Myrmecological News 12 219-235 Vienna, September 2009

Social among : a review (: Formicidae)

Alfred BUSCHINGER

Abstract The latest review of social parasitism in ants was published in 1990. Since then, comparatively few new parasitic have been discovered, but research has progressed our knowledge of the evolution of social parasitism and the mecha- nisms involved in the maintenance of parasitic relations between species. Temporary social parasitism, slave-making, inquilinism and xenobiosis are confirmed as the primary manifestations of social parasitism. So-called intraspecific social parasitism should be clearly set off against the obligatory interspecific relations of social parasite and host species. A few evolutionary transitions from one of the interspecific forms to another do occur, mainly from slave-making to a derived, workerless state. Nevertheless there is no evidence for the evolution of all types of social parasitism towards inquilinism via multiple pathways as had been formerly suggested. Emery's rule sensu lato has been confirmed by mole- cular techniques. Host-parasite recognition is mediated by cuticular signatures and involves imprinting. Increasingly, social parasitic ants are considered interesting with respect to understanding conflict and cooperation among ants. Co- evolution of social parasites with the respective host species and influence of social parasites on host populations are inten- sively studied. There are still unanswered questions with respect to the unequal distribution of social parasites among the extant ant subfamilies and genera, as well as their geographic distribution including the lack of slave-makers in the tropics. Key words: Social parasitism, slave-making, temporary parasitism, inquilinism, xenobiosis, evolution, Emery's rule, review. Myrmecol. News 12: 219-235 (online 17 July 2009) ISSN 1994-4136 (print), ISSN 1997-3500 (online) Received 25 March 2009; revision received 8 June 2009; accepted 8 June 2009 Prof. Dr. Alfred Buschinger, Rossbergring 18, D-64354 Reinheim, . E-mail: [email protected]

Introduction Social parasitism, the parasitic dependence of a social in- sary as had been suggested by BUSCHINGER & CROZIER sect species on one or several free-living social species, is (1987) (Appendix 2). an intriguing feature found in groups such as wasps, bees, Terminology around social parasitism: intraspecific so- and especially manifold in ants. Slave-makers, temporary parasites, inquilines and guest ants have been studied since cial parasitism, autoparasitism, non-social inquilines, guests, and parasites Pierre HUBER (1810) and Charles DARWIN (1859). The lat- est comprehensive overview of social parasitism in ants What is social parasitism and what is not? The answer was published in "The Ants" by HÖLLDOBLER & WILSON apparently depends a lot on personal preferences and ex- (1990). D'ETTORRE & HEINZE (2001) provided a recent periences of individual authors. A plethora of terms have review of ant . Ant social parasitism remains as fas- been in use to denote the various manifestations of social cinating as ever. Many additional details have been discov- symbiosis and parasitism among social , particularly ered and investigated during the past 20 years, and warrant among ants. Often several synonyms have been proposed, another comprehensive review. and even modern authors sometimes create substitutes for On the basis of general information this paper shall ad- well established terms, increasing confusion. Most recently, dress preferably those instances of social parasitism that HERBERS (2006, 2007) suggested replacing the terms "sla- have either been discovered or intensively studied recent- very", "slave-making ants" and "dulosis" by "piracy" and ly. In HÖLLDOBLER & WILSON (1990) many then already "pirate ants". These terms have been adopted by some, e.g., known details and a list of parasitic species can be found. by BONO & al. (2007) and TSUNEOKA (2007). Parasitism Nevertheless numerous genera and species have to be men- usually denotes the dependence of one species, the para- tioned in the text. For their and ranges see Ap- site, on one or more other species, the host(s). In obligatory pendix 1, as digital supplementary material to this article, parasitic relationships, parasites cannot survive without the at the journal's web pages. host. This holds true for social parasites among the social In this review, "" are defined according to func- insects as well. tion, with "queen" meaning a mated, egg-laying individual, However, the term "parasitism" sometimes is used also irrespectively of whether it is a dealate gyne, an inter- for intraspecific phenomena such as nest usurpation in bum- morph or a morphologically worker-like specimen. Since blebees or in birds, and some ant researchers have coined all kinds of such female reproductives occur in ants, and terms like "intraspecific social parasitism" and "intraspeci- often also in social parasitic ants, this statement is neces- fic slavery" (HÖLLDOBLER 1976, POLLOCK & RISSING 1989, HÖLLDOBLER & WILSON 1990, FOITZIK & HEINZE 1998, ants which cannot survive for longer time without the hosts. 2000, 2001). With focus on social bees, BEEKMAN & OLD- Different from the other three types of social parasitism ROYD (2008) provided an overview of such intraspecific where parasite brood rearing is accomplished by the host parasitism with a particularly valuable list of references. species, guest ants care for their own brood. Xenobiosis has The term "intraspecific social parasitism", however, may been included in this survey also because it had been dis- cause confusion and may blur the very particular character cussed as a possible precursor of inquilinism (e.g., WILSON of the obligatory social parasitism among different ant spe- 1971, HÖLLDOBLER & WILSON 1990). cies (e.g., SAVOLAINEN & VEPSÄLÄINEN 2003). Like in some Guest ant relations have been stated in three genera of non-parasitic ants, "intraspecific slave raids" have been ob- ants, , Polyrhachis and (possibly) Megalo- served occasionally also in slave-making species (TOPOFF myrmex. The guest ants of the myrmicine tribe Formico- & al. 1984, SCHUMANN 1992, LE MOLI & al. 1993). xenini now all are attributed to one apparently monophyle- BOLTON (1986a, b) has coined the term "autoparasitism" tic , Formicoxenus (see FRANCOEUR & al. 1985) (Ap- for the behaviour of young queens seeking adoption in con- pendix 1). They have small colonies with up to about a specific colonies, which later reproduce by budding or fis- hundred individuals. The colonies dwell the nest material sion. In polygynous species this is a reciprocal behaviour or the nest walls of their hosts, which are much bigger spe- in that the "autoparasitic" generation may become host for cies of the genera , Manica or Myrmica with large, the next generation. Therefore it should not be considered populous nests. These guest ants build their own little nests as "parasitic". well separated from the brood chambers of the hosts, and Social parasitism or inquilinism often has been stated they themselves care for their brood. They are dependent also for non-social organisms, so-called "guests" in nests of upon the hosts with respect to nutrition and perhaps shelter. social insects, such as mites, beetles and other Formicoxenus may solicit regurgitated food directly from (e.g., AKINO & al. 1999). The parasitism among two so- a host worker or participate in food exchange (trophal- cial species, however, is something particular. It should laxis) between two host specimens. Some Formicoxenus not be confounded with ordinary kinds of parasitism like species exhibit queen and male polymorphism (FRANCOEUR that of mites or nematodes that may plague both social & al. 1985) and the colonies may be functionally mono- and non-social hosts alike. Another instance of confusing gynous (BUSCHINGER & WINTER 1976, BUSCHINGER 1979). use of the term inquiline is for ants nesting in termite mounds LENOIR & al. (1997) have demonstrated a chemical mimi- (e.g.,WOOD & SANDS 1978, LEPONCE & al. 1999): as far cry between parasites and hosts in two species pairs, For- as is known they don't have social relations to each other. micoxenus provancheri / Myrmica incompleta and F. que- At best the ants prey upon their compulsory hosts. becensis / M. alaskensis. The guest ants acquire the cuticu- Finally, "social symbiosis" (e.g., HÖLLDOBLER & WIL- lar hydrocarbons from their hosts during the first days of SON 1990) is an inaccurate, although widely used, descrip- their adult life. tion of a social parasite's relationship with its host as "sym- Another, recently investigated instance of xenobiotic biosis" in other instances often refers to a relationship that exploitation of host species is represented by a couple of is mutually beneficial. Following myrmecological tradi- formicines living in association with certain Ponerinae. tion the term will not be used in this paper. This review Polyrhachis lama () in Java has been found liv- will only consider the interspecific forms of social para- ing in nests of a common Diacamma species (Ponerinae). sitism, the obligatory parasitism between ant species. Only very few among the parasitized nests contained a Polyrhachis queen, whereas in most nests only workers of Various types of obligatory ant social parasitism this species could be found together with a brood of both Social parasitism is expressed in many forms, particular- species (MASCHWITZ & al. 2000). Similarly, Polyrhachis ly in ants. The various heterospecific associations among loweryi (Formicinae) in Queensland, Australia, was found ants have been classified in different ways. HÖLLDOBLER in colonies of a large Rhytidoponera species (Ponerinae) & WILSON (1990), following a suggestion of WASMANN (MASCHWITZ & al. 2003). Again, a couple of mixed col- (1891), distinguished between "compound nests" and "mixed onies contained workers and a brood of host and parasite, colonies". The latter would comprise the temporary para- whereas a queen of the parasitic Polyrhachis was found in sites, the slave-makers and the inquilines, where the host only one mixed colony. The Polyrhachis workers were not species workers at least temporarily care for the parasite inseminated, though some of them laid male-destined eggs. brood. "Compound nests" covers all types of casual or regu- Evidently, in both Polyrhachis species the workers from lar nesting in close vicinity (plesiobiosis), stealing food queenright (i.e., containing a Polyrhachis queen) mixed col- from other species (cleptobiosis), stealing brood (lestobio- onies invade neighbouring host species nests, carry young sis) and sharing nests and trails but keeping the two spe- brood stages with them and rear this brood with food that cies' broods separate (parabiosis). Xenobiosis in this clas- is furnished by the host workers (MASCHWITZ & al. 2004). sification is listed among the "compound nests". Here, the There are more records of Polyrhachis species found obligatory parasitic ants shall be arranged in four basic in association with distantly related formicine (Campono- types, including xenobiosis (e.g., BUSCHINGER 1986), which tus spp.), myrmicine (Myrmicaria sp.) and ponerine spe- still appears justified and helpful, though a few excep- cies. Closer examination may reveal some more instances tional instances cannot unambiguously be attributed to one of xenobiosis in this group (KOHOUT 1990, MASCHWITZ & or the other. al. 2000). All the species that are suggested to coexist with Guest ant relations, xenobiosis. Xenobiotic ants in ponerine hosts belong to one species group, P. viehmeyeri general are distantly related to their respective hosts at best. group of subgenus Myrmhopla (see KOHOUT 1990, DOROW Parasite and host may even belong to different subfami- 1995). For the P. lamellidens group in Polyrhachis sub- lies. The association, however, is obligatory for the guest genus Polyrhachis, a couple of records exist in which a kind

220 of temporary parasitism in nests of Camponotus spp. has not been firmly demonstrated, and its existence in the ge- been suggested (for details see MASCHWITZ & al. 2000) nus still needs proof. (Appendix 1). A possible temporary parasitism also has been suggested Finally, species belonging to the genus Megalomyrmex for Solenopsis enigmatica from the West Indies, with par- sometimes have been mentioned as guest ants (BRANDÃO asite workers in the mixed nests, though the authors, DEY- 1990, HÖLLDOBLER & WILSON 1990). Whether or not they RUP & RUSAK (2008), have described the species as a new belong to this group is somehow questionable, however "inquiline". A further problem in this instance arises from (see "Evolutionary modifications of life cycles in parasitic the fact that the host species belongs to another genus, Phei- ants"). dole. Such instances should be very carefully studied since Temporary parasitism. In temporary parasitism, the temporary parasitism between members of different ge- parasitic species depends on a host species only during the nera would represent a novelty. founding phase of new colonies by young queens. Usually Permanent parasitism with slavery, dulosis. The per- after her and insemination, the parasitic queen manently parasitic species depend upon the hosts through- attempts to penetrate a host colony where she replaces the out their lives. In the case of the slave-making or dulotic original queen and manages to be tolerated by the workers. ants, the young queen has to penetrate a host species nest, A non-parasite worker force develops from the parasite's eliminate the host colony queen and take over her workers eggs, with the aid of the host colony workers, which even- and the brood. In some genera (Chalepoxenus, Harpago- tually disappear due to natural aging and losses. The col- xenus) all adult host workers are killed or evicted. The con- ony becomes a pure society of the parasitic species. Ma- quered brood comprises worker pupae from which new ture colonies of temporary social parasites grow as large slaves will soon emerge, and with their aid a number of as the host species colonies; they may live for many years slave-maker workers are subsequently reared. and rear numerous sexuals. The slave-maker workers are usually unable to forage, Some peculiar behaviours of queens have been observed to feed their larvae, or even to eat by themselves. On the during colony foundation. Queens of Lasius umbratus and other hand, they are often predisposed for effective fighting. related species in the subgenus Chthonolasius (subfamily Slave-maker workers may be equipped with specialized Formicinae), grasp and chew a worker of the host species piercing mandibles as in (Formicinae) and Stron- (L. niger) and then enter the host nest. There the parasite gylognathus (), or with toothless, pincers-like queen is said to become more attractive than the original mandibles for cutting off the appendages of their opponents queen (GÖSSWALD 1938), which finally dies of starvation or as in sublaevis (Myrmicinae) (see BUSCHIN- is expelled from the colony. A closely related species, L. GER & al. 1980, HÖLLDOBLER & WILSON 1990). Others have reginae, after invading a nest of L. alienus attacks the much strong stings (the myrmicine genus Chalepoxenus, see BU- bigger host queen and throttles her to death (FABER 1967). SCHINGER & al. 1980, EHRHARDT 1982), or produce ag- Queens of Bothriomyrmex decapitans and other species of gressive glandular secretions or "propaganda" substances this genus during colony take-overs cut off the head of the (Raptiformica, see REGNIER & WILSON 1971). They attack host species queen (of genus Tapinoma, both subfamily independent, neighbouring colonies of the slave, i.e., host, Dolichoderinae) (SANTSCHI 1906). species, fight against the defenders, and finally carry back Lasius fuliginosus (Formicinae) exhibits a social hyper- the brood to the slave-maker's nest. Thus, the slave stock parasitism in that the queen founds her colony in a nest of may be replenished several times a year (BUSCHINGER & al. L. umbratus which is itself a temporary parasite of L. niger 1980). Propaganda substances also are used by slave-raiding and a few related species (SEIFERT 2007). In certain in- Harpagoxenus sublaevis and by the inquiline ant, Lepto- stances the parasitic foundation of new colonies of Lasius thorax kutteri (see ALLIES & al. 1986). In quite a number (Chthonolasius) species may be pleometrotic, with several of presumed slave-making species slave raids as yet have parasite queens simultaneously invading a host colony (SEI- not been observed. This is the case in Strongylognathus, FERT & BUSCHINGER 2002). MATTHEIS (2003) provided evi- where raiding actually has been observed in only two or dence for pleometrotic foundation also of Lasius (Dendro- three among the 24 described species; e.g., SANETRA & lasius) fuliginosus colonies. He suggests that colony founda- GÜSTEN (2001) reported on slave raids of Strongylogna- tion occurs only in orphaned colonies of Lasius umbratus. thus afer in laboratory conditions. For a recent review of Temporary parasitism occurs in several (perhaps all) the sociobiology of slave-making ants see D'ETTORRE & species of wood ants of the Formica rufa group and of HEINZE (2001). Formica (Coptoformica) species. In some species the queens Formica (Raptiformica) sanguinea (Formicinae) is one may alternatively either penetrate a Formica (Serviformica) example that mediates between temporary parasitism and sp. nest, or join a polygynous colony of their own species. dulosis in that large colonies often exist without having Such colonies then reproduce by budding, often forming slaves. A sizeable fraction of the conquered pupae usually huge multi-nest supercolonies (HÖLLDOBLER & WILSON is eaten in these slave-maker's nests. 1990). (Formicinae) with four species from Myrmica vandeli might be a temporary social parasite , southwestern Russia and , , and of M. scabrinodis in marginal parts of its range, but is is characterized by its peculiar recruitment of nest free living in stronger populations (RADCHENKO & ELMES mates for slave raids: these ants carry each other to the 2003). SEIFERT (2007) discussed such a facultative tem- target nests of their slaves of genus (see MA- porary parasitism of M. vandeli as being very probable. RIKOVSKY 1974, BUSCHINGER & al. 1980, HÖLLDOBLER & FRANCOEUR (2007) suggested a temporary parasitic life WILSON 1990). history in the newly described Myrmica semiparasitica. The Amazon ants, genus Polyergus, are the most inten- Nevertheless temporary parasitism in this genus as yet has sively studied group at present. The genus has a Holarctic

