WU Li-hong ,ZHOU Cao ,LONG Gui-yun ,YANG Xi-bin ,WEI Zhi-yan ,LIAO Ying-jiang ,YANG Hong,,HU Chao-xing,

1 Guizhou Provincial Key Laboratory for Agricultural Pest Management of the Mountainous Region,Institute of Entomology,Guizhou University,Guiyang 550025,P.R.China

2 College of Tobacco Science,Guizhou University,Guiyang 550025,P.R.China

3 Scientific Observing and Experimental Station of Crop Pests in Guiyang of Ministry of Agriculture and Rural Affairs,Guiyang 550025.P.R.China

Abstract The fall armyworm (FAW),Spodoptera frugiperda Smith (Lepidoptera:Noctuidae) is an important agricultural pest that invaded China in the middle of December 2018.As a polyphagous pest,FAW is identified as a serious threat to agricultural production and food security in China.Pepper (Capsicum annuum L.),tomato (Solanum lycopersicum Mill.) and eggplant(Solanum melongena L.) are three of dominant solanaceous vegetables of this country.To our knowledge,the effects of these plants on the performances of FAW have not been well studied.In this study we assessed the fitness of this pest to these three plants.Results showed that FAW can complete its life cycle when fed with tomato and pepper,but not on eggplant.The population parameters of FAW fed with maize (Zea mays L.) and the three solanaceous vegetables were compared using the age-stage,two-sex life table method.Developmental duration was significantly different in the larval stage,but not in the pupae stage.FAW fed with pepper had the longest pre-adult period (41.73 d) and the lightest pupal weight (0.1134 g); the survival rate was lower than FAW fed with tomato.Significant differences were observed in the mean fecundity of female,with the highest (943.95 eggs) laid by FAW fed with tomato.FAW had the shortest mean generation time (T),the highest intrinsic rate of increase (r) and finite rate of increase (λ) on maize,and the highest net reproductive rate (R0) on tomato.Overall,FAW fitness on the three solanaceous vegetables was:tomato＞pepper＞eggplant.This study provides the foundation for further assessment of FAW risk to solanaceous vegetables and for establishing corresponding control strategies in China.

Keywords:Spodoptera frugiperda,life table,adaptability,tomato,pepper,eggplant

1.Introduction

The fall armyworm (FAW),SpodopterafrugiperdaSmith(Lepidoptera:Noctuidae) is a polyphagous pest native to tropical and subtropical America (Sparks 1979; Todd and Pooleet al.1980; Martinelliet al.2006).In 2016,FAW invaded Nigeria,Ghana and other sub-Saharan African countries,causing 20–50% loss of maize production(Goergenet al.2016; Cocket al.2017).In 2018,the FAW occurred in India and five other Southeast Asian countries(Sharanabasappaet al.2018).In the middle of December 2018,the first batch of the FAW population migrated into China (Sunet al.2021),and thereafter it spread rapidly across 26 provinces (autonomous regions,municipalities)in the country (Jianget al.2019).

FAW has a wide range of hosts,strong migratory ability and high reproductive capacity,rendering it the ability of causing serious damage.The fall armyworm consists of two strains:the “corn-strain” which mainly damages maize,cotton and sorghum; and the “rice-strain” which mainly damages rice and various forage grass (Pashleyet al.1985;Pashley 1988; Dumaset al.2015).The FAW that invaded China is the “corn-strain” as identified by molecular detection(Zhanget al.2019).

