Integrative taxonomy to assess the species richness of chalcidoid parasitoids (Hymenoptera) associated to Bruchinae (Coleoptera: Chrysomelidae) from Mexico
DOI:
https://doi.org/10.22201/ib.20078706e.2020.91.3492Palabras clave:
Host-parasitoid association, Neotropics, Bean weevils, COI, TaxonomyResumen
Chalcidoidea are a highly diverse group of Hymenoptera and the most common parasitoids, being associated to more than 15 hexapod orders. The identification of species in this superfamily is considerably difficult due to their small size, lack of comprehensive taxonomic studies for many groups and convergence of morphological features. In
this study, we aimed to identify the chalcidoid species that are associated to bruchine beetles (Chrysomelidae) from central and southern Mexico, using morphological and molecular (mitochondrial COI gene) evidence. We report a total of 39 bruchine species associated to 8 plant taxa. The gathered morphological and molecular evidence allowed to delimit 29 chalcidoid species, 6 of which are new records for Mexico. We found inconsistencies in the species delimitation between the morphological and molecular data in species of Eupelmus (Eupelmidae) and Horismenus (Eulophidae). This study highlights the considerable species richness of chalcidoid taxa that are associated to bruchine beetles, and the need to provide reliable host records for members of this group of parasitoids.
Citas
Ács, Z., Challis, R., Bihari, P., Blaxter, M., Hayward, A., Melika, G., Csóka, G., Pénzes, Z., Pujade-Villar, J., Nieves-Aldrey, J.-L., Schönrogge, K., and Stone, G. N. (2010). Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera, Cynipidae) of the Western Palearctic. Molecular Phylogenetics and Evolution, 55, 210–225. https://doi.org/10.1016/j.ympev.2009.12.004
Al Khatib, F., Cruaud, A., Fusu, L., Genson, G., Rasplus, J. Y., Ris, N., and Delvare, G. (2016). Multilocus phylogeny and ecological differentiation of the “Eupelmus urozonus species group” (Hymenoptera, Eupelmidae) in the West-Palaearctic. BMC Evolutionary Biology, 16, 13. https://doi.org/10.1186/ s12862-015-0571-2
Boucek, Z. (1977). A faunistic review of the Yugoslavian Chalcidoidea (Parasitic Hymenoptera). Acta Entomologica Jugoslavica 13(Supplement), 63, 145 p.
Boucek, Z. (1991). Four new genera of European Pteromalidae (Hymenoptera), with some taxonomic changes. Bollettino di Zoologia Agraria e Bachicoltura- Milano, 22, 195-206.
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C. H., Xie, D., Suchard, M. A., Rambaut, A., and Drummond, A. J. (2014). BEAST 2, A Software Platform for Bayesian Evolutionary Analysis. PLoS Computational Biology, 10, e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Burks, A. R. (2009). Phylogenetics of Pteromalidae and Eulophidae (Hymenoptera, Chalcidoidea) With a Study of Cranial Bridges in Chalcidoidea (Doctoral theses and Dissertations). University of California, Riverside, California, United States, 180 p.
Burks, B. D. (1956). The species of Chryseida (Hymenoptera, Eurytomidae). Bulletin of the Brooklyn Entomological Society, 51, 109-116.
Burks, B. D. (1971). The Nearctic species of Horismenus Walker (Hym., Eulophidae). Proceedings of the Entomological Society of Washington, 73, 68-83.
Burks, B. D. (1979). Torymidae (Agaoninae) and all other families of Chalcidoidea (excluding Encyrtidae). In Krombein, K.V., Hurd, P.D. jr., Smith, D.R., y Burks, B.D. (Ed) Catalog of Hymenoptera in America North of Mexico (1: 863). Smithsonian Institute Press, Washington, D.C.
Castro, L. R., Austin, A. D., and Dowton, M. (2002). Contrasting rates of mitochondrial molecular evolution in parasitic Diptera and Hymenoptera. Molecular Biology and Evolution, 19, 1100–1113. https://doi.org/10.1093/oxfordjournals. molbev.a004168
Cognato, A. I. (2006). Standard percent DNA sequence difference for insects does not predict species boundaries. Journal of Economic Entomology, 99, 1037–1045. https:// doi.org/10.1093/jee/99.4.1037
Crawford, J. C. (1908). Some new Chalcidoidea. Proceedings of the Entomological Society of Washington, 9,158.