221 range with P. breviceps and P. lucidus in North America parasite brood is reared by the host workers simultaneously and P. rufescens, P. nigerrimus and P. in tempe- with their own larvae. In a few instances, e.g., Anergates rate and Mediterranean Eurasia (Appendix 1). For colony atratulus, the parasite apparently invades only orphaned founding, the young queen penetrates a nest of the host host species colonies, whereas the so-called "ultimate para- species, eventually kills the host queen, and uses the host site" Teleutomyrmex schneideri sometimes rides on the back workers to rear her brood. A colony of Polyergus will con- or clings to the thorax of the host colony queen similar to an duct slave raids on nests of species of Formica (subgenus ectoparasite (KUTTER 1968). Serviformica), and worker pupae of the hosts are taken. The Occasionally a distinction is made between queen-tole- workers hatching from these pupae are necessary for forag- rant and queen-intolerant inquilines according to their co- ing and for feeding and rearing the slave-maker's brood existence with the host queens in the host nest, although in the mixed society, and for nest building. Polyergus wor- inquilines typically are queen-tolerant. The few queen- kers are incapable of surviving without slaves, even when intolerant inquilines either invade queenless colonies (Aner- plentiful food is available. North American Polyergus luci- gates atratulus) or actively eliminate the host queens such dus has at least three host species though single colonies as goesswaldi (see BUSCHINGER & KLUMP always contain only one of them. Raids target only at nests 1988) and a couple of species in the genera of the host species already present in the nest (GOODLOE and Chalepoxenus which presumably are degenerate slave- & al. 1987). The authors suggested imprinting of the slave- makers (Appendix 1). makers on the respective host species. Another distinction can be made with respect to mor- Recent progress has been made in studies on colony phology. Some species like Teleutomyrmex and Anergates foundation of Formica sanguinea (see MORI & LE MOLI appear highly specialized and are perhaps "old". For these 1998). After mating the females may return to a F. sangui- parasites a long evolutionary history has been assumed, nea colony, then join a slave raid of this colony and estab- perhaps including descent from slave-makers (KUTTER 1968, lish a colony in an invaded host nest. Polyergus species WILSON 1971, HÖLLDOBLER & WILSON 1990). Their par- colony foundation also was studied in more detail recently ticular morphological characters, which in part occur also (MORI & al. 2000, JOHNSON & al. 2001, 2002). The large in other inquilines, were termed "the anatomical parasitic Dufour's gland is responsible for a kind of chemical disguise syndrome" by WILSON (1984). (ERRARD & D'ETTORRE 1998). Only mated and egg-laying Other inquilines, e.g., the parasites of the formicine ge- host queens are attacked by a Polyergus foundress queen, nus Plagiolepis are anatomically less aberrant but may also probably due to a kairomonal effect signalling queen and have a long parasitic history. The parasitic group (formerly colony suitability (JOHNSON & al. 2002). After killing the genus Paraplagiolepis) comprises the two species, P. xene host queen the cuticular hydrocarbon profile of the Polyer- and P. grassei, and at least five undescribed ones (STUE- gus breviceps queen changes into that of the attacked host WER 1992, CAGNIANT 2006, A. Buschinger, unpubl.), as queen. Cuticular compounds from the host queen apparently well as the former genus Aporomyrmex with Plagiolepis are transferred to the parasite queen during the aggressive ampeloni and P. regis (Appendix 1). The most prominent interaction. features of this group are reduction in size (ARON & al. Slave-makers belonging to the tribe Formicoxenini, with 1999) and a marked polymorphism of both queens and genera Chalepoxenus, Harpagoxenus, Myrmoxenus, Proto- males. Only P. grassei has a few own workers. All the mognathus and certain species of genus , are species are living within highly polygynous and polydom- another focal point of recent interest. Their particular ad- ous colonies of the host species. vantage is small colony size which is favourable for labora- Numerous other inquiline species resemble closely their tory observations of slave-raiding and colony foundation host species, and are often systematically attributed to their (BUSCHINGER & al. 1980). Dense populations in the field host genera, such as Leptothorax kutteri, L. goesswaldi, and with often several host species colonies on one square meter L. pacis (all formerly genus Doronomyrmex); all three are enable studies on effects of the slave-makers on their hosts. difficult to tell apart from the host species L. acervorum. For more details see "Evolutionary aspects of social para- Curiously enough, sometimes two of these species may oc- sitism". cur in sympatry, all living with the one common host spe- Remarkably, since HÖLLDOBLER & WILSON (1990) only cies, and sometimes two of the parasitic species even share few other slave-making ant species have been described, a one host colony (BUSCHINGER 1986, 1990). Finally, some Rossomyrmex species each from Turkey (TINAUT 2007) and inquiline gynes appear as merely smaller specimens of the China (XIA & ZHENG 1995), and four species of Strongy- host species, e.g., Temnothorax minutissimus, though their lognathus, i.e., S. minutus and S. pisarskii from Europe, status as separate species is unquestionable (BUSCHINGER and S. potanini and S. tylonum from China (see Appendix & LINKSVAYER 2004). 1). In none of these instances information on life history Inquilinism is the most frequent type of social parasi- was provided. tism, and several new inquiline ant species have been dis- Permanent parasitism without slavery, inquilinism. covered since HÖLLDOBLER & WILSON (1990). HORA & al. Permanent parasites that do not enslave their host species (2005) and FEITOSA & al. (2008) recently described mini- often do not produce a worker . Termed inquilism, this ature queens of Ectatomma parasiticum (Ectatomminae) as syndrome is adaptive in that the host workers take over all an inquiline species. This is the first case of social parasi- husbandries and the parasite queen can invest all energy tism in the poneroid complex of ant subfamilies. HEINZE into the production of sexuals. Nonetheless, in a few in- (1989) and HEINZE & ALLOWAY (1991) described two new stances inquiline workers have been observed to exist (SUM- inquilines of Leptothorax spp. from North America, L. wil- NER & al. 2003). The reproductive females usually coexist soni and L. paraxenus. The latter is perhaps queen-intole- with the queens of the host species in their nests, and the rant, eliminating the host colony queen(s), though this has

222 not been firmly established (cf. ALLOWAY 2009). JOHN- & al. 2005). Moreover, among the huge subfamilies of Myr- SON (1994) provided additional information on the life his- micinae and the Formicinae the numerous parasitic species tory of the inquiline ant, Pogonomyrmex anergismus, a very are concentrated in only a few genera (BUSCHINGER 1986, rare parasite of Pogonomyrmex rugosus and P. barbatus. 1990). For example, the genus Camponotus with an esti- JOHNSON & al. (1996) studied P. colei, an extremely rare mated 1,500 species comprises but one known social para- inquiline of P. rugosus and supposedly its closest rela- site, the inquiline Camponotus universitatis (see TINAUT & tive. Myrmica schenckioides has been described as a new al. 1992). supposedly parasitic species from the Netherlands (BOER A survey of the parasites in different subfamilies re- & NOORDIJK 2005), though only one specimen had been veals that all four basic types of parasitic life habits (xeno- found in a pitfall trap. KINOMURA & YAMAUCHI (1992) biosis, temporary parasitism, dulosis and inquilinism) evolv- found a new workerless socially parasitic Vollenhovia, V. ed within both the Formicinae and the Myrmicinae, tem- nipponica, in Japan. For its life history see SATOH & OH- porary parasitism in addition among the Dolichoderinae KAWARA (2008). HÖLLDOBLER & WILSON (1990) did not (one genus, Bothriomyrmex) and Pseudomyrmecinae, and yet refer to any social parasites among the leaf-cutter ants inquilinism in the Myrmeciinae (BUSCHINGER 1986). With- (Attini). It is remarkable therefore that five inquiline taxa in in the myrmicine tribe Formicoxenini slave-making has this tribe now have been described (SCHULTZ & al. 1998, evolved apparently six times independently (BEIBL & al. SUMNER & al. 2004, SOUZA & al. 2007). AGOSTI (1994) 2005). Inquilinism in this tribe originated at least twice described the first inquiline, and social parasite, in the for- (BUSCHINGER 1981), and xenobiosis once (FRANCOEUR & micine genus . WARD (1996) reported a new al. 1985). Among the Formicinae the slave-maker genera workerless parasite in the ant genus Pseudomyrmex, P. Polyergus and Rossomyrmex have evolved independently inquilinus, the second one in the genus, and the third one from one another (HASEGAWA & al. 2002). WILSON (1984) in the subfamily Pseudomyrmecinae. Only one temporary assumed an independent, of nine pa- social parasite of this subfamily, genus Tetraponera, had rasitic species from the large myrmicine genus Pheidole. been known prior to HÖLLDOBLER & WILSON's listing Such polyphyletic origins of very similar parasitic life (1990) (Appendix 1). cycles indicate that there are certain widespread, though perhaps not universal features of normal social behaviour Frequency and systematic distribution of parasitic ants which often become the starting point for parasitic evolu- Among the ca. 12,500 described ant species (AGOSTI & tion (BUSCHINGER 1970, 1990). JOHNSON 2009), the ca. 230 known parasitic species repre- sent but a small fraction. For the very well known fauna Evolutionary aspects of social parasitism of , the census of KUTTER (1968) remarkably The most important and also the most controversial as- showed about one third of the ca. 110 ant species then pect of the evolution of social parasitism is how and why known to be parasitic. Most parasitic ant species are rare some ants have switched over from independent life to and not easily found in populations and colonies of their social parasitism. The problem may be split into several hosts. The actual global number of parasitic species thus questions. How to explain the generally close systematic might be considerably higher. As had been predicted (WIL- relationship between hosts and parasites? Which selective SON 1984), new species continue to be detected, particu- forces and which ecological conditions might be respon- larly in the tropics. sible for or might favour the development of parasitic life The distribution of social parasite species among the 22 habits? Which behaviours in normal social species give rise extant ant subfamilies (BOLTON 2003, plus Martialinae, to the particular parasitic behaviours, i.e., dependent colony RABELING & al. 2008) is surprisingly unequal. Although foundation and slave raiding? Recent molecular genetic the subfamilies apparently do not differ fundamentally in studies have brought a lot of new insights, and often also their form of social organization, social parasites are known support previously published assumptions. Nevertheless, the mainly among the Myrmicinae and the Formicinae (about questions remain under scrutiny. 33 out of 139 and 9 out of 25 genera, respectively). Some On the first question, concerning the close systematic genera consist of parasitic species only (e.g., Anergates, relationship between hosts and parasites, most authors are Bothriomyrmex, Chalepoxenus, Formicoxenus, Harpago- in accord. EMERY (1909) pointed out that all the inqui- xenus, Myrmoxenus, Polyergus, Protomognathus, Strongy- lines, slave-makers and temporary parasites are close re- lognathus, Teleutomyrmex). Other genera comprise numer- latives of their respective host species ("Emery's rule", LE ous independent and a few parasitic species each (e.g., For- MASNE 1956). The validity of Emery's rule has been inten- mica, Lasius, Leptothorax, Myrmica, Plagiolepis, Temno- sively discussed, particularly since genetic methods could thorax), sometimes due to recent synonymization of for- be applied. A major debate has dealt with this rule in a merly separate parasitic genera with their host genera (Ap- "strict" and in a "loose" form. pendix 1). Remarkably, the temporary parasitic genus Bo- In fact, EMERY (1909) had formulated his statement a thriomyrmex (Dolichoderinae) represents the most diverse bit thoughtlessly. At his time it had been known quite well taxon among the social parasites with ca. 38 valid species that slave-maker species each can parasitize two or more and numerous subspecies (JOHNSON 2007). slave species at once. Hence, Emery's rule in the strict sense, Although several ant subfamilies comprise few species saying that every parasitic species derives directly from in total, it is difficult to understand why parasites are (near- its host species was obsolete from the beginning (BU- ly) missing, for instance, from the large group of "ponero- SCHINGER 1970, 1990). Multiple host species may also oc- morph subfamilies" (BOLTON 2003), where a microgynic cur among inquilines (HEINZE & al. 1995). Molecular stud- social parasite of Ectatomma tuberculatum (Ectatomminae) ies have confirmed that Emery's rule usually applies but in only recently has been described as the first instance (HORA the loose sense: the parasites derive from the species group

