Prospects for Microbial Control of the Fall Armyworm Spodoptera Frugiperda: a Review

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Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review

Article in BioControl · June 2020 DOI: 10.1007/s10526-020-10031-0

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REVIEW

Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review

Jingfei Guo . Shengyong Wu . Feng Zhang . Chaolong Huang . Kanglai He . Dirk Babendreier . Zhenying Wang

Received: 2 January 2020 / Accepted: 16 June 2020 Ó International Organization for Biological Control (IOBC) 2020

Abstract The fall armyworm (FAW, Spodoptera Africa and Asia. However, concerns over the adverse frugiperda) is an important polyphagous insect pest in effects on environment and humans, and the develop- many crops. This highly invasive pest species origi- ment of resistance against insecticides have intensified nates from the Americas and recently spread rapidly efforts to develop alternatives that are effective and across more than 100 countries worldwide. It poses a low-risk, while at the same time cost effective. Given major threat to food security in a number of develop- that microbials are generally considered desirable ing countries due to its rapid spread and distinctive options for pest management, this review compiles ability to inflict widespread damage across multiple information on microbials in all phases of their crops. Chemical insecticides are used as the main development including entomopathogenic fungi, ento- management strategy to control FAW in many parts of mopathogenic nematodes, bacteria and baculoviruses, the world, particularly in the recently invaded areas in with a special focus on their efficacy against FAW. In addition, combinations of microbial agents and also mixtures with compatible insecticides for improved Handling Editor: Nicolai Meyling control of FAW are reviewed. The findings are discussed in light of improving management programs J. Guo Á S. Wu Á C. Huang Á K. He Á Z. Wang (&) of FAW State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China Keywords Spodoptera frugiperda Á Microbials Á e-mail: [email protected] Biological control Á Combined application

F. Zhang MARA-CABI Joint Laboratory for Bio-Safety, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China Introduction

C. Huang The fall armyworm (FAW), Spodoptera frugiperda (J. Engineering Research Center of Natural Enemy Insects/ Institute of Biological Control, Jilin Agricultural E. Smith) (Lepidoptera: Noctuidae), is a highly University, Changchun 130118, China polyphagous pest of global relevance, and in particular threatening maize production systems worldwide. & D. Babendreier ( ) This pest could result in a maize yield reduction of CABI Switzerland, Rue des Grillons 1, 2800 Dele´mont, Switzerland up to 70% when maize plants are attacked during early e-mail: [email protected] stages (Ayala et al. 2013; Hruska 2019). The FAW is 123 J. Guo et al. also causing significant damage to other crops, sustainable control of FAW in the newly invaded including cotton, rice, soybean, tomato, potato, onion, areas. bean, cabbage, sorghum, as well as several grass Microbial-based pesticides have long been consid- species by feeding on different organs of the plants ered in integrated pest management strategies (Souza (Day et al. 2017). FAW is indigenous throughout the et al. 2019), and have earlier been discussed in the Americas (Todd and Poole 1980) and has not been context of FAW control (Gardner et al. 1984). In a reported in any other parts of the globe until 2015. recent overview paper, Day et al. (2017) mentioned However, it was recorded in Africa in 2016 for the first that several microbials, including entomopathogenic time and it caused serious damage on maize in several fungi, entomopathogenic nematodes, viruses and countries that same year (Goergen et al. 2016). Within bacterium attack FAW, without going further into less than three years it invaded 44 African countries details. An interesting point is also that microbials can (Feldmann et al. 2019) as well as several Asian often be seen killing FAW larvae in African maize countries (CABI 2019; Guo et al. 2018). The spread of fields, especially under wet conditions (personal FAW into China has been documented with a first observation) and several organizations, including report in January 2019 from Yunnan Province (Zhang FAO or CABI, recommend smallholders to produce et al. 2019). Until autumn 2019, it has spread to 26 their own home brews from them (CABI 2019). For provinces across the country and has become a serious the present review, a search was conducted in the Web pest on maize (Jiang et al. 2019). Its enormous of Science covering the past 50 years, using the invasion capacities and potential harm have attracted keywords ‘Spodoptera frugiperda’ and ‘microbial’. the attention of many governments and scientists, The number of studies was refined to include those particularly from the area of applied pest management. where representative studies focused on laboratory It is thus expected that this review will be helpful and bioassays and field applications of each microbial timely for them, providing information about the agent against FAW. Information on field collections of efficacy of microbial-based pesticides allowing to microbials is also provided. Finally, we provide develop locally adapted strategies for FAW suggestions for improved FAW management practices management. based on microbials, with the aim of contributing to The control of FAW in the recently invaded areas reduced impact of this globally invasive species. has been a major issue because of the devastating economic damage it causes. In the native range, i.e. the Americas, a range of management tactics are being Entomopathogenic fungi applied against FAW. While the deployment of transgenic pest-resistant crops is the dominating Entomopathogenic fungi (EPFs) considered for FAW strategy, also insecticides and biological control are control mainly belong to Beauveria bassiana (Bal- used by farmers (Burtet et al. 2017). In Africa, cultural samo) Vuillemin, Metarhizium rileyi (Farlow) Kepler, control methods have been shown to be effective (Day SA Rehner and Humber (formerly in the genus et al. 2017), but the most commonly employed method Botrytis, Spicaria or Nomuraea) and Metarhizium is the use of chemical insecticides (Tambo et al. 2019). anisopliae (Metschn.) (Faria et al. 2015; Lezama- However, the heavy application of conventional Gutie´rrez et al. 1996; Wraight et al. 2010). All of them insecticides and reliance on them as single control have been associated with FAW in the field (see method may promote the development of resistant Table 1) and have demonstrated their potential to FAW populations, and in the long run, be ineffective control FAW. However, the development of fungal and unsustainable (Day et al. 2017). Specifically, infections and co-occurrence of pathogens in the host multiple applications or high dosages of insecticides is largely influenced by environmental conditions. are known to kill many beneficial insects, including Under suitable conditions, particularly high relative natural enemies of FAW, pollute the environment and humidity, external sporulation helps to spread the pose health risks to farmers and consumers (Kebede fungus and may cause an epizootic in FAW popula- and Shimalis 2018). Thus, there is an urgent need to tions (Hoverman et al. 2012; Khan and Ahmad 2015). develop and introduce biological alternatives for The EPF B. bassiana is widely distributed in nature and capable of infecting a variety of insects. 123 Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review

