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Ulmaeeae (Urticales) (Or [1873]And Justify (Terabayashi, (Omoriand The JapaneseSocietyJapanese Society forforPlant Plant Systematics ISSN OOOI-6799 Acta Phytotax. Geobot. 47 (2): 153--168 (1996) Trichome micromorphology in Celtidaceae and Ulmaeeae (Urticales) HIROSHI TOBE and TOKUSHIRO TAKASO 1laculty oflntegrated Hiaman Studies, K.voto University, 1<Yoto 606-Ol Abstract. Trichome micromorphology was examjned by scanning electron microscopy on 29 species in all IS genera of Ce]tjdaceae and Ulmaceae. The two famiEies, like other Urticales, have both clavate (or capitate), multicellular glandular trichomes and attenuate, unicellular, non-glandular trichomes. Glandular trichomes of Celtidaceae are diverse, while those of Ulmaceae aTe always shoTt clavate, A surface of non-glandu}ar trichomes is generally micro- papillate in Celtidaccae (except in Anu?elocera) but always smooth in Ulmaceae. Trichoine micromorphology thus distinguishes CeLtidaceae from LJImaceae, and further indicates that Celtidaceae (except Ampelocet'a) are more similar to other Urticales than to Ulmaceae. However, cemparisons with patative outgroups of Urticales (i.e., certain orders of HamameLididae or Dilleniidae) suggest that trichon]e character states shared by Celtidaccae and other Urticales are plesiomorphic, and those of Ulmaceae apomorphic. Although re- lationships of Celtidaccae are stilL uncertain. ULmaceae seem likely te be in an evolutionary line distinet from all other IJrticales. An isolated position of Ampelocera is also diseussed. Key words: Celtidaceae, morpho}ogy. trichome, Urmaceae. Urticales Received Marvh 2J, l996; accepted November 5, i996 Celtidaceae Link and Ulmaceae Mirbel in Urticales have often been treated as two distinct subfamilies (or tribes), Celtjdoideae (or Celteae) and Ulmoideae (or Ulmeae), in Ulmaceae sens. tat, (e.g., Cronquist, 1981; Dahlgren, 1983; Goldberg, 1986; Melchior, 1964; Takhtajan, 1986, 1987; Thorne, 1983, 1992). Celtidaceae (or Celtidoideae, or Celteae) as defined here comprise nine genera: Ampelocera, Aphananthe, Celtis, Chaetachme, Gironniera, Lozanelta, Parasponia, Pteroceltis, and T7ema. Ulmaceae (or Ulmoideae, or Ulmeae) as defined here consist of six genera: Hemiptelea, Holoptelea, Phyllostylon, Planera, Ulm"s, and Zelkova (generic assign- ments follow Planchon [1873] and Grudzinskaya [1967i). Sweitzer (t971) strongly supported retention of the broadly defined Ulmaceae, stating that "Celtidoideae" "Uimoideae" vegetative features interconnect with and do "Celtidoideae" not justify its separation into two families. However, his included Hemiptelea and Zelkova, which are usually placed in "Ulmoideae." `tUlmoideae" An assignment of Hemiptelea and Zelkova in is supported by evidence later obtained in studies on palynology (Taka- hashi, 1989), karyomorphology (Oginuma et al,, 199e), vernation pattern (Terabayashi, 1991), and gynoecial vascular anatomy (Omori and Tera- bayashi, 1993). On the contrary, distinctness of Celtidaceae from Ulmaceae has been NII-Electronic Library Service The JapaneseSocietyJapanese Society forforPlant Plant Systematics 154 Acta Phytotax, Geobot. Vol. 47 suggested by many other ]ines of evidence, for instance, from