223 or, more frequently, the genus to which their hosts belong described as separate, parasitic species. SAVOLAINEN & (e.g., BAUR & al. 1995, PARKER & RISSING 2002, SUMNER VEPSÄLÄINEN (2003) confirmed the species status of M. & al. 2004). microrubra and M. hirsuta with molecular methods but M. SMITH & al. (2007), studying social parasites and their microrubra was synonymized later with M. rubra (see hosts in allodapine bees, stated that "recent molecular phylo- STEINER & al. 2006). For queen polymorphism and queen genetic studies have revealed a mixture of the two forms size polymorphism see also BUSCHINGER & HEINZE (1992) [loose and strict Emery's rule] in various ant and wasp and HEINZE (2008). groups". They found both pairs of sister species where one Polygyny: origin of dependent colony foundation? species parasitizes the other and parasites less closely re- BUSCHINGER (1990) hypothesized that all forms of true so- lated to their respective hosts. Extinctions and host switches cial parasitism originate from the adoption of conspecific have to be taken into consideration when evaluating host- young queens in colonies of polygynous species. The so- parasite relationships (cf. BUSCHINGER 1970). cial organization of the ancestral, and eventual host species Either way, the close relationship of host and parasite (group), and the host's variation in space and time, may may be due to a common ancestor, or to parasites' ability to be responsible for the development of an emerging para- coexist only with very closely related host species (BU- site to become an inquiline, a temporary parasite, or a slave- SCHINGER 1986). In order to live in a mixed society the two maker. species must have compatible communication systems and Roughly one half of all ant species investigated for num- similar for nestmate recognition, and the para- bers of queens per colony are polygynous or at least facul- site's larvae must be adapted to, among others, the glan- tatively polygynous. In many species monogynous and po- dular food secretions and feeding habits of the host species lygynous colonies occur within a single population, whereas workers. When closely related species are involved, these other species are always polygynous (BUSCHINGER 1974, conditions are most easily fulfilled. KELLER 1993, HEINZE 2008). Primary polygyny may be a Sympatric or allopatric origin of social parasites? The rare consequence of pleometrosis. More frequently, how- question thus focuses on the sympatric or allopatric ori- ever, young queens are later accepted in already existing gin of parasite and host: whether the parasite has directly polygynous or perhaps also monogynous colonies (secon- evolved within and from an independent species, or whether dary polygyny). Polygyny often results in polydomy, where speciation first occurred, perhaps due to a geographical a single colony inhabits several neighbouring nest sites. barrier, and subsequently one species went over to para- Sometimes daughter colonies with one or several queens sitize its sister species. branch off and eventually may interrupt the contacts to the To date most authors lean towards the hypothesis of a mother colony (ROSENGREN & PAMILO 1983). sympatric origin of parasitic species, in the nests and pop- The adoption of newly inseminated queens in existing ulations of the independent ancestor, which then became conspecific colonies resembles the events when a young the host species (KUTTER 1968, BUSCHINGER 1970, BU- queen of a social parasite penetrates an allospecific, i.e., its SCHINGER 1990, FRANKS & BOURKE 1990, BOURKE & host species', colony. Therefore, several authors, including FRANKS 1991, WARD 1996, SAVOLAINEN & VEPSÄLÄINEN WHEELER (1910), KUTTER (1968), ALLOWAY & al. (1982), 2003). After a parasite and a host have established as differ- ELMES (1973, 1978), BOLTON (1986b), and BUSCHINGER ent species both the parasite and the host may go through (1970, 1986, 1990) have speculated that polygyny might be further evolution, adaptation and speciation. This may ex- the precursor of social parasitism. After all, this hypothesis plain the apparent host shift of some parasites and the use of is the only one that would provide an explanation for the several hosts by one parasite species (BUSCHINGER 1990). dependent colony foundation of all true social parasites (ex- Allopatric speciation of parasite and host, on the other hand, cept the xenobionts). had been favoured by, among others, WILSON (1971, 1975) BUSCHINGER (1990) suggested an intraspecific prepara- and by HÖLLDOBLER & WILSON (1990), probably influ- sitic stage of incipient social parasites. Because the assump- enced by the widespread belief that speciation can only oc- tion of a sympatric speciation and, even more so, the iso- cur when populations of a species are geographically sepa- lation of a preparasitic genotype within a deme and even rated. within the nests of a given non-parasitic species appear quite Direct evidence in favour of the allopatry scenario is unusual and unrealistic at the first glance, this suggestion lacking: not a single instance is known of two closely re- needs some explanation. lated or sister species with partially overlapping ranges, There are many reports on ants, e.g., of the genus For- where one species would parasitize the other in the contact mica, where sexual offspring from one and the same nest zone, and live independently in the remainder of its range. may exhibit alternative behaviours, some mating on top of In contrast, there is potential support of the sympatry sce- the nest, others flying off to swarm (ROSENGREN & PAMILO nario: there are a few cases particularly in the genus Myr- 1983). Such intranidal variation leads to assortative mat- mica, where small females, "microgynes", occur together ing (e.g., WEST-EBERHARD 1986, 2005). The process is with "macrogynes" in the same polygynous nest. In some similar to sympatric speciation by host shift (MUNDAY instances the microgynes are believed to still belong to & al. 2004). If a tendency to produce fewer workers in the same species as the queens of ordinary size (M. rugi- favour of sexual production (the "deficient genes" of BU- nodis, see ELMES 1976, 1978, PEARSON 1981; Temnothorax SCHINGER 1990) somehow is linked with the tendency to rugatulus, see RÜPPELL & al. 2001). PEARSON (1981) spec- mate near the nest, and for the females to remain there, ulated that the interactions of the macrogyne and micro- the genetic condition of an incipient parasite, a "prepara- gyne forms of Myrmica ruginodis "may provide informa- site", has been achieved. In polygynous species this link- tion about the early or pre-parasitic condition". In other in- age evidently can happen (BUSCHINGER 1990). Intranidal stances microgynes (M. microrubra, M. hirsuta) have been mating provides an at least partial sexual isolation be-

224 tween the swarming phenotypes and those remaining in alized predators of other ants, such as some Myrmecia, place. Nest-mating increases inbreeding, and thus the ac- Gnamptogenys, and several army ant species (HÖLLDOBLER cumulation of "deficient genes", and it can be expected & WILSON 1990). Cerapachys (see HÖLLDOBLER 1982) to gradually increase the genetic differences between nest- and Sphinctomyrmex (see BUSCHINGER & al. 1990) store mating and swarming genotypes. captured ant brood over days or weeks in their nests, but Other mechanisms may then enhance the speciation pro- then consume them all. cess. For example, a conceivable means to produce a higher Selective forces involved in the evolution of social number of sexuals would be to reduce them in size. Smal- parasitism. No really convincing answers exist to the ques- ler sexuals have less energy for a long mating flight and tion on the selective forces involved in the evolution of for independent colony foundation but tend to remain in the social parasitism. Several authors (e.g., KUTTER 1968) mother colony and indeed, inquiline and temporary para- have stressed that independent colony foundation by sin- sitic ant queens often are considerably smaller than the gle young queens is a hazardous period, and that this risk related host species queens (e.g., ARON & al. 1999). could be reduced either by joining a colony of their own In essence, there apparently are some traits in the social species (leading to polygyny), or by invading a foreign organization of ants which are involved in the frequent colony and becoming an inquiline or temporary parasite. and convergent formation of inquilines, slave-makers and However, penetrating a foreign colony is also a risky ven- temporary parasites. These traits probably are polygyny, ture. It could be selected for only when it is more successful polydomy, inbreeding, and perhaps territorial behaviour than independent colony founding. KUTTER (1968), HÖLL- (see below), which in various combinations may give rise DOBLER & WILSON (1990) and HEINZE (1993) also dis- to the major types of social parasitism. In most groups of cussed the difficulties of solitary founding in cold climates (potential) host species apparently only one option, inqui- as a possible reason for the high frequency of parasitic linism or temporary parasitism, is available. In other groups, ants in higher latitudes. e.g., the genera Leptothorax and Temnothorax, queen-tol- erant and queen-intolerant inquilines and slave-makers per- Evolutionary modifications of life cycles in parasitic ants haps evolved in a radiative manner from a common, pre- Apart from the fundamental questions on the evolutionary parasitic stage. origin of social parasitism a large body of information has Territorial behaviour as origin of slave-making? accumulated referring to evolutionary modifications of Much of the relevant literature on the origin of parasitic life cycles and behaviour within parasitic species groups. behavioural patterns from ordinary social ones refers to Considerable advances in this field have been achieved in the conspicuous behaviour of slave raiding. Territoriality is recent times. often observed among neighbouring conspecific ant colo- WILSON (1971) and HÖLLDOBLER & WILSON (1990) nies (HÖLLDOBLER 1976, 1979). A dominant colony may had suggested several evolutionary pathways, all of which invade a weaker one, kill the adults and rob its broods. end up in an ultimate state of permanent parasitism or in- From such brood items workers may develop which join quilinism. Therefore it should be of interest to look for such the workforce of the dominant colony. HÖLLDOBLER (1976) pathways particularly in groups or genera where several of described such "intraspecific slavery" in Myrmecocystus. the types of social parasitism are represented. However, WILSON (1975), ALLOWAY (1979, 1980), POLLOCK & RIS- the theory of there being gradual pathways to inquilinism SING (1989), and STUART & ALLOWAY (1982, 1983) put has been questioned (BUSCHINGER 1986, 1990, BOURKE & forward the hypothesis that interspecific dulosis origin- FRANKS 1991) because there is practically no evidence for ated from such intraspecific slavery. Intraspecific slavery, transitions from xenobiosis, temporary parasitism or slavery however, does not address the parasitic mode of colony to a typical inquilinism, as will be shown below. In addi- formation. ALLOWAY (1980), STUART & ALLOWAY (1983) tion, a major argument against these pathways is the fact and TOPOFF (1990) have tried to combine both territorial that inquilines are found in a comparatively high number of competition and the adoption of young queens as a pread- genera in which the other kinds of social parasitism, hence aptation for parasitic colony foundation. potential precursors, are unknown (BUSCHINGER 1990). Predation on foreign ant brood as origin of slave- A route from xenobiosis to inquilinism? The frequent making? Another hypothesis on the origin of slavery had coexistence of nests of different ant species in close proxi- been put forward already by DARWIN (1859). With refer- mity has, surprisingly, not often led to the evolution of ence to the then known slavery of Polyergus and Formica xenobiotic relations in ants in general. Within the apparently (Raptiformica) he suggested that slave-making originated monophyletic (FRANCOEUR & al. 1985) guest ant genus from predation on brood of other species. Pupae which by Formicoxenus, or in the tribe Formicoxenini, there is no wor- chance were not consumed could hatch and become an ad- kerless inquiline that could be postulated to have evolved ditional workforce. Selection would have favoured colo- from the guest ants (e.g., HEINZE 1995). In the other group nies gaining ever more slaves by this means. Apparently the that contains guest ants, Polyrhachis, again nothing points facultative slavery of the subgenus Raptiformica was a nice in the direction of an evolutionary transition from one of intermediate stage in the evolution of the highly special- the observed instances towards inquilinism. ized genus Polyergus the species of which are absolutely In the myrmicine genus Megalomyrmex, M. symmeto- dependent upon their slaves. chus is suggested as being a guest ant of the fungus-grow- This "predation hypothesis", however, like the "territo- ing Sericomyrmex amabilis (see BRANDÃO 1990, HÖLL- rial hypothesis", does not address the parasitic foundation DOBLER & WILSON 1990). However, this conclusion may of colonies in all known slave-making species. Another ma- be questioned since ADAMS & al. (2000) claimed that at jor counterargument is the fact that slavery did not evolve least one Megalomyrmex species conducts raids on the fun- among those groups of ants which are particularly speci- gus of its attine host, a behaviour that has been termed agro-

