Tritrophic associations and identification key for European species of the genus Binodoxys (Mackauer) (Hymenoptera: Braconidae: Aphidiinae)

Authors

  • Maja J. Lazarević University of Niš, Faculty of Sciences and Mathematics, Department of Biology and Ecology, Višegradska 33, 18000 Niš, Serbia https://orcid.org/0000-0002-5644-8176
  • Vladimir A. Žikić University of Niš, Faculty of Sciences and Mathematics, Department of Biology and Ecology, Višegradska 33, 18000 Niš, Serbia https://orcid.org/0000-0001-5716-8355
  • Darija N. Milenković University of Niš, Faculty of Sciences and Mathematics, Department of Biology and Ecology, Višegradska 33, 18000 Niš, Serbia https://orcid.org/0000-0003-1766-4252
  • Željko M. Tomanović 1. University of Belgrade, Faculty of Biology, Institute of Zoology, Studentski trg 16, 11158 Belgrade, Serbia; 2. Serbian Academy of Sciences and Arts, Kneza Mihaila 35, 11000 Belgrade, Serbia https://orcid.org/0000-0002-5063-5480

DOI:

https://doi.org/10.2298/ABS240510020L

Keywords:

Binodoxys, food chains, Europe, determination key, molecular analysis

Abstract

Paper description:

  • The genus Binodoxys, though widely distributed globally, is represented by only nine species in Europe.
  • Through a comprehensive literature review, morphological examination, and molecular analysis, this study elucidates tri-trophic associations and genetic distances.
  • New hosts were identified. Binodoxys similis exhibited a broader geographical distribution.
  • This research provides insights into the biology, morphology, and genetic diversity of European Binodoxys species, and a key for identification.

Abstract: The genus Binodoxys includes only nine species found in Europe, yet despite its frequent occurrence, it remains insufficiently studied. This study addresses this knowledge gap through an exhaustive literature review and material collection, and a compilation of a comprehensive list detailing tritrophic associations. Based on the available molecular data, we constructed a maximum likelihood tree and a TSC (‘Statistical Parsimony’) haplotype network for six European species. Several new hosts were identified for the first time, and the geographical distribution of one species was broadened. An identification key for females of European Binodoxys species is provided. Future studies should prioritize gathering host data and investigate the existence of cryptic species among polyphagous species. Furthermore, the status of the three species not analyzed in this study due to the lack of material should be investigated by encompassing both morphological and molecular approaches.

Downloads

Download data is not yet available.

References

Godfray HC. Parasitoids: behavioral and evolutionary ecology. Princeton University Press; 1994.

Chen XX, Achterberg C van. Systematics, phylogeny, and evolution of braconid wasps: 30 years of progress. Annu. Rev. Entom.. 2019;64:335-58. https://doi.org/10.1146/annurev-ento-011118-111856

Petrović A. Sizing the knowledge gap in taxonomy: The last dozen years of Aphidiinae research. Insects. 2022;13(2):170. https://doi.org/10.3390/insects13020170

Smith CF. The Aphidiinae of North America (Braconidae: Hymenoptera). The Aphidiinae of North America (Braconidae: Hymenoptera). Ohio State University; 1944. 154 p.

Mackauer M. Insect parasites of the green peach aphid, Myzus persicae Sulz., and their control potential. Entomophaga. 1968;13(2):91-106. https://doi.org/10.1007/BF02371780

Starý P, Rakhshani E, Havelka J, Tomanović Ž, Kavallieratos NG, Sharkey M. Review and key to the world parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Greenideinae aphids (Hemiptera: Aphididae), including notes on invasive pest species. Ann. Entomol. Soc. Am. 2010;103(3):307-21. https://doi.org/10.1603/AN09127

Kula RR, Johnson PJ, Heidel-Baker TT, Boe A. A new species of Acanthocaudus Smith (Braconidae: Aphidiinae), with a key to species and new host and distribution records for aphidiines associated with Silphium perfoliatum L. (Asterales: Asteraceae). Zootaxa. 2017;4236(3):543-52. https://doi.org/10.11646/ZOOTAXA.4236.3.8

Žikić V, Lazarević M, Milošević D. Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae). Zool. Anz. 2017a;268:75-83. https://doi.org/10.1016/j.jcz.2016.10.001

Boivin G, Hance T, Brodeur J. Aphid parasitoids in biological control. Can. J. Plant Sci. 2012;92(1):1-12. https://doi.org/10.4141/cjps2011-045

