BLUMEA 41 (1996) 223-230 Capparis buwaldae Jacobs (Capparaceae). A new Myrmecophyte from Borneo U. Maschwitz K. Dumpert J. Moog J.V. LaFrankie & I.Hj. Azarae Summary Capparisbuwaldae,aclimber ofprimary forestsendemic toBorneo,is amyrmecophytewith stem domatia.Thestemsbecome hollow by pith degenerationanddevelopovalopeningsallowingants to enter.Theseopeningsarelocalized atastrictly defined areaabovethe insertion ofthe leaves and a pairofnodal thornystipules. Theygraduallysplit openfrom theoutside.Theopeningsmay develop intoelevatedchimney-like structures orcloseagain bygrowthifnotkept openby ants. Theplant may beinhabited byvariousopportunistically nestingarborealants includingCremato- gaster,Monomorium,andCamponotusspecies. Specializedmyrmecophytic antscould notbefound. Neither nectaries,norfoodbodies,nor trophobioticendophytichomopteranscould beobserved. In the Rijksherbarium, Leiden 65 otherCapparisspecies and subspecies from the Indo-Australian region were examined forant-plantcharacters.Noneofthese speciesshowed anymyrmecophytic character. Introduction Inlatteryearsin SoutheastAsia anincreasing numberofdomatia-forming non-epi- phyticant-plants havebeen discoveredinvarious families.Highly evolvedsystems came to light withspecific partner ant species biting entrances into their domatia (Maschwitz et al., 1989, 1991;Moog & Maschwitz, 1994,and unpublished results), as well asmore generalistic ant-plants whose domatiaare opened by theplant itself through growthprocesses, giving access toa varietyofopportunistically nesting ar- boricolousants (Maschwitz etal., 1992, 1994a,1994b,unpublished results). In the lastfive years atleast 19plantspecies from 10generain 8 angiosperm familiesprov- edto benew ant-plants. Therefore, thenumberofknown Asiannon-epiphytic ant- plant generais nearly as large as thatoftheNeotropics (32 versus 39) whichuntil nowwas thought to beby farthelargest oftheworld (Davidson & McKey, 1993). During an excursion through Sarawak (East Malaysia) we came upon a further new ant-plant which belongs to the second association type. For thefirst timewe becameattentiveto its myrmecophytic characterbecausethestemoftheplant speci- men was severely damagedby arodentina characteristicway whichcan frequently beobserved inspecific Asianant-plants likeMacaranga andNeonauclea(unpublished data).Recognizable by thetracesofitsteeththisanimal(possibly a tree rat orsquir- rel) hadtorn upthehollowplantstemrepeatedly inasectionofhalfametre. Similar tracesofdestructioncouldbeobserved in5otherplant specimens. 1) Zoologisches Institutder J.W.Goethe-Universitat,Siesmayerstrasse70, D-60054Frankfurt am Main,Germany. 2) Center forTropicalForestScience,InstituteofEducation,Singapore. 3) University ofMalaya,DepartmentofZoology,KualaLumpur,Malaysia. 224 BLUMEA —Vol. 41, No. 1, 1996 Fig. 1.Capparisbuwaldae Jacobs,habitofthe upperpartoftheplant. Maschwitz,Dumpert,Moog,LaFrankie & Azarae: A newmyrmecophytefromBorneo 225 MATERIALSANDMETHODS Eightspecimens ofCapparis buwaldaewerefoundinLambirHills NationalPark, an undisturbedmixeddipterocarp lowlandforestnearMiriabout100mabove sealevel. They grewon aridge in adenseand dark undergrowth ofshrubs, tree saplings, and palms. IntheRijksherbarium (Leiden) specimens ofC.buwaldaeas well as other Capparis species fromtheIndo-Australianregion wereexaminedforpossible ant- plant characters. Driedspecimens ofC. buwaldaehavebeen deposited in theper- sonalcollectionofJ. Moog; later, they willbehandedover totheRijksherbarium at Leiden. RESULTS Capparis buwaldae(Capparaceac) is a climber2-15 m long (Jacobs, 1960,1976). Thefirstspecimen foundby us, whichwill be described inmore detail, was a deep- rooted, erect, woody, green-stemmed plant 1.5 m high,whichwas originally broken offata height of0.65 m(lower part)andhadformeda newshoot0.86m high,with 21 leaves inthe upperpart and 3 small sidebranches. The leathery, short-stalked, lanceolateleaves(length = 18.2± 2.2cm,width=3.7±0.5cm) withawater drain- ing tip(Fig. 1)were growing inawhorl. Theleaves were sittingbetweentwo small thorny stipules which wereslightly