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Issue: Vol. 3 No. 2: 30 Apr. 2026
Type: Article
Published: 2026-04-30
DOI: 10.11646/jihs.3.2.6
Page range: 199-211
Abstract views: 24
PDF downloaded: 4

Remarkable Parasitism of Spartocera granulata Stål, 1870 (Hemiptera: Coreidae) by Hexacladia hilaris Burks, 1972 (Hymenoptera: Encyrtidae): a New Host Record from Costa Rica and an Updated Checklist of Encyrtid Parasitoids of Coreidae Worldwide

Universidad Estatal a Distancia (UNED), Alajuela, Costa Rica.
Heteroptera Spartocerini gregarious endoparasitoid parasitoid emergence nymphal stage Ipomoea

Abstract

Spartocera granulata Stål, 1870 (Coreidae) is documented here as a new host for the encyrtid wasp Hexacladia hilaris Burks, 1972. This finding is significant because H. hilaris is a gregarious endoparasitoid of true bugs (Heteroptera), and all previous host records for this species were exclusively from the family Pentatomidae. The emergence process of the parasitoid wasps is detailed and illustrated with figures and two videos, and information on the biological interactions of Hexacladia species in the Neotropical Region is discussed. In addition, an updated global checklist of leaf-footed bugs (Coreidae) as hosts of Encyrtidae is provided.

 

