Abstract
The age of Trichogramma parasitoids could influence biological traits which are of great importance for effectiveness of mass rearing systems. Recent studies demonstrated that Trichogramma ostriniae (TO) could parasitize Antheraea pernyi eggs through multiparasitism along with other Trichogramma species, although few adults could emerge successfully. It is important to characterize the factors modulating the performance of TO on A. pernyi eggs, notably in order to try enhancing its quantitative emergence through multiparasitism for further use in biological control. In this context, irrespective of host age, we tested different ages of TO females (from 0.5-day- to 6-day-old postemergence) in multiparasitism with Trichogramma chilonis (TC) on A. pernyi eggs. The results of the present study confirmed that TO parasitism on A. pernyi eggs was largely age dependent. Higher percentage of multiparasitism and higher number of emerged TO adults were recorded in the treatment where 3-day-old TO females were used for parasitization with TC on A. pernyi host. In addition, we also tested different female ratios of both Trichogramma species to find out an optimal ratio for use in mass production. The highest percentage of multiparasitism, emergence and optimum emerged number of TO (per A. pernyi egg) was observed with the ratio 3:2 (TO:TC) per 1 host egg. This study demonstrated that the age of TO females can significantly affect their performance in multiparasitism of large A. pernyi eggs. These results prompt for more research in order to develop an effective multiparasitism-based production of TO at the industrial scale.
Similar content being viewed by others
References
Ayvaz A, Karasu E, Karaborklu S, Tuncbilek AS (2008) Effect of cold storage, rearing temperature, parasitoid age and irradiation on the performance of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). J Stored Prod Res 44:232–240
Barnay O, Pizzol J, Gertz C, Kienlen JC, Hommay G, Lapchin L (1999) Host density dependence of discovery and exploitation rates of egg patches of Lobesia botrana (Lepidoptera: Tortricidae) and Ephestia kuehniella (Lepidoptera: Pyralidae) by the parasitoid Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). J Econ Entomol 92:1311–1320
Biondi A, Desneux N, Amiens-Desneux E, Siscaro G, Zappalà L (2013) Biology and Developmental Strategies of the Palaearctic Parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the Neotropical Moth Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 106:1638–1647
Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread and management of the invasive South American tomato pinworm, Tuta absoluta: past, present and future. Annu Rev Entomol 63:239–258
Cabello T, Gamez M, Torres A, Garay J (2011) Possible effects of inter-specific competition on the coexistence of two parasitoid species: Trichogramma brassicae Bezdenko and Chelonus oculator (F.) (Hymenoptera: Trichogrammatidae, Braconidae). Community Ecol 12:78–88
Chailleux A, Biondi A, Han P, Tabone E, Desneux N (2013) Suitability of the pest-plant system Tuta absoluta (Lepidoptera: Gelechiidae)—tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. Econ Entomol 106:2310–2321
Chen KW, Liu HZ, He YR (2005) The relationship between fecundity and female age of Trichogramma ostriniae Pang et Chen. Acta Entomol Sin 48:712–717
Cusumano A, Peri E, Vinson SB, Colazza S (2012) Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids. Biocontrol 57:719–734
Cusumano A, Peri E, Colazza S (2016) Interspecific competition/facilitation among insect parasitoids. Curr Opin Insect Sci 14:12–16
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Desneux N, Barta RJ, Delebecque CJ, Heimpel GE (2009) Transient host paralysis as a means of reducing self-superparasitism in koinobiont endoparasitoids. J Insect Physiol 55:321–327
