1066 Florida Entomologist 95(4) December 2012

First record of an encyrtid wasp (: Chalcidoidea) as a True PRIMARY of (Hymenoptera: Formicidae)

Gabriela Pérez-Lachaud1, John Noyes2 and Jean-Paul Lachaud1,3* 1El Colegio de la Frontera Sur, Avenida Centenario Km 5.5, Chetumal 77014, Quintana Roo, México

2Natural History Museum, Department of Entomology, Cromwell Road, South Kensington, London SW7 5BD, UK

3Centre de Recherches sur la Cognition Animale, CNRS-UMR 5169, Université de Toulouse UPS, 118 route de Narbonne, 31062 Toulouse Cedex 09, France

*Corresponding author; E-mail: [email protected]; [email protected]

Abstract

Numerous cases of associations of encyrtid wasps with ants have already been reported. In the majority of these cases, however, wasps are associated only indirectly with ants (in- terference associations) through primary parasitism of the trophobionts (Coccoidea), which are exploited and protected by ants. Suspected direct parasitism cases are unusual and no direct attack of encyrtids on ants has ever been demonstrated. Here we provide both a revised list of all known cases of associations between encyrtid wasps and ants, and a report of the first record of a true primary encyrtid parasitoid of ants. Of two colonies of the arboreal ponerine , Pachycondyla goeldii (Forel), examined from French Guiana, one had 3 pupae parasitized by males and females of a gregarious, minute encyrtid wasp species, identified asBlanchardiscus pollux Noyes, and 2 other cocoons presented evidence of pararasitism. This first host record for the genusBlanchardiscus , which has always been placed near other genera that parasitize scale-, supports a hypothesis of a shift from a myrmecophilous host to an ant host. Our findings increase to 9 the number of families known to attack ants as primary hosts. A closer examination of other arboreal ants, particularly those involved in ant-garden building and nest weaving, will certainly yield new ant-parasitoid associations.

Key Words: primary parasitism, ant association, arboreal ants, ponerines, encyrtid wasps, Blanchardiscus

Resumen

Numerosos casos de asociaciones con hormigas han sido reportados para avispas de la fami- lia con anterioridad. Sin embargo, en la mayoría de estos casos, las asociaciones son indirectas (interferencia), a través del parasitismo primario de insectos trofobiontes (Coccoidea) que las hormigas explotan y protegen. Los casos de parasitismo directo sospe- chados son raros y ningún ataque directo por encírtidos sobre hormigas ha sido demostrado hasta la fecha. Aquí compilamos todos los casos conocidos de asociaciones entre avispas de la familia Encyrtidae y hormigas, y reportamos el primer registro de verdadero parasitismo primario de hormigas para esta familia. De dos colonias de la hormiga ponerina arbórea Pachycondyla goeldii (Forel) de Guyana Francesa que se examinaron, una tenía 3 pupas parasitadas por machos y hembras de un diminuto Encyrtidae gregario, identificado como Blanchardiscus pollux Noyes, y 2 pupas más presentaban señales de pararasitismo. Este primer registro de hospedero conocido para el género Blanchardiscus, el cual siempre ha sido considerado cercano a otros géneros de encírtidos parasitando escamas, tiende a apoyar la hipótesis de una deriva progresiva del parasitismo desde los mirmecófilos hacia las hor- migas. Este reporte permite incrementar a 9 el número de familias de avispas parasitoides conocidas por parasitar a hormigas. Es muy probable que el examen cuidadoso de otras especies de hormigas arbóreas, en particular aquellas involucradas en las construcción de jardínes de hormiga o de nidos tejidos, lleve a la detección de nuevas asociaciones entre hormigas y parasitoides.

