Summary. The larvae of mutillid wasps are parasitoids ofinsect host stages which are not actively feeding and are en-closed in some sort of package (cell, cocoon, puparium). Theliterature dealing with mutillids living in association witheusocial insects is surveyed and evaluated, and some newhost records are provided. Relatively few mutillid species areinvolved despite the potential for prolific reproduction onsocial hosts. The problems faced by such parasitoids aregreater than those encountered when using solitary hosts.Several species of mutillids parasitise social halictine bees, afew parasitise bumble bees and a few occasionally attackhoney bees; a few are parasitoids of commensals or symbiontsof ants. Their possible occurrence in the nests of other eu-social insects is briefly discussed.
The first description of the biology of a mutillid wasp was byChrist (1791). He kept bumble bees and sometimes foundseveral specimens of Mutilla europaea Linnaeus inside thenests. Because the bumble bees and the mutillids neverattacked each other, Christ assumed that they merely sharethe same nests. Christ’s observations were ignored for morethan 50 years, when Dahlbom (1847) and Drewsen (1847)confirmed that M. europaea lived in the nests of some Bom-bus species, but, independently of each other, they found thatthe mutillids were parasitic.
Most mutillids are solitary parasitoids of solitary hosts.Ionicus (1836) presumed that mutillids are parasites of otherbees or wasps because he saw them entering or near the nestsof various sphecids, andrenids and vespids, but the first hardrecord from a solitary host is by Sichel and Radoszkowski(1869). Recently it has been estimated that the hosts of onlyabout 2–3% of the described mutillid species are known, andfor some subfamilies there are no records at all (Brothers,1989; Quicke, 1997: 282). The mutillid larvae are alwaysectoparasitoids of host stages which are enclosed in somesort of package (cell, cocoon, puparium, ootheca) and whichare not actively feeding (Brothers, 1972, 1989). Besides oneknown case of cleptoparasitism (Krombein and Norden,1996), hyperparasitism sometimes occurs in agreement withthis rule. The known host spectrum (Mickel, 1928; Brothers,1989) spans mainly sphecid wasps and bees (Apoidea), withsome Vespoidea and a few species of the orders Diptera (firstrecorded by Eminson, 1915), Coleoptera (Péringuey, 1898),Lepidoptera (Seyrig, 1936) and Blattodea (Mickel, 1974).Invrea (1950) and Bürgis (1991) described mutillids fromDiptera species parasitic on isopods (Crustacea). An ambi-guous record which apparently indicates parasitism of adiapausing adult pentatomid (Hemiptera) (Mellor, 1933)doubtless represents hyperparasitism through a tachinid fly(Brothers, 1972). Mutillids obtained from cockroach oothe-cae would also fit the rule but may represent hyperparasitismthrough an evaniid (Hymenoptera). In rare cases more thanone mutillid larva develops on a single host individual(Brothers, 1984). Most mutillids have been found to be steno-phagous, but this may reflect our poor knowledge since a fewhave been recorded from several disparate hosts (Brothers,1989). Misidentifications have also confused the issue.
Problems encountered by any female mutillid mainlyinvolve finding suitable host individuals and penetratingtheir enclosures for egg laying. Solitary hosts are generally
Associations of mutillid wasps (Hymenoptera, Mutillidae) with eusocial insects
D.J. Brothers1, G. Tschuch2,* and F. Burger 3
1 University of Natal Pietermaritzburg, School of Botany and Zoology, Private Bag X01, Scottsville, 3209 South Africa, e-mail: [email protected] Martin-Luther-Universität, Institut für Zoologie, Abteilung Entwicklungsbiologie, Domplatz 4, D-06099 Halle, Germany,
Received 23 March 2000; revised 2 June 2000; accepted 22 June 2000.
* Author for correspondence.
scattered and often concealed. Mutillids apparently useodour signals (kairomones) while actively running in suitablelocations for finding such hosts, and must spend much timesearching, with little prospect of finding numerous hosts.Social hosts potentially provide many host individuals in asingle location, but have the considerable disadvantage that amutillid must contend with and overcome active host indivi-duals protecting the vulnerable stages before being able tolay eggs. Female mutillids are generally very heavily sclerot-ized and so able to withstand attack by hosts, and it is thus notsurprising that several species use social hosts, although thenumber of mutillid species involved is small when comparedwith the number in the family as a whole. Eusocial species,those where there is an overlap of adult generations, co-operative brood care and division of labour, often with dif-ferent castes (Wilson, 1971: 4–5; Michener, 1974: 38, 46),obviously provide the greatest potential for large numbers ofsuitable host individuals in a single nest, hence the emphasison them in this review, but it must be recognised that semi-social and even communal species could also provide similaradvantages and pose similar problems for mutillids.
