Bulletin of the Torrey Botanical Club 122(3), 1995, pp. 185—189

Wood anatomy of (): Ecological and phylogenetic considerations Sherwin Cariquist’ and Erika J. Wilson2 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105

CA.IuQuIsr, SHERwIN AND ER.II J. WILSoN (Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105). Wood anatomy of Drosophyllum: ecological and phylogenetic considerations. Bull. Torrey Bot. Club 122:185—189. —Drosophyllum lusitanicum. the sole woody species of Droseraceae, has wood anatomical features very much like those of Dioncophyllaceae and Nepenthaceae. Features in common include vessel elements with simple perforation plates, fibriform vessel elements, tracheids with large fully bordered pits, diffuse (plus variously grouped) axial parenchyma, and paedomorphic rays 1—2 cells wide. Wood anatomy thus validates the close relationships claimed among Drosophyllum, Dioncophyllaceae, and Nepenthaceae on the basis of recent DNA studies, Wood anatomy ofDrosophyllum is xeromorphic, in accord with the dry habitats of the species. Key words: Drosophyllum, Droseraceae, Nepenthaceae, wood anatomy.

Drosophyllum lusitanicum (L.) Link, sole spe (1979) that the Drosophyllum localities are “of cies of its genus, is a short lived subshrub or ten alkaline,” however, is questionable. Pines oc woody herb of Portugal, Spain, and Morocco cur in some Drosophyllum localities (Diels 1906), (Diels 1906; Juniper et al. 1989). As reported by and pines tend to be indicators of acid sands. Penzig (1877), Diels (1906) and others, Droso Juniper et al. (1989) cite “acidic sands” as a Dro phyllum differs from other Droseraceae in having sophyllum habitat, and Droseraceae other than secondary growth. in open areas may be Drosophyllu,n certainly show preferences for acid facultative biennials, but plants that grow (often soils. The wood anatomy of Drosophyllum is in a prostrate fashion) through other shrubs may worthy of examination with relation to dryness attain woody cylinders up to 1 cm in diameter of habitat. Droseraceae are often considered (Juniper Ct al. 1989). The other genera of Dro plants of bogs, but the majority of species (West seraceae have centric bundles with few vessels ern Australia, South Africa) occur in summer- and no perceptible cambial activity (Solereder dry acid sands; in these species, survival of the 1908; Metcalfe and Chalk 1950). Solereder (1908) dry season is achieved by tubers, scales covering reported that vessels of Drosophyllurn have sim the bud, annual habit, or other means (Diels ple perforation plates, but no other wood ana 1906). These mechanisms are absent in Droso tomical details have been reported for the genus. phyllum, and thus the nature of wood anatomy Presentation of a complete description of wood might be a prime tool in management of the features is desirable primarily because of the water economy of the . The deep taproot ecology of the genus, unusual for Droseraceae, reported for Drosophyllum (Juniper et al., 1989) and new information about probable phyletic may also be important to survival of the dry position of Drosophyllum. season, and the minimal surface provided by the The areas where Drosophyllum is or has been linear shape is doubtless also a factor. native are often described as dry (Lloyd, 1942; The familial position of D. lusitanicum has Juniper et al. 1989), although they occur on slopes been little doubted; it has universally been as near the western Mediterranean Sea and thus signed to Droseraceae (Linnaeus described it as tend to have a winter rainy season. Some Dro a species of Drosera). A recent study that inte sophyllum habitats are rocky (quartzite is men grates data from rbcL sequences and from mac tioned) or sandy (Diels 1906). The claim by Slack romorphology into a cladistic form (Williams et al. 1994) places Drosophyllum close to Triphy ophyllum (Dioncophyllaceae) and ‘Address for correspondence: 4539 Via Huerto, Santa (Nepenthaceae) in a dade terminating in other Barbara, CA 93110. genera of Droseraceae (Dionaea, Aidrovanda, and 2 Plant Scholars Program, Santa Barbara Botanic Garden. Drosera). Lack of DNA for in Received for publication December 7, 1994, and in the study of Williams et al. (1994) means that revised form March 11, 1995. resolution of their cladogram among Drosera 185 186 BULLETIN OF THE TORREY BOTANICAL CLUB IVOL. 122 ceae, Dioncophyllaceae, and Nepenthaceae Results. The description below is based on should be regarded as tentative. Their cladogram both stems and roots, qualitative features ofwhich raises the possibility that Droseraceae might not were identical in the material