Palabras Clave: parasitismo primario, asociación con hormigas, hormigas arbóreas, poneri- nas, encírtidos, Blanchardiscus pérez-Lachaud et al.: First Encyrtid Wasp as a True Primary Parasitoid of Ants 1067

Records of associations with ants involving hy- any ectoparasitoid. In particular, we looked for menopteran wasp include more than wasp remains (exuvia) within empty ant cocoons 500 wasp species, but only a fraction unambigu- denoting previous parasitoid emergence and for ously pertains to true parasitoids (Lachaud & the presence of scars upon ant larvae resulting Pérez-Lachaud 2012). Parasitoid wasps known from unsuccessful attacks of eucharitid first in- to attack adult ants or their brood belong to 8 star larvae. During June 2011, preserved mate- families: Diapriidae (Diaprioidea); Chalcididae, rial was revised again: all of the cocoons were Eucharitidae, Eulophidae, Eurytomidae and dissected under a stereomicroscope and ant pu- Perilampidae (Chalcidoidea); Braconidae and pae were this time thoroughly checked for the Ichneumonidae (Ichneumonoidea) (Wilson 1971; presence of both ecto- and endoparasitoids or for Kistner 1982; Hölldobler & Wilson 1990; Schmid- any evidence of parasitism. We discovered some Hempel 1998; Lachaud & Pérez-Lachaud 2012). encyrtids, some of these were slide-mounted and The Eucharitidae sensu stricto is the only group identified by direct comparison with type mate- whose known hosts are exclusively larval ants rial of the relevant species. Voucher specimens (Heraty 2002). were deposited in the Natural History Museum, Here we describe the first known case of true London, England and in the collection primary parasitism of a species of ant by an en- of El Colegio de la Frontera Sur-Chetumal, Quin- cyrtid wasp (Chalcidoidea: Encyrtidae). Our tana Roo, Mexico. results are based on ant specimens collected in 2002 in the course of investigations on the eucha- Results ritid fauna associated with formicids in French Guiana. An exhaustive recent review of all the The first nest collected was composed of 1 material preserved in alcohol, focusing on eucha- queen, 77 workers, 4 pupae, 2 larvae, and sev- ritid wasps associated with poneromorph ants eral eggs. The second nest contained no queen, (Lachaud et al. 2012), fortuitously allowed us to 5 alate females, 208 workers, 67 pupae (of which detect new examples of hymenopteran parasit- 16 large pupae, presumably winged sexuals), and oids of ants, other than eucharitids. Moreover, a neither larvae nor eggs. Initial cursory inspection survey of the literature over the last 100 years of the brood, in 2002, showed no signs of external allowed us to list both all the recorded cases of as- attack. sociations between encyrtid wasps and ants and During the later examination, in 2011, it was the exact nature of their known relationships. noted that the color of the gaster of some ant pu- pae looked slightly different and, in one instance, Materials and Methods very small dark points were visible through the cuticle. In this last case, dissection showed the Two nests of the arboreal ant-garden species, presence of already pigmented developing indi- Pachycondyla goeldii (Forel) (Formicidae: Poneri- viduals of a gregarious, very minute (body length nae), were collected on 12 Nov 2002 in French < 1 mm) endoparasitoid wasp. Five ant pupae Guiana, at Km 13 along the road leading to the from nest no. 2 were found to be parasitized. One Hydroelectric complex at Petit Saut, Sinnamary worker pupa contained 15 almost fully developed (N 05° 07’ 25.3” W 52° 57’ 16.7”). Pachycondyla and pigmented adult wasps (8 females, 7 males). goeldii is a monogynous, polydomous ponerine A second worker pupa contained 11 wasp pupae species (Denis et al. 2006) that colonizes pioneer (at that developmental stage sex could not be de- vegetal formations where plants are character- termined, see Fig. 1), and a female (queen) pupa ized by a rapid, continuous growth and a high contained 4 white wasp larvae-prepupae. Two production of leaves and soft wood (Corbara & De- other queen pupae had a hole in their gaster, from jean 1996; Dejean et al. 2000b). Founding queens which parasitoids had previously emerged (Fig. and first generation workers initiate their own 1). ant garden by building a cardboard-like structure The wasp was identified asBlanchardiscus into which epiphyte seeds are integrated. Follow- pollux Noyes (Chalcidoidea: Encyrtidae: Encyrti- ing the growth of the epiphyte, the colony estab- nae). Only 2 species of the genus Blanchardiscus lishes its nest within the root system (Corbara de Santis are currently known: B. scutellaris De & Dejean 1996; Orivel et al. 1998). Ant gardens Santis and B. pollux. Blanchardiscus scutellaris were transported to the laboratory, and their con- was described from a female collected with sweep tent preserved in alcohol for later examination. net upon vegetation in Tucuman, Argentina (De The presence and number of ant dealate fe- Santis 1964), and has been reported from Brazil males, alate females, males, workers, cocoons, (Noyes 1980), whereas B. pollux is known from and larvae, as well as the presence of any adult both the male and the female and was collected myrmecophile (especially eucharitid parasitoids), from Costa Rica and Belize (Noyes 2004). The were recorded. At first, the contents of cocoons biology of both species was heretofore unknown preserved in alcohol were superficially exam- and no host data were available for any of the two ined while backlit to check for the presence of species. 1068 Florida Entomologist 95(4) December 2012

