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Article

First Report of Field Efficacy and Economic Viability of Metarhizium anisopliae-ICIPE 20 for Tuta absoluta (Lepidoptera: Gelechiidae) Management on Tomato

by
Fred Peter Kabaale
1,2,3,
Venansio Tumuhaise
2,*,
William Tinzaara
2,
Geoffrey Turyasingura
4,
Sevgan Subramanian
1,
Fathiya Mbarak Khamis
1 and
Komivi Senyo Akutse
1,*
1
International Centre of Insect Physiology and Ecology (icipe), Nairobi P.O. Box 30772-00100, Kenya
2
Department of AgricultureProduction, Faculty of Agriculture, Kyambogo University, Kyambogo P.O. Box 1, Uganda
3
National Teachers’ College, Kaliro P.O. Box 65, Uganda
4
Department of Crop Production and Management, Faculty of Agriculture and Animal Sciences, Busitema University, Arapai Campus, Soroti P.O. Box 203, Uganda
*
Authors to whom correspondence should be addressed.
Sustainability 2022, 14(22), 14846; https://doi.org/10.3390/su142214846
Submission received: 23 September 2022 / Revised: 4 November 2022 / Accepted: 7 November 2022 / Published: 10 November 2022
(This article belongs to the Special Issue Sustainable Integrated Pest Management: Achievements and Challenges)
Versions Notes

Abstract

:
Eco-friendly pest control options are highly needed in food crop production systems to mitigate the hazards of synthetic chemical pesticides. Entomopathogenic fungal biopesticides—Metarhizium anisopliae strains ICIPE 20 (oil-formulation containing 1.0 × 109 conidia/mL) and ICIPE 69 (commercialized biopesticide known as Mazao Campaign®)—were evaluated against Tuta absoluta on tomato through inundative foliar spray and compared with the commonly used pesticide Dudu Acelamectin 5% EC (Abamectin 20 g/L + Acetamiprid 3%) and untreated plot. All the treatments were arranged in a randomized complete block design with three replicates. The field experiments were conducted for two consecutive cropping seasons in Mukono district, Uganda. Tuta absoluta infestation, injury severity on leaves and fruits, fruit yield loss, marketable fruit yield gain and cost–benefit ratio of the treatments were assessed. The results during both seasons showed a significant lower fruit yield loss in M. anisopliae ICIPE 20-treated plots compared to untreated plots, with a marketable fruit yield gain exceeding 22% and a cost–benefit ratio greater than 2.8 (BCR~3). Dudu Acelamectin 5% EC outperformed all the other treatments, but needs to be considered with caution due to its non-target effect and resistance development, whereas M. anisopliae ICIPE 69 performed the least well. In addition, the findings showed the high degree of efficacy and economic viability of these biopesticides as a potential T. absoluta control option in the field. However, it is important to further explore different formulations of these eco-friendly biopesticides, inoculum delivery approach, application frequency, their effectiveness in different agro-ecological zones and compatibility with commonly used pesticides in tomato production systems for sustainable management of T. absoluta.

1. Introduction

Tomato (Solanum lycopersicum L.) is grown and consumed worldwide for its nutritional and health benefits to humans [1,2]. Socioeconomically, the crop is a source of livelihood to many rural, peri-urban and urban farmers. In Africa, tomato yield loss due to biotic stress has been worsened by the invasive tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) [3]. Tomato is the primary host of this pest [4,5] onto which the larvae instars penetrate all aerial parts (stems, leaves, flowers and fruits) during cryptic feeding. This invasive pest from South America [6], if not aptly managed, could cause yield loss as high as 100% in certain situations [7,8]. In addition, it is classified as a quarantine pest which leads to tomato trade restrictions [3], and also lowers tomato fruit market value, increases crop protection costs and consequently upsurges tomato fruit price [9].
Farmers in Africa primarily apply synthetic pesticides to mitigate the impact of T. absoluta [3,10], leading to increased high-risk pesticides doses and increased crop protection costs as a result of more frequent spraying upon attack. Moreover, the efficacy of these synthetic pesticides is challenged by the rapid development of resistance [11] and the cryptic feeding behaviour of T. absoluta larvae [9]. The use of synthetic pesticides is associated with several untenable hazards to humans and the environment, for instance, suppression of non-target beneficial organisms, environmental pollution due to unbiodegradable constituent compounds, toxicity and poisoning to humans leading to chronic health problems such as asthma, hypertension, reproductive complications and cancer [12,13]. Consequently, management of the tomato leafminer using safer alternative control approaches is preferred [14]. Among the sustainable, one safe option being explored is to develop pest-specific microbial biopesticides from entomopathogens [15,16,17,18]. For instance, the fungal-based biopesticide is reported to kill the host insect in 7 to 21 days by contact through a process that starts with viable spores attaching to the cuticle of the insect, germinating and producing a penetrating germ tube and establishing a systemic infection which finally kills the host (https://realipm.com (accessed on 4 July 2019)) [19].
The potential pathogenicity of strains of entomopathogens against T. absoluta, mainly under laboratory conditions, has previously been reported, for instance, entomopathogenic bacteria [20,21], entomopathogenic nematodes [22,23,24] and entomopathogenic fungi (EPF) [25,26,27,28,29,30]. However, the efficacy results under laboratory conditions may not reflect the ecological host range and virulence of entomopathogens in the field [31,32,33]. Thus, the identified potent entomopathogens need to be validated in the field before being developed into commercial products, deployed, adopted and integrated into the IPM package for any pest.
Research is underway at the International Centre of Insect Physiology and Ecology (icipe) to develop entomopathogenic fungal strains of Metarhizium anisopliae (Metch.) into a microbial biopesticide for sustainable T. absoluta control [16]. For instance, among the strains evaluated under laboratory conditions, Akutse et al. [30] reported that M. anisopliae ICIPE 20 caused the 100% mortality of 4th instar larvae, as well as 87.5% mortality of T. absoluta adults. Hence, this isolate was earmarked and suggested to be fielded in efficacy trials—a key step in the development of a biopesticide. Meanwhile, the use of M. anisopliae ICIPE 69 (Campaign®) against T. absoluta in the field was reported [3]; however, the commercial product is not specifically registered for T. absoluta control [16] and field efficacy data are scant. We therefore hypothesized that M. anisopliae ICIPE 20 and ICIPE 69 are not effective and economically viable for managing Tuta absoluta in the field. Therefore, the purpose of this study was to evaluate the efficacy of M. anisopliae ICIPE 20 and ICIPE 69 against T. absoluta on tomato in the field. An assessment of T. absoluta infestation, crop injury severity on leaves and fruits, fruit yield loss and the economic viability of these candidate biopesticide products under natural infestation in the field was conducted.

