Ceratitis capitata Wiedemann (Diptera: Tephritidae) in Moroccan Citrus orchards: Chemical and Sustainable Control Methods and Priorities for Future Research doi.org/10.26538/tjnpr/v5i10.2
Main Article Content
Abstract
The Mediterranean fruit fly (Ceratitis capitata) infects fruits from over 300 plant species, causing substantial economic losses amounting to millions of dollars annually. Though it has its origin in the Mediterranean basin, it has spread to Asia, Europe, Central and South America, Africa, Australia, etc. Its control in Morocco has been principally based on chemical sprays. The review aims to provide information on control methods of Ceratitis capitata, mainly in citrus orchards in Morocco. Relevant literature was sourced from different search engines: Google scholar, science direct, PubMed, etc. The article highlighted the principal findings of previous studies, discussed current control methods, and proposed new innovative research and sustainable approaches to control medflies. Setting up an integrated long-term ecological monitoring program in Morocco and different African countries and incorporating new technologies into monitoring programs are urgently needed to fight this devastating pest. These programs must consider the climate conditions, phenology, infestation rates, and propagation speed of pests. Other methods include new organic pests and trapping, sterile insect technique (SIT), parasitoid enemies such as Diachasmimorpha longicaudata, pathogens like Beauveria bassiana, and introducing a self-limiting genetic method. These fundamental elements are suggested to control pests, respect the environment and public health.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Mazih A. Status of citrus IPM in the southern Mediterranean basin Morocco, North Africa. Acta Hortic. 2015; 1065(1964):1097-1104.
Afechtal M, Djelouah K, ocuzza G, D’Onghia AM. Large Scale Survey of Citrus Tristeza Virus (CTV) and Its Aphid Vectors in Morocco. Acta Hortic. 2015; 1065(1963):753-757.
Tudela-Marco L, Álvarez-Coque JMG, Martínez-Gómez V. Issues in Trade Liberalisation in Southern and Eastern Mediterranean Countries. Switzerland: Springer, Cham; 2015; 171-196p.
Montaigne E, Hadad-Gauthier FE, Khefifi L. Challenges in Citrus Market Chains in Tunisia and Morocco. Sustain Agric Dev [online]. 2015 [cited 2021 sept 11];227‑53. Available from: http://link.springer.com/chapter/10.1007/978-3-319-17813-4_9
Sraïri MT. New challenges for the moroccan agricultural sector to cope with local and global changes. Moroc Environ Soc Econ Issues 21st Century. 2017; 10(2):165-188.
Oubelkacem A, Scardigno A, Choukr-Allah R. Treated Wastewater Reuse on Citrus in Morocco: Assessing the Economic Feasibility of Irrigation and Nutrient Management Strategies. Integr Environ Assess Manag. 2020; 16(6):898-909.
Mac Loughlin TM, Peluso ML, Etchegoyen MA, Alonso LL, de Castro MC, Percudani MC, Marino Damián J. G. Pesticide residues in fruits and vegetables of the argentine domestic market: Occurrence and quality. Food Contr. 2018; 93(24):129-138.
Franco JC, Suma P, Da Silva EB, Blumberg D, Mendel Z. Management strategies of mealybug pests of citrus in Mediterranean countries. Phytoparasitica. 2004; 32(5):507-522.
Masui S, Katayama H, Kaneko S. Status and use of biological control of insect pests in citrus IPM. Jpn J Appl Entomol Zool. 2018; 62(3):137-148.
Urbaneja A, Grout TG, Gravena S, Wu F, Cen Y, Stansly PA. Citrus pests in a global world. The Genus Citrus. Amsterdam: Elsevier Inc. 2020; 333-348p.
Abad-Moyano R, Pina T, Dembilio Ó, Ferragut F, Urbaneja A. Survey of natural enemies of spider mites (Acari: Tetranychidae) in citrus orchards in eastern Spain. Exp Appl Acarol. 2009; 47(1):49-61.
