THE TAXONOMY, DISTRIBUTION AND ECOLOGY OF THE EPIPHYTIC MALESIAN ANT-FERN LECANOPTERIS REINW. (POLYPODIACEAE) H. Gay1, E. Hennipman2, C. R. Huxley1& F. J. E. Parrott3. 1: DeptofPlantSciences,SouthParksRoad,UniversityofOxford,0X1 3RA,U.K. 2: Zweerslaan34,3723HPBilthoven,TheNetherlands. 3: MinistryofAgriculture,FoodandFisheries,WhitehallPlace,London. EFFECTIVEPUBLICATIONDATE 31 MARCH 1994 : Abstract Lecanopteriscomprises13epiphyticspecieswithexpandedrhizomeswhichshelterantsinamutualisticassociation. Taxonomicdescriptionsandakeyaregiven. InsubgenusMyimecopteris,L.sinuosaoccursthroughoutMalesia,inmost m habitatsbelow800 a.s.l.,especiallyintheant-epiphytecommunitiesofdryforest. LecanopterisCrustaceaisconfined toBornean, SumatranandMalaysianlowlanddipterocarpcanopies. Itssisterspecies,L.sarcopusoccursinintactand disturbedforestfrom400-1200minthePhilippinesandSulawesi.LecanopterismirabilisisfoundinNewGuinea,Ambon andSeram,andislocallyabundantinundisturbedmid-montaneforest. SubgenusLecanopterisconsistsofthreegroups, typifiedbyL.curtisii,L.pumilaandL.darnaedii.LecanopteriscurtisiiformsdistinctracesinNewGuinea,thePhilippines, Sumatra,JavaandBorneo.Itisararememberofintactorolddisturbedhillforestbetween400mand1200m.TheL.pumila groupcontainsthreeendemicsoflowermontaneforestinSulawesi:L.celebica,L.carnosaandL.balgooyi,andaPhilippine endemic,L.luzonensis.Lecanopterispumilaisfoundinmid-montaneforestandridgetopsinMalaysia,SumatraandBorneo, whereitformsdistinctraces. TheL.darnaediigroupisendemictoSulawesi;thethreespeciesareallopatricandfoundin undisturbedmid-montaneforest. Myrmeco-epiphyticcommunities, inhabitedbyIridomyrmexcordatus,arefoundin BomeanheathforestandNewGuineansavannah. Theantscontributetothespreadofant-epiphytesbyplantingtheir propagulesintheantcartonsurrounding!,sinuosa.TheonlyecologicalcharacteristiccommontoLecanopterisapartfrom myrmecophytismisheliophily,confiningindividualstohabitatswithopencanopiesortreecrowns. Nopreferenceis manifestedforhostspecies,butLecanopteristendstogrowonrough-barkedtrees. Introduction Theant-associatedferngenusLecanopterisReinw. comprises 13 specieswhich arelargelyconfinedtoMalesia, andis characterisedby ahighly modifiedrhizome which shelters ants. Despite its remarkable biology and morphology, the genus remainedinrelative obscurityfor 150years afteritsfirstdescriptionby Reinwardt in 1828. Recently it has been the simultaneous subject ofa D. Phil, thesis and a taxonomic monograph (Gay 1990; E. Hennipman unpub.). This article provides taxonomic descriptions based on field and herbarium material and a detailed account ofthe ecology and distribution ofLecanopteris. Theantassociation,rhizome structureandevolutionofLecanopterishavebeen described by Gay (1990, 1991, 1993, inpress) and Gay & Hensen (1992). Every member ofthe genus possesses a hollow or expanded rhizome which is used as a domatium by ants. Rhizome form varies from a solid, arched domatium {L. mirabilis(C.Chr.)Copel.)todimorphismofsolidandhollowrhizomes(L.sarcopus 294 295 & Teysm. Binnend.), a single gallery (L. sinuosa Wall, ex Hook., L.pumila Bl.) or a double gallery (L. darnaedii Hennipman) (Gay 1993). In a given habitat, a constant ant species from the genera Crematogaster orIridomyrmexnests, rears