Family Tetracampidae (Insecta: Hymenoptera) as Parasitoids of the Orders Diptera, Coleoptera and Lepidoptera as Agricultural Pests

 

Carlos Henrique Marchiori1*

 

1Department of Biological Science, Instituto Federal Goiano, Goias, Brazil

 

*Correspondence to: Carlos Henrique Marchiori, PhD, Professor, Department of Biological Science, Instituto Federal Goiano, Rua T-65 No. 1050, Goiânia 74230120, Goias, Brazil; E-mail: chmarchiori@yahoo.com.br

 

DOI: 10.53964/jmab.2023011

 

Abstract

Many species of Tetracampidae are hosts that have been identified are plant-mining insects. The European species of the genus Dipriocampe are endoparasitoids of the eggs of flies or saw wasps. Species of the genus Foersterella from England are endoparasitoids of the eggs of Cassida spp. One species, Dipriocampe diprioni (Ferrière, 1935), has been introduced to Canada from Europe as a biological control of saw wasps but has failed to become established. The aim of this mini review is to consider the importance of the Tetracampidae family (Insecta: Hymenoptera) as parasitoids of the Diptera, Coleoptera and Lepidoptera orders as agricultural pests. The short commentary research was carried out based on studies related to the quantitative and conceptual aspects of Tetracampidae. A bibliographic search was carried out containing national and international articles from 1973 to 2022. The short commentary used digital platforms.

 

Keywords: endoparasitoids, eggs, dipterans, damage, coleopterans, lepidopterans

 

1 INTRODUCTION

The Tetracampidae are a small family of parasitic wasps in the superfamily Chalcidoidea. They are parasitoids of phytophagous insects, primarily flies. The 44 species in 15 genera are almost entirely absent from the new world. The biology of most species of Tetracampidae is little studied. Most of those whose hosts are known are associated with insects that mine in plants (Figure 1)[1].

 

JMAB202202042

Figure 1. Specimens of Tetracampidae family. A: Epiclerus sp. male; B: Pteromalus hieracii Thomson 1878. Sources: https://alchetron.com/Tetracampidae and https://www.discoverlife.org/mp/20q?search=Tetracampidae

 

1.1 Description

Head usually with occipital carina; antenna with 7 to 12 articles, usually with 3 flagellomeres club (rarely fused); mesoscutum with linear notaúlice; forewing with vein long marginal, stigmal vein extended beyond the apex of the short stigmal vein; protibia with short, apically bifurcated spur; tarsus with 4 or 5 tarsomeres; petiolate metasome. They measure from 0.8 to 3.5mm and are mostly metallic green (Figures 2-8)[2-4].

 

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Figure 2. Foersterella spp., antenna, lateral view, male. 7: Foersterella erdoesi Boucek 1958; 8: Foersterella reptans (Nees) sp. nov.; 9: Foersterella angusticornis sp. nov.; 10: Foersterella fuscicornis sp. nov.; 11: Foersterella sp., female, head and antennae, lateral view; 12: Foersterella sp.; 13: F. erdoesi. Source: https://zenodo.org/record/255285#.YxJLX3bMLIU

 

Foersterella erdoesi - Male

Figure 3. Foersterella erdoesi Boucek 1958. Source: https://www.nhm.ac.uk/our-science/data/chalcidoids/tetracampidae.html

 

Platynocheilus cuprifrons  - Male

Figure 4. Platynocheilus cuprifrons (Nees, 1834). The majority of those whose hosts are known are associated with insects that mine in plants. European species of one genus, Dipriocampe, are endoparasitoids of the eggs of diprionid sawflies and the British species are endoparasitoids of the eggs of Cassida spp. (Coleoptera, Cassididae). Source: https://www.nhm.ac.uk/our-science/data/chalcidoids/tetracampidae.html

 

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Figure 5. Afrocampe prinslooi gen. et sp. nov., holotype, ♀. A: Head and mesosoma in lateral view; B: Body in dorsal view; C: Metasoma and posterior part of mesosoma; D: Head and mesosoma in lateral view; E: Antenna; F: Mouth opening and clypeus; G: Pedicel, anellus and F1 (seta on anellus is arrowed). A-C: color imaging; D-G: SEM. Source: https://www.semanticscholar.org/paper/A-new-genus-of-Tetracampidae-(Hymenoptera)-from-Gumovsky/6b7ba0e8058cfb9c0e5e6a4177d884750cbad565/figure/2

