Spodoptera frugiperda population structure and influence of farmers’ practices on gut biodiversity for sustainable management of the pest in Kenya

Fall armyworm (FAW), Spodoptera frugiperda, is a highly polyphagous pest that recently invaded Kenya, among other African countries. Information on the pest’s genetic diversity and mechanisms conferring insecticide resistance, in addition to farmers’ knowledge and perceptions on the applicable mitigation measures, inform the development of sustainable management strategies. Therefore, this study collected cross-sectional data from 800 farmers in Kenya and documented their knowledge and perceptions on FAW and factors influencing their choice of FAW control methods. Additionally, we identified the strains present in 8 counties in Kenya using the mitochondrial Cytochrome Oxidase sub-unit I (mt COI) gene, and correlated pesticide use to gut microbiome diversity via 16S rRNA metagenomics to investigate the probable contribution of gut bacteria towards insecticide resistance evolution. All farmers reported FAW infestations, and 24% reported limited and total non-response of FAW to insecticides. Fall armyworm rice-strain and corn-strain were detected ravaging corn fields. However, the corn-strain revealed higher microbial diversity than the rice-strain. Furthermore, pathogenic bacterial genera were elevated in the insect gut in both corn and rice strains after chemical-treatments. Insecticide–endosymbiont interactions should be further explored, and farmers’ training on effective alternative pest control methods is recommended

One stone for two birds: Endophytic fungi promote maize seedlings growth and negatively impact the life history parameters of the fall armyworm, Spodoptera frugiperda

The fall armyworm (FAW) Spodoptera frugiperda, is a voracious pest of cereals native to the Americas and which invaded Africa in 2016. Chemical control is the main management option, which however remains ineffective and unsustainable. Fungal endophytes are increasingly used as alternative for the management of insect pests of economic importance. This study assessed the potential of eight endophytic fungal isolates to colonize maize plant and their ability to promote seedlings growth through seed and foliar inoculations, as well as their suppressive effects on FAW. Fungal colonization rates of different plant parts by the endophytes varied as per the inoculation methods. Beauveria bassiana ICIPE 279 colonized more than 60% of all the seedling parts while B. bassiana G1LU3 only colonized stem (25%) and leaf (5%) tissues through foliar inoculation. Trichoderma atroviride F2S21, T. asperellum M2RT4, T. harzianum F2R41, Trichoderma sp. F2L41, Hypocrea lixii F3ST1 and Fusarium proliferatum F2S51 successfully colonized all the plant parts and therefore were selected and further evaluated through seed inoculation for their endophytic persistence, effect on plant growth, and pathogenicity to Spodoptera frugiperda immature and adult stages. Weekly assessment showed varied effect of the endophytes on maize plant growth parameters compared to the control. During the first week, percentage colonization of the plant parts ranges between 90%–100%, 65%–100%, and 60%–100%, in the roots, stems, and leaves, respectively for all the five tested isolates. However, the colonization pattern/rates significantly decreased over time for H. lixii F3ST1 in the stems and leaves, and for T. harzianum F2R41 in the leaves and for T. asperellum M2RT4 in the roots. In addition, T. harzianum F2R41 outperformed all the other isolates in boosting the plant height, whereas H. lixii F3ST1 and T. asperellum M2RT4 outperformed all the other isolates in increasing the wet and dry shoots weight. Furthermore, the number of egg masses laid on endophytically-colonized maize plants varied among the treatments. Trichoderma asperellum M2RT4 and H. lixii F3ST1 endophytically-colonized maize plants significantly reduced the number of egg masses and the defoliation/feeding rates of the pest compared to the control. Additionally, T. harzianum F2R41 had the highest negative impact on the pupation and adult emergence of S. frugiperda with a female-biased sex ratio. Our findings indicate that T. asperellum M2RT4, T. harzianum F2R41, and H. lixii F3ST1 hold a potential to be developed as endophytic-fungal-based biopesticides for sustainable management of S. frugiperda and as plant growth promoters

The Endophyte Trichoderma asperellum M2RT4 induces the systemic release of methyl Salicylate and (Z)-jasmone in tomato plant affecting host location and herbivory of Tuta absoluta

