\ociobiologl 6l(-l): 2lJ6-292 (Scptcrribcr 2014) lX )l : I (1. I i I 02isoc iobiokrgr.v(r I i"1.2ll(r-192

Sociobiology An intemational .ioumal on social insccts

Mutualistic relationships between the shield , Meronoplus bicolor (Gu6rin-Meneville) (: Formicidae) and honeydew-producing hemipterans in guava plantation

I BURIKAM, D KANTHA

KASETSART UNIVERSIry, NAKH?N PATHOM, THAILAND

Article History Abstract Mutualistic relationships between the shield ant, Meronoplus bicolor (Guerin- Edited by M6neville), and two species of hemipteran, Aphis gossypii Glover and Ferrisio virgoto Jacques H. C. Delabie, UESC, Brazil (Cockerell), were investigated in an unsprayed guava plot at Kamphaeng Saen, Nakhon Received 10 Deceber 2013 field and laboratory lnitial acceptance 19 May 2014 Pathom, Thailand. The reciprocal benefits were observed in both Final acceptance 20 July 2014 studies. M. bicolor activity coincided with peak seasonal activity of both hemipterans during.lune-August. We indicated two sets of support evidence in M. bicolor honeydew Keywords preference: (i) statistically higher value of adjusted honeydew weight collected by ant cotton aphid, striped mealvbug, coc- workers from A. gossypiicompared with that from E virgoto (p-value = .005), and (ii) cinellids, syrphid fly, Psidium guojovo the higher value of the strength of effect (r1' = '62]'in the total variance of multi-species physical property on honeydew viscosity was discussed concerning Corresponding author association. The between-subjects lntawat Burikam ant preference. we used two-group, ant-tended and ant-excluded, benefits' Department of EntomologY multivariate analysis of variance (MANOVA) in order to show hemipteran Kamphaeng together with Faculty of Agriculture at Both hemipteran populations increased in the ant-tended treatment, Saen, Kasetsart UniversitY (Fabricius) and lesser amounts of two species of coccinellids , Menochilus sexmoculotus Nakhon Pathom 73140, Thailand fly, Pseudodorus clovotus coccinello tronsversalis Fabricius, and one species of syrphid E-Mail : [email protected] (Fabricius),comparedwiththeantexclusiontreatment(Svalue<.001).Thefacultative hemipteran species were mentioned' mutualistic relationships of M. bicolor and the two

(Delabie' 200 I )' are rnostll facultative or opportunistic lntroduction hctniplcrans Cienerally. ants benetrt liom associations with tbod source itl tlre lbrrl of (Cuerin-M6nevi I le) by obtaining carbohydrate-rich sh ield anl. il'le r u nLt pl u s b i c ol ttr The fronr hemipterans (e'g': Nixon' 195 l: ground nesting spe- "llon"yd.*; secreted (Hymenoptera: Formicidae). is a cotnmon "l Specifical11" the Way, 96-i; Hollclobler & Wilson' 1990) tbragirrg behavior' .i.,orthesubfamil.vMyrmicinae.andiswidelydistributed to ants have beetr focused on the Region (Schddlh' 1998)' The U.trlnt, throughout the entire Oriental (Stadler & Dixon' 20051 Grover et al'' 2007: as scaveugers' of rvorker ants not only forage on dead olr fittress betrefits *ork.., et aI..20 l0)' Sonre have concetrtt'alecl carbohydrate source tionl Kay & but also collect honeydew as growth (Grover et al ' 20071 [lehns Glover (He- in tertns of ant colony the cotton aphid' gossvpil ln rettrnr the berlefits' ants hemipterans. e.g. "lphis Vinson,2008; Wilder et al'' 20 Il)' I'crrisia virgttttt products' OOn'Oitl onO the striped rnealy'bug' contamination of their waste ,'OtJ*t eco- nray reduce hemipteran in agricultural natural enenries' and (Cockerell) (: Pseudococcidae)' ;";il dead individuals' protecting sites' resulting in the svstem.However,thetlophobioticrelationshipsornttrtualism hemipterans to new feecling 'J.,r..r' hemipterans are transport 1963: Nielsen andltoneydew-producing populations (e'g': Way' ii r,' ot u' abundance of hemiptetan 2005)' Ants e\ploit hcnripterans unknown. .ili.. ,oto, Stadler'& Dixori' alld honeydew-producing also as a.protein source Mutualism between ants for their honeyderv' btrt of relation- not only (B-uckleY' 1987: iientified as a contitluttnr us a conlmon prey hemipterans has been when tbraging on tl"re"' (Stadler & 200 l)' However' this rnutualistic to antagonistic Wilson' lg'nt ships ranging from by Htrlldobler & anA hemipterans tending '"tobi"' Dixon. 2005; eif f i'r tt;i-looz)'

