Abstract
The efficiency of four species of wax degrading bacteria, Serratia marcescens (Bizio) (Enterobacterales:Yersiniaceae), Pseudomonas putida (Trevisan) (Pseudomonadales: Pseudomonadaceae), Bacillus subtilis (Ehrenberg) (Bacillales:Bacillaceae) and Bacillus cereus (Frankland & Frankland) (Bacillales:Bacillaceae) for the management of a major citrus pest, the mealybug, Planococcus citri (Green) (Hemiptera:Pseudococcidae) was evaluated. The degrading ability of the bacteria, isolated from cadavers of P. citri was assessed in vitro on wax extracted from the mealybug, paraffin wax and low-density polyfilm along with lipase activity. Except B. cereus, all bacteria showed significant lethal and debilitating effects against P. citri in laboratory bioassays. Even though, we did not observe any lethal effect on 1st and 2nd instar nymphs, in the latter instars mortality rate could reach as high as 70.0% in case of S. marcescens. Adults that survived bacterial treatments had significantly reduced female longevity, fecundity and adult formation. In greenhouse trail conducted under controlled conditions, it was found that S. marcescens was the most promising bacteria in managing P. citri population after 14 days of application causing around 36.5% mortality of crawlers coupled with a significant reduction in the wax content and weight of mealybug. However, its application followed by a single spray of half a dose of chlorpyrifos at weekly intervals further enhanced the mortality rate up to 54.0%. Therefore, we conclude that sequential application of S. marcescens followed by a single spray of a half a dose of insecticide is effective for management of the P. citri.
Similar content being viewed by others
References
Abbas G, Arif MJ, Saeed S (2005) Systematic status of new species of genus Phenacoccus cockerell (Pseudococcidae), a serious pest of cotton Gossypium Hirsutum L. in Pakistan. Pak Entomol 27:83–84
Abbas G, Arif MJ, Muhammad A, Muhammad A, Shafqat S (2010) Host plants distribution and overwintering of cotton mealybug (Phenacoccus solenopsis; Hemiptera: Pseudococcidae). Int J Agric Biol 12(3):421–425
Ackonor JB (2002) Current levels of incidence of parasitism and predation in Planococcus citri Risso (Homoptera: Pseudococcidae) in Ghanaian cocoa (Theobroma cacao L.) farms. Int J Trop Insect Sci 22(2):105–112
Arunkumar N, Gulsar Banu J, Gopalakrishnan N, Prakash AH (2017) Wax degrading bacteria: scope and applications in agriculture. Int J Curr Microbiol Appl Sci 6(2):649–664
Awasthi S, Srivastava N, Singh T, Tiwary D, Mishra PK (2017) Biodegradation of thermally treated low density polyethylene by fungus Rhizopus oryzae NS 5. Biotech 7(1):73
Bennett JW, Bentley R (2000) Seeing red: the story of prodigiosin. Adv Appl Microbiol 47:1–32
Bushra S, Shad SA, Khan HAA, Muhammad A, Masood E, Afzal MBS (2014) Resistance in the mealybug Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) in Pakistan to selected organophosphate and pyrethroid insecticides. Crop Prot 66:29–33
Cid M, Pereira S, Segura A, Cabaleiro C (2006) Monitoring of the population of Planococcus citri Risso (Hemiptera: Pseudococcidae) in a vineyard in Ríasbaixas (Galicia). Bol Serv Plagas 32(3):339–344
Cloyd RA, Lindquist RK (2001) Tips on managing problems in interior plantscapes. O. F. A. Services Inc., Columbus
Daane KM, Almeida RP, Bell VA, Walker JT, Botton M, Fallahzadeh M, Mani M, Miano JL, Sforza R, Walton VM, Zaviezo T (2012) Biology and management of mealybugs in vineyards. In: Bostanian NJ, Vincent C, Isaacs R (eds) Arthropod management in vineyards. Springer, Dordrecht, pp 271–307
