Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-24T23:40:14.272Z Has data issue: false hasContentIssue false
  • English
  • Français

The green lacewing Chrysopa formosa as a potential biocontrol agent for managing Spodoptera frugiperda and Spodoptera litura

Published online by Cambridge University Press:  29 July 2022

Yu-Yan Li Open the ORCID record for Yu-Yan Li [Opens in a new window] ,
Ya-Nan Wang Open the ORCID record for Ya-Nan Wang [Opens in a new window] ,
Hong-Zhi Zhang Open the ORCID record for Hong-Zhi Zhang [Opens in a new window] ,
Mao-Sen Zhang Open the ORCID record for Mao-Sen Zhang [Opens in a new window] ,
Meng-Qing Wang ,
Jian-Jun Mao  and
Li-Sheng Zhang
Yu-Yan Li*
Affiliation:
Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China
Ya-Nan Wang
Affiliation:
Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China
Hong-Zhi Zhang
Affiliation:
Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China
Mao-Sen Zhang
Affiliation:
Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China
Meng-Qing Wang
Affiliation:
Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China
Jian-Jun Mao
Affiliation:
Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China
Li-Sheng Zhang*
Affiliation:
Key Laboratory of Natural Enemy Insects, Ministry of Agriculture and Rural Affairs, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R. China
*
Authors for correspondence: Yu-Yan Li, Email: liyuyan@caas.cn; Li-Sheng Zhang, Email: zhanglisheng@caas.cn
Authors for correspondence: Yu-Yan Li, Email: liyuyan@caas.cn; Li-Sheng Zhang, Email: zhanglisheng@caas.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Understanding predator–prey interactions is essential for successful pest management by using predators, especially for the suppression of novel invasive pest. The green lacewing Chrysopa formosa is a promising polyphagous predator that is widely used in the biocontrol of various pests in China, but information on the control efficiency of this predator against the seriously invasive pest Spodoptera frugiperda and native Spodoptera litura is limited. Here we evaluated the predation efficiency of C. formosa adults on eggs and first- to third-instar larvae of S. frugiperda and S. litura through functional response experiments and determined the consumption capacity and prey preference of this chrysopid. Adults of C. formosa had a high consumption of eggs and earlier instar larvae of both prey species, and displayed a type II functional response on all prey stages. Attack rates of the chrysopid on different prey stages were statistically similar, but the handling time increased notably as the prey developed. The highest predation efficiency and shortest-handling time were observed for C. formosa feeding on Spodoptera eggs, followed by the first-instar larvae. C. formosa exhibited a significant preference for S. litura over S. frugiperda in a two-prey system. In addition, we summarized the functional response and predation efficiency of several chrysopids against noctuid pests and made a comparison with the results obtained from C. formosa. These results indicate that C. formosa has potential as an agent for biological control of noctuid pests, particularly for the newly invasive pest S. frugiperda in China.

Keywords

Chrysopa formosafunctional responsepredation efficiencyprey preferenceSpodoptera
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 1 , February 2023 , pp. 49 - 62
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, M, Sayyed, AH, Saleem, MA and Ahmad, M (2008) Evidence for field evolved resistance to newer insecticides in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan. Crop Protection 27, 1367–1372.CrossRefGoogle Scholar
Ahmad, M, Ghaffar, A and Rafiq, M (2013) Host plants of leaf worm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in Pakistan. Asian Journal of Agriculture and Biology 1, 23–28.Google Scholar
Bale, JS, Van Lenteren, JC and Bigler, F (2008) Biological control and sustainable food production. Philosophical Transactions of the Royal Society B 363, 761–776.CrossRefGoogle ScholarPubMed