phplsociobrologv http //perrochcos uefs'brlols/indcx Open access .lournal' tSsN ult' t-t':r: Sociobiolog_v 6 l(3): 2lt6-2t)2 (Scptcnrhcr 201-l; 107 type of antagonistic relationships will not be treated here; tured in an empty hard gelatin capsule (size 0; outer diarneter we are looking at a concrete evidence of mutually benefits 7.6-5 nrnt. height 21.7 mnt. and volume 0.68 ml ol'Ibrpac among both partners. lnc." NJ), and shortly after. the capsule containing the arlcstecl In this stud1, we '"'elified, in both field and laboratorl ant was weighed on a digital balance. I hc aclu:il ant wcight experiments. thc reciprocal benefits of .l,l hicolor ancl two was obtained fronr the sutrtraction o1'the capsulc wciglrt. \\'e species o1'horreldew producing henr ipterans. . l. grr.r.r'r7,lli and rveighed. tionr lleld collectccl. t\vo scts (n 20()) lirraSirrg ants l'. virguttt. We concentrated lbr r)ver three ntonth period in visiting.l go.s.rr7rii. arrd one sct (n . 100) ol'ants v'isiring l. -lhe the guava plantation ol' llorticLrlture f)epartnrent, Kasetsart virguttt. honeyclera, loacls were corrlirrned ra,ith tlre labo- University. Nakhon Pathorrr, Thailand, observing rhe mutu- rator-v- set up by' l'eeding ol ll ltit'olor rvorkers rvith hone-r,- alism ofant hemipterans including the abundance ofnatural de'*'. A set of field collected workers (n: I00) leaving their enelxies. nlainly predatom. We tested three hypotheses: (i) ants nests for foraging were randonrly chosen. holding irr captivitl' receiving bencfits in temrs of lronevdew fiom rnutualistic lor 24 hours rvithout fbod, and subsequenlll captured inside associations in guava agroecosysterl; (ii) ants protecting he- the gelatin capsule tbr weighirrg. .4fter weighing. halt'ot-the mipterans fiom natural enenlies therefbre the densities of natu- 24-hcrur arrested ,\'l bicolor was offered with quava lea'"'es ral enemies decrease in the presence of ants; and (iii) in con- occupied by honeydew exudates of ..1. gr.r.r,r-r7rii. and the other sequence ofthe two hypotheses nrentioned earlier. resulting half of ants with honeydew fi'orn l. virgata. The ants were in the incrernents of henlipterarr densities in ant hemiptelan allowed to feed on honeydew until they either refused to feed associations compared with the ant exclusion arrangelnent. or left the guava leave. All tl'(. bic'olor wolkers were rveighed fol the second tinre in order to obtain honeydew loads befbre Vlaterials & Methods releasing back to their fbrnrer habitats.