Eusocial insects occur in the orders Isoptera (all species),Hemiptera (a few aphids), Thysanoptera (a few species) andHymenoptera (many species). Of these, only the Hymen-optera contain species (various ants, wasps and bees) whichcould qualify as mutillid hosts in accordance with Brothers’rule (above). This review deals with the relevant literature onmutillids associated with such hosts and includes some newfindings. The main aims are to correct the confusion in somepublications, and to encourage more investigations on thistopic. The higher classification of the Hymenoptera used isthat recommended by Brothers (1999) and Melo (1999), andwith reference to Roig-Alsina and Michener (1993); thegeneric classification of the bees follows that of Michener(2000) and the nomenclature for mutillids is from varioussources but particularly Lelej (1985).
Mutillids associated with ants
All ants (Vespoidea: Formicidae) are highly eusocial, andseveral species of mutillid have been found in ant nests, butthere are only guesses that they may parasitize formicidsdirectly. There are no observations of their actual activitieswithin the nests nor of how they enter. Lynch Arribálzaga(1878) mentioned an association of Ephuta infantilis (Bur-meister) with small ants. Wasmann (1925: 85) wrote in afootnote that he had received some specimens of an undeter-mined mutillid from Mexico caught by A. Dampf in the nestsof a Pheidole species and which was possibly regularly myr-mecophilous. Weber (1934) described the female of Myr-mosa (Myrmosa) unicolor Say (as M. dakotensis Weber) andmentioned that it crawled up on his hand as he was diggingup a colony of the ant, Myrmica scabrinoides lobicornis varfracticornis Emery, leading to the suggestion that this speciesof Myrmosa may parasitize Myrmica and other ants. Collinsand Markin (1971) reported on a female of a species ofTimulla which was collected from the mound of the ant
Solenopsis saevissima richteri Forel but considered this achance association. Brothers (1994) described the genusPonerotilla (4 species), females of which were found in thenests of Brachyponera lutea (Mayr) in Australia, and post-ulated that they and possibly Rhopalomutillinae are para-sitoids of ants (Brothers, 1989).
In some instances mutillids have been found mimickingants. André (1903) reported that Turner had collected Ephuto-morpha meranoploides André only with the ant Meranoplushirsutus Mayr which it mimicked, and suggested that thismight also represent a host-parasite relationship. Because ofthe great resemblance, Wheeler (1983) assumed that themutillid Pappognatha myrmiciformis (Cameron) is a para-sitoid of Camponotus sericeiventris (Guerin) ants. But this is probably only a case of Müllerian mimicry since Yanega(1994) found bees of the genus Euglossa (Apidae, Apinae) ashosts of P. myrmiciformis. Females of the Australian mutillidEphutomorpha pulchella (Smith) are very similar in size and coloration to the common meat ants (species of theIridomyrmex purpureus group) and have been collected inthe same areas, sometimes even running together (Brothers,pers. obs.).
In all other reports of associations with ants, the mutillidswere found to parasitize the enclosed larvae or pupae ofspecies of Coleoptera (Chrysomelidae: Cryptocephalinae (in-cluding Clytrini; Lawrence and Britton, 1991)) living in theant nests and probably feeding on vegetable matter there.Donisthorpe (1927: 61) found that the larvae of Clytra quadri-punctata (Linnaeus) in nests of Formica rufa Linnaeus fedpartly on vegetable refuse in the nest, but also on the drop-pings and pellets of the ants. McAtee (1932: 96) stated,however, that the larvae of Clytrini feed on the eggs of theants. Schöller (1998) found a clytrine to be both phytosapro-phagous and zoosaprophagous, and a cryptocephaline to bephytosaprophagous only. Further study on additional speciesis evidently needed.
As far as Clytrini are concerned, Rosenhauer (1852,1856: 372) obtained a pupa of “Clytra” (probably Lachnaiatristigma (Lacordaire)), from Malaga (Spain) from which amutillid wasp hatched. He named it Mutilla clythrae Rosen-hauer, but André (1899-1902) synonymised it with Steno-mutilla argentata var. bifasciata Klug. The correct name isprobably Stenomutilla argentata (Villers) but it may actuallybe Stenomutilla collaris (Fabricius), these two similar spe-cies both occurring in Malaga (Petersen, 1988; Nonveiller,1994); examination of Rosenhauer’s specimen, if it stillexists, is necessary. Péringuey (1898) described Mutillathyone (correctly Smicromyrme thyone (Péringuey): Invrea,1950) from specimens reared by H. Brauns from the cocoonsof a clytrine found in the nest of Crematogaster peringueyiEmery in South Africa. Brauns (1964: 126–127) stated thatSmicromyrme montana (Panzer) f. nigrita (Giraud) (correct-ly Physetopoda halensis (Fabricius), black form: Lelej, 1985;Petersen, 1988) was ectoparasitic on mature larvae and pupaeof Clytra quadripunctata in their cocoons in the nests ofFormica rufa and Formica exsecta Nylander in Europe.Petersen (1988) independently confirmed the host relation-ship, based on 3 males identified as Smicromyrme halensis
202 D.J. Brothers et al. Associations of mutillid wasps with social insects
(correctly Physetopoda halensis: Lelej, 1985) which hadbeen reared on 2 separate occasions from Clytra quadripunc-tata: one specimen with partially red mesosoma from a nestof Formica sanguinea Latreille (Germany) and 2 with blackmesosoma (Switzerland). Barbier (1976) obtained Smi-cromyrme punctata (Latreille) (correctly Physetopoda punc-tata: Lelej, 1985) from a cocoon of an Algerian species ofTituboea from a nest of Messor barbara (Linnaeus).
