RESEARCH ARTICLE

 

Identification of alternative hosts of the tomato leafminer Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) in West Africa

 

 

Wendnéyidé Mathieu Sawadogo^{I, II}; Besmer Régis Ahissou^{I, II}; Irénée Somda^II; Souleymane Nacro^III; Anne Legrève^IV; François Verheggen^II

^ILaboratoire Systèmes Naturels, Agrosystèmes et de l'Ingénierie de l'Environnement (SyNAIE), Institute of Rural Development, Nazi Boni University, Bobo-Dioulasso, Burkina Faso
^IIGembloux Agro-Bio Tech, TERRA, University of Liege, Gembloux, Belgium
^IIILaboratoire d'entomologie agricole, Institut de l'Environnement et de Recherches Agricoles (INERA), Ouagadougou, Burkina Faso
^IVPhytopathology, Earth and Life Institute, Faculté des Bioingénieurs, Catholic University of Louvain, Ottignies-Louvain-la-Neuve, Belgium

Correspondence

 

 

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ABSTRACT

Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) reached West Africa in 2012 and has since become a major tomato pest. Various alternative strategies for pest control have been identified worldwide, including crop rotation, to deprive the insect of its food. However, this method can only be implemented if a good knowledge of the local host plants of the leafminer have been identified. Here, we have assessed the capacity of Tuta absoluta to develop on 27 common vegetable crops in West Africa, representing the Poaceae, Apiaceae, Convolvulaceae, Amaranthaceae, Malvaceae, Lamiaceae, Cucurbitaceae, Fabaceae, Brassicaceae, Asteraceae, Solanaceae, and Amaryllidaceae. The tomato leafminer was only able to develop and complete its life cycle on crops within the genus Solanum. Among the 27 plant species tested, Solanum lycopersicum L. (tomato) was identified as the best host, allowing for rapid development (22.2 ± 1.4 days) and a high survival rate (84%). Solanum tuberosum L. (Irish potato) (24.4 ± 0.8 days; survival rate 40%), Solanum aethiopicum L. (African eggplant) (24.3 ± 0.6 days; survival rate 52%) and Solanum melongena L. (eggplant) (25.9 ± 1.8 days; survival rate 24%) were three other possible hosts. Larval development occurred on onion (Allium cepa L.), but not pupation. A strategy that includes a prolonged absence of the genus Solanum in a production area would be associated with a considerable reduction in leafminer population size.

Keywords: development cycle, host plants, pest control, Solanum, vegetable crops

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INTRODUCTION

The South American tomato leafminer Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) is an economic pest of tomato, which has been prevalent in South America since the 1960s (Biondi et al. 2018). The larvae feed on all aerial parts of the plant, destroying vegetative and reproductive organs, including fruits, and can cause production losses of up to 100% if no effective control methods are used (Desneux et al. 2010; Sawadogo et al. 2020a). After its discovery in Europe (Spain) in 2006 (Urbaneja et al. 2007), it has acquired the status of a global pest of tomato due to its discovery in several parts of the world (Biondi et al. 2018). It reached North Africa in 2008, West Africa in 2012, and the Caribbean in 2018 (Abbes et al. 2012; Pfeiffer et al. 2013; Sylla et al. 2017; Son et al. 2017; USDA-APHIS 2011; Verheggen & Fontus 2019). The invasiveness ofthe species could be attributed to its high reproductive capacity (i.e. a multivoltine species that can lay more than 240 eggs per female) (Fernandez & Montagne 1990; Germain et al. 2009), its rate of expansion (800 km per year) (Biondi et al. 2018), ability to easily locate its hosts (Bawin et al. 2017) , and above all its resistance to several chemical insecticides (Guedes et al. 2019; Han et al. 2019; Sawadogo et al. 2020b).

