Abstract
Globally, insect abundance and diversity are experiencing a rapid decline. Despite important inter-taxa and geographical variability, this can entail an extinction of ecological interactions and a decay of ecosystem functions. In this study, we compared the spatial distribution, abundance and species composition of Trichogramma spp. egg parasitoids (Hymenoptera: Trichogrammatidae) over a 30-year time period in China. During the 1980s and in 2016–2018, egg masses of the Asian corn borer (ACB), Ostrinia furnacalis, were systematically sampled from corn fields across the country. In 2018, five species were identified with Trichogramma ostriniae representing 90% of the species complex. Since the 1980s, two new species have made their appearance while nine (out of 12; i.e., 75%) species disappeared. These include comparative specialists but also generalists such as T. evanescens and T. exiguum. Across sites, species richness (R) and diversity (Shannon-Weiner index) have declined by a respective 25–86% and 56–100% (except for Heilongjiang province) over this time frame. We hypothesize that this is attributed to land use change, pesticide use and plant diversity decline in agro-landscapes. Conversely, no negative impacts were detected of augmentative biological control. Given the drastic reduction in ACB parasitoid richness, agro-ecological measures and diversification strategies should be deployed to restore the ecological resilience of local farming systems. Our work carries major implications for food security and helps to muster support for more nature-friendly, pest-resilient farming systems in China and abroad.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Babendreier D, Schoch D, Kuske S, Dorn S, Bigler F (2003) Non-target habitat exploitation by Trichogramma brassicae (Hym. Trichogrammatidae): what are the risks for endemic butterflies? Agri For Entomol 5(3):199–208. https://doi.org/10.1046/j.1461-9563.2003.00180.x
Burgio G, Maini S (1995) Control of European corn borer in sweet corn by Trichogramma brassicae Bezd. (Hym. Trichogrammatidae). J Appl Entomol 119(1–5):83–87. https://doi.org/10.1111/j.1439-0418.1995.tb01248.x
Burra DD, Pretty J, Neuenschwander P, Liu Z, Zhu ZR, Wyckhuys KAG (2021) Human health outcomes of a restored ecological balance in African agro-landscapes. Sci Total Environ 775:145872. https://doi.org/10.1016/j.scitotenv.2021.145872
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P et al (2012) Biodiversity loss and its impact on humanity. Nature 486(7401):59–67. https://doi.org/10.1038/nature11148
Cardoso P, Barton PS, Birkhofer K, Chichorro F, Deacon C, Fartmann T et al (2020) Scientists' warning to humanity on insect extinctions. Biol Conserv 242:108426. https://doi.org/10.1016/j.biocon.2020.108426
Consoli FL, Parra J, Zucchi RA (eds) (2010) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma , vol 9. Springer Science & Business Media. https://doi.org/10.1007/978-1-4020-9110-0
Crossley MS, Meier AR, Baldwin EM, Berry LL, Crenshaw LC, Hartman GL et al (2020) No net insect abundance and diversity declines across US Long Term Ecological Research sites. Nat Ecol Evol 4(10):1368–1376. https://doi.org/10.1038/s41559-020-1269-4
Cui ZL, Zhang HY, Chen XP, Zhang CC, Ma WQ, Huang CD et al (2018) Pursuing sustainable productivity with millions of smallholder farmers. Nature 555(7696):363–366. https://doi.org/10.1038/nature25785
Dainese M, Martin EA, Aizen MA, Albrecht M, Bartomeus I, Bommarco R et al (2019) A global synthesis reveals biodiversity-mediated benefits for crop production. Sci Adv 5(10):eaax0121. https://doi.org/10.1126/sciadv.aax0121
