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A Review of Myrmecophily in Ant Nest Beetles (Coleoptera: Carabidae: Paussinae): Linking Early Observations with Recent Findings

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A Review of Myrmecophily in Ant Nest Beetles (Coleoptera: Carabidae: Paussinae): Linking Early Observations with Recent Findings Naturwissenschaften (2007) 94:871–894 DOI 10.1007/s00114-007-0271-x REVIEW A review of myrmecophily in ant nest beetles (Coleoptera: Carabidae: Paussinae): linking early observations with recent findings Stefanie F. Geiselhardt & Klaus Peschke & Peter Nagel Received: 15 November 2005 /Revised: 28 February 2007 /Accepted: 9 May 2007 / Published online: 12 June 2007 # Springer-Verlag 2007 Abstract Myrmecophily provides various examples of as “bombardier beetles” is not used in contact with host how social structures can be overcome to exploit vast and ants. We attempt to trace the evolution of myrmecophily in well-protected resources. Ant nest beetles (Paussinae) are paussines by reviewing important aspects of the association particularly well suited for ecological and evolutionary between paussine beetles and ants, i.e. morphological and considerations in the context of association with ants potential chemical adaptations, life cycle, host specificity, because life habits within the subfamily range from free- alimentation, parasitism and sound production. living and predatory in basal taxa to obligatory myrme- cophily in derived Paussini. Adult Paussini are accepted in Keywords Evolution of myrmecophily. Paussinae . the ant society, although parasitising the colony by preying Mimicry. Ant parasites . Defensive secretion . on ant brood. Host species mainly belong to the ant families Host specificity Myrmicinae and Formicinae, but at least several paussine genera are not host-specific. Morphological adaptations, such as special glands and associated tufts of hair Introduction (trichomes), characterise Paussini as typical myrmecophiles and lead to two different strategical types of body shape: A great diversity of arthropods live together with ants and while certain Paussini rely on the protective type with less profit from ant societies being well-protected habitats with exposed extremities, other genera access ant colonies using stable microclimate (Hölldobler and Wilson 1990; Wasmann glandular secretions and trichomes (symphile type). We 1913; Wheeler 1960). The concentrated brood and accumu- compare these adaptations with other taxonomic groups of lated food items in ant nests constitute valuable resources, insects by joining contemporary research and early sources readily exploitable by associated organisms. Ant nests, and discuss the possibility of an attracting or appeasing however, are well-fortified, and due to their numerousness effect of the secretion. Species that are ignored by their host and chemical defence, ants are able to overwhelm intruders ants might use chemical mimicry instead. Furthermore, of large body size. Thus, the question of how ant-associated vibrational signals may contribute to ant–beetle communi- arthropods (myrmecophiles) freely roam an ant colony and cation, and chemical signals have proven to play a role in develop in the nest has received broad interest. The host finding. The powerful defense chemistry of paussines mechanisms of some ant–myrmecophile interactions, which can be termed “symbioses” duetotheclosespatial association, have become fairly well understood, as * : S. F. Geiselhardt ( ) K. Peschke chemical ecology has grown into an own discipline. On Institut für Biologie I, Albert-Ludwigs-Universität Freiburg, 79104 Freiburg, Germany the other hand, the enormous advances in ecological e-mail: [email protected] understanding of ant colonies as super-organisms have given a new paradigm for assessing the underlying P. Nagel proximate and ultimate processes (Bourke and Franks Institut für Biogeographie, Departement Umweltwissenschaften, Universität Basel, 1995; Crozier and Pamilo 1996; Hölldobler and Wilson 4056 Basel, Switzerland 1990). Sociobiological characteristics of an ant colony are 872 Naturwissenschaften (2007) 94:871–894 of elementary importance for the question as to whether a Investigating ant guests is particularly interesting, as they myrmecophile can successfully intrude an ant colony. The can help to understand recognition mechanisms and their pre-adaptation for being infiltrated differs between colonies deception. Among myrmecophilous arthropods, Paussinae of one species because some features may be displayed deserve special attention, as the origin of myrmecophily in facultatively (Crozier and Pamilo 1996; Hölldobler and the group is still unclear, and Paussini combine conspicuous Wilson 1990). One such characteristic is the queen number, adaptations, which are displayed by diverse other groups of which can range from one (monogyny) to multiple myrmecophiles. (polygyny). Because of the high