Metarhizium anisopliae and Isaria fumosorosea challenge the survival and immunity of the palm weevil, Rhynchophorus ferrugineus Olivier

Keywords: Biochemical resistance, pathogenicity, bio-control, entomopathogenic fungi, integrated pest management

Abstract

Aim of study: Rhynchophorus ferrugineus Olivier is an invasive pest of palm worldwide. The use of insecticides by farmers for its management has been found insignificant. This study evaluated the potential use of entomopathogenic fungi for R. ferrugineus management with a particular focus on the fungal infection on the activities of different detoxification enzymes.

Area of study: Grubs and adults of R. ferrugineus were collected from various infested date palm fields in the four provinces of Pakistan.

Material and methods: Fungi Isaria fumosorosea (If-02) and Metarhizium anisopliae (Ma-M2) were evaluated against R. ferrugineus, and its immune responses were biochemically characterized.

Main results: The highest mortality rate was recorded at concentration 3×108 spores mL-1 on the 7th day post infection in the populations treated with M. anisopliae from Punjab, Khyber Pakhtunkhwa (KPK), Sindh and Baluchistan (93.75, 90.0, 90.0 and 81.25% respectively). M. anisopliae with lowest LC50 (1.1×106 spores mL-1) from Sindh also proved to be the most lethal fungus against R. ferrugineus. Maximum acetylcholinesterase (AChE) and glutathione S-transferases (GSTs) activities were observed in Baluchistan (26.28 and 24.0 μmol min-1 mg-1 protein, respectively) and maximum esterases (EST) activity (35.4 μmol min-1 mg-1 protein) was observed in the KPK population on the 3rd-day post I. fumosorosea infection.

Research highlights: Fungal infection by I. fumosorosea caused a significant increase in AChE, GST and EST activities which may hinder R. ferrugineus development. However, M. anisopliae, to some extent, also inhibited enzyme activities and yielded a sudden increase in mortality. Future bio-pesticides could be developed for integrated pest management (IPM) of palm weevil.

Downloads

Download data is not yet available.

References

Abdel-Moety E, Lotfy H, Rostom Y, 2012. Trace determination of red palm weevil, Rhynchophorus ferrugineus, pheromone at trapping locations under Egyptian climate. Int J Agr Food Sci 2: 13-20.

Abdel-Rahman I, Abdel-Raheem M, 2018. Using entomopathogenic fungi as bio agents control on the red palm weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). J Entomol Zool Stud 6: 387-390.

Abraham V, Shuaibi MA, Faleiro J, Abozuhairah R., Vidyasagar PS, 1998. An integrated management approach for red palm weevil Rhynchophorus ferrugineus Oliv. a key pest of date palm in the Middle East. J Agric Marine Sci 3: 77-83. https://doi.org/10.24200/jams.vol3iss1pp77-83

Ahmed R, Freed S, 2021a. Biochemical resistance mechanisms against chlorpyrifos, imidacloprid and lambda-cyhalothrin in Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Crop Prot 143: 105568. https://doi.org/10.1016/j.cropro.2021.105568

Ahmed R, Freed S, 2021b. Virulence of Beauveria bassiana Balsamo to red palm weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Egyp J Bio Pest Control 31: 1-4. https://doi.org/10.1186/s41938-021-00422-5

Al-Ayedh HY, Rasool KG, 2010. Determination of the optimum sterilizing radiation dose for control of the red date palm weevil Rhynchophorus ferrugineus Oliv. (Coleoptera: Curculionidae). Crop Prot 29: 1377-1380. https://doi.org/10.1016/j.cropro.2010.06.019

Al-Dosary NM, Al-Dobai S, Faleiro JR, 2016. Review on the management of red palm weevil Rhynchophorus ferrugineus Olivier in date palm Phoenix dactylifera L. Emir J Food Agric: 34-44. https://doi.org/10.9755/ejfa.2015-10-897

AlJabr AM, Hussain A, Rizwan-ul-Haq M, Al-Ayedh H, 2017. Toxicity of plant secondary metabolites modulating detoxification genes expression for natural red palm weevil pesticide development. Molecules 22: 169. https://doi.org/10.3390/molecules22010169