Fig. 1. Cocoon of a Pachycondyla goeldii queen with a single emergence hole (white arrow) chewed by the encyr- tid parasitoids in the apical, ventral portion of the ant gaster. A Blanchardiscus pollux pupa (black arrow) is also shown for comparison.

According to our observations, B. pollux is a Discussion gregarious endoparasitoid of P. goeldii pupae. Wasp larvae pupate inside the ant host pupae, Encyrtid wasps are widespread and common which are protected by a cocoon. Developing throughout the world. The family currently in- wasps were found in the dorsal anterior portion cludes more than 480 genera and 4500 species of the gaster of the ant host, near the petiole. and is one of the most important chalcidoid fami- They were grouped in a compact mass, and for lies for biological control of pests (Noyes & the 15 nearly adult specimens whose sexual Hayat 1994; Noyes 2000, 2012; Trjapitzin 2008). gender could be assessed, the wings were some- Though a few species are egg predators (e.g. in what distorted. Only a small portion of the ant’s Microterys), most encyrtids are endoparasit- gaster was occupied by the parasitoids: B. pol- oids of insects and arachnids, including other lux adults measure less than 1 mm, whereas hymenopteran parasitoids. About half of all en- P. goeldii workers measure 9-12 mm. At emer- cyrtids whose host is known are parasitic upon gence, adult wasps chew a hole (1 mm in diam), Coccoidea (Noyes 2012). Two subfamilies are rec- in the host cuticle and through the host cocoon. ognized: the Tetracneminae with 111 genera and A single emergence hole was observed in the 848 species, and the Encyrtinae with 370 genera apical, ventral portion of the gaster, near the and 3700 species (Trjapitzin 1973a, 1973b; Noyes meconium (Fig. 1), in the 2 queen pupae from 2012). which wasps had already emerged. Both worker Numerous encyrtids have been recorded as- and queen pupae of P. goeldii were parasitized sociated with ants belonging to 3 subfamilies and both male and female wasps emerged from (Dolichoderinae, Formicinae, and ). the same host. It is unknown whether more than However, almost all these records referred to in- a single generation occurs inside the ant nest direct associations with ants (i.e. interference, see or whether adults leave the host nest to mate Table 1) through primary parasitism of the tro- and disperse, but the latter seems more likely phobionts that ants tend (e.g. Bartlett 1961; Cud- because both males and females were collected joe et al. 1993; Hübner & Völkl 1996; González- outside ant nests (Noyes 2004). However, even Hernández et al. 1999; Barzman & Daane 2001; if no free adult wasp was found within both P. Mgocheki & Addison 2009). These associations goeldii nests, they might have passed unnoticed are more numerous in Encyrtinae, with 27 spe- when nests were collected. cies from 17 genera involved in 45 associations pérez-Lachaud et al.: First Encyrtid Wasp as a True Primary Parasitoid of Ants 1069 R eferences . rjapitzin 1978 Daane et al. 2007 Zappalá et al. 2007 I tioka & noue 1996a, 1996b Krull & Basedow 2005 Guerrieri & N oyes 2002 S ugonyaev 1996a this work T M artinez-Ferrer et al. 2003 James et al. 1999 M artinez-Ferrer et al. 2003 Flanders 1945 M artinez-Ferrer et al. 2003 S ugonyaev 1998 S ugonyaev 1998 S ugonyaev 1998 S ugonyaev 1999 L iere & P erfecto 2008 Bartlett 1961*, Barzman & Daane 2001 Barzman & Daane 2001 James et al. 1999 Bartlett 1961, Barzman & Daane 2001 association