St.ud\' ,sltcc:ie.s I Ienriptct'an be ncfit.r

The study was conducted dLrring April-.December We randonrly' selected 30 guava trees. age 61'ears old. 20l2 in the unsprayed varietal collection plots (valieties: approximately 1.65 m in height and 2.5 2.75 rn in dianreter Phant Si Thong. Kim Ju" and Vhan Pi Roon). consisting ol' from the pesticide free guava plot as our study units. One of 336 guava trees, P.sicliunr guctf uvct, of Horliculture Depart- tr.r,cl similar branches rvas randonrly chosen lionr each selected nrent. Faculty of Agriculture at Kanlphaeng Saen. Kasetsart tree to perfornr ant-exclusion treatrnent. using sticky" barrier L.lniversity, Thailand ( 14.0358 "N. 99.9826 "E,). The predonr- around the base ofthe branch cov'ering 20 cnr in length. The inant ground'-nesting ant species in the study area was the na- tatget branch was first wrapped atound with plastic'uvrap" and tive ,1,1 bicolor. with only a few colonies of the invasive aut then applied with generic horticultural glue (colorless ancl species the tropical fire-ant. Solenopsis geminutct (Fabricius) odorless). The objective ofthe gluey barlier is to prevent ants near the perinleter of the plantation. The honeydew-producing and other crawling fiom reaching hemipteran colonies hemipterans were ..1 gossl,pii and l:. t'irguta. The natural at the guava shot'rts, allor.r'ing only the entering o1'air-borne enemies. mainly predators. were two species of coccinellid insects, including rvinged aphids. mealybug crarvlers" ladv- (' beetles. l'1 e nrsc hi I u s .s ex nacu I atu s ( Fabri ci us ) and oc c i nc I I Lt bugs, and syrphid llies. The barriers were exatninecl periocli- trunsversulis F'abricius (Coleoptera: Coccinellidae). and one cally, and reapplied the glue as required, in orcler to rnaintain species of syrphid ffy. Pseudodorus c'lat,altls (FabriciLrs) the efl'ectiveness as ant balriers throughout the experimental (Diptera: Syrphidae). period. The other branch rvas left untnanipulated as the ant presence treatnrent. There was the total of 60 experinrental .,1til henefit untl hone|dey, pre/ercnce units. This ant-exclusion/presence experinrerrt wtrs started in Vlay. treginning with equal nurnbers of both .'l go,r',r't7rii and The direct benefit ol ,\'1. bic'oltr was obtained by weigh- l'. t'i'g,uttt between the two tt'eatlrents on the satnc guava trec. ing a certain numbel of tbraging atrts, attd then calculating the observations were ntade during peak seasonal actil'i- difference of weight gain between lbragers descending and ties of both hemiptel'ans and their natural enenties in June ascending the guava branches. We trteasured weight gains of August 20 I 2. l,l hic:olor afler visiting hemipteran colonies as honeydew On each clrosen guava tree. we randomly selected one receiving. We randorrrlv chose foraging ants tionr the field to terminal shoot fi'om the total of J-5 shoots of each experi- rveigh tbr honevdew loading: 50 ant foragers ascending the mental unit. in order to make observations. All terminal shoot guava branch before leaching herniptelan colonies. and the belonging to each expelinretttal unit had att equal chancc to other' 50 individuals descending the blanch with full load of be picked on each data collection day.'lhe number of he- honeydew. I{oneydew loads were nleasured frotn the weight nripterans: A. gosst'pii. l'.'virguta; and lat'r'ae of predators: ,1'l. differences of ants filled with honeyderv atrd ants ascending sexnruarlalus. ('. lrunsversctlis, and P. c'luvatus, occupf ing the guava branch. Individual worker of l'1. bic'ttlor was cap- the branch terminal side of 30 cm in length of both presence