Ely A, Geall S, Song Y (2016) Sustainable maize production and consumption in China: practices and politics in transition. J Clean Prod 134:259–268. https://doi.org/10.1016/j.jclepro.2015.12.001
Feng J (1996) The effect and influence factors on the use of Trichogramma dendrolimi to control Ostrinia furnacalis. Entomol J East China 5:45–50
Feng JG, Tao X, Zhang AS, Yu Y, Zhang CW, Cui YY (1999) Studies on using Trichogramma spp. reared on artificial host egg to control corn pests. Chin J Biol Contr 15:97–99. https://doi.org/10.3969/j.issn.2095-039X.1999.03.001
Guo WC, He J, Xu JJ, Tuerxun., Tan YF, Mao G et al (2005) Studies on harmless control of Ostrinia furnacalis in maize field of Xinjiang. J Maize Sci 13:108–110. https://doi.org/10.3969/j.issn.1005-0906.2005.01.033
Guo JL, Fu XW, Zhao SY, Shen XJ, Wyckhuys KA, Wu KM (2020) Long-term shifts in abundance of (migratory) crop-feeding and beneficial insect species in northeastern Asia. J Pest Sci 93(2):583–594. https://doi.org/10.1007/s10340-019-01191-9
Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Ann Rev Entomol 62:91–109. https://doi.org/10.1146/annurev-ento-031616-035050
Habel JC, Trusch R, Schmitt T, Ochse M, Ulrich W (2019a) Long-term large-scale decline in relative abundances of butterfly and burnet moth species across south-western Germany. Sci Rep 9:14921. https://doi.org/10.1038/s41598-019-51424-1
Habel JC, Ulrich W, Biburger N, Seibold S, Schmitt T (2019b) Agricultural intensification drives butterfly decline. Insect Conserv Diver 12(4):289–295. https://doi.org/10.1111/icad.12343
Habel JC, Schmitt T, Gros P, Ulrich W (2022) Breakpoints in butterfly decline in Central Europe over the last century. Sci Total Environ 851:158315. https://doi.org/10.1016/j.scitotenv.2022.158315
Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H et al (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12(10):e0185809. https://doi.org/10.1371/journal.pone.0185809
Hawlitzky N, Dorville FM, Vaillant J (1994) Statistical study of Trichogramma brassicae efficiency in relation with characteristics of the European corn borer egg masses. Res Popul Ecol 36(1):79–85. https://doi.org/10.1007/BF02515088
He KL, Wang ZY, Zhou DR, Wen LP, Song YY, Yao ZY (2003) Evaluation of transgenic Bt corn for resistance to the Asian corn borer (Lepidoptera: Pyralidae). J Econ Entomol 96:935–940. https://doi.org/10.1093/jee/96.3.935
Heethoff M, Laumann M, Weigmann G, Raspotnig G (2011) Integrative taxonomy: combining morphological, molecular and chemical data for species delineation in the parthenogenetic Trhypochthonius tectorum complex (Acari, Oribatida, Trhypochthoniidae). Front Zool 8(1):1–10. https://doi.org/10.1186/1742-9994-8-2
Huang NX, Jaworski C, Desneux N, Zhang F, Yang PY, Wang S (2020) Long-term, large-scale releases of Trichogramma promote pesticide decrease in maize in northeastern China. Entomol Gen 40:331–335. https://doi.org/10.1127/entomologia/2020/0994
Janssen A, van Rijn PC (2021) Pesticides do not significantly reduce arthropod pest densities in the presence of natural enemies. Ecol Lett 24(9):2010–2024. https://doi.org/10.1111/ele.13819
Janzen DH (1971) The deflowering of central America. Nat History 83:49–53
Jiang YY, Liu J, Zhu XM (2019) Analysis on the occurrence dynamics and future trend of Spodoptera frugiperda invasion in China. Plant Prot 39:33–35. https://doi.org/10.3969/j.issn.1672-6820.2019.02.006
Jonsson M, Buckley HL, Case BS, Wratten SD, Hale RJ, Didham RK (2012) Agricultural intensification drives landscape-context effects on host–parasitoid interactions in agroecosystems. J Appl Ecol 49(3):706–714. https://doi.org/10.1111/j.1365-2664.2012.02130.x
