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Cuticle Micromorphology of Agathis Salisbury

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Cuticle Micromorphology of Agathis Salisbury Int. J. Plant Sci. 154(1):187-225. 1993. ? 1993 by The University of Chicago.All rightsreserved. 1058-5893/93/5401-0018$02.00 CUTICLEMICROMORPHOLOGY OFAGATHIS SALISBURY RUTH A. STOCKEY'AND IAN J. ATKINSON Departmentof Botany, University of Alberta,Edmonton, Alberta T6G 2E9, Canada Cuticle micromorphologyfrom all 21 species of the SouthernHemisphere conifer genus Agathis Sal- isbury was studied with scanning electron microscopy. Externaland internal features of abaxial and adaxial cuticles are characterizedfor the three recognizedsections of the genus. Externalcuticle surfaces of all species are undulatingand exhibit Florin rings and stomatal plugs, with most species being hypo- stomatic. Sunken stomata of various orientationsoccur in discontinuousrows and have three to nine subsidiarycells, fourbeing the common number,and bilobedpolar extensions. Epidermal cells are usually rectangular,but vary considerablyeven on one leaf. The cuticle on guardand subsidiarycell surfacesis smooth to striatedand pitted and can be useful in identifyingtaxa. Distinguishingcharacters useful at the levels of genus, section, and species are outlined. Micromorphologicalfeatures distinguishing Agathis from Araucariainclude the undulatingepidermal cell surfaces,the presence of Florin rings, stomatal orientations,and bilobed polarextensions. Subsidiary cell number,shape, and morphologyand stomatal orientationsare the best charactersto use when distinguishingfossil araucariancuticles from those of broad-leavedpodocarps. Introduction Materialand methods The family AraucariaceaeStrasburger contains Leaves from all 21 species of the genusAgathis two extant genera, Agathis Salisbury and Arau- were examined from preservedor herbariumma- caria de Jussieu, that are mostly confined to the terial (table 1). Leaves collected in 1977 and 1981 Southern Hemisphere. The family probablywas showed no cuticulardifferences between herbar- more diverse and widespread during the Meso- ium materialand leaves preservedin FPA (5 mL zoic, when Araucaria extended well into the formaldehyde,5 mL propionic acid, 90 mL 50% Northern Hemisphere (Stockey 1982; Stockey et ethanol). The only difference observed was the al. 1992b). The fossil record of Agathis, so far, absence of stomatal plugs on some dried herbar- can only be confirmed in the Southern Hemi- ium material. Some plugs are usually present in sphere(Florin 1963; Stockey 1982;Cantrill 1989). this material, but most probablywere lost when Leaves of extant species of Agathis were studied the leaves were pressed and dried. with light microscopy (LM) by Florin (1931), Cuticles were preparedby cutting the leaf into Cookson and Duigan (1951), Carr and Carr (in sections with the leaf marginintact, leaving both Hyland 1977), and Cantrill (1989). abaxial and adaxial epidermis attached (Stockey Cuticle micromorphologyof external surfaces and Ko 1986). All preparationswere immersed of some Agathis species was studied with scan- in 20%chromium trioxide solution for 96 h (Al- ning electron microscopy (SEM) by Page (1980). vin and Boulter 1974). All other protocol for Later,Stockey and Taylor (1981) examined three preparationfollows Stockey and Ko (1986). species using SEM of both internal and external Cuticles were washed in distilled water, air- cuticle surfaces.Since these studies,SEM has been dried, and mounted on stubs with silver con- used sporadicallyto compare fossil Agathis spe- ductive paint. Specimenswere sputtercoated with cies to a limited number of extant taxa (e.g., Big- 150 A Au on a Nanotek Sputter Coater and ex- wood and Hill 1985; Cantrill 1989). amined with a CambridgeStereoscan 250 at 20 In this article we use SEM to characterizethe kV. micromorphologyof both internal and external We found that in some species cuticularthick- cuticles of all 21 species of the genus Agathis. ening extended to the level of the hypodermis, Species delimitation in this group of closely re- and clean cuticles showing only the firstcell layer lated taxa has been notoriously difficult (Whit- were difficult to obtain. Descriptions disregard more 1980; Whitmore and Page 1980). Taxon- what is obvious extraneousdebris on cuticle sur- omy of the genus is examined in light of cuticle faces. Photographswere taken with the long axis micromorphology,and these data are used to es- of the leaf parallel to the long axis of the plate, tablish generic charactersand distinguishthe ge- and stomatal orientations are given with respect nus from Araucariaand the broad-leavedpodo- to that axis. Classificationfollows that of de Lau- carps. The usefulness of these data for benfels (1988). We have chosen to list the species paleobotanicalinvestigations is elucidated. in alphabeticorder to eliminate any preconceived ideas about what cuticular features were char- acteristicof the sections. Becauseof the closeness ' Author for correspondenceand reprints. of these taxa to one another and the lack of tax- Manuscriptreceived July 1992; revised manuscriptreceived onomic consensus as to the major divisions with November1992. the genus, we preferredto later assess the rela- 187 S c;.;i:v3 itg 8 , it t~~~~~~~~(39 t Q , rr Q E v 3 t e n C> r D (= o t5 <<v Q;n zn < ? 