Bulletin of the Torrey Botanical Club 123(2). 1996, pp. 135—147

Wood anatomy of Plumbaginaceae

Sherwin Carlquistt and Colby J. Boggs Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105

CARLQUIsT, SHDRwLN, AND COLBY J. Booas (Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105). Wood anatomy of Plumbaginaceae. Bull. Torrey Bot. Club 123:135—147. 1996.—Although few of the following wood characteristics may be synapomorphic, at least some species of Plumbaginaceae share the with Polygonaceae simple perforation plates, small pits on lateral vessel walls, libriform fibers as imperforate tracheary elements, paratracheal axial parenchyma, storying, silica bodies, and dark-staining amor phous deposits. These features suggest close relationship between the two families. A similar roster of features is cited as supporting placement of the two families close to Caryophyllales, a placement suggested recently on the basis of macromorphology and rbcL evidence. The latter evidence also links the two families with Nepen thaceae and Droseraceae. These latter families resemble each other in wood anatomy, although their wood features are significantly more primitive than those of Plumbaginaceae. Raylessness and paedomorphic rays in Plumbaginaceae suggest an herbaceous-or near-herbaceous ancestry for the family. Wood of Plumbaginaceae is markedly xeromorphic. Large fusiform silical bodies in axial xylem idioblasts and conjunctive tissue astroscler eids are newly reported for dicotyledons. Newly reported for Plumbaginaceae are vessel restriction patterns, pervasive axial parenchyma, abaxial axial parenchyma, raylessness, storying, and centripetal successive cambia. Key words: Aegialitis, Caryophyllales, Centrospermae, Droseraceae, ecological wood anatomy, Limonium, Ne penthaceae, Plumbaginaceae, Polygonaceae. systematic wood anatomy.

Wood anatomy of Plumbaginaceae has pre spect to systematic affinities. Concepts on affin viously been little studied, despite the potential ities of Plumbaginaceae have changed in recent interest of this topic. The summary of wood of years. Earlier, the family was placed in or close Plumbaginaceae offered by Metcalfe and Chalk to orders such as Primulales or Ericales (Pax (1950) is based on only one species, Plumbago 1891, Nowicke and Skvarla 1977, Thorne 1992). capensis. In terms of structural types in wood, Cronquist (1984) placed Plumbaginales, Polyg Plumbaginaceae is diverse (e.g., rays present or onales. and Caryophyllales together in subclass absent, cambium simple or multiple and succes Caryophyllidae, a treatment doubtless inspired sive). The family is relatively large (19 genera, by the study of Rodman et al. (1984), who chose 775 species: Thorne 1992), but few species de Plumbaginaceae and Polygonaceae as outgroups velop very much secondary xylem; lack of for cladistic and phenetic analysis of Caryophyl woodiness may account for neglect of the fam lales, but who also demonstrated the closeness ily. Although Plumbago reaches about 1.5 its, its of the two families to Caryophyllales in their stems are innovated from the shrub base and studies. A close relationship among Plumbagi they do not exceed about 1 cm in diameter. The naceae, Polygonaceae, and Caryophyllales was only shrubs in the family reported to attain 2 m supported by the rbcL analysis of Williams et or more are Limonium arborescens and L. den al. (1994). However in the cladograms of that droides (Svent.) Kunkel & Sund. (Bramwell and study, Plumbaginaceae and Polygonaceae are on Bramwell 1974), the woodiest products of an a branch that represents a sister group to Cary adaptive radiation in that genus on the Canary ophyllales and also a sister group to a branch Islands (Carlquist 1974). The presence of a few that includes Droseraceae and Nepenthaceae. woody species in a family that is predominantly Williams et al. (1994) also cite secondary com composed of herbaceous perennials leads one to pounds in support of this placement and wonder ask whether woodiness is primitive or has whether the salt glands of Plumbaginaceae may evolved secondarily in the family. Wood anato be close homologs of the glandular trichomes of my is worthy of study with respect to this ques Droseraceae and Nepenthaceae, an intriguing tion, as well as with respect to the divergent possibility in view of the divergent functions of growth forms in the family. glandular trichomes in the two families. Com Wood anatomy is often of interest with re parison of wood anatomy of Plumbaginaceae to that of Polygonaceae, Caryophyllales, Drosera ceae, and Nepenthaceae is warranted in view of Address for correspondence: 4539 Via Huerto, the Santa Barbara, CA 93110. results of these recent studies. Received for publication June 30, 1995, and in re Plumbaginaceae often occupy saline soils, the vised form Nov. 7, 1995. latter varying from brackish marshes (Limonium

135 136 BULLETIN OF THE TORREY BOTANICAL CLUB [VoL. 123

Table 1. Quantitative wood features of Plumbaginaceae. Key to columns: 1 (VG), mean number of vessels per group: 2 (VD), mean radial lumen diameter of vessels, p.m; 3 (VM), mean number of vessels per mm2; 4 (VL), mean length of vessel elements, jim; 5 (VW), mean thickness of vessel walls, tim; 6 (TL), mean length of imperforate tracheary elements, tim; 7 (TW), mean thickness of imperforate tracheary elements, tim; 8 (FV), F/V ratio (imperforate tracheary element length divided by vessel element length); 9 (MH), mean height of multiseriate rays, tim; 10 (MW), mean width of multiseriate rays, no. of cells: II (ME), Mesomorphy ratio (vessel diameter times vessel element length divided by no. of vessels per mm2). Collections and measurement conventions given in Materials and Methods.