larvaeanddepositsdebrisintherhizome, andmaybuildcartonrunwaysandkeep coccids in the vicinity. When the fern's geographical or altiditudinal range is widerthanthatoftheant,anotherantspeciesreplacesthemajorinhabitantbeyond thelimitsoftheformer'srange,showingthatinthismutualismhost/antspecificity isafunctionofecologyratherthanevolution. Antfaecesanddebrisdumpswithin the rhizome provide a source ofnutrients forLecanopteris (Gay inpress). The mutualism is based on acquisition ofa nest by the ants, and nutrient uptake for the ferns. Materials, Methods and Sources Ecological data were obtained from field observations in Papua New Guinea, Peninsular Malaysia, Borneo and Sulawesi for eight species of Lecanopteris(L. mirabilis,L. Crustacea,L.pumila,L. curtisiis.l.,L. sarcopus, L. sinuosa, L. celebica and L. darnaedii). Field sites are listed in Appendix 1 and shown in Fig. 1. Data were recorded using two proformas: the first described each individual Lecanopteris recorded at a site, and the second recordedthe habitat, following the technique developedby Webb, Tracey and Williams (1976) for comparative physiognomic analysis of Australian and New Guinean forest types. Herbarium specimen labels yielded limited information on habitats; relevant collections are appropriately cited. Herbarium specimens of all species, and wild and cultivated plants where possible, were examined for the taxonomic descriptions. Spore, sporangium and venation characters are from Hetterscheid and Hennipman (1984), Hennipman (1986) and Hennipman and Verduyn (1987). Other authors are cited where appropriate. Specimens from the following herbaria were used: Kew (K); the Natural History Museum (BM); Lae (LAE); Port Moresby (UPNG); Singapore (SING); Kepong (KEP); Leiden (L); Berlin (B); Utrecht (U); Bogor (BO); New York (NY); Munich (M) and Michigan (MICH). The distribution maps are based onherbariummaterialandareafterHennipman(1986, andunpub.). Thefollowing abbrevations are used in the text: G. = Gunung (mountain); S. = Sungei (river); s. n. = un-numbered herbarium specimen; s. d. = specimen without date. Taxonomic Account Lecanopteris Reinwardt Flora3:48(1825);OnychiumcarnosumReinwardt,inSyllog.Plantarum2:2(1824),nomilleg.nonkaultuss (1820);Copeland,Gen.Fil.:205(1947);Holttum,RevisedFloraofMalayaVolume2,FernsofMalaya:208 (1955);Hennipman,in KewBull.41: 783(1986); Hennipmanand Verduyn,Blumea32 : 313 (1987). 296 Type Lecanopteriscarnosa(Reinw.)Blume. : Myrmecophila(Christ)Nakai,inBotMag.Tokyo43:6(1929)nomilleg.nonRolfe(1917). Polypodiumsect. MyrmecophilaChrist,Farnkr.: 12(1987). MyrmecopterisPic.Ser.,inWebbia31:239(1977). Lectotype :Lecanopterissinuosa(Wall,exHook.)Copel.,selectedbyPichiSermolli. Epiphytic orvery rarely epilithic ferns ofmoderate size. Rhizome forming adomatium,creeping,muchtolittle-branched; monomorphic,rarelydimorphic or subdimorphic; hollow with one ortwo gallery systems, or solid and arched, pale green, opalescent or glaucous when living, black when dead; glabrous, spiny, or bearing filamentous hairs or coralloid excrescences (subg. Lecanopteris) or translucent, dark-centred, circular, dense or sparsely set peltate scales (subg. Myrmecopteris). Always ant-inhabited. Phyllopodia usually distinct, hollow