 

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Figure 6. Afrocampe prinslooi gen. sp. nov., holotype (color imaging), ♀. A: Habitus in lateral view; B: Face; C: Habitus in ventro-lateral view; D: Head and anterior part of mesosome; E: Habitus in dorsal view; F: Head and mesosoma in dorsal view. Source: https://www.semanticscholar.org/paper/A-new-genus-of-Tetracampidae-(Hymenoptera)-from-Gumovsky/6b7ba0e8058cfb9c0e5e6a4177d884750cbad565/figure/1

 

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Figure 7. Wing of Tetracampidae from Goulet and Huber, 1993. Source: http://drawwing.org/insect/tetracampidae-wings

 

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Figure 8. Eustochomorpha haeckeli Girault, 1915, female. 11: Head + prothorax, lateral; B: 12 Head + prothorax, dorsal; 13: Base of antenna, lateral (right antenna) and ventral (left antenna); 14: Apex of antenna; 15: Mesosome, dorsal; 16: Mesosome, posterolatero dorsal; 17: Mesosome, lateral; 18: Base of wings + mesosome, lateral (medial portion). Source: https://www.semanticscholar.org/topic/Tetracampidae/8532679

 

1.2 Biology

Parasitoids of miner and galling dipterans, as well as eggs of Chrysomelidae (Coleoptera) and Diprionidae (Hymenoptera) and larval parasitoids of flies (Agromyzidae) and Orthoptera. Very little is known of the biology of most Tetracampidae species. Most of the host species that have been identified are plant-mining insects. The European species of the genus Dipriocampe are endoparasitoids of the eggs of flies or saw wasps. Species of the genus Foersterella from England are endoparasitoids of the eggs of Cassida spp. One species, Dipriocampe diprioni (Ferrière, 1935), has been introduced to Canada from Europe as a biological control of saw wasps, but has failed to become established (Figure 9)[5-7].

 

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Figure 9. Egg mass of Aspidomorpha sanctaecrucis (Fabricius, 1792) (Coleoptera: Chrysomelidae) parasitized by Tetracampidae wasps. Source: https://en.wikipedia.org/wiki/Tetracampidae

 

The way of life of tetracampids is still not well known, however, host selection seems to be limited to mining larvae. Some species are of economic importance because they are among the pests of forest and arable crops parasitizing[7-9].

 

1.3 Distribution Geographic

Bosnia, Herzegovina, Denmark, Germany, France, Great Britain, Ireland, Italy, Yugoslavia, Croatia, Latvia, Macedonia, Moldova, Netherlands, Austria, Poland, Romania, Russia, Sweden, Switzerland, Slovakia, Slovenia, Spain, Czech Republic, Hungary and Belarus. In addition to Europe, this family is also found in the Middle East, the Nearctic, North Africa and the eastern Palaearctic[8-10].

 

1.4 Taxonomy

The family has a cosmopolitan distribution, with about 44 species in 12 genera. In the Neotropical Region, there is only the record of the genus Epiclerus in Costa Rica and Cuba.

 

Subfamilies: Tetracampinae, Platynocheilinae, Mongolocampinae and Distylopinae (Figure 10).

 

Pteromalus hieracii, I_MWS137397

Figure 10. Subfamily Tetracampinae. Source: https://www.discoverlife.org/mp/20p?see=I_MWS137397&res=640

 

Genus: Afrocampe Gumovsky, 2018 (South Africa), Diplesiostigma Girault, 1920, Undescribed species (Bouček, 1988), Epiclerus Haliday, 1844, (Senegal), Foersterella Dalla Torre, 1897, Kilomotoia Gumovsky, 2016 (Figures 11 and 12).

