State Key Laboratory for Biology of Plant Diseases and Insect Pests,Institute of Plant Protection,Chinese Academy of Agricultural Sciences,Beijing 100193,P.R.China

Abstract The fall armyworm (FAW),Spodoptera frugiperda (J.E.Smith) (Lepidoptera:Noctuidae),a notorious migratory pest native to tropical and subtropical America,invaded China in December 2018,then spread through 26 provinces (autonomous regions,municipalities) in 2019 and 27 in 2020,damaging 1.125 and 1.278 million hectares of crops,respectively.Maize was the most severely affected crop,although wheat and other plants were also ruined.Considering the biological characteristics,incidence regularity and migration patterns of the FAW populations,Chinese government implemented a regional control strategy and divided the areas infested with FAW into the annual breeding grounds in Southwest and South China,the transitional migration area in Jiangnan and Jianghuai and the key preventive area in the Huang-Huai-Hai region and North China.The National Agro-Tech Extension and Service Center constructed “the National Information Platform for the Prevention and Control of the Fall Armyworm” at the county level,which would entail people reporting and mapping the spread of fall armyworm.According to forecasting information,millions of extension workers and small-scale growers in entire country were rallied by local governments to fight the pest through comprehensive control tactics including chemical,physical,biological and ecological measures.Thanks to the joint prevention and control,the final loss of crops infested was controlled within 5% of the total in 2019 and 2020.This review also gives a discussion on existing problems and future management scenarios.

Keywords:Spodoptera frugiperda,genetic characteristics,occurrence and damage,monitoring and early-warning,control measures

1.Introduction

The fall armyworm (FAW),Spodoptera frugiperda(J.E.Smith) (Lepidoptera:Noctuidae) is a notorious migratory pest native to tropical and subtropical America (Sparks 1979).Since its invasion into Africa in January 2016,it has swept across 44 countries in sub-Saharan Africa (Goergenet al.2016; Prasannaet al.2018),then quickly migrated into India in May 2018 (CABI 2018; Sharanabasappaet al.2018).In March 2018,Chinese scientists launched monitoring project to counter FAW in Pu’er City,the border area between Yunnan Province of China and Myanmar (Sunet al.2021; Wuet al.2019a,b; Wuet al.2020).Migrations from Myanmar into China was first recorded on 11 December 2018,and in January 2019,field investigations confirmed that it had infested maize-growing areas in Pu’er (Sunet al.2021).Since then,it had spread rapidly to 26 provinces(autonomous regions,municipalities) in 2019,seriously threatening China’s agricultural production and food security(Jianget al.2019b).

Since the invasion of the pest into China,the Chinese Central Government gave priority to preventing and controlling the FAW (MARA 2019c,e,f; Wuet al.2020).All related ministries and commissions promptly mobilized relevant research institutions to study and formulate emergency measures,the Ministry of Agriculture and Rural Affairs (MARA) set up a national expert group guiding the prevention and control work (MARA 2019c,e,f),the Ministry of Science and Technology of China launched the special project named “Research and Integration Demonstration of Key Technologies for Prevention and Control of the Fall Armyworm” (MOST 2019).In cooperation with other research institutes and universities,the Chinese Academy of Agricultural Sciences started a research program to determine biological traits of the pest,type and extent of damage,and developed monitoring and control measures to combat the species (Wu 2020; Wuet al.2020).On the basis of the research results,the MARA and the National Agro-Tech Extension and Service Center (NATESC) released timely precautionary measures to the public in the form of prevention and control plans or recommendations,and organized the implementation of these strategies (MARA 2019d,2020; NATESC 2019).

The Ministry of Finance allocated special relief funds to local governments to prepare emergency supplies to beat the pest in time (MARA 2019a),the MARA commanded and deployed nationwide monitoring,early warning and prevention and control network (MARA 2019c,d,e,f).Local governments have mobilized the agricultural extension staff to go deep into the field to guide small farmers in controlling the pest (MARA 2019b,g,f).Fortunately,China did not suffer great losses thanks to the high vigilance of the government and sound plant protection system.This review synthesizes the invasion process of the pest,hazards,important biological traits,monitoring and early warning system and emergency practices used against the fall armyworm from 2018 to 2020 in China.Current issues and future management scenarios are also discussed.