and prominent or solid and unprotruding. Stipes absent to elongate, glabrous, often dark brown. Fronds pale to dark green, simpletodeeplypinnatifid,chartaceoustocoriaceous, articulatetophyllopodia, distichous along rhizome, erect to ascending. Aborted fronds sometimes presentas spines orexcrescences in subg. Lecanopteris. Venation a complex network of areoles with included free veins. Sori rounded, immersed in the lamina, either in a single row on either side of the midrib and costae (subg. Myrmecopteris) or on round, oval or boat-shaped extra-marginal projections (subg. Lecanopteris). Sporangia on triseriate stalk; annulus longitudinal, interrupted and consisting of c. 13 thickened cells. Usually 64, rarely 16, spores per sporangium. Spores monolete, orange, smooth and translucent, filamentous in L. mirabilis. Subgenus Myrmecopteris: Rhizome hollow or solid, densely covered with orbicular, dark-centred peltate scales with translucent margins which hide the rhizome colour. Rhizome does notblacken with age. Sori always immersedon the lamina. Rhizome usually, but not always, much-branched. Species: L. mirabilis, L. sarcopus, L. Crustacea, L. sinuosa. Subgenus Lecanopteris: Rhizome always hollow, glabrous, except for an indumentum ofscattered branched hairs and dark brown scales at the apices. Rhizome bright pale green, opalescent or glaucous when young, blackening with age. Sori immersed in re-curved extra-marginal lobes, except in L. spinosa andL. balgooyi, wherethey are are immersedon thelamina. Rhizome always much-branched. Species: L. curtisii, L.pumila, L. celebica, L. carnosa, L. luzonensis, L. balgooyi, L. spinosa, L. holttumii, L. darnaedii. 297 Key to the Species la. Rhizomewithadenseorscatteredcoveringofpeltatescaleswhichhidetherhizomecolour (subg.Myrmecopteris) 2 lb. Rhizomemacroscopicallyglabrous,brightgreenwhenyoung,blackeningwithage(subg.Lecanopteris)..5 2a. Rhizomesolid,archedandplate-like;scalesthinlyscatteredoveritssurface;frondspinnatifid I.L.mirabilis 2b. Rhizomecompletelyorpartlyhollow,notarchedandplate-like;denselycoveredwithscales;fronds pinnatifidorentire 3 3a. Rhizomedimorphic,consistingofsolidcylindricalfrond-bearingmainbranchesandhollow,ovate, frondlesssidebranches;peltatescalesblack-centred. Frondspinnatifid 2.L.sarcopus 3b. Rhizomemonomorphic,hollowexceptfortheapical2-3cm;peltatescalesblackorbrowncentred. Frondspinnatifidorentire 4 4a. Peltatescalesbrown-centred. Frondspinnate;rhizomemuch-branched 3.L.Crustacea 4b. Peltatescalesblack-centred. Frondsentire;rhizomemuchorlittle-branched 4.L.sinuosa 5a. Rhizomewithawaxysheen,glaucous,neverspiny;extra-marginalsoriboat-shaped 5.L.curtisii 5b. Rhizomegreen,withscatteredordensespinesderivedfromabortedfrondsorepidermal outgrowths,holloworsolid,orwithcoralloidexcrescencesderivedfromabortedphyllopodia, or spinelessbutbearinganindumentumofglandularhairs 6 6a. Spinesorexcrescencesderivedfrommodifiedundevelopedfrondsandreplacingsome fronds,intworowsalongtherhizome. Asinglegallerysystemwithinrhizome. Phyllopodiahollow,protruding 7 6b. Spinesderivedfromepidermaloutgrowthsanddenselycoveringrhizome. Twogallery systemsinrhizome. Phyllopodiasolid,notprotruding 11 7a. Spineshollow. Frondsentiretopinnatifid 6.L.balgooyi 