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Variation in egg mass scale thickness of three Spodoptera species and its effects on egg parasitoid performance

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Abstract

Egg batches of Spodoptera moths are protected by scales deposited by females around and/or over eggs as a physical defense. These scales may affect the parasitism of some parasitoids, rendering biocontrol of Spodoptera eggs ineffective. In this study, we investigated the daily oviposition pattern of moths and the dynamics of egg mass scales of three Spodoptera species and examined the fitnesses of three potential egg parasitoid species to different egg mass scale thicknesses. The observations revealed that the three Spodoptera species share similar scale dynamics. From initial oviposition, S. exigua egg batches maintained a relatively high level of scale thickness (> 134.7 μm) for 2 days and S. frugiperda and S. litura for 3 days (> 105.9 μm, > 161.2 μm, respectively). During this period, the scales effectively hindered parasitism by Trichogramma species (parasitized 0.4%–14.9% eggs). Thereafter, the thickness of the scales decreased daily. The scales of the three Spodoptera species were all relatively thin (< 20.0 μm) after oviposition for 8 days, and subsequently, Trichogramma parasitized eggs more actively (parasitized up to 33.4%–36.5% eggs). Relatively, Trichogramma dendrolimi on S. frugiperda eggs, and Trichogramma chilonis on S. exigua eggs had higher parasitism. Meanwhile, Telenomus remus maintained a very stable and better performance than Trichogramma on Spodoptera species eggs with different scale thicknesses (parasitized 100% egg masses and 46.2%–60.0% eggs), which demonstrated its excellent potential as a Spodoptera species biocontrol agent. The findings elucidate the effect of egg mass scale thickness on effective parasitism by these egg parasitoid species and provide baseline information for the mixed use of Te. remus and Trichogramma against Spodoptera species.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

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References

  • Abell KJ, Duan JJ, Bauer L et al (2012) The effect of bark thickness on host partitioning between Tetrastichus planipennisi (Hymen: Eulophidae) and Atanycolus spp. (Hymen: Braconidae), two parasitoids of emerald ash borer (Coleop: Buprestidae). Biol Control 63:320–325

    Article  Google Scholar 

  • Aminudin A, Ito F, Tita W, Agrintya KM, Hirzi IR, & Yogo S. (2022) Impact of the fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) invasion on maize and the native Spodoptera litura (Fabricius) in East Java Indonesia and evaluation of the virulence of some indigenous entomopathogenic fungus isolates for controlling the pest. Egypt J Biol Pest Co, 32 1 48.

  • Anand R, Prasad B, Tiwary BN (2009) Relative susceptibility of Spodoptera litura pupae to selected entomopathogenic fungi. Biocontrol 54:85–92

    Article  Google Scholar 

  • Awasthi A, Avasthi S (2018) Larvicidal activity of Kasaundi (Cassia occidentalis) against fruit borer Heliothis armigera and Spodoptera litura on tomato. Int J Entomol Res 3:89–91

    Google Scholar 

  • Azidah A, Sofian-Azirun M (2006) Some aspects on oviposition behaviour of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). J Entomol 3:241–247

    Article  Google Scholar 

  • Carneiro TR, Fernandes OA (2012) Interspecific interaction between Telenomus remus (Hymenoptera: Platygastridae) and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) on Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs. An Acad Bras Ciênc 84:1127–1135

    Article  PubMed  Google Scholar 

  • Cave RD (2000) Biology, ecology and use in pest management of Telenomus remus. Biocontrol News Inf 21:21N-26N

    Google Scholar 

  • Chen W, Li Y, Wang M et al (2019a) Natural enemy insect resources of the Fall Armyworm Spodoptera frugiperda, their application status, and existing problems and suggestions. Chin J Biol Control 35:658–673

    Google Scholar 

  • Chen W, Li Y, Wang M et al (2019b) Entomopathogen resources of the fall armyworm Spodoptera frugiperda, and their application status. Plant Prot 45:1–9