225 predation. Most Megalomyrmex species apparently are free- In this context note that experimental crossbreeding of living or at most pillagers of brood and fungus for food several Myrmoxenus species with very different life habits from certain attine species. Megalomyrmex mondabora is has clearly demonstrated that they belong to one genus and always associated with nests of several attine species and that they are very closely interrelated (JESSEN & KLIN- was, therefore, referred to as a social parasite (ADAMS & KICHT 1990, BUSCHINGER 2001). LONGINO 2007), although these "parasite" ants just con- An evolution obviously paralleling that of Myrmoxenus sume fungus and larvae of the "host". The Megalomyrmex has been observed in the genus Chalepoxenus, which also life histories are reminiscent of "thief ants", such as the belongs to the Formicoxenini, and which also comprises lestobiotic Solenopsis fugax (cf. HÖLLDOBLER & WILSON both actively dulotic species (C. muellerianus, C. kutteri) 1990). Again, there is no reason to assume the evolution and at least one apparently degenerate slave-maker (C. of inquilines from the (perhaps even non-existing) xeno- brunneus) (CAGNIANT 1985, EHRHARDT 1987, BUSCHINGER biosis in this group of about 31 species (BRANDÃO 2003) & al. 1988, 1989, SCHUMANN 1992) (Appendix 1). During (Appendix 1). slave-raids the Chalepoxenus workers sting their opponents A route from slave-making or temporary parasitism to death. Surprisingly, this genus, like Myrmoxenus, para- to inquilinism? Any discussion involving the evolution sitizes a couple of Temnothorax species, and even more of dulosis or temporary parasitism must take into consid- surprising, several Temnothorax species may be hosts of eration that both life histories comprise the feature of para- both a Chalepoxenus and a Myrmoxenus species. Both ge- sitic colony foundation. Nevertheless, many suggestions for nera are distributed around the Mediterranean. As in the the origin of slavery exclusively refer to the slave-making workerless Myrmoxenus species, the workerless Chale- process itself. poxenus brunneus also has preserved the host-killing be- DARWIN (1859) proposed an evolutionary scenario for haviour of its dulotic congeners. One major difference be- the wood ants (Formica and allied genera), that began with tween the dulotic Chalepoxenus species and C. brunneus is brood predation for food and led via the facultative slavery that the dulotic Chalepoxenus queens kill or drive off all of the subgenus Raptiformica to the obligatory dulosis of adult workers, and take over only the host species brood, the Amazon ants, genus Polyergus. Later, two workerless whereas the C. brunneus queen stings only few of the host inquilines, Formica talbotae and F. dirksi, were detected in workers, and somehow is accepted by the others. this group (WING 1949, TALBOT 1977). Whether the latter In a third group of social parasites of the tribe Formi- two species are descendants of temporary parasite ances- coxenini no evolutionary trend, such as one from slavery tors, or derive directly from independent polygynous forms, to inquilinism, is discernible. Harpagoxenus sublaevis, is open to question. Leptothorax (= Doronomyrmex) kutteri, L. (= D.) goess- Within the myrmicine tribe Formicoxenini (Appendix waldi and L. (= D.) pacis, the four European parasites of a 1), an evolution from slave-making species to workerless, common host species, , all exhibit permanently parasitic forms has been documented in the different strategies of host exploitation. Nevertheless all genus Myrmoxenus (= Epimyrma). The life history of this four, according to Emery's rule, should be closely related genus, which was supposedly a "remarkably clear evolu- to the host species, and thus also to each other. Morpho- tionary progression leading from temporary social parasi- logical, karyological and ethological evidence support this tism to full inquilinism" (WILSON 1975), had to be rewritten assumption (BUSCHINGER 1990): Harpagoxenus sublaevis completely (BUSCHINGER 1989a, HÖLLDOBLER & WILSON is an actively dulotic species with a life history similar to 1990). In this genus neither a temporary parasite nor a typ- that of Chalepoxenus. The one dissimilarity is that H. sub- ical full inquiline has been found as yet. Instead, five spe- laevis has a different fighting technique when raiding for cies conduct slave raids with group recruitment and sting- slaves or taking over a host colony. With secateur-like man- fighting. During colony foundation the young queen throt- dibles it cuts off the appendages of the host species wor- tles the host colony queen over weeks or even months until kers. Apart from L. acervorum which is the most frequent she finally dies. In Myrmoxenus kraussei the number of wor- host of H. sublaevis, L. muscorum and L. gredleri are also kers is drastically reduced to only about 3 - 5 (one popula- enslaved. Leptothorax kutteri is a typical inquiline. It is tion is workerless; BUSCHINGER 1989b), and slave-raiding workerless, and usually several reproductive queens coexist is, thus, ineffective, even though under laboratory condi- with the L. acervorum queens in a nest. Morphologically, tions the workers are still capable of performing all raid- L. kutteri has few peculiarities, and closely resembles the ing activities. host species (BUSCHINGER 1966, ALLIES & al. 1986). Lep- Finally, three Myrmoxenus species have been found with tothorax goesswaldi was long believed to represent another only queens and no workers (M. adlerzi, M. corsicus, M. workerless inquiline. However, the L. goesswaldi queen, birgitae). Nevertheless, the young queens throttle the host soon after mating in August, penetrates a host colony and queens to death as do their slave-making relatives. Thus, waits there until the next spring. She then develops ferti- they differ from true inquilines which coexist with the host lity and slowly kills the colony's L. acervorum queens by species queens or invade orphaned host colonies (WINTER cutting off their antennae (BUSCHINGER & KLUMP 1988). 1979, BUSCHINGER & al. 1983, BUSCHINGER & WINTER Leptothorax goesswaldi therefore may be termed a "murder- 1985, DOUWES & al. 1988). Also, in this genus an evolu- parasite" in the sense of FABER (1967), or a queen-intoler- tion from normal swarming behaviour of the alate sexuals ant inquiline. Leptothorax pacis, finally, is apparently a third to mating in the mother colony, and thus inbreeding, has inquiline of L. acervorum, which lives with functional been found. Three of the slave-raiding species have mating host queens. Host species sexuals are often produced along- flights; two slave-raiding species (M. algerianus, M. bern- side the parasites' offspring (BUSCHINGER 1971, BUSCHIN- ardi) and all the "degenerate slave-makers" and worker- GER & al. 1981). More recent observations, however, re- less species of the genus mate inside the nest (Appendix 1). vealed that the L. acervorum queens in nests infested by

226 L. pacis, albeit not showing signs of being physically dam- complex in Europe comprises at least seven species. Since aged, have reduced fertility (BUSCHINGER 1990). Host spe- it is very difficult a posteriori to attribute the records of cies sexuals are reared for one or two years after the inva- Tetramorium hosts in the literature to one or the other taxon sion of a colony by L. pacis, from larvae which are still among those newly detected it is preferable at present to present. In this group of Formicoxenini the larvae usually name the host species "Tetramorium sp." In any case, also hibernate once, and often twice, before pupation. It is not in the tribe Tetramoriini nothing points to an evolution of conceivable that the three workerless species, L. kutteri, L. the inquiline genera from slave-making ancestors. goesswaldi and L. pacis, which are morphologically very In summary, little evidence supports the hypothesis of similar to their common host L. acervorum (former genus different evolutionary pathways leading from xenobiosis, Doronomyrmex) have originated from the morphologically temporary parasitism or slavery to inquilinism as had been much more specialized slave-maker genus Harpagoxenus. suggested (e.g., HÖLLDOBLER & WILSON 1990). Instead, as The inquiline status of the North American species Lep- pointed out under "Evolutionary aspects of social parasitism", tothorax (= Doronomyrmex) pocahontas is questionable, a separate origin of inquilines directly from independent, and its life history remains enigmatic (BUSCHINGER & HEIN- i.e., non-social-parasite, ancestors appears more probable. ZE 1993). As in Europe, the tribe Formicoxenini in North America comprises several slave-making and inquiline gen- Mechanisms involved in the coexistence of two or more species in one nest era and species (BUSCHINGER 1981, BEIBL & al. 2005) (Ap- pendix 1) with a couple of slave-making ants (Temnothorax The first problem a parasite queen has to cope with is to duloticus, Temnothorax sp., Protomognathus americanus, be accepted in a host species colony. Many papers have Harpagoxenus canadensis) and a few inquilines (Temno- addressed this subject. LENOIR & al. (2001) discussed a thorax minutissimus, Leptothorax paraxenus, L. wilsoni). "chemical insignificance" of young social parasites when Harpagoxenus canadensis has a number of ill-defined slave penetrating a colony, just like callow ants that quite easily species that belong to the L. muscorum complex (BUSCHIN- can integrate into a foreign colony. In addition, host and GER & al. 1980, STUART & ALLOWAY 1983). Again, noth- parasite probably are similar in their semiochemistry and ing suggests that inquilines in this group originate from du- the two factors together may facilitate the "necessary mimi- lotic relatives. cry to bypassing the colony odor barrier". The authors also The social parasites in the tribe Tetramoriini, from the reviewed the various chemical weapons applied by social genera Strongylognathus, Anergates and Teleutomyrmex, parasites such as propaganda, appeasement or repellent require a special consideration. Strongylognathus is a Pa- substances mainly during the usurpation period. laearctic genus of ca. 25 species, all characterized by saber- More generally, the coexistence of two or, in slave- shaped piercing mandibles. They live as parasites together maker colonies, even more species within a colony implies with Tetramorium species, and probably most of them are a number of mechanisms ensuring mutual tolerance and active slave-makers. Two species, S. testaceus and S. kara- more or less perfect cooperation. On the other hand, this wajewi, apparently are queen-tolerant inquilines though they coexistence also gives rise to conflicts, more than in mono- have retained a comparatively high number of own workers specific colonies, that have been addressed in numerous re- (SANETRA & BUSCHINGER 2000). Anergates atratulus is a cent publications. long-known workerless inquiline of Tetramorium species Host specificity and host-parasite recognition, im- that probably invades already orphaned host colonies. The printing. Some progress has been achieved mainly with males are wingless, "pupoid". Mating thus occurs inside the respect to imprinting and host specificity. Slave-makers mother colony whereas mated gynes disperse on the wing. (Chalepoxenus muellerianus) are known to imprint on their The sex ratio is considerably female-biased (0.67 - 0.98 fe- specific slave species. The slave-maker workers search for, male sexuals / total sexuals), and males are able to mate and attack, preferably neighbouring colonies belonging to with at least three, but supposedly many more gynes (HEIN- the same species that is already present as slaves in their ZE & al. 2007). Several Anergates queens (up to four ob- colony (SCHUMANN & BUSCHINGER 1995). Young queens served) may coexist in one host colony. Inbreeding, thus, of C. muellerianus also tend to attempt to penetrate colo- occurs regularly but is not obligatory. Teleutomyrmex nies of the host species present in their colony of birth, schneideri, finally, is the famous "ultimate social parasite" for parasitic colony foundation (SCHUMANN & BUSCHINGER (HÖLLDOBLER & WILSON 1990), extremely rarely found 1994). Imprinting mainly occurs in young slave-maker in colonies of European Tetramorium spp. and probably workers and queens after hatching from pupae. However, sharing the host species with Anergates atratulus. Teleuto- the results also suggested a pre-imaginal learning already myrmex schneideri has been found in the Swiss and French during the larval and / or pupal instars (SCHUMANN & BU- Alps, in the Pyrenees, in Spain (ESPADALER & CUESTA SCHINGER 1994). Host choice apparently is due to a blend 2006), and once in Turkmenistan (BUSCHINGER 1995). A of predisposition and early learning. That host specificity second species, T. kutteri, was described from the Spanish thus is a matter of host choice in Myrmoxenus and Chalepo- Sierra Nevada (TINAUT 1990) (Appendix 1). xenus is further supported by experiments showing that In this tribe Tetramoriini, the parasitic genera Strongy- several species could be reared with non-natural hosts, i.e., lognathus, Anergates and Teleutomyrmex apparently have that the properties of the host species may be compara- separate phylogenetic origins in the host genus Tetramo- tively irrelevant (SCHUMANN & BUSCHINGER 1995, BU- rium (see SANETRA & BUSCHINGER 2000). The host species SCHINGER 2001). Even mate recognition during sexual be- among the Tetramoriini traditionally were named Tetramo- haviour of a parasite species may be influenced by the host rium caespitum and / or Tetramorium impurum. However, species that had reared the parasites (BEIBL & al. 2007). recent investigations of SCHLICK-STEINER & al. (2006) have The other way round, also the host species may imprint demonstrated that the Tetramorium caespitum / impurum on their slave-makers. BLATRIX & SERMAGE (2005) have

