Egg predation within the nests of social wasps: a new genus and species of Phlaeothripidae, and evolutionary consequences of Thysanoptera invasive behaviour : Thrips as Predators on

Egg predation within the nests of social wasps:a new genus and species of Phlaeothripidae, andevolutionary consequences of Thysanopterainvasive behaviour

ADRIANO CAVALLERI1*, ANDRÉ R. DE SOUZA2, FÁBIO PREZOTO2 andLAURENCE A. MOUND3

1PPG-Ecologia, Departamento de Ecologia, Instituto de Biociências, Universidade Federal do RioGrande do Sul, Porto Alegre, Brazil2PPG-Ciências Biológicas-Comportamento e Biologia Animal, Universidade Federal de Juiz de Fora,Juiz de fora, Brazil3CSIRO Ecosystem Sciences, Canberra, ACT, Australia

Received 20 November 2012; revised 11 January 2013; accepted for publication 11 January 2013

The insects known as thrips are commonly thought of as flower-living and pestiferous organisms, but we reporthere a novel interaction between a phlaeothripine thrips species, Mirothrips arbiter gen. et sp. nov. and threespecies of social paper wasps in Brazil. This thrips species breeds inside the wasp colonies, and larval and adultthrips feed on wasp eggs, which become severely damaged. Infested nests can contain up to 300 M. arbiter gen. etsp. nov. individuals. The closest relatives of M. arbiter are two presumably predaceous species: Mirothripsbicolor sp. nov., which inhabits abandoned Cecidomyiidae galls, and Mirothrips analis comb. nov., describedfrom individuals collected in the silken bags of the caterpillars of Psychidae moths. The behaviour exhibited byM. arbiter represents one of the most evolutionarily advanced lifestyles known among Thysanoptera, and wepredict that other polistine species serve as hosts for this thrips in Brazil. © 2013 The Linnean Society of London,Biological Journal of the Linnean Society, 2013, 109, 332–341.

ADDITIONAL KEYWORDS: invasive behaviour – Mischocyttarus – nest symbionts – paper wasps – Polistes– Polistinae – Thysanoptera.

INTRODUCTION

Insects of the order Thysanoptera, generally calledthrips, are mainly phytophagous or mycophagous,with a few species being predatory on other smallarthropods (Mound, 2005). Although thrips typicallybreed on leaves and in flowers, or for fungal-feedingspecies on dead branches and in leaf litter, a wide-spread behavioural attribute amongst these insects ispositive thigmotaxis (Lewis, 1973). This results inadults crawling into a wide diversity of small enclosedspaces. In Europe, Limothrips cerealium (Thripidae),

a pest of cereal crops, often causes problems by enter-ing fire-alarm smoke detectors (Lewis, 1987), and thisspecies is commonly found within other enclosedspaces such as framed pictures, packaged goods, andeven jewellery. In more natural situations thrips havebeen recorded inside the nests of birds and mammals(Pelikan et al., 2002), as well as the nests of socialinsects, including ants (De Santis, 1972) and termites(Hartwig, 1967). However, there is no evidence thatsuch intrusions by thrips involve any biological func-tion other than shelter. In contrast, many Acaciaspecies in Australia bear thrips-induced galls, andsome bear domiciles comprising pairs of leaves gluedtogether by thrips of several genera (Crespi, Morris &Mound, 2004). These galls and domiciles are com-monly invaded by various specialist species of phy-

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

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tophagous thrips, either as kleptoparasites or asinquilines (Gilbert, Mound & Simpson, 2012).

Obligate predation in Thysanoptera is not particu-larly common, but it has evolved in several lineages(Mound, 2005). Such predaceous species have beenrecorded, under exposed conditions, feeding on eggs ofcoccids, whiteflies, and other thrips species, as well onthe larva and adults of minute arthropods such asmites, psocids, and aphids (Ananthakrishnan, 1969;Palmer & Mound, 1991; Masumoto et al., 2012).Recent observations in Brazil have revealed aremarkable instance of predation by thrips that alsoincludes the invasion of a relatively enclosed andpresumably protected space, within the nests of socialpaper wasps (Vespidae, Polistinae). These thripsbreed inside wasp colonies, where both the larvae andthe adults feed on wasp eggs. In this study, wesuggest that this thrips species is a symbiont of thepaper wasp colonies that is highly dependent for foodon the wasp society during all of the thrips life cycle,and we provide biological information about thisnovel and singular symbiotic interaction. This thripsspecies belongs to a previously undescribed species,and its closest relatives are two presumably preda-ceous thrips species that also invade unusual micro-habitats. One is frequently recorded inside abandonedCecidomyiidae galls, whereas the other was describedfrom individuals collected in the bags made of silkand plant material produced by psychid moths (DeSantis, 1959). A new genus of Phlaeothripidae is hereerected for these three species of thrips, including thetransfer of Karnyothrips analis (De Santis, 1959) tothis new genus.

