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Research Article - (2021) Volume 5, Issue 6

Prospects of Biological Control Agents for Management of Invasive Pest Tuta Absoluta (Lepidoptera: Gelechiidae) In Africa
Never Zekeya*, Humphrey Peter and Ernest Mbega
 
1Department of Animal sciences, College of African Wildlife Management-Mweka, Moshi, Tanzania
2Department of Animal sciences, Tanzania Industrial Research and Development Organization, Msasani, Dar es Salaam, Tanzania
3Department of Sustainable Agriculture and Biodiversity Ecosystem Management, School of Life Science and Bioengineering, The Nelson Mandela African,Arusha, Institution of Science and Technology, Tanzania
 
*Correspondence: Never Zekeya, Department of Animal sciences, College of African Wildlife Management-Mweka, Moshi, Tanzania, Email:

Published: 25-Jan-2022

Abstract

Tuta absoluta (Meyrick) is a devastating agricultural pest of global concern, which has spread widely across continents causing substantial economic losses, particularly in tomato cultivation. In Africa the problem is much severe to the extent that farmers are abandoning the crop. Controlling T. absoluta by use of chemical pesticides is profoundly tricky due to development of rapid resistance. Alternative options such as biological controls are either scarce or expensive and only a handful of microbial agents are currently registered for management of T. absoluta in Africa. It has been observed that T. absoluta causes damage and loss in tomato ranging from 50-100% in South America, Europe and Africa where management options are most limited. Although several synthetic pesticides are registered for management of T. absoluta including; chlorantraniliprole spinetoram and emamectin benzoate group, little success are reported in Africa due to various factors including fast resistance development of T. absoluta. Commercially available biopesticides such as; Beauveria bassiana (Bals.), Metarhizium anisopliae (Metschn.), Bacillus thurungiensis (Bt), neem extract (Azadirachtin) and Spinosad (bacteria compound; spinosyn A and spinosyn D) are scarcely distributed in Africa. Although recently there are newly studied biocontrols including Aspergillus oryzae (Vuruga Biocide) that is registered in Tanzania, yet not distributed to most farmers across the country. However, some biocontrols have been reported for control T. absoluta in Africa including; Aspergillus flavus (Ahlb.) and Aspergillus oryzae (Ahlb.), they are not commercially available. This review highlights on the utilization and commercialization of various biological control agents for T. absoluta management in Africa.

Keywords

Tomato leafminer; Aspergillus oryzae; Management strategies; Microbial control agents

Introduction

Tuta absoluta (Meyrick), the tomato leafminer, is an invasive pest from South America that has spread extensively in Europe, Asia and Africa threatening tomato production [1,2,3,4,5]. T. absoluta and other pests, including mealybug and whitefly, aphids, cabbage lopper, cutworms, leafminer (Liriomyza sativa), tomato fruit worm, and flea beetles are the main threats to tomato producers in Africa and globally except USA where T. absoluta has not yet been properly reported [6,7,3,8,9,10,11]. T. absoluta and other lepidopterous pests reduce both the yield and the quality of tomato fruit, thus diminishing its value in the market [12,13,14].