Barbosa, MFC, Poletti, M and Poletti, EC (2019) Functional response of Amblyseius tamatavensis Blommers (Mesostigmata: Phytoseiidae) to eggs of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) on five host plants. Biological Control 138, 104030.CrossRefGoogle Scholar
Canard, M, Séméria, Y and New, TR (1984) Biology of Chrysopidae. Netherlands: Springer.Google Scholar
Cao, WX, Zhang, T, Yang, H, Xu, ZQ, Gu, JJ and Chen, HX (2020) Evaluation of predatory function of Chrysopa pallens to larvae of fall armyworm Spodoptera frugiperda. Journal of Plant Protection 47, 839–844.Google Scholar
Chen, WB, Li, YY, Wang, MQ, Mao, JJ and Zhang, LS (2021) Evaluating the potential of using Spodoptera litura eggs for mass-rearing Telenomus remus, a promising egg parasitoid of Spodoptera frugiperda. Insects 12, 384.CrossRefGoogle Scholar
Cuthbert, RN, Dick, JTA, Callaghan, A and Dickey, JWE (2018) Biological control agent selection under environmental change using functional responses, abundances and fecundities; the relative control potential (RCP) metric. Biological Control 121, 50–57.CrossRefGoogle Scholar
Cuthbert, RN, Dickey, JWE, Coughlan, NE, Joyce, PWS and Dick, JTA (2019) The functional response ratio (FRR): advancing comparative metrics for predicting the ecological impacts of invasive alien species. Biological Invasions 21, 2543–2547.CrossRefGoogle Scholar
Dhir, BC, Mohapatra, HK and Senapati, B (1992) Assessment of crop loss in groundnut due to tobacco caterpillar, Spodoptera litura (F.). Indian Journal of Plant Protection 20, 215–217.Google Scholar
Early, R, Gonzalez-Moreno, P, Murphy, ST and Day, R (2018) Forecasting the global extent of invasion of the cereal pest Spodoptera frugiperda, the fall armyworm. NeoBiota 40, 25–50.CrossRefGoogle Scholar
EPPO (2015) PM 7/124 (1) Spodoptera littoralis, Spodoptera litura, Spodoptera frugiperda, Spodoptera eridania. EPPO Bulletin 45, 410–444.CrossRefGoogle Scholar
FAO (2020) The Global Action for Fall Armyworm Control: Action Framework 2020–2022. Working Together to Tame the Global Threat. Rome: FAO. Available at https://doi.org/10.4060/ca9252en.Google Scholar
Feng, Y, Zhou, ZX, An, MR, Yu, XL and Liu, TX (2018) The effects of prey distribution and digestion on functional response of Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control 124, 74–81.CrossRefGoogle Scholar
Ganjisaffar, F and Perring, TM (2015) Prey stage preference and functional response of the predatory mite Galendromus flumenis to Oligonychus pratensis. Biological Control 82, 40–45.CrossRefGoogle Scholar
Greene, GL, Leppla, NC and Dickerson, WA (1976) Velvetbean caterpillar: a rearing procedure and artificial medium. Journal of Economic Entomology 69, 487–488.CrossRefGoogle Scholar
Gupta, M, Tara, JS, Sharma, S and Bala, A (2015) Biology and morphometry of Spodoptera litura Fabricus, a serious defoliator of mango (Mangifera indica) in Jammu Region (J&K). Munis Entomology and Zoology Journal 10, 215–221.Google Scholar
Gutierrez-Moreno, R, Mota-Sanchez, D, Blanco, CA, Whalon, ME, Teran-Santofimio, H, Rodriguez-Maciel, JC and DiFonzo, C (2019) Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. Journal of Economic Entomology 112, 792–802.CrossRefGoogle ScholarPubMed
Hassanpour, M, Mohaghegh, J, Iranipour, S, Nouri-Ganbalani, G and Enkegaard, A (2011) Functional response of Chrysoperla carnea (Neuroptera: Chrysopidae) to Helicoverpa armigera (Lepidoptera: Noctuidae): effect of prey and predator stages. Insect Science 18, 217–224.CrossRefGoogle Scholar
Hassanpour, M, Maghami, R, Rafiee-Dastjerdi, H, Golizadeh, A, Yazdanian, M and Enkegaard, A (2015) Predation activity of Chrysoperla carnea (Neuroptera: Chrysopidae) upon Aphis fabae (Hemiptera: Aphididae): effect of different hunger levels. Journal of Asia-Pacific Entomology 18, 297–302.CrossRefGoogle Scholar
Hassell, MP (1978) The dynamics of arthopod predator–prey systems. Monographs in Population Biology 13, 1–237.Google Scholar
