Wood Anatomy of Krameriaceae with Comparisons with Zygophyllaceae: Phylesis, Ecology and Systematics

Botanical Journal of the Linnean Society, 2005, 149, 257-270. With 20 figures

Wood anatomy of Krameriaceae with comparisons with Zygophyllaceae: phylesis, ecology and systematics

SHERWIN CARLQUIST FLS*

Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105, USA

Received March 2005; accepted for publication June 2005

Wood of nine species of Krameria (including all clades proposed within the genus) reveals a few characters related to infrageneric systematics; most relate primarily to ecology and habit. Wood of Krameria closely fits quantitative data reported for desert shrubs. Lack of vessel grouping correlates with the presence of densely pitted tracheids. Wood xeromorphy in Krameria may relate in part to hemiparasitism. Tracheid presence may also account for relatively low vessel density. Wood anatomy of six species of Zygophyllaceae (including both genera of Morkillioideae) is compared with that of Krameriaceae because recent phylogenies propose that these two families comprise the order Zygophyllales. Several wood characters appear to represent synapomorphies reflecting this relationship. Dif ferences in wood anatomy between Krameriaceae and Zygophyllaceae are believed to represent autapomorphies. Notable among these include Paedomorphic Type II rays (Krameriaceae), storying (Zygophyllaceae), presence of ves tured pits (Zygophyllaceae), and differentiation into vasicentric tracheids and fibre-tracheids (Zygophyllaceae). The latter feature is referable to the concept of fibre-tracheid dimorphism. Recognition of Krameriaceae as separate from Zygophyllaceae is supported by wood characters. Wood of Zygophyllales does not conflict with the idea that the order belongs to rosids, with Malpighiaceae as the outgroup of Zygophyllales. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 257-270.

ADDITIONAL KEYWORDS: axial parenchyma - ecological wood anatomy - paedomorphosis - rosids - storying — tracheid dimorphism - vessel grouping — vesturing — Zygophyllales.

INTRODUCTION phic wood (Carlquist, 1977; Carlquist & Hoekman, 1985). Simpson et at. (2004) considered Krameria, with 18 Ideas on the systematic relationships of Krameri species, to be the sole genus of Krameriaceae. The aceae have changed considerably. Earlier, the family range of the genus includes North America, West was considered a subfamily of Fabaceae (or even Indies and South America. Wood xeromorphy would be within Fabaceae, subfamily Caesalpinoideae), or else expected in these small-leaved shrubs, because of the near Polygalaceae (see Simpson, 1989; Simpson et al., relatively dry (at least seasonally) localities in which 2004). More recently, on the basis of data from DNA, they grow (see Simpson, 1989). The habits range from Krameriaceae have been aligned with Zygophyllaceae moderate-sized shrubs (to 6 m in Krameria cytisoides) (Chase etal., 1993; Savolainen et al., 2000; Soltis to subshrubs with somewhat woody underground et al., 2000). These newer studies form a striking stems and roots but prostrate herbaceous stems example of how molecular data have led to previously {Krameria lanceolata). The outline drawings in Simp unsuspected familial alliances within angiosperms. son (1989) demonstrate this range quite well. Such a When anatomical evidence is re-examined in the light range of habits invites comparisons with wood anat of molecular-based phylogenies, previously unappreci omy. The hemiparasitism of the genus (Cannon, 1910; ated similarities often become evident. In the present Simpson, 1989) is also relevant to interpretation of study, the resemblances between wood of Krameri wood anatomy; woody parasites have highly xeromor- aceae and Zygophyllaceae are so convincing that com parisons with families other than Zygophyllaceae are *E-mail: [email protected] only minimally considered.

