Metabarcoding is revolutionizing fundamental research in ecology by enabling large-scale detection of species and producing data that are rich with community context. However, the benefits of metabarcoding have yet to be fully realized in fields of applied ecology, especially those such as classical biological control (CBC) research that involve hyperdiverse taxa. Here, we discuss some of the opportunities that metabarcoding provides CBC and solutions to the main methodological challenges that have limited the integration of metabarcoding in existing CBC workflows. We focus on insect parasitoids, which are popular and effective biological control agents (BCAs) of invasive species and agricultural pests. Accurately identifying native, invasive and BCA species is paramount, since misidentification can undermine control efforts and lead to large negative socio-economic impacts. Unfortunately, most existing publicly accessible genetic databases cannot be used to reliably identify parasitoid species, thereby limiting the accuracy of metabarcoding in CBC research. To address this issue, we argue for the establishment of authoritative genetic databases that link metabarcoding data to taxonomically identified specimens. We further suggest using multiple genetic markers to reduce primer bias and increase taxonomic resolution. We also provide suggestions for biological control-specific metabarcoding workflows intended to track the long-term effectiveness of introduced BCAs. Finally, we use the example of an invasive pest, Drosophila suzukii, in a reflective "what if" thought experiment to explore the potential power of community metabarcoding in CBC.

Agriculture and Agri Food Canada Agassiz Research and Development Centre Agassiz British Columbia Canada

Biology Centre of the Czech Academy of Sciences Institute of Entomology Ceske Budejovice Czech Republic

Department of Biology Brooklyn College City University of New York New York City New York USA

Systematic Entomology Laboratory ARS USDA c o Smithsonian Institution National Museum of Natural History Washington DC USA

Zobrazit více v PubMed

Abram, P. K., Hoelmer, K. A., Acebes-Doria, A., Andrews, H., Beers, E. H., Bergh, J. C., Bessin, R., Biddinger, D., Botch, P., Buffington, M. L., Cornelius, M. L., Costi, E., Delfosse, E. S., Dieckhoff, C., Dobson, R., Donais, Z., Grieshop, M., Hamilton, G., Haye, T., … Wiman, N. G. (2017). Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. Journal of Pest Science, 90(4), 1009-1020.

Abram, P. K., Mcpherson, A. E., Kula, R., Hueppelsheuser, T., Perlman, S. J., Curtis, C. I., Fraser, J. L., Tam, J., Carrillo, J., Gates, M., Scheffer, S., Lewis, M., & Buffington, M. (2020). New records of Leptopilina, Ganaspis, and Asobara species associated with Drosophila suzukii in North America, including detections of L. japonica and G. brasiliensis. Journal of Hymenoptera Research, 78, 1-17. https://doi.org/10.3897/jhr.78.55026

Abram, P. K., & Moffat, C. E. (2018). Rethinking biological control programs as planned invasions. Current Opinion in Insect Science, 27, 9-15. https://doi.org/10.1016/j.cois.2018.01.011

Abram, P. K., Wang, X., Hueppelsheuser, T., Franklin, M. T., Daane, K. M., Lee, J. C., Lue, C.-H., Girod, P., Carrillo, J., WHL, W., Kula, R. R., Gates, M. W., Hogg, B. N., Moffat, C. E., Hoelmer, K. A., Sial, A. A., & Buffington, M. L. (2022). A coordinated sampling and identification methodology for larval parasitoids of spotted-wing Drosophila. Journal of Economic Entomology, 115, 922-942. https://doi.org/10.1093/jee/toab237

Andersen, K., Bird, K. L., Rasmussen, M., Haile, J., Breuning-Madsen, H., Kjaer, K. H., Orlando, L., Gilbert, M. T., & Willerslev, E. (2012). Metabarcoding of “dirt” DNA from soil reflects vertebrate biodiversity. Molecular Ecology, 21(8), 1966-1979. https://doi.org/10.1111/j.1365-294x.2011.05261.x

Asplen, M. K., Anfora, G., Biondi, A., Choi, D. S., Chu, D., Daane, K. M., Gibert, P., Gutierrez, A. P., Hoelmer, K., Hutchison, W., Isaacs, R., Jiang, Z.-L., Kárpáti, Z., Kimura, M., Pascual, M., Philips, C., Plantamp, C., Ponti, L., Vétek, G., & Desneux, N. (2015). Invasion biology of spotted wing Drosophila (Drosophila suzukii): A global perspective and future priorities. Journal of Pest Science, 88, 469-494.