2. Materials and Methods

2.1. Experimental Site, Field Preparation and Raising Seedlings

Field experiments were conducted at Mukono Zonal Agricultural Research & Development Institute (Mukono ZARDI), Mukono district, Uganda (0°23′02.3″ N 32°44′03.4″ E), for two cropping seasons: season 1 (April–July 2019) and season 2 (December 2019–March 2020). The experimental field was prepared by slashing, ploughing and harrowing. It was then divided into twelve experimental plots, each measuring 4 × 5 m with inter-plot spaces of 1 m in width.
The tomato seedlings (variety: Rambo F1) were raised in a screen house. The seeds were first sown into a seed tray and managed until germination. Polypots of 5 cm in diameter and 10 cm in height were filled with potting soil that was prepared by mixing sieved forest soil (2 parts) and coarse sand (1 part). The seedlings were pricked-out into polypots and managed up to four weeks, at which time they were transplanted.

2.2. Transplanting and Subsequent Field Management

In each experimental plot, transplanting holes were dug at a spacing of 0.60 m within a row and 0.75 m between rows, resulting into 6 rows with 9 plants per row and a population of 54 plants per plot. The transplanted seedlings were watered whenever necessary by means of a watering can, using water obtained from a fishpond. Weeding was conducted as required, mainly using a hand hoe. Mulching was conducted using dry grass. Staking was conducted using bamboo stems. No fungicides, fertilizer or other pesticides were applied to the experiment during the trials. The experimental field was regularly scouted to ascertain presence of T. absoluta, based on visual characteristic injury symptoms on the tomato plants [34,35,36]. The level of T. absoluta infestation and leaf and leaflet damage in experimental plots on the date of commencement of treatment application (prior to treatment) was recorded.

2.3. Experimental Design and the Treatments

The experiment was laid out in a randomized complete block design (RCBD) with three replicates. The four treatments involved were applied in the evening between 1600 and 1800 HRS (East African Time) at a weekly interval as a foliar spray. During application, separate hand-operated knapsack sprayers were used for the entomopathogenic fungal products and synthetic chemical pesticide to avoid cross contaminations. The treatments were:
i.
Metarhizium anisopliae isolate ICIPE 20: This was obtained from the International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya, as dry conidia produced on grain rice. The freshly produced dry conidia had a >95% viability. The haemocytometer quantification method described by Inglis et al. [37] was used to determine the concentration of conidia per gram of the isolate. A conidial suspension was prepared by adding 0.01 g of M. anisopliae ICIPE 20 dry conidia to 100 mls of sterile distilled water mixed with Triton X-100 (0.05%) in a conical flask, and vortexed for 5 min at ~700 rpm. From the suspension, 1 mL was pipetted into the improved Neubauer haemocytometer and, thereafter, conidia were counted under a light microscope. The average number of propagules per ‘cell’ was multiplied by the volume conversion factor (2.5 × 105) to obtain the number of propagules per ml of suspension. The quantity of dry conidia of M. anisopliae ICIPE 20 required to provide a concentration of 1.0 × 109 conidia/mL (equivalent to field application rate of the commercial product M. anisopliae ICIPE 69) for field application was computed. Subsequently, the procedure described by Ummidi and Vadlamani [38] was followed in the preparation of an oil-in-water formulation of M. anisopliae ICIPE 20. For the aqueous formulation, fungal spores were suspended in water containing 0.05% Integra (sticker, Greenlife Crop Protection Africa Ltd, Nairobi, Kenya) with 0.1% nutrient agar, 0.1% glycerine and 0.5% molasses added as protectants and attractants, respectively, whereas in oil formulation, spores were suspended in canola oil with similar proportions of the sticker, nutrient agar, glycerine and molasses, as described above in aqueous formulation. An aqueous M. anisopliae ICIPE 20 propagule suspension was prepared and added to a mixture of Triton X-100 (at 1% v/v) and canola oil (at 1% v/v). The mixture was then vortexed to obtain a homogenized stable formulation. During application, the oil-in-water formulation of M. anisopliae ICIPE 20 was mixed with water at a rate of 10 mL in 20 L of water and the mixture was applied at a rate of 400 mL/Ha.
ii.
Metarhizium anisopliae isolate ICIPE 69: This is commercially registered as Campaign® and was obtained from Real IPM (U) Ltd., Kampala, Uganda. It is an oil dispersion containing M. anisopliae ICIPE 69 at a concentration of 1.0 × 109 cfu/mL, with a pre-harvest interval (PHI) of 0 day. The product is registered in South Africa for control of mealybugs, thrips and leafminers, whereas in Uganda, it was registered for thrips, fruit flies, and mealybugs [16]. The microbial biopesticide kills the host insect in 7 to 21 days (https://realipm.com (accessed on 4 July 2019)). During application, the oil-in-water formulation of M. anisopliae ICIPE 69 was mixed with water at a rate of 10 mL in 20 L of water and the mixture was applied at the rate of 400 mL/Ha.
iii.
Dudu Acelamectin (Abamectin 20 g/L + Acetamiprid 3%): This was obtained from Africa One Farmer’s Shop, an agro-input shop in Container Village, Kampala, Uganda. Dudu Acelamectin 5% EC is recommended for effective control of leafminers, thrips, mites, beetles, fruit flies and plant bugs. It has the active ingredients Abamectin 20 g/L + Acetamiprid 3%, with PHI of 7 days (http://bukoolachemicals.com (accessed on 16 June 2019)). The recommended mixing of the pesticide is 20–30 mL of Dudu Acelamectin in 20 L of water, a rate equivalent to 400–500 mL/Ha, to be sprayed at an interval of 7–14 days. During application, this pesticide was mixed with water at a rate of 20 mL in 20 L of water and the mixture was applied at a rate of 400 mL/Ha.
iv.
Untreated plot: the negative control plots were sprayed with distilled sterile water at a rate of 400 L/Ha.