Krameriaceae and Zygophyllaceae are now consid acuminata Rose & Painter, 29 km from Victoria on ered the only two families of Zygophyllales, an order road to Jaumave, Tamaulipas, Mexico, Johnston 5370 placed in the clade Eurosid I by Soltis etal. (2000). (TEX); Tribulus zeyheri Sond., granitic rocks in pass, Maintenance of Krameriaceae as a monogeneric south side of Swakopmund River, about 20 km E family separate from Zygophyllaceae under these cir of Swakopmund, Namibia, Carlquist 8082 (RSA); cumstances can be questioned, and in this context, Viscainoa geniculata (Kell.) Greene, dunes 8 km S of presentation of wood anatomical differences between Mulege, Baja California Sur, Mexico, Daniel 6778 the two families becomes significant. The treatment (SBBG). of the family Zygophyllaceae here follows that of Material of K. lanceolata was received as living Sheahan & Chase (1996). Those authors excluded plants; stem and root portions were preserved in 50% Nitraria and Peganum as the families Nitrariaceae aqueous ethanol. Material of all other species of and Peganaceae, respectively, of the Sapindales. Krameria was available as dried stems; these were Sheahan & Chase (1996) included Balanites, segre boiled in water, stored in 50% aqueous ethanol and gated as a monogeneric family by some authors, sectioned with a sliding microtome. The material of within Zygophyllaceae. K. lanceolata was softened with ethylene diamine and Few data on wood of Krameriaceae have been sectioned in paraffin according to the schedule of Carl offered hitherto. Aside from Kunz (1913), the observa quist (1982). Sections were stained with a safranin- tions of Metcalfe & Chalk (1950) contain the most fast green combination. This usually reliable method information. Numerous papers and books contain is adequate for Krameria woods, but staining of ligni- observations on wood anatomy of Zygophyllaceae (see fied cells is less intense than is typical for dicotyledon Gregory, 1994), although most published information woods stained in this fashion. The ethylene diamine- is derived from study of three arborescent genera: treated material of K. lanceolata stained more deeply. Unstained sections of selected species were dried Balanites, Bulnesia and Guaiacum. The summary of between glass slides, sputter-coated with gold, and wood anatomy of Zygophyllaceae by Metcalfe & Chalk studied with a Hitachi S2600N scanning electron (1950) remains a convenient source of information. microscope (SEM). Macerations were prepared from alcohol-stained material with Jeffrey's Fluid and MATERIAL AND METHODS stained with safranin. The materials studied here show an adult pattern for their respective species The collections of Krameria studied are as follows: except for Viscainoa geniculata, in which a stem K. cistoidea J. W. Hook, and Arn., 30 km E of Combar- approximately two years old was studied. lala, Coquimbo, Chile, Simon 234 (RSA); K. cytisoides Cav., 9 km NE of Vizmon, Queretaro, Mexico, Zamudio Diameter of vessels was computed as lumen diam 2692 (MEXU); K. erecta Willd, & Schult. ex Schult eter because the latter has more significance than out (det. As K navae Rzed.), 2.6 km SE of Acuna, Guadal- side diameter with respect to xylem conductive cazar, San Luis Potosi, Mexico, Torres 15007 (MEXU); physiology. Vessels oval in transection were measured K. erecta (det. as K parvifolia Benth. var. imparata as an average of long and short chords. Measurements (Britton) J. F. Macbr.), near Jacumba, San Diego Co., presented in Table 1 are derived from averages of 25 California, Til forth 415 (RSA); K. grayi J. Rose & R. A. measurements per feature. The presentation of famil Painter, Coyote Pass, just E of Oatman, Mohave Co., ial means for Krameriaceae facilitates comparisons Arizona, Carlquist 15826 (RSA); K. grayi, 'Colorado within the genus Krameria and aids in ecological com Desert' (presumably Sonoran Desert of Arizona), coll. parisons. Terminology is in accord with the LAWA /. Webber, SJRw 27012; K. lanceolata Torr., Bracken- Committee on Nomenclature (1964). Usage of the ridge Field Station of the University of Texas, Austin, term 'tracheid' follows LAWA Committee on Nomencla Texas, herbarium specimen from live material sent by ture (1964) and Carlquist (1984, 2001) and use of the B. B. Simpson preserved as Carlquist 15947 (RSA); terms 'fibre-tracheid' and 'vasicentric tracheid' follows K. lappacea (Downey) Burdet & Simpson, Santa that of Metcalfe & Chalk (1950) and Carlquist (1985a, Catalina, Jujuy, Argentina, Zuloaga 6111 (MO); 2001). K. secundiflora Mocino & Sesse ex A.P. de Candolle, Hernandez 4571 (MEXU); K. sonorae Britton, Wiggins 244 (DS), USw-34156; K. tomentosa A. St.-Hil., Brazil, Mattos Silva 2995 (TEX). Collections of Zygophyl RESULTS laceae studied are as follows: Fagonia laevis Standley, GROWTH RINGS near Jacumba, San Diego Co., California, Tilforth 417 Most species of Krameria have at least some evidence (RSA); Guaiacum guatemalense (Planch.) Rydb. & of growth rings characterized by more numerous and Vail, Heimsch slide 14926; Larrea tridentata (Sesse & wider vessels in earlywood, with fewer and narrower Mocino ex DC) Coville, Bissing 200 (RSA); Morkillia vessels in latewood. No growth rings were observed in