Table 1 Incidence of microbials infesting FAW larvae from ﬁeld collections Microbialsa Crop Infection Country References rate

Bacillus thuringiensis (Bt) Soil samples from maize and – Mexico Lezama-Gutie´rrez et al. sorghum (2001) Beauveria bassiana Cotton – Brazil Kaur and Padmaja (2009) Maize 0.16% Mexico Rios-Velasco et al. (2011) Maize 0.65% Mexico Ordońez-Garcıá et al. (2015) Soil samples from maize and 0–1% Mexico Lezama-Gutie´rrez et al. sorghum (2001) Granulosis virus (GV) Maize, sorghum and pastures 3% USA Fuxa (1982) Heterorhabditis sp. Soil samples from maize and 0–15% Mexico Lezama-Gutie´rrez et al. sorghum (2001) Hexamermis spp. Maize 8% Mexico Ruiz-Na´jera et al. (2013) Metarhizium anisopliae Soil samples from maize and – Mexico Lezama-Gutie´rrez et al. sorghum (2001) Metarhizium rileyi Maize – Mexico Ayala-Zermenõ et al. (2017) Soil samples from maize and 0–17% Mexico Lezama-Gutie´rrez et al. sorghum (2001) Maize 9% Mexico Ordońez-Garcıá et al. (2015) Maize 0.75% Mexico Rios-Velasco et al. (2011) Maize 3% Mexico Ruiz-Na´jera et al. (2013) Maize – India Shylesha et al. (2018) Maize 2–14% India Mallapur et al. (2018) Maize – Colombia Villamizar et al. (2004) Nucleopolyhedrosis viruses Maize, sorghum and pastures 51% USA Fuxa (1982) (NPV) Maize 2% Mexico Rios-Velasco et al. (2011) Cordyceps fumosoroseab Soil samples from maize and – Mexico Lezama-Gutie´rrez et al. sorghum (2001) Steinernema sp. Sorghum and sudan grass 0–15% Mexico Molina-Ochoa et al. (2003) aMicrobials are listed alphabetically bCordyceps fumosorosea (Syn. = Isaria fumosorosea, Paecilomyces fumosoroseus)

Laboratory assays, in which the 2nd instar larvae of and Pringle 2004). Endophytic colonisation produce FAW were topically sprayed with conidial suspen- secondary metabolites in planta or induce plant sions of the commercial B. bassiana strain GHA responses, resulting in negative effects on insect registered in the USA as BotaniGardÒ, showed a herbivores (McKinnon et al. 2017). It was reported median lethal concentration (LC50) of 1213 conidia that B. bassiana inoculated in plant roots can be mm-2 while application at a dose of 4234 conidia subsequently recovered from stems and leaves (Tefera mm-2 caused 95% mortality (Wraight et al. 2010). and Vidal 2009), suggesting a new avenue for FAW Garcıá and Bautista (2011) reported that B. bassiana control. For instance, Ramirez-Rodriguez and Sań- (strain Bb42) obtained from field collected FAW chez-Penã(2016) assessed the pathogenicity of a larvae showed the virulence of 96.6% mortality to 2nd strain of the fungus B. bassiana, which was originally instar larvae at a concentration of 1 9 109 conidia isolated from soil, but thereafter introduced as endo- ml-1. phyte in maize, and confirmed that the endophytic Beauveria bassiana can behave as an endophyte strain caused 75% larval mortality by day 14 of the and colonize a variety of plants such as maize (Tefera experiment.