References

  1. Abudulai, M., B. M. Shepard, and P. L. Mitchell. 2001. Parasitism and predation on eggs of Leptoglossus phyllopus (L.) (Hemiptera: Coreidae) in Cowpea: Impact of endosulfan sprays. Journal of Agricultural and Urban Entomology18: 105–115.
  2. Baldin, E., R. Fujihara, Jr., A. Boica, and M. Almeida. 2010. Parasitismo de percevejos-praga do maracujazeiro no Brasil por Hexacladia smithii Ashmead (Hymenoptera: Encyrtidae). Neotropical Entomology 39: 306–307. https://doi.org/10.1590/S1519-566X2010000200025
  3. Barakat, M. C., D. A. Aquino, and M. F. Cingolani. 2022. Potential of Hexacladia smithii (Hymenoptera Encyrtidae) to parasitize Piezodorus guildinii (Hemiptera Pentatomidae) adults. Bulletin of Insectology 75: 177–182.
  4. Baranowski, R. M. and J. A. Slater. 1986. 12 Arthropods of Florida and Neighboring Land Areas: Coreidae of Florida (Hemiptera: Heteroptera). 1st ed. Florida Department of Agriculture and Consumer Services, Gainesville. 82 pp. https://doi.org/10.64338/fsca.af.12.hpn12
  5. Becker, M. and M. D. Prato. 1982. Natality and natural mortality of Spartocera lativentris Stål, 1870 (Heteroptera: Coreidae) in the egg stage. Anais da Sociedade Entomológica do Brasil 11: 269–281. https://doi.org/10.37486/0301-8059.v11i2.288
  6. Brailovsky, H. 2011. Insecta Hemiptera Heteroptera Coreidae. Faune de Madagascar 94. IRD, Éditions Quae, Publications scientifiques du Muséum, Paris et Marseille. 275 pp.
  7. Bruner, S. C., L. C. Scaramuzza, and A. R. Otero. 1946. Catálogo de los insectos que atacan a las plantas económicas de Cuba. Annals of the Entomological Society of America 39: 560–560. https://doi.org/10.1093/aesa/39.4.560
  8. Burgos-Dueñas, O., J. M. Coronado-Blanco, and A. Burgos-Solorio. 2023. Aportaciones sobre la biología de Hexacladia smithii Ashmead, parasitoide de Edessa conspersa Stål en Cerro Frío, Puente de Ixtla, Morelos, México. Southwestern Entomologist 48(3): 683–696. https://doi.org/10.3958/059.048.0320
  9. Burks, B. D. 1972. The genus Hexacladia Ashmead (Hymenoptera: Encyrtidae). Proceedings of the Entomological Society of Washington 74: 363–371.
  10. Cazorla, D. 2021. Coreidae (Hemiptera: Heteroptera) de Venezuela. Revista Nicaragüense de Entomología 246: 3–90. https://doi.org/10.5281/ZENODO.5453653
  11. Costa-Lima, A. 1930. Sobre insectos que viven em maracujás (Passiflora spp). Memorias do Instituto Oswaldo Cruz 23: 159–165. https://doi.org/10.1590/S0074-02761930000300003
  12. Cuda, J. P. and C. J. DeLoach. 1998. Biology of Mozena obtusa (Hemiptera: Coreidae), a candidate for the biological control of mesquite, Prosopis spp. (Fabaceae). Biological Control 13: 101–110. https://doi.org/10.1006/bcon.1998.0644
  13. Cuezzo. F. and P. Fidalgo. 1997. Hexacladia smithii Ashmead (Hymenoptera: Encytidae): A new record for Argentina and two new pentatomid hosts recorded, Antiteuchus variolosus Westwood and Edessa meditabunda F. (Hemiptera: Pentatomidae). The Entomologist 116: 11–14.
  14. De Santis, L. 1989. Catálogo de los Himenópteros Calcidoides (Hymenoptera) al sur de los Estados Unidos, segundo suplemento. Acta Entomólogica Chilena 15: 9–90.
  15. De Vol, J. E. and R. D. Goeden. 1973. Biology of Chelinidea vittiger with notes on its host-plant relationships and value in biological weed control. Environmental Entomology 2: 231–240. https://doi.org/10.1093/ee/2.2.231
  16. Fernandes, J. A. M., P. L Mitchell, L. Livermore, and M. Nikunlassi. 2015. Leaf-footed bugs (Coreidae), 549–605. In Panizzi, A. R, and J. Grazia, eds. True Bugs (Heteroptera) of the Neotropics. Springer Netherlands, Dordrecht. 902 pp. https://doi.org/10.1007/978-94-017-9861-7_19
  17. Grimm, C. and J. M. Maes. 1997. Insectos asociados al cultivo de tempate (Jatropha curcas) en el pacífico de Nicaragua. III Coreoidea (Heteroptera). Revista Nicaragüense de Entomología 42: 16–34.
  18. Huang, D. and J. S. Noyes. 1994. A revision of the Indo-Pacific species of Ooencyrtus (Hymenoptera: Encyrtidae), parasitoids of the immature stages of economically important insect species (mainly Hemiptera and Lepidoptera). Bulletin of the Natural History Museum 63: 1–136.
  19. Isagawa, K., T. Inoue, Y. Taguchi, S. Kagawa, K. Kadota, R. Makino, and H. Higuchi. 2022. Parasitoid species parasitizing the eggs of Cletus punctiger (Hemiptera: Coreidae) and seasonal changes in percentage parasitism. Annual Report of The Kansai Plant Protection Society 64: 1–6. https://doi.org/10.4165/kapps.64.1