Continent Confirmed countries Host Damage Invasion period Reference
South America Peru, Chile, Ecuador, Argentina, Brazil Bolivia, Colombia, Paraguay, Peru, Uruguay and Venezuela Tomato, potato, Datura spp, and Nicotiana spp Damage range from 80-100% Damage range 80-100% tomato damage 1914 - to date; still persisting Sylla et al., 2019;Desneux et al., 2011;[121] Luna et al., 2015
Central/ North America Canada, Haiti, USA, Mexico, Panama, Costa Rica Tomato, potato, Datura spp, and Nicotiana spp damage 30-50% Present with moderate impact Desneux et al., 2011; [125,126,128]
Europe Spain, Italy, Malta, France, Portugal, Germany, Bulgaria, UK, Serbia, Switzaland,Slovenia, Romania, Lithuania, Greece, Cosovo, Azerbaijan,Croatia, Belarus, Netherlands, Belgium, Czech-Republic, Denmark,Georgia, Guernsey,Hungray,North Macedonia,Norway,ukrain,Austria, Montenegro, Cyprus, Bosnia and Herzegovina Tomato, potato, and Datura spp, Nicotiana spp, Cape gooseberry, bean (Phaseolas vulgaris) Damage rate range from 50-80%s 50-80% crop damage in protected cultivation Late 2006 – to date. Continuing to invade new areas and cause damage [111]; Karadjova et al., 2013; [124]
Asia Turkey, India, Iran, Japan, China, Rusia, Yemen, Qatar,Bahrain, Kuwait, United Arab Emirate, Bangladesh, Iraq, Syria, Sultanate of Oman, Lebanon, Israel, Palestine, Saudi Arabia, China, Nepal, Afghanstan, Kazakhstan,Tajikistan, Uzbekistan,Pakistan and Burma Tomato and eggplant 50-100% tomato damage 2010 – onwards; gradually expand its range in the region Li et al., 2021; [115] Guimapi et al., 2020; Zhang et al., 2020; Han et al., 2019;[106]; [119] Rakha et al., 2017; [131]
Africa Algeria, Morocco, Libya, Egypt, Senegal, Sudan, Canary island, Eritrea, Nigeria, Ethiopia, Lesotho, Angola, Burundi, Cape Verde, Ghana, Botswana, Benin, Mayotte, Equatorial Guinea, Kenya, Tunisia, Niger, Tanzania, Zambia, Zimbabwe, D R Congo, Somalia, Bukina faso, Namibia, DR Sao Tome and Principe, Togo and Côte d'Ivoire Tomato, potato, night shade, eggplant,Datura spp, and Nicotiana spp Up to100% crop damage in open fields Since 2008 and currently expanding its invasion across the continent [120,113,134] Sawadogo et al., 2020; Smith et al., 2018; [109] Desneux et al., 2011; Rakha et al., 2017; Tonnang et al., 2015
Australia Not reported None reported Under risk due to high commercial Expect invasion on tomato Han et al., 2018; Verheggen et al., 2019

Table 1: Global distribution of Tuta absoluta, host range and damage incidences.

Tuta absoluta has spread globally and is now distributed across various agroecological regions of Africa causing losses tomato as well as other crops such as night shade, eggplant, pepper, and several weeds [15,16] (Table 1). The Tomato leaf miner is also a major impediment in the production of several other solanaceous vegetables in Africa [17,18], It has led to severe damage and yield losses, mainly due to insecticide resistance [19]. Since its arrival in 2014, Tanzanian farmers have experienced massive crop losses [20]. Its control has become a major challenge due to the broad host range and a higher reproductive rate [21,22]. Tuta absoluta attacks all developmental crop stages, from seedlings to mature fruits for field and greenhouse-grown solanaceas including S. tuberosum, S. nigrum, S. melongena and wild Solunum spp [23-25]. Studies have shown that Tuta absoluta larvae and adults prefer the aerial plant parts due to their higher sugar levels [26,27]. This pest is successful due to tolerance under extreme temperature conditions ranging from coldness to high temperature hence surviving in several regions and various seasons [28,29]. Hence, management of this pest is tricky requiring an effective, integrated and affordable biocontrol agent to avert the problem in Africa.

Management of T. absoluta in Tanzania and in other African countries rely heavily on application of conventional pesticides [30] without even detection of the pest by using pheromone and colored traps that assist in identification and monitoring of pest population [31]. Despite the popularity of chemical pesticides, studies have revealed the usefulness of using other options including host resistance mechanisms [32]. Generally, there are scarce reports on management options with ability of controlling all stages of Tuta absoluta. Biological pesticides including viruses, fungi, bacteria and nematodes have been reported to effectively control T. absoluta eggs and larvae [33,34]. However, few of these have undergone screening in Africa despite its widespread invasion.

