Global genomic signature reveals the evolution of fall armyworm in the Eastern hemisphere.

The major plant pest fall armyworm (FAW), Spodoptera frugiperda, is native to the Americas and has colonized Africa and Asia within the Eastern hemisphere since 2016, causing severe damage to multiple agricultural crop species. However, the genetic origin of these invasive populations requires more in-depth exploration. We analysed genetic variation across the genomes of 280 FAW individuals from both the Eastern hemisphere and the Americas. The global range-wide genetic structure of FAW shows that the FAW in America has experienced deep differentiation, largely consistent with the Z-chromosomal Tpi haplotypes commonly used to differentiate 'corn-strain' and 'rice-strain' populations. The invasive populations from Africa and Asia are different from the American ones and have a relatively homogeneous population structure, consistent with the common origin and recent spreading from Africa to Asia. Our analyses suggest that north- and central American 'corn-strain' FAW are the most likely sources of the invasion into the Eastern hemisphere. Furthermore, evidence based on genomic, transcriptomic and mitochondrial haplotype network analyses indicates an earlier, independent introduction of FAW into Africa, with subsequent migration into the recent invasive population.

Understanding the impact of fall armyworm (Spodoptera frugiperda J. E. Smith) leaf damage on maize yields.

Fall armyworm (Spodoptera frugiperda J. E. Smith), a serious pest of maize and other cereals, recently invaded the Old World potentially threatening the food security and incomes of millions of smallholder farmers. Being able to assess the impacts of a pest on yields is fundamental to developing Integrated Pest Management (IPM) approaches. Hence, working with an early maturing, medium maturing and late maturing variety, we inoculated maize plants with 2nd instar S. frugiperda larvae at V5, V8, V12, VT and R1 growth stages to investigate the effects of FAW induced damage on yield. Different plants were inoculated 0-3 times and larvae were removed after 1 or 2 weeks to generate a wide range of damage profiles. We scored plants for leaf damage at 3, 5 and 7 weeks after emergence (WAE) using the 9 point Davis scale. While at harvest we assessed ear damage (1-9 scale), and recorded plant height and grain yield per plant. We used Structural Equation Models to assess the direct effects of leaf damage on yield and indirect effects via plant height. For the early and medium maturing varieties leaf damage at 3 and 5 WAE, respectively, had significant negative linear effects on grain yield. In the late maturing variety, leaf damage at 7 WAE had an indirect effect on yield through a significant negative linear effect on plant height. However, despite the controlled screenhouse conditions, in all three varieties leaf damage explained less than 3% of the variation in yield at the plant level. Overall, these results indicate that S. frugiperda induced leaf damage has a slight but detectable impact on yield at a specific plant developmental stage, and our models will contribute to the development of decision-support tools for IPM. However, given the low average yields obtained by smallholders in sub-Saharan Africa and the relatively low levels of FAW induced leaf damage recorded in most areas, IPM strategies should focus on interventions aimed at improving plant vigour (e.g. through integrated soil fertility management) and the role of natural enemies, as these are likely to result in greater yield gains at lower cost than a focus on FAW control.

Abundance, diversity and richness of natural enemies of the fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), in Zambia.

The fall armyworm (FAW), Spodoptera frugiperda, an invasive pest originating from the Americas is a serious pest threatening cereal production and food security in Zambia. We studied the prevalence and abundance of natural enemies of FAW in three Agroecological regions (AERs I, II, and III) to identify those that could potentially serve as bio-control agents. Sampling of FAW parasitoids and predators was done along trunk roads at intervals of 10 km. Molecular sequence analysis and morphological characterization were used to identify natural enemies. Over 11 species of FAW natural enemies, including egg, egg-larval, and larval parasitoids, and predators, were identified in Zambia. The mean number of natural enemies and species richness was higher in AER I and IIa. Consequently, egg parasitism was highest in those two regions, at 24.5% and 12.2%, respectively. Larvae parasitism was highest in AER I (4.8%) and AER III (1.9), although no significant differences were observed. The most abundant and widely distributed parasitoid was Drino sp. (Diptera: Tachinidae), while Rhynocoris segmentarius (Germar) (Hemiptera: Reduviidae) and Belanogaster sp. (Hymenoptera: Vespidae) were the most prevalent predators. Our study reveals the presence of two natural enemies belonging to the genus Tiphia and Micromeriella, uncommon to FAW. Significant differences in the number of parasitoids were observed in polycropping, with the highest recovery of 12 ± 10% from maize + cowpeas + pumpkin and watermelon mixed cropping. The higher the rainfall, the lower the number of natural enemies recorded. Variations in rainfall patterns which affect FAW availability, cropping systems and the three AERs may explain natural enemies' species diversity in Zambia. The information provided in this study can aid the development of a national biological control programme for sustainable management of fall armyworm.

Biological control interventions reduce pest abundance and crop damage while maintaining natural enemies in sub-Saharan Africa: a meta-analysis.