pointing downward.Insteadofaleafsometimes apeculiar thread-likegreenappendage was found,0.2-1 cm long (Fig. 3a). About 3mmabovetheinsertionofleavessidebrancheshad developed. Ant-plant characters The stem did not form any distinct internodaldomatiaswellings but was hollow as awhole. However, itsupperregion was rather wide.The cavity was developing by degeneration ofthestempithintheupperparts, i.e., thepithbecamefragmented intothin,lamellous, translucent, whitishdiscs(Fig. 2). Thelowestandoldestparts ofthestem,5-6.5mmindiameter, were solid.With increasing height and diameter Fig.2.Pith degenerationinayoungshootofCapparisbuwaldae Jacobs. Scale bar= 1mm. 226 BLUMEA Vol. 41, No. 1, 1996 Fig. 3.Stagesofstomadevelopmentin Capparisbuwaldae Jacobs (fromatof).a. Stomaless node ofa shoot;instead ofaleaf afathom-like green structure has developedbetween a pairofthorny stipules; b. still closed young stoma; c& d.developingstoma;e. elder stomaopening, kept open by antinhabitants;f.unused stoma, closedagainbycallus growth. ofthestemthecavity was developing, measuring from4mm(stem diameter11mm) to6.5 mmin width(stem diameter 10-11 mm in theupper stemregion). In most hollowsections ofthe stem,wall openings (stomata) occurred. Theirdevelopment couldbe observedbest inthe upperstem part(Fig. 3). The openings were located about2-3mmabove themiddleoftheconnectionlineofthetwo thorny stipules, i.e., atthe same position wherealso the small side branchesoriginated. In some casesneitheranopening nor abranch haddeveloped. Theyoungeststillclosed open- ings consistedofsmall greenring-shaped bulges onthegreenstemwith awhitish centre (Fig. 3b). Inthis centre,beginning fromtheouter surfaceatiny, oblong, slit- likegroove(at firstonly visiblewith ahand lens) developed successively. Finally, theslitbrokethrough into theinteriorandformedasmall opening (Fig. 3c), which successively became larger(Fig. 3d). One such open oval stoma(1 mmlong,0.3 mm wide) couldbeobservedin theupperleafy partofthe new shoot. Inthelower leafy partbothstillclosedstomata and3 fullyopenholescouldbeobserved, theup- peronewas 1.2by 0.85mmin diameter,themiddlestoma hadatinybutrecogniz- Maschwitz,Dumpert,Moog,LaFrankie & Azarae: A new myrmecophytefrom Borneo 227 ableholeandtheloweronewas 0.6by 0.35 mmindiameter.As faras not destroyed by the predator very obvious stomata couldbefoundalso in the loweroldpart of theplant. They consistedofchimney-like elevationswiththick crater-likebulges and a centralhole(Fig. 3e). The largest elevationmeasured 10mmin length, 9mm in width,and3 mm inheight. Its holemeasured2 by 1 mm. Aslightly smaller second stomawas openas well,whilethreeothershadclosedagain byplant growth(Fig. 3f). Possibly, theants which hadinhabitedthestem priortoits partial destruction(and ofwhich only nest remnants andunidentifiableparts were left) hadkept open both holes. Similarlargestomata whichwerealso partly closedby growth were foundinthe lowerpart ofasecond plant(0.95 mlong). In itsupperpart thedevelopment ofnew stomatacouldbeobserved as describedabove. The third plant, 1.3 mlong,also hadbeenpartly destroyed atleastthreetimes. Here,too,large holescouldbe observed, partly atthenormalsitesabovethethorns andpartly atother sites, which apparently had beenproduced by gnawing ofthe predator andkept openby ants duringsubsequent regeneration ofthestem. Judging fromnest remainsin thestem interiorthis plant had been occupied by ants, which hadkept open theholes but laterhad disappeared. A youngsideshoot was thinner thanthemainstem (11 mmmaximum)buthollowas well (5.5-7mm outerdiameter withhollowwidth2.5-5 mm).Betweenthecavitiesofthemainoldandyoungshoot therewas ashortsolidstemsection. Thisshoothadneverbeeninhabitedby ants. We couldobserve neithernectariesnor foodbodieson thesurfaces ofleavesor stems. Fivefurtherplants withatypical lianashape couldbefoundduringasecondand thirdvisit atthesame site. Theplants all showedthesametypical ant-plant charac- ters. They were climbing on trees orgrowing along the ground and were 6,5, 3.5, 3, or 1.6 m long. All showed hollow internodesandthe