Taxonomic and Biological Aspects of the Azotidae Family (Insecta: Hymenoptera)

 

Carlos Henrique Marchiori1*

 

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

 

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

 

DOI: 10.53964/jmab.2023001

 

Abstract

The Azotidae are hyperparasitoids linked to alleridae, mealybugs (Insecta: Hemiptera), and egg parasitoids. Azotidae Family Nikol'skaya & Yasnosh, 1966 was accepted by the authority of the name: In the taxonomic catalog of the fauna of Brazil and list of flora of Brazil 2020. The Azotidae were formerly included as a subfamily of the Aphelinidae. This manuscript aimed to establish the biological characteristics of the Azotidae. The bibliographic research was carried out from 1970 to July 2022, using manuscripts present in digital platforms such as Biological Abstract, Periodicals, and Scielo. Thus, the present study increases our knowledge to better understand the intricacies of the bioecology, geographic distribution, and taxonomy of the Azotidae.

 

Keywords: hyperparasitoids, Diaspididae, Aleyrodidae, parasitoid, taxonomy

 

1 INTRODUCTION

Azotidae Family Nikol'skaya & Yasnosh, 1966 was accepted by the Authority of the name: In the taxonomic catalog of fauna of Brazil and list of flora of Brazil 2020. The Azotidae were formerly included as a subfamily of the Aphelinidae (Figure 1)[1,2].

 

Figure 1. Specimen of Azotidae Family. Source: http://www.waspweb.org/chalcidoidea/Azotidae/index.htm

 

1.1 Description

Pale lines or sutures on the head with the existence of a general groove. Female antennae include 7 knuckles, funicular with 4 knuckles, the 3rd reduced, apical nail entirely or weakly divided, antenna with some knuckles alternately yellow. Male antenna with a relatively short third flagellar segment (Figures 2 and 3)[3-7].

 

Figure 2. Female. 5: Antenna; 6: Forewing; 7: Mesosoma; 8: Ovipositor. Source: https://bioone.org/journals/florida-entomologist/volume-99/issue-3/024.099.0310/The-Species-of-Genus-Ablerus-Howard-Hymenoptera--Chalcidoidea/10.1653/024.099.0310.full

 

Figure 3. Female. 9: Body dorsal view; 10: Body ventral view; 11: Foreleg; 12: Mid-leg; 13: Hind leg. Source: https://bioone.org/journals/florida-entomologist/volume-99/issue-3/024.099.0310/The-Species-of-Genus-Ablerus-Howard-Hymenoptera--Chalcidoidea/10.1653/024.099.0310.full

 

Figure 4. Antenna-Ablerus-Female Azotidae Family. Source: Immokalee, Collier County, Florida, USA

 

1.2 Taxonomy

Anterior female wings are often spotted with smoky patterns, wing without oblique bald line, stigma vein with large rounded stigma, a wing lacking oblique bald line, a stigma vein with large rounded stigma, and a lack of post marginal vein. Gaster female with a prominent ovipositor. Tarsus with 5 knuckles. Family with 1 genus and 7 species on the peninsula. Formerly traditionally included in Aphelinidae

 

Taxonomic Hierarchy: Animalia→ Arthropoda von Siebold, 1848→ Hexapoda Latreille, 1825→ Insecta Linnaeus, 1758→ Hymenoptera Linnaeus, 1758→ Azotidae Nikol'skaya & Yasnosh, 1966. Genres Ablerus Howard. Lifeform and Substrate: Substrate terrestrial. Origin: Native. Endemism: Unknown. Environments: epicontinental. Geographic distribution: Southeast São Paulo) Brazil.

 

Synopsis for all Brazil; Species: 3 and Genus1 (Fernandes DRR, DalMolin A. Azotidae in taxonomic catalog of fauna of Brazil). Other countries are Argentina, Chile, Eritrea, Georgia, Mexico, and Uruguay Figures 4 and 5[8-12].