288 I Burikam, D Kantha - Meronoplus bicolor-hemipteran mutualism in guava

and absence of \l bicolor were counted at various inteNals \l !c-\klLtLulut .\'. larvae of ( trdtl\r'(,r.\uli\-. and larvac ol' throughout the duration ofthe experinrent frorl April De- P tltty'utus. All insect counts were translirrnred into log {),- cenlberl0ll. Wecouitedthe insects at inter,'al ofi 5dals. I ) lornrat; wherc v : nunlher of insect. in ordcr Io lrgrcc rr,itlr wilh thc lolal ()1 7 timcs pcr month during Junc /\ul-lusl. co, statisrical assurnptions. irlcided \vith fhe peak aclivities ofboth henripterans and their' Scrcral orrtputs \ere rccluestcri liotrr the \4,A\()\r\ predato$, and ercry l5 clays in other nlonths. Hor.rcver. the anal)sis ol'lBVl SPSS. Box's lest ofEqualitl,o1 ('ovariarrce ohservation dala or mLrltivariate responses of the five rlepen- Ma{rices expected to see il thc deperldcr)t variablc covarialtcc dent variables were derived fiont the average of 7 times x nralrices are eq(ral across the levels {)l lhc prcsencc abscncc 3 nronths = 2l field observations during peak activities of ol .ll hicolor. Ba lett s Test ofSphericitl was demanded to the insects in June August20l2. We recorded the numberof ascertain sufficient corrclation between depeDdcnt nlcasures ll 6icolor nrovirrg up or down (bidirectional) passed a fixed in order to pnrceed with the analr,sis. fhe core MANO\'.A outpul point on thc treatrnent branch witl'r no gluey ban ier for.i rnin rvas incluired lbr the nrullivariate null hypothesis evaluation period, to ascerlain ant activity throughout the overall e\per- ol no diflbrences between presence and absence o1 ,t1 hfuu/rrr on imental period I'ronr April-December 2012. All observations the compesite dependenl (nunrber ol'insects) !ariate. \\'hen in thc field rvere done duling 08:30 I l:i0 hours. the multivariate tesl is statistically sienificant. we can pro- ceed with sorre assessnrents of cach dcpendcnt variablc. \!t Statistical anab,ses pertbrnred the'lests ofBetrveen Subjects Effects to evalualc thc statistical significance of each depe[denl variahle sepa- To answer the qucstion on the difJitence of honcydcw ratcly. Bonfirroni corrcctcd alpha lcvcl rras appliccl to av,lid weights or ant's honeydew pref'erence between ,ll 6rcrlor' alpha inl'lation in order to evaluatc thcsc preseDce and xbseDce collecting ,.1. go.s.!)r)il honeydew conlpared with those of I of ,11 6ri'olo/ efibcts. Wedivided.05 bytherrurnberof A\O\As t,it'gcttu. \\e used analysis of covariance (ANCO\A ) of IBIVI and obtained .05i5 or a Bonfbrron i-con ected alpha level of .01. SPSS Statistics (Venna. 2013: Meyer et al.. 2013). Body weight of M. bicolor workers with empty stonrach (24 hour Results and Discussion unfed rvorkers) or weight before receiving honeydew was trealed as covariate, and the crirerion variable or dependent .11 lli'o1ol generally tirraged on honel'dov ol'hemiptcrans variable vvas ant veight alter eating honeydew lionr each he- as ca|boh)drale sourcc throulthoul thc )car in guit\a plan- mipteran species. The analysis of covariance approach was tation at Kamphaeng Saen. Monthll- averages (+ Sll) o1 ly' used in order to adiust the initial variations of ,11 hicolor 6lcolo| activity flonr April Decenrber 1012 are presented in worker size- l:ig l. .ll. hicolor activity coinciiled with population Iluctua- The honeydew-producing hemipteran benefits were tions of both hernipterans (.1. gosqpii. and /. l,.i,gdld). with demonstrated b) interlLrence ofants. predominantly .ll 6(o/r,r, peaks seasonal activities in June August ([:ig )). There were with sticky barrier applying around the base ofthe ntain branch very high colrc'lation coeflicienls {r's) hetwcen anl acti\il} in order to erclude the ant. The abundance of henriptelans and andeither I gr.rs.r_r.7rli or / r,//X.r/.r derrsity at r ".97 (// value natural enemies were compared bet\ae$ presence and absence .'.001;n -9)andr=.9i1 (p-value..001: n 9).respectivel). of Il bicolot We anticipated more hemipterans and less natural ll hicolor dominated the other ground nestin{ ant enemies in the ant attended guava branches. species. .lolerropsls get inlrtu, itl the studi!'d guava plol. al- Most studies of anl hemipteran interactions iucluded though .t .gcrilli(r.r has been considerecl as one of the most either ant or hemipteran !'enrovals from the study plants. and invasive ant species worldwide ('tlettercr. 20ll). but not in made conrparisons with the unnlanipulated partners. The con- this guava ecosystenr with history of pesticide applications. clusions. in ge,reral" relied on statistical anal),sis b) the uses There were no,\i. .gearlanla rvorkers observed on the cxpcri- of univariate analysis ofvariance (ANOVA), which concen- mental guavatrees. lhetolerarrce to pesticides ol ll hiLLtlrt' trated on one dependent variable. with attempts to nrake find- was probably duc lo the protectiou of long finc hair covcring ings from multiple analyses of ANOVA (e.g.: Flatt & weiss- the entire body (Schiidlh. 1998). together wiih thc dci'ensive er,2000; Billick et aI..2007i Daane et aI..2007i Mgooheki& behaviot o1 .l/ercarrplrrs by curling up the [rody and tiigncd Addison,2009; Styrsky & Eubanks.20l0). Herein we used dead when distutbed (lldlldobler', 1988 ). nrultivariate analysis of vafiance (MANO\A) ol IBM SPSS