Du WM, Xu J, Hou YY, Lin Y, Zang LS, Yang X, Zhang JJ, Ruan CC, Desneux N (2017) Trichogramma parasitoids can distinguish between fertilized and unfertilized host eggs. J Pest Sci 91:771–780
Fleury F, Bouletreau M (1993) Effect of temporary host deprivation on reproductive potential of Trichogramma brassicae. Entomol Exp Appl 68:203–210
Garcia P, Wajnberg E, Oliveira L, Tavares J (2001) Is the parasitization capacity of Trichogramma cordubensis influenced by the age females? Entomol Exp Appl 98:219–224
Gardner F, Wright MG, Kuhar TP, Pitcher SA, Hoffmann MP (2012) Dispersal of Trichogramma ostriniae in field corn. Biocontrol Sci Technol 22:1221–1233
Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Chichester
Guo XJ, Di N, Chen X, Zhu Z, Zhang F, Tang B et al (2019) Performance of Trichogramma pintoi when parasitizing eggs of the oriental fruit moth Grapholita molesta. Entomol Gen 39:239–249
Han SC, Chen QX, Liu WH, Zhang ML (1993) Studies on interspecific competition between Anastatus japonicus and Trichogramma dendrolimi on host eggs. Nat Enem Insect 15:10–13
Harvey JA, Gols R, Strand MR (2009) Intrinsic competition and its effects on the survival and development of three species of endoparasitoid wasps. Entomol Exp Appl 130:238–248
Harvey JA, Poelman EH, Tanaka T (2013) Intrinsic inter- and intraspecific competition in parasitoid wasps. Annu Rev Entomol 58:333–351
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
Hegazi EM, Khafagi WE (2001) Pattern of Egg Management by Trichogramma cacoeciae and T. dendrolimi (Hymenoptera: Trichogrammatidae). Biocontrol Sci Technol 11:353–359
Hohmann CL, Luck RF (2004) Effect of host availability and egg load in Trichogramma platneri Nagarkatti (Hymenoptera: Trichogrammatidae) and its consequences on progeny quality. Braz Arch Biol Technol 47:413–422
Hou YY, Yang XB, Zang LS, Zhang C, Lucie M, Nicolas D (2018) Effect of oriental armyworm Mythimna separata egg age on the parasitism and host suitability for five Trichogramma species. J Pest Sci 91:1181–1189
Huang SS, Zang LS, Ruan CC (2013) Parasitization ecology, mass production, and application of Trichogramma. Science Press, Beijing, pp 116–140
Huang J, Hua HQ, Wang LY, Zhang F, Li YX (2017) Number of attacks by Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) affects the successful parasitism of Ostrinia furnacalis (Lepidoptera: Crambidae) eggs. Bull Entomol Res 107:812–819
Iqbal A, Chen YM, Hou YY, Zhang L, Desneux N, Zang LS (2019) Factitious host species outcome of multiparasitism between egg parasitoids. J Pest Sci 92:1261–1269
Jervis MA, Kidd NAC (1996) Parasitoid adult feeding ecology and biocontrol. A review. Biocontrol News Inf 16:11–26
Jervis MA, Heimpel GE, Ferns PN, Harvey JA, Kidd NA (2001) Life-history strategies in parasitoid wasps: a comparative analysis of ‘ovigeny’. J Anim Ecol 70:442–458
Keinan Y, Kishinevsky M, Segoli M, Keasar T (2012) Repeated probing of hosts: an important component of superparasitism. Behav Ecol 23:1263–1268
Khanzada MS, Wang S, Huang NX, Pang H, Tan XL, Khanzada SR, (2019) Optimization of microencapsulated artificial diets for mass rearing of the predacious big eyed bug, Geocoris pallidipennis. Entomol Gen 39:353–363
Klomp H, Teerink B, Wei CM (1980) Discrimination between parasitized and unparasitized hosts in the egg parasite Trichogramma embryophagum (Hym.: Trichogrammatidae): a matter of learning and forgetting. Neth J Zool 30:254–277
Kogan M (1998) Integrated Pest Management: historical perspectives and contemporary developments. Annu Rev Entomol 43:243–270