123 J. Guo et al.

Metarhizium rileyi is a fungal entomopathogen when treated with a concentration of 5.3 9 105 which has been considered for control of many conidia ml-1 of M. anisopliae (strain CP-MA1) was lepidopteran insects, including FAW (Fronza et al. reported to be 72.5% at 72 h post-infection (Romero- 2017). Natural occurrence of this fungus has been Arenas et al. 2014). Similar bioassays recently showed demonstrated in the area of origin in Mexico with that three strains of M. anisopliae, Ma22, Ma41 and about 3% of FAW larval mortality (3rd–6th instar) in Mr8, caused 100% mortality in both eggs and neonate whorl stage maize (Ruiz-Na´jera et al. 2013). It has also larvae (Cruz-Avalos et al. 2019). Metarhizium aniso- been found to cause natural field epizootics of FAW pliae ICIPE 78 caused egg mortality of 87%, and M. larvae in maize in Colombia (Villamizar et al. 2004) anisopliae ICIPE 41 caused 96.5% in the neonate while Shylesha et al. (2018) recently found natural larvae (Akutse et al. 2019). Metarhizium anisopliae infections of FAW by M. rileyi in maize fields in India, Ma-San Rafel-2 caused 68.7% mortality in FAW i.e. in the year of introduction (Table 1). adults (Gutie´rrez-Ca´rdenas et al. 2019). Cha´vez et al. (2004) evaluated the activity of ten Sańchez-Penã et al. (2007) compared the activity of isolates of M. rileyi against 2nd instar larvae of FAW different strains of EPFs (isolated from soil or insects) by spraying the fungus at a concentration of 1 9 107 against FAW larvae by submerging insects in conidial conidia ml-1, and found one of the most effective suspension (1 9 108 ml-1). The study demonstrated isolates, Nm-07, causing 100% mortality, with lethal that the M. anisopliae strain UA-12 derived from soil times (LT50 and LT90) of 6.2 and 7.9 days, respec- was more active (90% mortality on FAW) than the B. tively (Table 2). Other bioassays showed that M. rileyi bassiana insect-derived strain (80% mortality on isolates obtained originally from FAW were highly FAW). This suggests that the isolation of M. aniso- virulent to FAW, with mortality rates of 53.3–82.2% pliae strains from local soils may be a promising and LT50 of 4.8–8.5 days, following treatments at a alternative for the biological control of FAW with low concentration of 1 9 108 conidia ml-1 (Tigano- environmental impacts. Milani et al. 1995). Grijalba et al. (2018) evaluated Additional EPFs for FAW management may the efficacy of M. rileyi formulated as an emulsifiable include Fusarium solani and M. robertsii. Both fungi concentrate against FAW larvae on maize plants under showed in vitro effectiveness against FAW, with 48% glasshouse conditions. The results showed LC50 and and 49% survival probability of FAW larvae after 4 8 -1 LC90 values of approximately 1.2 9 10 and seven days at concentrations of 1 9 10 spores ml , 4.0 9 106 conidia ml-1, respectively, and a 57% respectively. This effectiveness has been found to reduction in damage of plants at the rate of 1.3 9 1012 increase through the addition of vegetable oils (Her- conidia ha-1. The application of a granular formula- nandez-Trejo et al. 2019a). Recent field trials demon- tion of M. rileyi consisting of 1 mm particles of strated that M. robertsii decreased the incidence of defatted maize germ containing 107 conidia g-1 killed FAW larvae on maize from 41.3 to 2.8% by the first 80% of FAW larvae in laboratory bioassays (Pavone application and 17.4 to 8.3% in the second application. et al. 2009). Recently, large scale field trials in India Thus, M. robertsii shows potential as an effective involving a M. rileyi formulation (Institute of Organic biological control agent against FAW (Hernandez- Farming, UAS, Dharwad) at 2 g l-1 onto the maize Trejo et al. 2019b). leaf whorls revealed a 58.9 to 62.9% reduction of Cordyceps fumosorosea (Syn. = Isaria fumosoro- FAW incidence (Mallapur et al. 2018). sea, Paecilomyces fumosoroseus) and Isaria javanica Metarhizium anisopliae is a widespread soil borne were also highly pathogenic to both FAW eggs and fungal pathogens of insects, ticks and mites (Butt et al. larvae (Lezama-Gutie´rrez 1996). Laboratory bioas- 2014). Regarding FAW, laboratory bioassays have says and scanning electron microscopy observation shown M. anisopliae to be highly pathogenic to both showed that C. fumosorosea (isolate 4461) develop eggs and neonate larvae, with mortality rates of 100% visible penetrant hyphae in cuticle cross-sections of and LT50 values of 2.5 days for the egg stage and FAW larvae within 22 h after inoculation (Altre and 3.1 days for larvae after 48 h exposure to maize leaves Vandenberg 2001a, b). Further bioassays demon- previously immersed into a suspension of conidia strated that germinated conidia with either one or (1 9 108 ml-1) (Lezama-Gutie´rrez et al. 1996). The two germ tubes and hyphal bodies of C. fumosorosea mortality of 3rd instar larvae of FAW in the laboratory were more aggressive than ungerminated conidia 123 Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review

Table 2 Overview on tests for susceptibility of FAW larvae to microbials conducted under laboratory, greenhouse or ﬁeld conditions, including experimental set up, country and references Microbialsa Isolate Experimental System Mortality/control efﬁcacy Country References set up

