(Diptera: Syrphidae), a Social Parasite of Myrmica Ants
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Ecological Entomology (2011), 36, 135–143 DOI: 10.1111/j.1365-2311.2010.01253.x Distribution, host specificity, and the potential for cryptic speciation in hoverfly Microdon myrmicae (Diptera: Syrphidae), a social parasite of Myrmica ants SIMONA BONELLI,1 MAGDALENA WITEK,1 SARA CANTERINO,2 MARCIN SIELEZNIEW,3 ANNA STANKIEWICZ-FIEDUREK,4 ANDRAS´ TARTALLY,5,6 EMILIO BALLETTO1 andKARSTEN SCHONROGGE˝ 7 1Department of Animal and Human Biology, University of Turin, Turin, Italy, 2Department of Arboriculture and Pomology, University of Turin, Grugliasco, Italy, 3Department of Invertebrate Zoology, University of Białystok, Białystok, Poland, 4Laboratory of Social and Myrmecophilous Insects, Museum and Institute of Zoology, Polish Academy of Sciences, Warszawa, Poland, 5Department of Biology, Centre for Social Evolution, University of Copenhagen, Copenhagen, Denmark, 6Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary and 7Centre for Ecology and Hydrology, Wallingford, U.K. Abstract. 1. In 2002 Microdon myrmicae, a social parasite of Myrmica ants, was taxonomically separated from Microdon mutabilis. The original study in the U.K. found Microdon myrmicae to be specific to one ant species, Myrmica scabrinodis,yet it became apparent that the range of Microdon myrmicae includes at least the western Palaearctic. 2. Current knowledge of the European distributions of both Microdon myrmicae and Microdon mutabilis in Europe is reviewed. Also, in detailed studies of two Polish populations, Microdon myrmicae was found to survive equally well with two Myrmica ant species. We examine, however, the possibility that this reflects the presence of two separate Microdon species, each connected to one species of Myrmica. 3. Forty populations of Microdon myrmicae and 37 populations of Microdon mutabilis are currently known in Europe. All the populations in central and southern Europe that were visited after the separation of the two species were identified as Microdon myrmicae, while Microdon mutabilis’ recognised range is now restricted to the British Isles and Scandinavia. Myrmica scabrinodis was found to host Microdon myrmicae in 26 out of 31 populations investigated. Four other Myrmica species were identified to the host Microdon myrmicae: Myrmica gallienii (eight populations), Myrmica rubra (four), Myrmica vandeli (one), and Myrmica sabuleti (one). Microdon myrmicae occurs in waterlogged grassland habitats, mainly of the ‘Molinietum’ type, resulting in a patchy distribution relative to its host ants. 4. In two populations Myrmica scabrinodis and Myrmica gallienii are both abundant and rear Microdon myrmicae in equal proportions. Microdon myrmicae pupae from Myrmica gallienii nests were heavier and the anterior respiratory organs were of significantly different shape. In contrast, the comparisons of Microdon myrmicae pupae among all other populations showed no significant differences, suggesting only one species throughout the European range. Key words. Cryptic lineages, distributions, habitat preferences, Microdon,myrme- cophily. Correspondence: Simona Bonelli, Department of Animal and Human Biology, University of Turin, Via Accademia Albertina 13, 10126 Turin, Italy. E-mail: [email protected] © 2011 The Authors Ecological Entomology © 2011 The Royal Entomological Society 135 136 Simona Bonelli et al. Introduction from Microdon mutabilis are in morphological traits of the pupae and – according to the original study carried out in Non-ant social parasites in ant colonies, so-called myrme- the British Isles – in their host use, with Microdon mutabilis cophiles, have long been seen as enigmatic species in con- being specific to colonies of Formica lemani (Bondroit) and servation, partly because they have been shown to be very Microdon myrmicae to those of Myrmica scabrinodis (Nylan- sensitive to environmental change, but also because a large pro- der) (Schonrogge¨ et al., 2002). portion of species is recorded as rare and endangered (Settele Since the description of Microdon myrmicae, it has been &Kuhn,¨ 2009; Thomas et al., 2009). Yet, the conservation of recorded from Ireland, Sweden, Norway, the Netherlands, these species depends largely on gaining a good understand- Germany, Switzerland, Hungary, and Poland (Speight, 2002, ing of their host ant specificity, as well as on how consistent 2003; Stankiewicz, 2003; Beuker, 2004; Schmid, 2004; Bonelli such specificity is at a larger geographical scale (Thomas et al., et al., 2005; Gammelmo & Aarvik, 2007; Bartsch, 2009). Lit- 2005, 2009). This is particularly the case for Microdon myrmi- tle is known, however, about the consistency of host use by cae, which was separated from Microdon mutabilis on patterns Microdon