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Myrmica Ants Host Highly Diverse Parasitic Communities: from Social Parasites to Microbes

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Myrmica Ants Host Highly Diverse Parasitic Communities: from Social Parasites to Microbes Insect. Soc. (2014) 61:307–323 DOI 10.1007/s00040-014-0362-6 Insectes Sociaux REVIEW ARTICLE Myrmica ants host highly diverse parasitic communities: from social parasites to microbes M. Witek · F. Barbero · B. Markó Received: 23 December 2013 / Revised: 16 July 2014 / Accepted: 18 July 2014 / Published online: 22 August 2014 © International Union for the Study of Social Insects (IUSSI) 2014 Abstract Myrmica ants have been model species for present limitations of the knowledge at present of their studies in a variety of disciplines, including insect physio- impact on individuals and host colony fitness. In conclu- logy, chemical communication, ant social dynamics, ant sion, we argue that Myrmica ants serve as remarkable population, community ecology, and ant interactions with resource for the evolution of a wide variety of associated other organisms. Species belonging to the genus Myrmica organisms. can be found in virtually every habitat within the temperate regions of the northern hemisphere and their biology and Keywords Host–parasite interaction · Maculinea · systematics have been thoroughly studied. These ants serve Microdon · Myrmecophily · Nematodes · Rickia as hosts to highly diverse parasitic organisms from socially wasmannii parasitic butterfly caterpillars to microbes, and many Myrmica species even evolved into parasitizing species of their own genus. These parasites have various impacts both The Red Ants of the genus Myrmica on the individuals and on the social structure of their hosts, ranging from morphological malformations to reduction in In the temperate zone of North America, Asia and Europe colony fitness. A comprehensive review of the parasitic one of the most common insect groups is the Red Ants of the organisms supported by Myrmica and the effects of these genus Myrmica (Radchenko and Elmes, 2010). There are organisms on individuals and on whole ant colonies has not about 180 described species belonging to the genus Myrmica yet been compiled. Here, we provide a review of the in the Holarctic. Most of the species, however, are found in interactions of these organisms with Myrmica ants by dis- Europe and Asia, while a smaller proportion occurs in North cussing host and parasite functional, behavioral or physio- America (Radchenko and Elmes, 2010). They occur in logical adaptations. In addition, for all “symbiont groups” virtually every terrestrial habitat, including meadows, for- of Myrmica ants described in this paper, we examine the ests, steppes and mountains (Radchenko and Elmes, 2010). The variations in the habitats occupied across the range are likely to result in different diets, habits, and ant or non-ant M. Witek and F. Barbero equally contributed to the manuscript. associations. Myrmica colonies contain on average 200–500 M. Witek (&) workers and usually one, but sometimes a few functional Museum and Institute of Zoology, Polish Academy of Science, queens (Elmes and Petal, 1990; Wardlaw and Elmes, 1996). Wilcza 64, 00-679 Warszawa, Poland New nests can be founded by a single newly mated queen or, e-mail: [email protected] quite often, through the process known as colony budding F. Barbero (Elmes et al., 1998). Oviposition starts in early spring and Department of Life Sciences and Systems Biology, University of lasts through the summer until autumn (Radchenko and Turin, Via Accademia Albertina 13, 10123 Turin, Italy Elmes, 2010). Parts of the larvae develop rapidly, but others enter diapause and overwinter (Fig. 1). The latter group B. Markó Hungarian Department of Biology and Ecology, Babeş-Bolyai includes both workers and all the gyne-presumptive larvae University, Clinicilor 5-7, 400006 Cluj-Napoca, Romania (Brian and Kelly, 1967). 123 308 M. Witek et al. Fig. 1 The life cycle of Myrmica ants (My.) and some of their frequent social parasites: Microdon myrmicae (Mi.), Maculinea alcon pneumonanthe ecotype (Ma.) and Lomechusa pubicollis. The fungal ectoparasite Rickia wasmannii is located inside the nest as it infects both workers and queens. Arrows reflect moments of entering and leaving host colony by social parasites. Numbers I, II, III, IV refer to particular larval instars Myrmica ants have been model species for studies in a as the current knowledge on the impact of these organisms variety of disciplines, including insect physiology, chemi- on the individuals, and on the colony structure of their cal communication, social dynamics, ant population and Myrmica hosts. community ecology, phylogeography and speciation (Rad- chenko and Elmes, 2010). There are slightly more than 700 scientific publications on Myrmica ants recorded on the Exploitation of an ant society: social