Compared with the United States,China’s climatic conditions,cultivation patterns,farmers’ awareness,pesticide usage and other factors indicate that FAW can cause significant damage to many crops in China (Maet al.2019).As a polyphagous pest,when maize is absent or scarce,FAW can damage other vegetables which include many solanaceous crops,such as belladonna (AtropabeladonnaL.),angel’s-trumpet (BrugmansiacandidaPers),bell pepper (C.annuum),tobacco (NicotianatabacumL.),climbing nightshade (SolanumdulcamaraL.),tomato(SolanunlycopersicumMill),eggplant (S.melongena),sticky nightshade (SolanumsisymbriifoliumLam.) and potato (SolanumtuberosumL.) (Montezanoet al.2018).Among the solanaceous crops,tomato,pepper and eggplant are widely cultivated in China.According to statistical data of the Chinese vegetable industry,China’s pepper planting area in 2018 reached 2.133 million ha ranking the first among vegetable crops with an annual output value of about 250 billion CNY (Wanget al.2019).China is the country with the largest tomato planting area and the highest yield in the world,ranking first in the world in 2010 (Yuanet al.2016).According to FAO statistics,eggplant harvested area in China has increased yearly in recent 10 years.In 2018,China accounted for 63.13% of the world’s eggplant yield (FAO 2018).However,there lacks detailed assessments of FAW fitness to pepper,tomato,and eggplant in China.

In this study,we assessed FAW fitness to three important solanaceous vegetables (tomato,pepper and eggplant) in China; maize acted as the control.We used the age-stage,two-sex life table method (Chiet al.2020) to obtain the life table parameters of FAW and compare its fitness to the four tested plants.

2.Materials and methods

2.1.Insects

FAW individuals were collected from a maize field around Guizhou Academy of Agricultural Sciences on June 20,2019,and reared for four consecutive generations in the laboratory.Insects were kept in an artificial climate chamber((25±1)°C,(75±5)% RH and a photoperiod of 16 h L:8 h D).FAW larvae were reared individually in plastic cups (4 cm in height by 5.6 cm in diameter) and provided with fresh maize leaf seedlings daily until larval pupation.

2.2.Plants

Seeds of maizeZ.mays(Qiannuo 168; Guizhou Jiefeng Agricultural Seed Company,China),pepperC.annuum(Guiyan 13; Guizhou Lifeng Seed Industry Co.,Ltd.,China),tomatoS.lycopersicum(Jingang tomato; Guangzhou Huiyan Horticultural Seedling Co.,Ltd.,China) and eggplantS.melongena(Zilong 8; Xi’an Qinshu Agriculture Co.,Ltd.,China) were purchased from the market.The seeds were planted in flowerpots (19 cm in height by 22 cm in diameter) that were filled with soil collected from vegetable experimental base in Guizhou University.The plants were maintained in a greenhouse ((25±2)°C,(65±5)% RH and a photoperiod of 16 h L:8 h D).Leaves of maize,pepper,tomato and eggplant were cut at 25,65,60 and 62 d,respectively,for rearing FAW larva.

2.3.Larval feeding trials

The trials were performed from October to December at the Institute of Entomology,Guizhou University in Guizhou Province,China.The newly hatched neonates from egg mass were fed individually in plastic cups (4 cm in height by 5.6 cm in diameter) and provided daily with fresh seedling leaves of the four different tested plants (tomato,pepper,eggplant and maize) until pupation.We selected 87,72,74 and 50 newly hatched larvae feeding on maize,tomato,pepper and eggplant,respectively.Plastic cups with fresh leaves were changed daily to ensure sufficient food for larvae.The larval age and the number of deaths were recorded until pupation.Pupa was weighed on the 3rd day after pupation and placed individually in plastic cups (4 cm in height by 5.6 cm in diameter) until pupa emergence and then pupa duration was recorded.The pupae were mated(female:male=1:1) in 500-mL plastic cups bound with 120-mesh gauze and rubber bands.All adults were fed daily with 10% (v/v) honey water.FAW adults that mated successfully included 30 pairs that fed with maize,20 pairs that fed with tomato and only six pairs that fed with pepper.The pre-oviposition period,the number of eggs masses laid by each female daily was counted until the females died.Egg masses were individually transferred to plastic cups,and the number of neonates hatched from each egg mass was counted,adult survival rate was calculated until all adults died.All the FAW larvae and adults were placed in an artificial climate chamber with (25±1)°C temperature,(75±5)% RH and 16 h L:8 h D photoperiod.