Various strategies for control of Tuta absoluta have been implemented worldwide, including tolerant cultivars, beneficial species, entomopathogens, biopesticides, pheromones, and crop rotation (Abd El-Ghany et al. 2018; Cagnotti et al. 2021; Ferracini et al. 2019; Gharekhani & Salek-Ebrahimi 2014; Jallow et al. 2020; Caparros Megido et al. 2013a; Ndereyimana et al. 2019; Ouardi et al. 2012). The objective of crop rotation is to deprive the insect of its food by alternating tomato production with other vegetable crops. Such an approach is successfully implemented in some tomato production areas in the USA (Portakaldali et al. 2013). However, this method can only be implemented if a good knowledge of the local host plants of the tomato leafminer have been identified (Bawin et al. 2016; Cherif & Verheggen, 2019).

The main host plant of the tomato leafminer is tomato (Solanum lycopersicum L.), but it has been known to feed on other solanaceous plants, such as Irish potato (Solanum tuberosum L.), eggplant (Solanum melongena L.), Peruvian pepino (Solanum muricatum Aiton), and black nightshade (Solanum nigrum L.). The insect can also feed on other plant families, including the Amaranthaceae, Euphorbiaceae, Cucurbitaceae, Geraniaceae, Fabaceae, Asteraceae, and Malvaceae, where it can complete at least part of its cycle (Abbes et al. 2016; Cherif & Verheggen 2019; Mohamed et al. 2015; Sylla et al. 2019; Portakaldali et al. 2013; Vargas 1970).

Sawadogo et al. (2020a) identified 27 crops commonly used in rotation or association with tomato. We, therefore, decided to evaluate the ability of the tomato leafminer to develop on these plants species, paying attention to larval and pupal development, as well as survival rates at all stages of the life cycle.

 

MATERIAL AND METHODS

Insects

Three hundred larvae were collected in February 2020 in an open field of tomato located in the village of Goue (12°35'45" N, 01°24'00" W), province of Oubritenga, in Burkina Faso. We then built a tomato leafminer mass rearing facility within the Research and Training Centre of the Nazi Boni University at Bobo Dioulasso (11°09'53" N, 04°18'54" W). The insects were carefully contained in cages 80 cm long, 40 cm wide and 40 cm high and fed on Rossol tomato plants. During rearing the temperature was 28 ± 3 °C, the relative humidity 50 ± 15%, and the photoperiod equally split between dark and light (i.e. 12 h dark:12 h light per 24 h).

Plant material

Twenty-seven plant species were used in this trial (Table 1). They were cultivated in a greenhouse in jars containing soil that had been sterilised by heating at 60 °C overnight.

 

 

Experimental setup

Tomato leafminer eggs were collected from the rearing cages and five eggs deposited on a soft leaf of an approximately 1-month-old plant of each species. The leaf was then placed on moistened blotting paper contained in a Petri dish (8.9 cm diameter). The dish was then closed and sealed with parafilm. For each plant species, 25 eggs were used for the test (five replicates, with five eggs per replicate). After hatching, the larvae were fed exclusively on the leaves of the species on which they had emerged. Fresh leaves were provided daily and the boxes emptied of old leaves and excrement. Blotting paper was also moistened on-demand until pupation. After emergence, the adults were kept in the same plastic Petri dishes and always moistened, but no food provided, to evaluate their lifespan.

When L1 larvae could not develop, we collected L2 and L3 larvae from the Tuta absoluta rearing cages to check their ability to use the tested plant species as food and pursue their life cycle. Observations were made each morning and evening with a binocular magnifying glass to record the dates of hatching, pupation, emergence, and death of the adult.

Data analysis

After checking the normality of the data, we calculated the descriptive statistics for the data and used non-parametric Kruskal-Wallis tests to compare the duration of the different developmental stages of the pest on the different crops. The two-by-two comparison of the rankings of the averages was done using the post hoc Dunn's Multiple Comparison Test (at a 5% level of significance). These different analyses were carried out with the software XLSTAT and IBM SPSS statistics 25.