 

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Figure 11. Wings of Tetracampidae Myolepta nigritarsis Coe, 1957. Source: http://drawwing.org/insect/myolepta-nigritarsis-wing

 

Epiclerus_SAM-HYM-P010172_head_mesosoma_lateral

Figure 12. Epiclerus species. Source: http://www.waspweb.org/Chalcidoidea/Tetracampidae/Epiclerus/Epiclerus_species.htm

 

Some Species include Afrocampe prinslooi Gumovsky, 2018, Dipriocampe diprioni (Ferrière, 1935), Epiclerus agromyzae (Risbec, 1951), Epiclerus plectroniae (Risbec, 1952) (Madagascar), Foersterella africana (Ferrière, 1938) (Senegal, Uganda), Kilomotoia kitoko Gumovsky, 2016 (Democratic Republic of Congo, Uganda), Foersterella reptans (Nees, 1834), Platynocheilus cuprifrons (Nees, 1834) (Figures 13-15).

 

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Figure 13. Epiclerus plectroniae (Risbec, 1952) Syntypes. A: Upper side; B: Underside; C: Upper side; D: Underside; E and F: The female indicated by a red circle in A and B. Source: http://www.waspweb.org/Chalcidoidea/Tetracampidae/Epiclerus/Epiclerus_plectroniae.htm

 

Epiclerus temenus

Figure 14. Platynocheilinae: Platynocheilus cuprifrons (Nees, 1834) Female. The family currently includes 15 genera and 50 species placed in 6 subfamilies as follows: Baeomorphinae (1/4, fossil), Bouceklytinae (1/1, fossil), Distylopinae (1/1, fossil), Mongolocampinae (4/10), Platynocheilinae (1/4), Tetracampinae (7/30). Source: https://www.nhm.ac.uk/our-science/data/chalcidoids/tetracampidae.html

 

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Figure 15. Kilomotoia kitoko Gumovsky, 2016. A and B: Head, mesosoma and anterior part of metasoma, dorsal view; C: Entire: habitus; D: Dorsal view; E and F: Lateral views. (White arrows in A, C and D points to dorsal submediant ridge stretching to deep emargination of posterior margins of gastral tergites; white arrows in E point to lightly sculptured areas). Source: http://www.waspweb.org/Chalcidoidea/Tetracampidae/Kilomotoia/Kilomotoia_kitoko.htm

 

There are many fossil taxa in this group but their relationship to other chalcidoid families is not clear (Figures 16 and 17)[11-15].

 

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Figure 16. Fossil of Tetracampidae. Source: https://eol.org/pages/8149/media

 

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Figure 17. Phylogenetic tree of chalcid families. Based on Noyes, 1990; see the text for further explanations) with ranges of haploid chromosome numbers superimposed onto it (based on data from Gokhman, 2009 and recent updates by the first author. Most frequent "n" values are given in brackets. Source: https://www.researchgate.net/figure/Phylogenetic-tree-of-chalcid-families-based-on-Noyes-1990-see-the-text-for-further_fig2_247905145

 

1.5 Objective

The aim of this mini review is to consider the importance of the Tetracampidae family (Insecta: Hymenoptera as parasitoids of the Agromyzidae (Diptera), Chrysomelidae (Coleoptera) and Elachistidae (Lepdoptera) families as agricultural pests.

 

2 METHODS

The short commentary research from September to October 2021, using digital platforms such as: Abstract, Science Research.com, CAPES Periodicals, Google Academic, Bioline International, Scopus, Web of Science and Portal of Scientific Journals in Health Sciences[16].

 

3 STUDIES CONDUCTED AND SELECTED

3.1 Study 1

3.1.1 Tetracampidae Family and Subfamily Tetracampinae

Genus: Epiclerus

 

Identification: The genus Epiclerus includes wasps with 11 antennal segments, including 6 at the funicle. The pedicel is smaller than the first article of the funicle. The pronotum is bell-shaped, the mesoscutum short, has notauli complete. The scutellum is glabrous with 4 bristles. The marginal vein is large, 4 times larger than the radial. The female has 5 tarsal segments. The male has 4 segments at the tarsi (Figure 18).

 

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Figure 18. Genre: Epiclerus. Source: https://jessica-joachim.com/insectes/hymenopteres/tetracampidae/epiclerus-sp

 

Biology: Parasitoid of Diptera Agromyzidae.

