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Distribution, abundance and natural enemies of the invasive tomato leafminer, Tuta absoluta (Meyrick) in Kenya

Published online by Cambridge University Press:  17 May 2021

G. Kinyanjui*
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), P. O. Box 30772-00100, Nairobi, Kenya Department of Biological Sciences, University of Embu, P.O. Box 6-60100, Embu, Kenya
F. M. Khamis
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), P. O. Box 30772-00100, Nairobi, Kenya
F. L. O. Ombura
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), P. O. Box 30772-00100, Nairobi, Kenya
E. U. Kenya
Affiliation:
Department of Biological Sciences, University of Embu, P.O. Box 6-60100, Embu, Kenya
S. Ekesi
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), P. O. Box 30772-00100, Nairobi, Kenya
S. A. Mohamed
Affiliation:
International Centre of Insect Physiology and Ecology (icipe), P. O. Box 30772-00100, Nairobi, Kenya
*
Author for correspondence: G. Kinyanjui, Email: [email protected]

Abstract

Tuta absoluta (Meyrick) has become a serious menace to sustainable production of tomato in Kenya. A survey was conducted between April 2015 and June 2016 to determine its distribution, abundance, infestation, and damage levels on tomato, and associated natural enemies. Trap counts of T. absoluta moths were recorded in all surveyed 29 counties, which indicated its nationwide distribution irrespective of altitude. Tuta absoluta was present in both open fields and greenhouses. The highest moth/trap/day was 115.38 ± 15.90. Highest leaf infestation was 92.22% and the highest number of mines and larvae per leaf were 3.71 ± 0.28 and 2.16 ± 0.45, respectively. Trap captures in terms of moth/trap/day were linearly and positively related to leaf infestations in open fields (R2 = 0.81) and greenhouses (R2 = 0.61). Highest fruits’ infestation and damage were 60.00 and 59.61%, respectively, while the highest number of mines per fruit was 7.50 ± 0.50. Nesidiocoris tenuis (Reuter) and Macrolophus pygmaeus (Rambur) were identified as predators of T. absoluta larvae. Nine species of larval parasitoids were recovered from infested foliage, with a combined parasitism of 7.26 ± 0.65%. Hockeria species was the most dominant (31.25%) and accounted for 12.88 ± 1.47% parasitism. Two species of larval parasitoids, Hockeria and Necremnus were obtained from sentinel plants with an average parasitism of 1.13 ± 0.25. The overall abundance and parasitism rates of recovered natural enemies were low to effectively control the field populations of T. absoluta. These findings form the basis of researching and developing effective and sustainable management strategies for the pest.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abbes, K and Chermiti, B (2011) Comparison of two marks of sex pheromone dispensers commercialized in Tunisia for their efficiency to monitor and to control by mass trapping Tuta absoluta under greenhouses. Tunisian Journal of Plant Protection 6, 133148.Google Scholar
Abbes, K and Chermiti, B (2012) Failure of the biological control of Tuta absoluta using the predator Nesidiocoris tenuis in a protected tomato crop: analysis of factors. IOBC/WPRS Bulletin 80, 231236.Google Scholar
Abbes, K, Biondi, A, Zappalà, L and Chermiti, B (2014) Fortuitous parasitoids of the invasive tomato leafminer Tuta absoluta in Tunisia. Phytoparasitica 42, 8592.CrossRefGoogle Scholar
Aigbedion-Atalor, PO, Mohamed, SA, Hill, MP, Zalucki, MP, Azrag, AG, Srinivasan, R and Ekesi, S (2020) Host stage preference and performance of Dolichogenidea gelechiidivoris (Hymenoptera: Braconidae), a candidate for classical biological control of Tuta absoluta in Africa. Biological Control 144, 104215.CrossRefGoogle Scholar