227 studied this phenomenon in the slave-makers Chalepoxenus cognition in slave-making ants and their slaves the subject muellerianus and Myrmoxenus ravouxi. The principal host shall be only briefly addressed here. Chemical analyses of species of both, Temnothorax unifasciatus, imprints better and its slave species revealed that on the parasites than Temnothorax parvulus, a species that newly hatched slave-makers develop or acquire a cuticular in nature is never parasitized by any slave-maker or inqui- hydrocarbon profile matching that of the slave species pre- line. sent (D'ETTORRE & al. 2002). Social integration of P. ru- The mentioned findings in myrmicine slave-makers fescens workers into host colonies thus appears to be due match the observations of GOODLOE & al. (1987) in North to the ability to modify their cuticular hydrocarbon profile American Polyergus lucidus (Formicinae): in any single accordingly. In analogy, the slave-maker queen of Polyer- nest of this species only one out of three possible slave spe- gus breviceps kills a host colony queen and during this pro- cies has been found. The slave-makers raid only colonies cess she changes her cuticular hydrocarbon profile (JOHN- of that particular species. The Polyergus scouts must be SON & al. 2001). responsible for this selective raiding. BONO & al. (2007) Eggs, as other brood instars, of slave-making Polyergus also observed in an area with two sympatric hosts present breviceps must elicit rearing behaviour from several host (Formica occulta and Formica cf. argentea) that indivi- species. According to JOHNSON & al. (2005), two host spe- dual colonies of the slave-maker Polyergus breviceps dif- cies nevertheless discriminated against and rejected slave- fered in host preference during raiding and specialized on maker eggs, despite hydrocarbon analyses that revealed an only one of the two available host species. In line with this, adaptation to local host species. The authors suggested that for European Polyergus rufescens, LE MOLI & MORI (1987) host rearing of P. breviceps eggs might reflect an evolu- stated "we can assume that social experience immediately tionary equilibrium that is maintained by probability and following eclosion of F. cunicularia workers can fully ex- cost of recognition errors. plain their enslavement in nature and, therefore, the inter- Dominance behaviour. Among social parasites, parti- specific altruism of this host species towards the parasite." cularly among slave-maker workers, dominance behaviours Cooperation within a slave-maker colony. The neces- are frequently observed, mainly in orphaned colonies (i.e., sary cooperation within a slave-maker nest requires mutual where the parasite queen was lost). Slave-maker workers tolerance of the slaves which may have been captured as usually have well-developed ovaries but at least better de- pupae from several host colonies and which may even be- veloped ones than their slaves (BUSCHINGER 1990), and long to two or three host species. Interestingly, the pattern thus have a considerable reproductive potential (HEINZE of acceptance among slaves can differ from the accept- 1996). FRANKS & SCOVELL (1983) considered this in con- ance of slave brood by the slave-makers themselves, as in text with dominance hierarchies detected among slave- a topical example from SCHUMANN & BUSCHINGER (1991): maker workers. In their experiments, the queen solicited Harpagoxenus sublaevis enslaves up to three host species, food preferentially from dominant workers. The authors Leptothorax acervorum, L. muscorum and L. gredleri. The suggested that the queen thus might limit their production slave-makers raid on colonies of all host species indiscri- of eggs, and that the hierarchies, on the other hand, may be minately and on a few occasions all three host species have explained as competition for the production of males. been found within one and the same Harpagoxenus colony. BLATRIX & HERBERS (2004) studied dominance hierar- However, L. acervorum slaves refuse pupae of L. musco- chies in colonies of the slave-maker ant Protomognathus rum brought in by the Harpagoxenus, whereas L. musco- americanus. Both in queenright and queenless colonies rum slaves accept L. acervorum pupae. As a consequence, near-linear dominance hierarchies were found that were Harpagoxenus colonies with only L. acervorum slaves, correlated with reproductive activity. The queen, when pre- and with a mixed stock of L. acervorum and L. muscorum sent, dominates the workers and monopolizes reproduction. slaves are frequent, whereas colonies with L. muscorum In queenless nests only one of the Protomognathus wor- alone are rare, although H. sublaevis queens invade colonies kers lays eggs that develop into males. In contrast, in Po- of L. acervorum and L. muscorum for colony foundation at lyergus rufescens, the slave-maker workers produce up to about equal rates. 100% of the males reared by a queenright colony (BRUN- Slave species differ also in their inherent tendency to NER & al. 2005). The authors suggested that slave-maker cooperate with slave-makers, as follows from experiments workers are more strongly selected to increase direct fit- by MORI & al. (1996). These authors tested the accept- ness by producing sons than workers of independent spe- ance of slave-maker cocoons (Polyergus rufescens) by free- cies. living workers of two slave species, Formica cunicularia and F. rufibarbis. Workers of both species cared for the of social parasites and their hosts foreign brood and for conspecific brood at comparable In this section, further aspects of interactions between host rates. This was different, however, with cocoons of the and parasite species shall be addressed, namely those re- facultative slave-maker, Formica (Raptiformica) sanguinea: volving around the important question of whether and how They were not accepted by the two slave species although the antagonistic actions of the parasites, especially slave- both can serve as slaves in colonies of F. sanguinea. An makers, elicit measurable evolutionary reactions in the host interspecifically recognisable brood and brood species or their populations. Whereas an "evolutionary arms mimicry by Polyergus but lack of those in Raptiformica race" is clearly demonstrable on the side of the parasites and, more generally, a closer phylogenetic relationship be- with their sometimes conspicuous adaptations such as strong tween Polyergus and the slave species may be responsible mechanical armament, chemical secretions and changes for the observed differences. in life cycles, sex ratios and sexual behaviour, it is more Chemical recognition signals. Since D'ETTORRE & difficult to detect reactions of the host forms (DAVIES & HEINZE (2001) provided a detailed account of chemical re- al. 1989).

228 In this context, we have to consider the following. Though on the slaves already present. A couple of papers have nev- published data are rare, it is evident that social parasites, ertheless addressed the topic. One line of argument was that particularly the inquilines and the slave-makers, never oc- of GLADSTONE (1981) who argued that ant slaves have no cur throughout the range of the respective host species. In alternative to staying in the slave-maker nest because no fact, they often occupy only small parts of this range (e.g., other behaviour would increase their fitness. In this, the WILSON 1971, ZAMORA-MUÑOZ & al. 2003). Usually the author did not consider the possibility that slaves that have parasites are found in more or less isolated patches within absconded might reproduce by laying eggs and rearing the host range, and often these patches are characterized by male offspring which would spread genes for such rebel- particularly high densities of the host species (A. Buschin- lious behaviour. Several other authors have made oppos- ger, unpubl.). Consequently, population sizes of the para- ing observations. ALLOWAY & DEL RIO PESADO (1983) de- sites also are much smaller than those of the host species. scribed some kinds of slave aggression against the slave- Between three and ten parasitized colonies per 100 host makers, though in experiments under semi-natural condi- colonies is often a realistic estimate, within a patch where tions. CZECHOWSKI (1994) also observed some slave eman- the parasite is present at all. Inquilines may be even rarer: cipation in Formica sanguinea colonies that had been en- only 10 of 776 (1.3%) nests of Pogonomyrmex rugosus riched with many pupae of the non-natural host species, were parasitized by the inquiline, P. colei in a survey by Formica polyctena. Finally, ACHENBACH & FOITZIK (2009) JOHNSON & al. (1996), while at two other sites none out of found that slaves of the North American slave-maker, Pro- 1499 potential host colonies contained the parasite. Taking tomognathus americanus, destroy and eat considerable pro- a conservation point of view, TRONTTI & al. (2006) con- portions of the slave-maker's brood, particularly queen and cluded that populations of the rare Mediterranean Plagio- worker pupae. In this way they reduce the numbers of slave lepis xene, an inquiline of P. pygmaea, are genetically high- raids on neighbouring host species colonies, and the num- ly vulnerable, as a consequence of their rarity. bers of parasite colony foundations. Since the host colo- Of course a slave-maker colony can attack and deci- nies in the population are quite closely related among each mate several host colonies in the vicinity of its nest, but other, the rebellious slaves thus would gain indirect fitness there will always remain numerous host colonies that never by helping their non-enslaved relatives. experience any impact by slave-makers. Interestingly, dif- BRANDT & al. (2007) compared two slave-makers from ferent slave-maker species may harm their respective hosts Europe and North America using mitochondrial DNA and differently. According to HARE & ALLOWAY (2001) the microsatellite markers. They found "limited gene flow be- slave-maker Protomognathus americanus in exclosure ex- tween individual populations of both host and parasite spe- periments did not significantly damage one of its hosts, cies, allowing for a geographic mosaic of coevolution". So Temnothorax longispinosus, whereas another host, Temno- the host species in toto does not evolve any conspicuous thorax curvispinosus, experienced marked reductions in adaptations in response to parasite pressure. However, the productivity when the slave-maker Temnothorax duloticus authors were able to measure local reactions of the host pop- was present. ulations to the presence of the parasites, as well as adap- Given the restricted ranges of social parasites and the tations of the slave-maker Protomognathus americanus to very low densities as compared to their hosts it is altogether local host populations. hard to imagine how social parasitism should exert suffici- With an emphasis on coevolutionary dynamics, BRANDT ent selection pressure to stimulate the evolution of parti- & al. (2005) discussed the different interactions of host cular defensive mechanisms in a host species as a whole. and parasite in slave-makers, queen-tolerant and queen- Nevertheless, coevolution and the subject of coevoluti- intolerant inquilines, focusing on the myrmecine tribe For- onary arms race among hosts and parasites have been ad- micoxenini. According to these authors, slave-making ants dressed in recent times, frequently at the population level, act as parasites during colony foundation, while their fre- e.g., by BRANDT & FOITZIK (2004), BRANDT & al. (2005, quent slave raids follow a predator-prey dynamic; "… theory 2007), DAVIES & al. (1989), D'ETTORRE & HEINZE (2001), predicts that their associations are best described in terms FISCHER-BLASS & al. (2006), FOITZIK & al. (2003), JOHN- of a highly antagonistic coevolutionary arms race". In con- SON & HERBERS (2006). trast, BRANDT & al. (2005) further argued, queen-tolerant Little has been known on host-parasite coevolution with inquilines act as "true parasites", because of their rarity ex- respect to inquilines or temporary parasites. Of relevance in erting a low selection pressure on their hosts, and queen- this context, though, is that experimental introduction of intolerant inquilines are better classified as parasitoids. parasitic queens into host colonies often fails (ALLIES & al. Students of host-parasite systems other than ones in the 1986). Colony-founding dulotic Harpagoxenus queens fre- Formicoxenini also found evidence of local coevolution, quently are killed or driven off when they try to invade a partly differing from the conclusions by BRANDT & al. (too) large host colony. In laboratory experiments with small (2005). Thus, ZAMORA-MUÑOZ & al. (2003), investigating colonies of the host species Leptothorax acervorum, only the very rare and local slave-maker about one half of the Harpagoxenus queens were success- in Spain, observed that the host species Proformica longi- ful (WINTER & BUSCHINGER 1986). These and similar ob- seta is less aggressive towards the slave-maker in areas servations have led to the question whether enslaved ants where the parasite is present, as compared to Proformica may become rebellious and perhaps abscond from their from unparasitized populations. They found evidence sug- nest or even fight against the slave-makers, once they have gesting that the "low level of aggression might be an apo- been enslaved. morphic trait, evolved by the parasite selection pressure. A priori, such rebellions appear improbable given the For the first time in slave-maker ants, we demonstrate that fact that the slaves integrate into the slave-maker colony the decreasing of a trait (aggressiveness) could be consid- when hatching from pupae, imprinting on their masters and ered a counter-defense consequence of an arms race, a co-

229 evolutionary process in progress that matches with a Mafia parasitische Arten wurden seither entdeckt, doch wurden system" (ZAMORA-MUÑOZ & al. 2003). Fortschritte erzielt im Hinblick auf die Evolution des So- In contrast to this counterintuitive experience, D'ET- zialparasitismus und die an der Aufrechterhaltung der para- TORRE & al. (2004) reported that colonies of the slave spe- sitischen Beziehungen zwischen den Arten beteiligten Me- cies Formica rufibarbis may recognize the presence of slave- chanismen. Temporärer Sozialparasitismus, Dulosis, Inqui- maker nests (Polyergus rufescens) in their vicinity, and be- linismus und Xenobiose werden als die Hauptformen des come more aggressive towards the parasites than in areas Sozialparasitismus bei Ameisen bestätigt. Der so genannte where the slave-maker is lacking. The aggressiveness was intraspezifische Sozialparasitismus sollte gegen die obliga- particularly enhanced in the summer, when slave-makers torischen, interspezifischen Beziehungen zwischen Parasiten- are conducting their raids. und Wirtsarten klar abgegrenzt werden. All in all, at present it is difficult to figure out a clear, Es gibt einige wenige evolutive Übergänge zwischen general tendency in the issue of host-parasite coevolution for diesen Formen, hauptsächlich von der Dulosis zu einem any of the known types of social parasitism that would hold abgeleiteten Zustand ohne Arbeiterinnen. Dennoch ist kein across all major taxonomic ant groups with social parasites. Hinweis auf eine Entwicklung aller Formen des Sozial- parasitismus auf unterschiedlichen Wegen hin zum Inqui- Conclusion linismus zu finden, wie das früher vorgeschlagen worden As HEINZE (2008) has put it for ants in general, we are far war. Die Regel von Emery im weiteren Sinn wurde mittels from understanding the evolution also of social parasites, molekularer Untersuchungen bestätigt. Die Wirts-Parasit- and the appeal of TSCHINKEL (1991) to collect much more Erkennung beruht auf chemischen Cuticula-Merkmalen, data on ant life histories applies to social parasitic ants as wobei Prägung beteiligt ist. Sozialparasitische Ameisen well. Somehow it is disappointing to see that during the finden zunehmend Interesse mit Blick auf das Verständnis past 20 years fewer new parasitic species have been de- von Konflikt und Kooperation zwischen Ameisen. Koevo- scribed than over comparable earlier time stretches, al- lution von Sozialparasiten und deren jeweiligen Wirtsarten though it is likely that the discovery curve has not yet been sowie der Einfluss der Sozialparasiten auf die Wirtspopu- saturated. Also, often no or very few life history details lationen werden intensiv untersucht. Offene Fragen betref- have been provided for new species. fen die ungleichmäßige Verteilung von Sozialparasiten in- It is recommendable to search for unknown parasite nerhalb der lebenden Unterfamilien und Gattungen von species, particularly in regions where only few have been Ameisen, sowie ihre geografische Verbreitung einschließ- found as yet. Many known parasitic species remain to be lich des Fehlens von Sklavenhaltern in den Tropen. studied both in the field and in the laboratory in order to find out details of their life histories. The life history, tem- References porary parasitism, of Bothriomyrmex has been studied in ACHENBACH, A. & FOITZIK, S. 2009: First evidence for rebellion: only one out of the ca. 38 species! Sometimes surprising enslaved ant workers systematically kill the brood of their differences may be found when even very closely related social parasite Protomognathus americanus. – Evolution 63: parasite species are carefully studied. An impressive exam- 1068-1074. ple is the group of three presumed "inquilines" of Leptotho- ADAMS, R.M. & LONGINO, J.T. 2007: Nesting biology of the rax acervorum, one of which, L. goesswaldi, turned out to arboreal fungus-growing ant Cyphomyrmex cornutus and be- kill the host colony queens by the unique (and derived?) havioral interactions with the social-parasitic ant Megalomyrmex method of slowly biting off the host queen's antennae. As mondabora. – Insectes Sociaux 54: 136-143. was shown in the section on coevolution, even consider- ADAMS, R.M.M., MUELLER, U.G., SCHULTZ, T.R. & NORDEN, B. able intraspecific variation may occur in the relations of 2000: Agro-predation: usurpation of attine fungus gardens by parasites and their hosts when different populations are Megalomyrmex ants. – Naturwissenschaften 87: 549-554. compared. AGOSTI, D. 1994: A new inquiline ant (Hymenoptera: Formici- In essence, many interesting questions remain. Why is dae) in Cataglyphis and its phylogenetic relationship. – Journal social parasitism, and particularly dulosis, much more fre- of Natural History 28: 913-919. quent in temperate zones than in tropical countries? What AGOSTI, D. & JOHNSON, N.F. 2009: Antbase. World wide web is the reason for the unequal distribution of the different electronic publication. antbase.org, version (05/2005). – , retrieved on 16 January 2009. certain ant genera or tribes particularly rich in social para- AKINO, T., KNAPP J.J., THOMAS, J.A. & ELMES, G.W. 1999: Chem- sites? Why are certain species particularly preferred hosts ical mimicry and host specificity in the butterfly Maculinea for social parasites? What are the genetic implications of rebeli, a social parasite of Myrmica ant colonies. – Proceedings inbreeding which is so frequent in parasitic ants? – Myr- of the Royal Society B: Biological Sciences 266: 1419-1426. mecology, and particularly the study of social parasites, re- ALLIES, A.B., BOURKE, A.F.G. & FRANKS, N.R. 1986: Propa- mains exciting! ganda substances in the cuckoo ant Leptothorax kutteri and Acknowledgements the slave-maker Harpagoxenus sublaevis. – Journal of Chemi- cal Ecology 12: 1285-1293. The author thanks J. Heinze and an anonymous referee for ALLOWAY, T.M. 1979: Raiding behaviour of two species of slave- helpful comments. Thanks are due also to the editors for making ants, Harpagoxenus americanus (EMERY) and Lepto- their patience. thorax duloticus WESSON (Hymenoptera: Formicidae). – Ani- mal Behaviour 27: 202-210. Zusammenfassung ALLOWAY, T.M. 1980: The origins of slavery in leptothoracine Die letzte Übersicht über den Sozialparasitismus bei Amei- ants (Hymenoptera: Formicidae). – The American Naturalist sen wurde 1990 publiziert. Vergleichsweise wenige neue 115: 247-261.