fioral ana- tomy (Bechtel, 1921; Chernik, 1975, 1981; Omori and Terabayashi, 1993), palynology (Erdtman, 1966; Zavada, 1983; Zavada and Crepet, 1981; Zavada and Dilcher, 1986; Takahashi, 1989), flavonoid chemistry (Gianna- si, 1978), fruit wall anatomy (Chernik, 1980), and seed coat anatomy `tCeltidoideae" (Chernik, 1982). Grudzinskaya (1967) discussed that have "Ulmoideae," a greater morphologi"cal similarity to Moraceae than to and she provided the first concrete argument for establishing the family Celti- daceae, which was preposed by Link (1831). Grudzinskaya's view, howev- er, has not been accepted uniformly and is in need of reevaluation. The present paper reports on trichome micromorphology of Celti- daceae and Ulmaceae observed by scanning electron microscopy (SEM) and, based on the results, discusses whether or not it supports the separa- tion of Celtidaceae from Ulmaceae. Earlier studies on trichomes of Urti- cales have included only a limited number of species of Celtidaceae and Ulmaceae and were mainly based on microtome sections or on stereo- scopy, yet they have shown that Urticales have various types of glandular and non-glandular trichomes (e,g,, Bhat and Kachroo, 1979; Gangadhara and Inamdar, 1977; Metcalfe and Chalk, 1950; Solereder, 1908). A SEM survey has been made on trichomes of Cannabaceae (Behnke, 1984; Behn- ke and Barthlott, 1983; Dayanandan and Kaufman, 1976; Hammond and Mahlberg, 1973), and insufficiently on those of Cecropiaceae, Moraceae, Urticaceae, and Ulmaceae sens. Iat. (Behnke and Barth!ott, 1983; Hardin, 1981; Hardin and Sherman, 1987). According to Behnke and Barthlott (1983, p. 61), Urticales often show micropapillate sculpturing on trichomes, which is however not clearly developed jn the few species ex- amined of Ulmaceae sens. Iat. The micropapillate sculpturing has been "calcified known as warts" in Aphananthe, Celtis, Gironniera, and Trema (all Celtidaceae) (Solereder, 1908). In eur study we have further confirmed characteristic occurrence of micropapillate trichomes in nearly al! Celti- daceae but not in Ulmaceae, as discussed below. To hypothesize an evolu- tionary trend of trichome micromorphology, comparisons are made within Urticales and with putative outgroups of Urticales, i.e., Eucommiales- Hamamelidales (see Cronquist, 1981; Hallier, 1912; Melchior, 1964; Takh- tajan, 1980; Tippo, 1938), Fagales-Juglandales-Myricales (see Barabe et al,, 1987; Zavada and Dilcher, 1986; comparisons of trichomes made from literatures only), and Malvales (see Dahlgren, 1980, 1983; Takhtajan, 1986, 1987; Thorne, 1968, 1973, 1976, 1983, 1992). Materials and Methods Twenty-nine species from all 15 genera representing both Celtidaceae and UImaceae were investigated in this study (Table 1). Observations were made on the basis of trichomes on both abaxial leaf surface and ovary!fruit surface; basicalty one to three (or more) leaves or ovaries!fruits per speci- men were examined. Although trichomes are more abundant on the ab- axial leaf surface in general (Fig, 1), a certain type of trichome may be NII-Electronic Library Service TheTheJapaneseSocietyfor Japanese Society for PlantPlantSystematics Systematics December 1996 TOBE & TAKASO: Trichomes in Ulmaceae 155 TABLE