 

Figure 5. IndoBioSys Chalcidoidea Species Diversity Per Family (Red Line) Compared to the Universal Chalcidoidea Database (UCDB) Species Diversity (Blue Line). The Number of Species Is Presented between Parenthesis Close to the Family Name. Source: IndoBioSys/UCDB.

 

1.3 Objective

This manuscript aimed to establish the taxonomic and biological aspects of the Family Azotidae (Insecta: Hymenoptera).

 

2 METHODS

The method used to prepare this mini review was Marchiori 2021 methodology[13].

 

3 STUDIES CONDUCTED AND SELECTED

3.1 Study 1

Biology and taxonomy of the genus Ablerus in Spain.

Specie: Ablerus sp.

 

Transverse head, with pale lines or sutures, general groove present. Female antenna with 7 knuckles, funicular with 4 knuckles, the 3rd slightly reduced, apical nail entire or weakly divided, often with some knuckles alternately light and dark. Male antenna with funicular with 4 knuckles, F3 very small. 3-toothed jaws (Figure 6).

 

Figure 6. Ablerus Howard, 1894. Source: http://www.waspweb.org/chalcidoidea/Azotidae/Ablerus/Ablerus_species.htm

 

Wings are long and slender, with smoky or hyaline patterns on the female, with thicker hairiness over dark areas, marginal long cilia, wing without oblique bald line, stigma vein with large rounded stigma, postmarginal vein absent. Constitutes short and oval shape chest. The Gaster is longer than the combined length of head and thorax together, female with prominent ovipositor. Tarsus with 5 knuckles[14-16].

 

Biology: On diaspidids and aleirodids, often hyperparasitoids. Genus with 7 species on the peninsula, 11 on the  mainland.

 

I counted 7 articles on the antennae, the 1st long white ringed with black or the reverse (not super visible on the photos) and the others alternately white and black. There is a laying organ, the abdomen is dark blue, and it seems to me that it has only one relatively thick and short rib on the forewings.

 

3.2 Study 2

Ablerus chrysomphali (Ghesquière, 1960).

 

Description: Black and slightly blue body. Yellow head, with black vertex. Black antennae, with pedicel apex, white F2 and F4. Black legs, with trochanters, the apex of the thighs and the base of the light tibias. Anterior wings female with a longitudinal smoky band, extending from the basal smoky area to the apical margin. Antenna with slightly thickened escape, subequal flagellates except the 3rd smallest mace as long as the last 3 flagellomas (Figure 7).

 

Figure 7. Ablerus chrysomphali (Ghesquière, 1960) (Azotidae). Source: http://ponent.atspace.org/fauna/ins/fam/azotidae/ablerus_azo.htm

 

Wing with rounded stigma, marginal vein with 4 long cilia on the margin, surface with thick arrows gathered in small groups below the marginal vein's apex, subapical on the anterior margin, longitudinal strip on the dark spot, long marginal cilia = 0.4x wide wing. Medium tibias with waiting as long as the basitars or almost.

 

Biology: Hyperparasitoid on diaspidids Chrysomphalus, Diaspidiotus, Lepidosaphes, Parlatoria and Contigaspis.

 

Distribution: Mediterranean: Palaearctic distribution (Figure 8).

 

Figure 8. Chrysomphalus (Hemiptera: Diaspididae). Source: https://www.biotaxa.org/Zootaxa/article/view/zootaxa.4759.4.9

 

Found in: Thymus vulgaris L. (Lamiaceae) (Figure 9).

 

Figure 9. Adult of Gelechiidae (Lepidoptera). Source: https://britishlepidoptera.weebly.com/35-gelechiidae.html

 

Biology: Hyperparasitoids of different hymenopteran primary parasitoids, including chalcidoids. Some species are confirmed as oophagous.

 

Number of taxa: World-1 genus and 94 species, Palaearctic-1/14, Russia-½.

 

Type: Especies: Centrodora clisiocampae Ashmead, 1894 (Hymenoptera: Aphelinidae). Cosmopolitan.

 

Number of species: World-94, Palaearctic-14, Russia-2.

 

Biology: Encyrtus, hemipterans from Diaspididae, Lasiocampidae and Aphelinidae.