2.4. Assessing Tuta absoluta Infestation

The scouting of each plot was conducted to identify T. absoluta injury on tomato plants. Through visual observation and counting, the total number of plants in each plot and the number of plants with signs of T. absoluta injury were recorded prior to treatment and at the start of harvesting (after treatment). All the injured plants were left in the plots (non-destructive sampling). Tuta absoluta infestation was computed using Formula (1) [39]:
T u t a   a b s o l u t a   infestation = Total   number   of   injured   plants   in   a   plot Total   number   of   plants   in   the   plot   ×   100

2.5. Assessing Leaf and Leaflet Damage by Tuta absoluta

The ten innermost plants from each plot were assessed through visual observation to establish the leaves and leaflets injured by T. absoluta. On each plant, the total number of leaves and number of injured leaves were recorded. In addition, the total number of leaflets on injured leaves and number of specific leaflets bearing T. absoluta injury symptoms were recorded. As a non-destructive sampling approach, all injured leaves and leaflets were left on the plants. The percentages of damaged leaves and leaflets were then computed using Formulas (2) and (3) [39]:
Percentage   leaf   damage = Total   number   of   injured   leaves   on   the   plant   Total   number   of   leaves   on   the   plant   ×   100
Percentage   leaflet   damage = Total   number   of   injured   leaflets   on   the   plant   Total   number   of   leaflets   on   the   injured   leaves   ×   100

2.6. Assessing Fruit Damage by Tuta absoluta

The ten innermost plants from each plot were assessed through visual observation to establish fruits injured by T. absoluta. On each plant, the total number of fruits and the number of injured fruits was recorded (before the start of harvesting). All the injured fruits were left on the plants after assessment. The percentage fruit damage was then computed using Formula (4) [39]:
Percentage   fruit   damage = Total   number   of   injured   fruits   on   the   plant Total   number   of   fruits   on   the   plant   ×   100

2.7. Assessing Fruit Yield Loss Due to Tuta absoluta

The procedure followed was similar to the one described by Ghaderi et al. [40]. Mature fruits at the pink stage of ripening were harvested from the ten innermost plants of each plot. At each harvest, visual fruit inspection was conducted to sort injured fruits. The weights of both injured and healthy fruits were measured using a mechanical Salter kitchen weighing scale and recorded. The percentage fruit yield loss of each plot was then computed as per Formula (5):
Fruit   yield   loss   ( % ) = Weight   of   injured   fruits   ( Weight   of   healthy   fruits + Weight   of   injured   fruits )   ×   100

2.8. Assessing the Economic Viability of Treatments

2.8.1. Marketable Fruit Yield in Treated Plots Compared to Untreated Plot

The cumulative weight of healthy (marketable) fruits harvested from the ten innermost plants of each plot was recorded. This weight was used to compute marketable fruits weight per plant, then extrapolated to per plot and eventually marketable fruit yield (MFY) per hectare was computed as described by Shabozoi et al. [41]. The untreated plot was used as a standard for comparison with performance of treatments. The cumulative MFY in the treated plots above the untreated plots was considered as MFY gain, the percentage of which was computed using Formula (6) [42]:
MFY   gain   ( % ) = MFY   in   the   treated   plot   -   MFY   in   untreated   plot MFY   in   untreated   plot     ×   100