I. Speciesstudied, collection information andtrichome micromorphologyin Celtldaceae and Ulmaceae. MaterlalobH:i'ved/Ieaf GLa"dularTTichome Non-glandulartrichome/ Taxon Collccrien r5hape Noofconstdtnentm (L),ovury(O) surfacesculptvring ceUs Ccltidaoeae An]perocefa ettenrEtta Kuhlm. VENEZUEI.A. Est Zulia, Cerro Cinco de oLLOoLOLOLLOLLOLLOoLL?1.cl, 7)=10S.9??S-14S-1[14.12,????1-4SmoothSmoothMicropap.Micropap･Micmbpnp,MicropaP･SmoothSmoeth,trar.niicropap. Julio. Ste.verntark et al. 12S29S CMo), A. rt"iiii Klotzsch PERU. Oxupampu. Pvov. Pasco. Genay tp1,cl?p]PL1.cl, 4?ilO(k{o). AphanantiJeaspera CultivatecF,Kenmza-･uPtitk,'Iakyo.Japai. CThunb,}Planch, Tlakasv s, n, (MAK 23S444). A, czarpidata (Blume) PEOPLE'SREPUBLICOFCHINA. PIanch.A. Hainan, C. -L Lei 831 ('rl). rnonoica CHemsl.) MEXICO VerH Ciui, lpsTuxtlas, Dirio J,-F, Lerov s. n. in lgg7 Chafn} Celtis austraiis L, Cultivated, Botanisches Garlen, Zurich. En(lress s. n. in 19S4 (KYO). C. boninensis KoidT, JAPAN.Chichi-jima,Tekyo,Novoucher, cpT.cll.ci??cpcpcPcp C. sinensiy Pe[s. Cultivated.KomazawaPfirk.Tok)'o,Japan, I'ukaso s. n. In IL)8S CMAK 22486fi), C. spinosa Spreng. ARGENIINE, ISkm NE de CorrLentes. MicroPUP･SmeothMicropap.Micropnp,ismoeth Scitiitisn22SM(c['rEs). Chactachmeari,seata Cuttlvated.NationatBotunicGarden.Pretoriu, Planch. Republk,ofSeuthAfrica.Bttisinhas3577CKYO). KENYA,Muthaiga,ncurNuirobi. Piemeisei & Kepkan 21 (A), Gironnieraeeltidijblia FIJI. Nuitasirf, Vitj Lcvu. 1'arks 20074 Gaudich, (MAK).(/AMBOD[A, G, subaequaiis Planch, Kampet. Vidai S076 ('rNs). (?)5(?)S-6 Micropap.Mieropap,Mic[opap. G, ne-,osa Planch. THAILAND. Kh"o Sabap Nut. P"ik, Chanthtihuri. fiikuoka & iro T-34P3] (KYO). SINeAPORE. Muc Ritchie RcscrvoiT (?) Forcst. Samsuri Bin Ahmad s. n, in l9R7. No vouchcr, Lozcuteiiaenantiophyita MEXrCO, Clh]"pas, Neitl 5448 (Mo), LO s,cl 4 MIcropap.,'rnr. sm[)nih (Donn Sm,) Kil]ip & Morton L. permottis Killip & BOLIVIA. PFev. Murillo, Dpto La Paz. LOLOLOLLz.oLOLOLOs,cl,LctLcll.cL1.cli.cl?s.ci.g.cls.cl4.67-9 Micrapap.isrnooth Mortan Snlenton JJI33 (Mo}. Parasponia rigida Mcrr. NEW GUTNEA. Gatore s. n. in 19S3 C?}??1-7?444Mierupep,lsmuoth & Perrv (KYO).PEOPLE'SREPUBLICOFCHIpt'A. Preroceitis tararinowii Miciepap,ismuorh Maxim. Jiansu?iev., Nanjing. F. X. Liit S93 {n). Trema taniarkiana B]umc U.S.A. Monroc Co., Hnrida. C.boJe}, er Micropap,isrnooth al, Y25S (eH). T, micrantha Bhtme ARGENTrNIE.Ccmientes.Sc;Jin,ni2?S7i MicrnpupSmeuthSmoothSnloothSmooth CCTTES),JAPAN.C/hicbi-tim".Tekyo.Nuvouchei. T. oricntuiis Blume Ulmaceae Hemipteteadavidii C'ultivated. MotTis Arhoretum, U,S.A, Planch. KSein s. tL. in 1984 {Kyo). th)tuprett'atntagrij1]liaC/ultivated,l･'air[h[ldTropicn]Gardeii, MO). Planch. Flerriu. IJ.S,A. -latso,, 1937CFI'G Fhviios'tvtonbratiliensis MEXICO. Dz+bilchaltum. Y-catan, rvores Capan. ex Benth. & g575CXAL). Hook. f･ Plarrera agttatica J, F. U.S.A, Peurl RiverBusin. Louisiana, LOo s.cls.c] 44 SmoothSmooth Grnel, 7'kien s. n. {KYO). [Jtmirs elavidiana Cu]tix,ated,Nikk[)BotanicalGarden. Planch. tJniv. of Tokvo. Yoshida s. n. in 19Hl, No voucher. U, Iaciniata Mavi Cultivated, Nikko Botanicnl Garden. Univ. of oLOoLO s,cls.c]s,c]s.ci4C]-)444 Smoot]]Sn]oothSmc)othSrnooth Tekvo. Yoshida
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