Allen, EA and Humble, LM (2002) Nonindigenous species introductions: a threat to Canada's forests and forest economy. Canadian Journal of Plant Pathology 24, 103110.CrossRefGoogle Scholar
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403410.CrossRefGoogle ScholarPubMed
Assaf, LH, Hassan, FR, Ismael, HR and Saeed, SA (2013) Population density of tomato leaf miner Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) under plastic houses conditions (b). IOSR Journal of Agriculture and Veterinary Science 5, 710.CrossRefGoogle Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 118.CrossRefGoogle Scholar
Benvenga, SR, Fernandes, OA and Gravena, S (2007) Decision making for integrated pest management of the South American tomato pinworm based on sexual pheromone traps. Horticultura Brasileira 25, 164169.CrossRefGoogle Scholar
Biondi, A, Guedes, RNC, Wan, F-H and Desneux, N (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annual Review of Entomology 63, 239258.CrossRefGoogle ScholarPubMed
Boualem, M, Allaoui, H, Hamadi, R and Medjahed, M (2012) Biologie et complexe des ennemis naturels de Tuta absoluta à Mostaganem (Algérie). EPPO Bulletin 42, 268274.CrossRefGoogle Scholar
Cely, LP, Cantor, F and Rodriguez, D (2010) Determination of levels of damage caused by different densities of Tuta absoluta populations (Lepidoptera: Gelechiidae) under greenhouse conditions. Agronomía Colombiana 28, 401411.Google Scholar
Centre for Agricultural and Biosciences International (CABI) (2020) Invasive Species Compendium; Tuta absoluta (tomato leafminer). Available at https://www.cabi.org/isc/datasheet/49260 (Accessed 7 August 2020).Google Scholar
Chermiti, B, Abbes, K, Aoun, M, Othmen, SB, Ouhibi, M, Gamoon, W and Kacem, S (2009) First estimate of the damage of Tuta absoluta (Povolny) (Lepidoptera: Gelechiidae) and evaluation of the efficiency of sex pheromone traps in greenhouses of tomato crops in the Bekalta region, Tunisia. African Journal of Plant Science and Biotechnology 3, 4952.Google Scholar
Dehliz, A and Guénaoui, Y (2015) Natural enemies of Tuta absoluta (Lepidoptera: Gelechiidae) in Oued Righ region, an arid area of Algeria. Academic Journal of Entomology 8, 7279.Google Scholar
Desneux, N, Wajnberg, E, Wyckhuys, KAG, Burgio, G, Arpaia, S, Narváez-Vasquez, CA, González-Cabrera, J, Ruescas, DC, Tabone, E, Frandon, J, Pizzol, J, Poncet, C, Cabello, T and Urbaneja, A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion, and prospect for biological control. Journal of Pest Science 83, 197215.CrossRefGoogle Scholar
Desneux, N, Luna, MG, Guillemaud, T and Urbaneja, A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. Journal of Pest Science 84, 403408.CrossRefGoogle Scholar
Doğanlar, M and Yiğit, A (2011) Parasitoid complex of the tomato leafminer, Tuta absoluta (Meyrick 1917), (Lepidoptera: Gelechiidae) in Hatay, Turkey. Kahramanmaraş Sütcü İmam Üniversitesi Doğa Bilimleri Dergisi 14, 2837.Google Scholar
European and Mediterranean Plant Protection Organization (EPPO) (2020) Tuta absoluta. EPPO global database. Available at https://gd.eppo.int/taxon/GNORAB/distribution (Accessed 7 August 2020).Google Scholar
Ferracini, C, Ingegno, BL, Navone, P, Ferrari, E, Mosti, M, Tavella, L and Alma, A (2012) Adaptation of indigenous larval parasitoids to Tuta absoluta (Lepidoptera: Gelechiidae) in Italy. Journal of Economic Entomology 105, 13111319.CrossRefGoogle ScholarPubMed
Ferracini, C, Bueno, VHP, Dindo, ML, Ingegno, BL, Luna, MG, Gervassio, NGS, Sánchez, NE, Siscaro, G, van Lenteren, JC, Zappalà, L and Tavella, L (2019) Natural enemies of Tuta absoluta in the Mediterranean basin, Europe, and South America. Biocontrol Science and Technology 29, 578609.CrossRefGoogle Scholar
