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Issue: Vol. 5725 No. 3: 3 Dec. 2025
Type: Article
Published: 2025-12-03
DOI: 10.11646/zootaxa.5725.3.1
Page range: 301-340
Abstract views: 63
PDF downloaded: 2

DNA Barcoding of west European Strachiini questions the validity of several species of the genus Eurydema (Hemiptera. Heteroptera: Pentatomidae)

CBGP; INRAE; CIRAD; IRD; Institut Agro; Univ Montpellier; Montpellier; France
CBGP; INRAE; CIRAD; IRD; Institut Agro; Univ Montpellier; Montpellier; France
CEFE; PSL-EPHE (Biogéographie et Ecologie des Vertébrés); CNRS; Univ. Montpellier; Univ. Paul Valéry Montpellier 3; IRD; Montpellier; France
CBGP; INRAE; CIRAD; IRD; Institut Agro; Univ Montpellier; Montpellier; France
Hemiptera Strachiini Eurydema DNA barcoding

Abstract

The pentatomid tribe Strachiini includes numerous crop pests, notably the genus Eurydema Laporte, 1833, which comprises Palaearctic species feeding on cruciferous plants. In a context of reduced pesticide use and increased biological invasions, the damage caused by Strachiini to European crops has increased over the past few years. Rapid identification of these pests at all stages of their development is therefore becoming crucial. In this context, we investigated whether DNA barcoding can reliably distinguish all developmental stages of Western European Strachiini species and invasive congeners. We analysed 325 specimens collected worldwide, using both newly generated in-home and publicly available COI sequences. Species boundaries were assessed through distance-based and phylogenetic tree-based methods, including Neighbor-Joining (NJ) and Maximum Likelihood (ML). Morphological identification of Strachiini was generally consistent and reached a consensus, except for a few challenging species pairs such as Eurydema fieberi Schummel, 1837 / E. rotundicollis (Dohrn, 1860) and Eurydema spectabilis Horváth, 1882 / E. eckerleini Josifov, 1961. We therefore used as reference material in this study, specimens preserved in institutional or private collections, consensually identified by several generations of specialists. Our results confirms that Eurydema species of agronomic importance and their related invasive congeners can be reliably identified through DNA barcoding except for several species within the large genus Eurydema, for which discrepancies between morphological and molecular identifications were highlighted. A curated set of validated sequences has been deposited in the BOLD Systems (https://id.boldsystems.org/), GenBank, NCBI (https://www.ncbi.nlm.nih.gov/) and ARTHEMIS databases (https://arthemisdb.supagro.inrae.fr/) to support accurate molecular identification. The taxonomic issues highlighted in the large genus Eurydema are discussed. They will require further investigation and may lead to necessary taxonomic revisions, hence, some of these (e.g. involving the widespread pest species E. ornata) could have agronomic implications.

 