Cross, W. H., and Mitchell, H. C. (1968). Parasites of the boll weevil in Mexico. Folia Entomológica Mexicana, 18, 19-24.
Cruaud, A., Jabbour-Zahab, R., Genson, G., Cruaud, C., Couloux, A., Kjellberg, F., van Noort, S., and Rasplus, J. Y. (2010). Laying the foundations for a new classification of Agaonidae (Hymenoptera, Chalcidoidea), a multilocus phylogenetic approach. Cladistics, 26, 359–387. https://doi.org/10.1111/j.1096-0031.2009.00291.x
Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415. https://doi.
org/10.1111/j.1095-8312.2005.00503.x
De la Cruz, A., Romero, J., Carrillo, J. L., García, E., Grether, R., Sánchez, S., and Pérez, M. (2013). Brúquidos (Coleoptera, Bruchidae) del estado de Tabasco, México. Acta Zoológica Mexicana, 29, 1-95.
De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56, 879–886.
Deng, J., Yu, F., Li, H. B., Gebiola, M., Desdevises, Y., Wu, S. A., and Zhang, Y. Z. (2013). Cophylogenetic relationships between Anicetus parasitoids (Hymenoptera, Encyrtidae) and their scale insect hosts (Hemiptera, Coccidae). BMC Evolutionary Biology, 13, 275. https://doi.org/10.1186/1471-2148-13-275
Derocles, S. A., Plantegenest, M., Rasplus, J. Y., Marie, A., Evans, D. M., Lunt, D. H., and Le Ralec, A. (2016). Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes? Systematic Entomology, 41, 379-391. https:// doi.org/10.1111/syen.12160
DeSantis, L. (1967). Catálogo de los Himenópteros Argentinos de la Serie Parasitica, incluyendo Bethyloidea. Comision de Investigacion Cientifica, La Plata, 337 p.
DeSantis, L. (1979). Catálogo de los himénopteros calcidoideos de América al sur de los Estados Unidos. Publicación Especial Comisión de Investigaciones Cientificas Provincia de Buenos Aires, 356 p.
DeSantis, L. (1989). Catálogo de los himenópteros Calcidoides (Hymenoptera) al sur de los Estados Unidos, Segundo Suplemento. Acta Entomológica Chilena, 15, 9-90.
DeSantis, L., and Fidalgo, P. (1994). Catálogo de himenópteros Calcidoideos. Serie de la Academia Nacional de Agronomia y Veterinaria, 13, 154 p.
Dowton, M., and Austin, A. D. (1995). Increased genetic diversity in mitochondrial genes is correlated with the evolution of parasitism in the Hymenoptera. Journal of Molecular Evolution, 41, 958-965. https://doi.org/10.1007/BF00173176
Forister, G. W., and Johnson, C. D. (1971). Bionomics of Merobruchus julianus (Coleoptera, Bruchinae). Coleopterists' Bulletin, 24, 84-87.
Fujisawa, T., and Barraclough, T. G. (2013). Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology, 62, 707-724. https:// doi.org/10.1093/sysbio/syt033
Fusu, L. (2017). An integrative taxonomic study of European Eupelmus (Macroneura) (Hymenoptera, Chalcidoidea, Eupelmidae), with a molecular and cytogenetic analysis of Eupelmus (Macroneura) vesicularis, several species hiding under one name for 240 years. Zoological Journal of the Linnean Society, 181, 519-603. https://doi.org/10.1093/ zoolinnean/zlw021
Gahan, A. B. (1930). Synonymical and descriptive notes on Parasitic Hymenoptera. Proceedings of the United States National Museum, 77(2831), 1-12.