Achterberg C van, de Zugasti Carrón NF. Revision of the genus Paralipsis Foerster, 1863 (Hymenoptera, Braconidae), with the description of two new species. ZooKeys. 2016;(606):25-39. https://doi.org/10.3897/zookeys.606.9656

Kavallieratos NG, Lykouressis DP, Sarlis GP, Stathas GJ, Segovia AS, Athanassiou CG. The Aphidiinae (Hymenoptera: Ichneumonoidea: Braconidae) of Greece. Phytoparasitica. 2001;29:306-40. https://doi.org/10.1007/BF02981847

Tomanović Ž, Kavallieratos NG, Athanassiou CG, Stanisavljević LS. A review of the West Palaearctic aphidiines (Hymenoptera: Braconidae: Aphidiinae) parasitic on Uroleucon spp., with the description of a new species. Ann. Soc. Entomol. Fr. 2003;39(4)343-353. https://doi.org/10.1080/00379271.2003.10697392

Tomanović Ž, Kavallieratos N, Starý P, Žikić V, Tomić V, Lučić L. Redescription of two species of Aphidiinae (Hymenoptera: Braconidae) from high mountain areas of south-eastern Europe, with biological and biogeographical notes on co-occurring guild members. Entomol. Fenn. 2007;18(1):36-45. https://doi.org/10.33338/ef.84375

Derocles SA, Plantegenest M, RASPLUS JY, Marie A, Evans DM, Lunt DH, Le Ralec A. Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes? Syst. Entomol. 2016;41(2):379-91. https://doi.org/10.1111/syen.12160

Mackauer M. Die mittel-, west-und nordeuropäischen Arten der Gattung Trioxys Haliday (Hymenoptera: Braconidae, Aphidiinae). Eine monographische Revision. Beit. Entomol.= Contrib. Entomol. 1959;9(1-2):144-79. https://doi.org/10.21248/contrib.entomol.9.1-2.144-179

Mackauer M. Trioxys similis n. sp. (Hym. Braconidae, Aphidiinae), eine neue Blattlaus-Schlupfwespe aus Frankreich: Nebst einigen biocönologischen und nomenklatorischen Bemerkungen. Entomophaga. 1959;4:303-9. https://doi.org/10.1007/BF02373366

Mackauer M. Zur Systematik der Gattung Trioxys Haliday (Hymenoptera: Braconidae, Aphidiinae). Beit. Entomol.= Contrib. Entomol. 1960;10(1-2):137-60. https://doi.org/10.21248/contrib.entomol.10.1-2.137-160

Akhtar MS, Dey D, Usmani MK. 0151. A catalogue of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) from India. Insecta Mundi. 2011;11:1-31.

Yu DS, Achterberg C van, Horstmann K. Taxapad 2016. In: Ichneumonoidea 2016–Database on Flash–Drive; Ottawa, ON, Canada: ScienceOpen; 2016.

Starý P. Biology of Aphid Parasites (Hymenoptera: Aphidiidae) with respect to integrated control. Dordrecht: Springer; 1970. 644 p. (Series Entomologica; Vol. 6).

Starý, P. Biosystematical classification of Trioxys Hal. And related genera (Hymenoptera, Aphidiidae). Boll. Lab. Entomol. Agrar. 1981a;38:85-93.

Davidian EM. Check-list of the Aphidiid-Wasp subfamily Trioxinae (Hymenoptera, Aphidiidae) from Russia and adjacent countries. Entomol. Rev. 2016;96:1268-88. https://doi.org/10.1134/S0013873816090098

Davidian EM, Belokobylskij SA. New species of the aphid parasitoids of the genus Binodoxys Mackauer (Hymenoptera: Braconidae: Aphidiinae) from the fauna of Russia. Zootaxa. 2022;5209(3):373-8. https://doi.org/10.11646/zootaxa.5209.3.6

Kavallieratos NG, Tomanović Ž, Athanassiou CG, Starý P, Žikić V, Sarlis GP, Fasseas C. Aphid parasitoids infesting cotton, citrus, tobacco, and cereal crops in southeastern Europe: aphid-plant associations and keys. Can. Entomol. 2005;137(5):516-31. https://doi.org/10.4039/n05-020

Tomanović Ž, Žikić V, Petrović A. Fauna parazidoidnih osа (Hymenoptera, Braconidae, Aphidiinae) Srbije. Beograd: Srpska akademija nauka i umetnosti; 2021. 262 p.

Blackman RL, Eastop VF. Aphids on the World’s Plants: An online identification and information guide [Internet]. Chhichester: Wiley & Sons Ltd.; 2018 [cited 2023 Dec 17]. Available from: http://www. aphidsonworldsplants.info.

