TAXON 49- FEBRUARY 2000 27

Wood and stem anatomy of Sarcobatus (): systematic and ecological implications

Sherwin Carlquist’

Summary

Carlquist, S.: Wood and stem anatomy of Sarcobatus (C’aryophyllales): systematic and

ecological implications. — Taxon 49: 27-34. 2000. — ISSN 0040-0262. Quantitative and qualitative data are given for Sarcobatus vermiculatus (Hook.) Torr. stem anatomy in order to provide information relevant to Behnke’s segregation of Sarcobatus from Chenopodiaceae and his idea that Sarcobataceae belong in suborder Phytolaccineae rather than suborder Chenopodiineae. Sarcobatus has highly xeromorphic wood such as in xeric Chenopodiaceae (presence of vasicentric tracheids, narrow vessels, short vessel elements, numerous vessels per group, helical sculpturing of vessel walls), but these features could have evolved independently in both suborders. Nonbordered perforation plates, present in Sarcobatus, are widespread in C’aryophyllales s.str. and may prove to be a defining feature for the recently expanded Caryophyllales together with the neighbouring order Santalales. A single-layered lateral meristem occurs in genera of Chenopodiinae with successive cambia, but also in genera of Phytolaccineae. Likewise, raylessness occurs in both suborders. Stem and wood anatomy does not provide decisive evidence for placement of Sarcobatus in Phytolaccineae, but it does not provide any evidence against that treatment.

Introduction Behnke’s (1997) discovery of distinctive sieve tube in Sarcobatus led him to remove the genus from Chenopodiaceae. In an earlier issue of this journal, Behnke (1997) assembled much information about the genus and suggested that the new family he created, Sarcobataceae, belongs in close proximity to Phyto laccaceae. Behnke (1997) cited evidence from DNA analyses (Clement & Mabry, 1996; Downie & al., 1995, 1997) for this treatment. In the suborder Phytolaccineae, Behnke (1997) includes Achatocarpaceae, Agdestidaceae, Aizoaceae, Barbeui aceae, , , Rivinaceae, Sarcobataceae, and Stegno spermataceae. This suborder is a modification of Phytolaccineae as recognized by Heimerl (1934) and Thorne (in Cronquist & Thorne, 1994). The segregate families were mostly treated as subfamilies of Phytolaccaceae by Thome (in Cronquist & Thorne, 1994). Information from wood anatomy is often significant with respect to the classification system. Compilations of wood data for Caryophyllales have been offered by Metcalfe & Chalk (1950) and by Gibson (1994). A series of monographs on wood of these families is in progress in order to offer more extensive information. These papers include Caryophyllaceae (Carlquist, 1995), Portu lacaceae and Hectorellaceae (Cariquist, 1998a), Petiveria and Rivina (Carlquist, 1998b), Basellaceae (Carlquist 1999a), (Cariquist, 1999b), Stegno

1Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, 93105, U.S.A.

1). Fig. vessels, below band (out focus of tissue conjunctive softer of buckling

plus 4) (Fig. cracks small in resulted tissues the conjunctive of hardness

the and stem, the of portions only best represented at sections microtome

The sliding (1985). Carlquist on is based tracheid vasicentric of concept the

(1964); Nomenclature on Committee IAWA the follow Terms tissue. conjunctive

not exclude do and transactions of scans random on based are diameter vessel

on figures The diameter. lumen vessel mean as measured was diameter Vessel

artifacts. numerous creating

walls, of distortion and expansion in resulted also sectioning better allowed that

of softening degree any because unsuccessful proved agents Softening impedance.

a further provide tissue conjunctive the in crystals soft; are stem the within

strands phloem yet the hard, very are tissue conjunctive of the fibers The problems.

microtechnical challenging exceptionally provide of Sarcobatus stems The

safranin.

with and stained acid) % chromic 10 and formalin % 10 parts Fluid (equal Jeffrey’s

of means by prepared were Macerations (SEM). microscope electron scanning

Nanolab & Lomb a Bausch with examined and coated, sputter stubs, aluminium

on mounted slides, clean between dried unstained, left were sections Other 9). 4,

1- slides (Figs. as permanent Balsam Canada in mounted and green combination fast

a safranin with stained were sections Some microtome. sliding a with prepared were