MATERIAL AND METHODS

The thrips species studied here were collected fromseveral localities of southern and south-easternBrazil. Thrips associated with paper wasps were col-lected from active and abandoned nests of Mischocyt-tarus atramentarius, Mischocyttarus cassununga, andPolistes versicolor in different locations of the munici-pality of Juiz de Fora, Minas Gerais, from November2009 to December 2011. These Neotropical wasps areindependent founding paper wasps that live in a nestmade by a mixture of plant fibre and salivary secre-tions. Colonies of these social insects can be found allyear round (Reeve, 1991). Surrounding plants nearthe nests were also examined to detect any thrips.One thrips-infested colony of Polistes versicolor wasfilmed in the field for 8 hours using a digital camerapositioned 30 cm from the nest frontal surface. Labo-ratory observations were made in two infested colo-nies of Mischocyttarus atramentarius under astereomicroscope for 5 hours each. All behavioural

observations of wasps and thrips were made ad libi-tum (Altmann, 1974).

DEPOSITARIES AND ABBREVIATIONS

Depositaries: ANIC, Australian National Insect Col-lection, CSIRO, Canberra, Australia; ESALQ, Ento-mological Collection, Escola Superior de AgriculturaLuiz de Queiróz, Piracicaba, Brazil; MLP, Museo deCiencias Naturales de La Plata, La Plata, Argentina;UFRGS, Zoological Collection, Departamento de Zoo-logia, Universidade Federal do Rio Grande do Sul,Porto Alegre, Brazil.

Abbreviations: aa, pronotal anteroangular seta; am,pronotal anteromarginal seta; epim, pronotal epime-ral seta; ml, pronotal midlateral seta; pa, pronotalposteroangular seta; po, postocular seta.

SYSTEMATICSMIROTHRIPS GEN. NOV.

Small macropterous Phlaeothripinae, with one ormore prominent pairs of setae on prosternum. Headscarcely longer than wide, without stout cheek setae;one pair of long postocular setae; maxillary styletsmore than half of head width apart, not deeplyretracted into head, with slender maxillary bridge;mouth cone short, rounded, not extending across pros-ternal ferna. Antenna eight-segmented, III with twoor three sensoria, IV with three or four sensoria; VIIImore than 2.5 times longer than wide and constrictedat base. Pronotum transverse, with four pairs ofmajor capitate setae, am minute, aa and ml notgreatly separated; epimeral sutures complete. Pros-ternal basantra present, sometimes weak; one or twopairs of long, pointed setae anterolateral to ferna;mesopraesternum transverse, not boat-shaped. Forefemora not enlarged, tarsal tooth minute or absent.Metanotum weakly reticulate, with two pairs of finelyacute setae medially. Forewings weakly constrictedmedially, with few duplicated cilia; three long sub-basal setae present. Pelta triangular, recessed intoanterior margin of tergite II; abdominal tergites II–VII with two pairs of sigmoid wing-retaining setae,each anterior pair weaker than posterior pair; setalpair S1 on IX clearly expanded; tube about 2.0 timeslonger than basal width, anal setae longer than tube.Male sternite VIII with pore plate.

Type species: Mirothrips bicolor sp. nov.

SYSTEMATIC RELATIONSHIPS

Mirothrips belongs to the Tribe Haplothripini (Mound& Minaei, 2007), a diverse group that comprisesmore than 30 genera worldwide, with five recordedfrom the Neotropics: Apterygothrips, Haplothrips,

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Karnyothrips, Leptothrips, and Podothrips. All ofthese species have a well-developed maxillary bridgein the head, the prosternal basantra are present, andthe forewings are constricted medially (Mound &Marullo, 1996).