Kadoya T, Suda SI, Washitani I (2009) Dragonfly crisis in Japan: a likely consequence of recent agricultural habitat degradation. Biol Conserv 142(9):1899–1905. https://doi.org/10.1016/j.biocon.2009.02.033
Kehoe R, Frago E, Sanders D (2021) Cascading extinctions as a hidden driver of insect decline. Ecol Entomol 46(4):743–756. https://doi.org/10.1111/een.12985
Kenis M, Du Plessis H, Van den Berg J, Ba MN, Goergen G, Kwadjo KE 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(4):92. https://doi.org/10.3390/insects10040092
Koca AS, Mren M, HalilKütük. (2018) Determination of the genetic variation within the egg parasitoid,Trichogramma brassicae, Bezdenko (Hymenoptera: Trichogrammatidae) populations in Düzce Province. Turk Uluslararası Tarım ve Yaban Hayatı Bilimleri Dergisi 4(1):26–32. https://doi.org/10.24180/ijaws.395438
Kuske S, Widmer F, Edwards PJ, Turlings TC, Babendreier D, Bigler F (2003) Dispersal and persistence of mass-released Trichogramma brassicae (Hymenoptera: Trichogrammatidae) in non-target habitats. Biol Control 27(2):181–193. https://doi.org/10.1016/S1049-9644(02)00191-3
Laliberté E, Tylianakis JM (2010) Deforestation homogenizes tropical parasitoid–host networks. Ecology 91(6):1740–1747. https://doi.org/10.1890/09-1328.1
Li ZX (2007) Molecular differentiation of the four most commonly occurring Trichogramma species in China. Eur J Entomol 104(3):363–367. https://doi.org/10.14411/EJE.2007.054
Liao YL, Yang B, Xu MF, Lin W, Wang DS, Chen KW et al (2019) First report of Telenomus remus parasitizing Spodoptera frugiperda and its field parasitism in southern China. J Hymenop Res 73:95–102. https://doi.org/10.3897/jhr.73.39136
Lister BC, Garcia A (2018) Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc Natl Acad Sci B U S A 115(44):201722477. https://doi.org/10.1073/pnas.1722477115
Liu GQ (2019) Intra egg competition of Trichogramma dominant parasitic Asian corn borer (Ostrinia furnacalis) based on microsatellite markers, pp 23-29. Master's Thesis, Jilin Agriculture University, Changchun. https://doi.org/10.27163/d.cnki.gjlnu.2019.000151
Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56(4):311–323. https://doi.org/10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2
Nafus DM, Schreiner I (1991) Review of the biology and control of the Asian corn borer, Ostrinia furnacalis (Lep: Pyralidae). Trop Pest Manag 37:41–56. https://doi.org/10.1080/09670879109371535
Noyes JS (1982) Collecting and preserving chalcid wasps (Hymenoptera: Chalcidoidea). J Nat Hist 16:315–334. https://doi.org/10.1080/00222938200770261
Oztemiz S (2007) Trichogramma species (Hymenoptera: Trichogrammatidae) egg parasitoids of Lepidoptera in the Eastern Mediterranean Region of Turkey. Proc Entomol Soc Wash 109:718–720
Paolo SM, Cesar RS, Odair AF (2020) Release density, dispersal capacity, and optimal rearing conditions for Telenomus remus, an egg parasitoid of Spodoptera frugiperda, in maize. Biocontrol Sci Technol 30(10):1040–1059. https://doi.org/10.1080/09583157.2020.1776841
Perović DJ, Gámez-Virués S, Landis DA, Wäckers F, Gurr GM, Wratten SD et al (2018) Managing biological control services through multi‐trophic trait interactions: review and guidelines for implementation at local and landscape scales. Biol Rev 93(1):306–321. https://doi.org/10.1111/brv.12346
Pimentel D, Wilson C, McCullum C, Huang R, Dwen P, Flack J et al (1997) Economic and environmental benefits of biodiversity. Bioscience 47(11):747–757. https://doi.org/10.2307/1313097