Batovska, J., Piper, A. M., Valenzuela, I., Cunningham, J. P., & Blacket, M. J. (2021). Developing a nondestructive metabarcoding protocol for detection of pest insects in bulk trap catches. Scientific Reports, 11, 7946. https://doi.org/10.1038/s41598-021-85855-6

Beers, E. H., Beal, D., Smytheman, P., Abram, P. K., Schmidt-Jeffris, R., Moretti, E., Daane, K. M., Looney, C., Lue, C.-H., & Buffington, M. (2022). First records of adventive populations of the parasitoids Ganaspis brasiliensis and Leptopilina japonica in the United States. Journal of Hymenoptera Research, 91, 11-25. https://doi.org/10.3897/jhr.91.82812

Bik, H. M., Porazinska, D. L., Creer, S., Caporaso, J. G., Knight, R., & Thomas, W. K. (2012). Sequencing our way towards understanding global eukaryotic biodiversity. Trends in Ecology & Evolution, 27, 233-243. https://doi.org/10.1016/j.tree.2011.11.010

Biondi, A., Wang, X. G., & Daane, K. M. (2021). Host preference of three Asian larval parasitoids to closely related Drosophila species: Implications for biological control of Drosophila suzukii. Journal of Pest Science, 94, 273-283.

Bortolus, A. (2008). Error cascades in the biological sciences: The unwanted consequences of using bad taxonomy in ecology. Ambio, 37, 114-118.

Brandon-Mong, G. J., Gan, H. M., Sing, K. W., Lee, P. S., Lim, P. E., & Wilson, J. J. (2015). DNA metabarcoding of insect and allies: An evaluation of primers and pipelines. Bulletin of Entomological Research, 105, 717-727. https://doi.org/10.1017/s0007485315000681

Brodeur, J., Abram, P. K., Heimpel, G. E., & Messing, R. H. (2018). Trends in biological control: Public interest, international networking and research direction. BioControl, 63, 11-16.

Brower, A. V. Z., & DeSalle, R. (2002). Patterns of mitochondrial versus nuclear DNA sequence divergence among nymphalid butterflies: The utility of wingless as a source of characters for phylogenetic inference. Insect Molecular Biology, 7(1), 73-82. https://doi.org/10.1046/j.1365-2583.1998.71052.x

Brown, E. A., Chain, F. J. J., Zhan, A., Maclsaac, H. J., & Cristescu, M. E. (2016). Early detection of aquatic invaders using metabarcoding reveals a high number of non-indigenous species in Canadian ports. Diversity and Distributions, 22(10), 1045-1059. https://doi.org/10.1073/ddi.12465

Bush, A., Monk, W. A., Compson, Z. G., Peters, D. L., Poter, T. M., Shokralla, S., Wright, M. T. G., Hajibabaei, M., & Baird, D. J. (2020). DNA metabarcoding reveals metacommunity dynamics in a threatened boreal wetland wilderness. Proceedings of the National Academy of Sciences of the United States of America, 117(15), 8535-8549. https://doi.org/10.1073/pnas.1918741117

Callahan, B. J., Wong, J., Heiner, C., Oh, S., Theriot, C. M., Gulati, A. S., McGill, S. K., & Dougherty, M. K. (2019). High-throughput amplicon sequencing of the full-length 16S rRNA gene with single-nucleotide resolution. Nucleic Acids Research, 47(18), e103. https://doi.org/10.1093/nar/gkz569

Clare, E. L. (2014). Molecular detection of trophic interactions: Emerging trends, distinct advantages, significant considerations and conservation applications. Evolutionary Applications, 7, 1144-1157. https://doi.org/10.1111/eva.12225

Comtet, T., Sandionigi, A., Viard, F., & Carsiraghi, M. (2015). DNA (meta)barcoding of biological invasions: A powerful tool to elucidate invasion processes and help managing aliens. Biological Invasions, 17, 905-922. https://doi.org/10.1007/s10530-015-0854-y

Creedy, T. J., Andujar, C., Meramveliotakis, E., Noguerales, V., Overcast, I., Papadopoulou, A., Morlon, H., Vogler, A. P., Emerson, B. C., & Arribas, P. (2021). Coming of ago for COI metabarcoding of whole organism community DNA: Towards bioinformatic harmonisation. Molecular Ecology Resources, 22, 847-861.