Statistics ( Mel'er et al.. l0 t .j: Rencher & Christensen. 20 l2). 1 nl benclit untl hone\ Jet, ftaftrcn,e in orde| to draw onc solid conclusion ofant henlipteran mu- iualism based on the compat'ison offive dependent variables lD the studied guava plantaiiorl. ftlragers of .|y' fiilrrloi froln two groups^ presence and absenoe of ll hicolorolr.gt.la- leaving their nesls weighed approximatcll l.4lt m8, (S[: va lrranches. l hest' 6ve dependent variables or trlultivariate .08: n - 150). After visitirlg hemiptcrarl colonies, l/. hicolr.,r' responses were number of insects: i.e. nynlphs and adults rrith honel'dew loaded. descending the branch back to thcir (SE 150). The of .,1. go.!xl?li; nymphs and adults of F. ,l/'8(/.r; larvae of nests weighed on averagc 8.69 nlg ' 0.l: n Sociobiokrgl' (r l(3): 2tl6-21)2 (Scptenrher 20 141 lronevdera, loading is about 6.21 nr-rr (lt.69 - 2.48) or roughly, rvorker ant with honeydew loaded frorr 1.. virguttr (ad.justed esrimate around 2.5 tbld (6.1I - 2.48) of the nrean foraser mean - 10.-sJ; 59 - .072'^95co('l - I0 40ti-10.69.1) (Fis 2). .T'he -[-his r.reight de parture fiont their nests. weighting copacir) could indicate that J/. hit,oltn.wtir.kcrs prcfcr. horrcl,clcrv t'tl' ,l'1. hit'olrtr worlicrs was reconfirrncd in a conlincd stucly tionr.l gtt.tst,piito tlrat fiorn l. virguttt. of laboratorl, feeding of ant rvorkers to different kincls ol' Ants are expected to coltcentratc their honel clcrr col- honeyder.v tiom both henripteran species. Atier 2.1 hours in lection activities on henripteran species ofl'ering higher re - captivity-, ,l,l hicolttt' workers weighed -3.61 mg (S8..0.12; ward in terms of both quantitative and qualitative el}'ects. n -- 100) on average. We selected larger workers r,l,ith nrore Hemipteran species that produce larser amount of honeyclew, tolerance and easier fbr seizing in order to withstand the 24- or having honeydew tvith the presence ofpl-eferred sugars or hour starvation before obtaining honeydew. These workers arnino acids should be more attractive to certairr ant species were fully fed with honeydew from different henripteran spe- (Cushrnan. l99l: Vdlkl et al.. 1999: Yao, 2014).,\nt prcference cies, and later weighed approximately 10.70 mg (SE = 0.15; for particular sugals in hemipteran honeydew can be spccics spc- n ''. 100). The overall expected value of honeyderv loading is cific (Bltithgen & Fiedler, 2004). Several arrt species rcacr 7.09 mg ( 10.70 * 3.61 ), with an estinrate of 2.96-fbld (7.09 strongly to honevdew that holds large anrounts of rnelezitose - 3.6 I ) of the average worker weight after 24 hour in caging. (V