2.4.Life table study

Raw data for the life table were recorded based on the age-stage,two-sex life table theory (Chi and Liu 1985; Chi 1988).Basic life table parameters were calculated in the computer program TWOSEX-MSChart (Chi and Su 2006;Chi 2016).In each treatment,we obtained the adult preoviposition period of the female adult (APOP),total preoviposition period (from egg to first oviposition) (TPOP),oviposition period (OP),age-stage-specific survival rate(sxj;xis age in days,jis stage),female age-stage-specific fecundity (fxj) (daily number of eggs produced by a female at agexand stagej),population age-specific survival rate(lx),population age-specific fecundity (mx),age-specific life expectancy (exj) and age-stage-specific reproductive values(vxj).Thesxj,fxj,lx,mx,lxmx,exjandvxjcurves were drawn using SigmaPlot 12.5.

The net reproductive rate (R0) was calculated as:The intrinsic rate of increase (r) was estimated according to the Euler-Lotka equation with age indexed from zero,as:

The finite rate of increase (λ) was calculated as:λ=er.

The mean generation time (T) was calculated as:

2.5.Statistical analysis

The life table parameters for the three host treatments were calculated using the bootstrap method with 100 000 resampled data for estimating the means and standard error (SE) of life table parameters.For diet treatments,differences in population parameters,development duration and reproductive values were estimated using the paired bootstrap test in the program of TWOSEX-MSChart (P＜0.05).

3.Results

3.1.Effect of different plants on FAW development and reproduction

The duration of each developmental stage for FAW fed with different tested plants are presented in Table 1.FAW completed whole life cycles on tomato,pepper and maize,but not on eggplant.FAW fed with eggplant were unable to develop to the pupal stage and almost all died at 4th instar larvae.Significant differences were recorded in the developmental duration of 1st instar larvae (F=284.74,df=279;P＜0.000),2nd instar larvae (F=60.63,df=263;P＜0.000),3rd instar larvae (F=35.94,df=236;P＜0.000),4th instar larvae (F=47.06,df=223;P＜0.000),5th instar larvae(F=38.82,df=206;P＜0.000),6th instar larvae (F=26.03,df=183;P＜0.000),larval stage (1st–6th instar) (F=366.93,df=162;P＜0.000),pre-adult (F=241.85,df=162;P＜0.000),adult (F=12.09,df=162;P＜0.000) and total longevity(F=31.97,df=215,P＜0.000) of FAW fed with the three different tested plants,but not in the pre-pupa and pupae stages.FAW developed significantly faster on maize than on tomato and pepper in each larvae stage from the 1st–6thinstars.The developmental duration of the pre-pupa and pupae stages was generally equivalent for FAW fed with maize,tomato and pepper.Overall,pre-adult development was the longest on pepper (41.73 d),which was longer than on maize (31.17 d) and tomato (37.93 d).The adult stage development duration was the longest on tomato (9.07 d),which was longer than on maize (7.50 d) and pepper(7.23 d).Pupal weight was significantly higher on tomato than on maize and pepper (F=166.27,df=224;P＜0.000).The pre-adult survival rate of FAW fed with maize was significantly higher than with tomato and pepper (F=139.17,df=142;P＜0.000).

Table 1 Development,total longevity and pupal weight of Spodoptera frugiperda fed with maize and three solanaceous vegetables

FAW fed with maize and the three solanaceous vegetables showed different longevity and fecundity (Table 2).Adult longevity (both female and male) (female,F=5.14,df=53;P=0.009; male,F=7.12,df=106;P＜0.001) was significantly longer on tomato than on maize and pepper.The APOP(F=17.05,df=55;P＜0.000) and TPOP (F=106.01,df=52;P＜0.000) durations of female FAW were shortest when fed with maize.No significant differences were seen in the OP.The mean fecundity (F=8.03,df=54;P＜0.001) of females on tomato was 944,which was significantly higher than that on pepper (522) and maize (515).