the

of

nature

R elationship rue parasitoid I nterference I nterference I nterference I nterference Found in the nest Found in shelters T I nterference I nterference I nterference I nterference I nterference I nterference Found in the nest Found in shelters Found in shelters Found in the nest I nterference I nterference I nterference I nterference I nterference and , hosts

p rimary

their

of

and P rimary host , Pseudococcus viburni ( S ignoret) Phyllocnistis citrella S tainton Ceroplastes rubens M askell Ceroplastes rubens M askell Myzolecanium sp. A clerdid species Pachycondyla goeldii (Forel) Xanthogramma sp. Aonidiella aurantii ( M askell) Aonidiella aurantii ( M askell) and L . Aonidiella aurantii ( M askell) Aonidiella citrina C oquillet Aonidiella aurantii ( M askell) formicarii (Green) Coccus and Coccus hesperidum L . Coccus formicarii (Green) formicarii (Green) Coccus and Coccus hesperidum L . Megalocryptes bambusicola (Green) Azya orbigera M ulsant ( O livier) Saissetia oleae ( O livier) Aonidiella aurantii ( M askell) and Coccus hesperidum L . Saissetia oleae ( O livier) associates

ants

their

of , ants

with

A nt associate sp. [D] Tapinoma Linepithema humile ( M ayr) [D] Solenopsis invicta Buren [ M ] Lasius japonicus S antschi (= L. niger ( L .)) [F] Camponotus sp. [F] sp. [ M ] Pachycondyla goeldii (Forel) [ P ] Iridomyrmex rufoniger spp. [D] ( L owne) gr. Linepithema humile ( M ayr) [D] Linepithema humile ( M ayr) [D] Solenopsis xyloni M c C ook [ M ] Crematogaster sp. [ M ] Linepithema humile ( M ayr) (= Iridomyrmex humilis ) [D] Lasius niger ( L innaeus) [F] Formica aerata (Francoeur) [F] dohrni M ayr Crematogaster [ M ] dohrni M ayr Crematogaster [ M ] Crematogaster sp. [ M ] S mith) Azteca instabilis (F. [D] Linepithema humile ( M ayr) [D] Linepithema humile ( M ayr) [D] Iridomyrmex rufoniger spp. [D] ( L owne) gr. associated

be

to

known

asumatsu Y p s was

encyrtid

riapitsyn of

ist 1. L * R eferred to as M. lounsburyi [D] Dolichoderinae; [F] Formicinae; [ M ] yrmicinae; P onerinae. able rjapitzin & T T E ncyrtid wasp species Encyrtinae Acerophagus flavidulus (Brèthes) (= Pseudaphycus flavidulus ) Ageniaspis citricola L ogvinovskaya beneficus I shii & Arketypon vaderi Guerrieri & N oyes Astymachus phainae S ugonjaev Blanchardiscus pollux N oyes Bothriothorax intermedius C laridge bifasciata Howard Encyrtus ingae S ugonjaev Encyrtus ludmilae S ugonjaev Homalotylus shuvakhinae T anneckei Guerrieri & N oyes Metaphycus hageni Daane & C altagirone Metaphycus helvolus ( C ompere) 1070 Florida Entomologist 95(4) December 2012 . association