Cristescu, M. E. (2014). From barcoding single individuals to metabarcoding biological communities: Towards an integrative approach to the study of global diversity. Trends in Ecology & Evolution, 29, 566-571. https://doi.org/10.1016/j.tree.2014.08.001

Cuff, J., Kitson, J., Hemprich-Bennett, D., Tercel, M., Browett, S., & Evans, D. (2022). The predator problem and PCR primers in molecular ditary analysis: Swamped or silenced; depth or breadth? Molecular Ecology Resources. https://doi.org/10.1111/1755-0998.13705

Cuff, J. P., Windsor, F. M., Tercel, M. T. G., Kitson, J. J. N., & Evans, D. M. (2021). Overcoming the pitfalls of merging dietary metabarcoding into ecological networks. Methods in Ecology and Evolution, 13, 545-559.

Daane, K. M., Wang, X.-G., Biondi, A., Miller, B. E., Miller, J. C., Riedl, H., Shearer, P. W., Guerrieri, E., Giorgini, M., Buffington, M., van Achterberg, K., Han, S. Y., Gun, K. T., Bok, Y. H., Leui, J. C., Woon, L. D., Keun, C. B., Hoelmer, K. A., & Walton, V. M. (2016). First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. Journal of Pest Science, 89, 823-835. https://doi.org/10.1007/s10340-016-0740-0

Deagle, B. E., Jarman, S. N., Coissac, E., Pompanon, F., & Taberlet, P. (2014). DNA metabarcoding and the cytochrome c oxidase subunit 1 marker: Not a perfect match. Biology Letters, 10, 20140562. https://doi.org/10.1098/rsbl.2014.0562

Deiner, K., Bik, H. M., Machler, E., Seymour, M., Lacoursiere-Roussel, A., Altermatt, F., Creer, S., Bista, I., Lodge, D. M., de Vere, N., Pfrender, M. E., & Bernatchez, L. (2017). Environmental DNA metabarcoding: Transforming how we survey animal and plan communities. Molecular Ecology, 26, 5872-5895. https://doi.org/10.1111/mec.14350

Derocles, S. A. P., Plantegenest, M., Simon, J.-C., Taberlet, P., & Ralec, A. (2012). A universal method for the detection and ifentification of Aphidiinae parasitoids within their aphid hosts. Molecular Ecology Resources, 12(4), 634-645. https://doi.org/10.1111/j.1755-0998.2012.03131.x

DiGiacomo, G., Hadrich, J., Hutchison, W. D., Peterson, H., & Rogers, M. (2019). Economic impact of spotted wing Drosophila (Diptera: Drosophilidae) yield loss on Minnesota raspberry farms: A grower survey. Journal of Integrated Pest Management, 10, 11. https://doi.org/10.1093/jipm/pmz006

dos Santos, L. A., Mendes, M. F., Kruger, A. P., Blauth, M. L., Gottschalk, M. S., & Garcia, F. R. M. (2017). Global potential distribution of Drosophila suzukii (Diptera, Drosophilidae). PLoS One, 12(3), e0174318. https://doi.org/10.1371/journal.pone.0174318

Dueñas, M.-A., Hemming, D. J., Roberts, A., & Diaz-Soltero, H. (2021). The threat of invasive species to IUCN-listed critically endangered species: A systematic review. Global Ecology and Conservation, 26, e01476. https://doi.org/10.1016/j.gecco.2021.e01476

Elbrecht, V., & Leese, F. (2017). Validation and development of COI metabarcoding primers for freshwater macroinvertebrate bioassessment. Frontiers in Environmental Science, 5, 11. https://doi.org/10.3389/fenvs.2017.00011

Elbrecht, V., Taberlet, P., Dejean, T., Valentini, A., Usseglio-Polatera, P., Beisel, J.-N., Coissac, E., Boyer, F., & Leese, F. (2016). Testing the potential of a ribosomal 16S marker for DNA metabarcoding insects. Peer J, 4, e1966. https://doi.org/10.7717/peerj.1966

Evans, D. M., Kitson, J., Lunt, D. H., Straw, N. A., & Pocock, M. J. (2016). Merging DNA metabarcoding and ecological netowkr analysis to understand and build resilient terrestrial ecosystem. Functional Ecology, 30(12), 1904-1916. https://doi.org/10.1111/1365-2435.12659