Li TH, Tian CY, Zang LS, Hou YY, Ruan CC, Yang XB, Lucie M, Desneux N (2018) Multiparasitism with Trichogramma dendrolimi on egg of Chinese oak silkworm, Antheraea pernyi, enhances emergence of Trichogramma ostriniae. J Pest Sci 92:707–713
Li XY, Lei Q, Hua HQ, Song HF, Wang Su et al (2019) Impact of host suitability on oviposition preference toward fertilized and unfertilized host eggs in two Trichogramma parasitoid species. Entomol Gen 39:313–323
Liu SS, Zhang GM, Zhang F (1998) Factors influencing parasitism of Trichogramma dendrolimi on eggs of the Asian corn borer, Ostrinia furnacalis. Biocontrol 43:273–287
Liu ZC, Liu JF, Zhang F, Li DS, Feng XX (2000) Production and field application techniques of Trichogramma. Golden Shield Press, Beijing
Magdaraog PM, Harvey JA, Tanaka T, Gols R (2012) Intrinsic competition among solitary and gregarious endoparasitoid wasps and the phenomenon of ‘resource sharing’. Ecol Entomol 37:65–74
Makee H (2005) Effects of repeated and delayed exposure to codling moth eggs on reproduction of Trichogramma cacoeciae and Trichogramma principium (Hymenoptera: Trichogrammatidae) females. J Pest Sci 78:83–89
Mandour NS, Mahmoud MF, Osman MAN, Qiu B (2008) Efficiency, intrinsic competition and interspecific host discrimination of Copidosoma desantisi and Trichogramma evanescens, two parasitoids of Phthorimaea operculella. Biocontrol Sci Technol 18:903–912
Mohammed AAH, Desneux N, Fan YJ, Han P, Ali A, Song DL, Gao XW (2018) Impact of imidacloprid and natural enemies on cereal aphids: integration or ecosystem service disruption? Entomol Gen 37:47–61
Morais WCC, Plata-Rueda A, Martínez LC, Zanuncio AJV, Fernandes FL et al (2019) Potential of Diaphania hyalinata and Tenebrio molitor as alternative host for mass rearing of Palmistichus elaeisis (Hymenoptera: Eulophidae). Entomol Gen 39:285–294
Papaj DR (2000) Ovarian dynamics and host use. Annu Rev Entomol 45:423–448
Picciau L, Alma A, Ferracini C (2019) Effect of different feeding sources on lifespan and fecundity in the biocontrol agent Torymus sinensis. Biol Control 134:45–52
Pinto JD (1992) Novel taxa of Trichogramma from the New World tropics and Australia (Hymenoptera: Trichogrammatidae). J N Y Entomol Soc 100:621–633
Pizzol J, Desneux N, Wajnberg E, Thiéry D (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J Pest Sci 85:489–496
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
Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399
Reznik SY, Voinovich ND, Umarova TY (2001) Comparative behavioral analysis of ovipositing females and females with egg retention in Trichogramma principium Sug. et Sor. (Hymenoptera, Trichogrammatidae). Entomol Rev 81:895–903
SAS Institute (2010) SAS/STAT v.9.1. SAS Institute, Cary, NC, USA
Shi ZH, Liu SS (2003) Interspecific interactions between Cotesia plutellae and Oomyzus sokolowskii, two major parasitoids of diamondback moth, Plutella xylostella. Chin J Appl Ecol 14:949–954
Smith SM (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41:375–406
Stouthamer R, Hu J, van Kan FJPM, Platner GR, Pinto JD (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
Suarez L, Biancheri MJB, Sanchez G, Murua F, Funes CF et al (2019) Effects of releasing two Diachasmimorpha longicaudata population lines for the control of Ceratitis capitata infesting three key host fruit species. Biol Control 133:58–65
Tabone T, Bardon C, Desneux N, Wajnberg E (2010) Comparative assessment of parasitism of different Trichogramma spp. on Plutella xylostella L. on greenhouse cauliflower. J Pest Sci 83:251–256
Thiery D, Desneux N (2018) Host plants of the polyphagous grapevine moth Lobesia botrana during larval stage modulate moth egg quality and subsequent parasitism by the parasitoid Trichogramma cacoeciae. Entomol Gen 38:47–59