1 2 3 4 5 6 7 8 9 10 Ii Species VO VD VM VL VW TL TW FV MH MW ME Acantholimon caryophyllaceum 6.2 11 1969 102 2.2 0.6 Aegialitis annulata 2.6 19 169 123 3.1 399 4.2 3.2 14 Armeria maritima 5.0 9 1567 80 2—5 0.5 Ceratostigma griffithii 1.6 18 563 113 2.0 28 2.0 2.0 447 3.5 3.6 Limonium arborescens stem 1.8 31 195 147 3.4 391 6.3 2.7 362 5.3 2.3 root 1.6 25 276 141 3.2 364 4.8 2.5 553 6.0 13 L. cai(fornicum 2.7 13 217 67 5.1 147 2.2 2.2 1179 5.6 4.0 L. commune 1.3 14 231 60 4.7 302 2.5 5.0 1057 5.0 3.6 L. cretaceum 5.2 13 362 82 1—5 226 7.1 2.8 858 5.8 2.9 L. peregrinum 2.7 18 403 152 2.5 411 2.3 2.7 6.8 L. perezii 2.5 19 330 97 2.9 169 4.8 1.7 454 7.0 5.5 L. rumicifolium 2.4 29 245 103 4.8 311 7.7 3.0 614 5.0 12 Plumbago capensis 2.8 32 165 157 3.1 390 2.7 2.5 3247 4.1 30 Plumbaginaceae averaged 3.7 19 515 110 3.3 303 4.2 2.7 974 5.3 4.1

spp.) to marine bluffs (Armeria) to marine flats amining the unusual silica bodies of L. rurnici (the mangrove Aegialitis). Other Plumbagina folium and the vessel sculpturing of L. peregrin- ceae occupy habitats that are relatively dry, but urn. Macerations were prepared with Jeffrey’s not notably salty (Plumbago). All of these hab Fluid and stained with safranin. itats may be considered xeric, and thus exami Collection data for the specimens is as fol nation of wood anatomy with respect to xero lows. Acantholirnon caryophyllaceum Boiss., morphy is appropriate. rocks at bottom of agglomerate cliffs, river val ley W of Yukari Narlica to Bargessaray, 2200 Materials and Methods. The wood samples m, Turkey, J. C. Archibald 8007 (RSA); Aegi studied here were all available in dried form. alitis annulata R. Brown, shrubs to 2 m with Woods of Aegialitis annulata, Limoniurn pere widened bases, intertidal zone on rocky sub grinum, and L. rumicifolium were collected from strate, Lumaroo Beach, Darwin, Northern Ter wild-occurring plants (Table 1). Samples of Cer ritory, Australia, S. Carlquist 15207 (RSA); Ar atostigma gr(ffithii, L. arborescens and Plum meria maritima L., marine bluffs near Cambria, bago capensis were derived from cultivated San Luis Obispo Co., California, Tucker 211 specimens. The remaining wood samples were (SBG); Ceratostigma griffithii Clarke, cultivated derived from herbarium specimens listed (Table in the Huntington Gardens, San Marino, Cali 1). Wood samples were boiled in water and fornia; Lirnonium arborescens (Brouss.) 0. Kun stored in 50% ethanol. The harder wood samples tze, cultivated in gardens surrounding green (Lirnoniurn arborescens, L. peregrinum, L. per house, University of California at Santa Barbara, ezii, L. rumicifoliurn, and Plumbago capensis) S. Carlquist 8176 (SBG); L. califtrnicum were sectioned on a sliding microtome. Woods (Boiss.) Heller, erect perennial from heavy cau of the remaining Plumbaginaceae were sec dex, salt marsh with Scirpus spp., upper New tioned in paraffin after softening in ethylene di- port Bay, Orange Co., California, R. F Thorne amine, a procedure devised to deal with soft 45583 (RSA); L. commune S. F Gray, moist wood samples (Carlquist 1982). Sections were sand on bay side of Silver Strand, San Diego stained with a safranin-fast green combination. Co., California, E. A. Purer 5573 (RSA); L. cre Some sections of Lirnonium peregrinurn and L. taceum Tscherkassova, Akschagtau, Vil Dist., rurnicifoliurn were dried between clean slides, Aktjubinsk Prov., Kazakstan, I. Tcherkassova mounted on aluminum stubs, and studied with 5842 (RSA); L. peregrinum (Bergius) R. A. an ISI WB-6 scanning electron microscope Dyer; shrub to 1 m, branched from near base, (SEM). This procedure proved valuable in ex vicinity of Geelbek, Cape Prov., South Africa, 1996] CARLQUIST AND BOGGS: WOOD ANATOMY OF PLUMBAGINACEAE 137