: 9 90 6 8 E ll oo q igo 1 g : E 270 6 E

o60 5 E E 4 I\ro 7E 3 Eo !s 3 s! 2 Adiusredweitht 5rog ! Emptystomach Honeydewloadint E $ i20 rt 10 Fig 2. Mean rveight of ;\'lerant4tlu.s hitolor workers (rng) (2-1 nrc-an 0 with enrpty stomach hour rvithout firod). weight Apnl Mry June Jlt Aug6l Seplefrer odoher N@cder oeede, with honeyde'"v loading, and ad-justcd rncan rveishl liorn F'ig l. \'lonthly average ol .l.tercmo1tlu,s bicolor activit) (r different henripteran species, .1phi.s goss.r,pii and larrisitt SE, vertical line), and hemipteran densities (l;erui.siLt vitgutLt t,irgutu. Value on top of column clrart inclicates data label: and ,,|phis goss_vpii) from 30 ant tended guava branches at difl'erent letters fbllowed mean values represent statistically Kamphaeng Saer.r. Nakhon Pathonr. Thailand in year 20 12. significant differences (7l_values 5 .005). 290 I Burikam, D Kantha - Meronoplus bicolor-hemipteran mutualism in guava

llemipte run lvnalit.t henripteran species. krgether with lesscr allrounts ol'all rrirtu- ral enenrics compared rvith the ant .excludcd tleatrrrerrt (Fig -l A trvo group betu,een sub.iects M.{NOVA was done j). here was nrorc iibundarrt in clensitl. ol roLrr:h11 7.6 tbld orr logarithtnic transfcrrrned data Uog () + l)l y : obscrvation [{antilog(1.824) l} - {antilog(1.00]) l}or68.50 . 9.05 data] of five dependent variables: no. rrf ..1. no.r.r'rpili no. of /'.' .. 7.571 ol .1. gost,ltii than /'. t,irl:utLt {ionr .10 guava trccs in t,it'gLtltt: ncr. crf ,Il sexntttcululus larvae; no. of ('. lrunstersulis the study (Fig.l). larvaet and no. of 1l cluvcttus lan'ae. The independent variable In general. we rvould say that ,11 bit'ttlor preferred ()r tr eatnrent \vas thL' presence-absence of ants. partir;ularl1,,I/ to associatecl rvith ,.1 go.s,r17rri ntore than l'. r,i.rlrrlrr, in this hit'olrr'" in guava plantation. There were t\vo treatnrcnts. i.e. nreanins the prefelence ofhonc'yderv collectirre" as indicated ant tended and ant excluded. In general, the ant excluded treat- by higher valr"re of the strength of'ef{'ect or effect size (Levine ment with sticky barrier was quite effective against ,\'1. bic'olor. & Hullett.2002; Meyers et al.,20ll), i.e. q: ,= .62 and I'' .-52. the slor,v-movin-e ant species. Even though solne ants could respectively- ('Iable I ). I'his could be the second evidence in accidentally reach the colonies of hemipterans on the exclu- supporting the previous study of honeydew pref-erence ol'24 sion treatnlent fronr adjacent branches due to the contact with hour captured l.l bicolor. Among the three natural enenties nearby branches via wind blowing, however, these ants could or predators. ;tu'l. sexnutc'ululrr.s had nrore strength of effect (1' not letunl back to their nests or could not be able to recruit : .55), i.e. rvould be nrore effective pretlator. tharr the othcr two additional ant foragers. conrpetitors (11rs = -.it). ancl ..ll) in this '11 hitttlor hcnriptcran The santple consisted of 60 guava branches divided association (Table I ). Even tlrouglr the surphicl tly. l' tlut,uru.s. into equaf anrounts of presettce and absence of .ll. bic'olor. was more abundant than the othcr two coocinellid predators. The output of' Box's Test ol' Equality of C'ovariance Matri- but its appearance irr the guava plot uas restrict to JLrne till ces was statistically significant (Box's ..1./ = 69.9981 7r-valus ": August. In addition, there rvere no l'. c-lnt,ttltr.r larvae foLrnd .00 I ), showing that the dependent variable covariance rnatri- preying on the striped rrealybug. l- virguta. in our