The occurrence of Cryptocephalus (Cryptocephalini)species as hosts of mutillids in association with ants has beenreported only once, by Giner Marí (1944) who obtained asingle male of Smicromyrme rufipes (Fabricius) from anunidentified species of Cryptocephalus. Lelej (1985) listed 9hosts for S. rufipes, all aculeate Hymenoptera (Pompilidaeand Sphecidae s.l.), so this identification must be viewedwith caution; it is possible that a species of Physetopodawas actually involved since even Giner Marí himself notedthat males of P. halensis (as Smicromyrme montana) and S. rufipes are very similar.
While more than 20 species of the tribe Clytrini (Clytra,Coscinoptera, Gynandrophthalma (Smaragdina), Hockingia,Labidostomis, Lachnaia, Macrolenes, Megalostomis (Pygidio-carina), Saxinis, Tituboea) are well documented as commen-sals in the nests of more than 30 ant species of the generaCamponotus, Cataglyphis, Formica, Lasius, Plagiolepis (allFormicinae), Aphaenogaster, Atta, Crematogaster, Messor,Tetramorium (all Myrmicinae), and Tapinoma (Dolicho-derinae) (reviews in Erber, 1988, and Jolivet, 1991; addi-tional references not included in the reviews: Letzner, 1850;Kellner, 1873: 159; Wasmann, 1894: 159–160; Donisthorpe,1902; Rapp, 1934: 324–325; Essig, 1958; Hocking, 1970;Moldenke, 1970, and pers. comm.; Seifert, 1996: 88–90;Schöller, 1998), the occurrence of cryptocephaline species inant nests has only been described for a few species and seemsnot to be the rule (Jolivet, 1988). The first such reference isby Wasmann (1894: 159) who merely stated that, accordingto a letter from Weise, most species of Cryptocephalus ap-parently pupate inside ant nests. To date, 8 cryptocephalinespecies (genera Cadmus, Coenobius, Cryptocephalus, Isnusand Pachybrachys) have been recorded as living symbioti-cally with ants (genera Formica, Lasius and Crematogaster)(reviews in Erber, 1988, and Jolivet, 1991; additional referen-ces: Rapp, 1934: 336; Schöller, 1993, 1995, 1998). Thus it isnot surprising that there are more host records of mutillidsparasitizing Clytrini than Cryptocephalini in ant nests.
Mutillids associated with eusocial wasps
The family Vespidae (Vespoidea) is a large and diverse taxon,with many eusocial members in three of the six subfamilies(Stenogastrinae, Polistinae and Vespinae) (Carpenter, 1991).These generally construct multi-celled nests, often of paper,which are well protected against intruders by the wasps them-selves. There are nevertheless a few records of mutillids asassociates of eusocial vespids, but only of species of Polistes(Polistinae: Polistini). In Europe, De-Stefani Perez (1882)found several females of Ronisia brutia (Petagna) and
Tropidotilla litoralis (Petagna) headfirst in the cells ofPolistes (Polistes) biglumis (Linnaeus) and/or P. (P.) gallicus(Linnaeus) with only the tips of their abdomens protruding;they resisted extraction but the author had no explanation fortheir activities. Invrea (1964) suggested that the mutillidswere feeding on the Polistes larvae since other authors have observed female mutillids using food of animal origin.Females of Mutilla europaea were also found in a nest of P. gallicus by Beljavsky (1935) but he provided no furtherinformation. In Georgia, North America, Fattig (1943) re-corded a female of Dasymutilla castor (Blake) (as Dasymu-tilla mediatoria Mickel) as having emerged from a nest ofPolistes (Aphanilopterus) fuscatus (Fabricius) which hadbeen kept in the laboratory for a month. Fattig also commen-ted that he had observed other females of the same speciesrunning on branches of trees containing Polistes nests. Thisis the only record clearly showing a probable parasitic asso-ciation between a mutillid and a eusocial wasp, but it is probably erroneous. There have been extensive studies ofmany eusocial wasps in various parts of the world (includingextensive collecting and rearing of several Polistes species in Georgia over more than 10 years recently (James P. Pitts,pers. comm.)) without finding any mutillid parasitoids.
The other major group of wasps (the “sphecids”) com-prises the families Heterogynaidae, Ampulicidae, Sphecidae(s. s.) and Crabronidae (Apoidea). Despite the large numberof species in this group, eusociality has been found orstrongly suspected only in the small genera Microstigmus andArpactophilus (both Crabronidae: Pemphredonini: Spilome-nina) (Ross and Carpenter, 1991). These make small nests ofsilk and other materials. There are no records of mutillidsassociated with them.