 

Distribution: FE (PR). Azerbaijan and Australasia.

 

Biology: Ablerus pulcherrimus (Mercet, 1922) (Azotus). Diaspididae, Issidae. Russia: FE (PR). Europe (WE, SE, EE) (Figure 10).

 

Figure 10. Ablerus pulcherrimus (Mercet, 1922). Source: https://www.biodiversity4all.org/taxa/375478-Ablerus

 

Hosts: The whiteflies[14-16].

Azotidae Maltese Islands (Table 1) (Figure 11).

 

Table 1. Number of Species for Each Chalcidoidea Family Reported for the Maltese Islands

Notes: Source: https://www.um.edu.mt/library/oar/bitstream/123456789/12395/1/Chalcidoidea.pdf

 

Figure 11. Malaise Trap. Source: https://www.aimethods-lab.com/en/who-we-support/case-studies

 

3.3 Study 3

Azotidae from China.

Genus Ablerus Howard, 1894.

Distribution: Cosmopolitan.

 

1. Ablerus atomon (Walker, 1847) (Figure 12).

 

Figure 12. Ablerus atomon (Walker, 1847). Source: Pekka Malinen.

 

Hosts: Chionaspis stantophris Mercer, 1922, Chionaspis, Diaspidiotus and Leucaspis ulmi (L., 1758) and Aphelinidae (Figure 13).

 

Figure 13. Leucaspis Diaspididae Family. Source: http://v3.boldsystems.org/index.php/Taxbrowser_Taxonpage?taxid=593683

 

2. Ablerus pexus (Huang, 1994).

Host: Unknown.

Distribution: China (Fujian)[17-20].

 

3.4 Study 4

Egg parasitoid.

 

Parasitoids develop in the host's egg. Egg parasitoids are found in the following Families: Ichneumonidae, Encyrtidae, Mymaridae, Trichogrammatidae, Aphelinidae, Scelionidae Azotidae, Braconidae, Eurytomidae, Evaniidae, Pteromalidae, Signiphoridae, Eupelmidae, Tetracampidae, Eulophidae, Torymidae and Encyrtidae (Figure 14).

 

Figure 14. The Egg Parasitoid Wasp. Source: https://pk-photography.blogspot.com/2012/04/egg-parasitoid-wasp-trissolcus-basalis.html

 

Species of egg parasitoids: Telenomus edessae Fabricius, 1916, Telenomus podisi Ashmead, 1893, Telenomus sp., Ooencyrtus sp. (Encyrtidae) Trissolcus basalis (Wollaston, 1858), Trissolcus brochymenae Ashmead, 1881, Trissolcus sp., Trissolcus terettis Johnson, 1987, Trissolcus urichi Crawford, 1913 (Scelionidae), Anastatus auriceps Ashmead, 1904, Eupelmus sp. (Eupelmidae) and Ablerus sp. (Azotidae) (Figure 15)[21,22].

 

Figure 15. Life Cycle of an Egg Parastoid. Source: http://www.entomologa.ru/outline/263.htm

 

4 CONCLUSION

Little research has been conducted on the Azotidae Family, formerly considered a subfamily of the Aphelinidae Family. Therefore, this study was conducted to increase the knowledge of the bioecology, geographic distribution, and taxonomy of the Azotidae.

 

Acknowledgements

Not applicable.

 

Conflicts of Interest

The author declared no conflict of interest.

 

Author Contribution

Marchiori CH wrote the manuscript, provided all figures, and approved the final version.

 

References

[1] Hanson P, Gauld ID. The Hymenoptera of Costa Rica, 20th ed. Oxford University Press: Oxford, UK, 1995.

[2] Gibson GAP, Huber JT, Woolley JB. Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera), 1st ed. National Research Council Research Press: Ottawa, CA, 1997.

[3] Noyes JS. Universal Chalcidoidea database, 1st ed. The Natural History Museum: London, UK, 2003.