R eferences the

of

James et al. 1999 Barzman & Daane 2001 Bartlett 1961 S ugonyaev 1996b Bartlett 1961 Bartlett 1961 Bartlett 1961 S ugonyaev 1996b S ugonyaev 1996b C hantos 2007 Dejean et al. 2000a Dejean et al. 2000a Gibernau & Dejean 2001 Gibernau & Dejean 2001 N ovak 1994 N ovak 1994 N ovak 1994 C udjoe et al. 1993 C udjoe et al. 1993 C udjoe et al. 1993 nature

and , hosts

R elationship I nterference I nterference I nterference Found in shelters I nterference I nterference I nterference Found in the nest Found in the nest I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference p rimary

their

of

and , associates

P rimary host ants

Aonidiella aurantii ( M askell) and Coccus hesperidum L . Saissetia oleae ( O livier) Coccus hesperidum L innaeus undet. C occidae Saissetia oleae ( O livier) Coccus hesperidum L . Saissetia oleae ( O livier), Coc - cus hesperidum L . tessellatus ( S i - Eucalymnatus gnoret) tessellatus ( S i - Eucalymnatus gnoret) ( M askell) Euphyonarthex phyllostoma S chmidt Euphyonarthex phyllostoma S chmidt Caternaultiella rugosa S chouteden Caternaultiella rugosa S chouteden Cacopsylla crataegi ( S chrank), C. pyrisuga (Förster) Cacopsylla crataegi ( S chrank) Cacopsylla crataegi ( S chrank) Anagyrus lopezi (De Santis) Anagyrus lopezi (De Santis) Anagyrus lopezi (De Santis) their

of , ants

with

associated

be A nt associate

to

Linepithema humile ( M ayr) [D] Linepithema humile ( M ayr) (= Iridomyrmex humilis ) [D] Dolichoderus sp. [D] Camponotus brutus Forel [F] Camponotus brutus Forel [F] opaciventris E m - Myrmicaria ery [ M ] Lasius niger ( L innaeus) [F] Camponotus flavomargin atus M ayr [F] luctans Forel Crematogaster or C. kneri M ayr [ ] Iridomyrmex rufoniger spp. [D] ( L owne) gr. Crematogaster sp. [ M ] Linepithema humile ( M ayr) (= Iridomyrmex humilis ) [D] Linepithema humile ( M ayr) (= Iridomyrmex humilis ) [D] thoracicus (F. Dolichoderus S mith) (= D. bituberculatus M ayr) [D] Solenopsis invicta Buren [ M ] Camponotus acvapimensis M ayr [F] Formica pratensis R etzius [F] Lasius niger ( L innaeus) [F] Camponotus acvapimensis M ayr [F] Linepithema humile ( M ayr) (= Iridomyrmex humilis ) [D] known

p s was

encyrtid

of

imberlake) ist ) L ontinued 1. ( C [D] Dolichoderinae; [F] Formicinae; [ M ] yrmicinae; P onerinae. able T E ncyrtid wasp species Metaphycus lounsburyi (Howard) Metaphycus luteolus ( T Metaphycus monastyrskii S ugonjaev Metaphycus stanleyi C ompere Microterys nietneri ( M otschulsky) (= Microterys flavus Howard) Microterys roseni S ugonjaev Neodusmetia sangwani ( S ubba R ao) sp. Prionomitus mitratus (Dalman) Prionomitus tiliaris (Dalman) Prochiloneurus pulchellus S ilvestri insolitus ( A lam)) (= P. pérez-Lachaud et al.: First Encyrtid Wasp as a True Primary Parasitoid of Ants 1071 . A ddison 2009 A ddison 2009 A ddison 2009 association

R eferences the

ollerup 2007 of

C udjoe et al. 1993 Hübner & Völkl 1996 Hübner & Völkl 1996 2010 Veen S anders & Van N oyes & R en 1995 N oyes & R en 1995 N oyes 2000 N oyes 2000 N echols & S eibert 1985 González-Hernández et al. 1999 C udjoe et al. 1993 C udjoe et al. 1993 C udjoe et al. 1993 C udjoe et al. 1993 C ampos et al. 2006 T M gocheki & M gocheki & M gocheki & nature

and , hosts

R elationship I nterference I nterference I nterference I nterference I nterference Found in the nest Found in the nest Found in the nest I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference I nterference p rimary