2.8.2. Cost–Benefit Analysis

The cost of the pesticide, pesticide application equipment, labour for pesticide application and labour for harvesting the additional yield of the treated plot above the yield recorded from the untreated control plot were totalled. This total represented the season crop protection cost for each experimental plot, which was extrapolated to cost per hectare. The cost of each unit of M. anisopliae ICIPE 20 was equated to the price of each unit of M. anisopliae ICIPE 69 (UG Shs. 15,000 (USD 4.05) per 20 mL sachet). The pesticide application equipment bought at UG Shs. 150,000 (USD 40.5) was costed at UG Shs. 50,000 (USD 13.5) based on depreciation over an estimated 3-year lifespan. The costs for other items were taken as per the prevailing market prices. Labour for pesticide application per spray per hectare was fixed at UG Shs. 125,000 (USD 33.78). The harvesting of additional yield from treated plots above the yield from the untreated plot was fixed at an estimated average of UG Shs. 100,000 (USD 27.03) per tonne.
To compute the revenue per hectare for each experimental plot, the average farm-gate price of tomato fruits was fixed at UG Shs. 1200 (USD 0.32) per kilogram [43]. Then, price per kilogram of tomato fruits was multiplied by MFY (kg) per hectare. The revenue from the untreated plot was deducted from that of each treated plot to obtain the benefit (value of yield of treated plot above value of the yield of untreated plot) for the respective treatments, following the approach described by Shabozoi et al. [41]. Thereafter, the cost–benefit ratio (BCR) of each treatment was calculated using Formula (7) [44]:
Cost – benefit   ratio = Benefit   of   the   treatment   Treatment ’ s   total   crop   protection   cost  

2.9. Data Analysis

The data on T. absoluta infestation, percentage damage of leaves and leaflets within each experimental plot prior to treatment and after treatment were subjected to a t-test. To compare treatments’ T. absoluta infestation, damage of leaves, leaflets and fruits, fruit yield loss and marketable fruit yield, the data were subjected to analysis of variance (ANOVA). The differences in means were separated using Fisher’s protected least significant difference (LSD) at 5% probability. The analyses were conducted using GenStat computer software (12th Edition for Windows, VSN International Ltd., Hemel Hempstead, UK). The data on MFY gain due to treatment application were expressed as percentage [42], whereas the BCR of each treatment was evaluated using the rule for BCR [45].

3. Results

3.1. Tuta absoluta Infestation in the Experimental Field

Prior to treatment, T. absoluta infestation ranged from 29.58 ± 3.24 to 31.61 ± 1.25% and 27.03 ± 7.69 to 40.85 ± 3.48%, in season 1 and season 2, respectively. There was no significant difference in T. absoluta infestation among the treatment plots during both season 1 (F3,6 = 0.14, p = 0.932) and season 2 (F3,6 = 2.77, p = 0.133) (Table 1).
After treatment, the results showed the highest rise in T. absoluta infestation (though not significant) within untreated plots (t test: t2 = −1.36, p = 0.308), followed by M. anisopliae ICIPE 20 (t test: t2 = −0.63, p = 0.592) and M. anisopliae ICIPE 69 (t test: t2 = −0.34, p = 0.763) treated plots, during season 1. However, a significant (t test: t2 = 5.01, p = 0.038) reduction in T. absoluta infestation within Dudu Acelamectin-treated plots was observed (Table 1). During season 2, results showed a general reduction in T. absoluta infestation (though not significant) which was greatest within Dudu Acelamectin-treated plots, followed by M. anisopliae ICIPE 20, M. anisopliae ICIPE 69 and the lowest in untreated plots (Table 1). When the treatments were compared, the results showed a significant difference in T. absoluta infestation during season 1 (F3,6 = 9.72, p = 0.010), but not in season 2 (F3,6 = 3.53, p = 0.088) (Table 1). The highest T. absoluta infestation was observed in untreated plots and the lowest in Dudu Acelamectin-treated plots during both seasons 1 and 2 (Table 1).

3.2. Leaf Damage by Tuta absoluta

Prior to treatment, mean leaf damage by T. absoluta ranged from 4.94 ± 1.79 to 7.94 ± 2.54% and 7.30 ± 1.52 to 12.84 ± 6.21%, during season 1 and season 2, respectively. There was no significant difference in the level of leaf damage among the experimental plots during season 1 (F3,6 = 1.59, p = 0.288) and season 2 (F3,6 = 0.65, p = 0.611) (Table 2).
After treatment, season 1 results showed a significant rise in leaf damage by T. absoluta within untreated plots (t test: t2 = −12.86, p = 0.006). The rise in leaf damage by T. absoluta was not significant within the plots treated with M. anisopliae ICIPE 20 (t test: t2 = 1.04, p = 0.406) and M. anisopliae ICIPE 69 (t test: t2 = −0.95, p = 0.442), with the former showing the least. On the other hand, reduced leaf damage by T. absoluta (though not significant) was observed within Dudu Acelamectin-treated plots (Table 2). During season 2, the results showed reduction in leaf damage by T. absoluta (though not significant) which was greatest within Dudu Acelamectin, followed by M. anisopliae ICIPE 69 and lowest in M. anisopliae ICIPE 20-treated plots. The untreated plots showed increased leaf damage by T. absoluta, though this was not significant (Table 2). When the treatments were compared, the results showed a significant difference in leaf damage by T. absoluta during season 1 (F3,6 = 98.60, p < 0.001). Leaf damage levels were significantly lower in Dudu Acelamectin, M. anisopliae ICIPE 20- and M. anisopliae ICIPE 69-treated plots than untreated plots (Table 2). During season 2, there was no significant difference observed (F3,6 = 3.70, p = 0.081). The highest leaf damage by T. absoluta was observed in untreated plots, whereas the lowest was in Dudu Acelamectin-treated plots (Table 2).