Mutillids associated with eusocial bees
Halictines
Halictine bees (Apoidea: Apidae: Halictinae: Halictini) forma very large group with species ranging from being entirelysolitary to eusocial during all or part of their nesting cycles(Michener, 1974). They generally nest in the ground, makingramifying burrows with cells at the tips of short lateralbranches. Often there is a guard worker at the entrance to thenest and any intruding mutillid has to penetrate past theguard, often after a fight. Once inside, the mutillid seems tobecome accepted and is no longer harassed, like the situationwith bumble bees (see below), thus being able to search outand lay eggs in many cells of the host (Brothers, 1972).Because of the lack of detailed information on the biology of many, or even most, halictine species, identifying thosewhich are definitely eusocial or not is difficult. For the pur-poses of this paper, a species has been included (see Appen-dix 1) if there has been at least a presumption of eusocialityin the literature, but it should be recognised that the problemsfaced by mutillids when entering eusocial nests are oftensimilar to those faced when dealing with communal or semi-social hosts, so that the distinction is somewhat artificial.
Insectes soc. Vol. 47, 2000 Review article 203
It is possible that other species for which there are records ofmutillid associates but for which there is no clear informationon their social status may turn out to be eusocial; conversely,some papers incidentally mentioning mutillids as associatesof eusocial halictines may have been missed, so the list inAppendix 1 must be considered a first approximation. Mostmutillids associated with eusocial (and other) halictines aremembers of the Pseudomethocina (New World) and theMyrmillinae (Old World). The females of both groups tend tohave broad heads with long mandibles which may be partic-ularly effective when interacting with guard bees.
The most complete accounts of the biology of mutillids inhalictine nests are those of Brothers (1972, 1978) dealingwith Pseudomethoca frigida and Myrmosula parvula onLasioglossum zephyrum, but most species of mutillids andhosts appear to behave in very similar ways to judge fromother accounts also, and may be generalized as follows(mainly based on Brothers (1972) for P. frigida). Adultfemale mutillids patrol nesting areas and are generally unsuc-cessful in entering guarded nests of the hosts, often beingattacked by the bees and driven off. Neither guard bees normutillids are usually harmed. Once inside a nest a mutillidinitially penetrates as deeply as possible and is generallyunmolested by the bees; it may thus remain in the nest for along time, laying eggs in many cells. The mutillid exploresthe nest searching for completed cells and may consume oneor more host pupae or prepupae as food in addition to lappingup liquid from pollen-nectar balls in the cells. Prior to ovi-position, the mutillid locates and removes the plug to a cell,investigates the contents of the cell, and lays an egg anywherein the cell if the host is in a suitable stage of development,having consumed all of the provisions or defecated (becomea prepupa) or pupated recently. The host individual may beparalysed, particularly if it is a pupa. The cell is reclosed bythe mutillid. The egg hatches after about 4 days and the larvahas 5 instars, feeding externally and eventually consumingthe entire host individual. About 4 days after hatching, co-coon spinning starts and defecation occurs soon after com-pletion of the cocoon. If there is no diapause, the moult to the pupa occurs about 3 days after defecation and the pupalstage lasts about 12 days in the male and 14 days in the fe-male. After the moult to the adult, it remains in the cocoon for about one day, hardening and developing its full colour,after which it chews through the cocoon and cell plug, andleaves the host nest. Mating may occur immediately afterleaving the nest and females generally become unattractive tomales soon after mating. Overwintering is as prepupae in the host cells.
Knerer’s (1973) account of myrmillines associated withL. malachurum in Europe differs in a few respects. Thereadult female mutillids overwinter in concealed places andmore than one female may cooperate in fighting with a guardbee. If unable to overcome a guard, the mutillid digs a newtunnel adjacent to the nest entrance thus bypassing the guard.Guard bees are often killed, and are removed from the burrow.After this the female mutillid itself guards the entrance forseveral days. The entrance may then be closed by the mutil-lid, using soil particles. Later in the season mutillids general-
ly avoid nests containing large numbers of bees. The bees innests which are penetrated often block the burrow with soilfrom below as the mutillid digs down, sometimes to adistance of more than 500 mm, to the depth of the broodcells. Female mutillids apparently find host nests usingsmell, even when the nests have been closed by the singleestablishing bee early in the season.
Allodapines
The allodapine bees (Apoidea: Apidae: Apinae: Xylocopini:Allodapina) are unusual in that they do not have cell parti-tions in the nests, all immatures living in the same cavity andbeing tended by the workers in the social species, and the pupae not being enclosed in cocoons (Michener, 1974).Some species are primitively eusocial but there are norecords of mutillids being associated with them. This is notsurprising since they do not conform to Brothers’ rule, nostages being enclosed.