 

RESULTS

No plant species prevented the hatching of leafminer eggs. Nevertheless, we found differences in incubation times on the different plants (K = 256.45, P < 0.0001), which varied from 3.0 ± 0.3 days on Capsicum chinense Jacq. to 4.1 ± 0.4 days on Vigna unguiculata (L.) Walp..

Outside the Solanum genus, Tuta absoluta larvae were not able to develop and complete their life cycle (Table 2). For the genus Solanum, there were intrageneric differences in survival rates, with survival rates on Solanum lycopersicum (84%) greater than on Solanum aethiopicum L. (40%) and Solanum tuberosum (52%) respectively. Solanum melongena allowed complete development of Tuta absoluta, but with a lower survival rate (24%).

On other genera (i.e. not Solanum) larvae survived up to three days: from 1.3 ± 0.5 days on Cucumis sativus L. to 2.8 ± 0.3 days on Capsicum annuum L.. The larval lifespans were much higher on Solanum species (K = 435.64, P < 0.0001), than other species. For Solanum species, larvae had a shorter lifespan (K = 34.54, P < 0.0001) on Solanum lycopersicum (11.4 ± 0.3 days) than on the other three species, whose lifespans varied from 12.3 ± 0.5 on Solanum melongena to 12.5 ± 0.5 days on Solanum tuberosum. As for the L2 and L3 larvae collected in the tomato leafminer rearing cages and deposited on the leaves of the different species, all of them died in less than three days, except those deposited on Allium cepa L., where they were able to feed for seven days without reaching the pupal stage.

The duration of the chrysalis stage was affected by the host plant (K = 25.75, P < 0.0001), with the duration of the stage shorter on Solanum lycopersicum (6.8 ± 1.0 days) than on the other three species of Solanum (i.e. from 7.9 ± 0.9 days to 9.7 ± 1.4 days). Adults fed on Solanum lycopersicum (10.0 ± 4.7 days) lived longer (K = 8.61, P = 0.03) than those fed on the other three species (i.e. from 6.5 ± 3.9 to 7.0 ± 4.1 days).

The complete life cycle was consequently affected by the host plant (K = 32.32, P < 0.0001) and was shorter on Solanum lycopersicum (22.2 ± 1.4 days), than on the other three Solanum species (i.e. from 24.3 ± 0.6 to 25.9 ± 1.8 days).

 

DISCUSSION

Only the four commonly cultivated Solanum species can host Tuta absoluta, allowing the pest to complete its life cycle, with a high survival rate. These results confirm some of those of previous works (Brevault et al. 2014; Caparros Megido et al. 2013b; Negi et al. 2018; Pereyra & Sanchez 2006; Sylla et al. 2018) . We found that species belonging to the genus Capsicum (Capsicum annuum and Capsicum chinense), despite belonging to the Solanaceae, are not suitable host plants for this pest. These results contradict those obtained by Portakaldali et al. (2013) who found that Capsicum annuum was a host plant for the tomato leafminer in Turkey. We confirm the results of previous work, which found that Tuta absoluta was not able to complete its life cycle on plant species outside the Solanaceae. The larvae may be unable to mine and feed (due to the cellular structure of the tissues, and robustness of the epidermis), but other factors may also explain their low survivability, including poor organoleptic qualities of tissues, the presence of a toxin, and physical barriers formed by rough trichomes, which could injure the larvae when they move in search of better areas to mine (Awmack & Leather 2002; Krechemer & Foerster 2017; Pereyra & Sanchez 2006). We found a shorter duration of larval development on tomato than on the other three Solanum species tested, which confirms the finding of Negi et al. (2018), who found duration of the larval stage on tomato was shorter than on potato, or eggplant. This difference within the same genus could be due to the difference in genetic material (species or even varieties) used. Indeed, even within the same species, genetic variability leads to differences in palatability, nutritional and organoleptic quality as well as the ability to produce toxins to counter pest attacks (Awmack & Leather 2002; Bawin et al. 2015; Krechemer & Foerster 2017). Onion, on which L2 and L3 larvae were able to maintain themselves for seven days without being able to move to pupation, is a poor host. The nutritional value is low, or its leaves contain toxic substances whose activity is detrimental in the medium term. Species such as Nicotiana tabacum L., Vicia faba L., and Malva sylvestris L., are also able to support partial development of the tomato leafminer (Abdul-Ridha et al. 2012; Bawin et al. 2016; Cherif & Verheggen 2019).