References

  1. Ahmad, T. & Akhtar, N. (2015) Taxonomy and biological observations on two Pentatomid pests Dolycoris indicus Stål and Eurydema pulchrum Westwood attacking agricultural crops in Kashmir valley. International Journal of Entomological Research, 3 ( 2), 55–59.
  2. Akhter, N., Ahmad, S.T. & Azim, M.N. (2015) On the biology of agriculturally important pentatomid pests Dolycoris indicus Stål and Eurydema pulchrum Westwood (Hemiptera: Pentatomidae). New York Science Journal, 8 (2), 89–91.
  3. Aukema, B. (Ed.) (2025) Catalogue of the Palaearctic Heteroptera. Naturalis Biodiversity Center. Available from: https://catpalhet.linnaeus.naturalis.nl (accessed 18 April 2025)
  4. Aukema, B., Rieger, C. & Rabitsch, W. (2013) Catalogue of the Heteroptera of the Palearctic Region. Volume 6. Supplement. The Netherlands Entomological Society, Amsterdam, xxiv + 629 pp.
  5. Balachowsky, A. & Mesnil, L. (1936) Les insectes nuisibles aux plantes cultivées. Leurs moeurs. Leur destruction‎. Ed Busson, Paris, France, 1921 pp.
  6. Bergsten, J., Bilton, D.T., Fujisawa, T., Elliot, M., Monaghan, M.T., Balke, M., Hendrich, L., Geijer, J., Herrmann, J., Foster, G.N., Ribera, I., Nilsson, A.N., Barraclough, T.G. & Vogler, A.P. (2012) The Effect of Geographical Scale of Sampling on DNA Barcoding. Systematic Biology, 61 (5), 851–869. https://doi.org/10.1093/sysbio/sys037
  7. Blaxter, M.L. (2004) The promise of a DNA taxonomy. Philosophical Transaction of the Royal Society of London B, 359, 669–679. https://doi.org/10.1098/rstb.2003.1447
  8. Bonnemaison, L. (1952) Morphologie et biologie de la punaise ornée du chou (Eurydema ventralis Kol.). Annales des Epiphyties II, 1952, 127–172.
  9. Breeschoten, T., Doorenweerd, C., Tarasov, S. & Vogler, A.P. (2016) Phylogenetics and biogeography of the dung beetle genus Onthophagus inferred from mitochondrial genomes. Molecular Phylogenetics and Evolution, 105, 86–95. https://doi.org/10.1016/j.ympev.2016.08.016
  10. Bundy, C.S., Perring, T.M., Reed, D.A., Palumbo, J.C., Grasswitz, T.R. & Jones, W.A. (2018) Chapitre 3. Bagrada hilaris (Burmeiter). In: Mc Pherson, J.E. (Ed.), Invasive Stink Bugs and Related Species (Pentatomidae). CRC Press, Boca Raton, Florida, pp. 205–241. https://doi.org/10.1201/9781315371221-3
  11. Cruaud, A., Jabbour-Zahab, R., Genson, G., Kjellberg, F., Kobmoo, N., van Noort, S., Yang, D.-R., Peng, Y.-Q., P., Ubaidillah, R., Hanson, P.E., Santos-Mattos, O., Farache, F.H., Pereira, R.A., Kerdelhué, C. & Rasplus, J.-Y. (2011) Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea). BMC Ecology and Evolution, 11, 178. https://doi.org/10.1186/1471-2148-11-178
  12. Cruaud, P., Rasplus, J.-Y., Rodriguez, L.J. & Cruaud, A. (2017) High-throughput sequencing of multiple amplicons for barcoding and integrative taxonomy. Scientific Reports, 7, 1–12. https://doi.org/10.1038/srep41948
  13. Derjanschi, V. & Pericart, J. (2005) Faune de France 90. Hémiptère Pentatomoidea Euro-Méditerranéens. Vol. 1. Fédération française des sociétés de sciences naturelles, Paris, 494 pp.
  14. Doorenweerd, C., Leblanc, L., Hsu, Y.-F., Huang, C.-L., Lin, Y.-C., Jose, M.S. & Rubinoff, D. (2019) Taiwan’s Dacini Fruit Flies: Rare Endemics and Abundant Pests, along Altitudinal Gradients. Pacific Science, 73, 35. https://doi.org/10.2984/73.1.3
  15. Doorenweerd, C., Jose, M.S., Leblanc, L., Barr, N., Geib, S., Chung, A.Y.C., Dupuis, J., Ekayanti, A., Fiegalan, E.R., Hemachandra, K.S., Hossain, M.A., Huang, C.-L., Hsu, Y.-F., Morris, K.Y., Mustapeng, A.M., Niogret, J., Pham, T.H. & Sirisena, U.G.A.I., Rubinoff, D. (2020) DNA barcodes and reliable molecular identifications in a diverse group of invasive pests: lessons from Bactrocera fruit flies on variation across the COI gene, introgression, and standardization. BioRxiv. [published online] https://doi.org/10.1101/2020.11.23.394510
  16. Doorenweerd, C., San Jose, M., Leblanc, L. & Rubinoff, D. (2023) Inadequate molecular identification protocols for invasive pests threaten biosecurity. Systematic Entomology, 48 (3), 355–360. https://doi.org/10.1111/syen.12581