7b. Spinessolid,orreplacedbycoralloidexcrescences. Frondspinnatifid 8 8a. Rhizomecoveredwithshortcoralloidexcrescences1-3cmlong,derivedfrom modifiedundevelopedfronds 7.L.carnosa 8b. Rhizomewithamoreorlessdensecoveringofsolidspines,no excrescences 9 9a. Largestoutplants,rhizomediameter2.5-3.5cm. Frondsupto 1 mlong. Spinesabundantonrhizome 8.L.celebica 9b. Smalltomoderatesizedplantsrhizomediameter1.5-2.5cm. Frondsnot morethan45cmlong. Spinesverysparse, neverabundant 10 10a.Rhizomebearingadenseindumentumofbranchedhyalinetobrown glandularhairs. Luzon 9.L.luzonensis 298 10b. Rhizomeapiceswithanindumentumofscatteredbrownglandular hairsandscale. WestMalesia 10.L.pumila 11a. Frondsentirewithsoriinsertedonlaminaintworowson eithersideofrachis 11.L.spinosa 1lb. Frondspinnatifidwithsoriimmersedonextra-marginallobes orsessileonlamina 12 12a. Veinsstronglysclerified,appearingblack. 12.L.darnaedii 12b. Veinsslightlysclerified,appearinggreen. 13.L.holttumii Subgenus Myrmecopteris 1. Lecanopteris mirabilis (C. Chr.) Copel. Fig. 2. Univ.Calif.Pub.Bot. 16: 123(1929)('mirabile').,Gen.Fil.:205(1947). Myrmecopterismirabilis(C.Chr.) Pic.Ser.,inWebbia31;237(1977).PolypodiumimbricatumKarsten,inAnn.Bot.Jard.Buit.12:168(1895), nom.illeg.nonLiebm.(1849).PolypodiummirabileC.Chr,.,Ind.Fil.:545(1906),nom.nov.proPolypodium imbricatumKarsten(1895)nonLiebm.(1849). PleopeltisimbricataAlderw.,inBull.Dept.Agric.Ind.Neerl. 27:3(1909),nom.nov.proPolypodiumimbricatumKarsten(1895)nonLiebm.(1849).Polypodiumulotheca Brause,inBot.JahrbSyst.56:204(1920). Myrmecophilaulotheca(Brause)Ching,inSunyatsenia5(4):260 (1940). Myrmecopterisulotheca(Brause)Pic.Ser.,inWebbia31:237(1977). Type:Ledermann12641,New Guinea(B). Rhizome solid, arched and plate-like, 10-20 cm wide, forming a domatium between the dark-coloured rhizome underside and the host tree surface, ant- inhabited, branching sympodial and occasionally lateral, with scattered dark- mm centred, orbicular, peltate scales 1-1.5 diam., denseron therhizomeedges and underside. Phyllopodia solid, not prominent. Stipes dark brown, 10-30 cm long, basaldiameter2-5 mm. Frondsdarkgreen,deeplypinnatifid,wingedattheirbases, 10-15 x 30-90 cm, glabrous, coriaceous, monomorphic; apex and lobes rounded, lobes perpendicular to the rachis, basal lobes narrower than median ones; veins forming a series of areoles with a freely branching recurrent vein. Sori deeply mm immersed on lamina, 2 diameter, circular, in a single row on either side ofthe mm the main veins of the lamina lobes, forming projections high on the upper 1 frondsurface. Sporesfilamentous,75 x60jitm;filaments 1300-1900um, 16spores per sporangium. Representativespecimens: NewGuinea Croft539, Bululo-Asekiroad,20kmeast : ofAseki, Morobe Province, montane rain forest, 2300 m asl. (LAE); Womersley NGF 24942, Awande, nr. Okapa, Eastern Highlands Province, Castanopsis rain forest, 5800 ft asl. (LAE); Gay 960, Mt Mon, Milne Bay Province, mid-montane rain forest (K). & 2. Lecanopteris sarcopus (Teysm. Binnend.) Copel. Univ.Calif.Publ.Bot.16: 123(1929). DrynarialomarioidesJ.Sm.,inHook.J.Bot.3:397(1841),nom.nud.. Polypodium lomarioides kun/e ex Mett., in Ahb. Senckenb. Naturf. Ges. 2: 102 pi. 2 (1856). Pleopeltis 299 Fig. 2. Lecanopteris mirabilis A: maturefertilefrond D: peltatescales B: rhizome E: venationoffertilefrond C: rhizomeapex F: venationofsterilefrond DrawingbyJenniMarsh 300 lomarioides(KunzeexMett.)Copel.,in Univ.Calif.Publ.Bot. 16: 123 (1929).Myrmecopterislomarioides (KunzeexMett.)Pic.Ser.,inWebbia31:240(1977). Type:Cuming243,NuevaVizcaya,Luzon,Philippines (iso in BM, L, P, US). Polypodium sarcopus Teysm. & Binnend., in Natuurk. Ned. Ind. 29: 241 (1867). Pleopeltissarcopus(Teysm.