myrmicae at a European scale. Polish Microdon of its host ant use in the British Isles (Schonrogge¨ et al., 2002; myrmicae have been recorded from Myrmica gallienii (Bon- Thomas et al., 2005). Resolving questions on its patterns of droit), a species absent from the U.K. and Myrmica rubra host ant specificity on a broader geographical scale and on (Stankiewicz, 2003), yet the extent to which these species are how such variation might arise will be important for ensuring used by Microdon myrmicae is unclear. Also, beyond infor- its long-term survival. mation on the presence of the species in various countries Obligate social parasites of ants is a species-rich group with of Europe, very little is known about potential differences in an estimated 10 000 species worldwide, many of which are life-cycles or host use between populations of Microdon myr- listed in national and international red data books (Thomas micae across Europe as they have been described for other et al., 2005). Parasites of social insects and other parasitic social parasites such as Maculinea butterflies (Als et al., 2002; organisms are thought to be particularly prone to evolve cryptic Thomas et al., 2005; Nash et al., 2008). This may be an impor- lineages. The ability to circumvent host defences provides tant issue since Schonrogge¨ et al. (2002) suggest that Microdon strong selection, although often on physiological rather than hoverflies, as in other myrmecophilous social parasites, may morphological traits. One example is the use of chemical be prone to cryptic speciation. Selection on traits important mimicry to infiltrate host ant colonies (Akino et al., 1999; for the ant–parasite interaction is likely to be strong, yet the Elmes et al., 1999; Schonrogge¨ et al., 2004). The intricacy of traits themselves are likely to be physiological rather than the subterfuge for social parasites interacting with ants has morphological (Akino et al., 1999; Nash et al., 2008). The been demonstrated in detailed studies of chemical mimicry in existence of cryptic species has been demonstrated in many Maculinea butterflies (Akino et al., 1999; Thomas et al., 2002; different taxonomic groups, yet where cryptic lineages com- Schonrogge¨ et al., 2004; Thomas & Settele, 2004; Nash et al., prise a species complex of rare and endangered species with 2008). In one host–parasite pair, Myrmica rubra (Linnaeus) different ecological requirements this poses a particular prob- and Maculinea alcon (Denis and Shiffermuller),¨ it has been lem to conservationists (Blaxter & Floyd, 2003; Stuart et al., demonstrated that the combination of recognition compounds 2006). varies in both species at population level such that mosaic type We assess the host range and host use of Microdon myrmicae coevolution is the most likely explanation (Nash et al., 2008). across a large part of its European range, and ask whether they Another less well-studied group of social parasites are hov- vary at scales of regions or populations. We also examine the erflies of the sub-family Microdontinae where 405 species larval and pupal morphologies for indications of further cryptic are currently recognised worldwide. Most of the species lineages within the species Microdon myrmicae. are tropical, but all appear to have associations with ants (Cheng & Thompson, 2008). A number of them are obli- gate myrmecophilous social parasites where they act as preda- Materials and methods tors of ant brood in the host colonies (Elmes et al., 1999; Schonrogge¨ et al., 2006), whereas the adult stage lives outside Surveys for this study were carried out between 2002 and 2009 the nests. Five species of the genus Microdon are known from in seven European countries: Italy, Hungary, Great Britain, Europe: Microdon analis (Macquart), Microdon miki (Doczkal Poland, Slovakia, Romania, and Ukraine. Thirty-one popula- &Schmid),Microdon devius (Linnaeus), Microdon mutabilis tions of Microdon myrmicae were investigated and specimens (Linnaeus), and Microdon myrmicae (Schonrogge¨ et al.) (see from one Microdon mutabilis population on the Burren in Doczkal & Schmid, 1999; Stankiewicz, 2003; Gammelmo Ireland were used as a reference (Fig. 1). & Aarvik, 2007). Microdon myrmicae and Microdon muta- Myrmica ant nests of all species present were opened and bilis larvae have been described as predators of ant brood searched for parasites from the end of April until July when (Schonrogge¨ et al., 2002, 2006; Thomas et al., 2005), while fully grown larvae, pupae, or fresh exuviae can be found in the other three species associate with ants the nature of the the ant nests. These later developmental stages of Microdon relationship is as yet largely unknown (Andries, 1912; Doczkal myrmicae move to the top of the nests where they are easier to & Schmid, 1999). The adult stages of both