Table 1. Wood characteristics of Krameriaceae and Zygophyllaceae

1 2 3 4 5 6 7 8 9 Species VG VD VL VM TL AP RH UR ME

Krameriaceae Krameria cistoidea 1.23 25 192 243 437 d, da, m U 208 2d K. cytisoides 1.19 23 166 203 488 d, m U 100 19 K erecta Tilforth 415 1.16 26 91 289 251 b, d, da, m I' 177 8 K. erecta Torres 15007 1.52 21 168 160 373 b, d, da, m U 162 20 K. grayi Carlquist 15826 1.04 32 178 146 466 d, da, m Us 186 26 K. grayi SJRw-27012 1.07 27 130 179 403 d, m u 304 19 K. lanceolata stem 1.43 2.1 125 139 273 d, da, w u 171 28 K. lanceolata root 1.05 41 142 156 385 d, da, m u 223 37 K. lappacea 1.15 15 294 167 504 d, da, m u 110 7 K. secundiflora 1.29 27 239 114 178 d V 198 13 K. sonorae 1.03 25 88 223 736 (1 u 320 63 K. tomentosa 1.16 30 173 177 493 .1 u 121 :il Krameria genus averages 1.20 26 174 182 418 187 24 Zygophyllaceae Fagonia laevis 1.24 42 162 114 268 d USP 64 W Guaiacum guatamalense 1.01 32 47 110 173 a, d, da p 55 75 Larrea tridentata 1.02 29 88 125 172 d, da, m p 85 41 Morkillia acuminata 1.18 29 177 195 493 d u 196 32 Tribulus zeyheri 1.43 34 107 86 1180 d, vs usP 98 27 Viscainoa geniculata 1.23 41 84 240 669 d USp 212 117

Key to columns: 1 (VG), mean number of vessels per group; 2 (VD), mean vessel lumen diameter, um; 3 (VL), mean vessel element length, um; 4 (VM), mean number of vessels mm"-; 5 (TL), mean tracheary element length, um; 6 (AP), axial parenchyma types present (a, abaxial; b, narrow bands; d, diffuse; da, diffuse-in-aggregates; m, marginal; vs, vasicentric scanty; w, wide bands); 7 (RH), ray histology (u, upright; s, square; p, procumbent, upper case for more common occur rences); 8 (UR), mean height of uniseriate rays, um; 9 (ME), Mesomorphy Ratio (vessel diameter times vessel element length divided by vessels mm"2). Additional explanations in text. Collections cited in Material and Methods.

K. tomentosa. Minimal contrast between earlywood VESSELS and latewood is shown here for K. grayi (Fig. 1); K. erecta (Figs 5, 6) shows more marked differences Vessel grouping (Table 1, column 1) ranges from 1.02 between earlywood and latewood in diameter and to 1.43 vessels per group in Krameria, with the least number of vessels. Because the growth rings are nar vessel grouping in Sonoran Desert species such as row in K. erecta, vessels are more crowded in early- K. grayi (Fig. 1). Vessel grouping is somewhat elevated wood (Fig. 6). Growth rings similar to those in where growth rings are narrow; the earlywood vessels, K. grayi occur in Fagonia, Guaiacum (Fig. 16) and where numerous, are crowded and contacts are some Larrea. what more frequent (Fig. 6). The Zygophyllaceae stud Another feature of growth rings in most species of ied characteristically have solitary vessels (Figs 13, Krameria is the presence of marginal parenchyma. 14, 16). Presence of marginal parenchyma is indicated in Vessel lumen diameter (Table 1, column 2) is notably Table 1, column 6 Cm'). Diffuse-in-aggregates and nar narrow in Krameria. The range in diameters reported row banded axial parenchyma are scattered through for the genus by Metcalfe & Chalk (1950) is confirmed out woods of most species of Krameria, so that here. Vessels in the Zygophyllaceae studied are some separating those types from marginal parenchyma what wider than those of Krameriaceae (Figs 14, 16). is difficult. Whether the marginal parenchyma is Vessel density (Table 1, column 3) is often consid present in first-formed earlywood ('initial paren ered as approximately the inverse of vessel diameter chyma') or last-formed latewood ('terminal paren for any given species. However, species such as chyma') is difficult to discern because the marginal K. sonorae and Guaiacum guatemalense (Fig. 16) have bands are so narrow. The occurrence of terminal rather low vessel density. parenchyma seems more probable on the basis of my Vessel element length (Table 1, column 4) for observations. Krameriaceae is low, averaging 183 \im for the family.

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Figures 1-4. Wood sections of Krameria grayi (Carlquist 15826). Fig. 1. Transverse section. Arrow indicates a band of axial parenchyma that demarcates latewood from earlywood. Scale bar = 100 um. Fig. 2. Tangential longitudinal section; rays are uniseriate and are composed of upright cells. Scale bar = 100 um. Fig. 3. Transverse section. Dark-staining compounds fill the pit cavities and thereby show the bordered nature of the pits in tracheids (arrows indicate pit cavities in one tracheid). Scale bar = 20 um. Fig. 4. Upright ray cells from radial section; dark staining compounds are abundant in the cells and fill pit cavities; most pits are bordered. Scale bar = 20 um. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society. 2005, 149, 257-270 WOOD ANATOMY OF ZYGOPHYLLACEAE 261

Figures 5-8. Wood sections of Krameria. Scale bars = 10 |im. Figs 5-7. K. erecta (Tilforth 415). Fig. 5. TS; solitary vessels are common. Fig. 6. TS; a band of terminal parenchyma icentre) demarcates earlywood (above) from latewood (below); axial parenchyma cells do not have secondary walls. Fig. 7. TLS; vaguely storied axial parenchyma cells at upper left. Fig. 8. K. lanceolata above-ground stem; Axial parenchyma bands wide, variously shaped; parenchyma is so abundant that isolated strands of tracheids (arrows) occur.