Natural enemies, particularly Hemipteran predators, are effective against T. absoluta and other insect pests [35,36,37]. In addition, entomopathogenic microbes are also gaining popularity in insect pest management worldwide, including Africa [38,39,10,40].

The alternate use of different active ingredients biocontrol agents such as; predators, parasitoids, botanicals and microbials showed high efficacy with low or no rate resistance on the pest [8,41]. However, use of an integated pest management including use of botanicals such as neem extract, microbial pesticide and minimal chemical pesticides is highly recommended for effective synegetic effects and safety with natural enemies [42,43,35]. Microbial controls including fungi, bacteria and virus have high potential to be used as biocontrol agents for management of insect pests for crop protection [33,44]. Bacteria especially Bacillus spp have proven to be effective for controlling Tuta absoluta in many areas [45]. Several reports have proved the efficacy of entomopathogenic bacteria; B. thuringesis for the control of T. absoluta larvae in Africa [40,46]. However, the effectiveness and accessibility of these biopesticides vary with pest species and geographical areas whereas little success has been reported in controlling T. absoluta in Tanzania [47]. Entomopathogenic fungi have been highly used as foliar sprays/drenches directly on plant or as endophytes for controlling insect pests compared to the rest of microbial controls [48,49]. Beauveria bassiana is widely used as epiphyte or endophyte for pest control worldwide [48,50] with high efficacy as both an endophyte and a foliar spray. Other entomopathogenic fungi including Metarhizium anisopliae have been reported to be highly effective against different pests including T. absoluta [51]. On other hand, Aspergillus spp. have been screened and evaluated in laboratory with high efficacy against larvae, pupae and adults of T. absoluta in Algeria and Tanzania [52,47]. In Africa, entomopathogenic microbes have been introduced for pest management with few record of registed products [53].

Since the management of insect pests is shifting from reliance on chemicals to integrated approaches of biocontrols including pathogenic nematodes, bacteria, fungus and virus [54,55,56,53], it is evident that biopesticides will increasingly be adopted in many regions especially in Africa where the pest is recently invading abruptly. Hence, native microbial controls including Aspergillus species could be a potential biopesticide for control of T. absoluta as it has been revealed with promising results on T.absoluta in Africa [52,47]. This review highlights the global trends of T. absoluta, available and registered management options for controlling T. Absoluta. It also provides prospects for screening and registration of novel biopesticide from local context for effective management of T. absoluta in Africa where the pest available managent options are unaffordable by most farmers.

Current management strategies for controlling Tuta absoluta

Conventional pesticides

Synthetic chemical pesticides have been used worldwide with low success due to resistance in most regions [51,57]. Management of T. absoluta by single approach cannot suppress the pest below economic injury level due to the fact that there is no single option that can 100% control all stages [58]. Several studies reported the failure of chemical pesticides including Chlorantraniliprole and Amamectin benzoate for controlling T. absoluta [19,59]. Chemical pesticides are imported in Africa in which their effectiveness might be compromised during shipping and misused by farmers due pest panic as well as limited training on application of pesticides [47]. Additionally, synthetic pesticides are environmentally and economically unaffordable in most African countries with limited financial resources. However, proper use with integration with environmentally safe strategies including traps and biological agents should be promoted to enhance management of T. absoluta.

Pheromone traps

Pheromones and other semiochemicals are widely applied for controlling insect pests in integrated pest management (IPM) programs including monitoring, mass trapping, rule and killing (attact-inhilate) and mating disruption [32]. Studies show that pheromone traps are effective in controlling T. absoluta under protected cultivation [60]. However, although traps are useful for attracting mainly adult male moth and often for population monitoring [5], they are expensive, and are rarely used by farmers to control T. absoluta in Africa. Studies show that pheromone traps cannot be effective when used merely for control of pests because they are designed to disrupt mating and not killing [61]. However, other studies have revealed that incorporation of semiochemicals; attractants of different colors in pheromone traps in early growing season help detect pests and monitor population and gradually minimize pest impact in the field [32,5]. Proper selection and application of traps could be effective when integrated with biological controls to safely protect tomato and other vegetable crops against T. absoluta.