Bacillus 11 isolates Plastic cups Laboratory – Brazil dos Santos thuringiensis et al. (2009) (Bt) KN50, KN11 24-well tissue Laboratory – China Liu et al. KNR8 culture (2019) plates Maize leaves Field 61–87% China Liu et al. (2019) 1644, 344 Plastic cups Laboratory – Brazil Valicente and Lana (2010) – Plastic cups/ Laboratory 7% Puerto Viteri et al. artificial Rico (2018) diet Dendrolimus HD Biological Laboratory HD68: 100%, 4412: 80% Brazil Polanczyk 37, aizawai Oxigen et al. (2000) HD68, kurstaki Demand HD73, chamber darmstadiensis HD 146, thuringiensis 4412 Beauveria ABG6112 Soil Laboratory 37% USA Storey and bassiana Gardner (1986) – Maize leaves Laboratory 54–100% Mexico Lezama et al. (1996) Bb42, Bb18 Maize leaves Laboratory Bb42: 97%, Bb18: 93% Mexico Garcıá and Bautista (2011) UA-3 Plastic cups Laboratory 72–100% Mexico Sańchez-Penã UA-21 et al. (2007) – Maize plants Laboratory 98% Mexico Ramirez- Rodriguez and Sańchez- Penã(2016) CG1027 Maize leaves Laboratory 30–50% Brazil Faria et al. (2015) Many isolates 12-well plate Laboratory 61–97% USA Wraight et al. (2010) – Soybean Laboratory 83% USA Gardner et al. leaves (1977) Bb39, Bb19, Bb27, Maize leaves Laboratory Bb39: 70%, Bb19: 60% Mexico Cruz-Avalos Bb23, Bb21, Bb27: 54%, Bb23: 53% et al. (2019) Bb40 Bb21: 28%, Bb40: 19% ICIPE676 Maize leaves Laboratory 30% Kenya Akutse et al. (2019) Fusarium solani A1 Plastic cups/ Laboratory 30% Me´xico Hernandez- P3Maize 52% Trejo et al. leaves (2019a) P4 30%

123 J. Guo et al.

Table 2 continued Microbialsa Isolate Experimental System Mortality/control efﬁcacy Country References set up

Heterorhabditissp. – Eucalypt Laboratory – Brazil de Souza et al. plants (2012) H. bacteriophora – Plastic cups Laboratory 65% Nicaragua Zamora et al. and H. indica (2019) H.bacteriophoa – Asparagus Laboratory 68–78% (pre-pupa) Peru Alonso et al. plants Greenhouse 48–62% (pupae) (2018) – Maize leaves Field 73% Costa Pe´rez (2016) Rica Metarhizium – Maize leaves Laboratory – Mexico Lezama et al. anisopliae (1996) Ma91 Maize leaves Laboratory 79% Mexico Garcıá and Bautista (2011) – Maize leaves Field – Brazil Silva et al. (2008) UA-12, UA-11 Plastic cups Laboratory 60–100% Mexico Sańchez-Penã et al. (2007) Ma22, Ma41, Mr8 Maize leaves Laboratory 100% Mexico Cruz-Avalos et al. (2019) ICIPE78, ICIPE40, Maize leaves Laboratory eggs ? neonates Kenya Akutse et al. ICIPE20, ICIP41: 98%, ICIPE7: 96% (2019) ICIPE41, ICIPE4: 94% ICIPE7, ICIPE655, ICIPE20: 93% ICIPE78: 92% ICIPE655: 95% – Maize leaves Field 90% Costa Pe´rez (2016) Rica M. rileyi 10 isolates Maize leaves Laboratory 73–100% Tibaitata´ Cha´vez et al. (2004) Nr-003 Maize leaves Laboratory – Cuba Ce´spedes et al. (2008) Nm06 Maize plants Glasshouse 57% Colombia Grijalba et al. (2018) LPFIBE-3 Ricinus Laboratory 80% Venezuela Pavone et al. comunis (2009) leaves – Soybean Laboratory 98% USA Gardner et al. leaves (1977) – Maize leaves Field 59–63% India Mallapur et al. (2018) M. robertsii P1 Plastic Laboratory 43% Me´xico Hernandez- cups/maize Trejo et al. leaves (2019a) – Maize plants Field 9–39% Me´xico Hernandez- Trejo et al. (2019b) Nigrospora SFP2 Plastic cups/ Laboratory & 45% Me´xico Hernandez- sphaerica Maize Trejo et al. leaves (2019a) 123 Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review

Table 2 continued Microbialsa Isolate Experimental System Mortality/control efﬁcacy Country References set up

Nosema necatrix – Soybean Laboratory – USA Gardner et al. leaves (1977) Nucleopolyhedrosis Sf-2, Sf-NIC, Sf- Petri dish Laboratory – Spain Escribano viruses (NPV) AR, Sf-US et al. (1999) – Maize, millet Laboratory – USA Richter et al. signalgrass (1987) Cordyceps – Maize leaves Laboratory – Mexico Lezama et al. fumosoroseab (1996) 4461 12-well tissue Laboratory – USA Altre and culture Injection Vandenberg plates assays (2001a, b) 1576, 4461, 1576 12-well tissue Laboratory – USA Altre and culture Vandenberg plates (2001a, b) Isaria javanicac – Maize leaves Laboratory – Mexico Lezama et al. (1996) Penicillium citrinum P2 Plastic cups/ Laboratory & 30% Me´xico Hernandez- Maize Trejo et al. leaves (2019a) Photorhabdus SL0708 Glass tube Laboratory intra extracts: 10% Colombia Salazar- luminescens with cotton extracellular extracts: 93% Gutie´rrez subsp. cap et al. (2017) Steinernema – Petri dishes Laboratory 1–28% USA Espky and carpocapsae Capinera (1994) – Plastic cups/ Laboratory 35% Puerto Viteri et al. artificial Rico (2018) diet Steinernema feltiae – Vegetative Field 33–43% USA Richter and field maize Fuxa (1990) Steinernema – Plastic Laboratory 90% Mexico Leyva- riobrave box/filter Hernandez paper et al. 2018 Steinernema sp. – PVC pipes Greenhouse 78% Brazil Andalo´ et al. (2012a, b) aMicrobials are listed alphabetically bCordyceps fumosorosea (Syn. = Isaria fumosorosea, Paecilomyces fumosoroseus) cIsaria javanica (Syn. = Paecilomyces javanicus)