Velzen EV, Vila SP, Etienne RS (2016) The role of within-host competition for coexistence in multiparasitoid-host systems. Am Nat 87:48–59
Volkoff AN, Daumal J (1994) Ovarian cycle in immature and adult stages of Trichogramma cacoeciae and Trichogramma brassicae (Hym., Trichogrammatidae). Entomophaga 39:303–312
Wang CL, Zhang J, Huo ST (1998) Study, reproduction and utilization of Trichogramma. In: Bao JZ, Gu DX (eds) Biological control in China. Shanxi Science and Technology Press, Taiyuan, pp 67–123
Wang ZY, Lu X, He KL, Zhou DR (2000) Review of history, present situation and prospect of the Asian maize borer research in China. J Shenyang Agric Univ 31:402–412
Wang ZY, He KL, Yan S (2005) Large-scale augmentative biological control of Asian corn borer using Trichogramma in China: a success story. In: Conference paper: second international symposium on biological control of arthropods, Davos, Switzerland, pp 487–494
Wang ZY, He KL, Zhang F, Lu X, Babendreier D (2014) Mass rearing and release of Trichogramma for biological control of insect pests of corn in China. Biol Control 68:136–144
Wang Y, Xiang M, Hou YY, Yang X, Dai H et al (2019) Impact of egg deposition period on the timing of adult emergence in Trichogramma parasitoids. Entomol Gen 39:339–346
Watt TJ, Duan JJ, Tallamy DW, Goldstein JH (2015) Effect of parasitoid: host ratio and group size on fitness of Spathius galinae (Hymenoptera: Braconidae): implications for mass-rearing. J Econ Entomol 108:951–956
Wei K, Gao SK, Tang YL, Wang XY, Yang ZQ (2016) Determination of the optimal parasitoid-to-host ratio for efficient mass-rearing of the parasitoid, Sclerodermus pupariae (Hymenoptera: Bethylidae). J Appl Entomol 141:181–188
Wu H, Huang YC, Guo JX, Liu JB, Lai XS et al (2018) Effect of cold storage of Corcyra cephalonica eggs on the fitness for Trichogramma chilonis. Biol Control 124:40–45
Yamamoto D, Henderson R, Corley LS, Iwabuchi K (2007) Intrinsic, inter-specific competition between egg, egg—larval, and larval parasitoids of plusiine loopers. Ecol Entomol 32:221–228
Yuan XH, Song LW, Zhang JJ, Zang LS, Zhu L, Ruan CC, Sun GZ (2012) Performance of four Chinese Trichogramma species as biocontrol agents of the rice striped stem borer, Chilo suppressalis, under various temperature and humidity regimes. J Pest Sci 85:497–504
Zang LS (2015) Mass production of Trichogramma dendrolimi using eggs of Antheraea pernyi, and field application in the suppression of Ostrinia furnacalis in Jilin Province, China. IOBC Newsl 98:9
Zang LS, Wang S, Zhang F, Desneux N (2021) Biological control with Trichogramma in China: history, present status and perspectives. Annu Rev Entomol. https://doi.org/10.1146/annurev-ento-060120-091620
Zhang JJ, Desneux N, Benelli G, Zang LS, Du WM, Ruan CC (2017) Geographic variation of diapause induction rates in Trichogramma drendrolimi (Hymenoptera: Trichogrammatidae) in China. J Econ Entomol 110:386–391
Zhang JJ, Zhang X, Zang LS, Du WM, Hou YY, Ruan CC, Desneux N (2018) Advantages of diapause in Trichogramma dendrolimi mass production via eggs of the Chinese silkworm, Antheraea pernyi. Pest Manag Sci 74:959–965
Acknowledgements
This research was funded by the National Key R&D Program of China (2017YFD0201000) and the National Natural Science Foundation of China (31901946 and 31572058).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Communicated by M. Traugott.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Iqbal, A., Hou, YY., Chen, YM. et al. Impact of Trichogramma parasitoid age on the outcome of multiparasitism in the factitious host eggs of Chinese oak silkworm, Antheraea pernyi. J Pest Sci 93, 1347–1357 (2020). https://doi.org/10.1007/s10340-020-01239-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-020-01239-1