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Type: Article
Published: 2020-06-09
Page range: 348–370
Abstract views: 92
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Comparative morphology of myrmecophilous immature stages of European Microdon species (Diptera: Syrphidae): updated identification key and new diagnostic characters

Department of Science, University Roma Tre, Viale G. Marconi 446, 00146 Rome, Italy. Laboratorio Interdipartimentale di Microscopia Elettronica (LIME), University Roma Tre, Rome, Italy.
Locks Park Farm, Hatherleigh, Okehampton, Devon, EX20 3LZ, England.
Department of Science, University Roma Tre, Viale G. Marconi 446, 00146 Rome, Italy.
Department of Science, University Roma Tre, Viale G. Marconi 446, 00146 Rome, Italy.
Department of Science, University Roma Tre, Viale G. Marconi 446, 00146 Rome, Italy. Laboratorio Interdipartimentale di Microscopia Elettronica (LIME), University Roma Tre, Rome, Italy.
Diptera Hoverflies Social Parasites Cryptic Species Myrmecophiles Ants

Abstract

Hoverflies (Diptera: Syrphidae) of the genus Microdon Meigen have larvae that live in ant nests where they are predatory on ant larvae. Reflecting the exceptional challenges of this very specialized lifestyle, Microdon eggs, larvae and puparia are highly distinctive in their morphology. Detailed descriptions of these immature stages is, however, lacking for all but a very few species, and much of this has been limited through the sole use of light microscopes. Here, using Scanning Electron Microscopy (SEM), we present detailed, comparative descriptions of the immature stages of three European Microdon species: M. analis, M. devius and M. myrmicae. Given that many adult Microdon species are very similar to each other in their outward appearance, we demonstrate that the morphology of their immature stages can improve our understanding of the phylogeny of the genus. We also discuss how particular adaptations of the immature morphology may allow their myrmecophilous life within ant nests. In this paper new diagnostic features are also presented to distinguish M. myrmicae from its sibling species M. mutabilis—the two are morphologically indistinguishable as adults.

 

References

  1. Agosti, D. & Collingwood, C.A. (1987) A provisional list of the Balkan ants (Hym. Formicidae) with a key to the worker caste. II. Key to the worker caste, including the European species without the Iberian. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 60, 261–293.

    Akre, R.D., Alpert, G. & Alpert, T. (1973) Life cycle and behaviour of Microdon cothurnatus in Washington (Diptera: Syrphidae). Journal of the Kansas Entomological Society, 46, 327–338.

    Andrić, A., Šikoparija, B., Obreht, D., Đan, M., Preradović, J., Radenković, S., Pérez-Bañón, C. & Vujić, A. (2014) DNA barcoding applied: identifying the larva of Merodon avidus (Diptera: Syrphidae). Acta Entomologica Musei Nationalis Pragae, 54, 741–757.

    Bot, S. & Van De Meutter, F. (2018) Veldgids Zweefvliegen. KNNV Uitgeverij, Zeist, pp. 388.

    Cammaerts, R. (1995) Regurgitation behaviour of the Lasius flavus worker (Formicidae) towards the myrmecophilous beetle Claviger testaceus (Pselaphidae) and other recipients. Behavioural Processes, 34 (3), 241–264.

    https://doi.org/10.1016/0376-6357(94)00068-R

    Campoy, A., Pérez-Bañón, C., Nielsen, T. & Rojo, S. (2017) Micromorphology of egg and larva of Eristalis fratercula, with an updated key of Eristalis species with known third instar larvae (Diptera: Syrphidae). Acta Entomologica Musei Nationalis Pragae, 57, 215–227.

    https://doi.org/10.1515/aemnp-2017-0070

    Courtney, G.W., Sinclair, B.J. & Mejer, R. (2000) Morphology and terminology of Diptera larvae. In: Papp, L. & Darvas, B. (Eds.), Contributions to a Manual of Palaearctic Diptera. Vol. 1. Science Herald, Budapest, pp. 85–161.

    Czehowski, W., Radchenko, A. & Czehowska, W. (2002) The Ants of Poland. Natura Optima Dux Foundation, Warszawa, 496 pp.

    Di Giulio, A., Maurizi, E., Hlavac, P. & Moore, W. (2011) The long awaited first instar larva of Paussus favieri (Coleoptera: Carabidae: Paussini). European Journal of Entomology, 108, 127–138.

    https://doi.org/10.14411/eje.2011.016

    Di Giulio, A., Maurizi, E., Barbero, F., Sala, M., Fattorini, S., Balletto, E. & Bonelli, S. (2015). The Pied Piper: A Parasitic Beetle’s Melodies Modulate Ant Behaviours. PLoS ONE, 10 (7), e0130541.

    https://doi.org/10.1371/journal.pone.0130541

    Doczkal, D. & Schmid, U. (1999) Revision der mitteleiropäischen Arten der Gattung Microdon Meigen (Diptera, Syrphidae). Volucella, 4, 45–68.