Gates, M., and Burks, R. (2003). Hosts and ranges. Chalcid Forum 25,5
Gebiola, M., Goméz-Zurita, J., Monti, M. M., Navones, P., and Bernardo, U. (2012). Integration of molecular, ecological, morphological and endosymbiont data for species delimitation within the Pnigalio soemius complex (Hymenoptera, Eulophidae). Molecular Ecology, 21, 1190-2108. https:// doi.org/10.1111/j.1365-294X.2011.05428.x
Gibson, G. A. P. (1995). Parasitic wasps of the subfamily Eupelminae, classification and revision of world genera (Hymenoptera, Chalcidoidea, Eupelmidae). Memoirs on Entomology, International, 5, 1-421.
Gibson, G. A. P. (2011). The species of Eupelmus (Eupelmus) Dalman and Eupelmus (Episolindelia) Girault (Hymenoptera, Eupelmidae) in North America north of Mexico. Zootaxa, 2951, 33-41. https://doi.org/10.11646/zootaxa.2951.1.1
Gibson, G. A. P. (2013). Revision of the species of Jaliscoa Bouček within a review of the identity, relationships and membership of Jaliscoa, Catolaccus Thomson, Eurydinoteloides Girault, Lyrcus Walker and Trimeromicrus Gahan (Hymenoptera, Pteromalidae). Zootaxa, 3612, 1-85. https://doi.org/10.11646/zootaxa.3612.1.1
Gibson, G. A. P. (2016). Revision of the Neotropical genus Macroeupelmus Ashmead (Hymenoptera: Chalcidoidea: Eupelmidae). Zootaxa, 4161, 81–115. https://doi. org/10.11646/zootaxa.4161.1.3
Gibson, G. A. P., and Fusu, L. (2016). Revision of the Palaearctic species of Eupelmus (Eupelmus) Dalman (Hymenoptera, Chalcidoidea, Eupelmidae). Zootaxa, 4081, 1-331. https:// doi.org/10.11646/zootaxa.4081.1.1
Gibson, G. A. P., Huber, J. T., and Woolley, J. B. (eds). (1997). Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa, Canada: National Research Council of Canada Research Press.
Godfray, H. C., and Shimada, M. (1999). Parasitoids, a model system to answer questions in behavioral, evolutionary and population ecology. Researches on Population Ecology, 41, 3-10. https://doi.org/10.1007/PL00011980
Gómez, J. F., Hernández Nieves, M., Garrido Torres, A. M., Askew, R. R., and Nieves- Aldrey, J. L. (2006). Chalcidoidea (Hymenoptera) associated with galls of Cynipidae (Hymenoptera) in the Comunidad de Madrid (Spain). Graellsia 62 (número extraordinario), 293-331.
Graham, M. W. R. de V. (1984). New Chalcidoidea (Insecta, Hymenoptera) mainly from France, including several species of Eurytoma and Pteromalus associated with Euphorbia. Journal of Natural History, 18, 495-520. https://doi. org/10.1080/00222938400770431
Greathead, D. J. (1986). Parasitoids in classical biological control. En, Waage, J. K. and Greathead, D. J. (Ed). Insect Parasitoids (pp. 287–318). London: Academic Press.
Grissell, E. E. (1976). A revision of western Nearctic species of Torymus Dalman (Hymenoptera, Torymidae). University of California Publications in Entomology, 79, 1-120.
Hall, B. G. (2005). Comparison of the Accuracies of Several Phylogenetic Methods Using Protein and DNA Sequences. Molecular Biology and Evolution, 22(3),792-802. https:// doi.org/10.1093/molbev/msi066
Hansson, C. (2002). Eulophidae of Costa Rica (Hymenoptera, Chalcidoidea). Memoirs of the American Entomological Institute, 67, 1-290.
Hansson, C. (2009). Eulophidae of Costa Rica (Hymenoptera, Chalcidoidea). 3: The genus Horismenus. Memoirs of the American Entomological Institute, 82, 187 p.