  20. Japoshvili, G. O. and J. S. Noyes. 2006. New data on the European fauna of encyrtid wasps (Hymenoptera, Chalcidoidea, Encyrtidae). Entomological Review 86: 298–304. https://doi.org/10.1134/S0013873806030067
  21. Laraichi, M. 1979. Contribution to the specificity of parasitism in Ooencyrtus (Hymenoptera, Encyrtidae). Bulletin Section Regionale Ouest Palaearctique, Organisation Internationale de Lutte Biologique 11: 87–92.
  22. Lesieur, V. and A. O. Farinha. 2021. Responses of native egg parasitoids to the invasive seed bug Leptoglossus occidentalis. Agricultural and Forest Entomology 23: 323–333. https://doi.org/10.1111/afe.12434
  23. Maltese, M., V. Caleca, E. Guerrieri, and W. B. Strong. 2012. Parasitoids of Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) recovered in western North America and first record of its egg parasitoid Gryon pennsylvanicum (Ashmead) (Hymenoptera: Platygastridae) in California. The Pan-Pacific Entomologist 88: 347–355. https://doi.org/10.3956/2012-23.1
  24. Marsaro-Júnior, A. L., V. A. Costa, and A. R. Panizzi. 2020. First record of Hexacladia hilaris Burks (Hymenoptera: Encyrtidae) in Brazil and association with Chinavia erythrocnemis (Berg) (Heteroptera: Pentatomidae). EntomoBrasilis 13: e927, 1–4. https://doi.org/10.12741/ebrasilis.v13.e927
  25. Matteson, P. C. 1981. Egg parasitoids of hemipteran pests of cowpea in Nigeria and Tanzania, with special reference to Ooencyrtus patriciae Subba Rao (Hymenoptera: Encyrtidae) attacking Clavigralla tomentosicollis Stål (Hemiptera: Coreidae). Bulletin of Entomological Research 71: 547–554. https://doi.org/10.1017/S0007485300010063
  26. Nechols, J. R., J. L. Tracy, and E. A. Vogt. 1989. Comparative ecological studies of indigenous egg parasitoids (Hymenoptera: Scelionidae; Encyrtidae) of the squash bug, Anasa tristis (Hemiptera: Coreidae). Journal of the Kansas Entomological Society 62: 177–188.
  27. Noyes, J. S. and M. Hayat. 1994. Oriental mealybug parasitoids of the Anagyrini (Hymenoptera: Encyrtidae). CAB International, London. viii+554 pp.
  28. Noyes, J. S. 2010. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 3. Subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera, Neuroptera) and ticks (Acari). Memoirs of the American Entomological Institute 84: 1–848.
  29. Noyes, J. S. 2023. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 4 Subfamily Encyrtinae: tribes Arrhenophagini, Habrolepidini, Cerapterocerini, Cheiloneurini, Trechnitini, Cercobelini, Polaszekiini, Protyndarichoidini, Gahaniellini and Syrphophagini (part), mainly primary parasitoids and hyperparasitoids of Coccoidea and Psylloidea (Hemiptera). Taxonomic Monographs on Neotropical Hymenoptera 2: 1–921. https://doi.org/10.5281/ZENODO.8074943
  30. Noyes, J. S. 2024. Universal Chalcidoidea Database. Universal Chalcidoidea Database. World Wide Web electronic publication. http://www.nhm.ac.uk/chalcidoids [last accessed July 11, 2024].
  31. Oğuzoğlu, Ş. and M. Avci. 2020. Türkiye’de Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Coreidae) üzerine biyolojik gözlemler, parazitoitleri ve yayılışına katkılar. Ormancılık Araştırma Dergisi 7: 9–21. https://doi.org/10.17568/ogmoad.548950
  32. Oswald, S. 1990. Possibilities for the use of Ooencyrtus albicrus (Prinsloo) (Hym., Encyrtidae) in an integrated pest management approach against the coconut bug Pseudotheraptus wayi Brown (Hem., Coreidae) in Zanzibar. Journal of Applied Entomology 110: 198–202. https://doi.org/10.1111/j.1439-0418.1990.tb00113.x
  33. Paz-Neto, A. D. A., R. B. Querino, and C. B. Margaría. 2015. Egg parasitoids of stink bugs (Hemiptera: Coreidae and Pentatomidae) on soybean and cowpea in Brazil. Florida Entomologist 98: 929–932. https://doi.org/10.1653/024.098.0318
  34. Peck, O. 1963. A Catalogue of the Nearctic Chalcidoidea (Insecta: Hymenoptera). Memoirs of the Entomological Society of Canada 95: 5–1092. https://doi.org/10.4039/entm9530fv
  35. Phillips, J. S. 1941. A search for parasites of dasynine bugs in the Netherlands Indies. Transactions of the Royal Entomological Society of London 91: 119–144. https://doi.org/10.1111/j.1365-2311.1941.tb00257.x
  36. Ponce‐Herrero, L., A. O. Farinha, V. Pando Fernández, J. A. Pajares Alonso, and F. M. Alves Santos. 2022. Native egg parasitoids on Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae) in Spain: Potential biological control agents? Journal of Applied Entomology 146: 525–538. https://doi.org/10.1111/jen.12974