230 ALLOWAY, T.M. 2009: The inquiline parasite Leptothorax paro- BRANDT, M. & FOITZIK, S. 2004: Community context and specia- xenus. – , retrieved on 9 February 2009. – Ecology 85: 2997-3009. ALLOWAY, T.M., BUSCHINGER, A., TALBOT, M., STUART, R.J. & BRANDT, M., FOITZIK, S., FISCHER-BLASS, B. & HEINZE, J. 2005: THOMAS, C. 1982: Polygyny and polydomy in three North The coevolutionary dynamics of obligate ant social parasite American species of the ant genus Leptothorax MAYR (Hy- systems – between prudence and antagonism. – Biological Re- menoptera: Formicidae). – Psyche 89: 249-274. views 80: 251-267. ALLOWAY, T.M. & DEL RIO PESADO, M.G. 1983: Behavior of the BRUNNER, E., TRINDL, A., FALK, K.H., HEINZE, J. & D'ETTORRE, slave-making ant, Harpagoxenus americanus (EMERY), and its P. 2005: Reproductive conflict in social insects: male repro- host species under "seminatural" laboratory conditions (Hy- duction by workers in a slave-making ant. – Evolution 59: menoptera. Formicidae). – Psyche 90: 425-436. 2480-2482. ARON, S., PASSERA, L. & KELLER, L. 1999: Evolution of social BUSCHINGER, A. 1966 [1965]: Leptothorax (Mychothorax) kutteri parasitism in ants: size of sexuals, sex ratio and mechanisms n.sp., eine sozialparasitische Ameise (Hymenoptera, Formici- of caste determination. – Proceedings of the Royal Society B: dae). – Insectes Sociaux 12: 327-334. Biological Sciences 266: 173-177. BUSCHINGER, A. 1970: Neue Vorstellungen zur Evolution des BAUR, A., CHALWATZIS, N., BUSCHINGER, A. & ZIMMERMANN, Sozialparasitismus und der Dulosis bei Ameisen (Hym., For- F.K. 1995: Mitochondrial DNA sequences reveal close rela- micidae). – Biologisches Zentralblatt 88: 273-299. tionships between social parasitic ants and their host species. – Current Genetics 28: 242-247. BUSCHINGER, A. 1971: Zur Verbreitung und Lebensweise sozial- parasitischer Ameisen des Schweizer Wallis (Hym., Formici- BEEKMAN, M. & OLDROYD, B.P. 2008: When workers disunite: dae). – Zoologischer Anzeiger 186: 47-59. intraspecific parasitism in eusocial bees. – Annual Review of Entomology 53: 19-37. BUSCHINGER, A. 1974: Mono- und Polygynie in Insektensozie- täten. In: SCHMIDT, G.H. (Ed.): Sozialpolymorphismus bei In- BEIBL, J., STUART, R.J., HEINZE, J. & FOITZIK, S. 2005: Six origins sekten. – Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp. of slavery in formicoxenine ants. – Insectes Sociaux 52: 291- 862-896. 297. BUSCHINGER, A. 1979: Functional monogyny in the American BEIBL, J., D'ETTORRE, P. & HEINZE, J. 2007: Cuticular profiles and guest ant Formicoxenus hirticornis (EMERY) (= Leptothorax mating preference in a slave-making ant. – Insectes Sociaux hirticornis) (Hym., Form.). – Insectes Sociaux 26: 61-68. 54: 174-182. BUSCHINGER, A. 1981: Biological and systematic relationships BLATRIX, R. & HERBERS, J. 2004: Intracolonial conflict in the slave- of social parasitic Leptothoracini from Europe and North Ame- making ant Protomognathus americanus: dominance hierar- rica. In: HOWSE, P.E. & CLÉMENT, J.-L. (Eds.): Biosystematics chies and individual reproductive success. – Insectes Sociaux of social insects. – Academic Press, London and New York, 51: 131-138. pp. 211-222. BLATRIX, R. & SERMAGE, C. 2005: Role of early experience in BUSCHINGER, A. 1986: Evolution of social parasitism in ants. – ant enslavement: a comparative analysis of a host and a non- Trends in Ecology and Evolution 1: 155-160. host species. – Frontiers in Zoology 2: 13. BUSCHINGER, A. 1989a: Evolution, speciation, and inbreeding in BOER, P. & NOORDIJK, J. 2005: Myrmica schenckioides nov. sp., a new socially parasitic ant species (Hym., Formicidae). – Ento- the parasitic ant genus Epimyrma (Hymenoptera, Formicidae). mologische Berichten 65: 120-123. – Journal of Evolutionary Biology 2: 265-283. BUSCHINGER, A. 1989b: Workerless Epimyrma kraussei EMERY, BOLTON, B. 1986a: A taxonomic and biological review of the tetramoriine ant genus Rhoptromyrmex (Hymenoptera: Formi- 1915, the first parasitic ant of Crete. – Psyche 96: 69-74. cidae). – Systematic Entomology 11: 1-17. BUSCHINGER, A. 1990: Sympatric speciation and radiative evo- BOLTON, B. 1986b: Apterous females and shift of dispersal stra- lution of socially parasitic ants – heretic hypotheses and their tegy in the Monomorium salomonis-group (Hymenoptera: For- factual background. – Zeitschrift für Zoologische Systematik micidae). – Journal of Natural History 20: 267-272. und Evolutionsforschung 28: 241-260. BOLTON, B. 2003: Synopsis and classification of Formicidae. – BUSCHINGER, A. 1995: Nicht am Ende: Die "Endameise" Teleu- Memoirs of the American Entomological Institute 71: 1-370. tomyrmex schneideri. – Ameisenschutz aktuell 9: 1-7. BONO, J.M., BLATRIX, R., ANTOLIN, M.F. & HERBERS, J.M. 2007: BUSCHINGER, A. 2001: Multiple Hybridisierung von Arten der Pirate ants (Polyergus breviceps) and sympatric hosts (For- Ameisen-Gattung Epimyrma (Hymenoptera: Formicidae), und mica occulta and Formica sp. cf. argentea): host specificity Beobachtungen zur Ausbeutung der Wirtsarten durch die Para- and coevolutionary dynamics. – Biological Journal of the Lin- siten. – Myrmecologische Nachrichten 4: 25-35. nean Society 91: 565-572. BUSCHINGER, A., CAGNIANT, H., EHRHARDT, W. & HEINZE, J. 1989 BOURKE, A.F. & FRANKS, N.R. 1991: Alternative adaptations, sym- [1988]: Chalepoxenus brunneus, a workerless "degenerate slave- patric speciation and the evolution of parasitic, inquiline ants. maker" ant (Hymenoptera, Formicidae). – Psyche 95: 253-263. – Biological Journal of the Linnean Society 43: 157-178. BUSCHINGER, A. & CROZIER, R.H. 1987: Towards a unified re- BRANDÃO, C.R.F. 1990: Systematic revision of the Neotropical productive biology of the Hymenoptera. In: EDER, J. & REM- ant genus Megalomyrmex FOREL (Hymenoptera: Formicidae: BOLD, H. (Eds.): Chemistry and biology of social insects. – Myrmicinae), with the description of thirteen new species. – Verlag J. Peperny, München, pp. 251-252. Arquivos de Zoologia 31: 411-481. BUSCHINGER, A., EHRHARDT, W. & FISCHER, K. 1981: Dorono- BRANDÃO, C.R.F. 2003: Further revisionary studies on the ant myrmex pacis, Epimyrma stumperi und E. goesswaldi (Hym., genus Megalomyrmex FOREL (Hymenoptera: Formicidae: Myr- Formicidae) neu für Frankreich. – Insectes Sociaux 28: 67-70. micinae: Solenopsidini). – Papéis Avulsos de Zoologia 48: BUSCHINGER, A., EHRHARDT, W., FISCHER, K. & OFER, J. 1988: The 145-159. slave-making ant genus Chalepoxenus (Hymenoptera, Formi- BRANDT, M., FISCHER-BLASS, B., HEINZE, J. & FOITZIK, S. 2007: cidae). I. Review of literature, range, slave species. – Zoolo- Population structure and the co-evolution between social para- gische Jahrbücher, Abteilung für Systematik, Geographie und sites and their hosts. – Molecular Ecology 16: 2063-2078. Biologie der Tiere 115: 383-401.

