231

THE ANATOMY AND MORPHOLOGY TASMANIAN CUSHION SPECIES

Neil Gibson

(with one table, four text-figures and one plate)

A study of the anatomy and morphology of four Tasmanian cushion plant showed that anatomical convergence was not as well developed as the obviolls morphological convergence. The of well-developed xeromorphic features in the Tasmanian species is not consistent with the hypothesis previollsly suggesrcd that the cilshion fonn evolved plimarily as a strategy to maintain a positive water balance. Key Words: cushion plant, anatomy, morphology, convergent evolution, Tasmania.

In BANKS, M.R. et al. (Eds), 1991 (31:iii): ASPECTS OF TASMANIAN BOTANY -A TRIBUTE TO WiNIFRED CURTIS. Roy. Soc. Tasm. Hobart: 231-238.

INTRODUCTION (Epacridaceae) are endemic species while Donatia novae-zelandiae (Donatiaceae) and Phyllachne Convergent evolution of plants inhabiting similarly harsh colensoi (Stylidiaceae) also occur in New Zealand. The environments is a well-known phenomenon. Examples morphological convergence in the latter two species is include the sclerophyU shrubs of Mediterranean regions so extreme that the occurrence of P. colensoi was not (Specht 1979, Mooney & Dunn 1970), the giant rosette recognised until 1946 (Curtis 1946), despite collections plants of the tropical alpine regions (Hedberg & Hedberg having been made by L. Rodway in 1917. 1979, Smith & Young 1987), and the cushion plants of Morphological and anatomical studies on cushion the alpine regions of the Southern Hemisphere and the plants by Hauri & Schroter (1914), Hauri (1916) and subantarctic islands (Heilborn 1925, Rauh 1939, Godley Rauh (1939) have shown that many species are strongly 1978, Gibson & Hope 1986). xeromorphic. These and later authors have suggested There seems general consensus that these lifeforms that the evolution of the cushion fonn is primarily a evolve independently in different regions from different strategy to maintain a positive water balance (Hedberg floras by parallel adaptation to adverse environmental & Hedberg 1979). conditions (Hedberg & Hedberg 1979, Smith & Young However, studies by Komer & de Moraes (1979) on 1987), although the morphological changes by which Silene exscapa L. (a cushion species from the European they are achieved may be quite diverse (e.g. du Rietz Alps) showed no evidence of water stress despite high 1931, Rauh 1939). The restricted number of lifeforms leaf surface temperatures (25°C). Similar results have evolved in these environments implies that there may been reported for scree plants from New Zealand, where be only a few possible biological solutions to the surface temperatures may rise to 40-50°C (Fisher 1952). physiological demands of extreme habitats (Mooney & The availability of soil moisture and efficient transport Dunn 1970, Halloy 1983). systems appear to allow active plant growth under A precise definitions of cushion plants is difficult, conditions of high to very high temperature without due to the variety of structural morphologies by which reliance on xeromorphic features to survive such periods. this form may arise (Hauri & Schroter 1914, du Rietz In the Ecuadorian paramos (Heilbom 1925) and in 1931, Rauh 1939). In Tasmania, the term cushion (or Tasmania, cushion plants often grow in bog situations bolster) plant has generally been taken to include any and rarely, if ever, suffer summer moisture restriction species that, growing singly, takes on a hemispherical (Gibson 1988). During winter, however, high water or subhemispherical shape due to the close branching of deficits may develop if access to soil moisture is res­ its shoots and very short internodes. These species tend tricted by a frozen soil layer at times of high evaporative to be quite hard and may coalesce to form extensive demand (Wardle 1971, 1974; Tranquillini 1979). mats. The aim of work reported here was to undertake Four morphologically similar cushion species (from detailed anatomical studies of the four Tamanian cushion four different families) are found in the alpine and species to determine (a) the degree of anatomical subalpine regions of Tasmania. Abrotanella convergence in these species, and (b) the degree to Jorsteroides (Asteraceae) and Dracophyllum minimum which xeromorphic features were apparent, in order to 232 .N. Gibson

PlATE 1 Scanning electron micrographs ieaves cushion species: (AJ Donatia novae-zelandiae, (B) Dracophyllurn minimum, (C) Phyllachne colcnsoi, (D) Abrotanella forsteroides. (Scale bar = 0.5 mm.)

test the hypothesis that the water stress was a major RESULTS factor in the evolution of cushion plants in Tasmania, Although gross morphology and stmctural organisation of all four species are very similar, leaf morphology METHODS and anatomy are much more variahle.