Bumble bees
Bumble bees (Apoidea: Apidae: Apinae: Apini: Bombina)are primitively eusocial and generally nest in or on the ground(Michener, 1974). The only known mutillid parasitoids inbumble-bee nests in the Old World (about 20 species of Bombus in several subgenera, see Appendix 2) are the veryclosely related Mutilla europaea Linnaeus, Mutilla saltensisRadoszkowski, Mutilla mikado Cameron (these three taxahave often been regarded as synonymous or at most sub-specifically distinct, but are considered good species by Lelej(1985)) and, very rarely, the similar Mutilla marginata Baerwhich may have been confused with M. europaea in the olderliterature. All are members of the subtribe Mutillina (Mutil-linae, Mutillini). Bischoff (1923: 42.88–42.89) stated thatM. marginata (as M. differens 1) was a bumble-bee parasitebut gave no host records clearly attributable to it and did notmention it in his later books and papers (e.g. Bischoff, 1927:410–411). Sichel (in Sichel and Radoszkowski, 1869:148)recorded both sexes of Smicromyrme rufipes (Fabricius) ashaving been reared from a nest of Bombus hypnorum (Lin-naeus) (as B. apricus Fabricius) by Drewsen, and gave circum-stantial evidence for an association between S. rufipes andBombus lapidarius (Linnaeus); nobody else has found anyassociation between S. rufipes and bumble bees, so it is like-ly that this was an error. S. rufipes has been found to para-sitize only pompilid and sphecid hosts (Lelej, 1985).
204 D.J. Brothers et al. Associations of mutillid wasps with social insects
1 At least three species have been confused under the name differens;that name has sometimes been used for Mutilla marginata, but also forRonisia barbara var. ghilianii (Spinola) (see André, 1899–1902), andGiraud’s (1863) record of M. differens as a parasitoid of Ammophilaheydeni Dahlbom is generally accepted (e.g., Giner Marí, 1944;Invrea, 1964) as involving Dasylabris maura (Linnaeus).
The best description of the behaviour of females of M.europaea inside bumble-bee nests is from Hoffer (1886).Confirming Christ (1791), he mentioned that struggles be-tween bumble bees and mutillids are rare, but if a struggletakes place it always ends up with the death of the bumblebee. The only obstacle for the mutillid is to enter the nest andpass the guard bee. In contrast to some other enemies, aftersuccessfully entering the nest and hiding between the cells, amutillid can later move freely in the nest. This observationwas confirmed by Jordan (1935) for bumble bees but not forhoney bees. Hoffer’s guesses about the egg-laying behaviourand the development of the mutillid larva as endoparasitic inyoung bumble-bee larvae are doubtfully correct and shouldbe treated with caution since he did not observe actual egglaying but deduced that larvae hatched in 3 days from theeggs and then developed inside the bumble-bee larvae andalso pupated together with them (he could never perceive anexternal distinction between healthy larvae and those thatwere ‘occupied’ by Mutilla). Obviously accurate observa-tions by Hoffer (1886) are that the mutillid larva spins acocoon inside of the bumble-bee cocoon and that the dura-tion from pupation to adult emergence is 6 days longer thanthat of the bumble bees (10 to 14 days). He recorded up to 51(40 females, 11 males) mutillids from a single bumble-beenest taken from nature, and in all cases more females thanmales emerged. Jordan (1935) also always obtained morefemales than males and found a total of 30 days for the developmental time from egg to imago. Sometimes moremutillids than bumble bees emerged. Drewsen (1847), underartificial conditions, obtained 76 (52 females, 24 males)mutillids from a bumble-bee nest of more than 100 pupae, but only 2 specimens of the host. Eisuke Katayama (1973, inlitt. to DJB) stated that the most important enemy of bumblebees in Japan is M. mikado, and that “many colonies ofbumble bees are collapsed before their maturation by thismutillid”.
There is only one record of Mutillidae parasitizingbumble bees in the New World. In Georgia, U.S.A., Fattig(1943) claimed to have reared 2 females and one male ofDasymutilla occidentalis (Linnaeus) from a nest containing26 cocoons of Bombus (Fraternobombus) fraternus Smithafter a female mutillid had been observed entering the nest.Despite considerable work on the biology of New-Worldbumble bees, no other records of mutillid associations exist.Furthermore, Manley (1986) suggested that Sphex ichneu-moneus (Linnaeus) was a likely host of D. occidentalis, and Byers (1991), Charles D. Michener (pers. comm.) andDoug Yanega (pers. comm.) suggested Sphecius speciosus(Drury) as a probable host, Yanega having observed femalemutillids entering the burrows of the latter. Eric Eaton (pers. comm.) recorded specimens of D. occidentalis and of the host being reared from cocoons of Stictia carolina(Fabricius) collected in Mississippi in 1988, and Seiler reared D. occidentalis from the cocoons of Sphex dorsalisin Florida in 1974 (Justin O. Schmidt, pers. comm.). These“sphecid” species have very different nesting habits frombumble bees, casting doubt on Fattig’s observations whichthus require confirmation.