&Binnend.)Alderw.,inBull.Dept.Agric.Ind.Neerl.27:3(1909).Myrmecophila sarcopus(Teysm.&Binnend.)Ching,inSunyatsenia5(4):259(1940). Myrmecopterissarcopus(Teysm.& Binnend.) Pic. Ser., in Webbia 31: 240 (1977). Type: Teysmann andde Vries 75, Manado, Minahassa, Sulawesi(isoinBM,K,L).PolypodiumsauviniereiBaker,Ann.Bot.(1891),480. Type:DelaSauviniere382, "routedeSukuraSawan Minahassa,Sulawesi(K). , Rhizome creeping, dimorphic, consisting of solid, cylindrical, frond- bearing rhizomes 1-2 cm diameter which produce hollow, frondless lateral branches tapering at their apices, 2-3 cm diameter and forming an ant- inhabited domatium with a dark inner wall, much-branched; densely covered mm in translucent, orbicular, dark-centred, peltate scales, 1-2 diam. Phyllopodia solid, prominent, 1-1.5 cm high. Stipes 10-30 cm long, dark brown. Fronds mid-green, deeply pinnatifid, winged at their bases, 20-140 cm long, glabrous, coriaceous, monomorphic; apex and apices oflobes ovate; veins forming a series ofareoles with a freely branching recurrent vein. Sori mm deeply immersed in lamina, 1-2 diameter, circular, in a single row on either side of the rachis and main veins, forming projections on the upper frond surface. Sporangia c. 500 |Lim long. Spores biconvex. Representative specimens: Sulawesi: Koorders 17115b, Minahassa (L); Hennipman 6079, alongMalili- Soroakoroad, nrWasuponda, S Sulawesi,440 m asl. (L); Gay 1262, Lake Matano, nr Soroako. Philippines: Cuming 241, 242, Luzon (K). 3. Lecanopteris Crustacea Copel. Univ.Calif.Pub.Bot.12:406(1931).PolypodiumlomarioidesKunzeexMett.,Farng.1,Polypod.Tab.2,Figs 18-19(1856). Pleopeltislomarioides(KunzeexMett.)Moore,inInd.Fil.:78(1857). PhymatodesCrustacea (Copel.) Holttum,FernsofMalaya: 190(1955). Type:Burchard158,UC.391610(UC). Rhizome creeping, hollow, forming an ant-inhabited domatium with a dark innerwall, much-branched, sub-dimorphic, 3-5 cmdiameter; thicklycoveredin mm orbicularpeltatescales -2 diameterwithferruginouscentresandtranslucent 1 edges. Phyllopodia solid, not prominent. Stipes 10-15 cm long, dark brown. Fronds mid-green, deeply pinnatifid, wingedattheirbases, 30-60cmlong, lobe and frond apices rounded, fertile fronds more deeply lobed than sterile fronds; veins forming a series of areoles with a freely branching recurrent vein. Sori circular, deeply immersed on lamina in a single row on either side ofthe rachis mm and main veins, forming projections high on the upper lamina surface. 1 Spores biconvex. Representative specimens: Sarawak: Richards2259, Mt Dulit, rain forest, 300 m asl. (K). Sumatra: de Wilde & de WildeDuyfjes 19464, G. LeuserForestReserve, Acheh, recently logged forest (L). Kalimantan: Kostermans 9793, Mentawi 301 River, Balikpapan Dist., low wetland (BO). 