  17. Dupuis, C. (1951) Les espèces françaises du genre Eurydema Laporte (Hemiptera Pentatomoidea, subfam. Pentatominae). Révision systématique avec une introduction à l’étude morphologique des organes génitaux externe des Pentatomoidea. Annales de la Société Entomologique de France, 118, 1–28. https://doi.org/10.1080/21686351.1949.12279040
  18. Dupuis, C. (1959) Notes, remarques et observations diverses sur les Hémiptères. Quatrième série: Note XI- Les processus supérieurs de la chambre génitale mâle des Pentatomoidea. Cahiers des Naturalistes Parisiens, Bulletin des Naturalistes Parisiens, 15, 46–51.
  19. Hebert, P.D.N., Cywinska, A., Ball, S.L. & Dewaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B, 270, 313–321. https://doi.org/10.1098/rspb.2002.2218
  20. Jia, W., Chen, J., Ge, S., Zhang, Z., Xiao, Y., Qi, L., Zhao, Q. & Zhang, H. (2024) Phylogenetic and divergence analysis of Pentatomidae, with a comparison of the mitochondrial genomes of two related species (Hemiptera, Pentatomidae). PLoS ONE, 19 (10), e0309589. https://doi.org/10.1371/journal.pone.0309589
  21. Jung, S., Kerzhner, I.M. & Lee, S. (2011) Species of the genus Eurydema (Hemiptera: Heteroptera: Pentatomidae) in Far East Asia: an integrated approach using morphological, molecular, and data crossing analyses for taxonomy. Zootaxa, 2917 (1), 48–58. https://doi.org/10.11646/zootaxa.2917.1.3
  22. Kment, P. & Jindra, Z. (2008) New records of Eurydema fieberi from the Czech Republic with corrections to some previously published records of Palaearctic Eurydema species (Hemiptera: Heteroptera: Pentatomidae). Acta Musei Moraviae, Scientiae Biologicae, 93, 11–27.
  23. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) Phylogenetic and molecular evolutionary analyses were conducted using MEGA version X. Molecular biology and evolution, 35 (6), 1547–1549. https://doi.org/10.1093/molbev/msy096
  24. Lian, D., Wei, J., Chen, C., Niu, M., Zhang, H. & Zhao, Q. (2022) Comparative analysis and phylogeny of mitochondrial genomes of Pentatomidae (Hemiptera: Pentatomoidea). Frontiers in Genetics, 13, 1045193. https://doi.org/10.3389/fgene.2022.1045193
  25. Linnaeus, C. (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio Decima, Reformata. Impensis Direct. Laurentii Salvii, Holmiæ [Stockholm], iv + 824 pp. https://doi.org/10.5962/bhl.title.542
  26. Lupoli, R. (1997) Notes sur quelques punaises peu connues (Heteroptera, Pentatomidae, Eurydemini et Podopinae) rencontrées sur les Crucifères. Entomologiste, 53 (2), 87–91.
  27. Lupoli, R. & Dusoulier, F. (2015) Les punaises Pentatomoidea de France. Ancyrosoma, Fontenay-sous-bois, 429 pp.
  28. Martel, G. (2021) Évaluation en laboratoire du parasitoïde Gryon gonikopalense (Hym. Scelionidae) pour le contrôle biologique de Bagrada hilaris (Hem. Pentatomidae), une punaise invasive aux États-Unis. Microbiologie et Parasitologie. Montpellier SupAgro, 2021. [Français. NNT: 2021NSAM0023. tel-04051698, unknown pagination]
  29. Mc Pherson, J.E., Bundy, C.S. & Kuhar, T.P. (2018) Chapitre 6. Murgantia histrionica (Hahn). In: Mc Pherson, J.E. (Ed.), Invasive Stink Bugs and Related Species (Pentatomidae). CRC Press, Boca Raton, Florida, pp. 333–349. https://doi.org/10.1201/9781315371221-6
  30. Michalk, O. (1939) Über Färbungswandlungen einiger Heteropteren, Eurydema ornatum L. und E. oleraceum L. – Bericht der VII. Intern. Kongr. Ent., Berlin, II (1938), 1243–1276.
  31. Michalk, O. (1950) Über dir Färbungswandlungen, Generations- und Fortpflanzungsverhältnisse der mitteleuropäischen Eurydema-Arten (II. Beitrag). Proceedings Eighth International Congress of Entomologie, Stockholm, 1950, 240–254.
  32. Michalk, O. (1955) Der jetzige Stand unseres Wissens über die Färbungswandlungen der Eurydema-Arten. Bericht über der 7. Wanderversammlung Deutscher Entomologen 8 bis 10 September 1954 in Berlin, 1955, 121–133.