[4] Timms LL, Schwarzfeld M, Sääksjärvi IE. Extending understanding of latitudinal patterns in parasitoid wasp diversity. Insect Conserv Diver, 2016; 9: 74-86. DOI: 10.1111/icad.12144

[5] Broad GR. Checklist of British and Irish Hymenoptera-Introduction. Biodivers Data J, 2014; 2: e1113. DOI: 10.3897/BDJ.2.e1113

[6] Bennett AMR, Sheffield CS, Waard JR. Hymenoptera of Canada. Zookeys, 2019; 819: 311-360. DOI: 10.3897/zookeys.819.28510

[7] Heraty JM, Burks RA, Cruaud A et al. A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera). Cladistics, 2013; 29: 466-542.  DOI: 10.1111/cla.12006

[8] Medvedev GS. Key to insects of the European part of the USSR. Hymenoptera, 3rd ed. Institute of Zoology of Academy of Sciences of the USSR; Leningrad, USSR, 1978; 469-501.

[9] Belokobylskij SA, Samartsev KG, Ilinskaya AS. Annotated catalogue of the Hymenoptera of Russia. Apocrita: Parasitica. Proc Zool Inst Russ Acad Sci, 2019; 8: 10.31610. DOI: 10.31610/trudyzin/2019.supl.8.5

[10] Goulet H, Huber JT. Hymenoptera of the world: an identification guide to families, 1st ed. Research Branch Agriculture Canada: Ottawa, CA, 1993.

[11] Branstetter MG, Danforth BN, Pitts JP et al. Phylogenomic insights into the evolution of stinging wasps and the origins of ants and bees. Curr Biol, 2017; 27: 1019-1025. DOI: 10.1016/j.cub.2017.03.027

[12] Noyes JS. Universal Chalcidoidea Database. World wide web electronic publication. Accessed July 11, 2022. Available at https://www.nhm.ac.uk/our-science/data/chalcidoids/database

[13] Marchiori CH. Associations of mutillid wasps (Hymenoptera, Mutillidae) with eusocial insects. Open Access J Sci Technol, 2022; 5: 7-33. DOI: 10.53022/oarjst.2022.5.1.0049

[14] Askew RR, Blasco-Zumeta J, Pujade-Villar J. Chalcidoidea and Mymarommatoidea of a savin in the Monegros, 4th ed. Monographs Aragonese Emtomological Society: Sariñena, ES, 2001.

[15] Askew RR, Mifsud D. A preliminary check-list of the Chalcidoidea (Hymenoptera) of the Maltese Islands. Bull Entomol Soc Malta, 2016; 8: 47-72. DOI: 10.17387/BULLENTSOCMALTA.2016.04

[16] Farrugia C. Parasitic hymenoptera associated with scale insects on citrus trees in the Maltese Islands [master's thesis]. Valeta, MT: University of Malta; 1988.

[17] Wang ZH, Huang J, Polaszek A. The species of genus Ablerus Howard (Hymenoptera: Chalcidoidea: Azotidae) from China, with description of a new species. Fla Entomol, 2016; 99: 395-405. DOI: 10.1653/024.099.0310

[18] Xu ZH, Huang J. Chinese fauna of parasitic wasps on scale insects, 1st ed. Science and Technology Press: Shanghai, CN, 2004.

[19] Zhou QS, Polaszek A, Qin YG et al. Parasitoid-host associations of the genus Coccophagus (Hymenoptera: Aphelinidae) in China. Zool J Linn Soc, 2018; 182: 38-49. DOI: 10.1093/zoolinnean/zlx019

[20] Huang J. Systematic studies on Aphelinidae of China (Hymenoptera: Chalcidoidea). Contributions of the Biological Control Research Institute, Fujian Agricultural University Special Publication, 5th ed. Chongqing Publishing House: Chongqing, CN, 1994.

[21] Peters RS, Krogmann L, Mayer C et al. Evolutionary History of the Hymenoptera. Curr Biol, 2017; 27: 1013-1018. DOI: 10.1016/j.cub.2017.01.027

[22] Rafael JA. Insetos do Brasil: diversidade e taxonomia, 1st ed. Holos: Ribeirão Preto, BR, 2012.

 

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