    Google Scholar 

  • Chen W, Li Y, Wang M et al (2021) Evaluating the potential of using Spodoptera litura eggs for mass-rearing Telenomus remus, a promising egg parasitoid of Spodoptera frugiperda. InSects 12:384

    Article  PubMed  PubMed Central  Google Scholar 

  • Colmenarez YC, Babendreier D, Ferrer Wurst FR, Vásquez-Freytez CL, de Freitas BA (2022) The use of Telenomus remus (Nixon, 1937) (Hymenoptera: Scelionidae) in the management of Spodoptera spp.: potential, challenges and major benefits. CABI a&b 3:1–13

    Google Scholar 

  • Damalas CA, Eleftherohorinos IG (2011) Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res Public Health 8:1402–1419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  PubMed  Google Scholar 

  • Dong H, Zhu K, Zhao Q et al (2021) Morphological defense of the egg mass of Spodoptera frugiperda (Lepidoptera: Noctuidae) affects parasitic capacity and alters behaviors of egg parasitoid wasps. J Asia-Pac Entomol 24:671–678

    Article  Google Scholar 

  • Fukuda T, Wakamura S, Arakaki N, Yamagishi K (2007) Parasitism, development and adult longevity of the egg parasitoid Telenomus nawai (Hymenoptera: Scelionidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae). Bull Entomol Res 97:185–190

    Article  CAS  PubMed  Google Scholar 

  • Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273

    Article  Google Scholar 

  • Hafeez M, Ullah F, Musa Khan M, Li X, Zhang Z, Shah S, Imran M, Assiri MA, Fernández-Grandon GM, Desneux N, Rehman M, Fahad S, Lu Y (2022) Metabolic-based insecticide resistance mechanism and ecofriendly approaches for controlling of beet armyworm Spodoptera exigua: a review. Environ Sci Pollut Res 29:1746–1762

    Article  CAS  Google Scholar 

  • Hassan SA, Liscsinszky H, Zhang G (2004) The oak-silkworm egg Antheraea pernyi (Lepidoptera: Anthelidae) as a mass rearing host for parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae). Biocontrol Sci Technol 14:269–279

    Article  Google Scholar 

  • Hilliou F, Chertemps T, Maïbèche M, Le Goff G (2021) Resistance in the genus Spodoptera: Key insect detoxification genes. InSects 12:544

    Article  PubMed  PubMed Central  Google Scholar 

  • Hou YY, Ma Y, Xu W, Desneux N, Nkunika POY et al (2022) Spodoptera frugiperda egg mass scale thickness modulates Trichogramma parasitoid performance. Entomol Gen 42:589–596

    Article  Google Scholar 

  • Huang N, Jaworski CC, Desneux N, Zhang F, Yang P, Wang S (2020) Long-term and large-scale releases of Trichogramma promote pesticide decrease in maize in northeastern China. Entomol Gen 40:331–335

    Article  Google Scholar 

  • Huo L, Zhou J, Ning S et al (2019) Biological characteristics of Telenomus remus against Spodoptera frugiperda and Spodoptera litura eggs. Plant Prot 45:60–64

    Google Scholar 

  • Huo L, Wang M, Ning S et al (2020) Effect of egg masses scale layer on the parasitic efficacy of Telenomus remus against Spodoptera frugiperda and Spodoptera litura. Plant Prot 46(59–62):68

    Google Scholar 

  • Jiang X, Luo L, Hu Y (1999) Influence of larval diets on development, fecundity and flight capacity of the beet armyworm, Spodoptera exigua. Acta Entomol Sin 42:270–276

    Google Scholar 

  • Jung CR, Park YJ, Boo KS (2003) Optimal sex pheromone composition for monitoring Spodoptera exigua (Lepidoptera: Noctuidae) in Korea. J Asia-Pac Entomol 6:175–182

    Article  Google Scholar 

  • Kasige R, Dangalle C, Pallewatta N, Perera M (2022) Egg cluster characteristics of fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidea) in Sri Lanka under laboratory conditions. J Agric Sci Lanka 17:200–210. https://doi.org/10.4038/jas.v17i1.9620

