Updated assessment of potential biopesticide options for managing fall armyworm (Spodoptera frugiperda) in Africa

The fall armyworm (FAW, Spodoptera frugiperda) has recently spread to many countries in Africa, the Near East, Asia and the Pacific. In sub‐Saharan Africa (SSA), more than 300 million people depend on FAW’s preferred host plant, maize, as a staple crop. Hence, the spread of FAW in SSA has the potential to negatively affect livelihoods and food security. Many farmers have responded to FAW by increasing their use of synthetic pesticides, but these are not always used safely or effectively. More information on sustainable alternatives to high‐risk synthetic pesticides is needed to inform decisions by farmers and policy makers. In a previous paper, the authors responded to this information need by identifying fifty biopesticides which had been registered for FAW management in one or more of 30 countries in FAWs native region and Africa. For each biopesticide identified, detailed profiles with information on their efficacy against FAW; associated human health and environmental hazards; their agronomic sustainability; and whether or not they are practical for use by smallholder farmers were developed Research for development (R4D) efforts is ongoing in Africa and Asia for development and use of biopesticides for FAW management. Hence, in this study the authors assessed the current state of knowledge and documented how information gaps have been filled (or not) since the previous paper was published. The authors found that for many biopesticides there is a growing body of information on their efficacy in the field in Africa and increased availability of commercialized products. They also note remaining information gaps, particularly the compatibility of the biopesticides with other recommended management practices, and cost‐benefit analyses, important for developing and implementing sustainable IPM. An updated list of priority biopesticides for research, development and promotion is provided.

use of synthetic pesticides, but these are not always used safely or effectively. More information on sustainable alternatives to high-risk synthetic pesticides is needed to inform decisions by farmers and policy makers. In a previous paper, the authors responded to this information need by identifying fifty biopesticides which had been registered for FAW management in one or more of 30 countries in FAWs native region and Africa. For each biopesticide identified, detailed profiles with information on their efficacy against FAW; associated human health and environmental hazards; their agronomic sustainability; and whether or not they are practical for use by smallholder farmers were developed. Research for development (R4D) efforts is ongoing in Africa and Asia for development and use of biopesticides for FAW management.
Hence, in this study the authors assessed the current state of knowledge and documented how information gaps have been filled (or not) since the previous paper was published. The authors found that for many biopesticides there is a growing body of information on their efficacy in the field in Africa and increased availability of commercialized products. They also note remaining information gaps, particularly the compatibility of the biopesticides with other recommended management practices, and cost-benefit analyses, important for developing and implementing sustainable IPM. An updated list of priority biopesticides for research, development and promotion is provided.

| INTRODUC TI ON
Fall armyworm (FAW, Spodoptera frugiperda (J.E. Smith), Lepidoptera: Noctuidae) is a highly mobile, polyphagous species that has recently spread from the Nearctic and Neotropical regions to much of Africa, the Near East, Asia and the Pacific (FAO (Food and Agriculture Organization of the United Nations), 2020a; Goergen et al., 2016;;Sharanabasappa et al., 2018;Zhang et al., 2020). FAW is particularly a pest of cereals and one of the major pests of maize FAO, 2020b;Hruska, 2019;Kansiime et al., 2019;Kassie et al., 2020;Rwomushana et al., 2018;Tambo et al., 2020). As maize is a staple food crop for more than 300 million people in sub-Saharan Africa (SSA), FAW is a threat to livelihoods and food security.
Many farmers have responded to FAW by increasing their use of high-risk synthetic pesticides (Kansiime et al., 2019;Kassie et al., 2020;Kumela et al., 2019;Tambo et al., 2020), but these are not always used safely or effectively, (Rwomushana et al., 2018), and there is evidence that unsafe pesticide use is putting farmers' health at risk (Tambo et al., 2020). Given the concerns posed by high-risk synthetic pesticides, there is a pressing need for alternative management options that are appropriate for use by smallholder farmers. The identification of practices and products for FAW management that are effective, lower risk, sustainable, accessible and affordable such as biopesticides (refer to Table 1 for the definition used in this paper) is high on the list of near-term activities identified in action plans in Africa at national, regional and international levels.
In order to make information on biopesticides for FAW management readily available, in a previous review paper , the authors assessed 54 commercially available biopesticide active ingredients (AIs) which had been registered for use against FAW, Spodoptera spp. or Lepidoptera in general 1 in one or more of 30 countries in FAW's native range or Africa. They collated information on their efficacy, human and environmental safety profile, agronomic sustainability, practicality for use, availability and cost-effectiveness.
Based on the profiles of the AIs, they assessed whether their use would pose a significant risk to the farmers who would apply them as well as to the wider community and environment, and whether the AI is practical for smallholder farmers. Using these data, a decision matrix (Table S1) was developed to provide a basis to design interventions that would make suitable biopesticides more widely available for FAW control in Africa. While there was evidence of efficacy from the field in FAW's native range for several of the AIs, data from the field in Africa were minimal. Likewise, at the time, few biopesticide AIs had been registered for most countries in Africa, and almost none of the AIs had been specifically registered for use against FAW. Also, there was virtually no information available for their cost-effectiveness. The authors concluded the previous assessment by recommending 23 biopesticide AIs for follow-up actions (such as field trials, participatory trials or laboratory studies) .
This review paper follows up on that by Bateman et al. (2018) by providing updated information on the biopesticide AIs that have been registered and commercialized for the management of FAW in one or more of 30 countries in FAW's native range or in Africa. We compared our findings to those of the previous assessment to gain information on how the state of knowledge has changed.

| MATERIAL S AND ME THODS
For each of the 30 selected countries, the most up-to-date versions of registered pesticides and biopesticides were used to identify the full list of biopesticide AIs and their corresponding products that can be used to manage FAW (Table S2). The lists of registered pesticides and biopesticides were accessed between April and August of 2020 and were filtered for any biopesticides which are already registered 1 Products which are registered for other specific Lepidoptera genera or species that are not Spodoptera were not considered.