against 1st instar larvae of FAW, causing a mortality Entomopathogenic nematodes of 61% for larvae treated with hyphal bodies at a dosage of 3 9 104 propagules cm-2 (Fargues et al. Entomopathogenic nematodes (EPNs), especially 1994). Injection of FAW larvae with C. fumosorosea from the genera of Steinernematidae and Heterorhab- (isolate 4461) resulted in a signiﬁcantly longer devel- didae, have been effectively applied in pest control opment time to pupation compared to uninfected (Grewal et al. 2005) and proven to be virulent and larvae (Altre and Vandenberg 2001a, b). lethal to FAW in a recent laboratory study conducted

123 J. Guo et al. in South America (Zamora and Markelyn 2019). insects, water and grain dust (De Maagd et al. 2001). Isolates of either Heterorhabditis bacteriophora or H. Susceptibility of FAW to Bt has been tested by using indica caused 65% mortality of FAW larvae after 48 h several Cry endotoxins (Cry1Ac, Cry1Ab, Cry1Ca at a dose of 40 and 170 infective juveniles, respec- and Cry1Ea) and differences in susceptibility among tively (Zamora and Markelyn 2019). them was observed (Monnerat et al. 2006). Comparing Alonso et al. (2018) evaluated the effect of H. the two strains of FAW (rice strain and corn strain) bacteriophora on FAW and found that the most showed that the rice strain was more susceptible than efficient dose against prepupae and pupae of FAW was the corn strain to the endotoxin Cry1Ab for the 5000 EPNs ml-1, causing a mortality of 92 and 80% in parental, F1 and F2 generations (Rıós-Dıéz et al. the laboratory, and 78 and 62% mortality in the 2012). Recent susceptibility bioassays of FAW greenhouse, respectively. Infestations of FAW adults neonates to Cry1Ab, Cry1Ac, Cry1F, Cry2Ab and with an ectoparasitic nematode, Noctuidonema guya- Vip3A by using artificial diet overlay assays indicated nense, reduced longevity of adult males and females that the descending order of the lethal concentration by 30% and 15%, respectively, and the fertility of ranked as Vip3A [ Cry1Ab [ Cry1F [ Cry2Ab [ infested females was reduced by up to 20% (Simmons Cry1Ac, with LC50 values of 50.3, 161.3, 207.8, and Rogers 1994). Bioassays showed that Photorhab- 603.7 and over 800 ng cm-1, respectively (Li et al. dus luminescens SL0708 bacterial isolate, a symbiont 2019). of H. indica SL0708, is highly pathogenic for FAW Surveys in different geographical regions have larvae. Following a treatment with 1 9 103– shown that Bt is widely distributed in the world, while 1 9 104 CFU larvae-1, 100% mortality was attained the infectivity against FAW did not appear to be after 48 h (Salazar-Gutie´rrez et al. 2017). In labora- correlated with origin (Bernhard et al. 1997). Strains tory tests, Steinernema arenarium and Heterorhabdi- isolated from soil samples in different geographical tis sp. RSC02 at a concentration of 200 infective regions covering 96 counties in ten Brazilian states juveniles larvae-1 caused 100 and 97.6% mortality of were evaluated against FAW larvae in the laboratory. FAW larvae, respectively. In the greenhouse the same The results showed that the majority of strains (62% of nematodes caused 77.5 and 87.5% mortality, respec- the samples) caused 81% to 100% mortality, while tively, when compared to the control (7.5%) (Andalo´ 31% of the samples caused less than 20% mortality et al. 2012a). In contrast, S. carpocapsae has shown (Valicente and Barreto 2003). Additional virulence low levels of host infectivity of FAW larvae (from 1 to assays showed that suspensions of Bt (strains aizawai 28%) (Espky and Capinera 1994). HD 68 and thuringiensis 4412) containing 3 9 108 In vegetative field corn, spraying the nematode S. cells ml-1, induced mortalities of 100 and 80.4% in feltiae onto maize ears resulted in a significant 2nd instar larvae of FAW, with LC50 values of reduction of FAW larvae but did not positively affect 6.7 9 106 and 8.6 9 106 cells ml-1, respectively yield (Richter and Fuxa 1990). Recently, Fallet et al. (Polanczyk et al. 2000). Selective bioassays from one (2019) tested EPNs that have been isolated from soil hundred strains of Bt isolated from soil and water samples in Rwanda and found that they can effectively samples from different regions of Brazil showed that infect and kill FAW larvae in the laboratory. Since the only eight strains had toxicity above 70% to FAW larvae are targeted in the whorl, the most promising larvae on the fifth day (dos Santos et al. 2009). Some EPNs will be incorporated into a carrier to protect Bt isolates were reported to cause sublethal effects on them from desiccation and UV radiation (Fallet et al. FAW, such as changes in biological parameters of 2019). FAW, mainly larval and female pupae weight, which in some instances led to reduced female fecundity (Polanczyk and Alves 2005). The Bt strain 366-0476 Bacillus thuringiensis of subsp. kurstaki exhibited a sublethal effect observed as wing deformities in 20.8% of the newly emerged The entomopathogenic bacterium Bacillus thuringien- FAW adults (Arango et al. 2002). Recently, three sis Berliner (Bt) is a gram-positive bacterium that virulent Bt strains (KN50, KN11 and KNR8, Wuhan produces crystal proteins (d endotoxins) during the Kernel Bio-tech Co. Ltd, China) showed very high sporulation process and occurs naturally in soil, dead efficacy against neonates of FAW, with LC50 values of 123 Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review