3.2.Effect of different plants on FAW survival rate and fecundity

The curves of the age-stage specific survival rate (sxj) of FAW on different tested plants (Fig.1) indicate that the probability of FAW survive to agexand develop to stagej.In the early stage,the survival rates of 2nd and 3rd instar larvae on pepper (0.9729 and 0.8783,respectively) were higher than on maize (0.8506 and 0.5517) or tomato (0.9444 and 0.7639).The survival rate of pupa was much higheron maize (0.9770) than on tomato (0.7917) and pepper(0.4054).

Table 2 Adult longevity and reproduction of Spodoptera frugiperda fed with maize and the three solanaceous vegetables

Fig.1 Effect of maize (A),tomato (B) and pepper (C) on agestage-specific survival rate (sxj) of Spodoptera frugiperda.L1,L2,L3,L4,L5 and L6 represent 1st,2nd,3rd,4th,5th and 6th instar larvae,respectively.

The daily fecundity (number of eggs) of female FAW at agexand stagejwas shown withfxjin Fig.2.Thelxexplained variations in the survival rate of FAW with age.Thelxandmxof FAW were shown in Fig.2.Thefxjof FAW fed with maize,tomato and pepper all increased initially before decreasing,and peaked on the 28th,33rd and 41st d,respectively (Fig.2).

Theexjis the length of time that an individual of agexand stagejis expected to live after agex(Fig.3).Theexjof all individuals decreased with increasing instar.FAW fed with tomato (43.02 d) had the longestexjthan maize (38.96 d)and pepper (36.18 d).

Thevxjof FAW represents the contribution of all individuals at agexand stagejto the future population(Fig.4).Generally,female adults that fed with tomato,pepper and maize exhibited increasingvxjand peaked when FAW began to produce eggs.The female adults that fed with tomato,maize and pepper reached their highest reproductive values on the 28th,33rd and 37th d,with value of 1717,698 and 672,respectively.

3.3.Effect of different plants on FAW population life table parameters

TheR0,r,λ,andTof FAW on different hosts were estimated using the bootstrap method,and are listed in Table 3.TheR0for FAW fed with tomato was calculated as 275.32 offspring per female,much higher than on maize (177.43 offspring per female) and pepper (35.26 offspring per female).Therandλfor FAW fed with three tested plants have the same order,from the highest to the lowest was maize (r=0.164 d–1,λ=1.179 d–1),tomato (r=0.147 d–1,λ=1.158 d–1) and pepper(r=0.081 d–1,λ=1.084 d–1) (P＜0.05).In addition,Twas significantly shorter for FAW fed with maize (31.62 d) than with tomato (38.22 d) and pepper (44.11 d).

4.Discussion

FAW is a polyphagous and migratory pest and its invasion poses a serious threat to the grain and industrial crop production in China.In this study,we evaluated the fitness of FAW to three important solanaceous vegetables (tomato,pepper,and eggplant) in China,with maize as the control,using the age-stage,two-sex life table method.This allowed us to evaluate whether tomato,pepper and eggplant are suitable tested plants for FAW larvae.Results showed that FAW can complete a whole life cycle on pepper and tomato,but not on eggplant.Based on the developmental duration,survival rate,fecundity and other population parameters,we found that fitness of FAW larvae to tomato was higher than that to maize.

The age-stage,two-sex life table can reflect differences in the development rate between individuals and provide description of the performance of insect populations under experimental conditions (Chi 1988; Akcaet al.2015; Tuanet al.2016).Generally,short development duration,high survival rate and large reproduction capacity of herbivorous insects are important indicators of high host adaptability(Moreauet al.2006).In this study,we found survival rate and developmental time of lab-reared FAW differed much when fed with three solanaceous crops.Survival rate of FAW on other solanaceous crops was also evaluated.For instance,Xuet al.(2019) observed that the survival rate of FAW was only 7% on tobacco.

Fig.2 Effect of maize (A),tomato (B) and pepper (C) on agespecific survival rate (lx),female age-stage-specific fecundity(fx10),age-specific fecundity (mx) and age-specific maternity(lxmx) of Spodoptera frugiperda.

Fig.3 Effect of maize (A),tomato (B) and pepper (C) on Spodoptera frugiperda age-stage-specific life expectancy (exj).L1,L2,L3,L4,L5 and L6 represent 1st,2nd,3rd,4th,5th and 6th instar larvae,respectively.