stemsoffourplants were partially tornopen, presumably by arodent,intheway describedabove. Ant inhabitants Inthefirstplant, which appeared tohave been initially inhabitedby acolony of dolichoderineants (Tapinoma sp.?), smallMonomoriumworkers were found. The secondplant was colonizedby a groupofbroodlessworkers ofalargeCrematogas- ter species, whosemainnestwithqueenandbroodprobably was locatedelsewhere. Inthethirdplant only antcolony remnantsbut noliving antswere found. As already mentioned,theformerantinhabitantsappeared tohavebeenpreyedupon bythepred- ator(possibly arodent). Though antless, thisplanthadproduced new entrances atits young shoots. Thefourthplant, 1.6mlong, was inhabitedby aCrematogaster spe- cies as well. Thenest entrances witha diameter>3mmdifferedfromtheotheropen- ings by being protected witha 'carton' cover builtby theants.These'carton' covers showedsmall roundholes (diameter 1.5 mm), big enough to allowtheantsto enter. The hollowstem interiorwas separatedintoseveral compartmentsby 'carton' walls. All internodesofa youngsidebranch, 1.2mlong and withstill unopened stomata, were hollowbutnot colonizedby theants. Ofall fourplants withdamaged stemsonehadbeen abandonedcompletely by its ants whiletheintactstem sectionsoftheremaining threewere inhabitedby ants. One 228 BLUMEA —Vol. 41, No. 1, 1996 was occupied by acolonyofpolymorphic Crematogasterandtwoby coloniesoftwo Camponotus species, oneofthembelonging to thesaundersigroup,whoseworkers burstwhengripped withthefingers. All eightstudy plantslackedtrophobiotic homopterainthesteminterior.Noneof theplant specimens showedany signs ofcolonizationby aspecific ant. Herbariummaterial IntheRijksherbarium atLeidenwecouldcompareourplant samples with10Cap- parisbuwaldaespecimens collected inBorneo.Inallaspects oftheirouter vegetative morphology, i.e.,ofstem, thorny stipules, andleafstructures,no differencestoour plantscouldbe detected.Allotherspecies oftheregion differclearly fromCapparis buwaldaeinvegetative characters. Only 4ofthese 10specimens oftheLeidenherbariumwere largeenough indiam- eterto allowa meaningful investigation forant-plant characters. Oneofthesefour plants showedstem structures which weresimilar tosecondarily closedstomata,in- dicating apossible myrmecophytic characterofthisplant. However,itsstem, aswell asthestemsofthreeotherplants, were solidatthecutting site. In theLeidenherbarium65otherCapparis species andsubspecies fromtheIndo- Australianregion wereexaminedforpossible ant-plant characters. Twelve ofthese species wererepresented by 18or more specimens each, anumberwhich may be regarded sufficienttodecideifa myrmecophytic characterwas present.Noneofthe species checked showedany sign ofant-relatedstructures such as domatiaorpre- formedentrance holes: C. callophylla Blume(18 specimens), C. cantoniensisLour. (45), C. floribundaWight (24), C. lanceolarisDC. (41), C. lucida(Banks exDC.) Benth.(19), C. micracanthaDC. (121), C. pubiflora DC.(71), C. pyrifolia Lam. (44), C. quinifloraDC.(35), C. sepiaria L. (55), C. zeylanica L. (62), Ci . zippeliana Miq. (29). DISCUSSION Capparis buwaldaeisthe firstmyrmecophyte foundintheCapparaceae. Theants gain access to thecavitiesinthestemthrough spontaneously formedshortslit-likeopen- ings whichbecomeovalwhenenlarging. The smallsize andthecompact designof theopenings apparently does not compromise thestability ofthestem. They soon close again when not used or strengthen theirstability by growth whenkept open by ants.Generally, stemstability appearsan importantfactorindomatiaevolution. Neglected till now, ithas tobetakenintoaccount infutureinvestigations andreflec- tions. Theexaminationofherbariummaterialindicatesthat theformationofstomata is restrictedto C.buwaldae,all theother65species checkedare devoidofsuch struc- tures(although for somespecies, including C.buwaldae, the sample sizes were small). In SoutheastAsiasimilar spontaneously formedstomata areknown tooccur in speciesofvariousplantfamilies:Myrmeconauclea strigosa (Rubiaceae), severalZanth- oxylum species (Rutaceae), Ficusobscura