Fresh and preserved material from the four cushion plant species was collected from Ml Field West and Mt Donatia novae-zelandiae Hook. f. Wellington. Both wax and freezing microtome sectioning were used to obtain] 0-] 5 j.1m transverse (TS) Leaf morphology and longitudinal sections (LS) of the leaves and f;tcms Leaves are sessile 5-6 mm long linear·subulate with a of the cushion plants. Sections were stained with safranin pointed apex. The leaf base is widened and has dense and fast green or toluidine blue. Leaf sections were tufts of white hairs 2-3 mOl long in the leaf axis (Curtis obtained from a range of locl1tions the lamina, ! 9(3). Stomata are apparent on both surfaces with the· while stem sections were taken about 10 rnm below the guard cells being sUlTounded by a distinctive cuticular shoot apex. Anatomical diagrams were drawn a ridge 18). camera lucida. Investigations of the cuticle (both scanning electron micrographs and micrographs) Leaf surface of the four species have been published previously Stomata are 40 fun long and 30 Jlm wide, all alTanged (Gibson e/ al. 1987: pis 2 & :l). Nomenclature follows parailel to the axis of the leaf (pI. lA, fig. lB). Buchanan er ai. (1989) except where otherwise Epidennal cells are variable in shape but have signiti<;ant indicated. cell wall (Gibson et al. 1987). species 233

(e) Stam 1$

(A) Leaf TS

r-"'~---"------·----~-----; 500,um

(8) Stoma

t------'---, 500,UtYl

Fig. 1 - Anatomy of Donatia llovae-zelandiae: (A) (B) stoma, (C) stem TS.

LeafTS Dracophyllum minimum F. MueH. A single layer of epidermal cells is covered by a thick cuticle (fig. lA, B). No palisade mesophyll is present. Leaf morphology Spongy mesophyll with numerous chloroplasts is Leaves are sessile with a broad sheathing base about as traversed by three (-five) vascular bundles. The central long as the blade (3-4 mm), narrow-lanceolate and bundle is bound by a bundle sheath and is comprised of slightly concave, thick and rigid. The apex is acute with xylem and phloem and a large cap of sclerenchyma. leaf margins minutely senate (Curtis 1963). The stomata The minor vessels are similar, though without a bundle are very small (pI. IE) and occur on both surfaces. sheath (fig. lA). Toward the base of the leaf up to five vessels are present. The stomata occur regularly over Leaf surface both leaf surfaces. The distinct cuticular ridge The stomata are c. 15 ~m in length and arranged surrounding each stoma is formed by small outgrowths parallel with the long axis of the leaf. The epidermal of the guard cells, which effectively limit the extent of cells are much smaller than those of Donatio novae­ the cuticle (fig. lE). The guard cells also have ledges zelandiae and have highly sinuous walls. No trichomes into the stomata on both upper and lower surfaces. are present (Gibson et ai. 1987). Beneath the stomata, spongy mesophyll and large air spaces are found (fig. IB). There are no surface LeafTS trichomes. A thin cuticle covers a single layer of epidermal cells. A single layer of palisade mesophyll surrounds an inner Stem TS core of spongy mesophyll through which five (-nine) The stem of D. novae-zelandiae is simple. There is an vascular bundles pass (fig. 2A). The main bundle is epidermis sUlTounding a thick cortex layer (fig. I C), capped by a large bundle of sclerenchyma; two minor with a single vascular bundle surrounded by a bundle veins also have a sclereid cap while the remaining sheath. Stem diameter is approximately 2 mm. veins usually do not. Phloem in all bundles appears centrally. In the broad sheathing leaf base up to nine veins are present. The stomata occur regularly and are 234 N _ Gibson

(A) fe} Stem IS

~~---~---, 500Jjm

(8) Stoma' . Gt.lHd cell

500.um

25jJrn

Fig. 2 --- Anatomy of Dracophyllum minimum: (A) leajTS, (B) stoma, (C) stem TS.