Fagan-Jeffries, E. P., Cooper, S. J. B., Bertozzi, T., Bradford, T. M., & Austin, A. D. (2018). DNA barcoding of microgastrine parasitoid wasps (Hymenoptera: Braconidae) using high-throughput methods more than doubles the number of species known for Australia. Molecular Ecology Resources, 18(5), 1132-1143. https://doi.org/10.1111/1755-0998.12904

Farnsworth, D., Hamby, K. A., Bolda, M., Goodhue, R. E., Williams, J. C., & Zalom, F. G. (2017). Economic analysis of revenue losses and control costs associated with the spotted wing Drosophila, Drosophila suzukii (Matsumura), in the California raspberry industry. Pest Management Science, 73, 1083-1090.

Ficetola, G. F., Boyer, F., Valentini, A., Bonin, A., Meyer, A., Dejean, T., Gaboriaud, C., Usseglio-Polatera, P., & Taberlet, P. (2020). Comparison of markers for the monitoring of freshwater benthic biodiversity through DNA metabarcoding. Molecular Ecology, 30(13), 3189-3020. https://doi.org/10.1111/mec.15632

Ficetola, G. F., Pansu, J., Bonin, A., Coissac, E., Giguet-Covex, C., De Barba, M., Gielly, L., Lopes, C. M., Boyer, F., Pompanon, F., Rayé, G., & Taberlet, P. (2014). Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data. Molecular Ecology Resources, 15, 543-556. https://doi.org/10.1111/1755-0998.12338

Forbes, A. A., Bagley, R. K., Beer, M. A., Hippee, A. C., & Widmayer, H. A. (2018). Quantifying the unquantifiable: Why Hymenoptera, not Coleoptera, is the most speciose animal order. BMC Ecology, 18, 21. https://doi.org/10.1186/s12898-018-0176-x

Freeland, J. R. (2017). The importance of molecular markers and primer design when characterizing biodiversity from environmental DNA. Genome, 6, 358-374.

Gariepy, T. D., Bruin, A., Konopka, J., Scott-Dupree, C., Fraser, H., Bon, M. C., & Talamas, E. (2019). A modified DNA barcode approach to define trophic interactions between native and exotic pentatomids and their parasitoids. Molecular Ecology, 28(2), 456-470. https://doi.org/10.1111/mec.14868

Gariepy, T. D., Kuhlmann, U., Gillott, C., & Erlandson, M. (2007). Parasitoids, predators and PCR: The use of diagnostic molecular markers in biological control of Arthropods. Journal of Applied Entomology, 131(4), 225-240.

Giorgini, M., Wang, X.-G., Wang, Y., Chen, F. S., Hougardy, E., Zhang, H. M., Chen, Z. Q., Chen, H. Y., Liu, C. X., Cascone, P., Formisano, G., Carvalho, G. A., Biondi, A., Buffington, M., Daane, K. M., Hoelmer, K. A., & Guerrieri, E. (2019). Exploration for native parasitoids of Drosophila suzukii in China reveals a diversity of parasitoid species and narrow host range of the dominant parasitoid. Journal of Pest Science, 92(2), 509-522. https://doi.org/10.1007/s10340-018-01068-3

Girod, P., Borowiec, N., Buffington, M., Chen, G., Fang, Y., Kimura, M. T., Peris-Felipo, F. J., Ris, N., Wu, H., Xiao, C., Zhang, J., Aebi, A., Haye, T., & Kenis, M. (2018). The parasitoid complex of D. suzukii and other fruit feeding Drosophila species in Asia. Scientific Reports, 8(1), e11839. https://doi.org/10.1038/s41598-018-29555-8

Gompert, Z., Forister, M. L., Fordyce, J. A., & Nice, C. C. (2008). Widespread mito-nuclear discordance with evidence for introgressive hybridization and selective sweeps in Lycaeides. Molecular Ecology, 17(24), 5231-5244. https://doi.org/10.1111/j.1365-294X.2008.03988.x

Greathead, D. J., & Greathead, A. H. (1992). Biological control of insect pests by insect parasitoids and predators: The BIOCAT database. Biocontrol News and Information, 13, 61N-68N.

Grissell, E. (1999). Hymenopteran biodiversity: Some alien notions. American Entomologist, 45, 236-244.