Jacas JA and Urbaneja A. Integrated Management of Arthropod Pests and Insect Borne Diseases. Integr Manag Arthropod Pests Insect Borne Dis. 2010; 2(5):61-62.
Estrella SM, Arnaiz A, Rosa-Diaz I, González-Melendi P, Romero-Hernandez G, Ojeda-Martinez DA, Garcia A, Contreras E, Martinez M, Diaz I. Plant defenses against tetranychus urticae: Mind the gaps. Plants. 2020; 9(4):1-16.
Tena A and García-Marí F. Current situation of citrus pests and diseases in the Mediterranean Basin. IOBC-wprs Bull. 2011; 62(6):365-378.
Krasnov H, Cohen Y, Goldshtein E, Mendelsohn O, Silberstein M, Gazit Y, Blank L. The effect of local and landscape variables on Mediterranean fruit fly dynamics in citrus orchards utilizing the ecoinformatics approach. J Pest Sci. 2019; 92(2):453-463.
Rather BA, Mir MM, Iqbal U, Mir SA. Integrated Pest Management of Stone Fruits. In: Production Technology of Stone Fruits. Singapore: Springer; 2021; 397-422p.
Japan Exports of Fruit & Vegetables | 1983-2021 Data | 2022-2023 Forecast | Historical [online]. 2021 [cited 6 April 2021]. Available on: https://tradingeconomics.com/japan/exports-of-fruitvegetable
Boulahia-Kheder S. Review on major fruit flies (Diptera: Tephritidae) in North Africa: Bio-ecological traits and future trends. Crop Prot. 2021; 140(2):1-10.
Rachid E and Ahmed M. Current status and future prospects of Ceratitis capitata wiedemann (Diptera: Tephritidae) control in Morocco. J Entomol. 2018; 15(1):47-55.
Magaña C, Hernández-Crespo P, Ortego F, Castañera P. Resistance to malathion in field populations of Ceratitis capitata. J Econ Entomol. 2007;100(6):1836-1843.
Hammouti N, Griebeler EM, Barr N, Mazih A, Seitz A. Extension of the pathway analysis for the medfly (Ceratitis
capitata): mtDNA variation among Morocco populations. Ext Pathw Anal Medfly Ceratitis capitata MtDNA Var Moroc Popul. 2011; 62(3):163-176.
Imoulan A, Alaoui A, Meziane A El. Natural occurrence of soil-borne entomopathogenic fungi in the Moroccan
Endemic Forest of Argania spinosa and their pathogenicity to Ceratitis capitata. World J Microbiol Biotechnol. 2011; 27(11):2619-2628.
Maatala N, Lebailly P, Benabdellah M, Dehhaoui M. The Mode of Management of Irrigation Water Service: A Technical Efficiency Determinant of Citrus Farms in the Souss-Massa Perimeter. Tropicultura. 2019; 37(3):1-19.
Thomas MC, Heppner JB, Woodruff RE, Weems HV, Steck GJ, Fasulo TR. Mediterranean Fruit Fly, Ceratitis capitata(Wiedemann) (Diptera: Tephritidae). [online]. 2012 [cited 6 April 2021]. Available on: http://creatures.ifas.ufl.edu
Rachid E and Ahmed M. Current status and future prospects of Ceratitis capitata wiedemann (Diptera: Tephritidae)
control in Morocco. J Entomol. 2018; 15(1):47-55.
Jemâa JMB, Tersim N, Toudert KT, Khouja ML. Insecticidal activities of essential oils from leaves of Laurus nobilis L. from Tunisia, Algeria and Morocco, and comparative chemical composition. J Stored Prod Res. 2012; 48(1):97-104.
Matzrafi M. Climate change exacerbates pest damage through reduced pesticide efficacy. Pest Manag Sci. 2019; 75(1):9-13.
Reddy PP. Agro-ecological approaches to pest management for sustainable agriculture. (ed.). Switzerland AG: Springer; 2017; 1-339p.