Hansson, C., Aebei, A., y Benrey, B. (2004). Horismenus species (Hymenoptera, Eulophidae) in a bruchid beetle parasitoid guild, including the description of a new species. Zootaxa, 548, 1-16. https://doi.org/10.11646/zootaxa.548.1.1
Hebert, P. D. N., Cywinska, A., Ball, S. L. and DeWaard, J. R. (2003). Biological identification through DNA barcodes. Proceedings of the Royal Society of London Series A, Biological Sciences, 270, 96-99. https://doi.org/10.1098/ rspb.2002.2218
Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., and Hallwachs, W. (2004). Ten species in one, DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America, 101, 14812–14817. https://doi.org/10.1073/pnas.0406166101
Heraty, J. (2004). Molecular Systematics, Chalcidoidea and Biological Control. En, Ehler, L.E., Sforza, R., y Mateille, T. (Ed). Genetics, Evolution and Biological Control Massachusetts, USA: CABI Publishing, pp. 39-71.
Heraty, J. (2009). Parasitoid biodiversity and insect pest management. En, Foottit, R. G. and Adler, P. H. (Eds), Insect Biodiversity. UK: Wiley-Blackwell, pp. 445–462.
Heraty, J. M., Burks, R. A., Cruaud, A., Gibson, G. A. P., Liljeblad, J., Munro, J., Rasplus, J., Delvare, G., Janšta, P., Gumovsky, A., Huber, J., Woolley, J. B., Krogmann, L., Heydon, S., Polaszek, A., Schmidt, S., Darling, D. C., Gates, M. W., Mottern, J., Murray, E., Dal Molin, A., Triapitsyn, S., Baur, H., Pinto, J. D., van Noort, S., George, J., and Yoder, M . (2013). A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera). Cladistics, 29, 466–542. https://doi.org/10.1111/cla.12006
Herting, B. (1973). Coleoptera to Strepsiptera. A catalogue of parasites and predators of terrestrial arthropods. Section A. Host or Prey/Enemy. Commonwealth Agricultural Bureaux, Institute of Biological Control, 3, 185.
Hetz, M. and Johnson, C. (1988) Hymenopterous parasites of some Bruchid beetles of North and Central America. Journal of Stored Products Research, 24, 131–143. https://doi. org/10.1016/0022-474X(88)90010-0
Jeffery, N. W., Elías-Gutiérrez, M., and Adamowicz, S. J. (2011). Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada. Public Library of Science ONE, 6, e18364. https://doi. org/10.1371/journal.pone.0018364
Johnson, C. D., and J. M. Kingsolver. (1981). Checklist of the Bruchidae (Coleoptera) of Canada, United States, Mexico, Central America and the West Indies. The Coleopterists' Bulletin, 35, 409-422.
Kaartinen, R., Stone, G. N., Hearn, J., Lohse, K., and Roslin, T. (2010). Revealing secret liaisons, DNA barcoding changes our understanding of food webs. Ecological Entomology, 35, 623-638. https://doi.org/10.1111/j.1365-2311.2010.01224.x
Kenyon, S. G., Buerki, S., Hansoon, C., Alvarez, N., & Benrey, B. (2015). Uncovering cryptic parasitoid diversity in Horismenus (Chalcidoidea, Eulophidae). Plos One, 10, e0136063. https://doi.org/10.1371/journal.pone.0136063
Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120. https://doi.org/10.1007/BF01731581
Kingsolver, J. M. (2004). Handbook of the Bruchidae of the United States and Canada (Insecta, Coleoptera). U.S. D. A Technical Bulletin, 1, 1-324.
LaSalle, J. (1993). Parasitic Hymenoptera, biological control and biodiversity. En, LaSalle, J. and Gauld, I. D. (Ed). Hymenoptera and Biodiversity. Wallingford, UK: CAB International, pp. 197–216.
LaSalle, J., and Gauld, I. D. (1991). Parasitic Hymenoptera and the biodiversity crisis. Redia, 74, 315-334.
Li, Y., Zhou, X. I. N., Feng, G., Hu, H., Niu, L., Hebert, P. D., and Huang, D. (2010). COI and ITS2 sequences delimit species, reveal cryptic taxa and host specificity of fig‐associated Sycophila (Hymenoptera, Eurytomidae). Molecular Ecology Resources, 10, 31-40.
Luna C. J., Romero, N. J., and Jones, R. W. (2002). Lista de Bruchidae del Estado de Querétaro, México (Insecta, Coleoptera). Acta Zoologica Mexicana, 87, 17-28.