The use of endophytic fungi has dramatically increased plant performance through the enhancement of plant protection against abiotic and biotic stressors. We previously demonstrated that the endophytic fungus Trichoderma asperellum M2RT4 improves tomato defenses against the tomato leafminer Tuta absoluta through the reduction of oviposition, leafmining, pupation, and adult emergence. However, the underlying mechanism by which the presence of this endophytic fungus within tomato host plant affects T. absoluta host selection and life-history traits is unknown. We tested the behavioral responses of T. absoluta in Y-tube olfactometer bioassays and found that females preferred non-inoculated tomato plants against those inoculated by endophytes. Additionally, T. absoluta females were not attracted to non-inoculated infested nor to inoculated-infested tomato plants. Chemical analysis revealed the emission of methyl salicylate in inoculated tomato plant and an increase in the amounts of monoterpenes emitted from non-inoculated infested plants. Additionally, we found that upon herbivory, T. asperellum M2RT4 modulates tomato plant chemistry through the production of (Z)-jasmone thus activating both salicylic and jasmonic acid defense pathways. Further, T. absoluta females were attracted to monoterpernes including α-pinene, 2-carene, and β-phellandrene but repelled by methyl salicylate. Methyl salicylate could therefore be considered as a good semiochemical-based candidate for sustainable T. absoluta management using a “push-pull” approach. However, in dose-response bioassays, females of T. absoluta did not show any preference to the four component-blend (α-pinene, 2-carene, β-phellandrene, and methyl salicylate). (Z)-jasmone-treated tomato leaflets significantly reduced the leafmining activity of the pest at the concentration of 10 ng/µL and causing the highest larval mortality rate (83%) with the shortest LT50 (1.73 days) 7 days post-treatment. T. asperellum M2RT4 effect on herbivore performance was then (Z)-jasmone-mediated. These findings expand our understanding of how the endophytic fungus T. asperellum M2RT4 could mediate chemical interactions between T. absoluta and its host plant which are potentially important for development of environmentally friendly T. absoluta management programs.https://www.frontiersin.org/journals/plant-sciencedm2022Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Virulence and horizontal transmission of Metarhizium anisopliae by the adults of the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) and the efficacy of oil formulations against its nymphs

The pathogenicity of dry conidia and fungal suspensions of 16 entomopathogenic fungal isolates (10 Metarhizium anisopliae and six Beauveria bassiana) was evaluated against adults and second instar nymphs of the greenhouse whitefly, Trialeurodes vaporariorum respectively. All the tested isolates were pathogenic to T. vaporariorum and caused mortality of 45–93% against the adults and 24–89% against the nymphs. However, M. anisopliae strains showed higher virulence to both developmental stages as compared to B. bassiana strains. The three most virulent isolates that caused high mortalities in adults were M. anisopliae ICIPE 18, ICIPE 62 and ICIPE 69, with cumulative mortalities of 82, 91 and 93%, and median lethal times (LT50) of 5.20, 5.05 and 4.78 days, respectively. These isolates were further assessed for spore acquisition and retention by the adult insects at 0, 24, 48 and 72 h after exposure to dry conidia spores. There was no significant difference among isolates on their acquisition by the insects, although the effect of time on the number of spores retained by each insect was significant. For M. anisopliae ICIPE 62 and ICIPE 69, spore number was significantly higher immediately after exposure at 0 h than at 24, 48 and 72 h, whereas for M. anisopliae ICIPE 18, the spore number remained constant for all the days. The infected “donor” insects were able to horizontally transmit the acquired spores to uninfected “recipient” insects causing high mortality rates in both donor and recipient groups. Metarhizium anisopliae ICIPE 7, ICIPE 18 and ICIPE 62 were the most virulent isolates against the nymphs in aqueous formulation during the first screening with >80% mortality. However, in 2% (v/v) oil formulations at 1 108 conidia/ml, canola formulated ICIPE 62, ICIPE 18 and olive formulated ICIPE 18 were the most effective, resulting in 87.8, 88.1 and 99.4% nymphal mortalities respectively and with lower LT50. Oil formulations significantly enhanced the efficacy and virulence of the isolates against the nymphs compared to aqueous formulations.The German Academic Exchange Service (DAAD) through African Regional Postgraduate Programme in Insect Science (ARPPIS) of icipe. The icipe core funding provided by UK’s Foreign, Commonwealth and Development Office (FCDO); 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.http://www.cell.com/heliyonam2022Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Temperature‑dependent modelling and spatial prediction reveal suitable geographical areas for deployment of two Metarhizium anisopliae isolates for Tuta absoluta management