examined. Quan be monophyletic, but the cladistic arrangement titative data on stems are incorporated in the might have been somewhat different had DNA description, with data based on roots in a fol from Dioncophyllaceae been available. Wood lowing paragraph. The illustrations (Figs. 1—4) anatomy thus may be of significance in assessing are from root sections. the phyletic position of Drosophyllum. Recent data on wood anatomy are available for Dion STEM ANATOMY. Growth rings absent or cophyllaceae (Gottwald and Parameswaran 1968) boundaries faint (Fig. 1). Vessels mostly solitary and Nepenthaceae (Cariquist 1981). Williams et (Fig. 1), mean number of vessels per group, 1.16. aL (1994) consider Plumbaginaceae and Poly Mean vessel lumen diameter, 23 m. Mean num gonaceae to be outgroups of the dade described ber ofvessels per mm2, 248. Mean vessel element above, with somewhat more dis length, 301 m. Mean vessel wall thickness, 2.3 tant. Studies on wood anatomy of Plumbagina tm. Perforation plates simple. About a third of ceae and Polygonaceae are in progress (Cariquist, the vessels fibnform, with fusiform cell shape unpublished). A paper on wood anatomy of Car and subterminal (sometimes lateral) perforation yophyllaceae (Carlquist 1995) adds significant plates. Lateral wall pitting of vessels composed data because most recent cladograms place Car of alternate circular bordered pits, pit cavity di yophyllaceae as basal or near-basal in Cary ameter about 6 m, pit aperture circular (Fig. 3). ophyllales (see Cariquist 1995). These studies will Imperforate tracheary elements all tracheids. widen the comparisons offered here. Williams et Mean tracheid diameter at widest point, 18 zm. al. (1994) consider the glandular trichomes of Mean tracheid length, 380 m. Pits on tracheids Plumbaginaceae to be very similar to those of fully bordered, about 5 m in diameter (pit cavity the Drosophyllum-Dioncophyllaceae-Nepentha diameter), both pit cavities and pit apertures cir ceae-Droseraceae dade, an interesting anatom cular in outline (Fig. 4). Axial parenchyma dif ical link because the functions ofglands in Plum fuse, scanty vasicentric, and (less frequently) dif baginaceae are markedly different from those of fuse-in-aggregates. Axial parenchyma present as Drosophyllum dade. undivided cells, less commonly as strands of two cells. Axial parenchyma walls about 1.2 m thick. Materials and Methods. Material ofrelative Rays mostly uniseriate, less commonly biseriate ly mature cultivated plants of D. lusitanicum was (wider multiseriate rays in stems are extensions provided by Joseph Mazrimas. Dried voucher of primary rays). Rays, as seen in tangential sec specimens from these were prepared as Carlquist tion (Fig. 2) most often composed of 1—3 cells, 8173 (SBBG). Stem and root portions were pre usually overlapping rather than superposed. Ray served in aqueous 50% ethanol. Because of small cells mostly upright, less commonly square. Ray diameter of the woody cylinders and the hard cell walls about 1.2 m thick. Pits interconnect ness of the wood, sectioning them on a sliding ing ray cells and ray-to-tracheid pits vestigially microtome was not feasible. Instead, an alter bordered. Helical thickenings observed on walls native technique (Carlquist 1982) involving soft of a few ray cells in roots. ening ofwood with ethylene diamine, embedding in paraffin, and sectioning on a rotary micro- RooT ANATOMY. Quantitative features of root tome, was employed. Sections were stained with secondary xylem are as follows. Mean number safranin and fast green; safranin was absorbed of vessels per group 1.19. Mean vessel diameter, minimally, so the best staining was achieved by 30 m. Mean number of vessels per mm2, 125. prolonged exposure to fast green. Macerations Mean vessel element length, 292 m. Mean ves were prepared by means of Jeffrey’s Fluid and sel wall thickness, 2.3 tm. Mean tracheid di stained with safranin. ameter, 19 m. Mean tracheid length, 356 tm. Cell diameters and lengths are based on av Mean tracheid wall thickness, 2.4 m. Other erages of 25 measurements; other quantitative quantitative features as in stems. data are based on conditions thought to be typ The differences between root and stem wood ical. Vessel diameters are measured as lumen are probably not statistically different except for diameter at widest point. Terms are in accor vessel diameter. Vessels tend to be wider in roots dance with the IAWA Committee on Nomen than in stems ofa given species (Patel 1965). The clature (1964). fusiform (rather than oval) shape of ray cells as 19951 CARLQUIST AND WILSON: DROSOPHYLLUM WOOD ANATOMY 187