Insect pests are a major challenge to smallholder crop production in sub-Saharan Africa (SSA), where access to synthetic pesticides, which are linked to environmental and health risks, is often limited. Biological control interventions could offer a sustainable solution, yet an understanding of their effectiveness is lacking. We used a meta-analysis approach to investigate the effectiveness of commonly used biocontrol interventions and botanical pesticides on pest abundance (PA), crop damage (CD), crop yield (Y) and natural enemy abundance (NEA) when compared with controls with no biocontrol and with synthetic pesticides. We also evaluated whether the magnitude of biocontrol effectiveness was affected by type of biocontrol intervention, crop type, pest taxon, farm type and landscape configuration. Overall, from 99 studies on 31 crops, we found that compared to no biocontrol, biocontrol interventions reduced PA by 63%, CD by over 50% and increased Y by over 60%. Compared to synthetic pesticides, biocontrol resulted in comparable PA and Y, while NEA was 43% greater. Our results also highlighted that the potential for biocontrol to be modulated by landscape configuration is a critical knowledge gap in SSA. We show that biocontrol represents an effective tool for smallholder farmers, which can maintain yields without associated negative pesticide effects. Furthermore, the evidence presented here advocates strongly for including biocontrol practices in national and regional agricultural policies.

Low Impact of Fall Armyworm (Spodoptera frugiperda Smith) (Lepidoptera: Noctuidae) Across Smallholder Fields in Malawi and Zambia.

Fall armyworm (Spodoptera frugiperda Smith), a serious pest of cereals from the Americas, has spread across sub-Saharan Africa and Asia since 2016, threatening the food security and incomes of millions of smallholder farmers. To measure the impact of S. frugiperda under different management approaches, we established on-farm trials across 12 landscapes (615-1,379 mm mean annual rainfall) in Malawi and Zambia during the 2019/2020 and 2020/2021 seasons. Here we present the results from our conventional tillage, monocrop maize, no pesticide treatment, which served to monitor the background S. frugiperda impact in the absence of control measures. Median plot-level S. frugiperda incidence ranged between 0.00 and 0.52 across landscapes. Considering severe leaf damage (Davis score ≥5), the proportion of affected plants varied between 0.00 and 0.30 at the plot scale, but only 3% of plots had ≥10% severely damaged plants. While incidence and damage severity varied substantially among sites and seasons, our models indicate that they were lower in high tree cover landscapes, in the late season scouting, and in the 2020/2021 season. Yield could not be predicted from S. frugiperda incidence or leaf damage. Our results suggest S. frugiperda impacts may have been overestimated at many sites across sub-Saharan Africa. S. frugiperda incidence and damage declined through the cropping season, indicating that natural mortality factors were limiting populations, and none of our plots were heavily impacted. Long-term S. frugiperda management should be based on Integrated Pest Management (IPM) principles, including minimising the use of chemical pesticides to protect natural enemies.

The distribution of covert microbial natural enemies of a globally invasive crop pest, fall armyworm, in Africa: Enemy release and spillover events.

Invasive species pose a significant threat to biodiversity and agriculture world-wide. Natural enemies play an important part in controlling pest populations, yet we understand very little about the presence and prevalence of natural enemies during the early invasion stages. Microbial natural enemies of fall armyworm Spodoptera frugiperda are known in its native region, however, they have not yet been identified in Africa where fall armyworm has been an invasive crop pest since 2016. Larval samples were screened from Malawi, Rwanda, Kenya, Zambia, Sudan and Ghana for the presence of four different microbial natural enemies; two nucleopolyhedroviruses, Spodoptera frugiperda NPV (SfMNPV) and Spodoptera exempta NPV (SpexNPV); the fungal pathogen Metarhizium rileyi; and the bacterium Wolbachia. This study aimed to identify which microbial pathogens are present in invasive fall armyworm, and determine the geographical, meteorological and temporal variables that influence prevalence. Within 3 years of arrival, fall armyworm was exposed to all four microbial natural enemies. SfMNPV probably arrived with fall armyworm from the Americas, but this is the first putative evidence of host spillover from Spodoptera exempta (African armyworm) to fall armyworm for the endemic pathogen SpexNPV and for Wolbachia. It is also the first confirmed incidence of M. rileyi infecting fall armyworm in Africa. Natural enemies were localised, with variation being observed both nationally and temporally. The prevalence of SfMNPV (the most common natural enemy) was predominantly explained by variables associated with the weather; declining with increasing rainfall and increasing with temperature. However, virus prevalence also increased as the growing season progressed. The infection of an invasive species with a natural enemy from its native range and novel pathogens specific to its new range has important consequences for understanding the population ecology of invasive species and insect-pathogen interactions. Additionally, while it is widely known that temporal and geographic factors affect insect populations, this study reveals that these are important in understanding the distribution of microbial natural enemies associated with invasive pests during the early stages of invasion, and provide baseline data for future studies.

Comparing, evaluating and combining statistical species distribution models and CLIMEX to forecast the distributions of emerging crop pests.