3.3. Leaflet Damage by Tuta absoluta

Prior to treatment, mean leaflet damage was not significantly different among the various plots during season 1 (F3,6 = 1.12, p = 0.414) and season 2 (F3,6 = 1.03, p = 0.445). The level of leaflet damage ranged from 15.07 ± 1.77 to 18.78 ± 1.28%, and 19.81 ± 10.27 to 34.40 ± 2.39%, in season 1 and season 2, respectively (Table 3).
After treatment, the season 1 results showed general rise of leaflet damage by T. absoluta (though not significant) which was lowest within Dudu Acelamectin, followed by M. anisopliae ICIPE 20- and M. anisopliae ICIPE 69-treated plots, and greatest within untreated plots (Table 3). During season 2, the results showed reduction in leaflet damage by T. absoluta (though not significant) which was greater within M. anisopliae ICIPE 20 compared to M. anisopliae ICIPE 69-treated plots. Dudu Acelamectin-treated plots showed a significant reduction in leaflet damage (t test: t2 = 6.14, p = 0.026), whereas a rise of leaflet damage by T. absoluta (though not significant) was observed within untreated plots (Table 3). When the treatments were compared, the results showed a significant difference in leaflet damage by T. absoluta during season 1 (F3,6 = 17.08, p = 0.002). Leaflet damage levels were significantly lower in Dudu Acelamectin, M. anisopliae ICIPE 20- and M. anisopliae ICIPE 69-treated plots than untreated plots (Table 3). During season 2, there was no significant difference observed (F3,6 = 1.86, p = 0.238). However, leaflet damage by T. absoluta was lowest in Dudu Acelamectin-treated plots, followed by M. anisopliae ICIPE 20 and highest in untreated plots (Table 3).

3.4. Fruit Damage by Tuta absoluta

The results showed a significant difference in fruit damage by T. absoluta during season 1 (F3,6 = 5.17, p = 0.042). Fruit damage was lowest in Dudu Acelamectin-treated plots and highest in untreated plots. Significantly lower fruit damage was observed in plots treated with Dudu Acelamectin and M. anisopliae ICIPE 20 compared to untreated plots (Table 4). During season 2, there was no significant differences observed (F3,6 = 1.36, p = 0.341). However, fruit damage level was lowest in Dudu Acelamectin-treated plots followed by M. anisopliae ICIPE 20, M. anisopliae ICIPE 69 and highest in untreated plots (Table 4).

3.5. Fruit Yield Loss Due to Tuta absoluta

The results showed significant differences in fruit yield loss due T. absoluta during both season 1 (F3,6 = 22.38, p = 0.001) and season 2 (F3,6 = 68.81, p < 0.001). During season 1, fruit yield loss was significantly lower in Dudu Acelamectin, M. anisopliae ICIPE 20-and M. anisopliae ICIPE 69-treated plots compared to untreated plots (Table 4). During season 2, significantly higher fruit yield loss was observed in untreated plots compared to other treatments. In addition, fruit yield loss in Dudu Acelamectin-treated plots was significantly lower compared to M. anisopliae ICIPE 20- and M. anisopliae ICIPE 69-treated plots (Table 4).

3.6. Marketable Yield Gain Due to Treatments for Managing Tuta absoluta on Tomato in the Field

The results showed greater marketable fruit yield (MFY) in all treated plots compared to untreated plots during both season 1 and season 2 (Table 4). During season 1, the least well performing M. anisopliae ICIPE 69-treated plots showed 2.66 ton/ha above the untreated plots, whereas the best performing Dudu Acelamectin-treated plots showed an excess of 6.26 ton/ha. Accordingly, overall MFY gain exceeded 55% during season 1, lowest in M. anisopliae ICIPE 69-treated plots and highest in Dudu Acelamectin-treated plots (Table 4). During season 2, a similar trend of treatment performance was observed, with overall MFY gain exceeding 15%. The least well performing M. anisopliae ICIPE 69-treated plots showed 1.75 ton/ha above the untreated plots, whereas the best performing Dudu Acelamectin-treated plots showed an excess of 4.55 ton/ha (Table 4).

3.7. Cost–Benefit Ratio of the Treatments for Managing Tuta absoluta on Tomato in the Field

The results showed that revenue from MFY per hectare was lowest in untreated plots compared to other treatments during both season 1 and season 2. During season 1, the revenue was highest in Dudu Acelamectin-treated plots, followed by M. anisopliae ICIPE 20- and M. anisopliae ICIPE 69-treated plots, respectively. Accordingly, the benefit of treatment application was greatest in Dudu Acelamectin-treated plots, followed by M. anisopliae ICIPE 20- and M. anisopliae ICIPE 69-treated plots, respectively (Table 5). A similar trend of treatment performance was observed during season 2 (Table 5). The total crop protection cost was highest in M. anisopliae ICIPE 20-treated plots, followed by M. anisopliae ICIPE 69, and lowest in Dudu Acelamectin-treated plots, during both season 1 and season 2 (Table 5). Concomitantly, the highest BCR was observed in Dudu Acelamectin-treated plots, followed by M. anisopliae ICIPE 20-treated plots, and lowest in M. anisopliae ICIPE 69-treated plots, during both season 1 and season 2 (Table 5).