True honey bees
The true honey bees (Apoidea: Apidae: Apinae: Apini:Apina: Apis) comprise the 7 modern species of the genusApis (Engel, 1999). They form large colonies nesting in theopen or in cavities and are best known from the widespreadspecies, Apis mellifera Linnaeus, which is kept in hives. Inthe last half of the 19th and the first half of the 20th centuries,Mutilla europaea and “Mutilla differens”(generally consider-ed to be Mutilla marginata in this context) 2 were well knownas pests on A. mellifera in Europe (Alfonsus, 1930; De Jong,1978). Beekeepers, especially from mountainous regions ofCentral Europe, reported losses in their bee colonies: Schön-feld (1878) from Lower Austria, Scholz (1879) from theSudeten, Arnhart (1923, 1929) from Carinthia, Storch (1932:148-149) and Knötig (1934) from Bohemia, and Schwein-ster-Telfs (in Beljavsky, 1935) from the Tirol. For NorthAmerica, Bryant (1870) reported from Clarksville (Texas)that females of Dasymutilla occidentalis (Linnaeus) (asMutilla coccinea Fabricius) forced their way into beehivesand killed the bees. Cook (1899) pointed out that D. occiden-talis would be one of the greatest pests for beekeepers inIllinois and Texas and McAtee (1932:97) included mutillidsin a list of “serious insect enemies of honey bees”. Thereasons for such invasions are unclear; perhaps the mutillidsare searching for food or liquids.
Jordan (1935) gave a detailed account of the interactionsbetween Mutilla europaea females and honey bees, andreared specimens of M. europaea from a honeycomb. Afterseveral attacks on a mutillid, ending with the deaths of somebees in 7 to 21 minutes, most of the bees avoided approach-ing the mutillid. Although Jordan never observed egg-layingbehaviour, he found eggs in two cells with bee larvae that had finished feeding. In one case he observed a bee larvaspinning a cocoon while the mutillid egg stayed stuck to it.The cells containing mutillid eggs were never capped by the bee workers, and the unparasitized cells nearby were capped after a delay. Ten days after cocooning of the bee larva Jordan found a well developed mutillid pupa in its own cocoon within the bee cocoon. The total devel-opmental time from egg laying to emergence of the adultmutillid was 27 to 29 days, similar to the findings on bumble bees. It is possible that mutillids may hatch out in numbers large enough to cause the losses sometimesdescribed in the literature. The reason for changing host frombumble bees to honey bees is unknown, although Jordan(1935) ascribed it to a shortage of bumble bees that year.Likewise there is no good explanation for the fact that thisbehaviour is not recorded in the literature of the second half of the 20th century, although it may be related to changesin cultural practices, including hive design (but none of the above papers gave information on the types of hivesinvolved). There are no records of mutillids associated withany of the other species of Apis.
Insectes soc. Vol. 47, 2000 Review article 205
2 See footnote 1.
Stingless honey bees
The stingless honey bees (Apoidea: Apidae: Apinae: Apini:Meliponina) are very closely related to true honey bees andare also highly eusocial (Michener, 1974), usually nesting inthe soil or in tree trunks in the tropics. There are no recordsof mutillids associated with any of them.
Discussion
The larvae of mutillid wasps are claimed to be parasitoids of host stages which are enclosed in some sort of “hard”package and which are not actively feeding (Brothers, 1972,1989). This rule also applies to mutillids parasitic on eusocialinsects, including Mutilla europaea larvae that feed on pre-imaginal stages of bumble bees living in cells. Furtherobservations are necessary to clarify if the bumble-bee pupaeare consumed from the outside, as for all other mutillids forwhich such observations have been made, or if the Mutillalarvae are really endoparasitoids as asserted by Hoffer(1886). In ant associations, the well known occurrences of mutillids always involve parasitoidism of chrysomelidbeetles living in the ant nests and having hard cases. It isunknown whether other species of mutillids parasitize antsdirectly. Associations with termites are not known so far, and are unlikely to occur directly because that would violateBrothers’ rule, but they could occur via the parasitoidism ofcommensals, mutualists or parasitoids, especially becauseclytrines also occur in termite nests (Jolivet, 1952).
The sex ratio in mutillids also needs investigation. It isnot clear if the sex ratio observed in single host nests (onlyrecorded in any detail for bumble bees) is the true generalratio. Because of the haplo-diploid sex determination me-chanism of Hymenoptera, it is conceivable that there may be obligatory heteronomous heterotrophy in which the twosexes develop on entirely different hosts. Also possible is afacultative size-dependent sex allocation, with female andmale eggs being laid on hosts of different sizes (Brothers,1989; Matthews, 1998). This is unlikely in the case of thebumble-bee parasitoids, however, since the two sexes ofthose mutillids are very similar in size.
Halictine bees have been extensively used in studies in-vestigating the origins of eusociality because the groupincludes such diversity (Michener, 1974), but such studieshave been hampered by a lack of information on phylogene-tic relationships, and it has often been assumed that eusocial-ity has arisen separately on many occasions. Recently, how-ever, studies of the genus Halictus Latreille have shown thateusociality is plesiomorphic for the genus (Danforth et al.,1999), although eusociality seems to have arisen separatelyand repeatedly in the genus Lasioglossum Curtis (Danforth,1999). Although further light on the relationships of the beesmay conceivably be obtained from studies of the relation-ships of their associates, including mutillids, this is unlikelysince the mutillids seem not to be strongly host specific butrather more situation specific, as shown above and byBrothers (1989). Further data are needed.