very slightly sunken; they consist of a pair of small cells are 30 flm in length and have relatively thin cell guard cells, each situated above a subsidiary cell, both walls. No trichomes are present (pI. IC) (Gibson et al. having a cuticular covering; they are very simple with 1987). no ledges (fig. 2B). LeafTS Stem TS The leaf of P. colensoi is very simple, being composed The stem of a young Dracophyllum minimum plant is of a moderately thick cuticle over a single layer of very similar to Donatia novae-zelandiae except that the epidennal cells. This surrounds a core of spongy meso­ pith is more developed, often containing cavities. A phyll containing three vascular bundles, each surrounded single epidelmal layer encloses a cortex and a single by a bundle sheath (fig. 3A). There is no sclerenchyma vascular bundle. Stem diameter is approximately 1 mm in the leaf. The main vascular bundle is only slightly (fig. 2C). larger than the subsidiary veins. Stomata occur regularly over all surfaces. The guard cells are covered by a thin layer of cuticle, and raised cells have both upper and Phyllachne colensoi (Hook. f.) Bergg. lower ledges above a substantial air space. Guard cells are surrounded by a slightly modified subsidiary cell Leaf morphology (fig. 3B). Leaves sessile, 3-A mm long, glabrous, the lower half widened and flattened, the upper half linear and Stem TS thick with a glandular pore just below the apex on the The stem of P. colensoi is very similar to the related adaxial side (Curtis 1963). Stomata approximately Donatia novae-zelandiae, with an epidennis, an outer 25 flm in length occur on both surfaces (pI. 1C, fig. cortex layer and a single central vascular bundle with 3B). The leaves are often olive-green in colour. a central pith (fig. 3C). Although D. novae-zelandiae is placed in its own monogeneric family (Donatiaceae) by Leaf surface most authors, due to incomplete fusion of the style and The stomata are considerably larger than those of stamens, earlier work had placed it in the Stylidiaceae Dracophyllum minimum (25 !-lm cf 15 flm). Epidennal (Curtis 1963). Four Tasmanian cushion species 235

(A) Leaf TS (e; Stem TS

I Epidermis !ftt::::::==~~= Spongy rnesophyll ([~-- ::::"'"

(BJ Stoma

500Llm

Fig. 3 -Anatomy ofPhyllachne colensoi: (A) leafTS, (B) stoma, (C) stem TS.

Abrotanella forsteroides (Hook. f.) Benth. The bundle is enclosed in a sheath and includes a major duct, a fibre cap, phloem and xylem tissues (fig. 4A,C). Leaf morphology The duct appears empty and is surrounded by a distinct Leaves are sessile c. 4 mm long with a broad sheathing layer of cells. It is c. 100 flm in diameter and LS base. The leaf tip is hyaline and acuminate, the leaf sections show it to run the full length of the leaf. Its margins are obscurely serrulate (Curtis 1963, Gibson et function remains obscure. The phloem tissue is split aZ. 1987) (pI. lD). The hyaline leaf tip can give the into two discrete bundles by an intrusion of otherwise green cushion a silvery appearance when a sclerenchyma in the lower half of the leaf. The stomata hand or finger is run across its surface. Stomata occur appear on both leaf surfaces in broad bands running in bands up both surfaces. parallel to the leaf axis (Gibson et ai. 1987). The stomata are c. 30 11m in diameter and very simple, with LeafTS no ledges, ornamentation or specialised subsidiary The single layer of epidermal cells is covered by a thick cells. The leaf cuticle does not cover the guard cells layer of cuticle (fig. 4B). Sunken multicellulartrichomes (fig.4D). are scattered over the leaf surface (fig. 4A,B). These structures are made of 10--15 cells, are broadly cuneate Stem TS and are attached to the leaf surface by a modified The stem is similar to the other three species except for epidermal cell. The trichome tip is slightly sunken the inclusion of three major ducts (fig. 4E). A single­ below the leaf surface and is c. 30 11m in length and layered hypodemlis beneath the epidermis encloses a c. 25 11m broad at the top. Within the trichome cavity, cortex. The single vascular bundle is enclosed by a cuticle thickness becomes attenuated so that the sheath. Immediately outside this sheath are three ducts trichomes are almost completely free of cuticle (fig. 4B). identical in form to those found in the leaf. Stem diameter There are two layers of palisade mesophyll on the is c. I mm whilst the ducts are c. 100 llm diameter. adaxial side but only one on the abaxial side, a layer of spongy mesophyll traversed by a single vascular bundle. 236 N. Gibson

IA)

,----.~---~---'.------. 5"",,"

(e) Vascu'a, bundle

);:;("'~+\-SClcrenCh)lmo

r----, 25).m

)-r---Bundla sheath r---, 100"",

Cuticle

Epidermis (E) Stem TS

Palisade mesophyll

xY'"m~~

500,IJm

Fig. 4-· Anatomy of Abrotanella forsteroides: (A) leaf TS, (8) trichome, (C) vascular bundle, (D) stoma, (E) stem TS. [1'our Tasrnanian cushion 237