  37. Prinsloo, G. L. 1987. A revision of the genus Ooencyrtus Ashmead (Hymenoptera: Encyrtidae) in sub-saharan Africa. Entomology Memoir, Department of Agriculture and Water Supply, Republic of South Africa 67: 1–46.
  38. Rajadurai, S. 1989. Energy transfer efficiency in three hymenopteran egg parasitoids of Homoeocerus prominulus Tagus (Insecta, Heteroptera, Coreidae). Proceedings of the Indian Academy of Sciences (Animal Sciences) 98: 181–186. https://doi.org/10.1007/BF03179643
  39. Ramos-Santiago, M. P., A. Quevedo-Guerrero, and M. G. Velázquez-Silvestre. 2025. Primer registro de avispas parasitoides de huevos de Sagotylus confluens (Say, 1832) (Hemiptera: Coreidae) encontradas en Veracruz, México. Avances en Investigación Agropecuaria 29: 72–81. https://doi.org/10.53897/RevAIA.25.29.05
  40. Rasplus, J. Y., D. Pluot-sigwalt, J. F. Llosa, and G. Couturier. 1990. Hexacladia linci, N. SP. (Hymenoptera: Encyrtidae) endoparasite de Lincus malevolus Rolston (Heteroptera: Pentatomidae) au Pérou. Annales de la Société entomologique de France (N.S.) 26: 255–263. https://doi.org/10.1080/21686351.1990.12277664
  41. Roversi, P. F. 1988. Alternative hosts of Ooencyrtus pityocampae (Mercet) (Hymenoptera Encyrtidae) in Italy. Redia 71: 321–328.
  42. Santos, R. S. S., L. R. Redaelli, and L. M. G. Diefenbach. 2001. Ocorrência de parasitismo em ovos de Spartocera dentiventris (Berg) (Hemiptera: Coreidae) em cultura de fumo. Neotropical Entomology 30: 731–733. https://doi.org/10.1590/S1519-566X2001000400033
  43. Schaefer, C. W. and A. R. Panizzi. 2000. Heteroptera of Economic Importance. CRC Press LLC, Boca Raton. 828 pp. https://doi.org/10.1201/9781420041859
  44. Sousa, K. K., N. N. Silva, R. B. Querino, P. H. Silva, and J. Grazia. 2019. Diversity, seasonality, and egg parasitism of hemipteran (Coreidae and Pentatomidae) from a cowpea crop in northeastern Brazil. Florida Entomologist 102(1): 29–35. https://doi.org/10.1653/024.102.0105
  45. Stål, C. 1870. Enumeratio Hemipterorum. Hemiptera, Jemte Systematiska Meddlanden. Svenska Vetenskaps-Akademiens Handlingar 9: 1–232.
  46. Steinbauer, M. J. and A. R. Clarke. 1995. Xenoencyrtus hemipterus (Girault) (Hymenoptera: Encyrtidae), an egg parasitoid of Coreidae (Hemiptera) in Tasmania. Journal of the Australian Entomological Society 34: 63–64. https://doi.org/10.1111/j.1440-6055.1995.tb01280.x
  47. Takasu, K. and Y. Hirose. 1986. Kudzu-vine community as a breeding site of Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae), an egg parasitoid of bugs attacking soybean. Japanese Journal of Applied Entomology and Zoology 30: 302–304. https://doi.org/10.1303/jjaez.30.302
  48. Tracy, J. L. and J. R. Nechols. 1987. Comparisons between the squash bug egg parasitoids Ooencyrtus anasae and O. sp. (Hymenoptera: Encyrtidae): Development~ survival~and sex ratio in relation to temperature. Environmental Entomology 16: 1324–1329. https://doi.org/10.1093/ee/16.6.1324
  49. Trjapitzin, V. A. 1979. A new species of the genus Ooencyrtus Ashmead, 1900 (Hymenoptera, Encyrtidae) - a parasite in the eggs of the sorrel bug Coreus marginatus L. (Hemiptera, Coreidae) in Moldavia. Trudy Vsesoyuznogo Entomologicheskogo Obshchestva 61: 160–161.
  50. Trjapitzin, V. A., F. D. Bennett, E. Ruíz-Cancino, and J. M. Coronado-Blanco. 2004. Annotated check-list of encyrtids (Hymenoptera: Chalcidoidea: Encyrtidae) of Central America, the West Indies and Bermuda. First edition. Prograf, Imprenta y Diseño, Ciudad Victoria. 207 pp.
  51. Trjapitzin, V. A., S. N. Myartseva, E. Ruíz-Cancino, and J. M. Coronado-Blanco. 2008. Clave de géneros de Encyrtidae (Hymenoptera: Chalcidoidea) de México y un catálogo de las especies. Primera edición. Editorial Planea, Ciudad Victoria. 266 pp.
  52. Viggiani, G. 1971. Ricerche sugli Hymenoptera Chalcidoidea. XXXI. Descrizioni di Ooencyrtus gonoceri n.sp., parasita oofago del coreide Gonocerus acuteangulatus (Goeze), con notizie biologiche. Bollettino del Laboratorio di Entomologia Agraria “Filippo Silvestri”, Portici 29: 315–325.
  53. Zhang, Y. Z., W. Li, and D. W. Huang. 2005. A taxonomic study of Chinese species of Ooencyrtus (Insecta: Hymenoptera: Encyrtidae). Zoological Studies 44: 347–360.
  54. Zachrisson, B. A., J. Grazia, V. A. Costa, and G. Gutierrez. 2024. Hexacladia smithii Ashmead, 1891 (Hymenoptera: Encyrtidae) in Panama: first record and new association with Berecynthus hastator (Fabricius, 1798) (Hemiptera: Pentatomidae). Brazilian Journal of Biology 84: e263185, 1–3. https://doi.org/10.1590/1519-6984.263185