0.07, 0.23 and 0.43 lgg-1. Field trials using the strain Droplet feeding bioassays with 2nd instar larvae of KN50 at 32,000 IU mg-1 showed a control efﬁcacy of FAW indicated that the nucleopolyhedrovirus (NPV) 72.6 and 86.6% for 0.3 and 0.6 g m-2, respectively, isolates Sf-NIC and Sf-US showed the highest infec- against larval populations of mixed instars at seven - tivity among four strains isolated from infected FAW 5 5 days post-treatment (Liu et al. 2019). larvae, with LC50 values of 2.0 9 10 and 2.2 9 10 Transgenic maize is the main approach to combat OBs ml-1, respectively (Escribano et al. 1999).

FAW in the Americas, for example TC1507 maize SfMNPV isolates from Colombia had LC50 values expressing the Cry1F protein from Bt variety aizawai ranging from 2.2 9 105 to 7.0 9 105 OBs ml-1 for was registered in the USA in 2001 to control FAW FAW larvae (Valderrama et al. 2010). Spodoptera (Siebert et al. 2008). However, Bt crops are contro- littoralis nucleopolyhedrovirus (SpliNPV) has also versially discussed for Africa where it is currently shown to be virulent against the 1st–3rd instar larvae commercially available only in South Africa. Due to of FAW, and significantly increased larval duration, the intensive use of Bt crops, field resistance of FAW decreased pupation, larval weight, and in some cases to Cry1F maize has occurred in Puerto Rico, Brazil adult emergence (El-Sheikh 2015). Several studies and the USA (Yang et al. 2016). In order to tackle found evidence for vertical transmission of the virus issues with resistance to individual Bt toxins, combi- from parents to the progeny of host insects (Cory and nations of Bt proteins (stacked genes) are nowadays Myers 2003). For example, an NPV isolated from common practice in the deployment of transgenic FAW generated 14% mortality in offspring of infected plants. A recent study compared the toxicity of FAW larvae (Rothman and Myers 1996). Cry1Ab, Cry1Ac, Cry1Ca, Cry1Ea, Cry2Aa, Cry2Ab, Field trials with a wettable powder formulation of a Vip3Aa and Vip3Ca in single and combined assays nuclear polyhedrosis virus (SfNPV) for control of against neonate FAW, demonstrating synergistic FAW larvae on maize showed that the virus can be action occurring for all protein mixtures, with the used at dosages of 1.25 9 1012 PIBs (polyhedral highest toxicity observed for the mixture of Vip3Aa ? inclusion bodies) ha-1, causing 93.4% larval mortality Cry1Ab (Figueiredo et al. 2019). In light of the above (Cruz et al. 1997). Field application of a formulation positive results and resistance issues in general, based on microencapsulated SfMNPV at a dose of combinations of Bt toxins should also be more 8 9 1011 OBs ha-1 (800 g ha-1) can protect the maize strongly considered for spray applications, and such crop, with the level of fresh damage in maize plants work is ongoing at, e.g. International Centre of Insect maintained below the economic injury level in Physiology and Ecology (ICIPE) in Kenya. Colombia (Cubillos 2013). Littovir (RAVAGEX), which is a Spodoptera sp. baculovirus-based product initially developed for Nucleopolyhedrovirus control of S. littoralis, has successfully been tested and registered by Andermatt Biocontrol for control of Virus-based biopesticides, particularly those from the FAW in Cameroon (CABI 2018). Further research and Baculovirus group with their high host specificity and development projects are running to provide the most virulence, have been identified as having considerable effective baculovirus isolate, such as Spodoptera potential for sustainable FAW control (Barrera et al. frugiperda MNPV isolates. For another product, 2011). Recently it has been shown that FAW strains Fawligen, produced by AgBiTech and based on a resistant to chemical insecticides and Bt proteins were multiple nucleopolyhedrovirus isolate, efficacy testing susceptible to the Spodoptera frugiperda multiple is in progress in Africa (Rwomushana et al. 2018). nucleopolyhedrovirus (SfMNPV: Bentivenha et al. Given the good level of efficacy even under field 2018). However, sensitivity depends much on larval conditions and the favorable environmental profile of instar as it was reported that the LC50 of FAW larvae to NPV, there is generally great potential for their use in SfMNPV increased tenfold from 2nd to 5th and even sustainable FAW control. more drastically for the 6th instar (Escribano et al. 1999).