study. ces were not equal across the levels ofthe presence absence l"he nrutualistic relationships or trophobiotic intcrac- of 11. bicolor. Therefore. Pillai's trace was used to evaluate tions between either .,l go.t.s.r,pii or l vir.qtiltt with ants havc all multivariate effbcts (Meyer et al., 2013). Bartlett's Test of been classified as lircultative and very colrnrou phcnonrenon Sphericity rvas statistically significant (apploxirnate chi-square b1' Delabie (200 l). There are two rnain reasons liorr this ,, 99.838; p-value.: 001). indicating sufficient correlation study in supporting the abovc mentionecl: firstly. both he- between the dependent variables to proceed with the MANo- mipteran species are polyphagous and cosmopolitan species VA. Using Pillai's trace as the criteria. the combined dependent ( Blackman & Eastop, 2000; da Silva-'l-orres et al.. 20 l.i ), any variable was significantly affected by the presence-absence of nrutualistic relationship with ants should be opportunistic or ill. hicolor. Pillai's trace: .807, h'1,,r1 - 45.244,7r-value.< facultative rather than obligatory; and secondly. l,l. bic'olor .001. There rvere leliable multivariate diflerences between is the nrost comrlron species of the qenus .l.lerunoplrrs in the ant-tended and ant-excluded treatments on the combined Oriental Region (Schcjdlh. 1998). ancl is rvidel_v tlistributed dependent variate. The partial eta squared - .807 (panial 11:). .. nesting species in clisturbecl lrabitats ofagricultural eclr-rivalent to the full eta squared (Ir) in this two-group de- ::or,ld sign (Levine & Hullett.2002). indicating that,"ve had a very high propor-tion of the total variance (.807, or about gl9lo) ! Ant-tended d2 e.xplained b1 the activity ol' ,1.1. hic.olor. E Ant{xcluded Each dependent measure ,i ]otal average or each obser.vecl insect -9 density was assessed individually in orcler to deterntine the € r.s strength of the statistically, significant multivar.iate et}.ect. The : result of the tests of the urrivariate effects is shown in Table nr l. We had statistically E signilicance univariate effects on all dependent variables (Table l; p-values < .00 I ). Of all insect species under investigation. 9 o.s .1. go;;slpii pr.ovidcd the highest effect size (rt2 -. .62), while,tk,ro|nr,,lr,,,., had highest ef- f'ect size in terms of natural enemies (ll2 = .5-5) (Table l). The descriprive infbrmation il fbr the univariate analysis is presented in Fig 3; providing.u"h Fig 3. Effect of ;l.leranoplus o.p.nJ"nrir.urur.,, bicolor_exclusion on hemipterans seryed ou_ (,41this means" and total averages obtaining go,rs.ltpii and l.-erri.tiu from 30 guava trees virguttt) and their natural in the stud1. nties ene- The presence of ,1.1. (,l.lenocltilu.t ,sexmtrctrlafits, bicotoi_t.uJ.a tr.rripr.,rn. (.oc.cineltn tl,lru,.rvor,roti,, P.ye wlodont anrl inrpact on insect populations s c: I tn a tusl. Differ.ent l:1,1.-.""t'gerable_ nor onlv f .n.,.' on ar'of ,lort nemrprera, rhenrselves, but rui un-l n, also th.i,.'"";;;;i';;;,;;r.;; Tl:esent statistically si_qrrificant ,tifEr.n.., ant-tended treatn.lent. f, untr., , we detected frlgf,", .00 I ): nunrbers on top i.n.ities ot. both of.clear .utrn,,,. i,r',U.r,JOo,, o1'tcltal ,,,n.,, average .r grand nrean fionr -i0 grava trecs. Sociobiologl' 6 l(3): 2tl6-292 (Scptcnrher' 20 14,) 291 'lhble ' : l.'lests ol'Lutilariate cllbcts t>l' ,\,leruno;tlus I p h g t t,t s.t' t i i l t, l ) ( l t i hitttlor aclit itv on livc dcpcnclcnl raliatrlcs": i.: 1 : a rc i s i u i t' gu d :,\1 ! tk I u: se.xmo(ultilus- ('oct'inullrr lntnsvcrsuli.s- ttn