- - - their

of

and , associates

P rimary host ants

Anagyrus lopezi (De Santis) M ar ( cardui Lysiphlebus shall) M ar ( cardui Lysiphlebus shall) ( M ar fabarum Lysiphlebus shall) Cataenococcus sp. neobre - Pseudococcus sp. nr. vipes Beardsley Dysmicoccus brevipes ( C ock - erell) Dysmicoccus brevipes ( C ock - erell) Nipaecoccus vastator ( M askell) Dysmicoccus brevipes ( C ock - erell) Phenacoccus manihoti M atile-Ferrero Phenacoccus manihoti M atile-Ferrero Phenacoccus manihoti M atile-Ferrero Phenacoccus manihoti M atile-Ferrero Planococcus citri ( R isso) Planococcus ficus ( S ignoret) Planococcus ficus ( S ignoret) Planococcus ficus ( S ignoret) Planococcus ficus ( S ignoret) their

of , ants

with

associated

be A nt associate

to

Pheidole megacephala (Fa - bricius) [ M ] Myrmica rubra ( L innaeus) (= M. laevinodis ) [ M ] Crematogaster curvispinosa M ayr [ ] Crematogaster sp. [ M ] Paratrechina sp. [F] Camponotus flavomargin - atus M ayr [F] luctans Forel Crematogaster or C. kneri M ayr [ ] Pheidole megacephala (Fa - bricius) [ M ] Formica perpilosa W heeler [F] Lasius niger ( L innaeus) [F] Lasius niger ( L innaeus) [F] xanthochroa ( R oger) Azteca [D] Pheidole megacephala (Fa - bricius) [ M ] Camponotus acvapimensis M ayr [F] L. (= niger ( L innaeus) Lasius niger ( L atreille) [F] Anoplolepis steingroeveri (Forel) [F] Technomyrmex albipes F.Technomyrmex S mith [D] Crematogaster peringueyi E mery [ M ] Linepithema humile ( M ayr) [D] known p s was

A. brasil - A. encyrtid

alker) of

ist ) L S hafee, A lam & A garwal) ontinued 1. ( C [D] Dolichoderinae; [F] Formicinae; [ M ] yrmicinae; P onerinae. able T E ncyrtid wasp species aphidivorus ( M ayr) (= Aphidencyrtus aphidivorus ) Syrphophagus mamitus ( W Tetracneminae (= (Brues) tachigaliae Aenasius iensis M ercet) Anagyrus agraensis S araswat (= A. indicus Anagyrus ananatis Gahan Anagyrus lopezi (De S antis) (as Epidinocarsis lopezi ) Anagyrus pseudococci (Girault) Anagyrus sp. near pseudococci 1072 Florida Entomologist 95(4) December 2012 . A ddison 2009 A ddison 2009 A ddison 2009 rjapitzin 1979 association

R eferences the

of

Gordh & T Dahms & Gordh 1997 M gocheki & M gocheki & M gocheki & W heeler 1907, P eck 1963 M ann 1914 C ampos et al. 2006 Daane et al 2007 R oepke 1919 Bartlett 1961 Bartlett 1961 nature

and , hosts

R elationship I nterference I nterference I nterference I nterference I nterference S ymphilic S ymphilic I nterference I nterference P horesis I nterference I nterference p rimary

their

of

and , associates

P rimary host ants

? ? Planococcus ficus ( S ignoret) Planococcus ficus ( S ignoret) Planococcus ficus ( S ignoret) ? ? Planococcus citri ( R isso) Pseudococcus viburni ( S igno - ret) thoracicus (F. Dolichoderus S mith) (= D. bituberculatus M ayr) Pseudococcus gahani Green Pseudococcus gahani Green their

of , ants

with

associated

be A nt associate

to

P. king i) [ M ] instabili s, = P. P. Pheidole ceres W heeler (= tepaneca ) Pheidole ceres var. [ M ] Ochetellus glaber ( M ayr) (= Iridomyrmex glaber ) [D] Iridomyrmex rufoniger do - mesticus Forel (= I. domes - tica ) [D] Pheidole tepicana P ergande (= L. (= niger ( L innaeus) Lasius niger ( L atreille) [F] Linepithema humile ( M ayr) [D] thoracicus (F. Dolichoderus S mith) (= D. bituberculatus M ayr) [D] Linepithema humile ( M ayr) (= Iridomyrmex humilis ) [D] Anoplolepis steingroeveri (Forel) [F] Crematogaster peringueyi E mery [ M ] Linepithema humile ( M ayr) [D] Linepithema humile ( M ayr) (= Iridomyrmex humilis ) [D] known