123 J. Guo et al.

Enhancing the bioefficacy of microbials against As shown above, the combined use of microbials FAW has the potential to increase the efficiency to control lepidopteran pests. However, in some cases, co- As shown above, FAW is susceptible to many kinds of infections of the same insect by more than one microbials, some of which have the potential to play a pathogen species may naturally occur. This in turn significant role in the future management of FAW can result in negative (antagonistic) interactions, for (Bateman et al. 2018; Gardner et al. 1984; Hruska instance, when pathogens compete for host tissues, or 2019; Rwomushana et al. 2018). However, the control result in positive (synergistic) interactions, when efficacy when applied alone may be below what pathogens increase the susceptibility of virus-infected farmers like to see on a regular basis. As one reason, insects to the fungus (Souza et al. 2019). The adverse environmental conditions such as high tem- prevalence in co-infections depends on the host peratures might be responsible for lower mortality, species and inoculation strategy. Therefore, more therefore compromising their efficacy (Viteri et al. studies should be conducted to better understand how 2018). There is growing evidence that using combi- microbials interact with eachother, aiming to enhance nations of biocontrol agents can greatly improve pest their overall performance. control, e.g. due to synergistic or additive effects occurring between agents, an active field of research Combined use of insecticides with microbials during recent years (Sayed and Behle 2017; Viteri et al. 2018). Below we review information where Several laboratory and field studies have demonstrated different types of biological agents have been used in that the combined use of chemical insecticides and combination against FAW, as well as those studies EPFs may improve fungal infectivity of insect pests reporting on the combined use of insecticides with (Gosselin et al. 2009; Quintela et al. 2013). De Souza microbials. et al. (2012) found the insecticide imidacloprid did not affect the viability and infectivity of the EPNs Combined use of microbials Steinernema and Heterorhabiditis towards FAW. Bioassays showed that the use of the EPN S. The EPN H. bacteriophora and the EPF M. anisopliae carpocapsae in combination with low-toxicity insec- have been proven to be virulent to FAW and may be ticides chlorantraniliprole or spinetoram imposed considered for FAW control in combination as they higher mortality on FAW 5th instars compared to the were found to be compatible when mixed and applied use of these insecticides alone. The highest larval together (Pe´rez 2016). Results from laboratory and mortality of more than 90% was observed after 72 h greenhouse showed synergism and additive effects (Viteri et al. 2018). when EPNs and EPFs are used together and point Three EPNs, H. indica, S. carpocapsae and S. towards a great potential for more economical pest glaseri, are also considered to be compatible with the management (Ansari et al. 2008). Pe´rez (2016) majority of insecticides registered in Brazil for the reported that the combination of H. bacteriophora control of FAW in maize (Negrisoli et al. 2010a). A (0.67 ml m-2) and M. anisopliae (0.65 g m-2) field study evaluated the EPNs H. indica and S. produced a 100% mortality of FAW larvae five days carpocapsae mixed with the insecticides chlorpyrifos post-application under field conditions, while single and lufenuron for control of FAW in corn. The results applications of H. bacteriophora and M. anisopliae showed that the best treatment was the mixture of H. caused 80 and 93% larval mortality, respectively. A indica with lufenuron (0.15 1 ha-1), with 62.5 and combination was also tested in laboratory bioassays 57.5% larval mortality in the two consecutive years, involving the EPN S. carpocapsae and the commercial respectively (Negrisoli et al. 2010b). A study includ- product Bt DipelÒ WG (Sumitomo Chemical) with ing EPFs further found that a combined treatment of promising results, i.e. high larval mortality rates of H. bacteriophora ? M. anisopliae ? chlorpyrifos 81.3% observed after 96 h, compared to larval mor- can be an effective control measure for FAW, tality caused by Bt (6.7%) or S. carpocapsae (35%) resulting in minimum crop damage (Pe´rez 2016). when applied alone (Viteri et al. 2018). Rivero-Borja et al. (2018) reported that low doses of spinosad followed by B. bassiana applications 123 Prospects for microbial control of the fall armyworm Spodoptera frugiperda: a review produced synergistic mortality of 3rd instar larvae of immune-related genes, causing increased susceptibil- FAW. Not unexpectedly, however, the situation is ity to insect pathogens (Baradaran et al. 2019). somewhat different when fungicides are combined Nowadays, only a relatively small number of the with EPF, e.g. it was found that M. anisopliae strains identified biopesticides that can potentially be used are susceptible to some fungicides, such as azoxys- against FAW are registered (e.g. Bateman et al. 2018), trobin, which inhibits the growth of the fungus (France and most countries actually prefer to use indigenous and Yan˜ez 2010). microbial agents. In China, for example, there are currently no biopesticides registered for emergency use against FAW, despite potentially devastating Concluding remarks losses due to this highly invasive pest. Even if international biopesticidal products are available, In light of the vast damage potential and continuous smallholders, especially in regions newly invaded by spread of FAW throughout the world, and the known FAW, are often unwilling to buy these because of high adverse effects caused by pesticides, the development costs. In addition, farmers might also lack confidence of low-risk biologically based management in the reliablility of microbial pesticides, which they approaches for control of FAW is of utmost impor- think act slowly and give less crop protection. tance. This review showed that microbials might be Therefore, there is a growing need for international able to play an important role in this major task. collaboration in exchanging effective microbial However, for many of these microbials larger scale strains to facilitate management of this globally field testing is still required to verify their effective- important invasive species. It is finally suggested to ness for FAW control under field conditions. Because increase research efforts to study, e.g. the optimal sublethal effects of FAW caused by pathogenic combinations of biopesticides and conventional pes- microorganisms may occur, this aspect should also ticides, as well as to test innovative approaches such as be considered in the evaluation of effectiveness of improved formulations to make agents more effective biocontrol agents against FAW under field conditions. and protect them from detrimental environmental Furthermore, the different susceptibilities of FAW factors. Governments and international organizations populations from different geographical regions to also have an important role to play, e.g. by providing microbials, such as Bt, should be carefully considered knowledge and advice or subsidising biopesticides for in the development of pest control strategies (Mon- farmers. An example of the latter is Ghana where the nerat et al. 2006). government provided substantial amounts of Bt prod- Environmental factors like UV radiation and ucts to farmers after the recent invasion (Rwomushana intense heat might be detrimental to viability and et al. 2018). infectivity of microbial agents applied in the field (Raun et al. 1966). Therefore, when applying EPNs or Acknowledgements This research was supported by The EPFs on the maize crop, this should be done in the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202007) and China Agriculture Research early morning or late evening. Suggestions for an System (CARS-02). alternative approach is to isolate microbials from the extremely arid zone, such as the Atacama desert, and Compliance with ethical standards to evaluate their biological activity (Santiago et al. Conflict of interest The authors declare that they have no 2018). Another alternative is the use of specific conflict of interest. formulations, such as micro-encapsulation which may improve efficiency and tolerance of microbials Ethical approval This article does not contain any studies against adverse environmental effects (Barrera-Cubil- with human participants or animals performed by any of the authors. los et al. 2017). Additionally, innovative biotechnol- ogy methods may be used to enhance the efficacy of entomopathogens to manage pests (Karabo¨rklu¨ et al. 2018). In Lepidoptera, RNA interference (RNAi) technology has been used to knock down the