 

Similar species: The genus Platynocheilus has 7 funicular segments. In the other genera of the family, the pedicel is equal to or larger than the first segment of the funicle. I first took it for a Pteromalidae, but I was corrected on insecticide.org (Figures 19 and 20)[17].

 

JMAB202202047

Figure 19. Genre Platynocheilus. A: Hymenoptera; B: Chalcid wasp. Sources: https://eol.org/pages/75470 and https://bugguide.net/node/view/1670044/bgimage

 

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Figure 20. Liriomyza trifolii, Burgess, 1880. A: Egg inside a puncture on the leaf; B: Larvae inside a leaf, behind is a trail of mines, while the dark areas are the waste products; C: Pupa attached to the upper surface of a leaf; D: Adult dorsal view. Source: https://cipotato.org/riskatlasforafrica/liriomyza-trifolii

 

3.2 Study 2

3.2.1 Subfamily Tetracampinae

3.2.1.1 Genus Afrocampe Gumovsky, 2018

Afrocampe prinslooi Gumovsky, 2018 (South Africa) (Figure 21).

 

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Figure 21. Afrocampe prinslooi gen. et sp. nov., paratype (arrows), ♀, in a sample from the Grootvadersbosch Nature Reserve (Western Cape, South Africa) among other chalcidoid wasps. A–B: General view. Source: https://www.mindat.org/paleoimg.php?id=11051

 

Biology: Parasitoids of dipteran leaf miners (Agromyzidae). Recorded host species: Chromatomyia syngenesiae Hardy 1849, Liriomyza trifolii (Burgess, 1880), Ophiomyia beckeri (Hendel, 1923), Perittia weberella Whitebread 1984, Phytomyza phillyreae Hering 1930, Phytomyza rostrata Hering 1934 and Tropicomyia atomella Malloch, 1914.

 

3.2.1.2 Genus Diplesiostigma Girault, 1920

Biology: Unknown.

 

3.2.1.3 Undescribed Species (Bouček, 1988)

Biology: Unknown.

 

3.2.1.4 Genus: Epiclerus Haliday, 1844

Epiclerus agromyzae (Risbec, 1951) (Senegal) (Figure 22).

 

Figure 22. Epiclerus agromyzae (Risbec, 1951) (Senegal). Syntypes. A and B: General view of the MNHN slides from Risbec's collection; C: Female; D: Male (both are indicated in A); E and F: Ffemale (E) male (F) of the series of pinned specimens in BMNH. Source: http://www.waspweb.org/chalcidoidea/Tetracampidae/Epiclerus/Epiclerus_agromyzae.htm

 

3.2.1.5 Epiclerus Plectroniae (Risbec, 1952) (Madagascar) (Figure 23)

 

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Figure 23. Epiclerus plectroniae, Risbec, 1952. Source: http://www.waspweb.org/chalcidoidea/Tetracampidae/Epiclerus/index.htm

 

Biology: Parasitoid of leaf-mining Diptera on Plectronia umbellate Kuntze, 1891 (Penaeaceae) and an Asteraceae species (Risbec, 1952) (Figure 24).

 

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Figure 24. Plectronia umbellate Kuntze, 1891, Penaeaceae. Source: https://efloraofindia.com/2013/01/30/psydrax-umbellatus

 

3.2.1.6 Genus Foersterella Dalla Torre, 1897

Foersterella africana (Ferrière, 1938) (Senegal, Uganda) (Figure 25).

 

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Figure 25. Foersterella africana (Ferrière, 1938). Source: http://www.waspweb.org/Chalcidoidea/Tetracampidae/Kilomotoia/Kilomotoia_kitoko.htm

 

Biology: Egg parasitoid of Aspidomorpha spp. (Chrysomelidae, Cassidinae), most commonly Aspidomorpha tecta Boheman, 1854: and Aspidomorpha quinquefasciata (Fabricius, 1801) (Figure 26).

 

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Figure 26. Aspidomorpha quinquefasciata (Fabricius, 1801) (Coleoptera: Chrysomelidae). Source: https://www.kaefer-der-welt.de/aspidimorpha_quinquefasciata.htm

 

3.2.1.7 Genus Kilomotoia Gumovsky, 2016

Kilomotoia kitoko Gumovsky, 2016 (Democratic Republic of Congo, Uganda) (Figure 27).