De Sousa ALV, Costa MB, Souza B, Santa-Cecília LVC, Lima RR (2018) Host preference and biology of two cryptic species, Planococcus citri (Risso) and Planococcus minor (Maskell) (Hemiptera: Pseudococcidae). Sci Agrar 19(2):71–77
Downie DA, Gullan PJ (2004) Phylogenetic analysis of mealybugs (Hemiptera: Coccoidea: Pseudococcidae) based on DNA sequences from three nuclear genes, and a review of the higher classification. Syst Entomol 29(2):238–260
Fairolniza MS, Leow TC, Mukred AD, Bakar AS, Basri M, Rahman RNZRA (2007) Production of lipase by Bacillus sp. strain L2: nutritional and physical factors. J Basic Microbiol 47:406–412
Fatima H, Khan N, Rehman AU, Hussain Z (2014) Production and partial characterization of lipase from Pseudomonas putida. J Ferment Technol 4:1000112
Franco JC, Zada A, Mendel Z (2009) Novel approaches for the management of mealybug pests. In: Ishaaya I, Horowitz A (eds) Biorational control of arthropod pests. Springer Science and Business Media, Dordrecht, pp 233–278
Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GB (1981) Manual of methods for general bacteriology. American Society of Microbiology, Washington
Hall WJ (1926) The Hibiscus mealybug (Phenacoccus hirsutus, Green) in Egypt in 1925 with notes on the introduction of Cryptolaemus montrouzieri. Bulletin 70, Ministry of agriculture, Egypt.
Holt JG (1994) Bergey’s manual of determinative bacteriology. Williams & Wilkins, Baltimore
Jadhav RG, Madane NP, Kathamale DK (1996) Record of soybean as a new host in India for citrus mealybug. Insect Environ 2(3):90–100
Khan AM, Ashfaq M, Kiss Z, Khan AA, Mansoor S, Falk BW (2013) Use of recombinant tobacco mosaic virus to achieve RNA interference in plants against the citrus mealybug, Planococcus citri (Hemiptera: Pseudococcidae). PLoS ONE 8(9):e73657
Kulkarni SR, Patil SK (2013) Efficacy of different biopesticides and insecticides against mealybugs on custard apple. Pest Manag Hortic Ecosyst 19(1):113–115
Laflin HM, Parrella MP (2004) Developmental biology of citrus mealybug under conditions typical of California rose production. Ann Entomol Soc Am 97(5):982–988
Lopes FSC, Oliveira JVD, Oliveira JEDM, Oliveira MDD, Souza AMD (2019) Host plants for mealybugs (Hemiptera: Pseudococcidae) in grapevine crops. Pesqui Agropecu Trop 149:e54421
Marks GS, Bogorad L (1960) Studies on the biosynthesis of prodigiosin in Serratia marcescens. PNAS 46:25–28
Meyerdirk DE, Warkentin R, Attavian B, Gersabeck E, Francis A, Adams M, Francis G (1998) Biological control of the pink hibiscus mealybug project manual. United States Department of Agriculture, Washington
Miller DR, Williams DJ (1997) A new species of mealybug in the genus Pseudococcus (Homoptera: Pseudococcidae) of quarantine importance. Proc Entomol Soc Wash 99:305–311
Nandakumar R, Babu S, Viswanathan R, Sheel J, Raguchander T, Samiyappan R (2001) A new bio-formulation containing plant growth promoting rhizobacterial mixture for the management of sheath blight and enhanced grain yield in rice. BioControl 46:493–510
Narayanan K (2004) Insect defence: its impact on microbial control of insect pests. Curr Sci 86(6):800–814
Nawani NN, Kapadnis BP (2003) Chitin degrading potential of bacteria from extreme and moderate environment. Indian J Exp Biol 41:248–254
Okoye AU, Chikere CB, Okpokwasili GC (2019) Characterization of potential paraffin wax removing bacteria for sustainable biotechnological application. In: SPE Nigeria annual international conference and exhibition. Society of petroleum engineers. https://doi.org/10.2118/198799-MS