2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 257-270 262 S. CAELQUIST

Figures 9-12. Wood sections of Krameria. Figs 9, 10. K. secundiflora, SEM photographs of tangential sections. Fig. 9. Vessel inside surface (left) and outer surfaces of tracheids (right); pits are nonvestured. Scale bar = 10 um. Fig. 10. Inside surfaces of tracheids; helical thickenings are present. Scale bar = 10 um. Figs 11, 12. Crystals in radial sections of K. sonorae. Fig. 11. SEM photograph, showing that crystals are of diverse in size. Scale bar - 10 urn. Fig. 12. Distribution of crystals: vertical arrows indicate axial parenchyma cells that contain crystals; horizontal arrow points to crystals in rays cells. Scale bar = 50 um. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 257-270 WOOD ANATOMY OF ZYGOPHYLLACEAE 263

Figures 13-16. Wood sections of Zygophyllaceae. Figs 13-15. Larrea tridentata. Scale bars = 50 um. TS earlywood; axial parenchyma is in the form of diffuse and diffuse-in-aggregates cells; dark-staining compounds fill many axial parenchyma and ray cells. Fig. 14. TS of latewood; axial parenchyma is chiefly in the form of diffuse cells; arrows point to idiobiastic axial parenchyma cells that contain crystals. Fig. 15. TLS; fibre-tracheids and axial parenchyma are storied (left); rhomboidal crystals are present in idiobiastic axial parenchyma cells. Fig. 16. TS wood of Guaiacum guatemalense; axial parenchyma is abaxial to vessels (most easily seen at top of photograph>. Scale bar = 100 um. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 257-270 264 S. CARLQUIST

However, the notably long vessels of K. cytisoides (Fig. 9). The pits are relatively small for dicotyledons, (488 (im) skew the familial average upwards. Vessel and range between 3 and 4 um in diameter. elements of the Zygophyllaceae studied are relatively In all Zygophyllaceae studied, both vasicentric tra short compared with those of Krameriaceae (the rela cheids and fibre-tracheids are present. This feature is tively long vessel elements of Viscainoa are inter revealed by longitudinal sections, although macera preted as correlated with the juvenile nature of the tions are required to confirm it. Presence of both vasi branch studied). centric tracheids and fibre-tracheids was most obvious Vessels are circular to oval in outline in Krameri in Fagonia laeuis, Morkillia acuminata and Viscainoa aceae (Figs 1, 5, 6) and Zygophyllaceae, never angular. geniculata, although careful study of the other species Perforation plates of Krameriaceae are simple and also revealed the condition. Pits of the vasicentric tra minimally bordered (K. cistoidea, K. grayi) or nonbor- cheids and fibre-tracheids of Zygophyllaceae range dered (K lanceolata, K. lappacea), but in species other between 3 and 4 [im in diameter. The two cell types than these, both nonbordered and minimally bordered differ in pit density but little in pit diameter. perforation plates may be seen. A typical condition for Helical thickenings in the form of pairs of ridges the family is rendered in Figure 9 (left). Perforation accompanying grooves interconnecting pit aper plates of the Zygophyllaceae studied are minimally tures were observed in tracheids of K. erecta and bordered. K secundiflora (Fig. 10). No such thickenings were Pits on vessel elements have circular pit cavity out observed in any other Krameriaceae or in the Zygo lines. Pit apertures are narrow or slitlike (Fig. 9, left). phyllaceae studied. Appearances referable to 'helical thickenings' were Mean imperforate tracheary element length is observed in K. erecta (Tilforth 415). These are perhaps shown in Table 1, column 5. This feature shows a sur better described as thickenings accompanying grooves prising range in Krameria, from 178 (K secundiflora) that interconnect pit apertures, as shown in tracheids to 736 um (K sonorae). The range in imperforate tra in a species of Krameria (Fig. 10). Helical thickenings cheary element length in the Zygophyllaceae studied occur in vessels of K. lanceolata (in both stem and is much less, except for Viscainoa, in which relatively root). Pits are relatively crowded on walls of vessels of juvenile wood was studied. most species of Krameria (e.g. Fig. 9, left), but are more widely separated on vessel walls in K. tomentosa. Cavities of lateral wall pits on vessels of Krameria AXIAL PARENCHYMA range between 3 and 4 um in diameter Axial parenchyma is commonly diffuse in Krameri Vessel wall thickness in Krameria ranges from aceae, but aggregations ranging from a few cells to 2.5 um (K lappacea) to 3 urn (K erecta), 3.5 urn numerous cells may be seen (Table 1, column 6), most (K cytisoides), 4 um (K grayi), 5 um (K sonorae) and commonly as diffuse-in-aggregates. Axial parenchyma 6 um (K. secundiflora). In the Zygophyllaceae studied, cells are easily recognizable because of their relatively vessel wall thickness ranges from 3 um (Larrea triden- thin walls (e.g. the cell to the right of the tracheid sur tata) to 4 um (Fagonia laeuis, Morkellia acuminata, rounded by arrows, Fig. 3). The cell walls of axial Guaiacum guatamalense and Viscainoa geniculata). parenchyma are usually secondary walls as in K grayi Vesturing was not observed on vessel pits of Krame (Fig. 3), but in several other species are primary walls: ria examined with SEM (Fig. 9). However, in Zygo most notably in K. erecta (Fig. 6) and K. lanceolata phyllaceae, pronounced vesturing was observed in (Fig. 8). Small amounts of yellow-brown deposits that vessels of Viscainoa geniculata, as seen both from the stain darkly, often in the form of droplets, distinguish outside (Fig. 17) and the inside (Fig. 18) surfaces of axial parenchyma (Figs 5, 6). vessels. Vestures are not only present in vessel pits of The axial parenchyma of K lanceolata stems Morkellia acuminata, they are also present on vessel (Fig. 8) ranges from diffuse-in-aggregates to bands, surfaces adjacent to the pits (Fig. 20). Vesturing is some so extensive that vessels and tracheids occur as definitely present in the pits of vessels of Larrea isolated cells in a background of parenchyma (Fig. 8, tridentata (Fig. 19). The vessel pits of L. tridentata are arrows). relatively small (compared with those of dicotyledons Axial parenchyma strands, as seen in longitudinal at large), so vestures on them are inconspicuous, but sections, consist of a single strand, but strands of two proportionate to pit size, vestures are fully developed. to four cells were observed in K. grayi and K sonorae. Tangential bands of parenchyma one cell thick, as seen in transactions, or more than one cell thick, are IMPERFORATE TRACHEARY ELEMENTS more frequently present at the ends of growth rings. Throughout Krameriaceae, imperforate tracheary ele The presence of such bands more often at the ends of ments have distinctly bordered pits (Fig. 9), densely growth rings than scattered within the rings is taken enough placed to qualify these elements as tracheids as evidence that marginal parenchyma is present.