p s was

rjapitzin) encyrtid

of

imberlake) ist alker) ) L imberlake)) ontinued 1. ( C [D] Dolichoderinae; [F] Formicinae; [ M ] yrmicinae; P onerinae. able T E ncyrtid wasp species Ananusia australis (Gordh & T (= Myrmencyrtus australis ) Ananusia longiscapus (Girault) Coccidoxenoides perminutus Girault (= C. perminutus ( T Holcencyrtus wheeleri ( A shmead) (= Pheidoloxenus wheeler i) Leptomastix dactylopii Howard Leptomastix epona ( W prodeniae A shmead Taftia peregrina ( C ompere) Tetracnemoidea peregrinus ) (= Tetracnemus brevicornis (Girault) (= Tetracnemoidea pretiosus T Tetracnemus pérez-Lachaud et al.: First Encyrtid Wasp as a True Primary Parasitoid of Ants 1073 with ants, than in Tetracneminae, with 15 species (Kuwana), D. brevipes (Cockerell), Planococcus from 8 genera involved in 27 associations. Howev- citri (Risso), Pseudococcus gahani (Green), Sac- er, such a difference in the number of reported as- charicoccus sacchari (Cockerell), see Noyes & sociations likely reflects species richness within Hayat 1994; Noyes 2012) that are often associat- each subfamily, because there are more encyrtine ed with ants, and therefore association with ants than tetracmine species. might be fortuitous. Nevertheless, in the case Various encyrtid species reported in interfer- of H. wheeleri, considering that it seems to be a ence association with ants (Table 1) have a very regular myrmecophile in P. tepicana nests, that wide primary host range, and some are even hy- adults present subapterism, and that ant hosts perparasitoids: e.g. Prionomitus mitratus is para- are not associated with Aphididae or sitic on a fairly wide range of psyllids, Prochilo- (Wheeler 1907), such an association is unlikely to neurus pulchellus is a hyperparasitoid of many be only circumstancial; however, a primary para- species of , and Syrphophagus aphidi- sitic relationship was never proved and the wasp vorus is a hyperparasitoid of virtually any developmental stages remained unknown. There- that feeds on grasses or herbaceous vegetation. fore, our record of B. pollux from French Guiana Likewise, in numerous genera (Aenasius, Anagy- reared from pupae of the neotropical ant P. goeldii rus, Anicetus, Coccidoxenoides, Comperiella, Lep- constitutes both the first record of primary para- tomastix, Ooencyrtus, Prochiloneurus, Syrphoph- sitism of ants for the Encyrtidae and the first case agus, see Table 1), the indirect association with associating an encyrtid species with a ponerine the ant is not specific and can even involve species ant. Our finding increases to 9 the number of from different ant subfamilies. However, in some parasitic wasp families that attack ants. As hy- genera, e.g. Ananusia, Encyrtus, Holcencyrtus, pothesized by Huggert and Masner (1983) and Metaphycus, Microterys, Prionomitus, and Tetr- Hanson et al. (1995), a possible evolutionary path acnemoidea (Table 1), more specific interferences to the parasitism of ants by hymenopterous para- with ants—at species or, at least, at subfamily sitoids could have been through the occurence of level—can occur and could suggest some level of a shift from the initial primary host—an ant sym- selection of the ant associates by the parasitoids. biont—to the ant host through a gradual process A few cases of assumed direct associations in- of association and integration with the ant hosts. volving encyrtids and ants have been reported Such a hypothesis seems plausible for numerous (Table 1), but true primary parasitism has never families (Lachaud and Pérez-Lachaud 2012), and been demonstrated before. An unidentified spe- a supporting example has recently been proposed cies of encyrtid was recorded from a refuse heap among eulophids for 2 Horismenus species asso- of Eciton burchellii (Westwood) (Rettenmeyer et ciated with the weaver ant