The genus Mirothrips seems to be related to theNeotropical species placed in Karnyothrips, in thatthey bear minute pronotal am setae, have a similarshaped mesopraesternum, and males have a poreplate on abdominal sternite VIII. However, this newgenus is distinguished by the presence of a pair ofvery long, pointed setae on the prosternum, just ante-rior to the ferna. The presence of these setae on theprosternum has not been recorded previously for anymember of the Phlaeothripidae worldwide. Mirothripsspecies are also unusual in having two pairs ofmedian setae on the metanotum, and the presence ofsuch duplicated setae on the metanotum is not knownin any other Neotropical species of the Haplothripslineage. The long and basally constricted antennalsegment VIII in Mirothrips species contrasts with theNeotropical Karnyothrips species, in which thissegment is short and usually conical, and broadlyjoined to segment VII (Mound & Marullo, 1996).

The number of antennal sensoria varies widelywithin and among species of Haplothripini, from oneto three on segment III, and from three to four onsegment IV. This variation among individuals of thesame species has been noted by Okajima (2006) andalso by Goldarazena, Mound & zur Strassen (2008).Although a reduction in the sensoria on both seg-ments has occurred several times in this group, theplesiomorphic condition is possibly three on segmen-t III and four on segment IV (Mound & Minaei,2007). The number of sensoria on segment III seemsto be stable within each species of Mirothrips, butthe number on segment IV varies from two to fourin M. analis, with four being the most frequentnumber. A similar problem arises with the form ofthe prosternal basantra, as these are weak in M. ar-biter and also in some specimens of M. analis, andthis might reflect a progressive loss of this scleritewithin the genus. Such homoplastic and variablecharacters must be evaluated carefully when consid-ering phylogenetic relationships (Mound & Minaei,2007).

KEY TO MIROTHRIPS SPECIES

1. Body bicoloured (Fig. 9), abdominal segments I–VIII yellow, segments IX–X dark brown; legsyellow, also antennal segments III–V (Fig. 11)bicolor sp. nov.

–. Body brown, including abdomen, mid andhind femora and tibiae, and antennalsegments III–V (Figs 2, 17) 2

2. Forewing pale, without median dark line (Fig. 6);major setae on head, pronotum, and tergites unu-sually stout and parallel sided, considerablythicker medially than the stoutest pair of tergalsigmoid setae (Fig. 3); male sternite VIII withsmall, fragmented pore plate (Fig. 8)arbiter sp. nov.

–. Forewing pale with distinct median dark line(Fig. 19); major setae on head, pronotum, andtergites slender, and tapering to just below capi-tate apex (Fig. 14), more slender than stoutest pairof tergal sigmoid setae; male sternite VIII withlarge pore plate (Fig. 20)analis comb. nov.

MIROTHRIPS ANALIS (DE SANTIS, 1959)COMB. NOV. (FIGS 14–21)

Adraneothrips analis De Santis, 1959: 254.Karnyothrips analis (De Santis, 1959) Mound &

Marullo, 1996: 316.The major setae of this dark-brown species are

longer and more slender than in the other twospecies, antennal segments VI–VII are longer thanin M. bicolor, but are shorter than in M. arbiter, andthe male pore plate is similar to that of M. bicolor.Although the type series of M. analis is poorlymounted, we consider the specimens studiedhere from southern Brazil as belonging to thisspecies.

Material examined: ARGENTINA, 2�, 2� para-types. BRAZIL, Paraná, Lapa, 1� in Prunus persica(M.F.S. Souza); Rio Grande do Sul, Nova Petrópolis(29°21′S, 51°05′W, 570 m a.s.l.), 2�, 1� collectedfrom dead twigs, 09.III.2011 (A. Cavalleri); PortoAlegre (30°04′S, 51°07′W, 100 m a.s.l.), 2�, 3� indead twigs, 03.III.2011 (A. Cavalleri); 1� and 1�from grasses, 14.II.2011 and 28.II.2011, (A. Cav-alleri); 1� from Calliandra selloi, 23.XII.2010(A. Cavalleri); 1� from Borreria verticilata,11.II.2011 (A. Cavalleri); 1� from Passiflora elegans,17.I.2011 (A. Cavalleri); Viamão, 1� from Caleaserrata, 22.II.2002 (S.M.J. Pinent).