Figures 17-20. SEM photographs of vessel surfaces of wood of Zygophyllaceae from tangential sections. Scale bars = 5 urn. Figs 17, 18. Viscainoa geniculata. Fig. 17. Inner surface of vessel; vestures present in pit apertures. Fig. 18. Outer surface of vessel; vestures present around pit aperture, but a few smaller vestures also present in pit cavity. Fig. 19. Larrea tridentata; inner surface of vessel, showing pit cavities in which vestures are present. Fig. 20. Morkillia acuminata, inner surface of vessel; vesturing present on pit apertures, but also (below) on some areas of vessel wall.

2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 257-270 266 S. CARLQUIST

Aggregations of parenchyma cells several cells thick (1941). Rays of adult wood of Viscainoa are likely to that occasionally occur at the ends of growth rings in contain uniseriate plus multiseriate rays, with a K. grayi (Fig. 1) were interpreted as marginal paren greater abundance of procumbent cells in the multi- chyma. Prominent bands of marginal parenchyma are seriate rays. The ray type of Viscainoa can be desig illustrated here for K. erecta (Figs 5, 6). nated in either case as Heterogeneous Type II of Kribs In the Zygophyllaceae studied, axial parenchyma is (1935). exclusively diffuse in Fagonia laevis, but diffuse as The height of uniseriate rays in Zygophyllaceae is well as other types occur in the other genera (Table 1, less than half that of Krameriaceae (Table 1, column column 6). Abaxial axial parenchyma occurs in Gua- 8), except for Viscainoa, in which figures for ray height iacum guatemalense (Fig. 16). In Larrea tridentata, are doubtless related to the juvenile nature of the axial parenchyma (especially diffuse-in-aggregates) material studied. accumulates large amounts of dark-staining deposits Secondary walls occur on ray cells of all Zygophyl in some areas (Fig. 13), but in other parts of a single laceae studied. Bordered pits on tangential walls of section, wider diffuse axial parenchyma cells are ray cells were observed in Larrea tridentata. identifiable because they contain crystals (Figs 14, 15). STORIED STRUCTURE Absence of storying characterizes most woods of RAYS Krameriaceae. At most, only vague storying may be In Krameria, rays are almost all uniseriate (Figs 2, seen in axial parenchyma of larger stems of Krameria 7). A few biseriate rays were observed in the root of (Fig. 7, left). K. lanceolata, but even in that species, the rays were Storying is common in axial parenchyma of Larrea predominantly uniseriate. Rays are inconspicuous tridentata (Fig. 15). In Guaiacum guatamalense, rays in tangential sections of Krameria wood (Figs 2, 7), as well as axial parenchyma are storied. not only because rays are uniseriate, but because ray cells are almost exclusively upright (Table 1, col umn 7). The upright nature of ray cells is illus CRYSTALS trated in radial section for K. grayi (Fig. 4). A few Numerous rhomboidal crystals are present in axial ray cells square as seen in radial section were parenchyma (Figs 11, 12) and ray cells (Fig. 12, bot observed in K. grayi (Carlquist 15826). The rays of tom) of K sonorae wood. Rhomboidal crystals were Krameria fall into Paedomorphic Type III (Carl seen in a very few axial parenchyma cells of secondary quist, 2001). xylem of K. erecta (Tilforth 415). In all remaining col Mean height of uniseriate rays in Krameria is given lections of Krameria, no crystals were observed in sec in Table 1, column 8. Mean ray height is roughly the ondary xylem. same as mean vessel element length in the family, as In Zygophyllaceae, crystals are illustrated here for is most evident in the averages for Krameriaceae as a Larrea tridentata (Figs 14, 15). The axial parenchyma whole. cells bearing these crystals (Fig. 14, arrows) are wider Ray cells have secondary walls (Fig. 3, centre; than parenchyma cells that do not contain crystals Figs 4, 6), except for K lanceolata (Fig. 8). Bordered (Fig. 13); crystal-bearing cells may thus be termed pits were observed on tangential walls of ray cells idioblastic, following Metcalfe & Chalk (1950). In (Fig. 4). Borders are readily visible in sectional view Larrea tridentata, crystalliferous axial parenchyma but cannot be easily seen in face view. occurs in earlywood (Fig. 14), whereas noncrystallifer- In the Zygophyllaceae studied, both uniseriate and ous axial parenchyma tends to occur in latewood. biseriate rays are present in Larrea tridentata Large rhomboidal crystals occur in a few ray cells in (Fig. 15), and some upright as well as procumbent Tribulus zeyheri. cells are present. The ray type for Larrea is thus No crystals were observed in secondary xylem of Homogeneous Type I of Kribs (1935). Fagonia laevis, Morkillia acuminata or Viscainoa gen- Rays of Fagonia and