Hernández-Juárez, A, Aguirre-Uribe, LA, González-Ruíz, A, Chacón-Hernández, JC, Landeros-Flores, J, Cerna-Chávez, E, Flores-Dávila, M and Harris, MK (2015) Impact of endosulfan on the predatory efficiency of larval Chrysoperla carnea (Neuroptera: Chrysopidae) on the eggs of Heliothis virescens and Spodoptera frugiperda (Lepidoptera: Noctuidae). The Canadian Entomologist 148, 112–117.CrossRefGoogle Scholar
Holling, CS (1959) Some characteristics of simple types of predation and parasitism. The Canadian Entomologist 91, 385–398.CrossRefGoogle Scholar
Holling, CS (1965) The functional response of predators to prey density and its role in mimicry and population regulation. The Memoirs of the Entomological Society of Canada 97, 5–60.CrossRefGoogle Scholar
Hruska, AJ and Gould, F (1997) Fall armyworm (Lepidoptera: Noctuidae) and Diatraea lineolata (Lepidoptera: Pyralidae): impact of larval population level and temporal occurrence on maize yield in Nicaragua. Journal of Economic Entomology 90, 611–622.CrossRefGoogle Scholar
Huang, NX and Enkegaard, A (2010) Predation capacity and prey preference of Chrysoperla carnea on Pieris brassicae. BioControl 55, 379–385.CrossRefGoogle Scholar
Huang, H, Yan, JZ and Li, DQ (1990) Study on the predation of Chrysopa pallens (Rambur) to pest on cotton. Nature Enemies of Insects 12, 7–12.Google Scholar
Huang, HY, Liu, YN, Qi, YF, Xu, YY and Chen, ZZ (2020) Predatory responses of Chrysoperla sinica (Tjeder) larvae to Spodoptera frugiperda (J. E. Smith) eggs and larvae. Chinese Journal of Applied Entomology 57, 1333–1340.Google Scholar
Islam, Y, Shah, FM, Shah, MA, Musa Khan, M, Rasheed, MA, Ur Rehman, S, Ali, S and Zhou, X (2020) Temperature-dependent functional response of Harmonia axyridis (Coleoptera: Coccinellidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae) in laboratory. Insects 11, 583.CrossRefGoogle ScholarPubMed
Juliano, SA (2001) Nonlinear curve fitting: predation and functional response curves. In Cheiner, SM and Gurven, J (eds), Design and Analysis of Ecological Experiments, 2nd Edn. London: Chapman and Hall, pp. 178–196.Google Scholar
Kabissa, JCB, Yarro, JG, Kayumbo, HY and Juliano, SA (1996) Functional responses of two chrysopid predators feeding on Helicoverpa armigera (Lep.: Noctuidae) and Aphis gossypii (Hom.: Aphididae). Entomophaga 41, 141–151.CrossRefGoogle Scholar
Lai, Y and Liu, XY (2020) The natural enemy species of Chrysopidae from China and their applications in biological control: a review. Journal of Plant Protection 47, 1169–1187.Google Scholar
Lechowicz, MJ (1982) The sampling characteristics of electivity indices. Oecologia 52, 22–30.CrossRefGoogle ScholarPubMed
Lee, JH and Kang, TJ (2004) Functional response of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to Aphis gossypii Glover (Homoptera: Aphididae) in the laboratory. Biological Control 31, 306–310.CrossRefGoogle Scholar
Li, ZG, Zheng, JH, Ye, JW, Han, SC, Yan, Z and Chen, ZT (2010) Predation of the green lacewing Chrysopa formosa Brauer on the spiraling whitefly, Aleurodicus dispersus Russell. Journal of Environmental Entomology 32, 516–519.Google Scholar
Li, YY, Wang, MZ, Gao, F, Zhang, HZ, Chen, HY, Wang, MQ, Liu, CX and Zhang, LS (2018) Exploiting diapause and cold tolerance to enhance the use of the green lacewing Chrysopa formosa for biological control. Biological Control 127, 116–126.CrossRefGoogle Scholar
Li, P, Li, YY, Xiang, M, Wang, MQ, Mao, JJ, Chen, HY and Zhang, LS (2020) Predation capacity of Chrysopa pallens larvae to young larvae of Spodoptera frugiperda. Chinese Journal of Biological Control 36, 513–519.Google Scholar
Li, YY, Wang, MQ, Zhang, YY, Ma, M, Li, P, Mao, JJ, Chen, HY and Zhang, LS (2021) Predatory capacity of Chrysopa formosa on the eggs and young larvae of Spodoptera frugiperda. Plant Protection 47, 178–184.Google Scholar
McEwen, PK, New, TR and Whittington, AE (2010) Lacewings in the Crop Environment. Cambridge: Cambridge University Press.Google Scholar
Messelink, GJ, Vijverberg, R, Leman, A and Janssen, A (2016) Biological control of mealybugs with lacewing larvae is affected by the presence and type of supplemental prey. BioControl 61, 555–565.CrossRefGoogle Scholar