MIROTHRIPS ARBITER SP. NOV.(FIGS 1–8, 22–23)

Macropterous �Body uniformly dark brown, with no internal pigmen-tation; all major setae stout but hyaline; tarsi paler,tibiae yellow at base and apex; antennalsegments I–II dark brown, segment III brown, butyellow in basal third, segments IV–VIII uniformly

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Figures 1–8. Mirothrips arbiter sp. nov.: 1, head; 2, antenna; 3, pronotum; 4, meso- and metanotum; 5, prosternum(arrows indicate prosternal setae); 6, forewing basal third; 7, pelta; 8, male sternite VIII (arrows indicate fragmented poreplate).**

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brown; forewings pale, without median dark line,clavus light brown; abdominal tube slightly paler atapex.

Head about as long as wide, vertex with weaktransverse reticulation; po setae stout, apex broadlyexpanded; maxillary stylets more than half of headwidth apart, retracted into head almost to level of posetae; antennal segments III and IV each with threesensoria, segment IV sometimes with an additional

small sensorium; segments VI–VII elongate, longerthan segment III.

Pronotum transverse, with few lines of sculpture;four pairs of long, stout, capitate setae, am setaepointed and minute; aa and ml setae close together,distance between their bases scarcely greater thanthe basal diameter; prosternal basantra weakly scle-rotized; ferna broad, almost rectangular, with twopairs of setae on anterior margin and two pairs of

Figures 9–13. Mirothrips bicolor sp. nov.: 9, dorsal view; 10, head and pronotum; 11, antenna; 12, pterothorax andpelta; 13, male sternite VIII.

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much longer setae anterolaterally. Mesonotum withtransverse reticulation at anterior and posteriorregions, lateral setae stout and capitate. Metanotumweakly reticulate, posterior median setae pair longerthan anterior median pair. Forewings with about fiveduplicated cilia. Pelta with paired campaniform sen-silla; tergites II–VI with two pairs of stout, capitatesetae, tergite VII with lateral pair long and pointed;tergite IX setae S1 broad and expanded, S2 and S3long and finely acute. Tube about 1.9 times as long asgreatest width.

MeasurementsHolotype � (mm): Length about 1700; head length175, greatest width across cheeks 165, po setae length62, eye dorsal length 67; median length of pronotum

118, width 213, am setae length 8, aa length 60, mllength 62, epim length 62, pa length 65; widthof mesonotum 170; forewing length 670; tergite IXsetae S1 length 70, S2 110, S3 95; tergite X length112, basal width 60, apical width 30; length of anten-nal segments III–VIII 48, 48, 55, 57, 52, and 41,respectively.

Macropterous � (Fig. 7)Smaller than female but similar in colour and struc-ture; sternite VIII with small and fragmented poreplate; tergite IX setae S2 shorter than S1 andpointed.

MeasurementsParatype � (mm): Length about 1370; head length157, greatest width across cheeks 140, po setae length

Figures 14–21. Mirothrips analis comb. nov.: 14, head and pronotum; 15, prosternum with weak basantra;16, prosternum with well-developed basantra; 17, pterothorax and pelta; 18, antenna; 19, forewing; 20, male sternite VIII;21, female tergites IX–X.

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42, eye dorsal length 60; median length of pronotum100, width 178, am setae length 7, aa length 42, mllength 40, epim length 47, pa length 52; widthof mesonotum 155; forewing length 560; tergite IXsetae S1 length 52, S2 40, S3 100; tergite X length98, basal width 51, apical width 28; length of anten-nal segments III–VIII 38, 38, 47, 50, 42, and 38,respectively.

Holotype �BRAZIL, Minas Gerais, Juiz de Fora (21°46′S,43°21′W, 800 m a.s.l.), from Polistes versicolor nest,12.II.2010 (A.R. de Souza), in UFRGS. Paratypes:46�, 2� collected with holotype; 28�, 9� fromMischocyttarus atramentarius nest, 10.XII.2011(A. Cavalleri).