Guaiacum contain procumbent iculata. The stems of these were two to three years old, cells almost exclusively and thus those genera have and possibly crystals might be found in wood of older Homogeneous Type III of Kribs (1935). The material stems. studied of Viscainoa has upright and square cells, Secondary phloem axial parenchyma cells of Krame with occasional procumbent cells, in rays. This ria contain abundant rhomboidal crystals of various description is probably not applicable to mature wood sizes. Although suitable axial phloem material was of Viscainoa, judging from widely confirmed trends of not available for all Zygophyllaceae studied, rhomboi shift to a higher proportion of procumbent cells dur dal crystals, one per cell, were observed in inner cor ing ontogeny of rays demonstrated by Barghoorn tical parenchyma of Viscainoa geniculata.

WOOD ANATOMY OF ZYGOPHYLLACEAE 267

AMORPHOUS DEPOSITS Crystals in rays and/or axial parenchyma in at least In Krameria, yellowish to brownish droplets that stain one species of each family. darkly are often present in axial parenchyma cells The presence of tracheids (vasicentric tracheids in (Figs 5-7). In the K tomentosa sample, all tracheid the case of Zygophyllaceae) in both families is not lumina were filled with these materials. included in the above list. Probably it will prove to be In Zygophyllaceae, dark-staining deposits vary in a symplesiomorphy in at least some clades of rosids. quantity, but are clearly present in some species. Axial Crystals were reported in all Zygophyllaceae except parenchyma filled with such deposits is conspicuous in Balanites by Metcalfe & Chalk (1950), but subse some parts of Larrea tridentata wood (Fig. 13). The quently, Parameswaran & Conrad (1982) have demon wood of Guaiacum officinale, famous (as lignum vitae) strated rhomboidal crystals in rays of Balanites. The for its deep brown heartwood, owes its colour to these present paper contains the first report of crystals in deposits. Similar coloration of heartwood may be Krameriaceae. I did not find crystals in my wood observed in samples of Krameria stems with relatively material of Morkillia and Viscainoa, but crystal large diameter. absence in these samples is not conclusive because of their small stem diameter. Crystal occurrence is diverse in expression in Zygophyllaceae in terms of CONCLUSIONS cell types occupied by crystals, abundance and crystal size (Metcalfe & Chalk, 1950). SUPRAFAMILIAL RELATIONSHIPS The absence of uniseriate rays was claimed by Met Krameriaceae have been paired with Zygophyllaceae calfe & Chalk (1950) for Balanites but Parameswaran as the sole families of Zygophyllales (Chase et al., & Conrad (1982) did find uniseriate rays in Balanites. 1993; Savolainen et al., 2000; Soltis et al., 2000). The Krameriaceae form a sister group to Zygophyl question to be asked is not how wood anatomy sup laceae, according to Sheahan & Chase (1996) and ports this idea, but rather, how wood anatomy reflects more recent molecular phylogenies of dicotyledons. a relationship that seems very likely on the basis of One may well ask, however, whether a monogeneric DNA evidence. Below is a list of characters common to family, Krameriaceae, should be maintained as sepa the two families. Note should be taken that features rate from Zygophyllaceae if these are the only families widespread in dicotyledons (e.g. simple perforation of Zygophyllaceae. Sheahan & Chase (1996) find that plates in vessels) and therefore most likely to be sym- 'Krameria has a large number of autapomorphies'. On plesiomorphies where Zygophyllales are concerned the basis of the present study, differences between the are not included in this list: features likely to be syn- families, most of which are probably autapomorphies apomorphies are sought. Zygophyllaceae is used here for one family or the other, are shown in Table 2. as defined by Sheahan & Chase (1996): Nitraria and Peganum are excluded but Balanites is included. On the basis of wood (and secondary phloem) anat omy, Krameriaceae and Zygophyllaceaeae can readily Borders on perforation plates minimal. be separated. The features by which the families differ Lateral wall pits on vessels small (pit cavities 3-4 urn need discussion in view of the fact that many of these in diameter). character states are newly reported. Axial parenchyma mostly in strands of 1-2 cells. Vestured pits were not observed in vessels or Axial parenchyma diffuse and diffuse-in-aggregates tracheids of any Krameriaceae. In Zygophyllaceae, (as well as derived types). vestured pits in vessels were reported by Parameswa Uniseriate rays present and (except for Balanites), ran & Conrad (1982) for the genera Balanites, Bulne- predominant. sia and Guaiacum. In Balanites, the lumen surface of