4. Discussion

The results of both season 1 and season 2 generally demonstrated a degree of restriction of T. absoluta infestation and injury severity on leaves and fruits where M. anisopliae ICIPE 20 and M. anisopliae ICIPE 69 were applied. Similar findings have also been reported by El-Aassar et al. [46] in Egypt where the biopesticides Biovar® and Bioranza® with Beauveria bassiana (Balsamo.) and M. anisopliae as active ingredients, respectively, were found to be efficient against T. absoluta larvae and larval infestation in the field. In addition, this study found significantly lower leaf damage, leaflet damage and fruit damage during season 1 in M. anisopliae ICIPE 20-treated plots compared to untreated plots, as reported by Shiberu and Getu [47] when using B. bassiana to tackle the pest in Ethiopia. In fact, untreated plots generally showed highest T. absoluta infestation, leaf damage and leaflet and fruit damage in both season 1 and 2. Interestingly, tomato fruit yield loss was significantly lower in plots treated with M. anisopliae ICIPE 20 and M. anisopliae ICIPE 69 than that of untreated plots during both seasons. This phenomenon seems to point towards a level of field efficacy of these fungal entomopathogens for managing T. absoluta on tomato, as also reported by previous studies [46,47]. Although there exists scant information on the field efficacy of fungal entomopathogens against T. absoluta, the findings of this study seem to concur with previous field studies of: (i) El-Aassar et al. [46], where reduction in tomato leaf area infestation by application of M. anisopliae (Bioranza®) was reported, and (ii) Shiberu and Getu [47], which reported a reduction in tomato fruit yield loss due to application of M. anisopliae.
Our results further showed a marketable fruit yield gain in M. anisopliae ICIPE 20- and M. anisopliae ICIPE 69-treated plots. This is an indication of improved marketable fruit yield through the application of the fungal entomopathogens compared to untreated plots. The higher marketable fruit yield in the treated plots compared to the untreated plots seems to imply a level of suppression of the activity of T. absoluta. As a result, there was better photosynthesis, growth, development, flower and fruit retention by tomato plants, and hence better yields, and also less damaged fruits in the treated plots. In fact, the fruit yield gain can be a desirable efficacy parameter in the evaluation of these T. absoluta management products [48]. These findings seem to concur with field studies of Ndereyimana et al. [49] and Shiberu and Getu [47], that reported improved tomato productivity in plots treated with M. anisopliae compared to the untreated control. Alongside the marketable fruit yield gain, the cost–benefit ratio (BCR) of applying M. anisopliae ICIPE 20 and M. anisopliae ICIPE 69 exceeded 1, during both season 1 and 2. The BCR > 1 is among the indicators of economic viability of pest control measures. In spite of the shortage of data on the BCR of fungal entomopathogens against T. absoluta on tomato, the findings of this study seem to corroborate those on other lepidopteran pests where BCR values > 1 were reported such as (i) the use of M. anisopliae against Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) [50] and (ii) the use B. bassiana against H. armigera [51]. Our results further corroborate previous studies on non-lepidopteran pests including (i) the use of B. bassiana and Lecanicillium lecanii against the sucking pests of green gram [52], (ii) the use of B. bassiana against Clavigralla gibbosa Spinola (Hemiptera: Coreidae) [53] and (iii) the use of B. bassiana, Paecilomyces fumosoroseus and Verticillium lecanii against groundnuts pests [54].
The findings generally indicated that Dudu Acelamectin performed better than M. anisopliae ICIPE 20, which also performed better than M. anisopliae ICIPE 69 for all parameters assessed. The observed outperformance trend for Dudu Acelamectin was probably due to the quicker action and broad-spectrum nature of this synthetic pesticide (http://bukoolachemicals.com (accessed on 16 June 2019)). Furthermore, the performance of the fungal entomopathogens may probably be attributed to their slow infection mechanism as compared to synthetic pesticide [55]; the dosage used may not be the most ideal and their vulnerability to field weather conditions [33,56]. The better performance of M. anisopliae ICIPE 20 compared to M. anisopliae ICIPE 69 could be related to its high efficacy under laboratory conditions where mortality rates of 87.5 and 100% were recorded among T. absoluta adults and fourth instar larvae, respectively [30]. In addition, the lower performance of M. anisopliae ICIPE 69 compared to ICIPE 20 may be attributed to the fact that the former could be more effective in controlling leafminers other than T. absoluta [16].
Furthermore, although the synthetic pesticide Dudu Acelamectin consistently outperformed the biopesticide products (M. anisopliae ICIPE 20 and ICIPE 69) does not necessarily imply that it is the best option for managing T. absoluta. It is globally acknowledged that synthetic pesticides are a great danger to biodiversity as they kill non-target beneficial organisms and cause environmental pollution including toxicity and poisoning to humans which can lead to chronic health problems [12,13]. Therefore, in spite of the lower performance of M. anisopliae ICIPE 20 and ICIPE 69 compared to Dudu Acelamectin, the entomopathogenic fungal biopesticides are generally associated with plenty of non-monetary benefits. For instance, they are not toxic and poisonous to humans [57], are harmless to beneficial organisms such as pollinators [58], leave no toxins in the environment [59], leave no toxic residues in the food product [60] and the pest cannot develop resistance against them [16]. In addition, there is no risk of an alarming rise in the EPF inoculum levels in agricultural fields when applications are stopped [61], therefore strengthening the safety advantages of biopesticides as nature-based solutions to the environment, human and biodiversity health [62]. These attributes eventually make the fungal biopesticides more appealing in food crop farming systems. However, the study efficacy results reported herein might not be conclusive, as they are based on one agro-ecological zone, on small scale, using a single dosage and formulation of candidate entomopathogenic fungal biopesticide products.