Rezaei R, Safa L, Ganjkhanloo MM. Understanding farmers’ ecological conservation ehavior regarding the use of integrated pest management- an application of the technology acceptance model. Glob Ecol Conserv. 2020; 22(2):1-18.
Hallouti A, Zahidi A, Bouharroud R, El Mousadik R, Ait Ben Aoumar A, Boubaker H. Diversity of Entomopathogenic Fungi in Argane Forest Soil and Their Potential to Manage Mediterranean Fruit Fly (Ceratitis capitata). J Pharm Pharmacol. 2017; 5(10):746-754.
Samri SE, Baz M, Ghalbane I, El Messoussi S, Zitouni A, El Meziane A, and Barakate M. Insecticidal activity of a Moroccan strain of Streptomyces phaeochromogenes LD-37 on larvae, pupae and adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Bull Entomol Res. 1 avr 2017; 107(2):217-224.
Insecticidal activity of a Moroccan strain of Streptomyces phaeochromogenes LD-37 on larvae, pupae and adults of
the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). [online]. 2017 [cited 2021 April 6]. Available on: https://pubmed.ncbi.nlm.nih.gov/28276307/
El-Sayed AM, Suckling DM, Wearing CH, Byers JA. Potential of Mass Trapping for Long-Term Pest Management and Eradication of Invasive Species. J Econ Entomol. 2009; 99(5):1550–1564.
Asadi R, Elaini R, Lacroix R, Ant T, Collado A, Finnegan L, Siciliano P, Mazih A and Koukidou M. Preventative releases of self-limiting Ceratitis capitata provide pest suppression and protect fruit quality in outdoor netted cages. Int J Pest Manag. 2020; 66(2): 182-193.
de Bon H, Huat J, Parrot L, Sinzogan A, Martin T, Malézieux E, Deletre E, Bonafos R, Simon S, And Ngouajio M. Pesticide risks from fruit and vegetable pest management by small farmers in sub-Saharan Africa. A review. Agron Sustain Dev. 2014; 34(4):723-736.
Berni I, Menouni A, Ghazi El I, Duca RC, Kestemont MP, Godderis L, and El Jaafari S. Understanding farmers’ safety
behavior regarding pesticide use in Morocco. Sustain Prod Consum. 2021; 25(1):471-483.
de Mendoza AH, Álvarez A, Michelena JM, González P, Cambra M. Working Group Integrated Control in Citrus Fruit Crops. International Conference on Integrated Control in Citrus Fruit Crops Proceedings of the meeting. Int Organ Biol Integr Control. 2008; 38(November 2007):225-232.
Papanicolaou A, Schetelig MF, Arensburger P, Atkinson PW, Benoit JB, Bourtzis K, Castañera P, Cavanaugh JP, Chao H, Childers C, Curril I, Dinh H, Doddapaneni H, Dolan A, Dugan S, Friedrich M, Gasperi G, Geib S, Georgakilas G, Gibbs A, Giers SD, Gomulski LM, M González-Guzmán, Guillem-Amat A, Han Y, Hatzigeorgiou AG, Hernández-Crespo P, Hughes ST, Jones JW, Karagkouni D, Koskinioti P, Lee SL, Malacrida AR, Manni M, Mathiopoulos K, Meccariello A, Murali SC, urphy
TD, Muzny DM, Oberhofer G, Ortego F, Paraskevopoulou MD, Poelchau M, Qu J, Reczko M, Robertson HM, Rosendale AJ, Rosselot AE, Saccone G, Salvemini M, Savini G, Schreiner P, Scolari F, Siciliano P, Sim SB, Tsiamis G, Ureña E, Vlachos IS, Werren JH, Wimmer EA, Worley KC, Zacharopoulou A, Richards S, Handler AM. The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species. Genome Biol. 2016; 17(1):1-31.
Yuval B, Kaspi R, Shloush S, Warburg MS. Nutritional reserves regulate male participation in Mediterranean fruit
fly leks. Ecol Entomol. 1998; 23(2):211-215.