231 BUSCHINGER, A., EHRHARDT, W. & WINTER, U. 1980: The orga- DOUWES, P., JESSEN, K. & BUSCHINGER, A. 1988: Epimyrma ad- nization of slave raids in dulotic ants – a comparative study lerzi sp.n. (Hymenoptera: Formicidae) from Greece: morpholo- (Hymenoptera, Formicidae). – Zeitschrift für Tierpsychologie gy and life history. – Entomologica scandinavica 19: 239-249. 53: 245-264. EHRHARDT, W. 1982: Untersuchungen zum Raubzugverhalten der BUSCHINGER, A. & HEINZE, J. 1992: Polymorphism of female sozialparasitischen Ameise Chalepoxenus muellerianus (FINZI) reproductives in ants. In: BILLEN, J. (Ed.): Biology and evolu- (Hym., Formicidae). – Zoologischer Anzeiger 208: 145-160. tion of social insects. – Leuven University Press, Leuven, pp. EHRHARDT, W. 1987: Biosystematics of the slavemaking ant ge- 11-23. nus Chalepoxenus. In: EDER, J. & REMBOLD, H. (Eds.): Chem- BUSCHINGER, A. & HEINZE, J. 1993: Doronomyrmex pocahontas: istry and biology of social insects. – Verlag J. Peperny, Mün- not a workerless parasite but still an enigmatic taxon (Hymeno- chen, pp. 39-40. ptera, Formicidae). – Insectes Sociaux 40: 423-432. ELMES, G.W. 1973: Miniature queens of the ant Myrmica rubra L. BUSCHINGER, A. & KLUMP, B. 1988: Novel strategy of host- (Hymenoptera, Formicidae). – The Entomologist 106: 133-136. colony exploitation in a permanently parasitic ant, Doronomyr- ELMES, G.W. 1976: Some observations on the microgyne form mex goesswaldi. – Naturwissenschaften 75: 577-578. of Myrmica rubra L. (Hymenoptera, Formicidae). – Insectes BUSCHINGER, A. & LINKSVAYER, T.A. 2004: Novel blend of life Sociaux 23: 3-22. history traits in an inquiline ant, Temnothorax minutissimus, ELMES, G.W. 1978: A morphometric comparison of three close- with a description of the male (Hymenoptera: Formicidae). – ly related species of Myrmica (Formicidae), including a new Myrmecologische Nachrichten 6: 67-76. species from England. – Systematic Entomology 3: 131-145. BUSCHINGER, A., PEETERS, C. & CROZIER, R.H. 1990: Life pat- EMERY, C. 1909: Über den Ursprung der dulotischen, parasiti- tern studies on an Australian Sphinctomyrmex: functional po- schen und myrmekophilen Ameisen. – Biologisches Central- lygyny, brood periodicity and raiding behavior. – Psyche 96: blatt 29: 352-362. 287-300. ERRARD, C. & D'ETTORRE, P. 1998: Chemical disguise by the BUSCHINGER, A. & WINTER, U. 1976: Funktionelle Monogynie bei queen of the slave-making ant Polyergus rufescens during col- der Gastameise Formicoxenus nitidulus (NYL.) (Hym., Form.). ony foundation. – Social Life 2: 71-77. – Insectes Sociaux 23: 549-558. ESPADALER, X. & CUESTA, D. 2006: Teleutomyrmex schneideri BUSCHINGER, A. & WINTER, U. 1985: Life history and male KUTTER, 1950 en España (Hymenoptera, Formicidae). – Graell- morphology of the workerless parasitic ant Epimyrma corsica sia 62: 261-262. (Hymenoptera: Formicidae). – Entomologia Generalis 10: 65-75. FABER, W. 1967: Beiträge zur Kenntnis sozialparasitischer Amei- BUSCHINGER, A., WINTER, U. & FABER, W. 1983: The biology of sen, 1: Lasius (Austrolasius n. sg.) reginae n.sp., eine neue tem- RUZSKY, a slave-making ant (Hyme- porär sozialparasitische Erdameise aus Österreich (Hym. For- noptera, Formicidae). – Psyche 90: 335-342. micidae). – Pflanzenschutz-Berichte 36: 73-107. CAGNIANT, H. 1985: Contribution à la connaissance des fourmis FEITOSA, R.M., HORA, R.R., DELABIE, J.H.C., VALENZUELA, J. & marocaines: Chalepoxenus brunneus n.sp. (Hymenoptera, Myr- FRESNEAU, D. 2008: A new social parasite in the ant genus Ec- micidae). – Nouvelle Revue Entomologique (N.S.) 2: 141-146. tatomma F. SMITH (Hymenoptera, Formicidae, Ectatomminae). CAGNIANT, H. 2006: Liste actualisee des fourmis du Maroc (Hy- – Zootaxa 1713: 47-52. menoptera: Formicidae). – Myrmecologische Nachrichten 8: FISCHER-BLASS, B., HEINZE, J. & FOITZIK, S. 2006: Microsatellite 193-200. analysis reveals strong, but differential impact of a social para- CZECHOWSKI, W. 1994: Emancipation of slaves in Formica san- site on its two host species. – Molecular Ecology 15: 863-872. guinea LATR. colonies (Hymenoptera, Formicidae). – Annales FOITZIK, S., FISCHER, B. & HEINZE, J. 2003: Arms races between Zoologici 45: 15-26. social parasites and their hosts: geographic patterns of mani- DARWIN, C. 1859: On the origin of species by means of natural pulation and resistance. – Behavioral Ecology 14: 80-88. selection, or the preservation of favoured races in the struggle FOITZIK, S. & HEINZE, J. 1998: Nest site limitation and colony for life. – John Murray, London, 502 pp. takeover in the ant Leptothorax nylanderi. – Behavioral Ecol- DAVIES, N.B., BOURKE, A.F.G. & BROOKE, M. DE L. (1989): Cuck- ogy 9: 367-375. oos and parasitic ants: interspecific brood parasitism as an evo- FOITZIK, S. & HEINZE, J. 2000: Intraspecific parasitism and split lutionary arms race. – Trends in Ecology and Evolution 4: sex ratios in a monogynous and monandrous ant. – Behavi- 274-278. oural Ecology and Sociobiology 47: 424-431. D'ETTORRE, P., BRUNNER, E., WENSELEERS, T. & HEINZE, J. 2004: FOITZIK, S. & HEINZE, J. 2001: Microgeographic genetic structure Knowing your enemies: seasonal dynamics of host-social pa- and intraspecific parasitism in the ant Leptothorax nylanderi. rasite recognition. – Naturwissenschaften 91: 594-597. – Ecological Entomology 26: 449-456. D'ETTORRE, P. & HEINZE, J. 2001: Sociobiology of slave-making FRANCOEUR, A. 2007: The Myrmica punctiventris and M. cras- ants. – Acta ethologica 3: 67-82. sirugis species groups in the Nearctic region. In: SNELLING, D'ETTORRE, P., MONDY, N., LENOIR, A. & ERRARD, C. 2002: Blend- R.R., FISHER, B.L. & WARD, P.S. (Eds.): Advances in ant sys- ing in with the crowd: social parasites integrate into their host tematics (Hymenoptera: Formicidae): homage to E. O. Wilson colonies using a flexible chemical signature. – Proceedings – 50 years of contributions. – Memoirs of the American Ento- of the Royal Society B: Biological Sciences 269: 1911-1918. mological Institute 80: 153-185. DEYRUP, M. & RUSAK, Z. 2008: Solenopsis enigmatica, a new FRANCOEUR, A., LOISELLE, R. & BUSCHINGER, A. 1985: Biosys- species of inquiline ant from the island of Dominica, West tématique de la tribu Leptothoracini (Formicidae, Hymeno- Indies (Hymenoptera: Formicidae). – Florida Entomologist 91: ptera). 1 – Le genre Formicoxenus dans la region holarctique. 70-74. – Naturaliste Canadien 112: 343-403. DOROW, W.H.O. 1995: Revision of the ant genus Polyrhachis FRANKS, N.R. & BOURKE, A.F.G. 1990: The evolution of inqui- SMITH, 1857 (Hymenoptera: Formicidae: Formicinae) on sub- line ant parasites: the interspecific versus the intraspecific hypo- genus level with keys, checklist of species and bibliography. – thesis. In: VEERESH, G.K., MALLIK, B. & VIRAKTAMATH, C.A. Courier Forschungsinstitut Senckenberg 185: 1-113. (Eds.): Social insects and the environment. – Proceedings of

232 th the 11 International Congress of IUSSI, 1990. – Oxford & HUBER, P. 1810: Recherches sur les moeurs des fourmis indi- IBH Publishing Co., New Delhi, Bombay, Calcutta, pp. 149-150. gènes. – J.J. Paschoud, Paris, XIII + 328 pp. FRANKS, N.R. & SCOVELL, E. 1983: Dominance and reproduc- JESSEN, K. & KLINKICHT, M. 1990: Hybridization in the social tive success among slave-making worker ants. – Nature 304: parasitic ant genus Epimyrma (Hymenoptera, Formicidae). – 724-725. Insectes Sociaux 37: 273-293. GLADSTONE, D.E. 1981: Why there are no ant slave rebellions. – JOHNSON, C.A. & HERBERS, J.M. 2006: Impact of parasite sym- The American Naturalist 117: 779-781. patry on the geographic mosaic of coevolution. – Ecology 87: 382-394. GOODLOE, L., SANWALD, R. & TOPOFF, H. 1987: Host specificity in raiding behavior of the slave-making ant, Polyergus luci- JOHNSON, C.A., TOPOFF, H., VAN DER MEER, R.K. & LAVINE, B. dus. – Psyche 94: 39-44. 2002: Host queen killing by a slave-maker ant queen: when is a host queen worth attacking? – Behaviour 64: 807-815. GÖSSWALD, K. 1938: Grundsätzliches über parasitische Ameisen unter besonderer Berücksichtigung der abhängigen Kolonie- JOHNSON, C.A., TOPOFF, H., VAN DER MEER, R.K. & LAVINE, B. gründung von Lasius umbratus mixtus NYL. – Zeitschrift für 2005: Do these eggs smell funny to you?: an experimental wissenschaftliche Zoologie 151: 101-148. study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae). – Behavi- HARE, J.F. & ALLOWAY, T.M. 2001: Prudent Protomognathus oral Ecology and Sociobiology 57: 245-255. and despotic Leptothorax duloticus: differential costs of ant slavery. – Proceedings of the National Academy of Sciences JOHNSON, C.A., VANDER MEER, R.K. & LAVINE, B. 2001: Changes of the of America 98: 12093-12096. in the cuticular hydrocarbon profile of the slave-maker ant queen, Polyergus breviceps EMERY, after killing a Formica HASEGAWA, E., TINAUT, A. & RUANO, F. 2002: Molecular phylo- host queen (Hymenoptera: Formicidae). – Journal of Chemi- geny of two slave-making ants: Rossomyrmex and Polyergus cal Ecology 27: 1787-1804. (Hymenoptera: Formicidae). – Annales Zoologici Fennici 39: 267-271. JOHNSON, N.F. 2007: Hymenoptera Name Server version 1.5, 19. XII.2007. – , retrieved on HEINZE, J. 1989: Leptothorax wilsoni n. sp., a new parasitic ant 11 March 2009. from eastern North America (Hymenoptera: Formicidae). – Psyche 96: 49-61. JOHNSON, R.A. 1994: Distribution and natural history of the wor- kerless inquiline ant Pogonomyrmex anergismus COLE (Hy- HEINZE, J. 1993: Life history strategies of subarctic ants. – Arctic menoptera: Formicidae). – Psyche 101: 257-262. 46: 354-358. JOHNSON, R.A., PARKER, J.D. & RISSING, S.W. 1996: Rediscovery HEINZE, J. 1995: The origin of workerless social parasites in for- of the workerless inquiline ant Pogonomyrmex colei and addi- micoxenine ants. – Psyche 102: 195-214. tional notes on natural history (Hymenoptera: Formicidae). – HEINZE, J. 1996: The reproductive potential of workers in slave- Insectes Sociaux 43: 69-76. making ants. – Insectes Sociaux 43: 319-328. KELLER, L. (Ed.) 1993: Queen number and sociality in insects. HEINZE, J. 2008: The demise of the standard ant (Hymenoptera, – Oxford University Press, Oxford, New York, Tokyo, XII + Formicidae). – Myrmecological News 11: 9-20. 439 pp. HEINZE, J. & ALLOWAY, T.M. 1991: Leptothorax paraxenus n. KINOMURA, K. & YAMAUCHI, K. 1992: A new workerless soci- sp., a workerless social parasite from North America (Hyme- ally parasitic species of the genus Vollenhovia (Hymenoptera, noptera: Formicidae). – Psyche 98: 195-206. Formicidae) from Japan. – Japanese Journal of Entomology 60: 203-206. HEINZE, J., LAUTENSCHLÄGER, B. & BUSCHINGER, A. 2007: Female- biased sex ratios and unusually potent males in the social pa- KOHOUT, R.J. 1990: A review of the Polyrhachis viehmeyeri spe- rasite Anergates atratulus (Hymenoptera: Formicidae). – Myr- cies-group (Hymenoptera: Formicidae: Formicinae). – Mem- mecological News 10: 1-5. oirs of Queensland Museum 28: 499-508. HEINZE, J., TRUNZER, B., LECHNER, K. & ORTIUS, D. 1995: A KUTTER, H. 1968 [1969]: Die sozialparasitischen Ameisen der second host species of the inquiline ant Leptothorax wilsoni. Schweiz. – Neujahrsblatt herausgegeben von der Naturfor- – Psyche 102: 73-77. schenden Gesellschaft in Zürich 171: 1-62. HERBERS, J.M. 2006: The loaded language of science. – Chroni- LE MASNE, G. 1956: Recherches sur les fourmis parasites. Le cle of Higher 52: B5. parasitisme social double. – Comptes rendues des Séances de l'Académie des Sciences (Paris) 243: 1243-1246. HERBERS, J.M. 2007: The loaded language of science. – Notes from Underground 12-1, , retrieved traspecific slavery in Polyergus rufescens LATR. (Hymenoptera, on 24 March 2008. Formicidae): field and laboratory observations. – Insectes So- ciaux 40: 433-437. HÖLLDOBLER, B. 1976: Tournaments and slavery in a desert ant. – Science 192: 912-914. LE MOLI, F. & MORI, A. 1987: Why a slave ant species accepts and cares for cocoons of its slave maker. – Insectes Sociaux HÖLLDOBLER, B. 1979: Territoriality in ants. – Proceedings of the 34: 136-141. American Philosophical Society 123: 211-218. LENOIR, A., D'ETTORRE, P., ERRARD, C. & HEFETZ, A. 2001: Chem- HÖLLDOBLER, B. 1982: Communication, raiding behavior and prey ical ecology and social parasitism in ants. – Annual Review storage in Cerapachys (Hymenoptera; Formicidae). – Psyche of Entomology 46: 573-599. 89: 3-23. LENOIR, A., MALOSSE, C. & YAMAOKA, R. 1997: Chemical mimi- HÖLLDOBLER, B. & WILSON, E.O. 1990: The ants. – The Belknap cry between parasitic ants of the genus Formicoxenus and their Press of Harvard University Press, Cambridge, MA, 732 pp. host Myrmica (Hymenoptera, Formicidae). – Biochemical HORA, R.R., DOUMS, C., POTEAUX, C., FÉNÉRON, R., VALENZU- Systematics and Ecology 25: 379-389. ELA, J., HEINZE, J. & FRESNEAU, D. 2005: Small queens in the LEPONCE, M., ROISIN, Y. & PASTEELS, J.M. 1999: Community ant Ectatomma tuberculatum: a new case of social parasitism. interactions between ants and arboreal-nesting termites in New – Behavioral Ecology and Sociobiology 59: 285-292. Guinea coconut plantations. – Insectes Sociaux 46: 126-130.