5. Conclusions

The findings could be a promising milestone for the candidate entomopathogenic fungal biopesticides for managing T. absoluta on tomato sustainably in the field. The biopesticide products showed better results compared to untreated plot, with M. anisopliae isolate ICIPE 20 being found to be more efficacious than ICIPE 69, and with a BCR of 4.31. In addition, the marketable fruit yield gain and the cost–benefit ratio (BCR) of applying M. anisopliae ICIPE 20 and M. anisopliae ICIPE 69 exceeded 1 during both cropping seasons. Considering the BCR > 1 and safety of these tested bioproducts, which are among the key indicators of the economic viability of pest control measures, M. anisopliae ICIPE 20 could be developed as a potential biopesticide for the sustainable management of T. absoluta. However, further studies are warranted before they are developed into commercial products, and deployed and promoted for safer control of T. absoluta in tomato production systems. Therefore, further studies are recommended to assess M. anisopliae ICIPE 20 and M. anisopliae ICIPE 69 at different dosages and formulations, application frequency, different agro-ecological zones, large scale and also assess their compatibility with the pesticides commonly used in tomato production. In addition, despite the good performance of Dudu Acelamectin, this synthetic pesticide should be used with caution for T. absoluta management because of its toxicity, causing an increase in environmental pollution, and development of pest-resistant pest populations, as well as the effects on non-target organisms, especially pollinators and natural enemies, and the cost implications.

Author Contributions

Conceptualization, F.P.K., V.T., K.S.A., S.S., F.M.K. and G.T.; formal analysis, F.P.K., V.T. and K.S.A.; funding acquisition, V.T., F.M.K., S.S. and K.S.A.; investigation, F.P.K., V.T., K.S.A., G.T. and W.T.; writing original draft, F.P.K., V.T., K.S.A., G.T. and W.T.; writing review and editing, F.P.K., V.T., K.S.A., G.T., F.M.K., S.S. and W.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the BioInnovate Africa Phase I project “Promoting smallholder access to fungal biopesticides through Public Private Partnerships in East Africa” (BA/CI/2017-02 (PROSAFE), UK’s Foreign, Commonwealth & Development Office (FCDO) (DFID Biopesticide Project, B2291A-DFID-BIOPESTICIDE) and African Union (AU) (Tuta-IPM Project, Contract number: AURG II-2-123-2018), through the International Centre of Insect Physiology and Ecology (icipe) and Busitema University. The authors gratefully acknowledge icipe core funding provided by the Swedish International Development Cooperation Agency (Sida), the Swiss Agency for Development and Cooperation (SDC), the Federal Democratic Republic of Ethiopia and the Government of the Republic of Kenya.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data related to this work are available upon request from the corresponding author.