Foba, CN, Salifu, D, Lagat, ZO, Gitonga, LM, Akutse, KS and Fiaboe, KKM (2016) Liriomyza leafminer (Diptera: Agromyzidae) parasitoid complex in different agroecological zones, seasons, and host plants in Kenya. Environmental Entomology 45, 357366.CrossRefGoogle ScholarPubMed
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294297.Google Scholar
Food and Agriculture Organization (FAO) (2020) FAOSTAT statistical database. Available at http://www.fao.org/faostat/en/#data/QC (Accessed 8 August 2020).Google Scholar
Gabarra, R, Arnó, J, Lara, L, Verdú, MJ, Ribes, A, Beitia, F, Urbaneja, A, Téllez, MM, Mollá, O and Riudavets, J (2014) Native parasitoids associated with Tuta absoluta in the tomato production areas of the Spanish Mediterranean Coast. Biocontrol 59, 4554.CrossRefGoogle Scholar
Galdino, TVS, Picanço, MC, Ferreira, DO, Silva, GAR, de Souza, TC and Silva, GA (2015) Is the performance of a specialist herbivore affected by female choices and the adaptability of the offspring? PLoS One 10, e0143389.CrossRefGoogle ScholarPubMed
Geurts, K, Mwatawala, M and De Meyer, M (2012) Indigenous and invasive fruit fly diversity along an altitudinal transect in Eastern Central Tanzania. Journal of Insect Science 12, 12.CrossRefGoogle ScholarPubMed
Gharekani, GH and Salek-Ebrahimi, H (2014) Evaluating the damage of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on some cultivars of tomato under greenhouse condition. Archives of Phytopathology and Plant Protection 47, 429436.CrossRefGoogle Scholar
Gomide, EVA, Vilela, EF and Picanço, M (2001) Comparison of sampling procedures for Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato crop. Neotropical Entomology 30, 697705.CrossRefGoogle Scholar
Han, P, Zhang, Y, Lu, Z, Wang, S, Ma, D, Biondi, A and Desneux, N (2018) Are we ready for the invasion of Tuta absoluta? Unanswered key questions for elaborating an Integrated Pest Management package in Xinjiang, China. Entomologia Generalis 38, 113125.CrossRefGoogle Scholar
Horticultural Crops Directorate (HCD) (2017) Horticulture Validated Report 2016–2017. Available at http://horticulture.agricultureauthority.go.ke/wp-content/uploads/2016/02/horticulture-validated-data-2016-2017.pdf.Google Scholar
Horticultural Crops Directorate (HCD) (2018) Horticulture Validated Report 2017–2018. Available at https://agricultureauthority.go.ke/index.php/statistics/statistics/category/13-horticulture-repository.Google Scholar
Kenya Agricultural & Livestock Research Organization (KALRO) (2014) Tomato leafminer (Tuta absoluta). KARI E-mimea plant clinic. https://www.kalro.org/emimi/sites/default/files/tomato_tuta.pdf.Google Scholar
Kinyanjui, G, Khamis, FM, Ombura, FLO, Kenya, EU, Ekesi, S and Mohamed, SA (2019) Infestation levels and molecular identification based on mitochondrial COI barcode region of five invasive Gelechiidae pest species in Kenya. Journal of Economic Entomology 112, 872882.CrossRefGoogle ScholarPubMed
Luna, MG, Sánchez, NE, Pereyra, PC, Nieves, E, Savino, V, Luft, E, Virla, E and Speranza, S (2012) Biological control of Tuta absoluta in Argentina and Italy: evaluation of indigenous insects as natural enemies. Bulletin OEPP/EPPO Bulletin 42, 260267.CrossRefGoogle Scholar
Mansour, R, Brévault, T, Chailleux, A, Cherif, A, Grissa-Lebdi, K, Haddi, K, Mohamed, SA, Nofemela, RS, Oke, A, Sylla, S, Tonnang, HEZ, Zappalà, L, Kenis, M, Desneux, N and Biondi, A (2018) Occurrence, biology, natural enemies, and management of Tuta absoluta in Africa. Entomologia Generalis 38, 83112.CrossRefGoogle Scholar
Megido, RC, Haubruge, E and Verheggen, FJ (2013) Pheromone-based management strategies to control the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). A review. Biotechnology, Agronomy, Society and Environment 17, 475482.Google Scholar