Al-Rajhy D, Hussein HI, Al-Shawaf AMA, 2005. Insecticidal activity of carbaryl and its mixture with piperonylbutoxide against red palm weevil Rhynchophorus ferrugineus (Olivier) (Curculionidae: Coleoptera) and their effects on acetylcholinesterase activity. Pak J Biol Sci 8: 679-682. https://doi.org/10.3923/pjbs.2005.679.682

Bakr RF, Abd Elaziz MF, El-Barky NM, Awad MH, El-Halim A, Hisham M, 2013. The activity of some detoxification enzymes in Spodoptera littoralis (Boisd.) larvae (Lepidoptera-Noctuidae) treated with two different insect growth regulators. Egyp Acad J Biol Sci 5: 19-27. https://doi.org/10.21608/eajbsc.2013.16092

Baloch H, Rustamani M, Khuhro R, Talpur M, Hussain T, 1992. Incidence and abundance of date palm weevil in different cultivars of date palm. Proc Pak Cong Zool 12: 445-447.

Bilal M, Freed S, Ashraf MZ, Muhammad S, 2017. Enhanced activities of acetylcholinesterase, acid and alkaline phosphatases in Helicoverpa armigera after exposure to entomopathogenic fungi. Invertebr Surviv J 14: 464-476.

Bogwitz MR, Chung H, Magoc L, Rigby S, Wong W, O'Keefe M, McKenzie JA, Batterham P, Daborn PJ, 2005. Cyp12a4 confers lufenuron resistance in a natural population of Drosophila melanogaster. Proc Natl Acad Sci 102: 12807-12812. https://doi.org/10.1073/pnas.0503709102

Bradford MM, 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3

Caballero C, López-Olguin JF, Ruíz MA, Ortego F, Castañera P, 2008. Antifeedant activity and effects of terpenoids on detoxication enzymes of the beet armyworm, Spodoptera exigua (Hübner). Span J Agric Res 6: 177-184. https://doi.org/10.5424/sjar/200806S1-386

Cabello T, De La Pena J, Barranco P, Belda J, 1997. Laboratory evaluation of imidacloprid and oxamyl against Rhynchophorus ferrugineus. Tests Agrochem Cult 18: 6-7.

Cao G, Jia M, Zhao X, Wang L, Tu X, Wang G et al., 2016. Different effects of Metarhizium anisopliae strains IMI330189 and IBC200614 on enzymes activities and hemocytes of Locusta migratoria L. PloS One 11: e0155257. https://doi.org/10.1371/journal.pone.0155257

Cerenius L, Söderhäll K, 2004. The prophenoloxidase‐activating system in invertebrates. Immunol Rev 198: 116-126. https://doi.org/10.1111/j.0105-2896.2004.00116.x

Cito A, Mazza G, Strangi A, Benvenuti C, Barzanti GP, Dreassi E et al., 2014. Characterization and comparison of Metarhizium strains isolated from Rhynchophorus ferrugineus. FEMS Microbiol Lett 355: 108-115. https://doi.org/10.1111/1574-6968.12470

Colovic MB, Krstic DZ, Lazarevic-Pasti TD, Bondzic AM, Vasic VM, 2013. Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11: 315-335. https://doi.org/10.2174/1570159X11311030006

Damayanthi B, Karunaratne S, 2005. Biochemical characterization of insecticide resistance in insect pests of vegetables and predatory ladybird beetles. J Natl Sci Found Sri Lanka 33: 115-122. https://doi.org/10.4038/jnsfsr.v33i2.2341

Dembilio O, Jacas JA, 2011. Basic bio-ecological parameters of the invasive Red Palm Weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae), in Phoenix canariensis under Mediterranean climate. Bull Entomol Res 101: 153-163. https://doi.org/10.1017/S0007485310000283

Dembilio O, Jacas JA, Llácer E, 2009. Are the palms Washingtonia filifera and Chamaerops humilis suitable hosts for the red palm weevil, Rhynchophorus ferrugineus (Col. Curculionidae)? J Appl Entomol 133: 565-567.. https://doi.org/10.1111/j.1439-0418.2009.01385.x

Dembilio O, Jaques JA, 2015. Biology and management of red palm weevil. In: Sustainable pest management in date palm: current status and emerging challenges. Springer, pp: 13-36. https://doi.org/10.1007/978-3-319-24397-9_2