Tuta absoluta is one of the most devastating pests of Solanaceae crops in Africa. We previously demonstrated the efficacy of Metarhizium anisopliae isolates ICIPE 18, ICIPE 20 and ICIPE 665 against adult T. absoluta. However, adequate strain selection and accurate spatial prediction are fundamental to optimize their efficacy and formulations before field deployment. This study therefore assessed the thermotolerance, conidial yield and virulence (between 15 and 35 °C) of these potent isolates. Over 90% of conidia germinated at 20, 25 and 30 °C while no germination occurred at 15 °C. Growth of the three isolates occurred at all temperatures, but was slower at 15, 33 and 35 °C as compared to 20, 25 and 30 °C. Optimum temperatures for mycelial growth and spore production were 30 and 25 °C, respectively. Furthermore, ICIPE 18 produced higher amount of spores than ICIPE 20 and ICIPE 665. The highest mortality occurred at 30 °C for all the three isolates, while the LT50 values of ICIPE 18 and ICIPE 20 were significantly lower at 25 and 30 °C compared to those of ICIPE 665. Subsequently, several nonlinear equations were fitted to the mortality data to model the virulence of ICIPE 18 and ICIPE 20 against adult T. absoluta using the Entomopathogenic Fungi Application (EPFA) software. Spatial prediction revealed suitable locations for ICIPE 18 and ICIPE 20 deployment against T. absoluta in Kenya, Tanzania and Uganda. Our findings suggest that ICIPE 18 and ICIPE 20 could be considered as effective candidate biopesticides for an improved T. absoluta management based on temperature and location-specific approach.The African Union (AU), UK’s Foreign, Commonwealth & Development Office (FCDO) through the International Centre of Insect Physiology and Ecology (icipe). The icipe core funding provided by UK’s Foreign, Commonwealth & Development Office (FCDO); 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.https://www.nature.com/srepam2022Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Efficacy of Metarhizium anisopliae and (E)–2–hexenal combination using autodissemination technology for the management of the adult greenhouse whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae

DATA AVAILABILITY STATEMENT : The original contributions presented in the study are included in the article. Further inquiries can be directed to the corresponding author.The efficiency of an autodissemination technique in controlling adult whiteflies, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae) on tomato, Solunum lycopersicum was investigated with previously identified potent fungal isolates of Metarhizium anisopliae ICIPE 18, ICIPE 62 and ICIPE 69 under screenhouse or semi-field conditions. The autodissemination device was inoculated with dry conidia of the M. anisopliae isolates, while control insects were exposed to a fungus–free device. Sampling for conidia uptake, conidial viability and persistence, and insect mortality was done at 1, 2, 3, 5 and 8 days post–exposure, and collected insects were monitored for mortality over ten days. Overall, mortality was higher in insects exposed to ICIPE 18 (62.8%) and ICIPE 69 (61.8%) than in those exposed to ICIPE 62 (42.6%), with median lethal times, (LT50) ranging between 6.73–8.54 days. The control group recorded the lowest mortality rates (18.9%). A general linear reduction in conidial viability with exposure time was observed, although this was more pronounced with M. anisopliae ICIPE 62. Insects exposed to M. anisopliae ICIPE 69 also recorded the highest conidia uptake, hence selected for further evaluation with a T. vaporariorum attractant volatile organic compound, (E)–2–hexenal. The volatile inhibited fungal germination in laboratory compatibility tests, therefore, spatial separation of M. anisopliae ICIPE 69 and (E)–2–hexenal in the autodissemination device was conducted. The inhibitory effects of the volatile were significantly reduced by spatial separation at a distance of 5 cm between the fungus and the volatile, which was found to be more suitable and chosen for the subsequent experiments. Results showed that (E)–2–hexenal did not influence conidia uptake by the insects, while fungal viability and the subsequent mortality variations were more related to duration of exposure. The fungus–volatile compatibility demonstrated with spatial separation provides a basis for the optimisation of the volatile formulation to achieve better T. vaporariorum suppression with an excellent autodissemination efficiency when used in the management of whiteflies under screenhouse conditions.BioInnovate Africa Phase I project “Promoting smallholder access to fungal biopesticides through Public Private Partnerships in East Africa” (BA/CI/ 2017-02/PROSAFE), and UK’s Foreign, Commonwealth and Development Office (FCDO) (FCDO Biopesticide Project, B2291A - FCDO - BIOPESTICIDE) through the International Centre of Insect Physiology and Ecology (icipe). The icipe core funding provided by UK’s Foreign, Commonwealth and Development Office (FCDO); 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.https://www.frontiersin.org/journals/insect-sciencehj2023Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Endophytic fungi protect tomato and nightshade plants against Tuta absoluta (Lepidoptera : Gelechiidae) through a hidden friendship and cryptic battle