S. Cariquist 4550 (RSA); L. perezii Hubbard, tive figures for this feature are available only for cultivated in Santa Barbara, California; L. rum a scattering of families (but see Carlquist and icifolium (Svent.) Kunkel & Sund., perennial Hoekman 1985). A high degree of vessel group with short woody caudex, on cliffs well into ing is shown by Limonium cretaceum (Fig. 19), canyon from highway, Barranco de Angostura but appreciable vessel grouping can also be seen near Era del Cardon, Tenerife, Canary Islands, in other transections (Figs. 1, 2, 6, 10, 12, 14, Spain, S. Cariquist 2604 (RSA); Plumbago Ca 18, 20, 21). Vessels occur in radial chains in pensis Thunb., cultivated in Claremont, Califor earlier-formed secondary xylem of Plumbago nia. capensis (Fig. 1), but this pattern disappears in Quantitative data are given in Table 1. Vessel later-formed secondary xylem (Fig. 2). Radial diameter is measured as the widest radial lumen chains are also evident in Aegialitis annulata diameter. The mean number of vessels per group (Fig. 21). In the remaining Plumbaginaceae, ves is based on a single vessel 1, two vessels in sel grouping is in the form of pore multiples. contact = 2, etc. Figures for vessel density (no. Vessel lumen diameter (Table 1, column 2) of vessels per mm2) are derived from survey shows a range from 9 to 32 lIm, with a mean of only of secondary xylem; conjunctive tissue 19 m. The narrowness of vessels in Plumba (Aegialitis) is not included. Terminology follows ginaceae can be placed in proportion by men the IAWA Committee on Nomenclature (1964). tioning that Metcalfe and Chalk (1950) found a mean vessel diameter of 94 jm for the world Results. ANAToMicAL DEscRIvrioNs. Growth flora (probably mostly tree species), and Carl rings are present or absent in Plumbaginaceae. quist and Hoekman (1985) reported a mean ves Strictly diffuse porous species include Plumbago sel diameter of 35.2 pm for the woody southern capensis (Figs. 1, 2) and Limonium peregrinum California flora. Admittedly, both of those (Fig. 6). No growth rings were observed either means are based on external vessel diameter, but within or between successive secondary xylem that usually adds 6 pm or less to the diameter. strands of Aegialitis annulata (Fig. 21). In the Vessel diameter is a sensitive indicator of wood remaining species, there is a slight to marked xeromorphy, and will be discussed in connection differentiation in vessel diameter or abundance with the ecological conclusions later. with respect to season. At the center of the tran Vessel density (Table 1, column 3) is ex section photograph of Limonium arborescens pressed in mean number of vessels per mm2. (Fig. 10), vessels are somewhat more abundant. Vessel density for the family as a whole (515) In a section of a root of this species (Fig. 12), a is relatively high compared with other families. parenchyma band (top) includes both latewood In the woody southern Californian flora as a and some earlywood, with noticeable difference whole (Carlquist and Hoekman 1985), the mean in vessel diameter within the parenchyma band. figure is 100, and that figure is much higher than Noticeable change in vessel diameter is also what one finds in trees of wet forests. Relatively present in L. californicum (Fig. 18). Strongly low vessel density for the family occurs in marked growth rings are present in L. cretaceum Plumbago capensis (Figs. 1, 2) and Aegialitis (Fig. 19). In this species, growth rings begin annulata (Fig. 21). Both of these species have with relatively wide (for this species) vessels, what has been termed vessel restriction patterns but then vessels are followed by a band of thick (Carlquist 1988). In Plumbago capensis, vessels walled libriform fibers, after which more wide tend to occupy the central portions of fascicular vessels, then narrow latewood vessels are xylem in earlier-formed secondary xylem (Fig. formed. Growth rings in Acantholimon cary 1), with no vessels in contact with rays. In later- ophyllaceum are like those of L. cretaceum, but formed secondary xylem (Fig. 2), this pattern no libriform fibers are present. In L. peregrinum, vanishes. In Aegialitis annulata, vessels also the transition from latewood to earlywood (not tend to occur in radial chains in the centers of shown in Fig. 6) is evident in formation of wider xylem areas (Fig. 21) and are not distributed and fewer vessels in earlywood, followed by randomly within these areas of libriform fibers. narrower and more numerous vessels in late- Limonium cretaceum also has a type of vessel wood. restriction: vessels are absent midway into the Mean number of vessels per group (Table 1, growth ring, where they are replaced by thick- column 1) shows a range from 1.3 to 6.2. The walled libriform fibers (Fig. 19). mean. 3.7, is well above the mean one would Vessel element length (Table I, column 4) in find in most families of dicotyledons Compara Plumbaginaceae is notably low, 100 tim. The

tim).

10

(divisions 4 Fig.

= above

scale 4—5, pm); Figs. 10 (divisions I Fig. = above scale 1-3,

Figs.

(below). shaved not

is wall when appear they as pits and (above) grooves showing 5. Section apertures.

pit

interconnecting show

grooves as to so sectioning by shaved wall of part outer showing Section 4. section.

tangential

from

walls of

vessel Sections tall. 4—5. very are rays section; 3. Tangential chains. radial in not vessels

xylem;

secondary

of later-formed

2. Transection areas. of fascicular portions central to restricted chains, radial in

vessels xylem; secondary

earlier-formed of Transection 1. capensis. Plumbago of sections Wood 1—5. Figs.