Haye, T., Goulet, H., Mason, P. G., & Kuhlmann, U. (2005). Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid. Biological Control, 35(1), 55-67.

Haye, T., Mason, P. G., Gillespie, D. R., Miall, J. H., Gibson, G. A. P., Diaconu, A., Brauner, A. M., & Kuhlmann, U. (2015). Determining the host specificity of the biological control agent Trichomalus perfectus (Hymenoptera: Pteromalidae): The importance of ecological host range. Biocontrol Science and Technology, 25(1), 21-47.

Heimpel, G. E., & Cock, M. J. (2018). Shifting paradigms in the history of classical biological control. BioControl, 63(1), 27-37.

Heimpel, G. E., & Mills, N. J. (2017). Biological control. Cambridge University Press.

Hepler, J. R., Athey, K., Enicks, D., Abram, P. K., Gariepy, T. D., Talamas, E. J., & Beers, E. (2020). Hidden host mortality from an introduced parasitoid: Conventional and molecular evaluation of non-target risk. Insects, 11(11), 822.

Hrček, J., & Godfray, H. C. J. (2015). What do molecular methods bring to host-parasitoid food webs? Trends in Parasitology, 31(1), 30-35. https://doi.org/10.1016/j.pt.2014.10.008

Jeffs, C. T., Terry, J. C. D., Higgie, M., Jandová, A., Konvičková, H., Brown, J. J., Lue, C.-H., Schiffer, M., O'Brien, E. K., Bridle, J., Hrček, J., & Lewis, O. T. (2021). Molecular analyses reveal consistent food web structure with elevation in rainforest Drosophila - Parasitoid communities. Ecography, 44(3), 403-413. https://doi.org/10.1111/ecog.05390

Ji, Y., Ashton, L., Pedley, S. M., Edwards, D. P., Tang, Y., Nakamura, A., Kitching, R., Dolman, P. M., Woodcock, P., Edwards, F. A., Larsen, T. H., Hsu, W. W., Benedick, S., Hamer, K. C., Wilcove, D. S., Bruce, C., Wang, X., Levi, T., Lott, M., … Yu, D. W. (2013). Reliable, verifiable, and efficient monitoring of biodiversity via metabarcoding. Ecology Letters, 16, 1245-1527. https://doi.org/10.1111/ele.12162

Kaser, J. M., & Ode, P. J. (2016). Hidden risks and benefits of natural enemy-mediated indirect effects. Current Opinion in Insect Science, 14, 105-111.

Kennedy, S. R., Prost, S., Overcast, I., Rominger, A. J., Gillespie, R. G., & Krehenwinkel, H. (2020). High-throughput sequencing for community analysis: The promise of DNA barcoding to uncover diversity, relatedness, abundances, and interactions in spider communities. Development Genes and Evolution, 230, 185-201.

Kitson, J. J. N., Hahn, C., Sands, R. J., Straw, N. A., Evans, D. M., & Lunt, D. J. (2018). Detecting host-parasitoid interactions in an invasive Lepidopteran using nesting tagging DNA metabarcoding. Molecular Ecology, 28(2), 471-483. https://doi.org/10.1111/mec.14518

Konopka, J. K., Haye, T., Gariepy, T., Mason, P., Gillespie, D., & McNeil, J. N. (2017). An exotic parasitoid provides an invasional lifeline for native parasitoids. Ecology and Evolution, 7(1), 277-284.

Krehenwinkel, H., Pomerantz, A., Henferson, J. B., Kennedy, S. R., Lim, J. Y., Swamy, V., Shoobridge, J. D., Graham, N., Patel, N. H., Gillespie, R. G., & Prost, S. (2019). Nanopore sequencing of long ribosomal DNA amplicons enables portable and simple biodiversity assessments with high phylogenetic resolution across broad taxonomic scale. GigaScience, 8, giz006. https://doi.org/10.1093/gigascience/giz006

La Salle, J., & Gauld, I. (1991). Parasitic Hymenoptera and the biodiversity crisis. Redia, 74(3), 315-334.