Increased parasitic pressure has been suggested as play-ing a role in the evolution of social behaviour in halictinebees that are hosts of mutillids (Michener, 1958; Lin, 1964).However, Mutilla europaea and other mutillid species, in-cluding at least some of those attacking halictines, havedeveloped mechanisms to live inside the nests of eusocialinsects like nestmates. It is unknown how this operates and itdeserves further study.
Acknowledgements
Parts of this study were financially supported by the Deutsche For-schungsgemeinschaft grant number Ts 53/1-1 and Ts 53/1-2 (to GT) and the University of Natal Research Committee (to DJB). Pilar de la Rúa (University Halle) translated the Spanish references, TinoSchölz (University Halle) translated the Japanese reference, and JochenThamm (Library of the Academy Leopoldina, Halle) helped to findsome of the old papers. Eric Eaton (Forsyth, Missouri, U.S.A.), BertHölldobler (University of Würzburg, Germany), Charles Michener(University of Kansas, U.S.A.), Ray Miller (University of Natal),Ryoichi Miyanaga (Shimane University, Japan), Andy Moldenke(Oregon State University, U.S.A.), Laurence Packer (York University,Canada), James Pitts (University of Georgia, U.S.A.), Miriam Richards(Brock University, Canada), Justin Schmidt (Tucson, Arizona, U.S.A.)and Doug Yanega (University of California, Riverside, U.S.A.) assistedconsiderably with valuable advice, information and specimens. Theirassistance is much appreciated.
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Appendix 1
Species of Mutillidae associated with halictine bees; records generally accepted only if mutillids were reared from cells, were found in nests or wereobserved attempting to enter nests of the host (especially if fighting between mutillids and guards was recorded); names of species used in the litera-ture, if different from the currently accepted names, indicated in parentheses.
Lasioglossum (Evylaeus) nigripes (Lepeletier) (= Halictus nylanderi Perez) (De-Stefani, 1886: found in galleries; mutillid unidentified but very probably this species from description provided, compared with descriptions by Invrea (1964) and Suárez (1988))
Myrmosula parvula (Fox) (= Myrmosa (Myrmosula) parvula) (U.S.A.):Augochlorella persimilis (Viereck) (Ordway, 1964: seen crawling into nests)Augochlorella striata (Provancher) (Ordway, 1964: seen crawling into nests)Lasioglossum (Dialictus) imitatum (Smith) (= L. inconspicuum (Smith)) (Michener and Wille, 1961: reared)Lasioglossum (Dialictus) zephyrum (Smith) (Batra, 1965: females observed forcing their way into nests; Brothers, 1972: reared; Brothers, 1978:
reared)
Paramyrmosa brunnipes (Lepeletier) (= Myrmosa brunnipes) (Europe):Lasioglossum (Evylaeus) malachurum (Kirby) (Knerer, 1973: association stated as having been observed)Lasioglossum (Evylaeus) pauxillum (Schenk) (= Halictus pauxillus) (Minkiewicz, 1935: mutillid observed penetrating nest)
Halictus (Halictus) farinosus Smith (Nye, 1980: mutillid immatures found on bee larvae)
Paramutilla halicta Mickel (Costa Rica):Augochlorella edentata Michener (Eickwort and Eickwort, 1973: reared; Mickel, 1973: reared) (this species may be semisocial or eusocial
Augochlorella persimilis (Viereck) (Ordway, 1964: found in many nests)Augochlorella striata (Provancher) (Ordway, 1964: found in many nests)
Pseudomethoca frigida (Smith) (= Mutilla canadensis Blake, = Pseudomethoca canadensis, = P. f. frigida) (U.S.A. and Canada):Augochlorella striata (Provancher) (Michener and Wille, 1961: found in nests)Lasioglossum (Dialictus) imitatum (Smith) (= L. (Chloralictus) inconspicuum (Smith)) (Michener and Wille, 1961: found in nests; Brothers, 1972:
reared from cells probably of this species)Lasioglossum (Dialictus) laevissimum (Smith) (Brothers, 1972: found in burrows)Lasioglossum (Dialictus) rohweri (Ellis) (Michener and Wille, 1961: found in nests; Breed, 1975: mutillid pupae found in cells)Lasioglossum (Dialictus) versatum (Robertson) (Michener and Wille, 1961: found in nests; Michener, 1966: reared)Lasioglossum (Dialictus) zephyrum (Smith) (= Halictus (Chloralictus) zephyrus) (Melander and Brues, 1903: female mutillid fighting with bees