Endophytic fungi live within plant tissues without causing any harm to the host, promote its growth, and induce systemic resistance against pests and diseases. To mitigate the challenging concealed feeding behavior of immature stages of Tuta absoluta in both tomato (Solanum lycopersicum) and nightshade (Solanum scabrum) host plants, 15 fungal isolates were assessed for their endophytic and insecticidal properties. Twelve isolates were endophytic to both host plants with varied colonization rates. Host plants endophytically-colonized by Trichoderma asperellum M2RT4, Beauveria bassiana ICIPE 706 and Hypocrea lixii F3ST1 outperformed all the other isolates in reducing significantly the number of eggs laid, mines developed, pupae formed and adults emerged. Furthermore, the survival of exposed adults and F1 progeny was significantly reduced by Trichoderma sp. F2L41 and B. bassiana isolates ICIPE 35(4) and ICIPE 35(15) compared to other isolates. The results indicate that T. asperellum M2RT4, B. bassiana ICIPE 706 and H. lixii F3ST1 have high potential to be developed as endophyticfungal- based biopesticide for the management of T. absoluta.The icipe core funding provided by UK’s Foreign, Commonwealth and Development Office (FCDO); 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.http://www.nature.com/srepam2021Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Insights in the global genetics and gut microbiome of black soldier fly, hermetia illucens : implications for animal feed safety control

This study delineates genetic variability and unravels gut microbiome complex of wild-collected and domesticated BSF populations from six continents using mitochondrial COI gene and 16S metagenomics. Alpha-diversity showed that the Kenyan and Thailand populations had the highest and lowest microbe diversity, respectively; while microbial diversity assessed through Bray Curtis distance showed United States (Maysville) and Netherlands populations to be the most dissimilar. The 16S data depicted larval gut bacterial families with economically important genera that might pose health risks to both animals and humans. To minimize risk of pathogen contamination along the insect-based feed value chain, this study recommends pre-treatment of feedstocks.Netherlands Organization for Scientific ResearchWOTRO Science for Global Development (NWO-WOTRO)Australian Centre for International Agricultural Research (ACIAR)Rockefeller Foundatio

Endophytic colonisation of Solanum lycopersicum and Phaseolus vulgaris by fungal endophytes promotes seedlings growth and hampers the reproductive traits, development, and survival of the greenhouse whitefly, Trialeurodes vaporariorum

In the scope of mitigating the negative impacts of pesticide use and managing greenhouse whiteflies, Trialeurodes vaporariorum sustainably, 16 endophytic fungal isolates from five different genera (Beauveria, Trichoderma, Hypocrea, Bionectria, and Fusarium) were screened for their ability to colonise two preferred host plant species, namely, tomato (Solanum lycopersicum L.) and French bean (Phaseolus vulgaris L.), through seed inoculation. Seven and nine isolates were endophytic to P. vulgaris and S. lycopersicum, respectively, where significant differences in the endophytic colonisation rates were observed among the fungal isolates in P. vulgaris and its plant parts, with a significant interaction between the isolates and plant parts in S. lycopersicum. Hypocrea lixii F3ST1, Trichoderma asperellum M2RT4, Trichoderma atroviride F5S21, and T. harzianum KF2R41 successfully colonised all the plant parts of both hosts and therefore were selected and further evaluated for their endophytic persistence, effect on plant growth, and pathogenicity to T. vaporariorum adults and F1 progeny. The four endophytes remained in both host plants for the 5-week assessment with varied colonisation rates related to the strong interaction with the time, isolates, and plant parts in both hosts. The effect of the same endophytes on the different host growth parameters varied in P. vulgaris and S. lycopersicum, with T. asperellum M2RT4 not boosting the growth in both host plants while T. atroviride F5S21 resulted in enhanced shoot biomass in S. lycopersicum. T. atroviride F5S21 and T. harzianum KF2R41 inoculated S. lycopersicum plants and H. lixii F3ST1, T. asperellum M2RT4, and T. harzianum KF2R41 inoculated P. vulgaris plants had significantly lower oviposition, while nymph development in both hosts was significantly prolonged in all the endophytically– colonised plants. The endophytes H. lixii F3ST1 and T. asperellum M2RT4 significantly reduced the longevity/survival of the exposed T. vaporariorum adults and the progeny in both S. lycopersicum and P. vulgaris. The findings demonstrate the attributes of the various endophytes in host plant growth promotion as well as their effects on the lifehistory parameters of T. vaporariorum and could consequently be developed as potential endophytic fungal-based biopesticides for the sustainable management of the pest in S. lycopersicum and P. vulgaris cropping systems.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), and the Foreign, Commonwealth, and Development Office of United Kingdom (FCDO) (FCDO Biopesticide Project, B2291A- FCDO -BIOPESTICIDE) through the International Centre of Insect Physiology and Ecology (icipe). We thank the German Academic Exchange Service (DAAD) In-Region Post-graduate Scholarship for the financial assistance provided to VP through African Regional Postgraduate Programme in Insect Science (ARPPIS). We gratefully acknowledge the icipe core funding provided by the Foreign, Commonwealth, and Development Office of United Kingdom (FCDO); 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.http://www.frontiersin.org/Plant_Scienceam2022Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