    Gammelmo, Ø. & Aarvik, L. (2007) The myrmecophilous fly Microdon myrmicae Schönrogge et al., 2002 (Diptera, Syrphidae) in Norway. The Norwegian Journal of Entomology, 54, 43–48.

    Garnett, W.B., Akre, R.D. & Zack, R.S. (1990) External morphology of four species of Microdon immatures (Diptera: Syrphidae) from the Pacific Northwest. Annals of the Entomological Society of America, 83, 68–80.

    https://doi.org/10.1093/aesa/83.1.68

    Haas, F. (1924) Un Insecto Burlador. Buttleti de la Institució Catalána d’Història Natural, 4 (2), 148–149.

    Hölldobler, B. & Wilson, E.O. (1990) The Ants. Springer, Berlin, 739 pp.

    https://doi.org/10.1007/978-3-662-10306-7

    Ivens, A.B.F., von Beeren, C., Bluthgen, N. & Kronauer, D.J.C. (2016) Studying the complex communities of ants and their symbionts using ecological network analysis. Annual Review of Entomology, 61, 353–371.

    https://doi.org/10.1146/annurev-ento-010715-023719

    Lachaud J.P., Klompen, H. & Pérez-Lachaud, G. (2016) Macrodinychus mites as parasitoids of invasive ants: an overlooked parasitic association. Scientific Reports, 6, 29995.

    https://doi.org/10.1038/srep29995

    Pape, T., Beuk, P., Pont, A.C., Shatalkin, A.I., Ozerov, A.L., Woźnica, A.J., Merz, B., Bystrowski, C., Raper, C., Bergström, C., Kehlmaier, C., Clements, D.K., Greathead, D-, Kameneva, E.P., Nartshuk, E., Petersen, F.T., Weber, G., Bächli, G., Geller-Grimm, F., Van de Weyer, G., Tschorsnig, H.P., de Jong, H., van Zuijlen, J.W., Vaňhara, J., Roháček, J., Ziegler, J., Majer, J., Hůrka, K., Holston, K., Rognes, K., Greve-Jensen, L., Munari, L., de Meyer, M., Pollet, M., Speight, M.C., Ebejer, M.J., Martinez, M., Carles-Tolrá, M., Földvári, M., Chvála, M., Barták, M., Evenhuis, N.L., Chandler, P.J., Cerretti, P., Meier, R., Rozkosny, R., Prescher, S., Gaimari, S.D., Zatwarnicki, T., Zeegers, T., Dikow, T., Korneyev, V.A., Richter, V.A., Michelsen, V., Tanasijtshuk, V.N., Mathis, W.N., Hubenov, Z. & de Jong, Y. (2015) Fauna europaea: Diptera—brachycera. Biodiversity Data Journal, 3, e4187.

    https://doi.org/10.3897/BDJ.3.e4187

    Parker, J. & Grimaldi, D.A. (2014) Specialized myrmecophily at the ecological dawn of modern ants. Current Biology, 24, 2428–2434.

    https://doi.org/10.1016/j.cub.2014.08.068

    Pérez-Bañón, C., Hurtado, P., García-Gras, E. & Rojo, S. (2013) SEM Studies on immature stages of the Drone Flies (Diptera, Syrphidae): Eristalis similis (Fallen, 1817) and Eristalis tenax (Linnaeus, 1758). Microscopy Research and Technique, 76, 853–861.

    https://doi.org/10.1002/jemt.22239

    Pérez-Lachaud, G., Jervis, M.A., Reemer, M. & Lachaud, J.P. (2014) An unusual, but not unexpected, evolutionary step taken by syrphid flies: the first record of true primary parasitoidism of ants by Microdontinae. Biological Journal of The Linnean Society, 111, 462–472.

    https://doi.org/10.1111/bij.12220

    Reemer, M. (2012) Unravelling a Hotchpotch. Phylogeny and Classification of the Microdontinae (Diptera: Syrphidae). PhD thesis, Leiden University, Leiden, 384 pp.

    Reemer, M. (2013) Review and phylogenetic evaluation of associations between Microdontinae (Diptera: Syrphidae) and ants (Hymenoptera: Formicidae). Psyche, 538316, 1–9.

    https://doi.org/10.1155/2013/538316

    Reemer, M. & Ståhls, G. (2013a) Generic revision and species classification of Microdontinae (Diptera, Syrphidae). ZooKeys, 288, 1–213.

    https://doi.org/10.3897/zookeys.288.4095

    Reemer, M. & Ståhls, G. (2013b) Phylogenetic relationships of Microdontinae (Diptera: Syrphidae) based on molecular and morphological characters. Systematic Entomology, 38, 661–688.

    https://doi.org/10.1111/syen.12020

    Ricarte, A., Souba-Dols, G.J., Hauser, M., Marcos-García, M.Á. (2017) A review of the early stages and host plants of the genera Eumerus and Merodon (Diptera: Syrphidae), with new data on four species. PLoS ONE 12, e0189852.

    https://doi.org/10.1371/journal.pone.0189852

    Rotheray, G.E. (1991) Larval stages of 17 rare and poorly known British hoverflies (Diptera: Syrphidae). The Journal of Natural History, 25, 945–969.

    https://doi.org/10.1080/00222939100770621

    Rotheray, G.E. & Gilbert, F. (1999) Phylogeny of Palaearctic Syrphidae (Diptera): evidence from larval stages. Zoological Journal of Linnean Society, 127, 1112.

    https://doi.org/10.1111/j.1096-3642.1999.tb01305.x

    Rotheray, G.E. & Gilbert, F. (2011) The natural history of hoverflies. Forrest text, Tresaith, Wales, xiii + 333 pp.