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Villamizar L, Arriero C, Cotes A (2004) Development of pre- between insect natural enemies and entomopathogenic fungi formulated producı´s based on iiomuraea rileyi for control and developing multiple natural enemies for biocontrol of of Spodoptera frugiperda (Lepidoptera: Moctuidae). Rev insect pests. Colomb Entomol 30:99–105 Viteri DM, Linares AM, Flores L (2018) Use of the ento- Feng Zhang is an entomology research scientist at MARA- mopathogenic nematode Steinernema carpocapsae in CABI Joint Laboratory for Bio-safety, Institute of Plant combination with low-toxicity insecticides to control fall Protection, Chinese Academy of Agricultural Sciences (IPP, armyworm (Lepidoptera: Noctuidae) larvae. Fla Entomol CAAS). His research focus on the biological control, chemical 101:327–330 ecology, plant–insect and insect-parasitoid interactions. Cur- Wraight SP, Ramos ME, Avery PB, Jaronski ST, Vandenberg rently, he works on the biological control and chemical ecology JD (2010) Comparative virulence of Beauveria bassiana of invasive insect pests such as fall armyworm and brow isolates against lepidopteran pests of vegetable crops. marmorated stink bug. J Invertebr Pathol 103:186–199 Yang F, Kerns DL, Brown S, Kurtz R, Dennehy T, Braxton B, Chaolong Huang is a master student at Institute of Plant Head G, Huang FN (2016) Performance and cross-crop Protection, Chinese Academy of Agricultural Sciences (IPP, resistance of Cry1F-maize selected Spodoptera frugiperda CAAS). His research focus on the biological control of fall on transgenic Bt cotton: implications for resistance man- armyworm. agement. Sci Rep 6:28059 ´ Zamora R, Markelyn J (2019) Caracterizacion de aislados Kanglai He is a professor of entomology at IPP, CAAS. His ´ nativos de nematodos entomopatogenos y uso potencial research focus on agricultural entomology and pest control, contra Spodoptera frugiperda. Diss Universidad Nacional especially on biology, ecology and biological control of maize Agraria. https://repositorio.una.edu.ni/3830/ insect pests. Zhang L, Jin MH, Zhang DD, Jiang YY, Liu J, Wu KM, Xiao YT (2019) Molecular identiﬁcation of invasive fall army- Dirk Babendreier is an experienced researcher at CABI worm Spodoptera frugiperda in Yunnan province. Chin Switzerland. His research focus on agricultural entomology Plant Prot 45:19–24 and integrated pest management, especially on biology, ecology and biological control of insect pests in a number of Jingfei Guo is an assistant professor of entomology at crops. Currently, he works on the biological control of fall Institute of Plant Protection, Chinese Academy of Agricultural armyworm. Sciences (IPP, CAAS). Her recent research focus on the biological control of fall armyworm. Zhenying Wang is a professor of entomology at IPP, CAAS. His research focus on agricultural entomology and pest control, Shengyong Wu is an associated professor of entomology at especially on biology, ecology and biological control of maize Institute of Plant Protection, Chinese Academy of Agricultural insect pests. Currently, he works on the biology, ecology and Sciences (IPP, CAAS). His research focus on the interactions biological control of fall armyworm.

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