Pinto JD (1999) Systematics of the North American species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae). Memoirs Entomol Soc Wash 22(1998):1–287
Pinto JD, Velten RK, Platner GR, Oatman ER (1989) Phenotypic plasticity and taxonomic characters in Trichogramma (Hymenoptera: Trichogrammatidae). Ann Entomol Soc Am 83:414–425. https://doi.org/10.1093/aesa/82.4.414
Poorjavad N, Goldansaz SH, Machtelinckx T, Tirry L, Stouthamer R, Leeuwen TV (2012) Iranian Trichogramma: ITS-2 DNA characterization and natural Wolbachia infection. Biocontrol 57(3):361–374. https://doi.org/10.1007/s10526-011-9397-z
Raven PH, Wagner DL (2021) Agricultural intensification and climate change are rapidly decreasing insect biodiversity. Proc Natl Acad Sci USA 118(2):e2002548117. https://doi.org/10.1073/pnas.2002548117
Sánchez-Bayo F, Wyckhuys KA (2019) Worldwide decline of the entomofauna: A review of its drivers. Biol Conserv 232:8–27. https://doi.org/10.1016/j.biocon.2019.01.020
Sánchez-Bayo F, Wyckhuys KA (2021) Further evidence for a global decline of the entomofauna. Austral Entomol 60(1):9–26. https://doi.org/10.1111/aen.12509
Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Ann Rev Entomol 55:421–438. https://doi.org/10.1146/annurev-ento-112408-085432
Seibold S, Gossner MM, Simons NK, Blüthgen N, Müller J, Ambarlı D et al (2019) Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574(7780):671–674. https://doi.org/10.1038/s41586-019-1684-3
Soliveres S, Van Der Plas F, Manning P, Prati D, Gossner MM, Renner SC et al (2016) Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality. Nature 536(7617):456–459. https://doi.org/10.1038/nature19092
Song LQ, Wei LM, Wang ZY, He KL, Cong B (2009) Effect of infestation by the Asian corn borer together with Fusarium verticillioides on corn yield loss. Acta Phytophyl Sin 36:487–490. https://doi.org/10.3321/j.issn:0577-7518.2009.06.002
Stouthamer R, Hu J, Kan F, 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. https://doi.org/10.1023/A:1009937108715
Suverkropp BP (1994) Landing of Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) on maize plants. Nor J Agri Sci Supplement 16:243–254
Suverkropp BP (1997) Host-finding behaviour of Trichogramma brassicae in maize, p 249 . PhD Thesis, Wageningen University, The Netherlands.
Tan YQ (1999) Present status and prospect in Trichogramma application in Heilongjiang Province. Chin Agri Sci Bull 15:50–51
Tang FH, Lenzen M, McBratney A, Maggi F (2021) Risk of pesticide pollution at the global scale. Nat Geosci 14(4):206–210. https://doi.org/10.1038/s41561-021-00712-5
van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63(1):39–59. https://doi.org/10.1007/s10526-017-9801-4
Wagner DL, Grames EM, Forister ML, Berenbaum MR, Stopak D (2021) Insect decline in the Anthropocene: Death by a thousand cuts. Proc. Natl. Acad. Sci. USA 118(2):1–10. https://doi.org/10.1073/pnas.2023989118
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 Contr 68:136–144. https://doi.org/10.1016/j.biocontrol.2013.06.015
Wang YZ, Kim KS, Guo WC, Zhang YY, Wang ZY, Coates BS (2017) Introgression between divergent corn borer species in a region of sympatry: Implications on the evolution and adaptation of pest arthropods. Mol Ecol 26:6892–6907. https://doi.org/10.1111/mec.14387
Wu L, He NP, Hou DW (2001) Studies on controlling effect of Trichogramma chilonis to corn borer. J Jilin Agri Sci 26:35–37. https://doi.org/10.3969/j.issn.1003-8701.2001.06.007
Wu J, Guo WC, Turxun., He J, Xu JJ (2008) Effects of heat stress on parasitic functional response of Trichogramma pintoi. Xinjiang Agri Sci (S2), 122–126