Microbial control agents against T. absoluta

Microbial controls for pest management are becoming popular worldwide as effective and affordable control options against various insect pests on various crops [38]. In Europe and America, the application of microbial controls for crop protection has been commercialized and used intensively [62] whereas it has only been recently introduced in Africa. Microbes play a major role in balancing nutrients and proper utilization in agriculture [63]. A study by Buragohain et al. 2021 reported the effectiveness of integrating B. thuringiensis var kurstaki, B. bassiana and neem extract for management of T. absoluta under field conditions in India. This reveals that native biocontrol agents are potential for effective management of various insect pests [64,65,66]. Other microbial controls including viruses, bacteria and nematodes have been reported to be effective against eggs and larvae of T. absoluta under laboratory conditions [33,34] but their further validation is needed. Despite the fact that T. absoluta is widespread in Africa, few microbial controls have been registered and commercialized [47,67]. The commercially available bgacterial biopesticides are B. thuringiesis and B. subtilis [55,68,65,69,70]. Recently, entomopathogenic fungi are increasingly studied and reported to be effective pest controls [71,72,73]. Some fungi species including B. bassiana are reported as plant endophytes enhancing pest control [48,6], and also produce toxic metabolites for pest control [74,75]. On the other hand, M. anisopliae, B. bassiana, A. flavus and A. clavatus have shown high efficacy against several agricultural insect pests [76]. It has also been observed that most entomopathogenic fungi are effective in controlling lower stages of pests and some crop diseases when combined with chemical pesticides [77]. However, improving access, training on application and handling of available biopesticides particularly M. anisopliae, B. bassiana and B. thuringiensis and proper integration with other pesticides are critical, which could ensure potential market in Tanzania and Africa at large [78]. Since microbial control options for insect pest management are becoming popular globally, it is high time to embark on their commercialization in Africa.

Type Commercial name/ ingredients & source Efficacy Accessibility Reference
Synthetic pesticides Chlorantraniliprole (Coragen, E.I. DuPont de Nemours and Company, New York, USA); Emamectin benzoate (Wiltigo, King Quenson Group, Shenzhen, China); spinetoram (Radiant, Dow Agrosciences, Indianapolis, USA); S For controlling, eggs, larvae and pupae, but with high pest resistance within short time Low application in America, Europe, Asia, recently introduced and misused in Africa with little success [107,114]; Guedes & Picanço, 2012; [121,129]
Traps Pheromone traps (Tuta absoluta-Optima), Russell IPM Company (London, UK) Contain 0.5 mg lure (TDTA and TDDA)/trap for trapping adults America, Europe, Asia, Africa (limited access) mainly for monitoring Desneux et al., 2010; [122] Ostrauskas & Ivinskis, 2010
Botanicals Azadirachta indica Eggs and larvae Africa, America, Asia Kona et al.,2014
Microbial control Metarhizium anisopliae, Beauveria bassiana, Bacillus thuringiensis (Bt) Aspergillus oryzae (Vuruga Biocide) Larvae, eggs, pupae Canada, USA, Australia, Spain, Mexico, Colombia, South Africa, Kenya, Egypt, and Tanzania Fite et al., 2020;[102]; Contreras et al., 2014; Sabbour & Nayera, 2014; [130]
Nematodes Steinernema carpocapsae, Steinernema feltiae, Heterorhabditis bacteriophora Larvae, pupa and adults No commercialization information, no access in developing countries Batalla-Carrera et al., 2010
Predator Nabis pseudoperous Blaptostethus pallescensPoppius la Larvae, larvae and eggs (under laboratory) Spain [104,117]
Parasitoids Trichogramma achaeae, T. pretiosum, Neochrysocharis formosa, Necremnus tutae, Necremnus near artynes and Necremnus near tidius Eggs and larvae Europe and America, Argentina de Campos et al., 2020; Ballal et al., 2016;Biondi et al., 2013; [108]; Ferracini et al., 2012; Luna et al., 2011; Pratissoli & Parra, 2000
Resistant tomato varieties Unappealing leaf surface, trichome, repellant cues Egg, larvae, adult repellant None are commercially adopted [123] Rakha et al., 2017;[132]
Protected cultivation Application of green/net houses Preventing pest attack physically America, Europe, Asia but less adopted in African countries Cocco, Deliperi, & Delrio, 2013; [112];Ostrauskas & Ivinskis, 2010