Sourcc [)epcnrlerrl r ar llpc lll SS (ll MS 7r-r'a luc l:ta sqr"rated (t1r) .\nl .,1. gos.t.v'1tii .466 I .466 96. ffitt 000f 6lJ li. t,irgattr I .6t3 I I 1.68 I 6I.t{5e .(x)0 5 l(r

,\'l. .sa.xnot tr|utus I .141 I I .7{1 72.lrl .0(x) -5 5l ( . lntnsvcr:;olis .977 I .911 )7.876 .(XX) rl) j9-l P. clttvttt.rs .92 5 I .92 -5 37.515 .0(x)

l:rror ,1. goss.t,pii .28 r 58 .005 l. virgata 1.576 5ti .027 A,l. setmuculatus 1.402 58 .t\24 ('. lnmstcrsulis 2.034 58 035 P. t lowiltts 1.130 5{r .02 5

('orlcclcd totaI ,1. goss.t,pii 716 59 F yirgdkj 1.2 57 59

:l'1. sexmoc'ulatu.t -1. I .1(r 59 ('. tnusversalis 3.01 I 59 P. t'kn'olt.ts 2.,.r 55 59

h .(XX) inriicates < .00 l.

ecosystenr, theretbre the accluiring for tbod in the vicinitl References should be by seleotion ofnlost abundant resources. This studv shorved that ant attending had a considerable Billick, 1.. Hanrmer, S.. Reithel..l.S. & Abbot. P. (2007).,Ant- 'l eflbct on hernipterous pest densities in guava plantation. here aphid interactions: Are ants fiiends. enenries. or bttth'l Annals were nlore individuals ot'henripterans in the ant tendine gua- of the Entomological Society of Anrerica. 100: 887 892. va branches, together with lesser amounts of natural enemies Blackman. R.L. & Eastop. V.F. (2000). Aphids on the World's mainly predators because of ant guarding activities. ln return Crops: An identification and fornratiorr guide (2lrd edition). the benefit. ants leceived carbohydrate sources in telms of ('hichester: John \\'ilcv and Sons Ltcl. honeydew fionr both hernipterans. ln general, the results of this ant exclusiolt experintent using glue) barrier are agreed Bliithgen, N. & Fiedler. K. (200.1). Prcfertnces tbr suqan arrd arnirro with previous stutlies done in fi'uit orchards: e.g. cherry acids and theil conditionalit-v- in a diversc ncctar-lecding ant (Stutz & Schmidt-Entling. 20 I l). apple (Stewart-Jones et al., corrmunity. Journal of Aninral [:,cology.7-]: 155-166. 2008; I\4ifrarro et a1.,20 l0; Nagy et a1.,20 l3): and in vine- Buckley, R.C. ( 1987). lntemctions involving plants. Hontoptera. and yards (Mgocheki & Addison. 2009). ants. Annual Review of Ecology and Systernatics. I 8: I I I - I 35. In conclusion. mutualistic relationships between :11

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