parasites WoS (as of 12/05/2014), although most concentrate on a handful of species. In addition, a comprehensive mono- There are many definitions of social parasitism in ants (see graph on the biology and systematics of Myrmica ants in Buschinger, 2009). In our review we present organisms that the Palearctic has been recently published by Radchenko fit (i) the strict definition of social parasites, implying and Elmes (2010). interaction between two social species, and (ii) the more Myrmica ants support a highly diverse array of parasitic broad definition that applies to other insects exploiting the organisms, many of which also have conservation value resources of a single ant colony for a long period of time (see Thomas and Settele, 2004). The considerable amount (see also Nash and Boomsma, 2008). of published data on these parasitic species notwithstand- ing, a comprehensive review treating these organisms and Ants parasitizing ants their known or probable effects on Myrmica ants has not been published yet. In our paper, we focus on Myrmica ants Most ant social parasites of Myrmica species are members as hosts of many parasitic organisms belonging to various of the same genus (Radchenko and Elmes, 2003), with the taxonomic groups, including social parasites, ecto- and exception of Formicoxenus provancheri and F. quebecen- endoparasitic species, such as fungi and nematodes, and sis. These two latter species are xenobiotic ants, i.e., they microbial pathogens. Our aim is to review host and parasite are able to build their own nest and take care of their brood, functional, behavioral or physiological adaptations as well but they depend on their host for nutrition (Buschinger, 123 Myrmica Table 1 Records of association between Myrmica ant species and the wide spectrum of their parasites Taxonomic Parasite species Type of Myrmica host species References group of parasite association ants host highly diverse parasitic communities Ants Formicoxenus xenobiosis M. incompleta Francoeur et al., 1985 provancheri Formicoxenus xenobiosis M. alaskensis Francoeur et al., 1985 quebecensis Myrmica arnoldii temporal Myrmica sp. Radchenko and Elmes, 2010 inquilinism (?) Myrmica bibikoffi temporal M. sabuleti, M. spinosior Radchenko and Elmes, 2010 inquilinism Myrmica luteola temporal Myrmica sp. Radchenko and Elmes, 2010 inquilinism Myrmica semiparasitica temporal M. punctiventris Francoeur, 2007 inquilinism Myrmica vandeli temporal M. scabrinodis Radchenko and Elmes, 2010 inquilinism Myrmica nefaria not clear; M. rupestris Bharti, 2012 workers present Myrmica colax inquilinism M. striologaster Cole, 1957 Myrmica ereptrix inquilinism M. aimonissabaudiae Radchenko and Elmes, 2001 Myrmica hirsuta inquilinism M. sabuleti, M. lonae Radchenko and Elmes, 2010 Myrmica kabylica inquilinism M. cagnianti Radchenko and Elmes, 2010 Myrmica karavajevi inquilinism M. scabrinodis, M. sabuleti, M. lonae, M. rugulosa, M. Radchenko and Elmes, 2010; Witek et al., 2013a gallienii Myrmica lampra inquilinism M. alaskenisis Francoeur, 2002 Myrmica laurae inquilinism M. scabrinodis, M. spinosior Radchenko and Elmes, 2010 Myrmica lemasnei inquilinism M. sabuleti or M. spinosior Radchenko and Elmes, 2010 microgyne of M. rubra inquilinism M. rubra Radchenko and Elmes, 2010 Myrmica myrmicoxena inquilinism M. lobulicornis Radchenko and Elmes, 2010 Beetle Lomechusa pubicollis predatory/ Myrmica sp. Ho¨lldobler and Wilson, 1990 cuckoo 123 309 310 123 Table 1 continued Taxonomic Parasite species Type of Myrmica host species References group of parasite association Butterflies Maculinea alcon cuckoo M. ruginodis Thomas et al., 1989; Elmes et al., 1994; Als et al., 2004 pneumonanthe ecotype M. rubra Thomas et al., 1989; Elmes et al., 1994; Als et al., 2004 M. scabrinodis Ho¨ttinger et al., 2003; Elmes et al., 2003; Sielezniew and Stankiewicz, 2004; Tartally et al., 2008a; Witek et al., 2008 M. vandeli Sielezniew and Stankiewicz, 2004; Tartally et al., 2008a M. salina Tartally et al., 2008a M. aloba Arnaldo et al., 2011; Tartally et al., 2013 Maculinea alcon cuckoo M. schencki Thomas et al., 1989; Steiner et al., 2003; Stankiewicz et al., 2005a; Tartally cruciata ecotype et al., 2008a, Sielezniew and Dziekanska, 2009 M. sabuleti Thomas et al., 1989; Steiner et al., 2003; Tartally et al., 2008a M. scabrinodis Thomas et al., 1989; Steiner et al., 2003; Tartally et al., 2008a M. specioides Steiner et al., 2003;Tartally et al., 2008a M. sulcinodis Steiner et al., 2003 M. lonae Tartally et al., 2008a M. ruginodis Steiner et al., 2003 M. rugulosa Stankiewicz et al., 2005b Maculinea arion predatory M. sabuleti, M. scabrinodis Thomas et al., 1989; Sielezniew et al., 2010a M. schencki, M. lobicornis, M. hellenica, M. rugulosa Sielezniew and Stankiewicz, 2008; Sielezniew et al., 2010 Maculinea nausithous cuckoo/ M. lonae, M. sulcinodis Sielezniew et al., 2010b; Casacci et al., 2011 predatory
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