3

Ii

[VoL. 123 CLUB BOTANICAL TORREY THE OF BULLETIN 138 1996] CARLQUIST AND BOGGS: WOOD ANATOMY OF PLUMBAGINACEAE 139

‘it

Iii

Figs. 6—9. Wood sections of Lirnonium peregrinum. 6. Transection, no growth ring activity evident. 7. Tan gential section; rays absent. 8—9. SEM photographs of vessels from tangential section. 8. Wider vessel; helical thickenings less prominent. 9. Narrower vessel; helical thickenings more prominent. Figs. 6—7, scale above Fig. I; Figs. 8, 9, scales in upper left = 5 p.m.

m). 10

12 (divisions Fig. above 12, = scale Fig. 1. Fig. above scale 10, 13, 11, Figs. cells. upright

of

composed are

rays

section; tangential rumicifolium, L. 13. above. parenchyma, axial of band of root; section

12. Tran

portions.

central in cells procumbent rays contain of stem; Section Tangential 11. compound. staining

dark

contain rays stem; of

Transection 10. arborescens. L. 10—12. of Limoniuin. sections Wood 10—13. Figs.

123 [VoL. CLUB BOTANICAL TORREY THE OF BULLETIN 140 1996] CARLQIJIST AND BOGGS: WOOD ANATOMY OF PLUMBAGINACEAE 141

k 7

Figs. 14—17. Wood sections of Lünonium rumicifolium. 14. Transection; arrows indicate idioblasts that bear a single silica body each. 15. Tangential section; dark fusiform objects are silica bodies; arrows indicate stories in pairs of vessel elements. 16—17. SEM photographs of silica bodies from tangential section. 16. Portion of silica body; surface shaved by sectioning (upper 2/3 of photograph) shows pores in silica. 17. Tip of a silica body (left), showing rough surface; portion of silica body exposed by sectioning, extreme right. Figs. 14, 15, scale above Fig. 12; Figs. 16, 17, scales at upper left = 5 p.m.

12. Fig. above 1: scale 21, 19, Figs. Fig.

above 20, scale

18, Figs. xylem. secondary the in chain radial a form deposits): vessels dark-staining contains

(which

tissue conjunctive by sides all on surrounded tissue vascular of strand a of Transection 21. pith. in cambia

by

produced phloem) secondary associated xylem (with secondary of wedges of transection commune, L. 20.

earlywood.

the

amid formed are fibers libriform xylem: the fascicu]ar in types formed of cell sequence showing

transection

L.

19. cletaceum,

xylem.

secondary in earlier-formed present only are fibers libriform below: pith near

portion

of wood

transection L. cal(fornicunz 18. Aegialitis. and Limonium of sections Wood 18—21. Figs.

21

- 20 , .

•

I4 • • • •.

0’ 41

:

-.

.-• •

. :.. ,...-.

d* 1

r

T ‘-.