Wu Y, Xi X, Tang X, Luo D, Gu B, Lam SK et al (2018) Policy distortions, farm size, and the overuse of agricultural chemicals in China. Proc Natl Acad Sci USA 115(27):7010–7015. https://doi.org/10.1073/pnas.1806645115
Xu JJ, Guo WC, He J (2001) Primary report on control technique of Asian corn borer by using Trichogramma in Xinjiang. Xinjiang Agri Sci 38:315–317. https://doi.org/10.3969/j.issn.1001-4330.2001.06.006
Yang RS, Wang ZY, He KL, Bai SX (2008) Sequence analysis of mtDNA-COII gene and molecular phylogeny of Ostrinia spp. from China (Lepidoptera: Crambidae). Acta Entomol Sin 51:182–189. https://doi.org/10.16380/j.kcxb.2008.02.005
Yang RS, Wang ZY, He KL, Bai SX, Jiang YR (2011) Genetic diversity and phylogeny of the genus Ostrinia (Lepidoptera: Crambidae) inhabiting China inferred from mitochondrial CO I gene. J. Nanjing Agri Univ 34:73–80. https://doi.org/10.7685/j.issn.1000-2030.2011.05.014
Yang XM, Wyckhuys KA, Jia XP, Nie FY, Wu KM (2021) Fall armyworm invasion heightens pesticide expenditure among Chinese smallholder farmers. J Environ Manage 282:111949. https://doi.org/10.1016/j.jenvman.2021.111949
Yu SH, Wang ER, Zhang YL, Li GQ, Wen XF, Hao XR et al (1982) Primary study on the control of corn borer by pine Moth-Trichogramma Labelled With 32P. Appl. Atomic Ener. Agri. (2), 31–36
Yu DS, Achterberg CV, Horstman K (2016) Taxonomy, Biology, Morphology and Distribution. Database on flash-drive. Ontario, Canada. www.taxapad.com Taxapad 2016 - World Ichneumonoidea 2015
Zang LS, Wang S, Zhang F, Desneux N (2021) Biological control with Trichogramma in China: history, present status, and perspectives. Ann Rev Entomol 66:463–484. https://doi.org/10.1146/annurev-ento-060120-091620
Zeng J, Liu YQ, Zhang HW, Liu J, Jiang YH, Wyckhuys KA et al (2020) Global warming modifies long-distance migration of an agricultural insect pest. J Pest Sci 93(2):569–581. https://doi.org/10.1007/s10340-019-01187-5
Zhan GX, Liang GW (1999) Research and application of Trichogramma in China. Acta Agri Jiangxi 11:39–46. https://doi.org/10.19386/j.cnki.jxnyxb.1999.02.009
Zhang J, Wang GH, GE WF, Wang EJ, Chen XH, Fang YF (1979) Investigation of Trichogramma Species in Liaoning Province (preliminary report). J Shenyang Agri Univ (01),75–84 + 59
Zhang J, Wang JL, Cong B, Yang CC (1990) A faunal study of Trichogramma species on Ostrinia furnacalis in China. Chin J Biol Contr 6:49–53. https://doi.org/10.16409/j.cnki.2095-039x.1990.02.001
Zhou DR, Wang YS, Li WD (1988) Studies on the identification of the dominant corn borer species in China. Acta Phytophyl Sin 15:145–152. https://doi.org/10.13802/j.cnki.zwbhxb.1988.03.001
Funding
This study was supported by the Agricultural Science and Technology Innovation Program, and China Agriculture Research System of MOF and MARA (CARS-02). Scientific Research Project of Beijing Vocational College of Agriculture (XY-YF-18-10).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. ZW and KH designed experiments, ZH, ZW, TZ, SB and YYM carried out material preparation, data collection and analysis. ZH and KAGW contributed the first draft of the manuscript. ZW, KW and ZL helped perform the analysis with constructive discussions. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.
Additional information
Communicated by Akihiro Nakamura.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hu, Z., Myint, Y.Y., Zhang, T. et al. Loss of parasitoid diversity in China’s corn agro-ecosystem over a 30-year time period. Biodivers Conserv 32, 1309–1325 (2023). https://doi.org/10.1007/s10531-023-02554-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-023-02554-6