    Article  Google Scholar 

  • Kenis M, Du Plessis H, Van den Berg J et al (2019) Telenomus remus, a candidate parasitoid for the biological control of Spodoptera frugiperda in Africa, is already present on the continent. InSects 10:92

    Article  PubMed  PubMed Central  Google Scholar 

  • Kenis M, Benelli G, Biondi A, Calatayud PA, Day R et al (2022) Invasiveness biology ecology and management of the fall armyworm Spodoptera frugiperda. Entomol Gen. https://doi.org/10.1127/entomologia/2022/1659

    Article  Google Scholar 

  • Li H, Han X, Zhao Y (2017) Potential use of Beauveria bassiana in combination with Scleroderma guani for improved control of Apriona germari. Can J for Res 47:10–15

    Article  Google Scholar 

  • Pizzol J, Pintureau B, Khoualdia O, Desneux N (2010) Temperature-dependent differences in biological traits between two strains of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). J Pest Sci 83:447–452

    Article  Google Scholar 

  • Pomari AF, Bueno ADF, De Freitas Bueno RCO, Junior DOM, A, (2012) Biological characteristics and thermal requirements of the biological control agent Telenomus remus (Hymenoptera: Platygastridae) reared on eggs of different species of the genus Spodoptera (Lepidoptera: Noctuidae). Ann Entomol Soc Am 105:73–81

    Article  Google Scholar 

  • Powell J, Common I (1985) Oviposition patterns and egg characteristics of Australian Tortricine moths (Lepidoptera: Tortricidae). Aust J Zool 33:179–216

    Article  Google Scholar 

  • Pozebon H, Marques RP, Padilha G, O’Neal M, Valmobida I, Bevilaqua JG et al (2020) Arthropod invasions versus soybean production in Brazil: a review. J Econ Entomol 113:1591–1608

    Article  CAS  PubMed  Google Scholar 

  • Queiroz A, de Bueno A, F, Pomari-Fernandes A, et al (2017a) Low temperature storage of Telenomus remus (Nixon)(Hymenoptera: Platygastridae) and its factitious host Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). Neotrop Entomol 46:182–192

    Article  CAS  PubMed  Google Scholar 

  • Queiroz A, de Freitas BA, Pomari-Fernandes A et al (2017b) Quality control of Telenomus remus (Hymenoptera: Platygastridae) reared on the factitious host Corcyra cephalonica (Lepidoptera: Pyralidae) for successive generations. Bull Entomol Res 107:791–798

    Article  CAS  PubMed  Google Scholar 

  • Salazar-Mendoza P, Rodriguez-Saona C, Aparecido Fernandes O (2020) Release density, dispersal capacity, and optimal rearing conditions for Telenomus remus, an egg parasitoid of Spodoptera frugiperda, in maize. Biocontrol Sci Technol 30:1040–1059

    Article  Google Scholar 

  • Schwenke RA, Lazzaro BP, Wolfner MF (2016) Reproduction–immunity trade-offs in insects. Annu Rev Entomol 61:239

    Article  CAS  PubMed  Google Scholar 

  • Sparks TC, Crossthwaite AJ, Nauen R et al (2020) Insecticides, biologics and nematicides: Updates to IRAC’s mode of action classification-a tool for resistance management. Pestic Biochem Physiol 167:104587

    Article  CAS  PubMed  Google Scholar 

  • Stouthamer R, Hu J, van Kan FJ et al (1999) The utility of internally transcribed spacer 2 DNA sequences of the nuclear ribosomal gene for distinguishing sibling species of Trichogramma. Biocontrol 43:421–440

    Article  Google Scholar 

  • Sun J-W, Dai P, Xu W et al (2020) Parasitism and suitability of Spodoptera frugiperda (Smith) eggs for four local Trichogramma species of northeastern China. J Environ Entomol 42:36–41

    Google Scholar 

  • Tang Q, Zhang C (2013) Data Processing System (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci 20:254–260

    Article  PubMed  Google Scholar 

  • Tian J, Lu Y, Wang G et al (2020) The Parasitic Capability of Five Trichogramma Species on Eggs of Fall Armyworm Spodoptera frugiperda. Chin J Biol Control 36:485–490