Montezano, DG, Specht, A, Sosa-Gomez, DR, Roque-Specht, VF, Sousa-Silva, JC, Paula-Moraes, SV, Peterson, JA and Hunt, TE (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology 26, 286–300.CrossRefGoogle Scholar
Mushtaq, T and Khan, AA (2010) Functional and aggregational response of Chrysoperla sp. (carnea-group) (Neuroptera: Chrysopidae) on Brevicoryne brassicae (Linnaeus) (Hemiptera: Aphididae). Journal of Biological Control 24, 28–34.Google Scholar
Nachappa, P, Braman, SK, Guillebeau, LP and All, JN (2006) Functional response of the tiger beetle Megacephala carolina carolina (Coleoptera: Carabidae) on twolined spittlebug (Hemiptera: Cercopidae) and fall armyworm (Lepidoptera: Noctuidae). Journal of Economic Entomology 99, 1583–1589.CrossRefGoogle ScholarPubMed
Nan, JK, Song, LW, Zuo, TT, Yang, LY, Wang, Y and Sun, SH (2019) Study on the predation effect of Chrysopa formosa Brauer and Harmonia axyridis Pallas on Hyphantria cunea (Drury). Journal of Shenyang Agricultural University 50, 161–166.Google Scholar
Noppe, C, Michaud, JP and De Clercq, P (2012) Intraguild predation between lady beetles and lacewings: outcomes and consequences vary with focal prey and arena of interaction. Annals of the Entomological Society of America 105, 562–571.CrossRefGoogle Scholar
Nordlund, DA and Morrison, RK (1990) Handling time, prey preference, and functional response for Chrysoperla rufilabris in the laboratory. Entomologia Experimentalis et Applicata 57, 237–242.CrossRefGoogle Scholar
Nunes, GS, Nascimento, IN, Souza, GMM, Oliveira, R, Oliveira, FQ and Batista, JL (2017) Biological aspects and predation behavior of Ceraeochrysa cubana against Spodoptera frugiperda. Revista Brasileira de Ciências Agrárias – Brazilian Journal of Agricultural Sciences 12, 20–25.CrossRefGoogle Scholar
Pan, MZ, Zhang, HP, Zhang, LS and Chen, HY (2019) Effects of starvation and prey availability on predation and dispersal of an omnivorous predator Arma chinensis Fallou. Journal of Insect Behavior 32, 134–144.CrossRefGoogle Scholar
Pappas, ML, Broufas, GD and Koveos, DS (2007) Effects of various prey species on development, survival and reproduction of the predatory lacewing Dichochrysa prasina (Neuroptera: Chrysopidae). Biological Control 43, 163–170.CrossRefGoogle Scholar
Pappas, ML, Broufas, GD and Koveos, DS (2011) Chrysopid predators and their role in biological control. Journal of Entomology 8, 301–326.CrossRefGoogle Scholar
Parajulee, MN, Shrestha, RB, Leser, JF, Wester, DB and Blanco, CA (2006) Evaluation of the functional response of selected arthropod predators on bollworm eggs in the laboratory and effect of temperature on their predation efficiency. Environmental Entomology 35, 379–386.CrossRefGoogle Scholar
Pogue, GM (2002) A World Revision of the Genus Spodoptera Guenée (Lepidoptera: Noctuidae). Philadelphia: American Entomological Society.Google Scholar
Qin, Z, Wu, J, Qiu, B, Ali, S and Cuthbertson, AGS (2019) The impact of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) on control of Dysmicoccus neobrevipes Beardsley (Hemiptera: Pseudococcidae). Insects 10, 131.CrossRefGoogle ScholarPubMed
Rao, GVR, Wightman, JA and Rao, DVR (1993) World review of the natural enemies and diseases of Spodoptera litura (F.) (Lepidoptera: Noctuidae). Insect Science and Its Application 14, 273–284.Google Scholar
Rogers, D (1972) Random search and insect population models. Journal of Animal Ecology 41, 369–383.CrossRefGoogle Scholar
Sattayawong, C, Uraichuen, S and Suasa-ard, W (2016) Larval preference and performance of the green lacewing, Plesiochrysa ramburi (Schneider) (Neuroptera: Chrysopidae) on three species of cassava mealybugs (Hemiptera: Pseudococcidae). Agriculture and Natural Resources 50, 460–464.CrossRefGoogle Scholar
Schenk, D and Bacher, S (2002) Functional response of a generalist insect predator to one of its prey species in the field. Journal of Animal Ecology 71, 524–531.CrossRefGoogle Scholar
Solomon, ME (1949) The natural control of animal populations. Journal of Animal Ecology 18, 1–35.CrossRefGoogle Scholar