RemarksThis species differs from the other two described herein this genus in having the major setae remarkably

stout but translucent (Fig. 3); setae of this form havenot been described in any other species of Phlae-othripidae. Mirothrips arbiter also has the prosternalbasantra much more weakly developed than in theother two species, sometimes not clearly visible, andthe fragmented pore plate on sternite VIII of males isunusual.

MIROTHRIPS BICOLOR SP. NOV. (FIGS 9–13)

Macropterous �Body sharply bicoloured; head, thorax, and abdominaltergites IX–X dark brown, remaining tergites andlegs clear yellow, except fore and median coxae darkbrown and fore tibiae light brown; antennalsegments I–II brown, segments III–V yellow, seg-ment VI shaded light brown apically, segments VII–VIII uniformly brown; forewings pale, withoutmedian dark line, clavus uniformly pale; tergite Xdark brown, slightly paler at extreme base.

Figures 22–25. Mirothrips and associated habitats: 22, Mirothrips arbiter female feeding on Mischocyttarus atra-mentarius egg; 23, Mirothrips arbiter larva feeding on Mischocyttarus atramentarius egg; 24, leaf of Guapira oppositawith an abandoned Cecidomyiidae gall (arrow); 25, bags made of silk and plant material produced by Oiketicus kirbyimoth (arrow).

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Head about 1.2 times as long as wide; po setaecapitate, not extending far beyond posterior margin ofeye; maxillary stylets wide apart, more than half ofhead width apart, retracted into head about halfwaybetween posterior margin and po setae. Antennalsegment III with two sensoria, segment IV with foursensoria; segments VI–VII subequal in length to seg-ment III, segment VIII not elongate.

Pronotum transverse, with few lines of sculpture;four pairs of slender, capitate setae, am pointed andminute; basantra present, wider than long; fernabroad, with two pairs of setae on anterior margin andtwo longer pairs anterolaterally. Mesonotum withtransverse reticulation at anterior and posterior,lateral setae capitate but slender. Metanotum sculp-ture absent medially, two pairs of pointed mediansetae, posterior pair longer. Forewings with fourduplicated cilia. Pelta triangular, with paired cam-paniform sensilla; tergites II–VI with two pairs oflong slender, capitate setae, tergite VII with lateralpair long and pointed; tergite IX setae S1 slender andcapitate, S2 and S3 long and finely acute. Tube about2.0 times as long as greatest width near base, apicalwidth about 0.5 of basal width.

MeasurementsHolotype � (mm): Length about 1240; head length 145,greatest width across cheeks 125, po setae length 27,eye dorsal length 55; median length of pronotum 83,width 162, am setae length 3, aa length 30, ml length32, epim length 42, pa length 35; width of mesonotum122; forewing length 460; tergite IX setae S1 length62, S2 95, S3 85; tergite X length 90, basal width 48,apical width 27; length of antennal segments III–VIII36, 37, 36, 35, 28, and 26, respectively.

Macropterous �Smaller than female, but similar in colour and struc-ture; basantra present, but variable in shape, usuallyabout as long as wide; sternite VIII pore plate occu-pies most of sternite area; abdominal tergite IX setaeS2 shorter than S1 and pointed.

MeasurementsParatype � (mm): Length about 1180; head length140, greatest width across cheeks 123, po setae length27, eye dorsal length 55; median length of pronotum87, width 162, am setae length 5, aa length 23, mllength 27, epim length 41, pa length 37; forewinglength 500; tergite IX setae length S1 53, S2 25, S392; tergite X setae length 82, basal width 42, apicalwidth 25; length of antennal segments III–VIII 37,37, 37, 37, 30, and 27, respectively.

Holotype �BRAZIL, Rio Grande do Sul, Porto Alegre (30°04′S,51°07′W, 100 m a.s.l.), in litter, close to dead twigs,

22.II.2011 (A. Cavalleri), in UFRGS. Paratypes: samelocality, 2� collected in dead twigs, 20.X.2010 and27.I.2011; 1� from Trema micrantha, 27.I.2011(A. Cavalleri); 2� collected in empty Cecidomyiidaegalls in Guapira opposita leaves, 30.IV.2012 and08.III.2012 (A. Goulart); Nova Petrópolis (29°21′S,51°05′W, 570 m a.s.l.), 1� collected in dead twigs,08.III.2011 (A. Cavalleri).