(misidentified as Halictus (Chloralictus) pruinosus Robertson, see Brothers, 1972, Krombein, 1992) when trying to enter nest; Krombein, 1938:female mutillid attacked by female bee and attempted to enter nest; Michener and Wille, 1961: found in nests; Lin, 1964: female mutillids attackedby bees when attempting to enter nests, sometimes entered nest; Batra, 1965: reared; Brothers, 1972: reared; Krombein, 1992: female mutillidfighting with bee at nest entrance)Lasioglossum (Evylaeus) cinctipes (Provancher) (Knerer and Atwood, 1967: reared)Lasioglossum (Dialictus) sp. (= Halictus (Chloralictus) sp.) (Rau, 1934: mutillid near nest entrance attacked by bee)
Pseudomethoca hesperus Brothers (Panama):Halictus (Seladonia) hesperus Smith (Brothers, 1982: female mutillids common in nesting area and repeatedly attempting to enter nests; Brooks
and Roubik, 1983: female mutillids attacked by bees when repeatedly attempting to enter nests, sometimes entered nests)
Pseudomethoca sp. (Costa Rica):Augochlora (Oxystoglossella) nominata Michener (This paper: specimen found in nest by G.C. and K. Eickwort, seen by DJB in Cornell Univer-
sity collection)
Myrmillinae
Blakeius bipunctata (Latreille) (= Myrmilla bipunctata, = Bisigilla bipunctata) (Europe, North Africa):Lasioglossum (Evylaeus) malachurum (Kirby) (= Halictus malachurus) (Ferton, 1898: females observed entering open and closed nests; Knerer,
1973: reared)Lasioglossum (Evylaeus) nigripes (Lepeletier) (Knerer and Plateaux-Quénu, 1970: females observed entering nests “to oviposit on larvae
or pupae”)Halictus (Halictus) cochlearitarsis Dours (Knerer, 1973: association stated as having been observed)Halictus (Halictus) resurgens Nurse (= Halictus holtzi Schulz) (Knerer, 1973: association stated as having been observed)Halictus (Halictus) fulvipes Klug (Knerer, 1973: association stated as having been observed)Lasioglossum (Evylaeus) glabriusculum (Morawitz) (Knerer, 1973: association stated as having been observed)
Myrmilla (Myrmilla) calva (Villers) (Europe):Lasioglossum (Evylaeus) malachurum (Kirby) (Knerer, 1973: association stated as having been observed)Lasioglossum (Dialictus) morio (Fabricius) (Knerer, 1973: association stated as having been observed)
Myrmilla (Myrmilla) erythrocephala (Latreille) (Europe):Halictus (Halictus) sexcinctus (Fabricius) (This paper: several mutillid specimens found in bee nests at Daimonia, Greece by M. Richards,
pers. com.)
Myrmilla (Pseudomutilla) capitata (Lucas) (= Mutilla capitata) (Europe, North Africa):Halictus (Halictus) scabiosae Rossi (De-Stefani, 1886: found in galleries)Lasioglossum (Evylaeus) malachurum (Kirby) (= Halictus malachurus) (Ferton, 1898: females observed entering closed nests and being attacked
by female bees; Knerer, 1973: reared, specimens have bimodal size distribution corresponding to that of host)Lasioglossum (Evylaeus) nigripes (Lepeletier) (= Halictus nylanderi Perez) (De-Stefani, 1886: found in galleries)
Sigilla dorsata (Fabricius) (= Myrmilla dorsata) (Europe):Lasioglossum (Evylaeus) malachurum (Kirby) (Knerer, 1973: association stated as having been observed)Lasioglossum (Evylaeus) nigripes (Lepeletier) (Knerer and Plateaux-Quénu, 1970: females observed entering nests “to oviposit on larvae
or pupae”)
Mutillinae, Mutillini, Smicromyrmina
Mickelomyrme hageni (Zavattari) (Japan):Lasioglossum (Evylaeus) subtropicum Sakagami, Miyanaga and Maeta (This paper: many mutillid specimens found in area where only this bee
nested by R. Miyanaga, pers. com.)
Smicromyrme rufipes (Fabricius) (= Mutilla (Smicromyrme) rufipes) (Europe):“Halictus” spp. (may not be eusocial) (Adlerz, 1906: found in cells; Forsius, 1927: [females] observed seeking entry into nest holes, none
reared; Aerts, 1950: females observed crawling into the nests) (records doubtful since Lelej (1985) recorded only pompilid and sphecid hosts, see above)
210 D.J. Brothers et al. Associations of mutillid wasps with social insects
Appendix 2
Bumble-bee hosts of Mutillidae; regarded as such if mutillids were actually reared from host cocoons or were found in the nests; in parentheses, nameused in source of record if different, and reference.
Meidell, 1934);B. (Th.) pascuorum or B. (Th.) muscorum (Bombus muscorum Fabricius: Christ, 1791; Sichel and Radoszkowski, 1869;
Smith, 1876 (according to Schmiedeknecht, 1907: 39, in the nineteenth century the name B. muscorum was sometimes used for B. agrorum Fabricius = B. pascuorum));