Camponotus sp. near al. 2011), but direct interaction with this ant host textor (Hansson et al. 2011). Phylogenetically, has not been observed and the encyrtid may have Blanchardiscus is very probably near genera that only been a prey. The 2 females of Taftia prodeniae include species known to parasitize scale-insects. Ashmead found by Roepke (1919) clanging to the Our record of B. pollux parasitizing ants may also antennae of Dolichoderus thoracicus (Fr. Smith) support this hypothesis. (referred to as D. bituberculatus Mayr) may have Little is known about the diversity of parasit- been phoretic rather than parasitic. Only Holcen- oids of ants in general, though knowledge on this cyrtus wheeleri (Ashmead) (referred to as Pheido- topic has significantly increased in the last two loxenus wheeleri), found in nests of the myrmicine decades (Lachaud & Pérez-Lachaud 2012). Like- ants Pheidole tepicana Pergande (referred to as wise, the hosts of most parasitic hymenopteran P. instabilis) (Wheeler 1907) and P. ceres Wheeler species already described are still unknown, (referred to as P. ceres var. tepaneca Wheeler) especially those of rare or rarely collected spe- (Mann 1914), seems to have symphilic relation- cies. Several recent reports (Hansson et al. 2011; ships with its hosts and has been suspected of be- Lachaud et al. 2012; Lachaud & Pérez-Lachaud ing “probably also entoparasitic on these ants or 2012; Gates & Pérez-Lachaud 2012) have called their progeny during its larval stages” (Wheeler attention to the diversity of parasitoids that at- 1910). Wheeler (1907) stated that this “exquisite tack ants, particularly in the case of arboreal ant little Chalcidid . . . runs about in the dense throng species. For example, hymenopterous myrmeco- of Pheidole workers like one of their number. It philes associated with the neotropical weaver ant is not easily detected, as it resembles the workers Camponotus sp. near textor, another arboreal ant, in its small size (1 mm) and in being subapter- include 2 species of Eucharitidae, 2 of Eulophi- ous or practically wingless”. In some occasions as dae, and 1 of Eurytomidae (Hansson et al. 2011; many as 6 or 8 H. wheeleri have been observed Gates & Pérez-Lachaud 2012; Pérez-Lachaud in a single nest of P. tepicana (Wheeler 1907). It & Lachaud, unpublished data). Those findings is worth noting that 2 related encyrtid species, and the present record of a new family of para- Holcencyrtus osborni Timberlake and H. myr- sitic wasps attacking ants inhabiting ant-gardens micoides (Compere & Zinna), have been reared strongly suggest that arboreal ant nests may con- from hosts (e.g. Dysmicoccus boninsis stitute a hot spot of diversity that has little been 1074 Florida Entomologist 95(4) December 2012

studied. As highlighted by Schmid-Hempel (1998) Dejean, A., Corbara, B., Orivel, J., Snelling, R. R., and Lachaud & Pérez-Lachaud (2012), parasitic Delabie, J. H. C., and Belin-Depoux, M. 2000b. The wasps associated with ants as the primary host importance of ant gardens in the pioneer vegetal for- are diverse, but most associations still await dis- mations of French Guiana (Hymenoptera: Formici- covery. dae). Sociobiology 35: 425-439. Denis, D., Orivel, J., Hora, R. R., Chameron, S., and Fresneau, D. 2006. First record of polydomy in a mo- Acknowledgments nogynous ponerine ant: a means to allow emigration between Pachycondyla goeldii nests. J. Insect Behav. We thank all the team of the Laboratoire Envi- 19: 279-291. ronnement at Petit Saut (HYDRECO) for both logis- Flanders, S. E. 1945. Coincident infestations of Aonidi- tic help and assistance with local accommodation. We ella citrina and Coccus hesperidum, a result of ant are also grateful to Jérôme Orivel (ECOFOG, French activity. 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