DISCUSSION the severe water stress that under conditions of restricted soil mOlsture and ambient All four species of cushion plant show a high degree of temperature. From these anatomical studies it appears morphological convergence. All have closely com­ that cushion would primarily cope with pacted, highly branched stems with very short demand by stomat.al closure, since internodes. All the leaves are sessile .. small and the common features shared the four are a with stomata on both surfaces. thick, cuticularised The sunken The internal structure is much less unifonn and stomata and protective trichomcs suggest wch consequently more difficult to compare. Of the four of stress brief. species Donatia Ilovae-zelandiae and rninirnum colensoi are the most similar, which is not have and vascular given the taxonomic affinity between these bundles in their bundles/leaf in D. (Curtis 1963). The major difference between the two is the lack of sclereids in P. colensoi. The intemal structure and stomata are very similar (figs 1, 3). Dracophyllum minimum has quite distinct leaf anatomy, with a palisade mesophyll and numerous minor consistent with all four species efficient water veins all running parallel with the axis ..Its internal uptake mechanisms capable of dealing with of structure is almost identical to the closely related New temperature during Slimmer, when an excess of Zealand cushion plantD. muscoides Hook. f .. except for soil water is available. the absence of the second palisade layer on the adaxial Beadle (I966, 1968) has suggested thaI surface (Hauri 1916). are extremely resistant to mineral starvation. He {1brotanella jorsteroides shows the most complex that where phosphorus and nitrogen are excess arlatomy, with the presence of well-developed ducts ,'o,rh"h,,,ir"',, from photosynthesis is converted into cell through leaves and stem, and the presence of sunken wall material in sclereids). This eXjDla:natlOn multicellular trichomes (fig. 4B). The function of both to cushion these structures is obscure, but the ducts may be important in the aeration of plants growing in highly vAfJ"'""~U to be very jow' in available anaerobic peats. (Swift et al. 1979). It is difficult to quantify the degree of Other studies of the comparative anatomy of cushion between the four cushion species because no have reported a similar degree of anatomical comparative data are available for other lifeforms found variability (Ancibor ]971, 1980, 1981). In a study of 14 in this environment and the functional significance of species from the cold arid puna region of Argentina many anatomical features is poorly understood (c.g. (rainfall c. 300 mm; altitudes 3400-5100 m a.s.!.), ducts in A. jorsteroides). where high levels of water stress might be expected, it All species do exhibit some xeromorphic characters was found that most of the anatomical features could be that are generally equated with severe water strcss interpreted in terms of minimising the effects of strong (Jeffrey 1987) (table 1). However, none could be radiation, low temperatures and wind rather than a considered to be particularly well adapted to cope with response to water deficits (Ancibor 1980). It appears

Table 1 Xeromorphic Characters often Associated with to Water Stress*

Donatio Dracophyllum Phyllachne Abrotanella

Microphyllous habit + + + + Thick epidennis + + + + Abundant sdcrenchyma + + + Thick cuticle + + + + Tightly packed mesophyll + + Sunken stomata Numerous protective trichomes