Fig.4 Effect of maize (A),tomato (B) and pepper (C) on agestage-specific reproductive value (vxj) of Spodoptera frugiperda.L1,L2,L3,L4,L5 and L6 represent 1st,2nd,3rd,4th,5th and 6th instar larvae,respectively.

Table 3 Population life table parameters of Spodoptera frugiperda on three tested plants

Differences in fecundity reveal the effect of different hosts on insect reproductive capacity.FAW fed with tomato laid significantly more eggs per female than that on maize and pepper.The mean fecundity of female was not significantly different between maize and pepper and was lower than the 1 500 eggs per female reported by Kebede and Shimaliset al.(2019).For this,one possible explanation is that tested plants do not meet the required nutritional composition for FAW and hence result in smaller individuals,decreased egg development and reduced fecundity (Carrière 1992).Further research is required to determine the egg hatching rate of the descendant generation of FAW on the three different solanaceous vegetables,especially on tomato.

TheR0,r,λ,andTare bio-parameter statistics that integrate insect growth and development,reproduction and survival changes and indicate the capacity for population growth in a specific environment (Liu 1986; Wuet al.2006).Therof FAW fed with tomato (0.147 d–1) was similar to maize (0.164 d–1),but significantly lower for pepper(0.081 d–1).FAW fed with pepper had a lower population increase capacity (R0,randλwas lower,butTwas longer)than tomato.These results suggested that tomato could be host for the growth and development of FAW.Status of pupal stage can,to some extent,reflect fitness of larvae to specific host or environment (Eduardoet al.2018).In our study,FAW fed with tomato had a significantly higher pupal weight (0.1929 g) than maize (0.1771 g) or pepper(0.1134 g),suggesting that FAW larvae fed with tomato had the best nutrition.

The fitness of pests to plants may be related to the ability of plants to resist insects.Rostamiet al.(2017) found great differences in both growth and population growth parameters ofTutaabsolutain different tomato varieties.The complex defense system in plants can produce strong resistance to insects and pests (Liet al.2019).Secondary metabolites-such as capsaicin,tannin and total phenols -in different pepper varieties are closely related to pest resistance (Jiaet al.2018).Further studies are needed to understand the mechanisms that affect FAW growth between the different tomato and pepper varieties.

Although “corn-strain” of FAW prefers to host of maize,when maize is insufficient or FAW population density is high,FAW may transfer to other solanaceous vegetables (Baet al.2020).In China,it is very common to intercrop maize with solanaceous vegetables.Thus,when FAW female lays egg masses on maize,their offspring will transfer damage to adjacent solanaceous vegetables fields,even though the early instar development of FAW occurs on maize,later instar are able to move to solanaceous vegetables fields after attacking maize.In addition,FAW damage to solanaceous vegetables in a maize-solanaceous crops intercropping system may be more serious than that in single cropping systems of solanaceous vegetables,according to observations of damage in a sugarcane–maize intercropping system (Taiet al.2019).Above factors will maximize the potential damage of FAW to other solanaceous crops.Further studies should monitor and assess FAW in the field to determine the method of prevention.

5.Conclusion

Our study analyzed how three solanaceous vegetables affect FAW growth,development and reproduction,with maize as the control.FAW could complete its life cycle on tomato and pepper,but no on eggplant.The order of FAW fitness to three solanaceous hosts was:tomato＞pepper＞eggplant.Overall,FAW may not be harmful to eggplant,but may damage tomato and pepper in China.Our study provides the basis for assessing FAW risk to solanaceous vegetables and for constructing corresponding control strategies in China.

Acknowledgements

The authors would like to thank Yuan Min,a graduate student majoring in plant protection at Guizhou University,for providing guidance on making figures.This work was supported by the Science and Technology Program of Guizhou Province,China ([2019]2412),and the Basic Research Program (Science and Technology) of Guizhou Province,China ([2020]1Z021).

Declaration of competing interest

The authors declare that they have no conflict of interest.