‘c > -

i

•Q

[VoL. 123 CLUB BOTANICAL THE TORREY OF BULLETIN 142 19961 CARLQUIST AND BOGGS: WOOD ANATOMY OF PLUMBAGINACEAE 143 mean length for the woody southern Californian jim in Plumbaginaceae. The length of imperfo flora is 233 jim (Carlquist and Hoekman 1985), rate tracheary elements roughly parallels that of and the figure for the world flora is given as 649 vessel elements. Imperforate tracheary elements jim by Metcalfe and Chalk (1950). Vessel ele were not observed at all in Acantholimon cary ment length is closely related to wood xeromor ophyllaceum or Armeria maritima; in these spe phy or mesomorphy (Carlquist 1988) and will cies, axial parenchyma substitutes for imperfo be discussed below with respect to ecological rate tracheary elements. A few vasicentric tra conclusions. cheids were observed in Acantholimon cary Mean vessel wall thickness (Table 1, column ophyllaceum. 5) for the family is relatively great (3.3 jim) con The wall thickness of imperforate tracheary sidering the narrowness of vessels (in dicotyle elements is shown in Table 1, column 7. Rela dons at large, wider vessels tend to have thicker tively thin-walled libriform fibers occur in Plum walls). The vessels of Aegialitis annulata (Fig. bago capensis (Figs. 1, 2) and Ceratostigma 21) are typical for the family. Vessels of Limon griffithii, whereas relatively thick-walled libri ium rumicifolium (Fig. 14) are relatively thicker form fibers are present in Limonium arborescens than the average for the family. In L. cretaceum (Fig. 12), L. perezii, L. rumic(folium (Fig. 14), (Fig. 19), there is a marked fluctuation in vessel and L. cretaceum (Fig. 19). wall thickness: narrower vessels have thinner One can compute a ratio between imperforate walls. tracheary element length and vessel element All vessels in Plumbaginaceae have simple length (Table 1, column 8). This ratio, some perforation plates. Lateral wall pits of vessels in times called the “F/V ratio,” is, within limits, Plumbaginaceae are relatively small. Lateral an indicator of phyletic advancement: ratios be wall pits circular in outline with a pit cavity di tween 1.0 and 1.5 indicate primitiveness; higher ameter of about 3 jim were observed in Limon ratios (ratios above 4.0 are infrequent) indicate ium arborescens, L. perezii, and L. rumicifolium. a greater degree of division of labor between the Circular pits about 4 jim in diameter occur in conductive (vessels) and the mechanical systems Acantholimon caryophyllaceum, Plumbago Ca (fibers) in woods (Carlquist 1975). The F/V val pensis (Fig. 5), and L. perezii (Figs. 8, 9). Cir ues for Plumbaginaceae are relatively high com cular pits about 2.5 jim in diameter occur in Ae pared to those found in families commonly gialitis annulata and Ceratostigma griffithii. thought to have primitive wood (e.g., Illici Pseudoscalariform pits (pits alternate in arrange aceae). ment, yet greatly widened laterally) occur in Axial parenchyma in Plumbaginaceae consists vessels of Armeria maritima, L. caitfornicum, L. of undivided cells except for Ceratostigma grif commune, and L. cretaceum. fithii, in which axial parenchyma is subdivided There are two forms of sculpturing on vessel into strands of two cells, and Plumbago capen walls of Plumbaginaceae. Pluinbago capensis sis, in which strands consist of 1—6 (mostly 3— has grooves interconnecting pit apertures (Figs. 4) cells. As seen in wood transections, axial pa 4, 5). Grooves of this sort also occur in Aegi renchyma consists of occasional paratracheal alitis annulata, Limonium perezii, and L. rumi cells. These can be seen as relatively thin-walled cifolium. Helical thickenings on vessel walls are (and therefore wide-lumened) cells adjacent to a second type of sculpturing, and were observed vessels in Fig. 21. In Limonium arborescens in L. peregrinum (Figs. 8, 9). In this species, (Figs. 10, 12), L. peregrinum (Fig. 6), L. perezii, helical thickenings are less pronounced in wider and L. ru.’nicifolium (Fig. 14), axial parenchyma vessels (Fig. 8) than in narrower vessels (Fig. is scanty but almost always abaxial to the vessel 9). Similar helical thickenings were observed in in position. Axial parenchyma is both paratra Acantholimon caryophyllaceum. cheal scanty and abaxial in Ceratostigma griffi Imperforate tracheary elements in Plumbagi thu and Plumbago capensis (Figs. 1, 2). naceae have simple pits except for Limonium Toward the periphery of the root of Limonium perezii and L. rumicifolium, in which very nar arborescens, there are bands of marginal axial row vestigial borders were observed. Nucleate parenchyma (one such band, Fig. 12, top). Acan libriform fibers bearing a single septum were tholimon caryophyllaceum has, in addition to seen in Plumbago capensis; 2—4 septa per libri scanty paratracheal parenchyma, diffuse-in-ag form fiber occur in Ceratostigma griffithii. gregates and terminal bands. Limonium creta Mean imperforate tracheary element length ceum (Fig. 19) has axial parenchyma throughout (Table 1, column 6) ranges from 226 jim to 411 fascicular areas except for the middle portions

con- of

a background in outline, transectional in much larger and 17) (Fig. shape in fusiform are

to oval strands, circular form of takes the tissue bodies silica The rays. of cells tip as occur few

vascular The cambia. by successive produced A arrows). 14, (Fig. wood the of portion fibrous

phloem secondary and xylem secondary have the in diffusely distributed idioblasts in occur

does annulata Aegialitis doubtful. as tholimon bodies silica These arborescens). L. in rarely,

Acan for type this of wood of report (1936) (also, rumicfoliuni L. perezii and L. in present

Record’s regard we therefore and phloem, is occurrence mode of unusual an with body ica

contain not do bands these but parenchyma, sil type of unusual very A in Plumbaginaceae.

of terminal bands prominent has Acantholimon reported been hitherto not have bodies Silica

of material Our and Limoniastrum. gialitis, 13). (Fig. rumicifolium L. and (Fig. Ii) cens

Ae Acantholimon, in (1936) by Record reported arbores L. by illustrated are family the for ical

was cambia successive from produced Wood typ more Conditions family. the for tall usually

1988). (Carlquist 3) un are (Fig. capensis Plumbago of 9). Rays

in Plumbaginaceae reported been not previously column 1, (Table and narrow 9) column I, ble

has Storying derivatives. initial cambial form (Ta short relatively are family the in Rays type.

from fusi mature they as little elongate that strands to referable are studied Plumbaginaceae

or cells axial parenchyma and elements the sel of rays all thus and 1988), II Type (Carlquist

Ves pattern. storied the obscuring thereby ently, to Paedomorphic correspond cells upright of

differ elongates each element 8), and column mostly consist that and only multiseriate are that

1, Table ratio, F/V (see considerably elongate Rays cretaceum. L. and commune, L. fornicum,

elements tracheary imperforate Plumbaginaceae, cali L. griffithii, Ceratostigmcz annulata, alitis

In of elongation. cell because cells in wood in Aegi observed were cells ray upright Only

be evident not may storying species, most in but as well. 3) (Fig. capensis Plumbago and iu.’n,

in Plumbaginaceae, uncommon are not cambia perezii, rumicifol L. L. in occurs situation This

likely, storied Very carefully. sections tangential are upright. ray cells of the half than more cies

one examines fibers if libriform in many seen be spe in that 11), but Fig. arborescens, Limonium

can storying capensis, Plumbago and gr(ffithii (e.g., species some in of rays centers the in cells