Dembilio O, Quesada-Moraga E, Santiago-Álvarez C, Jacas JA, 2010a. Potential of an indigenous strain of the entomopathogenic fungus Beauveria bassiana as a biological control agent against the red palm weevil, Rhynchophorus ferrugineus. J Invertebr Pathol 104: 214-221. https://doi.org/10.1016/j.jip.2010.04.006

Dembilio O, Llácer E, Martínez de Altube MM, Jacas JA, 2010b. Field efficacy of imidacloprid and Steinernema carpocapsae in a chitosan formulation against the red palm weevil Rhynchophorus ferrugineus (Coleoptera: Curculionidae) in Phoenix canariensis. Pest Manag Sci 66: 365-370. https://doi.org/10.1002/ps.1882

Dubovskiy I, Grizanova E, Ershova N, Rantala M, Glupov V, 2011. The effects of dietary nickel on the detoxification enzymes, innate immunity and resistance to the fungus Beauveria bassiana in the larvae of the greater wax moth Galleria mellonella. Chemosphere 85: 92-96. https://doi.org/10.1016/j.chemosphere.2011.05.039

Dubovskiy I, Slyamova N, Kryukov VY, Yaroslavtseva O, Levchenko M, Belgibaeva A et al., 2012. The activity of nonspecific esterases and glutathione-S-transferase in Locusta migratoria larvae infected with the fungus Metarhizium anisopliae (Ascomycota, Hypocreales). Entomol Rev 92: 27-31. https://doi.org/10.1134/S0013873812010022

Ellman GL, Courtney KD, Andres Jr V, Featherstone RM, 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88-95. https://doi.org/10.1016/0006-2952(61)90145-9

El-Mergawy R, Al-Ajlan A, 2011. Red palm weevil, Rhynchophorus ferrugineus (Olivier): economic importance, biology, biogeography and integrated pest management. J Agric Sci Technol 1: 1-23.

El-Sabea AM, Faleiro J, Abo-El-Saad MM, 2009. The threat of red palm weevil Rhynchophorus ferrugineus to date plantations of the Gulf region in the Middle-East: An economic perspective. Outlooks Pest Manag 20: 131-134. https://doi.org/10.1564/20jun11

EPA, 1992. Probit analysis program used for calculating LC/EC values, version 1.5. http://www.epa.gov/nerleerd/stat2/probit.zip.

Etebari K, Bizhannia A, Sorati R, Matindoost L, 2007. Biochemical changes in haemolymph of silkworm larvae due to pyriproxyfen residue. Pestic Biochem Physiol 88: 14-19. https://doi.org/10.1016/j.pestbp.2006.08.005

Faleiro J, 2006. A review of the issues and management of the red palm weevil Rhynchophorus ferrugineus (Coleoptera: Rhynchophoridae) in coconut and date palm during the last one hundred years. Int J Trop Insect Sci 26: 135-154.

Ferry M, Gomez S, 2002. The red palm weevil in the Mediterranean area. Palms 46: 172-178.

Finney D, 1971. Probit analysis, Cambridge University Press, Cambridge, UK.

Fong J, Siti N, Wahizatul AA, 2018. Virulence evaluation of entomopathogenic fungi against the red palm weevil, Rhynchophorus ferrugineus (Coleoptera: Dryopthoridae). Malays Appl Biol J 47: 25-30.

Francardi V, Benvenuti C, Roversi PF, Rumine P, Barzanti G, 2012. Entomopathogenicity of Beauveria bassiana (Bals.) Vuill. and Metarhizium anisopliae (Metsch.) Sorokin isolated from different sources in the control of Rhynchophorus ferrugineus (Olivier) (Coleoptera Curculionidae). Redia 95: 49-55.

Ghazavi M, Avand-Faghih A, 2002. Isolation of two entomopathogenic fungi on red palm weevil, Rhynchophorus ferrugineus (Olivier) (Col., Curculionidae) in Iran. Appl Entomol Phytopathol 9: 44-45.