Sparks, AN (1979) A review of the biology of the fall armyworm. The Florida Entomologist 62, 82–87.CrossRefGoogle Scholar
Stewart, CD, Braman, SK and Pendley, AF (2002) Functional response of the azalea plant bug (Heteroptera: Miridae) and a green lacewing Chrysoperla rufilabris (Neuroptera: Chrysopidae), two predators of the azalea lace bug (Heteroptera: Tingidae). Environmental Entomology 31, 1184–1190.CrossRefGoogle Scholar
Sultan, A and Khan, MF (2014) Functional response of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) to sugarcane whitefly Aleurolobus barodensis (Maskell) in laboratory conditions. Journal of Insect Behavior 27, 454–461.CrossRefGoogle Scholar
Tauber, MJ, Tauber, CA, Daane, KM and Hagen, KS (2000) Commercialization of predators: recent lessons from green lacewings (Neuroptera: Chrysopidae: Chrysoperla). American Entomologist 46, 26–38.CrossRefGoogle Scholar
Tavares, WS, Cruz, I, Silva, RB, Serrao, JE and Zanuncio, JC (2011) Prey consumption and development of Chrysoperla externa (Neuroptera: Chrysopidae) on Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs and larvae and Anagasta kuehniella (Lepidoptera: Pyralidae) eggs. Maydica 56, 283–289.Google Scholar
Tong, H, Su, Q, Zhou, X and Bai, L (2013) Field resistance of Spodoptera litura (Lepidoptera: Noctuidae) to organophosphates, pyrethroids, carbamates and four newer chemistry insecticides in Hunan, China. Journal of Pest Science 86, 599–609.CrossRefGoogle ScholarPubMed
Van Lenteren, JC (2011) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57, 1–20.CrossRefGoogle Scholar
Van Lenteren, JC, Hemerik, L, Lins, JC and Bueno, VH (2016) Functional responses of three neotropical mirid predators to eggs of Tuta absoluta on tomato. Insects 7, 34.CrossRefGoogle ScholarPubMed
Viteri Jumbo, LO, Teodoro, AV, Rego, AS, Haddi, K, Galvao, AS and de Oliveira, EE (2019) The lacewing Ceraeochrysa caligata as a potential biological agent for controlling the red palm mite Raoiella indica. PeerJ 7, e7123.CrossRefGoogle ScholarPubMed
Wan, J, Huang, C, Li, CY, Zhou, HX, Ren, YL, Li, ZY, Xing, LS, Zhang, B, Qiao, X, Liu, B, Liu, CH, Xi, Y, Liu, WX, Wang, WK, Qian, WQ, McKirdy, S and Wan, FH (2021) Biology, invasion and management of the agricultural invader: fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Integrative Agriculture 20, 646–663.CrossRefGoogle Scholar
Wang, YN, Li, P, He, WW, Zhang, MS, Wang, MQ, Zhang, LS and Li, YY (2022) Predation of the eggs and young larvae of Spodoptera litura by the third instar larvae of Chrysopa formosa. Chinese Journal of Biological Control 38, 1–9. doi: 10.16409/j.cnki.2095-039x.2021.11.009.Google Scholar
Xu, QX, Wang, S, Tian, RB, Wang, S, Zhang, F, Ma, J, Li, S and Di, N (2019) Study on the predation potential of Chrysopa pallens on Spodoptera frugiperda. Journal of Environmental Entomology 41, 754–759.Google Scholar
Yan, Z (2012) Biological Characteristic of Chrysopa formosa Brauer and It's Predation Efficiency on Dysmicoccus neobrevipes (Beardsley) (Master thesis). Hainan University, Hainan, China.Google Scholar
Yang, NW, Zang, LS, Wang, S, Guo, JY, Xu, HX, Zhang, F and Wan, FH (2014) Biological pest management by predators and parasitoids in the greenhouse vegetables in China. Biological Control 68, 92–102.CrossRefGoogle Scholar
Zanuncio, JC, da Silva, CA, de Lima, ER, Pereira, FF, Ramalho, FD and Serrao, JE (2008) Predation rate of Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae with and without defense by Podisus nigrispinus (Heteroptera: Pentatomidae). Brazilian Archives of Biology and Technology 51, 121–125.CrossRefGoogle Scholar
Zhou, HX, Yu, Y, Tan, XM, Chen, AD and Feng, JG (2014) Biological control of insect pests in apple orchards in China. Biological Control 68, 47–56.CrossRefGoogle Scholar
Ziaei Madbouni, MA, Samih, MA, Namvar, P and Biondi, A (2017) Temperature-dependent functional response of Nesidiocoris tenuis (Hemiptera: Miridae) to different densities of pupae of cotton whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). European Journal of Entomology 114, 325–331.CrossRefGoogle Scholar