Table 2. Differences between Krameriaceae and Zygophyllaceae

Krameriaceae Zygophyllaceae

Vessels with nonvestured pits Vessels with vestured pits Imperforate tracheary elements all tracheids Imperforate tracheary elements tracheids + fibre-tracheids Axial parenchyma usually with one cell per strand Axial parenchyma usually with 2-4 cells per strand Rays Paedomorphic Type III Rays Heterogenerous Types II & III, Homogeneous Type III Storying absent or nearly so Storying present in axial parenchyma, sometimes in rays Crystals many per cell, of varied sizes; rare in wood but Crystals one per cell or septate portion of cell in wood or common in axial parenchyma of secondary phloem. secondary phloem.

© 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 257-270 268 S. CARLQUIST the vessel is vestured (Parameswaran & Conrad, woods of most Zygophyllaceae (extending even to sto 1982). In the present study, vestured pits are demon rying of rays) is an apomorphy in that family. In turn, strated in vessels of Larrea, Morkillia, Tribulus and storying is related to shortness of fusiform cambial ini Viscainoa. Sheahan & Chase (1996) list vesturing as tials (of which vessel element length is an accurate absent in Bulnesia, Guaiacum, Larrea, Tribulus and indicator for any given species). Storying occurs in Viscainoa. Vesture presence in zygophyllaceous gen species with relatively short tracheary elements era based on SEM study is convincing on the basis of (Bailey & Tupper, 1918), notably Guaiacum and present and earlier studies (Jansen, Smets & Baas, Larrea in the present study. 1998). Thus far, there is no evidence supported by Crystal occurrence modes show interesting diver SEM studies that vestures are absent in vessels of gences between Krameriaceae and Zygophyllaceae. Zygophyllaceae. Crystals are notably absent in the secondary xylem of Morkillia and Viscainoa were included in the Krameriaceae (except for K. sonorae), but small crys present study because they constitute a subfamily, tals of various sizes fill axial parenchyma of secondary Morkillioideae, that is an outgroup to the remainder phloem in Krameria stems. In contrast, most Zygo of Zygophyllaceae according to Sheahan & Chase phyllaceae have rhomboidal crystals that occur singly (1996). Therefore, one would expect autapomorphies per cell, whereas crystals have not yet been reported for the family Zygophyllaceae to be present in Morkil in secondary phloem of Zygophyllaceae. These diver lioideae. Because vestured pits are indeed present in gences are best interpreted as autapomorphies of one the two morkillioid genera, whereas vestured pits are or both families. absent in Krameriaceae as far as is known, the most The phylogenetic work of Sheahan & Chase (1996) logical interpretation at present is that absence of indicates that Malpighiaceae in particular and rosids vestured pits is a symplesiomorphy in the order in general would represent outgroups to Zygophyl Zygophyllales. laceae. Although no rosids were examined for the Vestured pits have been reported not only for vasi- present study, wood features of rosid families do not centric tracheids, but for fibre-tracheids in Balanites contradict the idea of a rosid placement for Zygophyl (Parameswaran & Conrad, 1982). Further studies of lales. The presence of vestured pits in Zygophyllales imperforate tracheary elements in Zygophyllaceae are can be considered an autapomorphy of that family. desirable. Vesturing is absent in tracheids of Krame Vestured pits have been reported in Malpighiaceae, riaceae observed with SEM. but only in a few members of 'derived' clades of that Vasicentric tracheids were observed in all of the family (Jansen, Baas & Smets, 2001). The interpreta Zygophyllaceae studied here, in agreement with the tion of these authors is clearly that presence of ves findings of Metcalfe & Chalk (1950) and Parameswa tured pits represents several autapomorphies within ran & Conrad (1982) for the family. In Krameriaceae, Malpighiaceae. In the present study, comparison of all tracheids are relatively uniform with respect to wood characters of Zygophyllales with a single family pitting. Presence of tracheids thus could be a symple of rosids, such as Malpighiaceae, was not undertaken siomorphy for Zygophyllales. In this case, the differ because the patterns of wood character homoplasies in entiation into vasicentric tracheids and fibre-tracheids rosids need much more study. observed in Zygophyllaceae would be an example of the phyletic pathway described as tracheid dimor phism (Carlquist, 1988). SPECIES DISTINCTIONS WITHIN KRAMERIACEAE Diffuse axial parenchyma occurs in all species, but groupings that probably represent unusual types of Crystal occurrence easily demarcates K. sonorae from aggregation of diffuse cells (e.g. abaxial parenchyma K. grayi and other species of Krameria on the basis of in Guaiacum) seem to be apomorphies. The same may present evidence. Krameria grayi and K sonorae are be said for the unusually wide rays of Balanites. The similar in having weakly demarcated growth rings ray type in Krameriaceae, Paedomorphic Type III, is and few vessels per group; these two species may be an unusual one in dicotyledons. It has been reported closely related, judging from the cladogram of Simp in families such as Empetraceae (Carlquist, 1989) and son et al. (2004). In K. tomentosa, pits on vessel walls Myrothamnaceae (Carlquist, 1976) and other families are sparser than they are in other species. Vessel wall or genera most of which consist of small shrubs thickness has a wide range within the genus, and (Carlquist, 2001). Permanent juvenilism in wood of some portions of that range probably correspond to Krameriaceae is also signalled by the lack of storying species limits. Axial parenchyma cells that have pri in even relatively old stems of that family. Storying mary walls only probably represent a species charac tends to increase with diameter of stem (Bailey, 1923). ter for some species, cited above. Distinctions other All but relatively young stems of Zygophyllaceae show than the above seem more directly related to habit and storying in secondary xylem. The marked storying in ecology and are discussed below.