Ceratostigma perezii. In L. and arborescens procumbent are there However, II. Type geneous

L. seen in also sort was this of Storying rows). Homo to Kribs’s be referred could they cells,

ar 15, (Fig. rumic(folium Limonium of cells procumbent of consisted rays these If served.

parenchyma and axial vessels the all, of means ob were rays no uniseriate Plumbaginaceae,

no by but some, in be seen can Storying in multiseriate are rays All Figs. 1—3). (e.g.,

spots). blackish 21, rays primary of extensions are rays most that

(Fig. annulata of Aegialitis tissue conjunctive rays, and few relatively initiates cambium the

in prominently occur compounds Dark-staining that suggesting Plumbaginaceae, other most in

material. unstained in yellowish appear often infrequent relatively are Rays present. is lessness

compounds 12). These (Fig. in as vessels as well ray of form partial a so rays, no adds lar areas

10) (Fig. arborescens L. cells of ray in seen be in fascicu cambium the cajyophyllaceum; mon

can prominently stain that compounds of posits Acantholi of wood in present are rays primary

de Massive substance. tanninlike a of position of extensions Only 7). (Fig. peregrinum monium

de suggesting perhaps color, red-brown a have Li and maritima in Armeria are absent Rays

Limonium of woods aspect, gross seen in As by parenchyma. axial replaced

17). (Fig. surface warty only partly are fibers libriform because cheal,

almost rough, and surface) shaved in vealed paratra and pervasive between intermediate

re pores 16, (Fig. structure porous 1988): quist is parenchyma commune, L. In of photograph).

Carl (see elsewhere silica bodies seen in half istics bottom growth, secondary in earlier formed

character show SEM with studied when bodies fibers libriform of patches (Fig. 18; nicum

silica The 17). Fig. in left at body silica in break califor Limonium characterizes also renchyma

(note broken are in sections bodies of silica the pa axial Pervasive 1995a). (Cariquist pervasive

most and brittleness, their size of long. Because termed been has that a type type, this of ma

p.m 100 than are more L. ezii and rumicifolium parenchy has axial maritima Armeria elements.

per L. of bodies silica the whereas diameter, in tracheary imperforate all replaces it that species

p.m 50 exceed not do and ovoid to spherical are some in so abundant is parenchyma Axial

silica bodies dicotyledons, most In 1976). Welle fibers. libriform

(ter

dicotyledons in elsewhere bodies silica than thick-walled of consists which rings, of growth

123 CLUB [VoL. BOTANICAL TORREY THE OF BULLETIN 144 1996] CARLQUIST AND BOGGS: WOOD ANATOMY OF PLUMBAGINACEAE 145 junctive tissue (Fig. 21). Some strands of vas autochthonously from herbaceous or minimally cular tissue that are tangentially wider in this woody ancestors (Carlquist 1974). The woodi species may contain one or two rays that have ness of the two shrubby Canarian Limonium spe been derived from cambial action, and these rays cies relates to minimal frost in the habitats consist of upright cells. Conjunctive tissue be where those species occur. tween the strands of vascular tissue does not qualify as ray tissue. ECOLOGICAL CoNcLUsIoNS. Wood xeromorphy The conjunctive tissue of Aegialitis annulata can be measured by means of a formula termed (Fig. 21) is composed of thin-walled parenchy the Mesomorphy Ratio (vessel diameter times ma cells with dark-staining contents. In addition, vessel element length divided by number of ves there are numerous idioblastic astrosclereids in sels per mm2: see Carlquist and Hoekman 1985). the conjunctive tissue. These sclereids take the The Mesomorphy Ratio value for desert shrubs form of cells with cuboidal shapes from which of southern California is 20.9; the value for al slender arms radiate. pine southern Californian shrubs is 27.1 (Carl Successive cambia are commonly found in the quist and Hoekman 1985). These values are no cortex of stems or roots of dicotyledons, but in tably low compared with those of woods from a few instances, successive cambia form in the more mesic regions, but they are higher than the pith (Carlquist 1988). These latter cambia have Mesomorphy Ratio values of Plumbaginaceae been termed centripetal cambia, and have been (Table I, column 11). The mean Mesomorphy reported for only a few families of dicotyledons Ratio value for the family is 4.1. This accords (see Cariquist 1988: 262). There is secondary with the concept that Plumbaginaceae character xylem and secondary growth produced by the istically grow in dry and/or saline habitats. Not action of centripetal cambia in the pith of Li surprisingly, Plumbago capensis, which has monium californicum and L. commune (Fig. 20). broad thin leaves and grows in moderately moist Each of these cambia produce considerable sec scrub, has the highest value for the family (30). ondary growth, which can be accommodated as Limonium arborescens also has a value relative growth proceeds because of the large diameter ly high for the family (23); it occurs in moder of the pith and the ability of the thin-walled pith ately moist scrub on the north side of Tenerife cells to collapse. (Bramwell and Bramwell 1974). The next high est value for the family is represented by the Conclusions and Discussion. HABITAL CON mangrove Aegialitis annulata. One can make a CLUSIONS. Raylessness has been associated with case that a mangrove is not in a dry situation, herbaceous groups in which a transition to (or since the water supply is unlimited, although a sometimes possibly from) a woody habit is oc mangrove must counter the osmotic pressure of curring (Barghoorn 1941, Carlquist 1970, Gib saltwater. However, Aegialitis annulata is an in son 1978). Raylessness in Armeria maritima and tertidal mangrove, and its roots are occasionally Limonium peregrinum may therefore indicate exposed. The lowest Mesomorphy Ratio values secondary woodiness in those species. Acan for the family occur in species characteristic of tholimon catyophyllaceum does not initiate rays localities that are both dry and salty: Acanthol from fascicular cambium areas, and thus is, in a imon caryophyllaceum (0.6) and Armeria man sense, rayless. The occurrence of paedomorphic tima (0.5). One can view wood xeromorphy in rays in the remainder of Plumbaginaceae may terms of any of the three quantitative vessel el also be an indication of secondary woodiness. ement features that make up the Mesomorphy The woodiest species of Plumbaginaceae are Li Ratio, but these three measures tend to run par monium arborescens and L. dendroides on the allel to each other. Canary Islands. These likely are woody deriva Another quantitative vessel feature that tends tives of more nearly herbaceous ancestors. An to indicate wood xeromorphy is the mean num alternative hypothesis would have to say that ber of vessels per group. Vessels tend to stay these restricted insular species are relicts from solitary in woods that have tracheids as the im which the remainder of this worldwide genus perforate tracheary element type, regardless of have been derived—a hypothesis that seems ecology, but if a wood has fiber-tracheids or li quite unlikely. The habital diversification of Li briform fibers, greater degrees of vessel group monium on the Canary Islands seems much like ing indicate greater xeromorphy. This is shown what has happened on other islands where di by the fact that the two species with the lowest verse woody growth forms have been derived Mesomorphy Ratio values for the family, Acan 146 BULLETIN OF THE TORREY BOTANICAL CLUB [VoL. 123