Patil CD, Patil SV, Salunke BK, Salunkhe RB (2011) Prodigiosin produced by Serratia marcescens NMCC46 as a mosquito larvicidal agent against Aedes aegypti and Anopheles stephensi. Parasitol Res 109(4):1179–1187
Perscott MP, Harley SA (2005) Microbiology. McGraw Hill, New York
Rasheed M, Bushra S, Tariq M (2014) Use and impact of insecticides in mealybug control. J Adv Biol 1(2):1–11
Sakthipriya N, Doble M, Sangwai JS (2015) Biosurfactant from Pseudomonas species with waxes as carbon source–their production, modeling and properties. J Ind Eng Chem 31:100–111
Salunkhe RB, Patil CD, Salunke BK, Rosas-García NM, Patil SV (2013) Effect of wax degrading bacteria on life cycle of the pink hibiscus mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae). BioControl 58(4):535–542
Sartiami D, Saptayanti N, Syahputra E, Mardiasih WP (2020) Mealybugs (Hemiptera: Pseudococcidae) Associated with dragon fruit in Indonesia. In: International conference and the 10th congress of the Entomological Society of Indonesia. Atlantis Press pp. 29–34.
Sikorowski P, Lawrence AM (1998) Transmission of Serratia marcescens (Enterobacteriaceae) in adult Heliothis virescens (Lepidoptera: Noctuidae) laboratory colonies. Biol Control 12(1):50–55
Sontakke PP, Chowdhury S (2015) Biological control of mealybugs on important horticultural crops at chittoor district in Andhra Pradesh. India J Entomol Res 39(4):327–331
Tanwar RK, Jeyakumar P, Monga D (2007) Mealybugs and their management. Bulletin 19, National centre for integrated pest management LBS building, Pusa campus, New Delhi, India.
Tena A, García-Bellón J, Urbaneja A (2017) Native and naturalized mealybug parasitoids fail to control the new citrus mealybug pest Delottococcus aberiae. J Pest Sci 90(2):659–667
Tielen P, Rosenau F, Wilhelm S, Jaeger KE, Flemming HC, Wingender J (2010) Extracellular enzymes affect biofilm formation of mucoid Pseudomonas aeruginosa. Microbiology 156:2239–2252
Toharisman A, Suhartono MT, Spindler-Barth M, Hwang JK, Pyun YR (2005) Purification and characterization of a thermostable chitinase from Bacillus licheniformis Mb-2. World J Microbiol Biotechnol 21(5):733–738
Xie Y, Zheng L (2002) The chemical composition of waxes secreted by a scale insect Eriopeltis festucae (Homoptera: Coccoidea). Acta Sci Nat Univ Sunyatseni 35(1):1–6
Yesuf SN (2020) Population dynamics of cotton mealybug, Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae) and its major natural enemies in middle awash, Ethiopia. PhD dissertation, Hawassa University.
Acknowledgements
We thank Dr. Paul Rude (University of California, Berkeley, USA) and Dr. Curtis Takahashi (California Department of Food and Agriculture) for professional editing of the manuscript. Our sincere thanks are also due to Dr. Robert Zuparko (Department of Entomology, California Academy of Sciences) and Dr. Emmanuelle Jousselin (Biology Center for Population Management, France) for technical and English editing of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
This article does not contain any studies with human participants or animals performed by any of the authors.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Handling Editor: Éverton Kort Kamp Fernandes
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gupta, R.K., Kour, R., Gani, M. et al. Potential of wax degrading bacteria for management of the citrus mealybug, Planococcus citri. BioControl 67, 49–61 (2022). https://doi.org/10.1007/s10526-021-10120-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-021-10120-8