 

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Figure 27. Kilomotoia kitoko Gumovsky, 2016. A and B: Holotype (from D.R. Congo); A and B: Habitus in lateral and dorsal views; C: Habitus in lateral view; D: Head in frontal view; E: Head and mesosoma enlarged; F: Head in frontal view; G: Antenna; H: Mandible. Source: http://www.waspweb.org/Chalcidoidea/Tetracampidae/Kilomotoia/Kilomotoia_kitoko.htm

 

Biology: Unknown[18,19].

 

3.3 Study 3

3.3.1 Foersterella Angusticornis Hansson, 2016 (Figure 28)

 

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Figure 28. Foersterella spp., habitus in lateral view. 1: Foersterella angusticornis Hansson, 2016, male holotype, specimen length 1.1mm; 2: Foersterella erdoesi Bouček, 1958, male non-type from Sweden (Skåne); 3: Foersterella reptans (Nees, 1834), male; 4: Foersterella fuscicornis Hansson, 2016, male Head, frontal view, males: 5: F. angusticornis, holotype; 6: F. erdoesi. Source: https://www.mindat.org/paleoimg.php?id=12161

 

Host: Unknown, but based on records for other species in Foersterella it probably is an egg parasitoid of some species of Cassida (Coleoptera: Chrysomelidae) (Figure 29).

 

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Figure 29. Genus Foersterella. Source: https://treatment.plazi.org/id/E56F87C43E2CFF80FF550389FE1F49AD

 

Distribution: Swedena (Figure 30).

 

JMAB202202049

Figure 30. Cassida. A: Cassida (Coleoptera: Chrysomelidae); B: Cassida viridis L., 1758 (Coleoptera: Chrysomelidae). Sources: https://www.flickr.com/photos/coleoptera-us/51306979961 and https://www.flickr.com/photos/coleoptera-us/51331318562

 

3.3.2 Foersterella Erdoesi Bouček, 1958

Host: Endoparasitoid in eggs of Cassida viridis L., 1758 (Coleoptera: Chrysomelidae) (record checked).

 

Distribution: Hungary (Bouček 1958), Romania, Sweden, United Kingdom (all records checked).

 

3.3.3 Foersterella Fuscicornis Hansson, 2016

Host: Unknown, but based on records for other species in Foersterella it probably is an egg parasitoid of some species of Cassida (Coleoptera: Chrysomelidae).

 

Distribution: France and Sweden.

 

3.3.4 Pteromalus Reptans Nees, 1834

Hosts: Endoparasitoid in eggs of Cassida deflorata Suffrian (Labeyrie, 1961), Cassida murraea L., 1758) (Bouček & Askew 1968), Cassida rubiginosa (Bouček, 1958), and Cassida viridis L. (Bouček 1958) (Coleoptera: Chrysomelidae). I have not seen any reared specimens of this species, and in view of the confusion with species identification, host records in literature must be regard with caution (Figure 31).

 

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Figure 31. Cassida deflorata Suffrian (Labeyrie, 1961). Source: https://www.insecte.org/forum/viewtopic.php?t=193830

 

Distribution: Austria, Czechoslovakia, Denmark, Germany, Hungary, Sweden, Yugoslavia (all seven records in Bouček 1958), France, Italy, Romania and United Kingdom)[20-24].

 

3.4 Study 4

Eight species of Tetracampidae are recorded in Britian and Ireland, but only three species are recorded as parasitods of British and Irish miners.

 

3.4.1 Epiclerus Nomocerus (Masi, 1934)

Distribution: Croatia Czechoslovakia, Europe rance, Germany, Hungary Moldova, Morocco, North Africa, Romania, Serbia, Slovakia, Sweden, Turkmenistan, United Kingdom and England (Figure 32).

 

JMAB202202049

Figure 32. Epiclerus. A: Epiclerus nomocerus (Masi, 1934); B: Epiclerus panyas (Walker, 1839). Sources: http://ponent.atspace.org/fauna/ins/fam/tetracampidae/epiclerus_tet.htm and http://v3.boldsystems.org/index.php/TaxBrowser_Taxonpage?taxid=968813

 

Plant associates: Family: Fabaceae: Pisum sp. and Pisum sativum L. Family: Solanaceae: Lycopersicon esculentum Mill.