RemarksThis species differs from the other two members ofthis genus not only in being sharply bicoloured, butalso in having the postocular setae and antennalsegments VI–VII relatively short. The male is similarto M. analis in having the pore plate occupying mostof the eighth abdominal sternite.

LIFE HISTORY AND ECOLOGY OF MIROTHRIPS

All Thysanoptera recorded within wasp nests belongto M. arbiter, and its prevalence in paper wasp colo-nies ranged from 9% in P. versicolor to 23% in M. at-ramentarius. Adults of both sexes, eggs, larvae, andpupae or hatched eggs of thrips were found inside fiveout of 22 nests of M. atramentarius, seven out of 35nests of M. cassununga, and five out of 55 nests ofP. versicolor. Living M. arbiter were recorded only inactive colonies of wasps, and no individuals werefound in the surrounding vegetation of the studysites.

Thrips eggs were observed at the internal base ofnest cells, over the wasp larval meconium. Thenumber of M. arbiter per colony ranged greatly, from30 in M. atramentarius to 300 in P. versicolor. Weobserved both larval and adult thrips feeding activelyon paper wasp eggs (Figs 22, 23), which collapsedafter a few hours. Mirothrips arbiter adults were veryactive during laboratory observations, and were fre-quently observed walking around the nest, and enter-ing and leaving the cells. Conversely, the larvaestayed for long periods in the bottom of the cells, closeto the meconium, and only walked to feed upon theeggs. We did not observe any wasp attack againstM. arbiter. However, adult wasps displayed an alarmbehaviour in infested colonies, characterized by theopening of wings and vigorous activity on the surfaceof the nest.

Mirothrips analis was described from specimenscollected inside silk bags of Oiketicus kirbyi moths(Psychidae) (Fig. 25) in Argentina. This Neotropicallepidopteran is found in lowlands from Argentina toMexico, and also on the Caribbean Islands (Rhainds,Davis & Price, 2009); however, there was no indica-tion that immature stages of M. analis were foundwith the adults. According to Stephens (1962), eggmasses of the bagworm are frequently attacked by

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mites, and personal observations have indicated agreat abundance of psocids in abandoned bags insouthern Brazil. Thus, it is possible that M. analismight be predatory on these small arthropods. InBrazil, this thrips species has been found in lownumbers and in a wide range of habitats: dead twigs,on Passiflora elegans and grass leaves, as well as onflowers of Borreria verticilata, Calea serrata and Cal-liandra spp.

Mirothrips bicolor has always been found solitary,and usually associated with dead twigs; however, onthree occasions, solitary adults and eggs were alsofound inside the empty galls induced by Bruggmaniaelongata (Cecidomyiidae) on leaves of Guapiraopposita (Nyctaginaceae) (Fig. 24). These abandonedstructures were infested with mites, upon whichM. bicolor larvae and adults presumably feed. Simi-larly, Karnyothrips species, including Karnyothripsflavipes and Karnyothrips melaleucus, are frequentlycollected from dead branches, and these species areassumed to be predatory on other small arthropods(Palmer & Mound, 1991). Moreover, predation byCrematogaster ants upon immature lepidopteransand psocids on G. opposita leaves was observed, andthese empty galls might serve as an important shelterfor thrips against such natural enemies.

DISCUSSION

The large diversity of microhabitats in which thripscan be found is associated with their wide range offeeding habits. Although closely related, the membersof the Haplothripini lineage are diverse in theirfeeding associations. Haplothrips species usually feedand breed in flowers, including some in grass flowers,with a few on leaves, and a relatively few are speciespredaceous. In contrast, Leptothrips and Karnyo-thrips species are all predatory, and are often foundon dead branches, and Podothrips species are appar-ently predatory on coccoids living on Poaceae. Fromits systematic affinities, it is likely that Mirothripshas evolved from a predaceous ancestor. In fact, ourobservations suggest that M. analis and M. bicolorare generalist predators on small arthropods. Moreo-ver, both species exhibit a strong invasive behaviour,and are found to be solitary in a wide range ofmicrohabitats.