ECOLOGY AND HABIT studied are also relatively low. To be sure, the sam pling for the family here is small, but quantitative Krameria is a hemiparasite (Cannon, 1910), a condi data for vessels in Zygophyllaceae seem correlated tion well documented by Simpson (1989). Woody hemi- with dry habitats rather than mesic ones. parasites such as Loranthaceae, Misodendraceae and Krameria lanceolata is distinctive in having promi Viscaceae have xeromorphic wood as judged from nent bands and strands of axial parenchyma in wood shortness of vessel elements (Carlquist, 1977, 1985b; of the above-ground stem. From the above-ground Carlquist & Hoekman, 1985). Short, narrow vessel stem in K lanceolata, prostrate herbaceous branches elements, numerous per unit transactional area, char originate. Very likely, the parenchyma bands provide acterize xeromorphic woods (Carlquist, 1966). Krame- sites of origin for initiation of the lateral branches, and riaceae occupy dry habitats, not a few species occur in for interconnection of their conductive systems with desert areas (Simpson, 1989). Separating hemipara- that of the main stem. Such parenchyma bands are sitism from adaptation to aridity relative to wood notably absent in secondary xylem of the root of xeromorphy does not seem feasible. Both are probably K. lanceolata. The vessel elements of the roots in involved in the woods of Krameria. Because Krameria K. lanceolata are wider and longer than those of the parasitizes shrubs that live in xeric habitats (at least stem. This accords with the findings of Patel (1965) seasonally so), wood of Krameria would be expected to and others for root wood as compared to stem wood in be at least as xeromorphic as that of host plants. dicotyledons as a whole. Vessel element length in the Krameriaceae studied (182 um) is virtually the same as in Californian desert shrubs (190 um). Vessel lumen diameter in the sam ACKNOWLEDGEMENTS pling of Krameria is 26 Jim, vessel diameter (outside diameter) in Californian desert shrubs 25.9 (im (Carl Prof. Beryl B. Simpson kindly provided material of quist & Hoekman, 1985), again, a close match. With Krameria lanceolata, K. tomentosa and Morkillia respect to vessel density, however, Krameriaceae have acuminata. Prof. Mark Olson of UNAM (Mexico City) fewer vessels mm"2 (174) than the Californian desert made wood of three species of Krameria available to shrub sampling (361). Possibly the tracheids of me. In addition, thanks for materials are due to Krameria form a conductive system adequate as a sub Charles Heimsch and to the curators of RSA, SBBG, stitute for greater vessel denseness. SJRw and USw. 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