Our study did not take into account non-crop species but it appears that several species belonging to the Solanaceae family, namely Atropa belladonna L., Datura stramonium L., Datura ferox L, Lycium barbarum L., Nicotiana glauca Graham, Solanum dulcamara L., Solanum nigrum, Solanum elaeagnifolium Cav., and Lycopersicum puberulum Phil., are potential hosts of the tomato leafminer (Bawin et al. 2016, 2015; García & Espul 1982). In particular, studies conducted by Idris et al. (2020) and Campos et al. (2021), show that the black nightshade Solanum nigrum allows Tuta absoluta to complete its life cycle. In comparison to tomato, the leafminer has slightly lower fecundity and longevity on Solanum nigrum. Particular attention should be paid to this plant, especially as it is a perennial and widely distributed plant in Africa.

In a context where (1) vegetable production is market-oriented, (2) production is increasingly subject to economically important pests, (3) the massive use of pesticides increases production costs and considerably reduces producers' earnings, and (4) more and more producers on production sites are organized in groups, associations or cooperatives, it is time to think about pest management on the scale of the production site or drainage basin (MAAH 2019; Sawadogo et al. 2020a). This could become a reality where producers within a group of this nature unanimously choose the crops they will produce according to market characteristics and pests. For tomato leafminer management, where the four Solanum crops studied are among the main marketed vegetable crops in the country, they could be rotated yearly with onion, cabbage (the two most important vegetable crops in terms of production) or okra, which represent a very large market share in all regions of the country (MAAH 2019). Even if these crops are rotated, special attention should also be given to the monitoring of weeds and perennials that act as shelters for the leafminers (e.g. Solanum nigrum), in order to avoid even minimal maintenance of the leafminer population during intercropping with a non-host species.

 

ACKNOWLEDGMENTS

This research was funded by the Academy of Research and Higher Education-Commission Development Cooperation (ARES-CDD), as part of the PRD-ProDuIRe project. The authors declare that they have no conflict of interest.

 

ORCID IDs

Wendnéyidé Mathieu Sawadogo - https://orcid.org/0000-0002-6448-4804

Irénée Somda - https://orcid.org/0000-0002-0707-8367

Francois J Verheggen - https://orcid.org/0000-0002-5849-1661

Besmer Regis Ahissou - https://orcid.org/0000-0003-0898-8431

 

REFERENCES

Abbes K, Harbi A, Chermiti B. 2012. The tomato leafminer Tuta absoluta (Meyrick) in Tunisia: Current status and management strategies. EPPO Bulletin 42: 226-233.         [ Links ]

Abbes K, Harbi A, Elimem M, Hafsi A, Chermiti B. 2016. Bioassay of three Solanaceous weeds as alternative hosts for the invasive tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae) and insights on their carryover potential. African Entomology 24: 334-342. https://doi.org/10.4001/003.024.0334        [ Links ]

Abd El-Ghany NM, Abdel-Razek AS, Djelouah K, Moussa A. 2018. Efficacy of bio-rational insecticides against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on tomatoes. Bioscience Research 15:28-40.         [ Links ]

Abdul-Ridha M, Alwan S, Helal S, Aziz KA. 2012. Alternative hosts of South American tomato moth Tuta absoluta (Gelechiidae: Lepidoptera) in some tomato farms of Najaf province. Euphrates Journal of Agriculture Science 4: 130-137.         [ Links ]