Whole genome comparisons reveal panmixia among fall armyworm (Spodoptera frugiperda) from diverse locations

Background: The fall armyworm (Spodoptera frugiperda (J.E. Smith)) is a highly polyphagous agricultural pest with long-distance migratory behavior threatening food security worldwide. This pest has a host range of > 80 plant species, but two host strains are recognized based on their association with corn (C-strain) or rice and smaller grasses (R-strain). The population genomics of the United States (USA) fall armyworm remains poorly characterized to date despite its agricultural threat. Results: In this study, the population structure and genetic diversity in 55 S. frugiperda samples from Argentina, Brazil, Kenya, Puerto Rico and USA were surveyed to further our understanding of whole genome nuclear diversity. Comparisons at the genomic level suggest a panmictic S. frugiperda population, with only a minor reduction in gene flow between the two overwintering populations in the continental USA, also corresponding to distinct host strains at the mitochondrial level. Two maternal lines were detected from analysis of mitochondrial genomes. We found members from the Eastern Hemisphere interspersed within both continental USA overwintering subpopulations, suggesting multiple individuals were likely introduced to Africa. Conclusions: Our research is the largest diverse collection of United States S. frugiperda whole genome sequences characterized to date, covering eight continental states and a USA territory (Puerto Rico). The genomic resources presented provide foundational information to understand gene flow at the whole genome level among S. frugiperda populations. Based on the genomic similarities found between host strains and laboratory vs. field samples, our findings validate the experimental use of laboratory strains and the host strain differentiation based on mitochondria and sex-linked genetic markers extends to minor genome wide differences with some exceptions showing mixture between host strains is likely occurring in field populations.Fil: Schlum, Katrina A.. University of Tennessee; Estados UnidosFil: Lamour, Kurt. University of Tennessee; Estados UnidosFil: Placidi de Bortoli, Caroline. University of Tennessee; Estados UnidosFil: Banerjee, Rahul. University of Tennessee; Estados UnidosFil: Meagher, Robert. United States Department Of Agriculture. Center For Medical Agric And Vet Entomology; Estados UnidosFil: Pereira, Eliseu. Universidade Federal de Viçosa; BrasilFil: Murúa, María Gabriela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Tecnología Agroindustrial del Noroeste Argentino. Provincia de Tucumán. Ministerio de Desarrollo Productivo. Estación Experimental Agroindustrial "Obispo Colombres" (p). Instituto de Tecnología Agroindustrial del Noroeste Argentino; ArgentinaFil: Sword, Gregory A.. Texas A&M University; Estados UnidosFil: Tessnow, Ashley E.. Texas A&M University; Estados UnidosFil: Viteri Dillon, Diego. Universidad de Puerto Rico; Puerto RicoFil: Linares Ramirez, Angela M.. Universidad de Puerto Rico; Puerto RicoFil: Akutse, Komivi S.. International Centre Of Insect Physiology And Ecology; KeniaFil: Schmidt Jeffris, Rebecca. United States Department Of Agriculture. Center For Medical Agric And Vet Entomology; Estados UnidosFil: Huang, Fangneng. State University of Louisiana; Estados UnidosFil: Reisig, Dominic. North Carolina State University; Estados UnidosFil: Emrich, Scott J.. University of Tennessee; Estados UnidosFil: Jurat Fuentes, Juan Luis. University of Tennessee; Estados Unido