It is not clear how M. arbiter invaded and estab-lished within paper wasp nests, as previous records ofinteractions between thrips and social wasps involvea very different association. For instance, Polisteshabraeus has been observed feeding actively onRhipiphorothrips cruentatus (Thripidae) larvae inIndia (Dhaliwal, 1975). Conversely, we reveal herethat M. arbiter is a predator on polistine eggs, and itsentire life cycle, from egg to adult, is completed inside

the paper wasp colonies. Moreover, both adults andlarvae exhibit the same predatory behaviour insidethe nests, and the large number of thrips inside thecolonies suggests that they impose important fitnesscosts to paper wasps by killing a great number of eggs(A. Cavalleri & A. R. de Souza, pers. observ.).

Our observations suggest that M. arbiter can beconsidered paper wasp symbionts (sensu Hölldobler &Wilson, 1990), and are probably highly dependent forshelter and food on the wasp colonies. In addition, thesocial behaviour displayed by polistine hosts possiblyplays an important role in thrips infestation, provid-ing a great amount of resources for a large number ofindividuals and protection against natural enemies.Although these ideas are suggestive, we are not ableto characterize M. arbiter as a social parasitic species,and a more detailed study on the infested colonies isneeded. The only known and comparable situation ofsymbiosis between Thysanoptera and social insects isexhibited by the social parasite Akainothrips francisi(Phlaeothripidae) in Australia. This phytophagousspecies invades, and breeds within, the domiciles ofthe subsocial thrips Dunatothrips aneurae (Phlae-othripidae) on Acacia phyllodes, and similarly to thepredaceous thrips recorded here, the invader alsoexploits the social benefits of their hosts (Gilbertet al., 2012). On the other hand, A. francisi does notkill its host and no evidence of antagonistic host–inquiline interactions was observed.

Paper wasp broods are frequently attacked bymany nest predators (Nelson, 1968; Jeanne, 1979;Strassmann, 1981), which lead adult wasps to displaytypical alarm behaviour. As we found no predatorsother than thrips it is likely that adult wasps candetect M. arbiter, or at least the chemicals released bythe preyed upon eggs, as in all of the infested coloniesthe adult wasps displayed alarm behaviour. However,given the high number of thrips inside the infestednests, adult wasps were probably not capable ofremoving them from the colony. Mechanical andchemical cues are among the most frequent strategiesused by parasites and symbionts to invade wasp andant societies (Hölldobler & Wilson, 1990), and furtherbehavioural and chemical approaches will investigatethe defensive mechanisms exhibited by these thrips.Although it is not clear how these Thysanopterainvade the wasp colonies, the nest architecture shouldbe a limiting factor for thrips infestation. Interest-ingly, all hosts have vulnerable nests, characterizedby having one single uncovered comb linked to thesubstratum by a peduncle (Richards, 1978).

Independent-founding social wasps such as Polistesand Mischocyttarus species are particularly commonin South America (Richards, 1978), and it is surpris-ing that previous studies have not detected the pres-ence of M. arbiter in those nests. Similarly, given the

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widespread distribution of the wasps species attackedby thrips in Brazil, we predict that this remarkableinteraction is likely to be found in a wider area thanreported here, and perhaps other polistine speciesserve as hosts for M. arbiter.

Indeed, the exploitation of this rich, but particu-larly protected ecological niche, inside a wasp colony,represents one of the most evolutionarily advancedand rarest lifestyles known among Thysanoptera.Although few studies have recorded the presence ofthrips inside colonies of termites in Africa (seeHartwig, 1967) and Camponotus ants in SouthAmerica (De Santis, 1972), their occurrence seems tobe accidental in most cases. Nevertheless, the infor-mation presented here provides evidence that thripscan occupy a vast number of microhabitats andinvade complex ecological systems, such as colonies ofsocial insects.

ACKNOWLEDGEMENTS

We thank Bruno Barbosa and Newton José de JesusSilva for their assistance during fieldwork, and LucasKaminski for his criticism of an early version of thearticle. We are grateful to Gilberto Palma for kindlyproviding the Oiketicus kirbyi photograph and AlineGoulart for Cecidomyiidae identification. We aregrateful to María del Carmen Coscarón for the loan ofspecimens from MLP, and to the three anonymousreviewers for their helpful comments. This projectwas supported by Conselho Nacional de Desenvolvi-mento Científico e Tecnológico (N°143326/2008-2 toA.C.).

REFERENCES

Altmann J. 1974. Observational study of behavior: samplingmethods. Behaviour 49: 227–267.