var. borneensis(Moraceae) andCleroden- Maschwitz,Dumpert,Moog,LaFrankie& Azarae: A new myrmecophyle fromBorneo 229 drumfistulosum (Verbenaceae) (Maschwitz et al., 1989, 1992, 1994a, 1994b). All theseplantsare colonizedby avarietyofnon-specific ants.Hostspecificity is not ex- pected tobestrongly developed since manydifferentantsareableto colonizethestem ifan entrance holeisprovided by thehost-plant. In contrast,ant-plantswith (moreor less) specialized ant tenants,forinstanceAmericanCecropia, Triplaris,AfricanLeo- nardoxa andAsianMacaranga, form atmostweak spots in thestem wallsthrough whichthecolony-founding queenspenetrateintotheplantcavities. Only few ant spe- cies are ableto tunnel entrances into living plant tissueand thus donot depend on herbivorousstem boring insects toestablishprotected permanentnest sites in living plantparts. Such traitsin colony-founding antqueens, whichlead tohost specificity, cannot develop or will be lostifpreformed stomata permit thecolonizationofthe host-plant by opportunistically nesting non-specific ant species. In C. buwaldaewe expectto findspecies offurtherantgeneraas regularinhabitantsofthehollowstems. Theant species foundin C.buwaldaedidnot cultivate homopteran trophobionts insidethestems. Otherfoodsources fortheantslikenectariesandfoodbodiescould notbeobserved.The absenceofanyobviousfoodrewardsuggests thattheants have toleavetheirCapparis hosttoforage. Davidson &McKey (1993) discussedinMyr- meconaucleathepossibility ofnutrientaugmentation by theants.Thestorageofre- fuse andfaecesin thedomatiaby theants couldconcentrate nutrientswhich, ifthey couldberesorbed, wouldenhance hostfitnessin nutrient-poorenvironments. At present, evidencefor suchapositive effectto Myrmeconauclea orCapparis by their inhabitantsis lacking. InSouthAmericathesubtropical shrubCapparis retusa possesses nectariesandis oftenvisitedby nectarivorousants.Forexample, oneofthesenectary visitors, Cam- ponotus blandus,whilenot nesting inthis Capparis species, nonethelesslowersthe level ofleafdamageinflictedbytheleaf-cutting antAcromyrmex (Farji Breneretal., 1992). In somecases, myrmecophytism canbe detrimentalto thehost-plant becauseof damage doneby destructivevertebratepredators ofantbrood. Damage tomyrmeco- phytes by woodpeckers and mammalswas often observed(Davidson & McKey, 1993;Maschwitz etal., 1994a). In C.buwaldaewe recognized thesame phenome- nonpresumably causedby arodent. Six out ofeight plants found(=75%) showed damaged stemparts. Similartracesofdestructionwereobserved inhost-plants ofthe myrmecophytic ant genusCladomyrma, i.e., inNeonauclea,Drypetes, andinSaraca (unpubl. results). Somepredators seemto learnwheretofindtheantprey sincemost otherhost-plants inthevicinity suffereddamageas well.Butwhiletheproportion of damaged plants in apopulation appearstobe ratherlow, the impact of vertebrate damage onthemaintenanceofmyrmecophytic associationsis not easily assessed. ACKNOWLEDGEMENTS Wearegratefultothe directoroftheHerbarium /Hortus Botanicus,Leiden,Prof.P.Baas,foraccess totheherbarium material. Wethank Mr. K.M.Kochummen andDr. L.G.Saw foraccess totheher- barium attheForest Research InstituteMalaysia(FRIM) atKepong, Malaysia, and for theirkind helpwith plantidentification.R.Klein and an anonymousrefereeprovidedmany valuable comments. This study wassupportedbytheDeutsche Forschungsgemeinschaft(DFG). 230 BLUMEA —Vol. 41, No. 1, 1996 REFERENCES Davidson,D.W., & D. McKey. 1993.Theevolutionaryecology ofsymbionticant-plantrelation- ships. J.Hym. Res. 2: 13-83. Farji Brener, A.G., P. Folgarait & J. Protomastro. 1992. Associacion entre el arbusto Capparis retusa (Capparidaceae)y las hormigas Camponotusblandus y Acromyrmex striatus (Hymen- optera:Formicidae).Rev. Biol. Trop.40: 341-344. Jacobs,M. 1960.Capparidaceae.Flora Malesiana,SeriesI, Vol. 6:61-105. Jacobs,M. 1976.Capparaceae.Flora Malesiana(Addenda,corrigendaetemendanda),Series I,Vol. 7: 822. Maschwitz, U., B.Fiala,Y.F.Lee,C.K. Chey& F.L. Tan. 1989.New and little known myrme- cophyticassociationsfrom Borneanrainforests. 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