2.Genetic characteristics of invading S.frugiperda

During its evolution,the FAW differentiated into two subpopulations in the Americas,the “rice-strain” (R-strain)and the “corn-strain” (C-strain),which differ in their host preference,mating behaviors and environmental adaptability(Whitfordet al.1988; Quisenberry 1991; Pashleyet al.1992;Meagheret al.2011; Juárezet al.2012; Cañas-Hoyoset al.2016).The resistance level of FAW to chemical pesticides and genetically modified crops expressingBacilllusthuringiensis(Bt) also varies widely from one region to another.Organophosphates,carbamates and pyrethroids were the most popular insecticides in the American continent before the 1990s,however,their intensive application and indiscriminate use led to high resistance in FAWs (Diez-Rodrigues and Omoto 2001; Ríos-Díez and Saldamando-Benjumea 2011; Carvalhoet al.2013).Consequently,in the mid-1990s,Bt crops were rapidly adopted to address these control failures in the Americas (Huanget al.2011).Due to their outstanding performance in controlling pests,Bt crops have been widely planted in America for a long time (Huanget al.2011; Fatorettoet al.2017; Huang 2020),but FAWs in Brazil and Argentina have evolved resistance to Bt crops(Storeret al.2010; Omotoet al.2016; Chandrasenaet al.2018).Thus,planting Bt crops in combination with applying chemicals is the primary management practices to control the pest in recent years (Burtetet al.2017; Fatorettoet al.2017; Joneset al.2018; Huang 2020).

Elucidating genetic characteristics of invading populations is the foundation for developing monitoring,early warning and control strategies.Scientists from Agricultural Genomics Institute at Shenzhen,Chinese Academy of Agricultural Sciences reported the high-quality assembly of a 390.38-Mb chromosome-level genome of fall armyworm using Pacific Bioscience (PacBio) and Hi-C sequencing technologies (Zhang Let al.2020).Both genome-wide resequencing and molecular identification confirmed that the invasive FAW originated from a complex inter-strain hybrid population,mainly with the C-strain genetic background and less of the R-strain genetic information (Zhanget al.2019;Zhang Let al.2020).Genetic analysis suggested that the risk of FAW evolving resistance to organophosphates and pyrethroids is very high,while amides,Bt biopesticides and Bt crops are recommended as good control measures for these pests (Guanet al.2020; Zhang Let al.2020).These recommendations were further supported by laboratory bioassays and field trials (Zhang Let al.2020).The Chinese pest samples share a similar COI mitochondrial gene sequence with hybrid populations from South Africa,India and Florida in the United States (Zhanget al.2019)and thus,the invasive populations in Asia and Africa likely originated from the southeastern United States (Nagoshiet al.2019; Zhanget al.2019).

3.Occurrence and damage of Spodoptera frugiperda in China

3.1.Long-distance migration

Laboratory experiments revealed that the FAW has a great capacity for long-distance migration,during 24-h consecutive tethered flight,the FAWs could have the longest flight distance up to 62.98 km,and the overall flight performance was equal to that ofProtoschinia scutosabut weaker than those ofAgrotis segetumandMamestra brassicae(Geet al.2019).When they were tethered on a flight mill for five consecutive nights (i.e.,10 h/night),adult insects demonstrated strong flight capacity,163.58 km as the longest flight distance and 46.73 h as the longest flight time (Geet al.2021a).To elucidate the relationship between flight and reproduction,1–3-day-old moths were subjected to a 10-h flight,while some 1-day-old adults were paired kept in the plastic cups as the control,the results demonstrated that tethered FAW females had a significantly shorter pre-oviposition period and enhanced oviposition synchronization than the never-flown control group,while no marked variation appeared in the other reproductive variables (Geet al.2021b).Dissection of the reproductive organs from tested adults also revealed that flight activity promotes ovarian and testicular development and the mating percentage of the flighted adults is higher than the control FAW (Geet al.2021b).

Migratory insects are either obligate migrants or facultative migrants.Obligate migrants (i.e.,Mythimna separata) must engage in long-range flight to boost ovarian development after eclosion (Jianget al.2011); facultative migrants (i.e.,Helicoverpa armigera) do not necessarily need to migrate or fly long distances to reach sexual maturity and their migration is usually initiated by unfavorable conditions (i.e.,lack of host plants and overcrowded population) (Wu and Guo 2007).Because adult FAW needs to fly to stimulate ovarian development,we can presume FAW is a new obligate migrant in China (Geet al.2021a,b).

