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 ß-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, ß-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.

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.

Infection of the Stable Fly, Stomoxys calcitrans, L. 1758 (Diptera: Muscidae) by the Entomopathogenic Fungi Metarhizium anisopliae (Hypocreales: Clavicipitaceae) Negatively Affects Its Survival, Feeding Propensity, Fecundity, Fertility, and Fitness Parameters.

Entomopathogenic fungi can cause substantial mortality in harmful insects. Before killing the insect, these pathogens start by negatively affecting the biological parameters of the host. Prior to our study, the information about how fungal exposure affects the biological parameters of the stable fly, Stomoxys calcitrans was still elusive. Therefore, we aimed to assess the infection of S. calcitrans with some Metarhizium anisopliae strains, and their impact on feeding, fecundity, fertility and other life-history traits of this fly. Among the 11 M. anisopliae strains screened, we identified ICIPE 30 as the most virulent strain against S. calcitrans. We observed that the infectivity of this strain was sex and age-dependent. Infected male S. calcitrans died earlier than their counterpart females. Older infected S. calcitrans died faster than infected young ones. Also, male and female S. calcitrans successfully transmitted ICIPE 30 conidia to their mates. We demonstrated that infection by ICIPE 30 extended the feeding time of S. calcitrans and consequently reduced the feeding probability of the fly and the amount of blood taken. Using a dual test oviposition bioassay, we determined that uninfected gravid female S. calcitrans avoided laying eggs on substrates amended with ICIPE 30 conidia. We showed that these conidia could lower the hatchability of the eggs deposited by gravid females. Using, a no-choice test, we showed that gravid female S. calcitrans infected with ICIPE 30 laid fewer eggs than uninfected females and those eggs hatched less. Using 11 strains of M. anisopliae and four high concentrations of ICIPE 30 conidia, we verified that S. calcitrans larvae were not susceptible to fungal infection. Further, we showed that though these larvae were tolerant to fungal infection, there was a significant effect on their fitness, with contaminated larvae having a small bodyweight coupled with longer developmental time as compared to uncontaminated larvae. Our study provides detailed information on how fungal infection affects the biology of S. calcitrans and the potential of using M. anisopliae ICIPE 30 as a biopesticide to reduce the fly population. Such knowledge can assist in developing fungal-based control strategies against this harmful fly.

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 endophytic-fungal-based biopesticide for the management of T. absoluta.

Influence of Rearing Substrates and Nontarget Hosts on the Bionomics of the Tachinid Parasitoid Nemorilla maculosa (Diptera: Tachinidae).

The tachinid Nemorilla maculosa Meigen (Diptera: Tachinidae) was introduced from Taiwan to Benin for evaluating its potential as a biocontrol candidate against the cowpea pest Maruca vitrata (Fabricius) (Lepidoptera: Crambidae). To optimize its rearing, we assessed the influence of M. vitrata larval age and rearing substrate-cowpea germinating grains and peabush leaves-on its life table parameters, while its host specificity was investigated with regard to nontarget effects. Parasitism rates were higher when older larvae (10- and 14-d old) were offered to females of N. maculosa compared to the younger (2-, 4-, and 6-d old) host larvae. Regardless of the rearing substrate, development time was longer for females than males, and females lived longer than males irrespective of the age of the host. Sex ratio did not vary significantly with host ages or rearing substrate. The average number of eggs laid by a female reared from M. vitrata larvae feeding on cowpea germinating grains or peabush leaves was 94.2 ± 4.38 and 71.9 ± 1.70 eggs, respectively. The host suitability of N. maculosa was assessed by testing four nontarget Lepidoptera species: Spodoptera littoralis Boisduval (Lepidoptera: Noctuidae), Sesamia calamistis Hampson (Lepidoptera: Noctuidae), Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae), and Eldana saccharina Walker (Lepidoptera: Pyralidae). Larvae of S. littoralis and C. cephalonica were successfully parasitized while N. maculosa did not develop in the larvae of E. saccharina and S. calamistis although they were parasitized. Despite the potential of N. maculosa as a biological control agent against the pod borer M. vitrata, more detailed nontarget studies, extending to other native Crambidae species, are needed before making decisions on field releases.