0<z ? Q w9 D t Q ?E sQ < Q Q V ChV t9 VCJEO) )t r .. , vX rCh t X r r ., tP., .D ,, xO < t<<DE<>tE<ttAl D"C < > ez n.fB C zS;Zoz z zca . C1 ve r >~~~~~~~~~~~~e......... X===X===......... en .. .. Q . .............~~~~~~~~~~~~ C. : . ll3 C Eo 3 > : : * : : : : e Q : . Q . .3 e e UD = *'':^) ta i . D t > t X > m * E * 3 >> .en c)~~~~~~~m m3Nmm mmmc C) "Cm 188 tWJ~~~~~~~~~~~~~~~~~~~~A \% D - -Ae t I'V Figs.1-11 Agathis atropurpurea.Fig. 1, Inner view, abaxial cuticle, region of stomatal apparatus,with four subsidiarycells (SC); x 850. Fig. 2, Inner view, abaxial cuticle, stomatal rows; x 145. Fig. 3, Inner view, abaxial cuticle, stomata, showing variablesubsidiary cell number; x 250. Fig. 4, Outerview, abaxialcuticle, showingFlorin rings around stomata and undulating epidermal cell surfaces; x 170. Fig. 5, Inner view, adaxial cuticle, showing epidermalcell wall flanges; x 210. Fig. 6, Inner view, adaxialcuticle on epidermalcell surface;x 2,100. Fig. 7, Outerview, abaxialcuticle, showingstomatal plug morphology; x 2,300. Fig. 8, Inner view, abaxial cuticle, stomatal apparatuswith five subsidiarycells; x 850. Fig. 9, Inner view, abaxial cuticle,showing bilobed polarextension; x 900. Fig. 10, Innerview, abaxialcuticle, showing two stomatasharing eight subsidiary cells; x 550. Fig. 11, Inner view, abaxial cuticle on guardcell surface; x 4,500; F = flangeof cuticle between guardcells. 189 .sy ~~~~~~~~~~~~kP14# _ ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~'I >.~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~. Figs.12-24 Agathis australis. Fig. 12, Inner view, abaxial cuticle, adult foliage, region of stomatal apparatus,with four subsidiarycells; x 925. Fig. 13, Outer view, abaxial cuticle, adult foliage, showing Florin rings and undulatingepidermal cell outlines; x 115. Fig. 14, Outer view, abaxial cuticle, juvenile foliage, showing stomatal plug; x 1,300. Fig. 15, Inner view, abaxial cuticle, juvenile-foliage, showing stomatal rows; x 165. Fig. 16, Inner view, abaxial cuticle, adult foliage, showing stomatal rows; x 130. Fig. 17, Innerview, abaxialcuticle, juvenile foliage, showingcuticle on guardcell surface;x 3,500. Fig. 18, Inner view, abaxial cuticle, juvenile foliage, stomatal row, with large and small stomatal apparati;x 350. Fig. 19, Inner STOCKEY & ATKINSON-AGATHIS CUTICLE 191 tionships of these taxa. All stubs are deposited in ly oriented, however, polar extensions are con- the University of Alberta PaleobotanicalCollec- fluent with subsidiary cell wall flanges, and the tion (UAPC-ALTA). Specimensjointly collected bilobed nature of the extension is not visible (fig. by McPhersonand Stockey (table 1) were studied 1). The cuticle on the guardcell surfacesis rugose from duplicates of those housed at the Missouri and pitted near the stoma (fig. 1 1), with a lon- Botanical Garden, St. Louis (MO). gitudinal crease present near the subsidiary cell wall flange (fig. 1). The flange of cuticle between Results guard and subsidiary cells is thick and rugose (figs. 1, 10). AGATHISATROPURPUREA (FIGS. 1-11) Epidermal cells are irregularin shape, often Adult leaves were taken from a tree in the rain broaderthan long on adaxialsurfaces (fig. 5). Cells forest of the Queensland Mountains, south of are more elongate between stomatal rows (fig. 2), Atherton at 1,130 m (table 1). Leaves are oval- but due to crowdingmany irregularshapes result lanceolateto oblong-elliptic(Silba 1986), 3-7 cm (figs. 2, 3). Epidermalcell wall flangesare straight long and 0.5-2.0 cm wide, with short petioles to curving but on abaxial surfaces appear irreg- (Hyland 1977). Stomata were observed only on ular because of cuticle extension to the hypoder- abaxial surfaces. mal level (fig. 3). Cuticle on the epidermal cell The external cuticle surface is distinctly un- surfacesis rugose (fig. 6). dulating,with epidermalcell outlines clearly vis- ible (fig. 4). Stomata are sunken and surrounded AGATHISAUSTRALIS (FIGS. 12-24) by Florin rings (Buchholz and Gray 1948). Sto- Both juvenile and adult leaves of this species matal plugs are rare in the pressed herbarium were examined. Adult leaves were taken from a material; however, when present they are com- large tree at 90 m elevation, Bay of Islands, New posed of very short rods (fig. 7). Zealand, and at the forestry station at Imbil, Inner cuticle surfaces show crowded stomata Queensland(table 1).
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