 

3.4.2 Epiclerus Panyas (Walker, 1839)

Distribution: Canary Islands, Czech Republic, Czechoslovakia, Europe, Germany, Hungary, Italy, Macedonia, Slovenia, Spain, Sweden, Turkey, United Kingdom, England and Wales.

 

Associates: Family: Asteraceae: Centaurea scabiosa L., Cirsium arvense L, Cirsium palustre L., Eupatorium cannabinum L., Inula conyza (Griess.), Senecio sp., Sonchus sp., Sonchus asper L., Tanacetum sp., and Taraxacum sp., Family: Chenopodiaceae: Atriplex halimus L., Family: Cucurbitaccae: Cucumis sativus L., Family: Plantaginaceae; Plantago lanceolata L., Family: Poaceae: Holcus sp., Holcus lanatus L., Holcus mollis L., Poa sp. Family: Tamaricaceae: Tamarix canariensis Willd.

 

3.4.3 Epiclerus Temenus (Walker, 1839)

Distribution: Czech Republic, Czechoslovakia, Europe, France, Germany, Hungary, Italy, Netherlands, Slovakia, Sweden, Switzerland, United Kingdom, England and Scotland.

 

Associates: Family: Agromyzidae: Phytomyza rostrata Hering 1934.

 

Order: Lepidoptera: Family: Elachistidae: Perittia weberella Whitebread, 1984 (Figure 33)[25-28].

 

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Figure 33. Perittia weberella Whitebread, 1984. Source: https://lepiforum.org/wiki/page/Perittia_weberella

 

4 CONCLUSION

Tetracampidae parasitoids of miner and galling dipterans, as well as eggs of Chrysomelidae (Coleoptera) and Diprionidae (Hymenoptera) and larval parasitoids of flies (Agromyzidae) and Orthoptera. Very little is known of the biology of most Tetracampidae species. Most of the host species that have been identified are plant-mining insects.

 

Acknowledgements

Thanks to the Editors and their working group for publishing the manuscript in the Journal of Modern Agriculture and Biotechnology.

 

Conflicts of Interest

The author declared no conflict of interest.

 

Author Contribution

Marchiori CH contributed to the manuscript and approved the final version.

 

References

[1] Hanson PE, Gauld ID. The Hymenoptera of Costa Rica, 1st ed. Oxford University Press: Oxford, UK, 1995.

[2] Fernandez F, Sharkey MJ. Introduction to the hymenoptera of the neotropical region, 1st ed. Colombian Society of Entomology and National University of Colombia: Bogota, CO, 2006.

[3] LaSalle J, Gauld ID. Hymenoptera: their diversity and their impact on the biodiversity of other organisms. Hymenoptera Biodiversity, 1993; 1-26.

[4] Polaszek A. African cereal stem borers: Economic importance, taxonomy, natural enemies and control, 1st ed. CAB International: Wallingford, UK, 1998.

[5] Simon van Noort. Accessed September 18, 2022. Available at http://www.waspweb.org/Chalcidoidea/Tetracampidae/Afrocampe/Afrocampe_prinslooi.htm

[6] Hanson PE, Gauld IB. Hymenoptera of the Neotropical region, 1st ed. Memoirs of the American Entomological Institute: Devon, UK, 2006.

[7] LaSalle J. Parasitic Hymenoptera, biological control, and biodiversity. Hymenoptera Biodiversity, 1993; 197-215.

[8] Naumann ID. Hymenoptera (wasps, bees, ants, sawflies): The insects of Australia, 2nd ed. Cornell University Press: New York, USA, 1991.

[9] Resh VH, Cardé RT. Encyclopedia of insects, 1st ed. Academic Press Amsterdam: Amsterdam, NL, 2003.