Main substance groups
Sub-groups

TA B L E 1
For the purposes of this study, the national regulations were followed for those countries that identify which AI are biopesticides (or the equivalent) and, for countries where biopesticides are not identified, we used the same definition as the previous paper  and allowed for use against FAW, Spodoptera or Lepidoptera in general. As noted in Table 1, the registered pesticides list for 12 countries specifically identify biopesticide AIs, and the lists of registered pesticides for 19 countries include information about the specific pests for which the products are registered. Assessment of the lists of registered pesticides for countries in the Near East, Asia and the Pacific was beyond the scope of this study.
The profiles of previously identified AIs were updated based on any new information that has been published since the initial profiles were developed, and additional profiles were developed for newly identified AIs following the same approach as the previous assessment .

| Overview of identified biopesticide AIs
Analysis of the national lists of registered pesticides and biopesticides for the 30 countries identified 41 biopesticide AIs in total that are registered and allowed for use for FAW management in at least one country (listed in Table S3). Among them, there are four biopesticide AIs which were not identified in the previous assessment: Aspergillus oryzae, Autographa californica multiple nucleopolyhedrovirus (AcMNPV), Spodoptera littoralis nucleopolyhedrovirus (SpliNPV) and thyme oil.

F I G U R E 1
Numbers of active ingredients (AIs, left) and corresponding products (right) registered in three or more countries in 2018 (pale) and 2020 (dark) Three inorganic compounds (borax, cryolite and silicon dioxide), two microbial fermentation products (emamectin benzoate and spinetoram) and two insect growth regulators (lufenuron and methoxyfenozide) previously designated as biochemical biopesticides by at least one government are no longer categorized as such by any of the assessed countries, and, as a consequence, they were not assessed under the current study. Two other inorganic compounds (kaolin and sulphur), one other microbial fermentation product (spinosad) and one other insect growth regulator (s-methoprene) continue to be designated as biochemical biopesticides by one or more countries, though these AIs would not be considered as biopesticides by many definitions. No products were found to be registered for use against FAW or its relatives for three AIs that were identified through the Biopesticide AIs which were registered and allowed for use for FAW management in three or more countries are shown in Detailed profiles of the biopesticides are provided in the supplementary data, and each category of information below is summarized in Table S5.

| Efficacy
The

| Hazard profiles of identified biopesticide AIs
Detailed information on the hazards associated with each AI is given in Table S3. Twenty-six of the hazard profiles were unchanged from the previous assessment; data gaps were filled for five AIs; three were assigned higher toxicity categories and three to lower categories. All 41 AIs have relatively low levels of hazard.  Data on agronomic sustainability of matrine and oxymatrine were not available.

| Practicality in use for farmers
Literature and product labels indicated that 27 of the biopesticide AIs would be practical for smallholder farmers to use whereas six could be difficult for smallholder farmers to use, at least not immediately (allyl isothiocyanate, soybean oil, Steinernema carpocapsae, Steinernema feltiae and Trichogramma spp.). This assessment is virtually unchanged from the previous study's findings. These AIs were deemed impractical for smallholders for a variety of reasons, for example application equipment requirements, high frequency of application, storage requirements, shelf life and the need for application of an area-wide management approach.
Biopesticide AIs and products registered for use against FAW in its native range in the Americas.
Information on the registration of AIs by country is given in Table   SH. For each country in FAW's native range, the number of biopesticide AIs and products registered in 2020 has either increased or remained the same as compared to 2018 (Figure 3). In FAW's native range, the country with the highest number of biopesticide AIs registered for use against it was the United States (40 AIs).

| Registration status and availability of identified biopesticide active ingredients in Africa
The

| Affordability
For most of the biopesticide AI, there were no specific figures available on their cost and there was very little information on cost-effectiveness. Based on data on costs in Africa from field trials and farmer surveys, there are indications that azadirachtin is cost-effective, and relatively affordable (Babendreier et al., 2020), whereas ethyl palmitate (Rwomushana et al., 2018) and maltodextrin (Babendreier et al., 2020) are less cost-effective, and not as affordable to smallholder farmers. In assessments of cost-effectiveness for other pests or in other continents, there was evidence that the following AI were cost-effective: capsaicin, Chromobacterium subtsugae, garlic extracts, Isaria fumosorosea, Metarhizium anisopliae, spinosad and Trichogramma spp. (Dougoud et al., 2019;Kivett et al., 2015;Manisha et al., 2020;Nayak et al., 2019).

| D ISCUSS I ON
Given that many smallholder farmers are frequently using highly hazardous pesticides (Hopes) without personal protective equipment (Rwomushana et al., 2018) (Hruska, 2019). Without support from such programmes, the costs of some AIs may be prohibitively high, as demonstrated by the case of maltodextrin (Babendreier et al., 2020). For many of these AIs, further field work would be beneficial to establish the most cost-effective methods of use.
The conclusions developed using the decision matrix are listed in With increased travel and movement of goods, new invasive species are likely to be more and more common and the FAW invasion provides an interesting case study in terms of the global response, in much the same way as COVID-19 has provided a case study in how to respond to future pandemics.

ACK N OWLED G EM ENTS
CABI is an international intergovernmental organization, and we gratefully acknowledge the core financial support from our

CO N FLI C T O F I NTE R E S T
The authors declare that they have no conflict of interest and confirm that there are no disputes over the ownership of the data presented and all contributions have been attributed appropriately.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are openly available in the CABI data repository's Fall Armyworm Community at https:// ckan.cabi.org/data/datas et/updat ed_biope stici des_faw.