    Scarparo, G., Cerretti, P., Mei, M. & Di Giulio, A. (2017) Detailed morphological descriptions of the immature stages of the ant parasite Microdon mutabilis (Diptera: Syrphidae: Microdontinae) and a discussion of its functional morphology, behaviour and host specificity. European Journal of Entomology, 114, 565–586.

    https://doi.org/10.14411/eje.2017.071

    Schmid, U. (2004) Microdon rhenanus and Microdon eggeri var. major (Diptera, Syrphidae) revisited. Volucella, 7, 111–124.

    Schönrogge, K., Barr, B., Wardlaw, W.J.C., Napper, E., Gardner, M.G., Breen, J., Elmes, G.W. & Thomas, J.A. (2002) When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biological Journal of The Linnean Society, 75, 291–300.

    https://doi.org/10.1111/j.1095-8312.2002.tb02070.x

    Speight, M.C.D. (1987) External morphology of adult Syrphidae (Diptera). Tijdschrift voor Entomologie, 130, 141–175.

    Speight, M.C.D. (2004) Fauna Europaea: Syrphidae. In: Pape, T. (Ed.), Fauna Europaea: Diptera, Brachycera. Version 1.1. Available from: http://www.faunaeur.org (accessed 15 May 2018)

    Speight, M.C.D. (2013) Species accounts of European Syrphidae (Diptera). In: Speight, M.C.D., Castella, E., Sarthou, J.P. & Monteil, C. (Eds.), Syrph the Net, the Database of European Syrphidae. Vol. 72. Syrph the Net Publications, Dublin, pp. 1–316.

    Speight, M.C.D. & Sarthou, J.-P. (2017) StN keys for the identification of the European species of various genera of Syrphidae 2017. In: Speight, M.C.D., Castella, E., Sarthou, J.P. & Monteil, C. (Eds.), Syrph the Net, the database of European Syrphidae (Diptera). Vol. 99. Syrph the Net publications, Dublin, pp. 1–139.

    Ståhls, G., Hippa, H., Rotheray, G., Muona, J. & Gilbert, F. (2003) Phylogeny of Syrphidae (Diptera) inferred from combined analysis of molecular and morphological characters. Systematic Entomology, 28, 433–450.

    https://doi.org/10.1046/j.1365-3113.2003.00225.x

    Thomas, J.A., Schönrogge, K. & Elmes, G.W. (2005) Specializations and host associations of social parasites of ants. In: Fellowes, M.D.E., Holloway, G.J. & Rolff, J. (Eds.), Insect Evolutionary Ecology. CABI, Wallingford, pp. 479–518.

    https://doi.org/10.1079/9780851998121.0479

    Thompson, F.C. (1972) A contribution to a generic revision of the Neotropical Milesinae (Diptera: Syrphidae). Arquivos de Zoologia, 23, 73–215.

    Thompson, F.C. (1981) Revisionary notes on nearctic Microdon flies (Diptera: Syrphidae). Proceedings of the entomological Society of Washington, 83 (4), 725–758.

    Van Veen, M.P. (2010) Hoverflies of Northwest Europe, Identification Keys to the Syrphidae. KNNV Publishing, Utrecht, 254 pp.

    https://doi.org/10.13140/RG.2.1.3697.4567

    Wheeler, W.M. (1908) Studies on myrmecophiles. III. Microdon. Journal of the New York Entomological Society, 16, 202–213.

    Witek, M., Patricelli, D., Pietro Casacci, L., Barbero, F., Balletto, E. & Bonelli, S. (2011) Notes on the biology and host ant specificity of the myrmecophilous syrphid fly Microdon major (Diptera: Syrphidae), a social parasite of Formica ants (Hymenoptera: Formicidae). Sociobiology, 57 (2), 261–269.

    Wolton, R. (2011) Observations on ecology and behaviour of Microdon myrmicae Schönrogge et al. (Diptera, Syrphidae), with a description of egg and early instar morphology. Dipterists Digest, 18, 55–67.

    Young, A.D., Lemmon, A.R., Skevington, J.H., Mengual, X., Ståhls, G., Reemer, M., Jordaens, K., Lemmon, E. M., Hauser, M., De Meyer, M., Misof, B. & Wiegmann, B.M. (2016) Anchored enrichment dataset for true flies (order Diptera) reveals insights into the phylogeny of flower flies (family Syrphidae). BMC Evolutionary Biology, 16 (143), 1–13.

    https://doi.org/10.1186/s12862-016-0714-0