After Jeffery (l98h 238 IV. Gibson that, while the particular environments may prefer- GIBSON, N., KrER.'1AN, K.W. & MACPHAIL, M.K., 1987: A facilitate the evolutiem of the cushion form, the fossil bolster plant from the King River, Tasmania, selective pressures for this may be acting at the Pap. Pmc. Roy, Soc. Tasln, 121: 35-42. morphological rather than the anatomical level. All GODLEY, EJ., 1978: Cushion bogs, In Troll, C. & Lauer, W, four Tastnallian species show some development of (Eds.): GROECOLOGlCAL RELATIONS BRTWEEN iRE SOUTHERN TEMPERATE ZONE chaTacters. However, these are not AND THE TROPICAL MOUNTAINS. Steiner, consisten t with the that these would Weisbaden: 141-158. undergo significant of winter desiccation, HALLO¥, S., 1983: The use of convergence and divergence in Rather, some features, such as reduced leaves and well­ the interpretation of adaptation in high mountain to be either genetic or biota. Evo!. Theory 6: 232--255. to extreme environmcntal HAURI, H., 1916: Anatomische Untersuchungen an Polster parameters (e.g. ablation, winds), while other pflanzen nebsl morphologischcn und okologischen features may be adaptations related to mineral starvation Nolizen. Beih. Bot. Zbl, 33: 275-293. or waterlogged conditions. The extent to which these HAURI, H. & SCHPOTER, C, 1914: V crsuch einer Ubersicht der siphonogamell Polsterpf1anzen, Bot, Jahrh. Syst. anatomical features are fixed is unclear, Pflanzengesch, Pjlanzengeogr. 50 (Suppl.). HEDBERG, I. & HEDBERG, 0., 1979: Tropical-alpine life-fonns of vascular plants. Oikos 33: 297-307. REFERENCES HElLBORN, 0., 1925: Contributions to the ecology of the Ecuadorian paramos with special reference to cushion ANclBOR, E., 1971: Estudio anaromico y morfologico de una plants and osmotic pressure. Svensk. Bot. Tidks. 19: crucifera atHlina en Lithodraba 153-170. rnendocinensis, Darwiniana 5 J 9-561. JEFFREY, D.W., 1987: SOIL PLANT RELATIONSHIPS. AN ANcmoR, E., 1980: Estudio anatomico de la vegetation de la ECOLOGICAL APPROACH. Croom Helm, puna de jujuy. II _.- Anatomia de las plantas en London. cojin. Bol, Soc. Arg. Bot. 19: 157--202, KORNER, C.H. & DE MORAES, J,A., 1979: Water potential and ANClBOR, E., 1981: Estudio anatomico de la vegetacion de la diffusion resistance in alpine cushion plants on clear puna de jujuy. IV -- Anatomia de las plantas en summer days, Oecol. Plan/, 14: lO9-120. roseta. Ulloa 35: J 25-136. MOONEY, H.A. & DUNN, E.L., 1970: Convergent evolution of BEADLE, N.C.W" J 966: Soil phosphate and its role in mediterrarlean climate evergreen sclerophy\l shrubs. moulding segments of the Australian flora and Evol. 24: 292-303. vegetation, with special reference to xeromorphy RAUH, W., 1939: Uber polster fonnigen Wuchs. Nova Acta and sclerophylly. Ecol. 47: 992-1007. Leopold. 7: 267-508. BEADLE, N.C.W" 1968: Some aspects of the ecology and SPECHT, R.L., 1979: Heathlands and related shrublands of the physiology of Australian xeromorphic plants. Aust. world. In Specht, RL. (Ed): HEATHLANDS AND J. Sci. 30: 348-356. RELATED SHRU13LANDS. ECOSYSTEMS OF THE BUCHANAN, AM., MCGEARy-BROWN, A. & ORCHARD, AE., WORLD 9A. Elsevier Scientific Publishing 1989: A census of the vascular plants of Tasmania. Company, Amsterdam: 1-17. Tas. Herb, OCC'. Pub!. 2: 1-82 SMITH, A.P. & YOUNG, T.P., 1987: Tropical alpine plant Cuwns, W.M" 1946: Phyllachne colensoi (Berggren), an ecology. Ann. Rev. Ecol. Syst. 18: 137-158, addition to the list of subantarctic plants in the SWIFT, M.J., HEAL, O.W. & ANDERSON, 1.M. 1979: Tasmanian flora. Pap. Proc. Roy, Soc. Tas. 80: 31- DECOMPOSITION IN TERRESTRIAL ECO­ 33, SYSTEMS. Blackwell, London. CURTJS, W.M., 1963: THE STUDENT'S FLORA OF TRANQUILLINI, W., 1979: PHYSIOLOGICAL ECOLOGY OF TASMANIA, PART Ii. Government Printer, Hobart. ALPINE TIMBERLINES. Springer-Verlag, Berlin. DU RIETZ, G.E., 1931: Life-fonns ofterrestrial flowering plants. WARDLE, P., 1971: An explanation of alpine timberlines. N. Z. Acta Phylogeogr, Suecica 3: 1-95, J. Bot. 9: 371-402. FISHER, FJ.F., 1952: Observations on the vegetation of the WARDLE, P., 1974: Alpine timberlines. In Ives,J.D, & Barry, screes in Canterbury, New Zealand . .J. beo!. 40: 156- R.G. (Eels): ARCTIC AND ALPINE 167. ENVIRONMENTS, Methuen, London: 371-402, GmsoN, N., 1988: A study of the biology of four Tasmanian cushion species. Unpubl. PhD thesis, University of (accepted 10 August 1990) Tasmania. Gmso", N, & HOPE, G.S., 1986: On the origin and evolution N. Gibson of Australasian alpine cushion plants. In Barlow, B.A. Wildlife Research Centre, Dept of Conservation and Land (Ed.): FLORA AND FAUNA OF ALPINE Management, PO Box 51, Wanneroo, W A, Australia 6065; AUSTRALASiA, CSIRO, Melbourne: 63-82, fonnerly Department of Geography, University of Tasmania