Lee, J. C., Wang, X. G., Daane, K. M., Hoelmer, K. A., Isaacs, R., Sial, A. A., & Walton, V. M. (2019). Biological control of spotted-wing Drosophila (Diptera: Drosophilidae): Current and pending tactics. Journal of Integrated Pest Management, 10(1), 13. https://doi.org/10.1093/jipm/pmz012

Leung, K., Ras, E., Ferguson, K. B., Ariens, S., Babendreier, D., Bijma, P., Bourtzis, K., Brodeur, J., Bruins, M. A., Centurión, A., Chattington, S. R., Chinchilla-Ramírez, M., Dicke, M., Fatouros, N. E., González-Cabrera, J., TVM, G., Haye, T., Knapp, M., Koskinioti, P., … Pannebakker, B. A. (2020). Next-generation biological control: The need for integrating genetics and genomics. Biological Reviews, 95(6), 1838-1854. https://doi.org/10.1111/brv.12641

Liu, M., Clarke, L. J., Baker, S. C., Jordan, G. J., & Burridge, C. P. (2020). A practical guide to DNA metabarcoding for entomological ecologists. Ecological Entomology, 45, 373-385.

Louda, S. M., Pemberton, R. W., Johnson, M. T., & Follett, P. (2003). Nontarget effects-the Achilles' heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annual Review of Entomology, 48(1), 365-396.

Lue, C.-H., Buffington, M. L., Scheffer, S., Lewis, M., Elliott, T. A., Lindsey, A., Driskell, A., Jandova, A., Kimura, M. T., Carton, Y., Kula, R. R., Schlenke, T. A., Mateos, M., Govind, S., Varaldi, J., Guerrieri, E., Giorgini, M., Wang, X., Hoelmer, K., … Hrcek, J. (2021). DROP: Molecular voucher database for identification of Drosophila parasitoids. Molecular Ecology Resources, 21(7), 2437-2454. https://doi.org/10.1111/1755-0998.13435

Mason, P. G., De Clerck-Floate, R. A., Gallant, B., Gillespie, D. R., Floate, K., Bourchier, R., Douglas, H., Vincent, C., & Boivin, G. (2017). Guide for the First-Time Importation and Release of Arthropod Biological Control Agents in Canada. Agriculture and Agri-Food Canada, Biological Control Working Group. http://www.publications.gc.ca/pub?id=9.843006&sl=0

Mata, V. A., da Silva, L. P., Veríssimo, J., Horta, P., Raposeira, H., McCracken, G. F., Rebelo, H., & Beja, P. (2021). Combining DNA metabarcoding and ecological networks to inform conservation biocontrol by small vertebrate predators. Ecological Applications, 31, e02457.

Mazzi, D., Bravin, E., Meraner, M., Finger, R., & Kuske, S. (2017). Economic impact of the introduction and establishment of Drosophila suzukii on sweet cherry production in Switzerland. Insects, 8(1), 18. https://doi.org/10.3390/insects8010018

Meier, R., Blaimer, B. B., Buenaventura, E., Hartop, E., von Rintelen, T., Srivathsan, A., & Yeo, D. (2021). A re-analysis of the data in Sharkey et al.'s (2021) minimalist revision reveals that BINs do not deserve names, but BOLD Systems needs a stronger commitment to open science. Cladistics, 38(2), 264-275. https://doi.org/10.1111/cla.12489

Meusnier, I., Singer, G. A. C., Landry, J.-F., Hicket, D. A., Hebert, P. D. N., & Hajibabaei, M. (2008). A universal DNA mini-barcode for biodiversity analysis. BMC Genomics, 9, 214. https://doi.org/10.1186/1471-2164-9-214

Miall, J. H., Abram, P. K., Cappuccino, N., & Mason, P. G. (2014). Potential impact of the native hyperparasitoid Conura albifrons (Hymenoptera: Chalcididae) on the exotic biological control agent Diadromus pulchellus (Hymenoptera: Ichneumonidae). Biocontrol Science and Technology, 24(6), 611-624.

Miller, K. E., Polaszek, A., & Evans, D. M. (2021). A dearth of data: Fitting parasitoids into ecological networks. Trends in Parasitology, 37, 863-874.

Miller, S. E., Hausmann, A., Hallwachs, W., & Janzen, D. H. (2016). Advancing taxonomy and bioinventories with DNA barcodes. Philosophical Transactions of the Royal Society Biological Sciences, 371(1702), 20150339. https://doi.org/10.1098/rstb.2015.0339

Moran, V. C., & Hoffmann, J. H. (2015). The fourteen international symposia on biological control of weeds, 1969-2014: Delegates, demographics and inferences from the debate on non-target effects. Biological Control, 87, 23-31.