Awmack CS, Leather SR. 2002. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47: 817-844. https://doi.org/10.1146/annurev.ento.47.091201.145300        [ Links ]

Bawin T, Collard F, De Backer L, Yarou BB, Compère P, Francis F, Verheggen FJ. 2017. Structure and distribution of the sensilla on the antennae of Tuta absoluta (Lepidoptera: Gelechiidae). Micron 96: 16-28. https://doi.org/10.1016/j.micron.2017.01.008        [ Links ]

Bawin T, Dujeu D, De Backer L, Fauconnier M-L, Lognay G, Delaplace P, Francis F, Verheggen FJ. 2015. Could alternative solanaceous hosts act as refuges for the tomato leafminer, Tuta absoluta? Arthropod-Plant Interactions 9: 425-435. https://doi.org/10.1007/s11829-015-9383-y        [ Links ]

Bawin T, Dujeu D, De Backer L, Fauconnier M-L, Lognay G, Delaplace P, Francis F, Verheggen FJ. 2016. Ability of Tuta absoluta (Lepidoptera: Gelechiidae) to develop on alternative host plant species. Canadian Entomologist 148: 434-442. https://doi.org/10.4039/tce.2015.59        [ Links ]

Biondi A, Guedes RNC, Wan F, 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: 239-258. https://doi.org/10.1146/annurev-ento-031616-034933        [ Links ]

Brévault T, Sylla S, Diatte M, Bernadas G, Diarra K. 2014. Tuta absoluta Meyrick (Lepidoptera: Gelechiidae): A new threat to tomato production in Sub-Saharan Africa. African Entomology 22: 441-444. https://doi.org/10.4001/003.022.0202        [ Links ]

Cagnotti CL, Arias AE, Ermantraut EN, Andorno AV, Viscarret MM, Lopez SN. 2021. Life history study of the mirid Tupiocoris cucurbitaceous feeding on Tuta absoluta eggs: implications for biological control and its combination with inherited sterility. BioControl 66: 207-216. https://doi.org/10.1007/s10526-020-10054-7        [ Links ]

Campos MR, Amiens-Desneux E, Béarez P, Soares MA, Ponti L, Biondi A, Harwood JD, Desneux N. 2021. Impact of low temperature and host plant on Tuta absoluta. Entomologia Experimentalis et Applicata. 169(11): 984-996. https://doi.org/10.1111/eea.13094        [ Links ]

Caparros Megido R, Haubruge E, Verheggen FJ. 2013a. Pheromone-based management strategies to control the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae ). A review. Biotechnology Agronomy Society Environment 17: 475-482.         [ Links ]

Caparros Megido R, Brostaux Y, Haubruge E, Verheggen FJ. 2013b. Propensity of the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), to develop on four potato plant varieties. American Journal of Potato Research 90: 255-260. https://doi.org/10.1007/s12230-013-9300-9        [ Links ]

Cherif A, Verheggen FJ. 2019. A review of Tuta absoluta (Lepidoptera: Gelechiidae) host plants and their impact on management strategies. Biotechnology Agronomy Society Environment 23: 270-278.         [ Links ]

Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Ruescas DC, Tabone E, Frandon J, et al. 2010. Biological invasion of European tomato crops by Tuta absoluta: Ecology, geographic expansion and prospects for biological control. Journal of Pest Science 83: 197-215. https://doi.org/10.1007/s10340-010-0321-6        [ Links ]

Fernandez S, Montagne A. 1990. Preferencia de oviposicion de las hembras y duracion, crecimiento y sobrevivencia de las larvas de Scrobipalpula absoluta (Meyrick) en diferentes Solanaceas. Boletín de Entomología Venezolana 5: 89-99.         [ Links ]