Giblin-Davis R, 2001. Insect borers in palms. In: Insects on palms; Howard FW et al. (eds). CABI Publications, Wallingford, UK. pp: 267-304. https://doi.org/10.1079/9780851993263.0267

Giblin-Davis RM, Faleiro JR., Jacas JA, Peña JE, Vidyasagar PSPV, 2013. Biology and management of the red palm weevil, Rhynchophorus ferrugineus. In: Potential invasive pests of agric crops; Peña JE (ed), CABI, pp: 1-34. https://doi.org/10.1079/9781845938291.0001

Gindin G, Levski S, Glazer I, Soroker V, 2006. Evaluation of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana against the red palm weevil Rhynchophorus ferrugineus. Phytoparasitica 34: 370-379. https://doi.org/10.1007/BF02981024

Gopalakrishnan S, Chen FY, Thilagam H, Qiao K, Xu WF, Wang KJ, 2011. Modulation and interaction of immune-associated parameters with antioxidant in the immunocytes of crab Scylla paramamosain challenged with lipopolysaccharides. Evid Based Comp Altern Med 824962. https://doi.org/10.1155/2011/824962

Güerri‐Agulló B, Gómez‐Vidal S, Asensio L, Barranco P, Lopez‐Llorca LV, 2010. Infection of the red palm weevil (Rhynchophorus ferrugineus) by the entomopathogenic fungus Beauveria bassiana: a SEM study. Microsc Res Tech 73: 714-725.

Hussain A, Rizwan-ul-Haq M, Al-Jabr AM, 2013. Red palm weevil: Understanding the fungal disease mechanism and host defense. In: Microbial pathogens and strategies for combating them: Science, Technology and Education; Formatex Research Center: Badajoz, Spain, pp: 1278-1286.

Hussain A, Rizwan-ul-Haq M, Al-Ayedh H, M Al-Jabr AM, 2014. Mycoinsecticides: potential and future perspective. Rec Pat Food Nutr Agric 6: 45-53. https://doi.org/10.2174/2212798406666140613113905

Hussain A, Rizwan-ul-Haq M, Al-Ayedh H, Ahmed S, Al-Jabr AM, 2015. Effect of Beauveria bassiana infection on the feeding performance and antioxidant defence of red palm weevil, Rhynchophorus ferrugineus. Biocontrol 60: 849-859. https://doi.org/10.1007/s10526-015-9682-3

Jun Z, Dunlun S, Jianxin C, 2003. Physiological and biochemical changes of the silkworm, Bombyx mori infected by Cordyceps militaris. Acta Entomol Sinica 46: 674-678.

Kawachi I, Fujieda T, Ujita M, Ishii Y, Yamagishi K, Sato H et al., 2001. Purification and properties of extracellular chitinases from the parasitic fungus Isaria japonica. J Biosci Bioeng 92: 544-549. https://doi.org/10.1016/S1389-1723(01)80313-3

Kliot A, Ghanim M, 2012. Fitness costs associated with insecticide resistance. Pest Manag Sci 68: 1431-1437. https://doi.org/10.1002/ps.3395

Kono Y, Tomita T, 2006. Amino acid substitutions conferring insecticide insensitivity in Ace-paralogous acetylcholinesterase. Pestic Biochem Physiol 85: 123-132. https://doi.org/10.1016/j.pestbp.2005.12.002

Kontodimas D, Vassiliou V, 2015. Entomopathogenic fungi for the control of red palm weevil Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). 16th Panhellenic Entomological Conference. https://www.researchgate.net/publication/301634447.

Litchfield JJ, Wilcoxon F, 1949. A simplified method of evaluating dose-effect experiments. J Pharmacol Exp Ther 96: 99-113.

Liu W, Xie Y, Xue J, Zhang Y, Zhang X, 2011. Ultrastructural and cytochemical characterization of brown soft scale Coccus hesperidum (Hemiptera: Coccidae) infected by the Lecanicillium lecanii (Ascomycota: Hypocreales). Micron 42: 71-79. https://doi.org/10.1016/j.micron.2010.07.011

Llácer E, Dembilio O, Jacas J, 2010. Evaluation of the efficacy of an insecticidal paint based on chlorpyrifos and pyriproxyfen in a microencapsulated formulation against Rhynchophorus ferrugineus (Coleoptera: Curculionidae). J Econ Entomol 103: 402-408. https://doi.org/10.1603/EC09310

Lopes RB, Michereff-Filho M, Tigano MS, Neves P, Lopez EL, Fancelli M, da Silva JP, 2011. Virulence and horizontal transmission of selected Brazilian strains of Beauveria bassiana against Cosmopolites sordidus under laboratory conditions. Bull Insectol 64: 201-208.

Manachini B, Lo Bue P, Peri E, Colazza S, 2009. Potential effects of Bacillus thuringiensis against adults and older larvae of Rhynchophorus ferrugineus. IOBC/wprs Bull 45: 239-242.