Nomano, F. Y., Kasuya, N., Matsuura, A., Suwito, A., Mitsui, H., Buffington, M. L., & Kimura, M. T. (2017). Genetic differentiation of Ganaspis brasiliensis (Hymenoptera: Figitidae) from East and Southeast Asia. Applied Entomology and Zoology, 52(3), 429-437. https://doi.org/10.1007/s13355-017-04930

Novkovic, B., Mitsui, H., Suwito, A., & Kimura, M. T. (2011). Taxonomy and phylogeny of Leptopilina species (Hymenoptera: Cynipoidea: Figitidae) attacking frugivorous drosophilid flies in Japan, with description of three new species. Entomological Science, 14(3), 333-346. https://doi.org/10.1111/j.1479-8298.2011.00459.x

Ollivier, M., Lesieur, V., Tavoillot, J., Bénetière, F., Tixier, M. S., & Martin, J. F. (2021). An innovative approach combining metabarcoding and ecological interaction networks for selecting candidate biological control agents. Journal of Applied Ecology, 58(12), 2866-2880. https://doi.org/10.1111/1365-2664.14016

Olmos, A., Boonham, N., Candresse, T., Gentit, P., Giovani, B., Kutnjak, D., Liefting, L., Maree, H. J., Minafra, A., Moreira, A., Nakhla, M. K., Petter, F., Ravnikar, M., Rodoni, B., Roenhorst, J. W., Rott, M., Ruiz-García, A. B., Santala, J., Stancanelli, G., … Massart, S. (2018). High-throughput sequencing technologies for plant pest diagnosis: Challenges and opportunities. Bulletin OEPP, 48(2), 219-224. https://doi.org/10.1111/epp.12472

Paynter, Q., Fowler, S. V., & Groenteman, R. (2018). Making weed biological control predictable, safer and more effective: Perspectives from New Zealand. BioControl, 63(3), 427-436.

Pinol, J., Senar, M. A., & Symondson, W. O. C. (2018). The choice of universal primers and the characteristics of the species mixture determine when DNA metabarcoding can be quantitative. Molecular Ecology, 28, 407-419. https://doi.org/10.1111/mec.14776

Piper, A. M., Batovska, J., Cogan, N. O. I., Weiss, J., Cunningham, J. P., Rodoni, B. C., & Blacket, M. J. (2019). Prospects and challenges of implementing DNA metabarcoding for high-throughput insect surveillance. GigaScience, 8(8), giz092. https://doi.org/10.1093/gigascience/giz092

Puppato, S., Grassi, A., Pedrazzoli, F., De Cristofaro, A., & Ioriatti, C. (2020). First report of Leptopilina japonica in Europe. Insects, 11(9), 611. https://doi.org/10.3390/insects11090611

Ratnasingham, S., & Hebert, P. D. N. (2013). A DNA-based registry for all animal species: The barcode index number (BIN) system. PLoS One, 8(7), e66213. https://doi.org/10.1371/journal.pone.0066213

Rosen, D. (1986). The role of taxonomy in effective biological control programs. Agriculture, Ecosystems & Environment, 15(2-3), 121-129.

Ruppert, K. M., Kline, R. J., & Rahman, M. S. (2019). Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: A systematic review in methods, monitoring, and applications of global eDNA. Global Ecology and Conservation, 17, e00547. https://doi.org/10.1016/j.gecco.2019.e00547

Schaffner, U., Hill, M., Dudley, T., & D'Antonio, C. (2020). Post-release monitoring in classical biological control of weeds: Assessing impact and testing pre-release hypotheses. Current Opinion in Insect Science, 38, 99-106.

Schmidt, J. M., Acebes-Doria, A., Blaauw, B., Kheirodin, A., Pandey, S., Lennon, K., Kaldor, A. D., Toledo, P. F. S., & Grabarczyk, E. E. (2021). Identifying molecular-based trophic interactions as a resource for advanced integrated pest management. Insects, 12(4), 358. https://doi.org/10.3390/insects12040358

Seehausen, M. L., Ris, N., Driss, L., Racca, A., Girod, P., Warot, S., Borowiec, N., Tosevski, I., & Kenis, M. (2020). Evidence for a cryptic parasitoid species reveals its suitability as a biological control agent. Scientific Reports, 10, 19096. https://doi.org/10.1038/s41598-020-76180-5

Servick, K. (2018). Control freaks. Science, 2018, 542-545.