degree of relatedness While the taxonomy and biogeography of paussines are among individuals and the sophisticated nestmate recogni- fairly well examined (e.g. Ball and McCleve 1990; tion, monogynous colonies are suspected to be less prone to Darlington 1950; Deuve 2001a, b; DiGiulio et al. 2003; intrusion. Aggressiveness, however, seems to be more Luna de Carvalho 1989; Nagel 1986b, 1987b; Stork 1985), pronounced in polygynous colonies (Hölldobler and Wilson reports of behaviour and ant–paussine interactions are 1977). Polygyny may be combined with occupation of scarce and often were by-products of taxonomic inves- multiple nest sites by one colony (polydomy). Recognition tigations. We provide a comprehensive review of the mechanisms in polydomous colonies differ from those in known facts about the association of ant nest beetles and monodomous colonies based on the lack of constant nest their hosts to spark interest in these rare beetles and odour exchange (Soroker et al. 2003), and connecting trails encourage field observations. Beyond this, we want to might further enhance colony finding by intruders. Addition- contribute to the understanding of myrmecophily—not only ally, colony movement frequency, colony size, habitat choice in paussines—by discussing ant nest beetle biology in the and nesting materials can be variables that influence the context of other myrmecophilous arthropod groups. suitability of an ant colony for a particular myrmecophile. Formerly, myrmecophiles had been categorised by the degree of acceptance in the ant colony as synechthrans, General morphology synoeketes, symphiles and true parasites (Wasmann 1890, 1896). This nomenclature is now considered as outdated The subfamily Paussinae comprises Metriini, Ozaenini, because several organisms fit in more than one category. Protopaussini and Paussini (Fig. 1), which are small or Today, it is common to distinguish myrmecophiles, which medium sized (2.8–22.0 mm) and predominantly brownish. are only occasionally tended by ants (facultative interac- The body shape of Metriini and Ozaenini (Fig. 2) is similar tion), from those that invariably depend on ants, at least to those of other carabids, but some genera display during some life-stages (obligate association). Relation- characters that call to mind myrmecophilous adaptations ships may range from mutual benefaction (mutualism) to of other beetles, such as crassate antennae, reduction in unidirectional impairment (parasitism), and taking ly- tactile setae or flattened body and legs. The body shape of caenid butterflies (Lepidoptera: Lycaenidae) as an exam- Protopaussini and Paussini is either slender or compact and ple, we find the whole span of interaction types from reflects two different morphological strategies of integration mutualism (Fiedler and Saam 1995) to obligate parasitism in host colonies, which will be described later on. Many (Wardlaw et al. 2000) within one taxon (Pierce and Young species of the tribe Paussini are characterised by enlarged 1986; Pierce et al. 2002). antennae (Fig. 2). Like most nest-inhabiting myrmeco- Since the extensive work of Wasmann (e.g. Wasmann philes, paussines are not shaped like an ant, i.e., are not 1903, 1913; Wasmann and Brauns 1925), many myrmeco- myrmecomorphic. Morphological ant-resemblance—al- philes have been described, and among them are numerous though frequent in ant guests—seems to be restricted to beetle species (e.g. Kistner 1993; Päivinen et al. 2002). species wandering near ant trails outside the nests (Cushing Recent investigations involve, for example, the families 1996; McIver and Stonedal 1993; Taniguchi et al. 2005; Staphylinidae, Pselaphidae (Akino 2002), Scarabaeidae Wasmann 1925; Wheeler 1960). (Vander Meer and Wojcik 1982) and Coccinellidae (Orivel et al. 2004). Associations of paussine beetles (Carabidae: Paussinae) Distribution and activity pattern with ants have been reported early in literature (Dohrn 1851; MacLeay 1838) and were most thoroughly studied by Paussines are found in all continents except Antarctica, but Wasmann and his contemporaries (e.g. Eidmann 1937; their main distribution is restricted to subtropical and Escherich 1898, 1899b, 1907; Reichensperger 1924;Van tropical areas, with the highest diversity in the paleotropics Emden and Wasmann 1925; Wasmann 1890, 1903, 1906, (see Appendix). The Nearctic Metriini are extratropical, 1913, 1920, 1929, 1934). Afterwards, investigation of the while a few Ozaenini, Protopaussini and Paussini reach the behavioural aspects of the taxon diminished. southernmost parts of the Nearctic and Palearctic regions. Naturwissenschaften (2007) 94:871–894 873 Fig. 1 Hypothesised phyloge- netic relationships of Paussinae genera based on the current knowledge of adult and larval structural characters (amended from DiGiulio et al. 2003). Fossil genera are marked in asterisks Amber fossils from the European Baltic and the North
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