Medflies S. Breakfast of Champions or Kiss of Death? Survival and Sexual Performance of Protein-Fed, Sterile Mediterranean Fruit Flies (Diptera: Tephritidae). 2000; 90(1):115-122.
Chapman T, Miyatake T, Smith HK, Partridge L. Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proc R Soc B Biol Sci. 1998; 265(1408):1879-1894.
Gomulski LM, Dimopoulos G, Xi Z, Scolari F, Gabrieli P. Transcriptome Profiling of Sexual Maturation and Mating in the Mediterranean Fruit Fly, Ceratitis capitata. PLoS ONE. 2012; 7(1):1-10.
Benelli G, Rizzo R, Zeni V, Govigli A, Samková A, Sinacori M, loVerde G, Pavela R, Cappellaci L, Petrelli R Spinozzi E, Morshedloo MR, Maggi F, Canale A. Carlina acaulis and Trachyspermum ammi essential oils formulated in protein baits are highly toxic and reduce aggressiveness in the medfly, Ceratitis capitata. Ind Crops Prod. 2021; 161(3):1-10.
Rachid E and Ahmed M. Current status and future prospects of Ceratitis capitata wiedemann (Diptera: Tephritidae)
control in Morocco. J Entomol. 2018; 15(1):47-55.
Yahia EM, Jones RW, Thomas DB. Quarantine pests of tropical and subtropical fruits and their control. In: Postharvest Biology and Technology of Tropical and Subtropical Fruits. (1st ed.). Sawston: Woodhead Publishing; 2011; 224-287 p.
Jacas JA, Karamaouna F, Zappalà L. Integrated Management of Arthropod Pests and Insect Borne Diseases. Integr Manag Arthropod Pests Insect Borne Dis. (1st ed.). Paris: Lavoisier 2010. 366 p.
Moore SD and Duncan LW. Microbial Control of Insect and Mite Pests of Citrus. Microbial Control of Insect and Mite Pests: From Theory to Practice. (2nd ed.). Amsterdam: Elsevier Inc. 2017. 283-298 p.
Jaronski ST. Ecological factors in the inundative use of fungal entomopathogens. Bio Contr. 2010; 55(1):159-185.
Peña JE, Hoddle MS, Aluja M, Palevsky E, Ripa R, Wysoki M. Insect and mite pests. The avocado: botany, production
and uses. (2nd ed.). Florida: CABI. 2013; 423-488 p.
Garcia FRM, Ovruski SM, Suárez L, Cancino J, Liburd OE. Biological control of tephritid fruit flies in the Americas and Hawaii: A review of the use of parasitoids and predators. Insects. 2020; 11(10):1-32.
de Pedro L, Tormos J, Harbi A, Ferrara F, Sabater-Muñoz B, Asís JD, Beitia F. Combined use of the larvo-pupal parasitoids Diachasmimorpha longicaudata and Aganaspis daci for biological control of the medfly. Ann Appl Biol.
; 174(1):40-50.
Di Ilio V and Cristofaro M. Polyphenolic extracts from the olive mill wastewater as a source of biopesticides and their effects on the life cycle of the Mediterranean fruit fly Ceratitis capitata (Diptera, Tephriditae). Int J Trop Insect Sci. 2021; 41(1):359-366.
Mokrini F, Laasli SE, Benseddik Y, Joutei AB, Blenzar A, Lakhal H, Sbaghi M, Imren M, Özer G, Paulitz T, Lahlali R & Dababat AA. Potential of Moroccan entomopathogenic nematodes for the control of the Mediterranean fruit flyCeratitis capitata Wiedemann (Diptera: Tephritidae). Sci Rep. 2020; 10(1):1-11.
Hallouti A, Ait Hamza M, Zahidi A, Ait Hammou R, Bouharroud R, Ait Ben Aoumar A, Boubaker H. Diversity of entomopathogenic fungi associated with Mediterranean fruit fly (Ceratitis capitata (Diptera: Tephritidae)) in Moroccan Argan forests and nearby area: impact of soil factors on their distribution. BMC Ecol. 2020; 20(1):1-13.