[10] Noyes JS. A study of five methods of sampling Hymenoptera (Insecta) in a tropical rainforest, with special reference to the Parasitica. J Nat Hist, 1989; 23: 285-298. DOI: 10.1080/00222938900770181

[11] Sharkey MJ. Phylogeny and classification of Hymenoptera. Zootaxa, 2007; 1668: 521-548. DOI: 10.11646/zootaxa.1668.1.25

[12] Munro JB, Heraty JM, Burks R et al. A molecular phylogeny of the Chalcidoidea (Hymenoptera). PLoS One, 2011; 6: e27023. DOI: 10.1371/journal.pone.0027023

[13] Gumovsky A. A review of genera and described Afrotropical species of Tetracampinae (Hymenoptera: Tetracampidae), with description of a new genus from East Central Africa. Zootaxa, 2016; 4111: 393-420. DOI: 10.11646/zootaxa.4111.4.4

[14] Mifsud D, Askew RR. New records of Chalcidoidea (Hymenoptera) from the Maltese Islands with an updated checklist. Zootaxa, 2019; 4560: 365-374. DOI: 10.11646/zootaxa.4560.2.9

[15] Gumovsky A. A new genus of Tetracampidae (Hymenoptera) from South Africa. Eur Taxon, 2018; 447: 1-13. DOI: 10.5852/ejt.2018.447

[16] Marchiori CH. Check the biodiversity of the Lonchaeidae Family (Diptera). Open Access Res J Life Sci, 2022; 4: 27-43. DOI: 10.53022/oarjls.2022.4.1.0054

[17] Epiclerus sp. Accessed September 18, 2022. Available at https://jessica-joachim.com/insectes/hymenopteres/tetracampidae/epiclerus-sp

[18] Hansson C. Lasalleistichus a new genus of Tetrastichinae (Hymenoptera: Eulophidae) from the Neotropical region, including four new species. J Nat Hist, 2020; 54: 621-633. DOI: 10.1080/00222933.2020.1715500

[19] Gumovsk A. A review of genera and described Afrotropical species of Tetracampinae (Hymenoptera: Tetracampidae), with description of a new genus from East Central Africa. Zootaxa, 2016; 4111: 393-420. DOI: 10.11646/zootaxa.4111.4.4

[20] LaSalle J. North American genera of Tetrastichinae (Hymenoptera: Eulophidae). J Nat Hist, 1994; 28: 109-236. DOI: 10.1080/00222939400770091

[21] Bouček Z. Australasian Chalcidoidea (Hymenoptera): A biosystematic revision of fourteen families, with a reclassification of species, 1st ed. CAB International: Wallingford, UK, 1988.

[22] Nieves-Aldrey JL, Richard AR. Two new species of Tetrastichinae (Hymenoptera: Eulophidae) from Spain, the first known native European gall inducing tetrastichine and its parasitoid. Ann Soc Entomol Fr, 2011; 47: 154-161. DOI: 10.1080/00379271.2011.10697707

[23] Herting B. A catalogue of parasites and predators of terrestrial arthropods. Section A. Host or prey/enemy: Coleoptera to Strepsiptera, 3th ed. Agricultural Offices Institute of Biological Control: Wallingford, UK, 1973.

[24] Hansson C. The European species of Foersterella Dalla Torre (Hymenoptera: Tetracampidae), including the description of two new species. Zootaxa, 2016; 4137: 561-568. DOI: 10.11646/zootaxa.4137.4.8

[25] Sousa VR, Paiva PC, Takiya DM et al. Effects of climate, seasonality, and parasitoid abundance on Liriomyza Mik (Diptera: Agromyzidae) populations on important crops in Northeastern Brazil. Iheringia Ser Zool, 2021; 111: e2021001. DOI: 10.1590/1678-4766e2021001

[26] Abe Y. Invasion of Japan by exotic leafminers Liriomyza spp. (Diptera: Agromyzidae) and its consequences. Appl Entomol Zool, 2017; 52: 175-182. DOI: 10.1007/s13355-017-0486-z

[27] Boucek Z. New taxa of North American Pteromalidae and Tetracampidae, with notes. J Nat Hist, 1993; 27: 1239-1313. DOI: 10.1080/00222939300770741

[28] Epiclerus nomocerus (Masi) (Hym., Tetracampidae), a new parasitoid of Liriomyza trifolii Burgess (Dip., Agromyzidae) in glasshouse culture. Accessed September 18, 2022. Available at https://agris.fao.org/agris-search/search.do?recordID=FR9201055

 

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