The capture of insect migrants on islands far from the continent and without host plants also provides strong evidence that FAW migrates long distances.Studies carried out on isolated Yongxing Island (16°49´59´´N,112°19´55´´E)confirmed that FAW migrates frequently across the South China Sea from April to September.Trajectory analysis revealed these adults fly more than 1 000 km from southcentral coastal Vietnam to south-central coastal China (Zhouet al.2021).Searchlight trapping on the small island of Beihuang (38°24´N; 120°55´E) in the center of the Bohai Strait revealed the species usually migrated across the Bohai Gulf waters from August to October (Jiaet al.2021).Thus,FAW migrates across most parts of Southeast and East Asia with the aid of East Asian monsoon and Indian monsoon (Maet al.2019; Li X Jet al.2020; Wuet al.2020).

3.2.Major host plants

FAW,a polyphagous pest,can infest at least 353 different plant species from 76 families in its native continent(Montezanoet al.2018).Since its invasion into China,field inspections have confirmed that it has infested many staple crops,destroying vast swaths of maize (Jianget al.2019b; Xuet al.2019; Sun X Xet al.2020),wheat (Jianget al.2019b; Yanget al.2020a),rice (Jianget al.2019b),sorghum (Jianget al.2019b),barley (Zhaoet al.2020),oat(Tanget al.2020),prosomillet (Zhaoet al.2020),peanut (Heet al.2020),oilseed (Heet al.2021c) rape (Heet al.2021c),soybean (Heet al.2021c),sunflower (Heet al.2021c),potato(Zhao Met al.2019),ginger (Jianget al.2019b),arrowroot(Jianget al.2019b),pepper (Jianget al.2019b),sugarcane (Li A Met al.2020),cabbage (Liuet al.2020),Chinese cabbage(Liuet al.2020),banana (Jianget al.2019b),tea plant (Sun X Let al.2020),curcuma (Jianget al.2019b) and tobacco(Xuet al.2019).In China,more than 1.125 million hectares of cropland were infested by FAW in 2019 and 1.278 million hectares in 2020 according to the data from the “National Information Platform for the Prevention and Control of the Fall Armyworm”.Maize was the most seriously affected,accounting for 98.1% of the total attacked area in 2019.In addition to crops,many farm weeds,such asAlopecurus aequalis,Digitaria sanguinalisandEchinochloa crusgallivar.mitis,are vulnerable to this destructive caterpillar (Yaoet al.2020; Zhang Y Het al.2020).

As the most favored host plants of FAW(Xuet al.2019;Heet al.2021b),maize can be damaged at any stage,especially young leaves and growing points (Wuet al.2020).It is also the most preferred oviposition plants for adults; the hatching rate and survival rate on maize are significantly higher than on other plants (Xuet al.2019).The larvae feast on leaves,bore spikelets and sometimes entire wheat grains (Zhang Zet al.2020).There is also high possibility that the larvae feed on upland rice in the absence of a suitable host,even though they are not voracious feeders of rice plants (Heet al.2021b; Wu 2020).Rather,larvae prefer to infest sugarcane; an estimated 11 847.9 ha of sugarcane were damaged in China in 2019(Jianget al.2019b).Young leaves,growing points and stem bases are the most vulnerable (Chormuleet al.2019;Li A Met al.2020).Larvae have also damaged potato in Shandong Province,causing wilting and death of potato seedlings (ZhaoMet al.2019).Numerous holes appear on the outer leaves and heart leaves of Chinese cabbage and cabbage from larval damaged,thus reducing vegetable quality (Liuet al.2020).

3.3.Regional migratory regularity

FAWs were present in 1 524 counties of 26 provinces(autonomous regions and municipalities) in 2019 and 1 426 counties of 27 provinces (autonomous regions and municipalities) in 2020,covering the tropical,subtropical and temperate climate zones of China (Fig.1).Variations in climate and crop production patterns also affect the regularity of the pest in a region compared with others.