BACKGROUND: Forecasting the spread of emerging pests is widely requested by pest management agencies in order to prioritise and target efforts. Two widely used approaches are statistical Species Distribution Models (SDMs) and CLIMEX, which uses ecophysiological parameters. Each have strengths and weaknesses. SDMs can incorporate almost any environmental condition and their accuracy can be formally evaluated to inform managers. However, accuracy is affected by data availability and can be limited for emerging pests, and SDMs usually predict year-round distributions, not seasonal outbreaks. CLIMEX can formally incorporate expert ecophysiological knowledge and predicts seasonal outbreaks. However, the methods for formal evaluation are limited and rarely applied. We argue that both approaches can be informative and complementary, but we need tools to integrate and evaluate their accuracy. Here we develop such an approach, and test it by forecasting the potential global range of the tomato pest Tuta absoluta. RESULTS: The accuracy of previously developed CLIMEX and new statistical SDMs were comparable on average, but the best statistical SDM techniques and environmental data substantially outperformed CLIMEX. The ensembled approach changes expectations of T. absoluta's spread. The pest's environmental tolerances and potential range in Africa, the Arabian Peninsula, Central Asia and Australia will be larger than previous estimates. CONCLUSION: We recommend that CLIMEX be considered one of a suite of SDM techniques and thus evaluated formally. CLIMEX and statistical SDMs should be compared and ensembled if possible. We provide code that can be used to do so when employing the biomod suite of SDM techniques. © 2021 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Microsatellites reveal that genetic mixing commonly occurs between invasive fall armyworm populations in Africa.

Understanding the population structure and movements of the invasive fall armyworm (FAW, Spodoptera frugiperda) is important as it can help mitigate crop damage, and highlight areas at risk of outbreaks or evolving insecticide resistance. Determining population structure in invasive FAW has been a challenge due to genetic mutations affecting the markers traditionally used for strain and haplotype identification; mitochondrial cytochrome oxidase I (COIB) and the Z-chromosome-linked Triosephosphate isomerase (Tpi). Here, we compare the results from COIB and Tpi markers with highly variable repeat regions (microsatellites) to improve our understanding of FAW population structure in Africa. There was very limited genetic diversity using the COIB marker, whereas using the TpiI4 marker there was greater diversity that showed very little evidence of genetic structuring between FAW populations across Africa. There was greater genetic diversity identified using microsatellites, and this revealed a largely panmictic population of FAW alongside some evidence of genetic structuring between countries. It is hypothesised here that FAW are using long-distance flight and prevailing winds to frequently move throughout Africa leading to population mixing. These approaches combined provide important evidence that genetic mixing between invasive FAW populations may be more common than previously reported.

Genetic structure and insecticide resistance characteristics of fall armyworm populations invading China.

The rapid wide-scale spread of fall armyworm (Spodoptera frugiperda) has caused serious crop losses globally. However, differences in the genetic background of subpopulations and the mechanisms of rapid adaptation behind the invasion are still not well understood. Here we report the assembly of a 390.38-Mb chromosome-level genome of fall armyworm derived from south-central Africa using Pacific Bioscience (PacBio) and Hi-C sequencing technologies, with scaffold N50 of 12.9 Mb and containing 22,260 annotated protein-coding genes. Genome-wide resequencing of 103 samples and strain identification were conducted to reveal the genetic background of fall armyworm populations in China. Analysis of genes related to pesticide- and Bacillus thuringiensis (Bt) resistance showed that the risk of fall armyworm developing resistance to conventional pesticides is very high. Laboratory bioassay results showed that insects invading China carry resistance to organophosphate and pyrethroid pesticides, but are sensitive to genetically modified maize expressing the Bt toxin Cry1Ab in field experiments. Additionally, two mitochondrial fragments were found to be inserted into the nuclear genome, with the insertion event occurring after the differentiation of the two strains. This study represents a valuable advance toward improving management strategies for fall armyworm.

Farmer perception of fall armyworm (Spodoptera frugiderda J.E. Smith) and farm-level management practices in Zambia.

BACKGROUND: This paper documents farmer perceptions and management practices for fall armyworm (Spodoptera frugiderda J.E. Smith), providing a baseline for the development of sustainable pest management strategies. RESULTS: 91% of farmers correctly identified fall armyworm, and reported it as the most important maize pest during 2016/2017 cropping season, affecting nearly half of cultivated area. Estimated maize yield loss during the season, attributed to fall armyworm was 28%. A majority of farmers (60%) used pesticides for fall armyworm control, along with other cultural/physical practices - hand picking and crushing egg masses/caterpillars (36%), and application of ash/sand in the funnel (19%). Farmers used various pesticide active ingredients, and protective measures were inadequate; >50% of farmers did not use any protective measures while spraying. Significantly more male than female farmers used pesticides (P = 0.05), and the reverse was true for cultural practices. Significant maize yield differences (P = 0.001) were observed by gender, attributed to differences in utilization of production inputs/practices. At least 77% of farmers received and shared agricultural advice, which can be optimized to spread information on fall armyworm management options. CONCLUSION: Increased use of pesticides to manage fall armyworm poses health and environmental risks, besides the high cost for farmers and governments. Research into cultural and indigenous practices used by farmers will offer opportunities for alternative and sustainable management practices. Research efforts should pay attention to gender differences in access to resources and inputs. Tackling fall armyworm at the farm level, and averting yield losses will require integrated messaging addressing other production risks. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.