tholimon ccnyophyllaceum and Armeria mariti basis of so few species, these distinctions may ma, have the highest figures for number of ves prove consistent for the two subfamilies. sels per group. With respect to affinity of Plumbaginaceae to In addition to quantitative vessel features, other families, wood anatomy is of interest be there are qualitative wood features that indicate cause new ideas have recently been been offered xeromorphy. Helical thickenings in vessels are on relationships of the family. Rodman et al. indicative of greater degrees of physiological (1984) hypothesized that Plumbaginaceae and drought (Carlquist 1975). In the present study, Polygonaceae are close to each other and to Car Acantholimon caryophyllaceum and Limonium yophyllales; Williams et al. (1994) agreed with peregrinum have helical thickenings. Helical this conclusion, but place Droseraceae and Ne thickenings may be lacking in other species for penthaceae equally close to Plumbaginaceae. various reasons; for example, the pseudoscalar Nepenthes has xylem more primitive than that iform pitting may preclude the formation of he of Plumbaginaceae in several significant re lical thickenings. spects: scalariform as well as simple perforation Presence of parenchyma instead of imperfo plates; tracheids as imperforate tracheary ele rate tracheary elements characterizes the two ments; diffuse-in-aggregates axial parenchyma; woods with the lowest Mesomorphy values, and presence of both multisenate and uniseriate Acantholimon caryophyllaceum and Armeria rays (Carlquist 1981). The wood of Drosophyl maritima. A relatively high degree of parenchy lum (Droseraceae) is very similar to that of Ne matization characterizes other Plumbaginaceae: penthes, but has simple perforation plates exclu Limonium californicum and L. commune. One sively. Wood anatomy thus validates the conclu can hypothesize that parenchyma of conjunctive sion of Williams et al. (1994) that Droseraceae tissue in Aegilitis is physiologically equivalent and Nepenthaceae are close to each other, but to parenchyma within the wood of other Plum wood data, interpreted according to usual crite baginaceae. Parenchyma likely serves for water ria, would place that pair of families at a lower storage to some degree. In this connection, it level of specialization than Plumbaginaceae, Po expands and contracts with water availability. If lygonaceae, or Caryophyllales. parenchyma contracts and expands, adjacent PLumbaginaceae have simple perforation vessels would be affected. The presence of pseu plates exclusively, minute pits on lateral walls doscalariform pitting in vessels of Armeria mar of vessels, libriform fibers as the imperforate tra itima, Limonium californicum, L. commune, and cheary element type (vestigial borders on pits in L. cretaceum is notable may permit increase ves a few species), paratracheal axial parenchyma, sel flexibility, and certainly those species do multiseriate rays or no rays. All of these features have abundant axial parenchyma. can be seen in Polygonaceae also, as can two features reported newly here for Plumbagina SYSTEMATIC CoNcLusioNs. Wood anatomy ceae: storying and presence of silica bodies (Carl only infrequently is useful at the species level. quist 1988). To be sure, the mode of occurrence Howevei the wood anatomy of Limonium per of silica bodies in Plumbaginaceae is different ezii is virtually identical to that of L. rumicfo1- from that in Polygonaceae. Polygonaceae differ ium. This supports the idea of Bramwell and from Plumbaginaceae in ray type: Polygonaceae Bramwell (1974) that L. rumicifolium represents have both multiseriate and uniseriate rays, and an inland population very similar to L. perezii most species studied do not have paedomorphic and the that two populations may be conspecific. rays like those of Plumbaginaceae. These differ Plumbaginaceae are divided into two subfa ences between the two families could easily be milial groups, currently called Plumbaginoideae due to different ancestry: Polygonaceae (at least and Staticoideae (Pax 1891; Thorne 1992). Of the typically woody species) probably derive the genera in the present study, Ceratostigma from a woody