Müller P, Donnelly MJ, Ranson H, 2007. Transcription profiling of a recently colonised pyrethroid resistant Anopheles gambiae strain from Ghana. BMC Genom 8: 1-12. https://doi.org/10.1186/1471-2164-8-36

Naeem A, Freed S, Akmal M, 2020. Biochemical analysis and pathogenicity of entomopathogenic fungi to Diaphorina citri Kuwayama (Hemiptera: Liviidae). Entomol Res 50: 245-254. https://doi.org/10.1111/1748-5967.12434

Nussenbaum A, Lecuona R, 2012. Selection of Beauveria bassiana sensu lato and Metarhizium anisopliae sensu lato isolates as microbial control agents against the boll weevil (Anthonomus grandis) in Argentina. J Invertebr Pathol 110: 1-7. https://doi.org/10.1016/j.jip.2012.01.010

Sabry K, Abdel-Raheem M, El-Fatih MM, 2011. Efficacy of the entomopathogenic fungi; Beauverai bassiana and Metarhizium anisopliae on some insect pests under laboratory conditions. Egyp J Biol Pest Control 21: 33-38.

Serebrov V, Gerber O, Malyarchuk A, Martemyanov V, Alekseev A, Glupov V, 2006. Effect of entomopathogenic fungi on detoxification enzyme activity in greater wax moth Galleria mellonella L. (Lepidoptera, Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. Biol Bull 33: 581-586. https://doi.org/10.1134/S1062359006060082

Sewify G, Fouad S, 2006. Integrated control of red palm weevil Rhynchophorus ferrugineus (Coleoptera: Curculionidae). J Agric Sci Mansoura Univ 31: 2415-2426. https://doi.org/10.21608/jppp.2006.235206

Shaju S, Kumar R, Gokulapalan C, 2003. Occurrence of Beauveria sp. on red palm weevil, Rhynchophorus ferrugineus (Oliv.) of coconut. Insect Environ 9: 66-67.

Singh S, Rethinam P, 2005. Trapping-a major tactic of BIPM strategy of palm weevils. Cord 21: 34-60. https://doi.org/10.37833/cord.v21i01.401

Sokolova YY, Sundukov O, 1999. Inhibition of esterase activity as a property of microsporidial pathogenesis in cricket Gryllus bimaculatus. Parazitologiya 33: 527-537.

Song Z, Feng L, Jing Y, 2002. Changes of some biochemical estimates in the hemolymph and body wall of Dendrolimus punctatus infected by Metarhizium anisopliae. China J Appl Entomol 39: 297-300.

Vidhya D, Rajiv P, Padmanabhan N, 2016. Impact of entomopathogenic fungal infection on the detoxifying enzyme in cotton leaf worm Spodoptera litura (Fabricius). Int J Pharma Bio Sci 7: 943-948. https://doi.org/10.22376/ijpbs.2016.7.4.b943-948

Xu J, Xu X, Shakeel M, Li S, Wang S, Zhou X, et al., 2017. The entomopathogenic fungi Isaria fumosorosea plays a vital role in suppressing the immune system of Plutella xylostella: RNA-Seq and DGE analysis of immunity-related genes. Front Microbiol 8: 1421-1434. https://doi.org/10.3389/fmicb.2017.01421

Yasin M, Wakil W, Ghazanfar MU, Qayyum MA, Tahir M, Bedford GO, 2019. Virulence of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae against red palm weevil, Rhynchophorus ferrugineus (Olivier). Entomol Res 49: 3-12. https://doi.org/10.1111/1748-5967.12260

Yu Y, Cao Y, Xia Y, Liu F, 2016. Wright Giemsa staining to observe phagocytes in Locusta migratoria infected with Metarhizium acridum. J Invertebr Pathol 139: 19-24. https://doi.org/10.1016/j.jip.2016.06.009

Published
2022-08-05
How to Cite
Ahmed , R., Freed, S., Naeem, A., Akmal, M., & Dietrich, C. H. (2022). Metarhizium anisopliae and Isaria fumosorosea challenge the survival and immunity of the palm weevil, Rhynchophorus ferrugineus Olivier. Spanish Journal of Agricultural Research, 20(3), e1004. https://doi.org/10.5424/sjar/2022203-18979
Section
Plant protection