    Google Scholar 

  • Tsankov G (1990) Egg parasitoids of the pine processionary moth, Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Thaumetopeidae) in Bulgaria: Species, importance, biology and behaviour 1. J Appl Entomol 110:7–13

    Article  Google Scholar 

  • Wang X, Jennings DE, Duan JJ (2015) Trade-offs in parasitism efficiency and brood size mediate parasitoid coexistence, with implications for biological control of the invasive emerald ash borer. J Appl Ecol 52:1255–1263

    Article  Google Scholar 

  • Wang Y, Zou ZP, Hou YY, Yang XB, Wang S et al (2020) Manually-extracted unfertilized eggs of Chinese oak silkworm, Antheraea pernyi, enhance mass production of Trichogramma parasitoids. Entomol Gen 40:397–406

    Article  Google Scholar 

  • Wang P, Li MJ, Bai QR et al (2021) Performance of Trichogramma japonicum as a vector of Beauveria bassiana for parasitizing eggs of rice striped stem borer, Chilo suppressalis. Entomol Gen 41:147–155

    Article  Google Scholar 

  • Weinberg J, Ota N, Goergen G, Fagbohoun JR, Tepa-Yotto GT, Kriticos DJ (2022) Spodoptera eridania: Current and emerging crop threats from another invasive, pesticide-resistant moth. Entomol Gen. https://doi.org/10.1127/entomologia/2022/1397

    Article  Google Scholar 

  • Xie L, He Z, Long X et al (2022) Investigation of two egg parasitoid species of Spodoptera frugiperda in fields. Plant Prot 48:265–271

    Google Scholar 

  • Yang J, Cai P, Chen J et al (2018) Interspecific competition between Fopius arisanus and Psyttalia incisi (Hymenoptera: Braconidae), parasitoids of Bactrocera dorsalis (Diptera: Tephritidae). Biol Control 121:183–189

    Article  Google Scholar 

  • Yuan X, Deng W-L, Guo Y et al (2022) Evaluation of parasitism on eggs of Spodoptera frugiperda (J.E. Smith) by Trichogramma chilonis. J Environ Entomol 44:290–296

    Google Scholar 

  • Zang L-S, Wang S, Zhang F, Desneux N (2021) Biological control with Trichogramma in China: history, present status and perspectives. Annu Rev Entomol 66:463–484

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Zhang X, Zang LS, Du WM, Hou YY et al (2018) Advantages of diapause in Trichogramma dendrolimi mass production via eggs of the Chinese silkworm, Antheraea pernyi. Pest Manag Sci 74:959–965

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Wang HC, Du WM, Zang LS, Ruan CC et al (2021) Multi-parasitism: a promising approach to simultaneously produce Trichogramma chilonis and T. dendrolimi on eggs of Antheraea pernyi. Entomol Gen 41:627–636

    Article  Google Scholar 

  • Zheng X-L, Wang P, Lei C-L et al (2013) Effect of soil moisture on overwintering pupae in Spodoptera exigua (Lepidoptera: Noctuidae). Appl Entomol Zool 48:365–371

    Article  Google Scholar 

  • Zhou S, Lu X, Zhang G et al (2014) Research on the induction and termination of diapause in Trichogramma dendrolimi. Chin J Appl Entomol 51:45–52

    Google Scholar 

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Funding

This research was funded by the National Natural Science Foundation of China (32172469), and Program of Introducing Talents to Chinese Universities (111 Program, D20023).

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Correspondence to Lian-Sheng Zang.

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The authors declare no conflict of interest. Nicola Desneux serves as Editor-in-Chief of Journal of Pest Science and was not involved in the review process and decisions related to this manuscript.

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Li, TH., Ma, Y., Hou, YY. et al. Variation in egg mass scale thickness of three Spodoptera species and its effects on egg parasitoid performance. J Pest Sci 96, 1393–1402 (2023). https://doi.org/10.1007/s10340-023-01608-6

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