ancestry, whereas Plumbagina and Plumbago belong to Plumbaginoideae, ceae likely have had an herbaceous or relatively whereas the remaining genera studied are placed less woody ancestry. in Staticoideae. Ceratostigma and Plumbago are Rodman et al. (1984) chose Plumbaginaceae alike in having nucleate septate fibers that tend and Polygonaceae as outgroups for their cladis to be clearly storied, and also agree in having tic and phenetic study of Caryophyllales, and the strands of more than one cell in axial parenchy results of that study tend to support that choice. ma. Alternative conditions occur in the Staticoi Williams et al. (1994) confirm such a relation deae. Although conclusions are premature on the ship on the basis of rbcL sequence data. All of 19961 CARLQUIST AND BOGGS: WOOD ANATOMY OF PLUMBAGINACEAE 147 the features listed in the preceding paragraph 1988. Comparative wood anatomy. Springer can be found in Caryophyllales. However, tra Verlag, Berlin. 436 p. 1 995a. Wood and bark of Ranunculaceae (in cheids rather than fiber-tracheids or libriform fi cluding Hydrastis) and Galucidiaceae. Aliso 14: bers occur in Stegnospermataceae (Bedell 1980) 65—84. and some Caryophyllaceae (Cariquist 1995b). If 1995b. Wood anatomy of Caryophyllaceae: tracheids are a presumably more primitive wood ecological, habital, systematic, and phylogenetic implications. Aliso 14: 1—17. expression, can Stegnospermataceae and Cary AND D. A. H0EKMAN. 1985. Ecological wood ophyllaceae be derived from a group that only anatomy of the woody southern California flora. have libriform fibers or fiber-tracheids like libri IAWA Bull., n.s., 6: 3 19—347. form fibers? Currently accepted concepts of AND E. J. WILsoN. 1995. Wood anatomy of wood evolution would say this is unlikely. An Drosophyllurn (Droseraceae); ecological and phy logenetic considerations. Bull. Torrey Bot. Club other possibility is that now-vanished tracheid 122: 185—189. bearing ancestors of Plumbaginaceae and Poly CR0NQuIsT, A. 1988. The evolution and classification gonaceae gave rise to the line that led to Cary of flowering plants, ed. 2. The New York Botanical ophyllales. Except for this feature, wood of Car Garden, Bronx, New York. 555 p. GIBsoN, A. C. 1978. Rayless secondary xylem of Hal compatible with the possibility yophyllales is ophytum. Bull. Torrey Bot. Club 105: 39—44. that order has been derived from an ancestor IAWA C0MMrrrEE ON NoMENcLATURE. 1964. Multi with wood like that of Plumbaginaceae or Po lingual glossary of terms used in wood anatomy. lygonaceae. However, we need more informa Verlagbuchanstalt Konkordia, Winterthur, Switzer tion on wood of Caryophyllales, and we need land. 186 p. KRIBS, D. A. 1935. Salient lines of structural special more information on wood of Polygonaceae. ization in the wood rays of dicotyledons. Bull. Tor When woods of these groups, currently under rey Bot. Club 64: 177—186. study, are better understood, more precise phy METcALFE, C. R., AND L. CHALK. 1950. Anatomy of letic analyses will be possible. the dicotyledons. Clarendon Press, Oxford. NowIci, J. W. AND J. J. SKvAIuA. 1977. 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A tax of Plantago and the problem of raylessness. Bull. onomic analysis and revised classification of Cen Torrey Bot. Club 97: 353—361. trospermae. Syst. Bot. 9: 297—323. 1974. Island biology. Columbia University TER WELLE, B. J. H. 1976. Silica grains in woody Press, New York. 660 p. plants of the neotropics, especially Surinam, pp. 1975. Ecological strategies of xylem evolu 107—142. In P Baas, A. J. Bolton and D. M. Catling tion. University of California Press, Berkeley. 259 p. [eds.1, Wood structure in biological and technolog 1981. Wood anatomy of Nepenthaceae. Bull. ical research Leiden Bot. Ser. 3, Leiden Univ. Torrey Bot. Club 108: 324—330. Press, Leiden 1982. The use of ethylene diamine in soft THORNE, R. F 1992. Classification and geography of ening hard plant structures for paraffin sectioning. the flowering plants. Bot. Rev. 58: 225—348. Stain Technol. 57: 311—317. WILLIAMs, S. E., V. A. ALBERT AND M. W CHASE. 1984. Vessel grouping in dicotyledon woods: 1994. 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