In tropical zones with the minimum temperature higher than 15°C in winter,including areas of Hainan,and southern parts of Yunnan,Guangdong and Taiwan,the FAW can breed continuously.The tropical zone is also the principal winter corn region of China,so the FAW can successively produce 9–12 generations each year in this area (Chenet al.2020; Yanget al.2020b).Besides native-breeding populations,FAW from neighboring South East Asian countries (Myanmar,Laos and Viet Nam,etc.) can also be carried into this area by the prevailing monsoon in spring and summer (Wuet al.2019a,b).The subtropical zone,with daily lowest winter temperature higher than 10°C,mainly includes areas from southern Qinling Mountains–Huaihe River to areas north of the tropical climate zone,and a vast area in eastern part of the Hengduan Mountains,which can be subdivided into subtropical,middle subtropical and northern subtropical regions where FAW can survive bitter winters (Jianget al.2019a; Yanget al.2021).The central subtropical and northern subtropical regions are transitional zones for the migratory FAW.In the spring,they fly northward where they can produce 6–8 generations,infesting maize,wheat and rape among others,then return to the south in the autumn,because they cannot survive harsh northern winters.In the temperate zone,FAW is mainly found in areas of the northern Qinling Mountains–Huaihe River and southern Helan Mountain and Yinshan Mountain and eastern and southern of the Daxing’anling Mountains,where the FAW can produce 3–5 generations a year.However,only 1–2 generations are produced in the high altitudes of Gansu,Inner Mongolia and other regions in Northeast China,which is at higher latitudes (Chenet al.2020).Overall,tropical and south subtropical zones in China are the reservoir pool of the FAW,where pests can breed year-round.From April to May,the population in the Yangtze River Valley can spread into the Huang-Huai Region,where they propagate for 1–2 generations,and move into North China.Offspring produced in northern China can reach Northeast China from June to July.By autumn,populations in Northeast China,North China,Huang-Huai-Hai and Yangtze River regions successively sweep into winter-breeding zones (southern tropical and south tropical regions in China and Southeast Asia) (Wuet al.2020,2021).

Fig.1 Topographical map of China and migration pattern of fall armyworm in China.AH,Anhui; BJ,Beijing; CQ,Chongqing; FJ,Fujian; GD,Guangdong; GS,Gansu; GX,Guangxi; GZ,Guizhou; HA,Henan; HB,Hubei; HE,Hebei; HI,Hainan; HK,Hongkong;HN,Hunan; HLJ,Heilongjiang; JL,Jilin; JS,Jiangsu; JX,Jiangxi; LN,Liaoning; MO,Macao; NMG,Inner Mongolia; NX,Ningxia;SC,Sichuan; SD,Shandong; SH,Shanghai; SX,Shanxi; SN,Shaanxi; TJ,Tianjin; TW,Taiwan; XJ,Xinjiang; XZ,Xizang; YN,Yunnan; ZJ,Zhejiang.The two migratory routes were reproduced from Wu et al. (2021) and Jiang et al. (2019a).

4.Population monitoring and earlywarning system

Population monitoring and an early-warning program form the foundation for prevention and control of FAW.The Ministry of Agriculture and Rural Affairs requires plant protection institutions in China to carry out regional joint monitoring using a unified method.The NATESC constructed the“National Information Platform for the Prevention and Control of the Fall Armyworm” at the county level,which would entail people to report and map the spread of FAW.Through the implementation of the system of “discover and report in one day” in FAW-free regions and “two reports a week” in affected areas,the Chinese government can fully grasp the dynamics of the FAW and realize real-time dissemination of information and “coordinating all the activities of the nation like moves in a chess game” strategy (MARA 2019d,2020;NATESC 2019).

On the basis of the migratory patterns and damage characteristics of FAW,Chinese government has set up various monitoring stations such as vertically pointed searchlights and sex attractants in fields to enable rapid detection and response to migratory adults.Emitting highpower and high-intensity light-columns,search lights can attract migrants above the crop canopy,while ground lamps and sex traps can be used to monitor adults under the canopy(Wu 2020; Zhouet al.2020).By examining the ovarian and testis of adult insects,inspectors can assess the physiological nature of migrants and forecast the population dynamics of eggs and larvae (Heet al.2019; Zhao S Yet al.2019).During an outbreak,plant protection staff systematically survey maize,wheat,sugar cane,sorghum and other favorite hosts every three days for eggs,larval density and ratio of damaged to undamaged plants.This forecast information is posted to public through internet,radio,TV and other media outlets.

5.Technical measures for population control

Considering the regional strategy,joint prevention and control and comprehensive management,the MARA divided FAW-infested areas into:(1) the annual breeding area in Southwest and South China,(2) the transitional migration area in Jiangnan and Jianghuai and (3) the key preventive area in the Huang-Huai-Hai region and North China (Yanget al.2019).According to the divided three FAW-infested zones,authorities selected 205 counties from 17 provinces(autonomous regions,municipalities) along the migration routes to construct three control belts in Southwest and South China,Yangtze River Basin and the Huang-Huai-Hai region,the MARA urged local governments in these control belts to enhance field monitoring and strengthen employment of vertical-trapping light and sex attractant.Based on the results of ongoing filed surveys,millions of extension workers and smallholder farmers throughout China have been rallied by local governments to fight FAW using a comprehensive chemical,physical,biological and ecological control measures (MARA 2019c,d,e,f).Flexible management practices have been adopted in farmlands to contain the species; chemical pesticides are sprayed 1–2 times in large areas,3–5 times in seriously infested fields,with specific measures largely depending on the local severity.With the help of concrete,powerful management steps,the overall disposal rate of national crops infected by the pest was higher than 90%,and the final loss was controlled within 5% of the total in 2019 and 2020 (MARA 2020).