Table 2: Current management strategies for controlling Tuta absoluta in invaded regions.

Microbial pesticide potential for commercialization

Aspergillus species particularly A. oryzae have been revealed to infect several insect life stages [47] registered (BCA/IN0005) for controlling Spodoptera frugiperda (fall armyworm) and T. absoluta in Tanzania. This novel microbial control agent could further be evaluated in other African counties as biocontrol of T. absoluta and other pests. Other fungal species such as Aspergillus species have been reported to control various pests in tropical countries [52,79], hence should be further evaluated and commercialized for control of T. absoluta in Africa. This review informs researchers to screen and commercialize new microbial control agents including A. oryzae that is reported to control different stages of T. absoluta including adult females to effective control crop damage in the field (Table 3).

Name Target Activeingredient/utility Application Reference
Bacillus thuringesis, Bacillus sublilis Eggs, larvae Spore/colony forming units commercially available in America, Europe, Asia and Africa Foliar sprays and seed coats for seed and seedling protection Abdullah, 2020; Kamal et al., 2019; Gowtham et al., 2018; Sabbour, 2014; Abd El-Ghany et al. 2016b
Metarhizium anisopliae Eggs, larvae Conidia/metabolites commercialized in America and Europe Applied as direct foliar spray, root endophytes of conidia [127] Contreras et al., 2014)
Beauveria bassiana Eggs, larvae and pupae Conidial formulations commercialized in developed countries Endophytes and foliar spray of formulated conidia [116], Inanli, YoldaÃÃÃÃÂ?????, & Birgücü, 2012; Urbaneja et al., 2012; Abd El-Ghany et al. 2016b
Trichoderma album, Trichoderma harzianum Eggs, larvae and adults Conidia of T. album and T. harzianum in a neem blend no commercial product for T. absoluta Laboratory tested but not commercialized Kaoud, 2014; [118,135-137]
Aspergillus flavus, Aspergillus oryzae (BCA/IN/0005) Eggs, larvae, pupae and adult Infective conidia of A. flavus reported in laboratory where A. oryzae- registered in Tanzania for controlling lepidopterous pests With broad application as biopesticide and potential endophyte of crops in Africa [110,138,139]; Lakhdari et al., 2016; Zekeya et al., 2019; FAO-highlights, 2020

Table 3: List of potential microbial control agents for controlling T. absoluta.

Natural enemies

Parasitoids and predators including Macrolophus pygmaeus and Hymenopteran, respectively, are effective in controlling T. absoluta eggs and larvae and several insect pests helping to reduce damage and suppress population [80-83]. Table 2 shows a list of parasitoids with their revealed efficacy in developed countries [27] few parasitoids are reported for controlling T. absoluta in Africa [80]. However, lack of expertise on parasitoids rearing and parasitism efficacy could be one of the obstacles of utilizing this approach for controlling insect pests in Africa. Hence there is a need for screening and registration of parasitoids as natural controls of T. absoluta in the region.