  33. Musolin, D. (2012) Surviving winter: diapause syndrome in the southern green stink bug Nezara viridula in the laboratory, in the field, and under climate change conditions. Physiological Entomology, 37, 309–322. https://doi.org/10.1111/j.1365-3032.2012.00846.x
  34. Nicolas, V., Carapezza, A., Rider, D.A. & Kment, P. (2024) New records, diagnostics and preliminary checklist of the superfamily Pentatomoidea (Hemiptera: Heteroptera) from the Comoro Islands. Zootaxa, 5481 (1), 1–29. https://doi.org/10.11646/zootaxa.5481.1.1
  35. Nylander, J.A., Ronquist, F., Huelsenbeck, J.P. & Nieves-Aldrey, J.L. (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology, 53 (1), 47–67. https://doi.org/10.1080/10635150490264699
  36. Paddock, F.B. (1918) Studies on the harlequin bug. Texas Agricultural Experimental Station Bulletin, 227, 1–65.
  37. Palumbo, J.C. & Natwick, E.T. (2010) The Bagrada bug (Hemiptera: Pentatomidae): A new invasive pest of cole crops in Arizona and California. Online. Plant Health Progress. Available from: https://www.ndsu.edu/pubweb/~rider/Pentatomoidea/index.htm (accessed 20 October 2025) https://doi.org/10.1094/PHP-2010-0621-01-BR
  38. Panizzi, A.R. & Grazia, J. (2015) True Bugs (Heteroptera) of the Neotropics. Springer, Dordrecht, 902 pp. https://doi.org/10.1007/978-94-017-9861-7
  39. Phillips, J.D., Gillis, D.J. & Hanner, R.H. (2019) Incomplete estimates of genetic diversity within species: Implications for DNA barcoding. Ecology and Evolution, 9, 2996–3010. https://doi.org/10.1002/ece3.4757
  40. Pohjoismaki, J.L.O., Kahaanpaa, J. & Mutanen, M. (2016) DNA Barcodes for the Northern European Tachinid Flies (Diptera: Tachinidae). PLoS One, 11 (11). https://doi.org/10.1371/journal.pone.0164933
  41. Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
  42. Putshkov, V.G. (1961) Plant bugs (Heteroptera, Miridae) from Poltavsk Region. Pratsi Institutu Zoologii, Kiev, 17, 71–85.
  43. Raupach, M.J., Hendrich, L., Kuchler, S.M., Deister, F., Morinière, J. & Gossner, M.M. (2014) Building-up of a DNA barcode library for true bugs (Insecta: Hemiptera: Heteroptera) of Germany reveals taxonomic uncertainties and surprises. PLoS One, 9 (9), e106940. https://doi.org/10.1371/journal.pone.0106940
  44. Reymonet, C. & Lupoli, R. (2017) Hybridation interspécifique naturelle viable entre Eurydema oleracea (L., 1758) et E. ornata (L., 1758) (Hemiptera Pentatomidae). L’Entomologiste, 73 (4), 225–233.
  45. Rider, D.A. (2006) Family pentatomidae Leach, 1815, pp. 233–402. In: Aukema, B. & Rieger, C.H. (Eds.), Catalogue of the Heteroptera of the Palaearctic region. Vol. 5. Pentatomomorpha II. The Netherlands Entomological Society, Amsterdam, the Netherlands, pp. 364–374.
  46. Rider, D. (2015) Pentatomoidea Home page. Available from: https://www.ndsu.edu/pubweb/~rider/Pentatomoidea/index.htm (accessed May 2023)
  47. Rider, D.A., Schwertner, C.F., Vilímová, J., Rédei, D., Kment, P. & Thomas, D.B. (2018) Higher Systematics of the Pentatomoidea. In: McPherson, J.E. (Ed.), Invasive Stink Bugs and Related Species (Pentatomoidea): Biology, Higher Systematics, Semiochemistry, and Management. CRC Press, Taylor & Francis Group, Boca Raton, London and New York, pp. 25–201. https://doi.org/10.1201/9781315371221-2
  48. Sannier, D. (2019) Une nouvelle espèce de punaise découverte en France dans le département des Pyrénées-Orientales: Eurydema (Eurydema) sea Péricart & De la Rosa, 2004 (Hemiptera, Pentatomidae). Les cahiers de la fondation d’entreprise pour la Biodiversité. Biotope, 30, 1–16.
  49. Schaefer, C.W. & Panizzi, A.R. (2000) Heteroptera of economic importance. CRC Press, Boca Raton, 828 pp. https://doi.org/10.1201/9781420041859
  50. Schlee, M.A. (1986) Avian Predation on Heteroptera: Experiments on the European Blackbird Turdus m. merula L. Ethology, 73, 1–18. https://doi.org/10.1111/j.1439-0310.1986.tb00995.x
  51. Sforza, R.F.H., Bon, M.C., Martel, G., Augé, M., Roche, M., Mahmood, R. & Smith, L. (2017) Initial Evaluation of Two Native Egg Parasitoids for the Control of Bagrada hilaris, an Invasive Stink Bug in Western USA. In: Proceedings of the 5th International Symposium on Biological Control of Arthropods, Langkawi, Malaysia, 11–15 September 2017. CABI, Wallingford, Oxfordshire. [unknown pagination] https://doi.org/10.1079/9781786394118.0221