4. Lecanopteris sinuosa (Wall, ex Hook.) Copel. Fig. 3. Univ.Calif.Pub.Bot. 12: 123(1929). PolypodiumsinuosumWall,exHook.,Spec.Fil.5: 61,pi.284 (1864) Pleopeltis sinuosa (Wall, ex Hook.) Beddome, FernsofBritish India pi. 8 (1865); Alderw., in Bull. Dept. Agric. Ind. Neerl. 27: 3 (1909). Phymatodes sinuosa (Wall, ex Hook.) J. Sm., Ferns British and Foreign, 2nd ed.: 296 (1877). Myrmecophilasinuosa (Wall, exHook.) Nakai exIto, in J. Jap. Bot. 11: 98 (1935). Myrmecopteris sinuosa (Wall, ex Hook.) Pic. Ser., in Webbia 31: 240 (1977). Type: Wallich 2231, (K). Rhizome hollow, forming an ant-inhabited domatium with a dark inner wall, stout, creeping, 1-2 cm diameter, little or much-branched, densely covered with mm orbicular, dark-centred peltate scales with translucent margins 1-2 diam. Phyllopodiahollow,prominent, 1-1.5cmhigh. Stipesbrowntogreen,3-8cmlong. Fronds mid to pale bright green, entire, occasionally slightly crenate (especially fertile fronds), winged at their bases, glabrous, 2-3 x 15-30 cm, coriaceous, monomorphic, apex rounded; veins forming a series of large areoles with a branchingrecurrentvein. Soriimmersed,circulartorarelyelliptical,inasinglerow mm onthelaminaoneithersideoftherachis, 3-5 diameter,formingprojectionson the upper lamina surface. Sporangia c. 300 jum long. Spores biconvex. Representative specimens: New Guinea: Croft 496, nr Agamoia, Fergusson Is., m Milne Bay Province, disturbed lowland forest, 50 asl. (LAE); Howcroft, Lae m 64023, Wutung, Vanimo Subdistrict, onhooppine, 800 asl. (LAE). Peninsular Malaysia: Gay1208, banks on S. Tahan, TamanNegara, 30masl. (K). Sulawesi: Darnaedi 1851, Lake Matano area, Soroako, S. Sulawesi (BO,L) Subg. Lecanopteris. 5. Lecanopteris curtisii Baker Fig. 4. J.Bot.19(n.s.)10:366(1881).LecanopterissaccataAlderw.,inBull.Jard.Buit.2(23):14(1916). Type: Curtis, Sumatra,s. n.,s. d. (K). Lecanopterisphilippinensis Alderw., in Bull. Jard. Bot. Buit. 2 (1); 8 (1911).Type:Elmer10491,TodayaDistrictofDavao,MtApo (L,K, Piso). Lecanopterisdeparioides (Ces.) Baker, inJ. Bot. 19n.s. 10: 366 (1881). Polypodiumdeparioides Christ,Farnkrauteder Erde: 116(1897),nom.illeg.nonBaker(1879). DavalliadeparioidesCes.,Fel.diBor.: 13(1876). Lecanopteris incurvataBaker,inAnn.Bot.8(30): 123 (1894).Type:Hancock88,Between Kroeand Liwa,Barisan Mts, Sumatra (K). Lecanopteris macleayi Baker, Malesia 2: 244 (1886). Pleopeltis macleayi (Baker) Alderw., in Bull. Dept. Agric. Ind. Neerl. 27: 2 (1909). Polypodium barisanicum Alderw., Malayan Ferns,: 627(1908),nom. nov. proLecanopterisincurvatum Baker(1894) nonPolypodiumincurvatum Blume(1828).PolypodiumnaviculareAlderw.,MalayanFerns,:627(1908),nom.nov.proLecanopteris curtisiiBaker (1881) nonPolypodium curtisiiBaker (1881). Polypodiumpatelliferum Burck., in Ann. Jard. Bot. Buit. 4: 96. Tab. 7 (1884). Rhizomecreeping,hollow,forminganant-inhabiteddomatiumwithadarkinner wall, much branched, 2-3 cm diameter, glaucous with a waxy sheen, glabrous exceptforascatteringofscalesattheapex. Phyllopodia prominent, 1-1.5cmhigh, hollow. Stipes 10-25 cmlong, darkbrown. Fronds mid-green, 10-20 x 30-70cm. 302 E Fig. 3. Lecanopteris sinuosa A: fertilefrond D: peltatescales B: rhizome E: venationofsterilefrond C: rhizomeapex F: venationoffertilefrond DrawingbyJenni Marsh