Botanical extracts

Botanical extracts have been and are currently used for controlling insect pest although only few exist commercially [84,85]. Neem extract has been widely used for the management of crop pests with efficacy against T. absoluta eggs, larvae and pupae [1]. Another study by [103] revealed the potential of using piper extracts for control of T. absoluta on tomato. Studies revealed that botanical extracts are potential sources of active ingredients for controlling pests, particularly T. absoluta and can have enhanced activity when combined with synthetic pesticides [86]. A study by [105] revealed that Orange peel oil have high insecticidal activity against larvae of T. absoluta. Again, other studies revealed that plant extracts are potential larvicides of T. absoluta when prepared and applied appropriately. However, botanical pesticides should be careful handled as they might have side effects as synthetic chemical pesticides in some circumstances [87-89]. Hence, this review highlights potential biological pesticides due to high efficacy, potential for commercialization and safety for sustainable crop production.

Future outlook for controlling Tuta absoluta in Africa

Integrated pest management approach could be effective for sustainable control of Tuta absoluta [90]. Biopesticides from B. bassiana, M. anisoplia B. subtilis and B. thuringiensis have promising results for controlling a broad range of pests [38,91,66]. However, their effectiveness on host pests is diminutive,due context variations compared to native strains that have shown high efficiency on T. absoluta [66].

Thus, there is an urgent need for screening for effective alternative options available in local contexts. Figure 1 summarizes the potential applicability of genus Aspergillus as a biocontrol agent and shows how Aspergillus species can promote plant growth through production of growth hormones such as gibberellins [63,92].

journal-animal-pest

Figure 1: The potential for formulation of novel biopesticide and various modes of application of Aspergillus Species as endophyte/epiphyte enriching plant nutrient levels (NL),in soil upon saprophytic activity and pest control via foliar application to kill eggs,larvae,pupae and moth suppressing pest below economic injury level (EEL) in fields.

It also shows that Aspergillus spp produces phytohormones and has insecticidal activities against agricultural pests [76] and can act as bio-fertilizers by decomposing organic materials [101]. Aspergillus species has a good record in nutrient enhancement and promotion of healthy plant growth [93] whereas A. flavus and A. awamori act upon industrial waste water and heavy metals, providing nutrients and minerals and crop protection [94-96]. A. fumigatus and A. parasiticus are reported to have endophytic activity in plants through production of essential minerals and metabolites [97]; A. oryzae has been reported as a marine endophyte that produces protective metabolites against pests [98]. Aspergillus species are also known for producing metabolites that enhance plant defense against pests and diseases (Sun et al., 2018) and act as a source of metabolites in various environments [99]. Furthermore, [79] have reported activity of A. oryzae against locusts and, more recently, A. flavus has shown significant activity against T. absoluta in Algeria [52]. Locally available entomopathogenic fungi could be potential suppressers of all life stages of T. absoluta including adult moths, and reduce its impact in Africa [47]. However, integrated pest management and biological control are essential for enhancing efficacy [100]. Hence an Aspergillus-based biopesticide could have multiple and integrated applications with other biological control agents. It could be incorporated in irrigation systems, foliar sprays and drenching applications to maximize pest control efforts

Conclusion

Tuta absoluta is a tricky pest to be controlled by a single strategy. Various management options are available in other regions but with little success in Africa. Besides a wider use of synthetic pesticides for management of T. absoluta in most regions, their effectiveness is context based due to varied agroecological conditions leading to failures and increasing cultivation cost. Due to these shortcomings of the available pest management options, this review recommends for commercialization of locally available biocontrol agents in Africa. However, screening for novel microbial agents should be funded and promoted to enhance efficacy, accessibility and applicability for effective management of destructive pest, T. absoluta in Africa.

References

Citation: Zekeya N, Peter H, Mbega E (2021) Prospects of Biological Con trol Agents for Management of Invasive Pest Tuta Absoluta (Lepidoptera:Gelechiidae) In Africa. J Anim Sci Livest Prod Vol:5 No:6

Copyright: This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.