Matosevic, D., and Melika, G. (2013). Recruitment of native parasitoids to a new invasive host, first results of Diyocosmus kuriphilus parasitoid assemblage in Croatia. Bulletin of Insectology, 66, 233-235.
Meier, R., Shiyang, K., Vaidya, G., and Ng, P. (2006). DNA barcoding and taxonomy in Diptera, a tale of high intraspecific variability and low identification success. Systematic Biology, 55, 715–728. https://doi.org/10.1080/10635150600969864
Melika, G., Csoka, G., Stone, G. N., and Schonrogge, K. (2002). Parasitoids reared from galls of Andricus aestivalis Giraud, A. grossilaria Giraud, A. multiplicatus Giraud, and A. vindobonensis Muellner in Hungary (Hymenoptera, Cynipidae). Folia Entomologica Hungarica, 63, 105-112.
Noyes, J. S. (1978). On the numbers of genera and species of Chalcidoidea (Hymenoptera) in the world. Entomologist's Gazette, 29, 163-164.
Noyes, J. S. (2018). Universal Chalcidoidea Database. World Wide Web electronic publication. http,//www.nhm.ac.uk/chalcidoids (29th of August 2018).
Noyes, J. S. and Hayat, M. (1994). Oriental Mealybug Parasitoids of the Anagyrini (Hymenoptera, Encyrtidae). Wallingford, UK: CAB International.
Oliveira, D. C. S. G., Raychoudhury, R., Lavrov, D. V., and Werren, J. H. (2008). Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera, Pteromalidae). Molecular Biology and Evolution, 25, 2167-2180. https:// doi.org/10.1093/molbev/msn159
Padial, J. M., Miralles, A., De la Riva, I., and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7, 1-14. https://doi.org/10.1186/1742-9994-7-16
Peck, O. (1963). A catalogue of the Nearctic Chalcidoidea (Insecta, Hymenoptera). Canadian Entomologist (Supplement), 30, 221.
Peréz, G., and Bonet, A. (1985). Hymenopterous parasites of Acanthoscelides obtectus (Say) (Coleoptera, Bruchinae) in Tepoztlan, Morelos. Folia Entomológica Mexicana, 59, 71-78.
Pérez-Benavides, A. L., Hernández-Baz, F., Gonzalez, J. M., and Riverón, A. Z. (2019). Updated taxonomic checklist of Chalcidoidea (Hymenoptera) associated with Bruchinae (Coleoptera: Chrysomelidae). Zootaxa, 4638, 301-343. https://doi.org/10.11646/zootaxa.4638.3.1
Pérez-Benavides, A. L., Hernández-Baz, F., González, J. M., and Riverón, A. Z. (2020). A new species of Torymus (Hymenoptera: Torymidae) associated with two genera of Bruchinae (Coleoptera: Chrysomelidae) in México. Florida Entomologist, 102, 713-716. https://doi. org/10.1653/024.102.0407
Pikart, T. G., Souza, G. K., Costa, V. A., Hansson, C., and Zanuncio, J. C. (2011). Paracrias pluteus (Hymenoptera, Eulophidae) in Brazil, new distribution and host records, and with a new host group for Paracrias. ZooKeys, 2011,77-82. https://doi.org/10.3897/zookeys.102.1343
Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D., Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595-609. https://doi. org/10.1080/10635150600852011
Ratnasingham, S., and Hebert, P. D. (2013). A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PloS one, 8, e66213. https://doi.org/10.1371/journal. pone.0066213
Rivera, J., & Currie, D. C. (2009). Identification of Nearctic black flies using DNA barcodes (Diptera, Simuliidae). Molecular Ecology Resources, 9, 224–236. https://doi. org/10.1111/j.1755-0998.2009.02648.x
Robinson, E. A., Blagoev, G. A., Hebert, P. D. N., and Adamowicz, S. J. (2009). Prospects for using DNA barcoding to identify spiders in species-rich genera. Zookeys, 16, 27-46. https:// doi.org/10.3897/zookeys.16.239
Rojas-Rousse, D., Poitrineau, K., and Basso, C. (2007). The potential of mass rearing of Monoksa dorsiplana (Pteromalidae) a native gregarious ectoparasitoid of Pseudopachymeria spinipes (Bruchidae) in South America. Biological Control, 41, 348-353. https://doi.org/10.1016/j. biocontrol.2007.03.009
Romero N., J. (2002). Bruchidae. En, Llorente, J., Morrone, J. J. Biodiversidad, Taxonomía y Biogeografía de Artrópodos de México, Hacia una Síntesis de su Conocimiento, UNAM, México, pp. 513-534.
