S. & Pervez A. (2014) Inference on arthropod demographic parameters: computational advances using R. Journal of Economic Entomology 107(1), 432-439.
Meyer, J. S., Ingersoll, C. G., McDonald, L. L. & Boyce, M. S. (1986) Estimating uncertainty in population growth rates: Jackknife vs. Bootstrap techniques. Ecology 67, 1156-1166.
Moharramipour, S., Monfared, A. & Fathipour, Y. (2003) Comparison of intrinsic rate of increase and relative growth rate of cabbage aphid (Brevicoryne brassicae L.) on four rapeseed (Brassica napus L.) varieties in a growth chamber. Agricultural Science 13, 79- 86.
Nazemi, A. M., Moravvej, Gh., Karimi, J. & Talaei-Hassanlouei, R. (2014) Pathogenicity of Lecanicillium longisporum (Ascomycota: Hypocreomycetidae) on the aphid Cinara pini (Hemiptera: Lachnidae) in laboratory conditions. Journal of Crop Protection 3(2), 159-171.
Powell, W. & Pell, J. K. (2007) Biological control. pp: 469-514 in Harrington, R., Emden, V. H. (Eds) Aphids as Crop Pests. CABI International. Publishing, UK.
Rashki, M., Kharazi-pakdel, A., Allahyari, H. & van Alphen, J. J. M. (2009) Interactions among the entomopathogenic fungus, Beauveria bassiana (Ascomycota: Hypocreales), the parasitoid, Aphidius matricariae (Hymenoptera: Braconidae), and its host, Myzus persicae (Homoptera: Aphididae). Biological Control 50 (3), 324-328.
Rashki, M. & Shirvani, A. (2013) The effect of entomopathogenic fungus, Beauveria bassiana on life table parameters and behavioural response of Aphis gossypii. Bulletin of Insectology 66 (1), 85-91.
Safavi, S. A., Rassulian, Gh. R., Kharrazi Pakdel, A. & Askari, H. (2002) Pathogenicity and virulence of entomogenous fungus, Verticillium lecanii on the pea aphid, Acyrthosiphon pisum. Journal of Science and Technology of Agriculture and Natural Resources 6(1), 245-255.
SAS Institute (1992) SAS. 9.1 User's guide. SAS Institute Inc., Cary, NC, USA.
Seyed Talebi, F. S., Kheradmand, K., Talaei Hassanloui, R. & Talebi Jahromi, K. (2012) Sublethal effects of Beauveria bassiana on life table parameters of two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Biocontrol Science and Technology 22 (3), 293-303.
Stark, J. D. & Bank, J. E. (2003) Population level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology 48, 505-519.
Taheri Sarhozaki, M. & Safavi, S. A. (2014a) Population growth parameters of the cabbage aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae), exposed to sublethal doses of thiacloprid. Archives of Phytopathology and Plant Protection 47 (4), 464-471.
Taheri Sarhozaki, M. & Safavi, S. A. (2014b) Sub-lethal effects of tiametoxam on life table parameters of the cabbage aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae) under laboratory conditions. Archives of Phytopathology and Plant Protection 47 (4), 508-515.
Ujjan, A. A. & Shahzad, S. (2012) Use of entomopathogenic fungi for the control of mustard aphid (Lipaphis erysimi) on canola (Brassica napus L.). Pakistan Journal of Botany 44(6), 2081-2086.
Wright, M. S., Raina, A. K. & Lax, A. R. (2005) A strain of the fungus Metarhizium anisopliae for controlling subterranean termites. Journal of Economic Entomolgy 98, 1451-1458.
Zaki, F. N. (1998) Efficiency of the entomopathogenic fungus, Beauveria bassiana (Bals), against Aphis crassivora Koch and Bemesia tabaci Gennandius. Journal of Applied Entomology 122, 397-399.
Zare, R. & Gams, W. (2001) A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium gen. Nova Hedwigia 73, 1-50.
Zarghami, S., Allahyari, H., Bagheri, M. R. & Saboori, A. (2010) Effect of nitrogen fertilization on life table parameters and population growth of Brevicoryne brassicae. Bulletin of Insectology 63(1), 39-43.