  52. Sinoglou, K.B. & Dioli, P. (2017) First report of caper (Capparis spinosa) serious infestation by Eurydema eckerleini in Cyclades Islands, Greece (Hemiptera: Heteroptera, Pentatomidae). Fragmenta Entomologica, 49 (1), 65–69. https://doi.org/10.4081/fe.2017.232
  53. Shokralla, S., Spall, J.L., Gibson, J.F. & Hajibabaei, M. (2012) Next-generation sequencing technologies for environmental DNA research. Molecular Ecology, 21, 1794–1805. https://doi.org/10.1111/j.1365-294X.2012.05538.x
  54. Shokralla, S., Porter, T.M., Gibson, J.F., Dobosz, R., Janzen, D.H., Hallwachs, W., Golding, G.B. & Hajibabaei, M. (2015) Massively parallel multiplex DNA sequencing for specimen identification using an Illumina MiSeq platform. Scientific Reports, 5, 9687. https://doi.org/10.1038/srep09687
  55. Stamatakis, A. (2006a) Phylogenetic models of rate heterogeneity: A High Performance Computing Perspective. International Parallel and Distributed Processing Symposium (IPDPS 2006), Rhodes Island, 8 pp. https://doi.org/10.1109/IPDPS.2006.1639535
  56. Stamatakis, A. (2006b) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
  57. Stankevych, S., Zabrodina, I., Yushchuk, D., Dolya, M., Balan, H., Yakovlev, R., Kosylovych, H., Holiachuk, Y., Zakharchuk, N., Galagan, T., Nemerytska, L., Zhuravska, I., Romanov, O., Romanova, T., Bragin, O., Hudym, O. & Hordiienko, I. (2021) Eurydema bugs: review of distribution, ecology, harmfulness, and control. Ukrainian Journal of Ecology, 11 (9), 131–149.
  58. Stichel, W. (1955–1962) Illustrierte Bestimmungstabellen der Wanzen. II. Europa. (Hemiptera – Heteroptera Europae). Vols. 1, 2, 3, & 4. Stichel, Berlin-Hermsdorf, 2284 pp. [Vol. 1: pp. 1–160 (1955) + 161–168 (1956), Vol. 2 169–480 (1956) + 481–704 (1957) + 705–907 (1958), Vol. 3: 1–32 (1958) + 33–192 (1959) + 193–428 (1960), Vol. 4: 1–96 (1957) + 97–224 (1958) + 225–384 (1959) + 385–544 (1960) + 545–768 (1961) + 769–838 (1962) + 1–111. General-Index (1962)]
  59. Streito, J.-C. & Bout, A. (2019) Punaises phytophages, quelle diversité sur nos cultures. Phytoma, 722, 53–56.
  60. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology Evolution, 30 (12), 2725–2729. https://doi.org/10.1093/molbev/mst197
  61. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25 (24), 4876–4882. https://doi.org/10.1093/nar/25.24.4876
  62. Velikova, V., Salerno, G., Frati, F., Peri, E., Conto, E., Colazza, S. & Loreto, F. (2010) Influence of Feeding and Oviposition by Phytophagous Pentatomids on Photosynthesis of Herbaceous Plants. Journal of Chemical Ecology, 36, 629–641. https://doi.org/10.1007/s10886-010-9801-7
  63. Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876. https://doi.org/10.1093/bioinformatics/btt499
  64. Zhao, W., Zhao, Q., Li, M., Wei, J., Zhang, X. & Zhang, H. (2017a) Characterization of the complete mitochondrial genome and phylogenetic implications for Eurydema maracandica (Hemiptera: Pentatomidae). Mitochondrial DNA, Part B, 2 (2), 550–551. https://doi.org/10.1080/23802359.2017.1365649
  65. Zhao, W., Zhao, Q., Li, M., Wei, J., Zhang, X. & Zhang, H. (2017b) DNA Barcoding of Chinese species of the genus Eurydema Laporte, 1833 (Hemiptera: Pentatomidae). Zootaxa, 4286 (2), 151–175. https://doi.org/10.11646/zootaxa.4286.2.1
  66. Zhao, W., Zhao, Q., Li, M., Wei, J., Zhang, X. & Zhang, H. (2019) Comparative Mitogenomic Analysis of the Eurydema Genus in the Context of Representative Pentatomidae (Hemiptera: Heteroptera) Taxa. Journal of Insect Science, 19, 20. https://doi.org/10.1093/jisesa/iez122

How to Cite

Genson, G., Pierre, Éric, Montgelard, C. & Streito, J.C. (2025) DNA Barcoding of west European Strachiini questions the validity of several species of the genus Eurydema (Hemiptera. Heteroptera: Pentatomidae). Zootaxa, 5725 (3), 301–340. https://doi.org/10.11646/zootaxa.5725.3.1