Ferracini C, Bueno VHP, Dindo ML, Ingegno BL, Luna MG, Gervassio NGS, Sánchez NE, Siscaro G, Lenteren JCV, Zappalà L, et al. 2019. Natural enemies of Tuta absoluta in the Mediterranean basin, Europe and South America. Biocontrol Science and Technology 29: 578-609. https://doi.org/10.1080/09583157.2019.1572711        [ Links ]

García M, Espul J. 1982. Bioecology of the tomato moth (Scrobipalpula absoluta) in Mendoza , Argentine Republic. Revista Investigaciones Agropecuarias 17: 135-146.         [ Links ]

Germain JF, Lacordaire AI, Cocquempot C, Ramel JM, Oudard E. 2009. Un nouveau ravageur de la tomate en France: Tuta absoluta. PHM-Revue Horticole 512: 37-41.         [ Links ]

Gharekhani G, Salek-Ebrahimi H. 2014. Life table parameters of Tuta absoluta (Lepidoptera: Gelechiidae) on different varieties of tomato. Journal of Economic Entomology 107: 1765-1770.         [ Links ]

Guedes RNC, Roditakis E, Campos MR, Haddi K, Bielza P, Siqueira HAA, Tsagkarakou A, Vontas J, Nauen R. 2019. Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook. Journal of Pest Science 92: 1329-1342. https://doi.org/10.1007/s10340-019-01086-9        [ Links ]

Han P, Desneux N, Becker C, Larbat R, Le Bot J, Adamowicz S, Zhang J, Lavoir AV. 2019. Bottom-up effects of irrigation, fertilization and plant resistance on Tuta absoluta: implications for Integrated Pest Management. Journal of Pest Science 92: 1359-1370. https://doi.org/10.1007/s10340-018-1066-x        [ Links ]

Idriss GEA, Du Plessis H, Khamis FM, Ekesi S, Tanga CM, Mohamed SA. 2020. Host range and effects of plant species on preference and fitness of Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Economic Entomology 113: 1279-1289. https://doi.org/10.1093/jee/toaa002        [ Links ]

Jallow MFA, Dahab AA, Albaho MS, Devi VY, Jacob J, Al-Saeed O. 2020. Efficacy of mating disruption compared with chemical insecticides for controlling Tuta absoluta (Lepidoptera: Gelechiidae) in Kuwait. Applied Entomology and Zoology 55: 213-221. https://doi.org/10.1007/s13355-020-00673-y        [ Links ]

Krechemer FS, Foerster LA. 2017. Development, reproduction, survival, and demographic patterns of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) on different commercial tomato cultivars. Neotropical Entomology 46: 694-700. https://doi.org/10.1007/s13744-017-0511-5        [ Links ]

MAAH [Ministère de l'Agriculture, et des Aménagements Hydroagricoles]. 2019. Rapport de l'Enquête maraichère 2018. MAAH, Ouagadougou, Burkina Faso. pp 1-58.

Mohamed ESI, Mahmoud MEE, Elhaj MAM, Mohamed SA, Ekesi S. Host plants record for tomato leaf miner Tuta absoluta (Meyrick) in Sudan. EPPO Bulletin 45: 108-111. https://doi.org/10.1111/epp.12178

Ndereyimana A, Nyalala S, Murerwa P, Gaidashova S. 2019. Pathogenicity of some commercial formulations of entomopathogenic fungi on the tomato leaf miner, Tuta absoluta ( Meyrick ) (Lepidoptera: Gelechiidae). Egyptian Journal of Biological Pest Control 29: 1-5. https://doi.org/10.1186/s41938-019-0184-y        [ Links ]

Negi S, Sharma PL, Sharma KC, Verma SC. 2018. Effect of host plants on developmental and population parameters of invasive leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Phytoparasitica, 46: 213-221. https://doi.org/10.1007/s12600-018-0661-y        [ Links ]