García RLE. The Influence of Entrepreneurial Orientation, Innovation and Characteristics of Entrepreneurs on Business Performance in Wid Area. J Chem Inf Model. 2013; 53(9):1689-1699.
Grogan KA and Goodhue RE. Citrus growers vary in their adoption of biological control. California Agric. 2012; 66(1):29-36.
Benedict MQ. Sterile Insect Technique: Lessons from the Past. J Med Entomol. 2021; 58(5):1-6.
Mazih A and Debouzie D. Infestation rate of argan fruit (Argania spinosa) by the Mediterranean fruit fly (Ceratitis
capitata) in relation to phenology and maturation of the fruit. Entomol Exp Appl. 1996; 81(1):31-38.
Shahini S, Bërxolli A, Kokojka F. Effectiveness of bioinsecticides and mass trapping based on population fluctuations for controlling Tuta absoluta under greenhouse conditions in Albania. Heliyon. 2021; 7(1):1-7.
De Meyer M, Copeland RS, Wharton RA, McPheron BA, Barnes BN. On the geographic origin of the Medfly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Proc 6th Int Symp Fruit Flies Econ Importance. 2004;(May 2002):45-53.
Morocco Sterilizes the Mediterranean Fruit Fly [online]. [cited 2021 April 6]. available on: https://www.moroccoworldnews.com/2019/06/275841/morocco-sterilizes-the-mediterranean-fruit-fly/
Egziabher TBG, Edwards S. technogie of irradiatin citrus marocan. Afr Potential Ecol Intensif Agric. 2013; 53(9):1689-1699.
Harbouze R, Pellissier J-P, Rolland J-P, Khechimi W. Synthesis report on agriculture in Morocco [online]. 2019 [cited 2021 Sep 12] p. 104. Available from: https://hal.archives-ouvertes.fr/hal-02137637
Aloui O and Kenny L. The cost of compliance with SPS standards for Moroccan e ports : a case study. undefined [online]. 2005 [cited 2021 Sep 12]; Available from: https://www.semanticscholar.org/paper/The-cost-ofcompliance-with-SPS-standards-for-%3A-a-AlouiKenny/89fa138c8725c34f01f6448192a3d4aec94d8674
Assouguem A, Kara M, Mansouri I, Imtara H, Alzain MN, Mechchate H, Conte R, Squalli W, Farah A, Lazraq A. Evaluation of the effectiveness of spirotetramat on the diaspine scale parlatoria pergandii in citrus orchards. Agron. 2021;11(8):1-11.
Elaini R, Asadi R, Naish N, Koukidou M, Ahmed M. Evaluation of rearing parameters of a self-limiting strain of the mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Insects. 2020; 11(10):1-11.
Pereira R, Yuval B, Liedo P, Teal PEA, Shelly TE, McInnis DO, Hendrichs J. Improving sterile male performance in support of programmes integrating the sterile insect technique against fruit flies. J Appl Entomol. 2013; 137(SUPPL.1):178-190.
Yamada H, Vreysen MJ, Gilles JR, Munhenga G, Damiens DD. The effects of genetic manipulation, dieldrin treatment
and irradiation on the mating competitiveness of male Anopheles arabiensis in field cages. Malar J. 2014; 13(1):1-10.
Shelly TE, Whittier TS, Kaneshiro KY. Sterile insect release and the natural mating system of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Ann Entomol Soc Am. 1994; 87(4):470-481.
Lance DR, McInnis DO, Rendon P, Jackson CG. (Diptera: Tephritidae) in Field Cages in Hawaii and Guatemala. Ann Entomol Soc Am. 2000; 93(5):1179-1185.
Rendón P, McInnis D, Lance D, Stewart J. Medfly (Diptera:Tephritidae) genetic sexing: Large-scale field comparison of males-only and bisexual sterile fly releases in Guatemala. J Econ Entomol. 2004; 97(5):1547-1553.