Figs. 1—4. Wood Sections of root of Drosophyllum lusitanicum, Carlquist 8173. Fig. 1. Transection; vessels are narrow, mostly solitary. Fig. 2. Tangential section; rays are not readily visible because ray cells are fusiform in outline and overlap. Fig. 3. Radial section, showing fully bordered pits on narrow vessel (wide cell at right) and, to left of vessel, a tracheid. Fig. 4. Radial section, showing large circular bordered pits on vessels (left two- thirds of photograph) and vestigially bordered pits on axial parenchyma cells (right third of photograph). Figs. 1, 2, scale above Fig. 1 (divisions = 10 gm); Figs. 3, 4, scale above Fig. 3 (divisions = 10 nm).

that one. to clades close All, construction. their of bases the on depending

on as

as well belongs,

Drosophyllum to which differ, et (1994) al. Williams by provided grams

the dade

on proceed studies as consideration of clado various The Correlations. Systematic

worthy is feature This nonwoody. relatively been

might have all of ancestor a common that ity

possibil the suggests species. 1988) Carlquist of scheme

in this elements vessel I fibriform of the in Type as abundance Paedomorphic classified be

of the because perhaps trend, this would (rays groups three all exemplify in rays domorphic

does not Drosophyllum pae of 1988). 1966, occurrence The (Carlquist Violaceae). of in woods

woods xeromorphic with found be characterize may to specializations tend of range wide

also elements a vessel Short (e.g., 1994). related al. et closely they if were (Hargrave even expect

conditions summer hot not in would vessels one wide than specialization—which phyletic

readily less embolize of vessels level at same narrow the are that groups finding, three the ship,

physiological a with correlates relation This phyletic of indicative 1966). quist features in tical

(e.g., Carl xeromorphy of iden virtually groups wood indicators as three the are only Not

cited been have vessels Narrow large. at plants relationships.

flowering of those with compared narrow tively phyletic of indicative a not is feature diameter sel

are rela Drosophyllum of elements vessel The ves Thus, Nepenthaceae. and Dioncophyllaceae

instances. such identify to made was attempt in an habit scandent with correlates diameter wide

one, and than rather vessels of pair a as section, to and habit, related also it but is to ecology,

a in tran seen as ends, overlapping the count to is related diameter vessel above, mentioned As

one lead may elements vessel fibriform of ping Drosophyllum. than in Nepenthaceae and laceae

overlap marked The Drosophyllum. of wood in Dioncophyl greater in is much diameter vessel

occurs grouping vessel of degree low a thus and Mean reported. are cells four to three of strands

1984), (Carlquist present are tracheids which in Dioncophyllaceae, in and common, are two

woods in minimally but occurs it fibers, briform of strands Nepenthes, in subdivided, not monly

or Ii fiber-tracheids with woods in romorphy is com parenchyma axial Drosophyllum, nor. In

to xe proportionately occurs grouping Vessel mi relatively are groups the three among gences

areas. dry typically in occur weather wet of diver of similarities, list this with contrast In

periods brief when flows peak accommodate can square. to upright are cells ray groups, the three all

woods these in plates perforation simple The 5). 32 In wide. cells than two rarely more and eriate,

322— 1988: Carlquist in (review elements vessel his commonly less uniseriate, mostly are groups

than a extent greater to embolism cheids resist all in three The rays Drosophyllum. in gregates

because tra conditions dry to adaptive is diffuse-in-ag groups and vasicentric scanty both laceae,

these in oftracheids presence The plates. Dioncophyl foration vasicentric in scanty Nepenthes, in

per simple with elements vessel with combined diffuse-in-aggregates parenchyma: axial ings of

found be may tracheids which in areas dry group some but in also parenchyma, axial diffuse

represented families of examples are some have Rosaceae three All fibers. libriform and cheids

and Proteaceae, Cistaceae, 1985). (Carlquist areas fiber-Ira than rather 1964) Nomenclature on

dry of woods in presence tracheid with dealing Committee (sensu IAWA tracheids have groups

a paper in tracheids) vasicentric to opposed (as (US). three All 14178 Baldwin Shaw, Airy tatum

tracheids

true lists of in cited are groups these of pet Triphyophyllum the specimen from author