Ouardi K, Chouibani M, Rahel MA, El Akel M. 2012. Stratégie nationale de lutte contre la mineuse de la tomate Tuta absoluta Meyrick. EPPO Bulletin 42: 281-290. https://doi.org/10.1111/epp.2568        [ Links ]

Pereyra PC, Sanchez EN. 2006. Effect of two solanaceous plants on developmental and population parameters of the tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology 35: 671-676.         [ Links ]

Pfeiffer D, Muniappan R, Sall D, Diatta P, Diongue A, Dieng E. 2013. First Record of Tuta absoluta (Lepidoptera: Gelechiidae) in Senegal. Florida Entomologist 96: 661-662. https://doi.org/10.1653/024.096.0241        [ Links ]

Portakaldali M, Ôztemiz S, Kütük H. 2013. A new host plant for Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Turkey. Journal of the Entomological Research Society 15: 21-24.         [ Links ]

SSawadogo MW, Somda I, Nacro S, Legrève A, Verheggen F. 2020a. Cinq années d' invasion: Impact de Tuta absoluta (Meyrick) sur la production de tomate au Burkina Faso. Tropicultura 38: 1-14. http://hdl.handle.net/2268/261621        [ Links ]

Sawadogo MW, Somda I, Nacro S, Legrève A, Verheggen FJ.2020b. Insecticide susceptibility level and control failure likelihood estimation of Sub-Saharan African populations of tomato leafminer: Evidence from Burkina Faso. Physiological Entomology 45: 147-153. https://doi.org/10.1111/phen. 12332        [ Links ]

Son D, Bonzi S, Somda I, Bawin T, Boukraa S, Verheggen F, Francis F, Legreve A, Schiffers B., 2017. First Record of Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) in Burkina Faso. African Entomology 25: 259-263. https://doi.org/10.4001/003.025.0259        [ Links ]

Sylla S, Brévault T, Bal AB, Chailleux A, Diatte M, Desneux N, Diarra K. 2017. Rapid spread of the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), an invasive pest in Sub-Saharan Africa. Entomologia Generalis 36: 269-283. https://doi.org/10.1127/entomologia/2017/0453        [ Links ]

Sylla S, Brévault T, Monticelli LS, Diarra K, Desneux N. 2019. Geographic variation of host preference by the invasive tomato leaf miner Tuta absoluta: implications for host range expansion. Journal of Pest Science 92: 1387-1396. https://doi.org/10.1007/s10340-019-01094-9        [ Links ]

Sylla S, Seydi O, Diarra K, Brevault T. 2018. Seasonal decline of the tomato leafminer, Tuta absoluta, in the shifting landscape of a vegetable-growing area. Entomologia Experimentalis et Applicata 166: 638-647. https://doi.org/10.1111/eea.12722        [ Links ]

Urbaneja A, Vercher R, Navarro V, Mari GF, Porcuna LJ 2007. La polilla del tomate, "Tuta absoluta'' Phytoma España 194: 16-24.         [ Links ]

USDA-APHIS. 2011. Federal import quarantine order for host materials of tomato leafminer, Tuta absoluta (Meyrick). Washington, DC: United States Department of Agriculture. https://www.aphis.usda.gov/import_export/plants/plant_imports/federal_order/downloads/2011/Tutaabsoluta5-5-2011.pdf        [ Links ]

Vargas C. 1970. Observations on the bionomics and natural enemies of the tomato moth, Gnorimoschema absoluta ( Meyrick ) ( Lep . Gelechiidae ). Idesia 47: 75-110.         [ Links ]

Verheggen F, Fontus RB. 2019. First record of Tuta absoluta in Haiti. Entomologia Generalis 38: 349-353. https://doi.org/10.1127/entomologia/2019/0778        [ Links ]

 

 

Correspondence:
Francois Verheggen
Email: fverheggen@uliege.be

Received: 23 August 2021
Accepted: 22 September 2021