Hebert PD, Cywinska A, Ball SL, DeWaard JR. Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B. Biol. Sci.. 2003;270(1512):313-21. https://doi.org/10.1098/rspb.2002.2218

Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 2021;38(7):3022-7. https://doi.org/10.1093/molbev/msab120

Nei M, Kumar S. Molecular evolution and phylogenetics. Oxford University Press, USA; 2000.

Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980;16:111-20. https://doi.org/10.1007/BF01731581.

Čkrkić J, Petrović A, Kocić K, Ye Z, Vollhardt IM, Hebert PD, Traugott M, Tomanović Ž. Hidden in plain sight: Phylogeography of an overlooked parasitoid species Trioxys sunnysidensis Fulbright & Pike (Hymenoptera: Braconidae: Aphidiinae). Agr. Forest Entomol. 2019;21(3):299-308. https://doi.org/10.1111/afe.12332

Derocles SA, Le Ralec A, Plantegenest M, Chaubet B, Cruaud C, Cruaud A, RASPLUS JY. Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae). Mol. Ecol. Res. 2012;12(2):197-208. https://doi.org/10.1111/j.1755-0998.2011.03083.x

Derocles SA, Lunt DH, Berthe SC, Nichols PC, Moss ED, Evans DM. Climate warming alters the structure of farmland tritrophic ecological networks and reduces crop yield. Mol. Ecol. 2018;27(23):4931-46. https://doi.org/10.1111/mec.14903

Elias M, Fontaine C, Van Veen FF. Evolutionary history and ecological processes shape a local multilevel antagonistic network. Curr. Biol. 2013;23(14):1355-9. https://doi.org/10.1016/j.cub.2013.05.066

Lazarević M, Stanković SS, Petrović A, Milošević MI, Tomanović Ž, Ivanović A, Žikić V. Comparative morphometric analysis of petioles and forewings of the European Binodoxys Mackauer species (Hymenoptera: Braconidae: Aphidiinae). Zool. Anz. 2020;284:7-15. https://doi.org/10.1016/j.jcz.2019.10.003

Žikić V, Stanković SS, Petrović A, Ilić Milošević M, Tomanović Ž, Klingenberg CP, Ivanović A. Evolutionary relationships of wing venation and wing size and shape in Aphidiinae (Hymenoptera: Braconidae). Org. Div. Evol. 2017;17:607-17. https://doi.org/10.1007/s13127-017-0338-2

Starý P. The Foci of Aphid Parasites (Hymenoptera, Aphidhdae) in Nature. Państwowe Wydawnictwo Naukowe. Oddział. 1964;12:529-54.

Starý P. A review of hymenopterous parasites of citrus pest aphids of the world and biological control projects (Hym., Aphidiidae; Hom., Aphidoidea). Acta Entomol. Bohemoslov. 1967;64:37-61.

Čkrkić J, Petrović A, Kocić K, Tomanović Ž. Insights into phylogenetic relationships between Trioxys Haliday, 1833 and Binodoxys Mackauer, 1960 (Hymenoptera, Braconidae, Aphidiinae), with a description of a new species of the genus Trioxys. Zoosystema. 2021;43(8):145-54. https://doi.org/10.5252/zoosystema2021v43a8

Kavallieratos NG, Tomanović Ž, Starý P, Athanassiou CG, Sarlis GP, Petrović O, Niketić M, Veroniki MA. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology. 2004;39(3):527-63. https://doi.org/10.1303/aez.2004.527

Mackauer M. Blattlaus-Schlupfwespen der Sammlung FP Müller, Rostock (Hymenoptera: Ichneumonoidea; Aphidiidae). Beit. Entomol.= Contrib. Entomol. 1962;12(5-6):631-61. https://doi.org/10.21248/contrib.entomol.12.5-6.631-661

Starý P. Aphid parasitoids of the Czech Republic. Prague: Academia. 2006. 292 p.

Starý P, Remaudière G, Leclant F. Nouvelles données sur les Aphidiides de France (Hym.). Ann. Soc. Entomol. Fr. 1973;9(2):309-29. https://doi.org/10.1080/21686351.1973.12278139

Downloads

Published

2024-10-25

How to Cite

1.
Lazarević MJ, Žikić VA, Milenković DN, Tomanović Željko M. Tritrophic associations and identification key for European species of the genus Binodoxys (Mackauer) (Hymenoptera: Braconidae: Aphidiinae). Arch Biol Sci [Internet]. 2024Oct.25 [cited 2024Dec.22];76(3):281-30. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/9833

Issue

Section

Articles

Most read articles by the same author(s)