Ministry of Agriculture Livestock and Fisheries (MoALF) (2015) Economic review of agriculture [ERA] 2015. Available at http://www.kilimo.go.ke/wp-content/uploads/2015/10/Economic-Review-of-Agriculture_2015-6.pdf.Google Scholar
Mohamed, ESI, Mohamed, ME and Gamiel, SA (2012) First record of the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Sudan. Bulletin OEPP/EPPO Bulletin 42, 325327.CrossRefGoogle Scholar
Mollá, O, Montón, H, Vanaclocha, P, Beitia, F and Urbaneja, A (2009) Predation by the mirids Nesidiocoris tenuis and Macrolophus pygmaeus on the tomato borer Tuta absoluta. IOBC/WPRS Bulletin 49, 209214.Google Scholar
Mollá, O, Gonzalez-Cabrera, J and Urbaneja, A (2011) The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. BioControl 56, 883891.CrossRefGoogle Scholar
Mugo, W (2014) New pest poses danger to tomato production. The Organic Farmer 113, 3. ICIPE-African Insect Science for Food and Health, Nairobi. 8 pp.Google Scholar
Nannini, M, Atzori, F, Murgia, G, Pisci, R and Sanna, F (2012) Use of predatory mirids for control of the tomato borer Tuta absoluta (Meyrick) in Sardinian greenhouse tomatoes. Bulletin OEPP/EPPO Bulletin 42, 255259.CrossRefGoogle Scholar
Nderitu, WP, Muturi, JJ, Mark, O, Esther, A and Jonsson, M (2018) Tomato leaf miner (Tuta absoluta) (Meyrick 1917) (Lepidoptera: Gelechiidae) prevalence and farmer management practices in Kirinyanga County, Kenya. Journal of Entomology and Nematology 10, 4349.CrossRefGoogle Scholar
Otolo, JRA and Wakhungu, JW (2013) Factors influencing livelihood zonation in Kenya. International Journal of Education and Research 1, 110.Google Scholar
Pratt, CF, Constantine, KL and Murphy, ST (2017) Economic impacts of invasive alien species on African smallholder livelihoods. Global Food Security 14, 3137.CrossRefGoogle Scholar
R Development Core Team (2015) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org (Accessed 6 August 2020).Google Scholar
Smith, MA, Wood, DM, Janzen, DH, Hallwachs, W and Herbert, PDN (2007) DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences of the United States of America 104, 49674972.CrossRefGoogle Scholar
Tonnang, HEZ, Mohamed, SF, Khamis, F and Ekesi, S (2015) Identification and risk assessment for worldwide invasion and spread of Tuta absoluta with a focus on Sub-Saharan Africa: implications for phytosanitary measures and management. PLoS ONE 10, e0135283.CrossRefGoogle ScholarPubMed
Urbaneja, A, Montón, H and Mollá, O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus caliginosus and Nesidiocoris tenuis. Journal of Applied Entomology 133, 292296.CrossRefGoogle Scholar
Urbaneja, A, Desneux, N, Gabarra, R, Arnó, J, González-Cabrera, J, Mafra-Neto, A, Stoltman, L, Pinto, A and Parra, JRP (2013) Biology, ecology, and management of the South American tomato pinworm, Tuta absoluta. In Peña, JE (ed.), Potential Invasive Pests of Agricultural Crops. UK: CAB International, pp. 98125.CrossRefGoogle Scholar
Wafula, GO, Waceke, JW and Macharia, CM (2018) Role of mass trapping in the management of leafminer (Tuta absoluta) on tomato in the central highlands of Kenya. Journal of Agriculture and Life Sciences 5, 2833.Google Scholar
Zappalà, L, Biondi, A, Alma, A, Al-Jboory, IJ, Arnò, J, Bayram, A, Chailleux, A, El-Arnaouty, A, Gerling, D, Guenaoui, Y, Shaltiel-Harpaz, L, Siscaro, G, Stavrinides, M, Tavella, L, Aznaar, RV, Urbaneja, A and Desneux, N (2013) Natural enemies of the South American moth, Tuta absoluta in Europe, North Africa and Middle East and their potential use in pest control strategies. Journal of Pest Science 86, 635647.CrossRefGoogle Scholar