Ananthakrishnan TN. 1969. Indian Thysanoptera: CSIRzoological monograph, n°1. New Delhi: Publications andInformative Directorate CSIR.

Crespi BJ, Morris DC, Mound LA. 2004. Evolution ofecological and behavioural diversity: Australian acaciathrips as model organisms. Canberra: Australian BiologicalResources Study & CSIRO Entomology.

De Santis L. 1959. Adiciones a la fauna Argentina deTisanópteros II. Acta Zoológica Lilloana 17: 87–93.

De Santis L. 1972. Descripcion preliminar de uma nuevaespécie de Heterothrips del Brasil (Thysanoptera: Heter-othripidae). Studia Entomológica 15: 431–432.

Dhaliwal JS. 1975. Polistes hebraeus (Fabricius) preyingupon Rhipiphorothrips cruentatus Hood (Thripidae, Thysa-noptera). Current Science 44: 368–368.

Gilbert JDJ, Mound LA, Simpson SJ. 2012. Biology of a

new species of socially parasitic thrips (Thysanoptera:Phlaeothripidae) inside Dunatothrips nests, with evolution-ary implications for inquilinism in thrips. BiologicalJournal of the Linnean Society 107: 112–122.

Goldarazena A, Mound LA, zur Strassen R. 2008. Nomen-clatural problems among Thysanoptera (Insecta) of CostaRica. Revista Biologia Tropical 56: 961–968.

Hartwig EK. 1967. Termitophilous Thysanoptera from SouthAfrica. Journal of the Entomological Society of South Africa29: 44–47.

Hölldobler B, Wilson EO. 1990. The ants. Cambridge:Harvard University Press.

Jeanne RL. 1979. Construction and utilization of multiplecombs in Polistes canadensis in relation to the biology of apredaceous moth. Behavioral Ecology and Sociobiology 4:293–310.

Lewis T. 1973. Thrips, their biology, ecology and economicimportance. London: Academic Press.

Lewis T. 1987. An introduction to the Thysanoptera – Asurvey of the group. Antenna 11: 92–99.

Masumoto M, Ohno S, Ganaha-Kikumura T, Miyagi A,Okajima S. 2012. Review of the genus Scolothrips (Insecta,Thysanoptera, Thripidae) from Japan. Zootaxa 3183: 36–48.

Mound LA. 2005. Thysanoptera – Diversity and Interactions.Annual Review of Entomology 50: 247–269.

Mound LA, Marullo R. 1996. The Thrips of Central andSouth America: an Introduction. Memoirs on Entomology,International 6: 1–488.

Mound LA, Minaei K. 2007. Australian insects of the Hap-lothrips lineage (Thysanoptera – Phlaeothripinae). Journalof Natural History 41: 2919–2978.

Nelson JM. 1968. Parasites and symbionts of Polistes wasps.Annals of the Entomological Society of America 61: 1528–1539.

Okajima S. 2006. The Suborder Tubulifera (Thysanoptera).The Insects of Japan 2: 1–720.

Palmer JM, Mound LA. 1991. Thysanoptera. In: Rosen D,ed. The armored scale insects, their biology, natural enemiesand control, Vol B. Amsterdam: Elsevier, 67–76.

Pelikan J, Fedor P, Krumpal M, Cyprich D. 2002. Thrips(Thysanoptera) in nests of birds and mammals in Slovakia.Ekologia (Bratislava) 21: 275–282.

Reeve HK. 1991. Polistes. In: Ross KG, Matthews RW, eds.The social biology of wasps. New York: Comstock/CornellUniversity Press, 99–148.

Rhainds M, Davis DR, Price PW. 2009. Bionomics ofBagworms (Lepidoptera: Psychidae). Annual Review ofEntomology 54: 209–226.

Richards OW. 1978. The social wasps of the Americasexcluding the vespinae. London: British Museum (NaturalHistory).

Stephens CS. 1962. Oiketicus kirbyi (Lepidoptera: Psychi-dae) a pest of bananas in Costa Rica. Journal of EconomicEntomology 55: 381–386.

Strassmann JE. 1981. Parasitoids, predators, and group sizein the paper wasp, Polistes exclamans. Ecology 62: 1225–1233.

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