The MARA set up control threshold to guarantee crop safety,specifically,the crop damaged rate should be controlled within 8,5 and 3% in the annual breeding area,the transitional migration area and the key preventive area,respectively (MARA 2020).When insect density is higher than the established control threshold,officially recommended chemicals (spinetoram,indoxacarb,emamectin benzoate,chlorantraniliprole,etc.) with high efficiency and low risk of resistance could be alternatively sprayed in fields (MARA 2020).In the annual breeding zones,biological control agents,including Bt,Beauveriaand nucleopolyhedrosis virus,have received priority to combat FAW (Chenet al.2019).Field surveys demonstrated that natural predatory (Coccinellidae,Carabidae,Reduviidae,etc.) and parasitic enemies (Braconidae,Ichneumonidae,Eulophidae,Tachinidae,etc.) can constrain the development of FAW population to some extent (Tanget al.2019).These insect enemies of FAW should be protected and fully used to enhance ecological control.Based on the phototaxis and chemotaxis of adult FAW (Heet al.2021a),verticalsearch lights,ground lamps and sex attractants can be set up in areas where moths are expected to break out or pass through (Wuet al.2020).Eliminating potential host weeds should also greatly reduce damage from next-generation larvae and agricultural control measures such as tillage and irrigation during the pupal period can decrease the number of emerging moths (Wuet al.2020).

6.Outlook

Since the invasion of FAW,China has quickly integrated a complete system of monitoring,early warning and control protocols,which successfully controlled the pests in China.Despite its excellent performance in reducing pest damage,the system has two problems:(1) vast labor and material investment are required,(2) chemicals pollute the environment and induce insect resistance.Thus,the system does not meet the needs of green,high-quality and sustainable agriculture.Fortunately,breakthroughs in information technology and biological sciences have shed new light on these dilemmas,and Chinese scientists are doing their best to develop advanced control technologies.

With the maturation of entomological radar technology,China is stepping up its efforts to construct national-scale entomological radar networks (Wu 2020; Wuet al.2020;Zhouet al.2020).The radar is smart enough to identify insect species based on the physical parameters and flight behaviors,which contributes to monitoring and forecasting migrating populations and guiding regional prevention works(Zhouet al.2020).An intelligent application that relies on an image recognition system has been launched for farmers to identify the allied insect species during field inspections.By simply taking a photograph and uploading the image to the website http://migrationinsect.cn,users can identify the FAW in real-time (Wuet al.2020).With respect to biotechnology,food attractant and trans-genetic maize are also receiving attention.Food attractants developed from chemical communication mechanisms ofFAWefficiently trap adults of both sexes.Chinese domestic Bt-Cry1Ab and Bt-(Cry1Ab+Vip3Aa) maize also have high control efficacy against the FAW (Zhang and Wu 2019) and significantly reduce the population density and prevent migration by controlling source populations when planted commercially in the annual breeding region (Wu 2020).Comprehensive use of these innovative techniques will help China build a green,low-cost and high-quality monitoring,early warning and control systems for FAW,achieving the strategic goal of sustainable control.

7.Conclusion

The alien pest,FAW,has settled down in Southwest and South China,threatening crop production,with maize bearing the brunt of attack,in tropical,subtropical and temperate monsoon zones.Faced with the severe challenge of FAW,China established a national coordination mechanism to prevent damage from the FAW in a relatively short time.By implementing regional control strategy and constructing monitoring,early warning and control system,China did not suffer large blows from the pest in 2019 and 2020.In addition,advancements in info-technology and bioscience have led to innovations in monitoring and control,which will alleviate the intensive labor and material resources investment and chemical applications required by the current emergency management system.Looking to the future,by virtue of info-technology and biotechnology,China will develop a green,low-cost,high-quality monitoring,early warning and control system for FAW,realizing the strategic goal of sustainable control.

Acknowledgements

This work was supported by the National Key R&D Program of China (2019YFD0300102),the Central Public-interest Scientific Institution Basal Research Fund,China (CAASZDRW202007) and the earmarked fund for China Agriculture Research System (CARS-15-19).

Declaration of competing interest

The authors declare that they have no conflict of interest.