Most

plates.

perforations

simple

with elements sel senior the by prepared a maceration in visible are

ves with

combination in occur

tracheids

groups

but Dioncophyllaceae, in reported hitherto been

of number a in plates),

perforation

scalariform

not have elements vessel

Fibriform

sel

elements.

with vessels (e.g., vessels primitive with bined

ves fibriform groups have

three

All

plates. ration

be to

com

thought

often are tracheids though

perfo simple

with elements vessel

have three

Al

xeromorphic.

are

Drosophyllum of wood

All

to features. other extend not does contrast

the of features Several

Conclusions. Ecological

this but not, do Nepenthes and Drosophyllum

whereas 1968), and Parameswaran (Gottwald

cambia successive have Dioncophyllaceae 2). (Fig.

features? wood similar share groups three elements vessel fibriform or tracheids guish from

these Do Nepenthaceae. and Dioncophyllaceae, to distin difficult cells ray make arrangement

Drosophyllum, of closeness show however, and overlapping their section tangential in seen

rVoL. 122 CLUB BOTANICAL THE TORREY OF BULLETIN 188 1995] CARLQUIST AND WILSON: DROSOPHYLLUM WOOD ANATOMY 189

Literature Cited H.jtGvE, K. R., K. J. K0LB, F. W. Ewmts S. D. DAvis. 1994. Conduit diameter and drought-in CAIUQuIsT, S. 1966. Wood anatomy of Compositae. duced embolism in Salvia mellfera Greene (La A summary, with comments on factors influencing biatae). New Phytol. 126: 695—705. wood evolution. Aliso 25—44. 62: IAWA C0MMITrEE ON NoMENcLATuRE. 1964. Mul 1981. Wood anatomy of Nepenthaceae. Bull. tilingual glossary of terms used in wood anatomy. Torrey Bot. Club 108: 324—330. Konkordia, Winterthur, Switzerland. 185 p. 1982. The use of ethylenediamine in soft JUNIPER, B. E., R. J. Roair.is AND D. M. JoEL. 1989. ening hard plant structures for paraffin sectioning. The carnivorous plants. Academic Press, London. Stain Technol. 57: 311—317. 353 p. 1984. Vessel grouping in dicotyledon woods: LLoyD, F. E. 1942. The carnivorous plants. The Ron significance and relationship to imperforate tra ald Press, New York. 352 p. cheary elements. Aliso 10: 505—525. MErct, C. R. o L. CHAuC. 1950. Anatomy of 1985. Vasicentric tracheids as a survival the dicotyledons. Clarendon Press, Oxford. 1500 mechanism in the woody p. flora of southern Cali PAm, R. N. 1965. A comparison of the anatomy of fornia and similar regions; review of vasicentric the secondary xylem in roots and stems. Holzfor tracheids. Aliso 11: 37—68. schung 19: 72—79. 1988. Comparative wood anatomy. Springer Pzio, 0. 1877. Untersuchungen über Drosophyl Verlag, Berlin & Heidelberg. 436 p. lum lusitanicum. Thesis, Breslau. 1995. Wood anatomy of Caryophyllaceae: SoutRErm, H. 1908. Systematic anatomy of the di- ecological, habital, systematic and phylogenetic im cotyledons (trans. by L. A. Boodle and F. E. Fritsch). plications. Aliso 14: 1—17. Clarendon Press, Oxford. 1182 p. DIEI.s, L. 1906. Droseraceae. A. Engler In [ed.], Das Wius, S. E., V. A. AlBERT .im M. W. CEIAEE. Pflanzenreich IV(l 12). Verlag Wilhelm Engelmann, 1994. Relationships of Droseraceae: cladistic Leipzig. A analysis of rbcL sequence and morphological data. GorrwAw, H. N. PkrtaswAI. 1968. Das Amer. J. Bot. 81: 1077—1037. sekundäre Xylem und die systematische Stellung der Ancistrocladaceae und Dioncophyllaceae. Bot. Jahrb. 88: 49—69.