Shokralla, S., Spall, J. L., Gibson, J. F., & Hajibabaei, M. (2012). Next-generation sequencing technologies for environmental DNA research. Molecular Ecology, 21, 1794-1805.

Sint, D., Sporleder, M., Wallinger, C., Zegarra, O., Oehm, J., Dangi, N., Giri, Y. P., Kroschel, J., & Traugott, M. T. (2016). A two-dimensional pooling approach towards efficient detection of parasitoid and pathogen DNA at low infestation rates. Methods in Ecology and Evolution, 7(12), 1548-1557. https://doi.org/10.1111/2041-210X.12621

Song, H., Buhay, J. E., Whiting, M. F., & Crandall, K. A. (2008). Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America, 105, 13486-13491. https://doi.org/10.1073/pnas.0803076105

Sow, A., Brevault, T., Benoit, L., Chapuis, M., Galan, M., Coeur d'acier, A., Delvare, G., Sembene, M., & Haran, J. (2019). Deciphering host-parasitoid interactions and parasitism rates of crop pests using DNA metabarcoding. Scientific Reports, 9, 3646. https://doi.org/10.1038/s41598-019-40243-z

Sow, A., Haran, J., Benoit, L., Galan, M., & Brévault, T. (2020). DNA metabarcoding as a tool for disentangling food webs in agroecosystems. Insects, 11(5), 294. https://doi.org/10.3390/insects11050294

Tedersoo, L., & Anslan, S. (2019). Towards PacBio-based pan-eukaryote metabarcoding using full-length ITS sequences. Environmental Microbiology Reposts, 11(5), 659-668. https://doi.org/10.1111/1758-2229.12776

Tedersoo, L., Tooming-Klunderud, A., & Anslan, S. (2018). PacBio metabarcoding of fungi and other eukaryotes: Errors, biases and perspectives. New Phytologist, 210, 1370-1385. https://doi.org/10.1111/nph.14776

Thomsen, P. F., Kielgast, J., Iversen, L. L., Wiuf, C., Rasmussen, M., Gilbert, M. T. P., Orlando, L., & Willerslev, E. (2012). Monitoring endangered freshwater biodiversity using environmental DNA. Molecular Ecology, 21, 2565-2573.

Toju, H., & Baba, Y. (2018). DNA metabarcoding of spiders, insects, and sprintails for exploring potential linkage between above-and below-ground good webs. Zoological Letters, 4(4), 4. https://doi.org/10.1186/s40851-018-0088-9

van Lenteren, J. C., Cock, M. J., Hoffmeister, T. S., & Sands, D. P. (2006). Host specificity in arthropod biological control, methods for testing and interpretation of the data. In F. Bigler, D. Babendreier, & U. Kuhlmann (Eds.), Environmental impact of invertebrates for biological control of arthropods: Methods and risk assessment (pp. 38-63). CABI Publishing.

Wang, X., Lee, J. C., Daane, K. M., Buffington, M. L., & Hoelmer, K. A. (2020). Biological control of Drosophila suzukii. CAB Reviews, 15, 054.

Weber, D. C., Hajek, A. E., Hoelmer, K. A., Schaffner, U., Mason, P. G., Stouthamer, R., Talamas, E. J., Buffington, M., Hoddle, M. S., & Haye, T. (2021). Unintentional biological control (Chapter 5). In P. G. Mason (Ed.), Biological control: Global impacts, challenges and future directions of pest management. CSIRO Publishing.

Wyckhuys, K. A., Lu, Y., Zhou, W., Cock, M. J., Naranjo, S. E., Fereti, A., Williams, F. E., & Furlong, M. J. (2020). Ecological pest control fortifies agricultural growth in Asia-Pacific economies. Nature Ecology & Evolution, 4(11), 1522-1530.

Ye, Z., Vollhardt, I. M. G., Girtler, S., Wallinger, C., Tomanovic, Z., & Traugott, M. (2017). An effective molecular approach for assessing cereal aphid-parasitoid-endosymbiont networks. Scientific Reports, 7(1), 3138. https://doi.org/10.1038/s41598-017-02226-w

Zenni, R. D., Essl, F., Garcia-Berthou, E., & McDermott, S. M. (2021). The economic costs of biological invasions around the world. NeoBiota, 67, 1-9. https://doi.org/10.3897/neobiota.67.69971