233 MARIKOVSKY, P.I. 1974: The biology of the ant Rossomyrmex SANETRA, M. & GÜSTEN, R. 2001: The socially parasitic ant genus proformicarum K. W. ARNOLDI (1928). – Insectes Sociaux 21: Strongylognathus MAYR in North Africa (Insecta: Hymeno- 301-308. ptera: Formicidae). – Zootaxa 20: 1-20. MASCHWITZ, U., DOROW, W.H.O., BUSCHINGER, A. & KALYTTA, SANTSCHI, F. 1906: A propos de moeurs parasitiques temporaires G. 2000: Social parasitism involving ants of different subfam- des fourmis du genre Bothriomyrmex. – Annales de la Société ilies: Polyrhachis lama (Formicinae) an obligatory inquiline Entomologique de 75: 363-392. of Diacamma sp. (Ponerinae) in Java. – Insectes Sociaux 47: SATOH, A. & OHKAWARA, K. 2008: Dominance hierarchies and ag- 27-35. gressive behaviour among queens of the inquiline ant Vollen- MASCHWITZ, U., GO, C., DOROW, W.H.O., BUSCHINGER, A. & hovia nipponica. – Insectes Sociaux 55: 200-206. OHOUT K , R.J. 2003: Polyrhachis loweryi (Formicinae): a guest SAVOLAINEN, R. & VEPSÄLÄINEN, K. 2003: Sympatric speciation ant parasitizing Rhytidoponera sp. (Ponerinae) in Queensland, through intraspecific social parasitism. – Proceedings of the Australia. – Insectes Sociaux 50: 69-76. National Academy of Sciences of the United States of Ame- MASCHWITZ, U., GO, C., KAUFMANN, E. & BUSCHINGER, A. 2004: rica 100: 7169-7174. A unique strategy of host colony exploitation in a parasitic ant: SCHLICK-STEINER, B.C., STEINER, F.M., MODER, K., SEIFERT, B., workers of Polyrhachis lama rear their brood in neighbouring SANETRA, M., DYRESON, E., STAUFFER, C. & CHRISTIAN, E. host nests. – Naturwissenschaften 91: 40-43. 2006: A multidisciplinary approach reveals cryptic diversity in MATTHEIS, F. 2003: Bemerkungen zur temporär sozialparasiti- western Palaearctic Tetramorium ants (Hymenoptera: Formi- schen Koloniegründung von Lasius (Dendrolasius) fuligino- cidae). – Molecular and Evolution 40: 259-273. sus. – Ameisenschutz aktuell 17: 7-19. SCHULTZ, T.R., BEKKEVOLD, D. & BOOMSMA, J.J. 1998: Acro- MORI, A., D'ETTORRE, P. & LE MOLI, F. 1996: Selective accept- myrmex insinuator new species: an incipient social parasite of ance of the brood of two formicine slave-making ants by host fungus-growing ants. – Insectes Sociaux 45: 457-471. and non-host related species. – Insectes Sociaux 43: 391-400. SCHUMANN, R.D. 1992: Raiding behavior of the dulotic ant Cha- MORI, A., GRASSO, D.A., VISICCHIO, R. & LE MOLI, F. 2000: lepoxenus muellerianus (FINZI) in the field (Hymenoptera: Colony founding in Polyergus rufescens: the role of the Du- Formicidae, Myrmicinae). – Insectes Sociaux 39: 325-333. four's gland. – Insectes Sociaux 47: 7-10. SCHUMANN, R.D. & BUSCHINGER, A. 1991: Selective acceptance MORI, A. & LE MOLI, F. 1998: Mating behavior and colony found- of host species pupae by slaves of the dulotic ant, Har- ing of the slave-making ant Formica sanguinea (Hymeno- pagoxenus sublaevis (Hymenoptera, Formicidae, Myrmicinae). ptera: Formicidae). – Journal of Insect Behavior 11: 235-245. – Ethology 88: 154-162. MUNDAY, P.L., VAN HERWERDEN, L. & DUDGEON, C.L. 2004: SCHUMANN, R.D. & BUSCHINGER, A. 1994: Imprinting effects on Evidence for sympatric speciation by host shift in the sea. – host-selection behaviour of colony-founding Chalepoxenus Current Biology 14: 1498-1504. muellerianus (FINZI) females (Hymenoptera, Formicidae). – PARKER, J.D. & RISSING, S.W. 2002: Molecular evidence for the Ethology 97: 33-46. origin of workerless social parasites in the ant genus Pogono- SCHUMANN, R.D. & BUSCHINGER, A. 1995: Imprinting effects on myrmex. – Evolution 56: 2017-2028. host-selection behaviour of slave-raiding Chalepoxenus muel- PEARSON, B. 1981: The electrophoretic determination of Myr- lerianus (FINZI) workers (Hymenoptera: Formicidae). – Ethol- mica rubra microgynes as a social parasite: possible signifi- ogy 99: 243-251. cance in the evolution of ant social parasites. In: HOWSE, P.E. SEIFERT, B. 2007: Die Ameisen Mittel- und Nordeuropas. – lutra & CLEMENT, J.-L. (Eds.): Biosystematics of social insects. – Verlags- und Vertriebsgesellschaft, Tauer, 368 pp. Academic Press, London, New York, Toronto, Sydney, San SEIFERT, B. & BUSCHINGER, A. 2002: Pleometrotische Kolonie- Francisco, pp. 75-84. gründung von Lasius meridionalis (BONDROIT, 1920) bei La- POLLOCK, G.B. & RISSING, S.W. 1989: Intraspecific brood raid- sius paralienus SEIFERT, 1992, mit Bemerkungen über mor- ing, territoriality, and slavery in ants. – The American Nat- phologische und ethologische Anpassungen an die sozialpara- uralist 133: 61-70. sitische Koloniegründung (Hymenoptera: Formicidae). – Myr- RABELING, C., BROWN, J.M. & VERHAAGH, M. 2008: Newly dis- mecologische Nachrichten 4: 11-15. covered sister lineage sheds light on early ant evolution. – Pro- SMITH, J.A., TIERNEY, S.M., PARK, Y.C., FULLER, S. & SCHWARZ, ceedings of the National Academy of Sciences of the United M.P. 2007: Origins of social parasitism: the importance of di- States of America 105: 14913-14917. vergence ages in phylogenetic studies. – Molecular Phylogen- RADCHENKO, A. & ELMES, G. 2003: A taxonomic revision of the etics and Evolution 43: 1131-1137. socially parasitic Myrmica ants (Hymenoptera: Formicidae) SOUZA, D.J., SOARES, I.M.F. & DELLA LUCIA, T.M.C. 2007: Acro- of the Palaearctic region. – Annales Zoologici (Warszawa) myrmex ameliae sp. n. (Hymenoptera: Formicidae): a new so- 53: 217-243. cial parasite of leaf-cutting ants in Brazil. – Insect Science 14: REGNIER, F.E. & WILSON, E.O. 1971: Chemical communication 251-257. and "propaganda" in slave-maker ants. – Science 172: 267-269. STEINER, F.M., SCHLICK-STEINER, B.C., KONRAD, H., MODER, K., ROSENGREN, R. & PAMILO, P. 1983: The evolution of polygyny CHRISTIAN, E., SEIFERT, B., CROZIER, R.H., STAUFFER, C. & and polydomy in mound-building Formica ants. – Acta En- BUSCHINGER, A. 2006: No sympatric speciation here: multiple tomologica Fennica 42: 65-77. data sources show that the ant Myrmica microrubra is not a RÜPPELL, O., HEINZE, J. & HÖLLDOBLER, B. 2001: Complex de- separate species but an alternate reproductive morph of Myr- termination of queen body size in the queen size dimorphic ant mica rubra. – Journal of Evolutionary Biology 19: 777-787. Leptothorax rugatulus (Formicidae: Hymenoptera). – Here- STUART, R.J. & ALLOWAY, T.M. 1982: Territoriality and the origin dity 87: 33-40. of slave raiding in leptothoracine ants. – Science 215: 1262-1263. SANETRA, M. & BUSCHINGER, A. 2000: Phylogenetic relation- STUART, R.J. & ALLOWAY, T.M. 1983: The slave-making ant, ships among social parasites and their hosts in the ant tribe Harpagoxenus canadensis M.R. SMITH, and its host species Tetramoriini (Hymenoptera: Formcidae). – European Journal NYLANDER: slave raiding and territo- of Entomology 97: 95-117. riality. – Behaviour 85: 58-90.

234 STUEWER, S. 1992: Morphologische Untersuchungen an Parasiten Psychologie und Entwicklungsgeschichte der Ameisengesell- und selbständigen Ameisen der Tribus Plagiolepidini. – Di- schaften. – Aschendorffsche Buchdruckerei, Münster in West- ploma Thesis, Darmstadt University of Technology, 115 pp. falen. VII + 262 pp. SUMNER, S., AANEN, D.K., DELABIE, J. & BOOMSMA J.J. 2004: The WEST-EBERHARD, M.J. 1986: Alternative adaptations, speciation evolution of social parasitism in Acromyrmex leaf-cutting ants: and phylogeny. – Proceedings of the National Academy of a test of Emery’s rule. – Insectes Sociaux 52: 37-42. Sciences of the United States of America 83: 1388-1392. SUMNER, S., NASH, D.R. & BOOMSMA, J.J. 2003: The adaptive sig- WEST-EBERHARD, M.J. 2005: Developmental plasticity and the nificance of inquiline parasite workers. – Proceedings of the origin of species differences. – Proceedings of the National Royal Society B: Biological Sciences 270: 1315-1322. Academy of Sciences of the United States of America 102: TALBOT, M. 1977 [1976]: The natural history of the workerless 6543-6549. ant parasite, Formica talbotae. – Psyche 83: 282-288. WHEELER, W.M. 1910: Ants: their structure, development, and TINAUT, A. 1990: Teleutomyrmex kutteri, spec. nov. A new species behavior. – Columbia University Press, New York, London, from Sierra Nevada (Granada, Spain). – Spixiana 13: 201-208. XXV + 663 pp. TINAUT, A. 2007: A new species of the genus Rossomyrmex AR- WILSON, E.O. 1971: The insect societies. – Belknap Press of Har- NOLDI, 1928 from Turkey (Hymenoptera, Formicidae). – Graell- vard University Press, Cambridge, MA, X + 548 pp. sia 63: 135-142. WILSON, E.O. 1975: Sociobiology, the new synthesis. – Belknap TINAUT, A., ESPADALER, X. & JIMÉNEZ, J.J. 1992: Camponotus Press of Harvard University Press, Cambridge, MA, IX + 697 pp. universitatis FOREL, 1891, en la Península Ibérica. Descripción WILSON, E.O. 1984: Tropical social parasites in the ant genus de sus sexuados (Hymenoptera, Formicidae). – Nouvelle Revue Pheidole, with an analysis of the anatomical parasitic syndrome d'Entomologie (n.s.) 9: 233-238. (Hymenoptera: Formicidae). – Insectes Sociaux 31: 316-334. TOPOFF, H. 1990: Slave-making ants. – American Scientist 78: WING, M.W. 1949: A new Formica from northern Maine, with a 520-528. discussion of its supposed type of social parasitism (Hymeno- TOPOFF, H., LAMON, B., GOODLOE, L. & GOLDSTEIN, M. 1984: ptera: Formicidae). – The Canadian Entomologist 81: 13-17. Social and orientation behavior of Polyergus breviceps during WINTER, U. 1979: Epimyrma goesswaldi MENOZZI, eine sklaven- slave-making raids. – Behavioral Ecology and Sociobiology haltende Ameise. – Naturwissenschaften 66: 581-582. 15: 273-279. WINTER, U. & BUSCHINGER, A. 1986: Genetically mediated queen TRONTTI, K., ARON, S. & SUNDSTRÖM, L. 2006: The genetic popu- polymorphism and caste determination in the slave-making ant, lation structure of the ant Plagiolepis xene – implications for Harpagoxenus sublaevis (Hymenoptera: Formicidae). – Ento- genetic vulnerability of obligate social parasites. – Conserva- mologia Generalis 11: 125-137. tion Genetics 7: 241-250. WOOD, T.G. & SANDS, W.A. 1978: The role of termites in eco- TSCHINKEL, W.D. 1991: Insect sociometry, a field in search of systems. In: BRIAN, M.V. (Ed.): Production ecology of ants and data. – Insectes Sociaux 38: 77-82. termites. – Cambridge University Press, Cambridge, London, TSUNEOKA, S. 2007: Host colony usurpation by the queen of the New York, Melbourne, pp. 245-292. Japanese pirate ant, Polyergus samurai (Hymenoptera: Formi- XIA, Y. & ZHENG, Z. 1995: A new record genus and a new spe- cidae). – Biological Journal of the Linnean Society 91: 565-572. cies of Formicidae (Hymenoptera) from China. – Entomotaxo- WARD, P.S. 1996: A new workerless social parasite in the ant nomia 17: 219-221. genus Pseudomyrmex (Hymenoptera: Formicidae), with a dis- ZAMORA-MUÑOZ, C., RUANO, F., ERRARD, C., LENOIR, A., HE- cussion of the origin of social parasitism in ants. – Systematic FETZ, A. & TINAUT, A. 2003: Coevolution in the slave-parasite Entomology 21: 253-263. system Proformica longiseta-Rossomyrmex minuchae (Hyme- WASMANN, E. 1891: Die zusammengesetzten Nester und ge- noptera: Formicidae). – Sociobiology 42: 1-19. mischten Kolonien der Ameisen. Ein Beitrag zur Biologie,

235