Romero, N. J. (2009). Dos nuevos registros de géneros de Bruchidae (Insecta, Coleoptera) para México. Acta Zoológica Mexicana, 25, 671–672.
Romero N., J., and Johnson, C. D. (2004). Sinopsis de los brúquidos de México (Insecta, Coleoptera). En, Morales, M., Ibarra, A. M., Rivera, A. P., and Stanford, S (Ed). Entomología Mexicana, Vol. 3, pp. 758-763.
Romero, J. (2009). Dos nuevos registros de géneros de Bruchidae (Insecta, Coleoptera) para México. Acta Zoológica Mexicana, 25, 671-672.
Santos, A. M. C., Besnard, G., and Quicke, D. J. (2011). Applying DNA barcoding for the study of geographical variation in host-parasitoid interactions. Molecular Ecology Resources, 11, 46-59. https://doi.org/10.1111/j.1755-0998.2010.02889.x
Schauff, M. E. (1985). Taxonomic study of the Nearctic species of Elachertus Spinola (Hymenoptera, Eulophidae). Proceedings of the Entomological Society of Washington, 87, 843-858.
Sheffield, C. S., Hebert, P. D. N., Kevan, P. G., and Packer, L. (2009). DNA barcoding a regional bee (Hymenoptera, Apoidea) fauna and its potential for ecological studies. Molecular Ecology Resources, 9, 196-207. https://doi. org/10.1111/j.1755-0998.2009.02645.x
Smith, M. A., Rodriguez, J. J., Whitfield, J. B., Deans, A. R., Janzen, D. H., Hallwachs, W., and Hebert, P. D. N. (2008). Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences of the United States of America, 105, 12359-12364. https://doi.org/10.1073/pnas.0805319105
Southgate, B. J. (1979). Biology of the Bruchidae. Annual Review of Entomology, 24, 449-73.
Stojanova, A., Civelek, H. S., Yörük, B., Sari, S., and Atahan, T. (2012). Checklists of Turkish Eurytomidae Walker, 1832 and Torymidae Walker, 1833 (Hymenoptera, Chalcidoidea). Turkiye Entomoloji Dergisi, 36, 77.
Sun, X. J., Xiao, J. H., Cook, J. M., Feng, G., and Huang, D. W. (2011). Comparison of host mitochondrial, nuclear and endosymbiont bacterial genes reveal cryptic fig wasp species and the effects of Wolbachia on host mtDNA evolution and diversity. BMC Evolutionary Biology, 11, 1-8. https://doi. org/10.1186/1471-2148-11-86
Thompson, W. R. (1955). A catalogue of the parasites and predators of insect pests. Section 2). Host parasite catalogue, Part 3). Hosts of the Hymenoptera (Calliceratid to Evaniid). Commonwealth Agricultural Bureaux, Ottawa, Ontario, Canada, 315 p.
Triplehorn, C., and Johnson, N. (2005). Borror and DeLong’s introduction to the study of insects, 7th edition, USA: Cengage Learning.
Will, K. G, Mishler, B. D., and Wheeler, Q. D. (2005). The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54, 844–851. https://doi. org/10.1080/10635150500354878
Xiao, J. H, Jia, J. G., Murphy, R.W., and Huang, D.W. (2011). Rapid evolution of the mitochondrial genome in chalcidoid wasps (Hymenoptera, Chalcidoidea) driven by parasitic lifestyles. Public Library of Science ONE, 6(11), e26645. https:// doi.org/10.1371/journal.pone.0026645
Zerova, M. D. (1980). A new species of the genus Chryseida Spinola (Hymenoptera, Eurytomidae) from Central America. Entomologicheskoe Obozrenie, 59, 176-178.