Acknowledgments

Experiments of this study were hosted at MuZARDI, for which the authors are grateful.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Table
Table 1. Tuta absoluta mean infestation (±SE) during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Table 1. Tuta absoluta mean infestation (±SE) during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Treatment/SeasonMean ± SE (%)t-Valuep-Value (df = 2)
Prior to TreatmentAfter Treatment
Season 1
Untreated plot30.01 ± 6.06 a36.88 ± 2.88 b−1.360.308
Dudu Acelamectin29.58 ± 3.24 a20.05 ± 2.00 a5.010.038
M. anisopliae ICIPE 6931.61 ± 1.25 a32.64 ± 1.82 b−0.340.763
M. anisopliae ICIPE 2030.74 ± 2.29 a32.47 ± 1.18 b−0.630.592
p-value (df = 3)0.9320.010
Season 2
Untreated plot33.92 ± 1.17 a30.94 ± 1.74 a1.150.370
Dudu Acelamectin39.79 ± 6.83 a18.51 ± 4.50 a3.540.071
M. anisopliae ICIPE 6927.03 ± 7.69 a22.12 ± 4.58 a1.450.283
M. anisopliae ICIPE 2040.85 ± 3.48 a29.51 ± 1.89 a3.430.076
p-value (df = 3)0.1330.088
df = degrees of freedom. SE = standard error. In a season, means with the same letter in a column are not significantly different by Fisher’s protected LSD test (p = 0.05).
Table
Table 2. Mean leaf damage (±SE) by Tuta absoluta during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Table 2. Mean leaf damage (±SE) by Tuta absoluta during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Treatment/SeasonMean ± SE (%)t-Valuep-Value (df = 2)
Prior to TreatmentAfter Treatment
Season 1
Untreated plot4.94 ± 1.79 a18.58 ± 2.39 d−12.860.006
Dudu Acelamectin7.94 ± 2.54 a6.06 ± 1.46 a2.500.130
M. anisopliae ICIPE 696.91 ± 1.78 a12.76 ± 1.49 c−0.950.442
M. anisopliae ICIPE 207.82 ± 1.46 a8.78 ± 2.39 b1.040.406
p-value (df = 3)0.288<0.001
Season 2
Untreated plot7.30 ± 1.52 a11.36 ± 2.68 a−1.850.205
Dudu Acelamectin10.46 ± 4.26 a4.86 ± 1.56 a1.800.214
M. anisopliae ICIPE 6912.84 ± 6.21 a8.96 ± 2.77 a0.790.513
M. anisopliae ICIPE 208.12 ± 5.34 a6.96 ± 2.32 a0.220.846
p-value (df = 3)0.611 0.081
df = degrees of freedom. SE = standard error. In a season, means with the same letter in a column are not significantly different by Fisher’s protected LSD test (p = 0.05).
Table
Table 3. Mean leaflet damage (±SE) by Tuta absoluta during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Table 3. Mean leaflet damage (±SE) by Tuta absoluta during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Treatment/SeasonMean ± SE (%)t-Valuep-Value (df = 2)
Prior to TreatmentAfter Treatment
Season 1
Untreated plot15.07 ± 1.77 a28.84 ± 1.62 c−3.620.069
Dudu Acelamectin15.50 ± 1.93 a15.54 ± 0.65 a0.600.612
M. anisopliae ICIPE 6918.78 ± 1.28 a23.94 ± 1.32 b−2.350.143
M. anisopliae ICIPE 2017.06 ± 0.33 a20.93 ± 1.50 b−3.500.073
p-value (df = 3)0.4140.002
Season 2
Untreated plot21.16 ± 2.13 a24.17 ± 5.17 a−0.990.427
Dudu Acelamectin34.40 ± 2.39 a14.40 ± 2.04 a6.140.026
M. anisopliae ICIPE 6919.81 ± 10.27 a17.33 ± 3.54 a0.360.752
M. anisopliae ICIPE 2022.25 ± 5.66 a15.12 ± 3.19 a2.48 0.131
p-value (df = 3)0.4450.238
df = degrees of freedom. SE = standard error. In a season, means with the same letter in a column are not significantly different by Fisher’s protected LSD test (p = 0.05).
Table
Table 4. Fruit damage, fruit yield loss, marketable fruit yield (MFY) and MFY gain during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Table 4. Fruit damage, fruit yield loss, marketable fruit yield (MFY) and MFY gain during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Treatment/SeasonMean ± SE (%)MFY
(ton/ha)		MFY Gain 1
(%)
Fruit DamageFruit Yield Loss
Season 1
Untreated plot26.48 ± 4.13 b43.41± 2.63 b4.81± 0.71 a-
Dudu Acelamectin10.87 ± 1.62 a6.73 ± 3.64 a11.07± 1.18 a130.15
M. anisopliae ICIPE 6918.84 ± 2.61 ab18.41 ± 2.94 a7.47± 1.94 a55.30
M. anisopliae ICIPE 2013.92 ± 1.89 a10.48 ± 4.92 a8.28± 1.72 a72.14
p-value (df = 3)0.0420.0010.173
Season 2
Untreated plot6.03 ± 2.21 a13.01 ± 0.47 c11.04± 2.86 a-
Dudu Acelamectin2.81 ± 0.61 a2.82 ± 0.48 a15.59± 1.06 a41.21
M. anisopliae ICIPE 694.47 ± 1.41 a6.58 ± 1.14 b12.79± 1.38 a15.85
M. anisopliae ICIPE 203.21 ± 1.06 a4.90 ± 0.95 b13.47± 2.25 a22.01
p-value (df = 3)0.341<0.0010.536
df = degrees of freedom. SE = standard error. In a season, means with the same letter in a column are not significantly different by Fisher’s protected LSD test (p = 0.05). 1 Equation (6).
Table
Table 5. Revenue, benefit, crop protection cost and cost–benefit ratio (BCR) per hectare for the treatments during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Table 5. Revenue, benefit, crop protection cost and cost–benefit ratio (BCR) per hectare for the treatments during season 1 (April–July 2019) and season 2 (December 2019–March 2020).
Treatment/SeasonRevenue/ha
(USD)		Benefit/ha 1
(USD)		Crop Protection Cost/ha (USD)BCR 2
Pesticide LabourSprayerTotal
Season 1
Untreated plot1560.00------
Dudu Acelamectin3590.272030.2717.84196.2113.51227.568.92
M. anisopliae ICIPE 692422.70862.70121.62115.9413.51251.073.43
M. anisopliae ICIPE 202685.411125.41121.62125.6713.51260.804.31
Season 2
Untreated plot3580.54------
Dudu Acelamectin5056.221475.6817.84202.9713.51234.326.30
M. anisopliae ICIPE 694148.11567.57121.62129.7313.51264.862.14
M. anisopliae ICIPE 204368.65788.11121.62142.7013.51277.832.84
1 (Revenue from each treatment minus revenue from untreated plot). 2 Equation (7).
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Kabaale, F.P.; Tumuhaise, V.; Tinzaara, W.; Turyasingura, G.; Subramanian, S.; Khamis, F.M.; Akutse, K.S. First Report of Field Efficacy and Economic Viability of Metarhizium anisopliae-ICIPE 20 for Tuta absoluta (Lepidoptera: Gelechiidae) Management on Tomato. Sustainability 2022, 14, 14846. https://doi.org/10.3390/su142214846

AMA Style

Kabaale FP, Tumuhaise V, Tinzaara W, Turyasingura G, Subramanian S, Khamis FM, Akutse KS. First Report of Field Efficacy and Economic Viability of Metarhizium anisopliae-ICIPE 20 for Tuta absoluta (Lepidoptera: Gelechiidae) Management on Tomato. Sustainability. 2022; 14(22):14846. https://doi.org/10.3390/su142214846

Chicago/Turabian Style

Kabaale, Fred Peter, Venansio Tumuhaise, William Tinzaara, Geoffrey Turyasingura, Sevgan Subramanian, Fathiya Mbarak Khamis, and Komivi Senyo Akutse. 2022. "First Report of Field Efficacy and Economic Viability of Metarhizium anisopliae-ICIPE 20 for Tuta absoluta (Lepidoptera: Gelechiidae) Management on Tomato" Sustainability 14, no. 22: 14846. https://doi.org/10.3390/su142214846

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