Sections ethanol. % 50 aqueous in preserved were stems The (RSA). 8038 Carlquist

1989, Jun 12 Co., California, Mono Lake, Mono of margins saline on the

from collected was diameter, in mm 8 to up vermiculatus, S. of material Stem

methods an4 Material

the order. as within as well Caryophyllales

outside genera from needed are their origin, of nature the as well as cambia,

successive these of products and action the concerning genera numerous more

from Details terminology. and interpretations various to subject been have families,

dicotyledon other of those as well as Caryophyllales, these of cambia successive

The cambia. has successive 1994), & Mabry, by Behnke as circumscribed order

(=

the s.str. Caryophyllales of genera and families other many like Sarcobatus,

order. the of systematics the to for comparison important more even becomes

wood data from adopted, is Caryophyllales of definition new broader If this (1994).

al. & Williams data of the on largely based 1998), (APG, Group Phylogeny sperm

Angio by the Polygonaceae) (Ancistrocladaceae, families allied and some ceae)

Nepentha (Droseraceae, glands digestive with families as as well Tamaricaceae)

Plumbaginaceae, (Frankeniaceae, glands salt with families to as include so widened

been recently has Caryophyllales of definition The years. recent in radically

most but 1994), & Thome, (Cronquist century past the over considerably changed

has of Caryophyllales concept The the order. for system classification the revising

in usable base data complete more a supply to undertaken been has Caryophyllales

of and genera families of This survey press). in (Cariquist, Phytolaccaceae rivinoid

and and phytolaccoid 1999d), (Carlquist, Barbeuia 1999c), (Carlquist, spermataceae

2000 49- FEBRUARY TAXON 28 TAXON 49- FEBRUARY 2000 29

— 1’ . . d i i ii ___I.1 •i ‘.

Figs. 1-4. Sections of stem of Sarcobatus vermiculatus. — I, transection from near surface of stem (top) inward; the lateral meristem is indicated by the pair of arrows; 2, transection of inner portion of stem, showing several vascular strands; arrows indicate terminus of a growth ring; 3, transection of vascular strand and adjacent tissues (f conjunctive tissue fibers, p = phloem, c = conjunctive tissue parenchyma); 4, tangential section, to show storied nature of phloem (darker vertical strand

to left of center) and lack of rays. — Figs. 1, 2, 4, magnification scale below Fig. 1 (divisions = 10 tim); Fig. 3, divisions = 10 jim.

is pattern storied this 4); (Fig. storied are walls lignified with tissue parenchyma

conjunctive and elements tube 4). Sieve Fig. in shown as of rays, criteria

the meet not do strands vascular between parenchyma or fibers tissue conjunctive

of (zones absent are Rays into strands. not subdivided is parenchyma Axial

tracheids. vasicentric or vessels with contact are in cells all parenchyma sparse,

moderately is 5, 6). parenchyma Axial (Figs. grooves the accompany ridges of pairs

vessels, the of many In 5-7). (Figs. apertures pit interconnecting grooves of form

the in is tracheids vasicentric and vessels of surfaces inner the on Sculpturing

7, right). (Fig. oval are apertures pit 7);

(Fig. diameter .im in 2.5 about are cavities pits, pit nonvestured bordered circular

have vessels of walls Lateral walls). thicker have vessels (wider m 2.0-4.0 about

thickness, wall Vessel nonbordered. simple, all plates Perforation sum. 93 length,

element vessel Mean 417. surveyed), area in included tissue (conjunctive transaction

of mm 2 per vessels of number Mean abundant. equally about are tracheids

vasicentric and vessels very narrow macerations, In tm). 20 diameter, lumen (mean

.tm 7 46 to from diameter in lumen range 7.3). Vessels group, per of vessels number

(mean multiples radial in grouped are 2). Vessels Fig. (arrows, observed were rings

growth a few xylem, the secondary 8). In (Fig. crystals elongate slender numerous

contains parenchyma Phloem cells. parenchyma tissue conjunctive the as length

same about the are 4) 3, (Figs. parenchyma phloem and elements tube Sieve

9). (Fig. crystals elongate three

to one contain cells

parenchyma the of Some 4 um). 244 (mean tissue conjunctive =

the of fibers the to compared .tm) 98 (mean short = relatively are cells parenchyma

The tissue. vascular of strands interconnect that bands tangential of the form

in occurs parenchyma 3). The (Fig. diameter lumen greater their of because starch

of quantities larger contain and walls lignified thinner have which cells, parenchyma

and starch; of amounts small contain and walls lignified thick relatively have which

fibers, cells: of kinds two of consists tissue conjunctive The tissue. conjunctive

the throughout scattered are 1) (Fig. or bands 2) (Fig. strands vascular These xylem.

secondary and phloem secondary which yields each of cambia vascular (successive)

at intervals, and, tissue conjunctive produces meristem lateral the interior, the To

crystals. elongate smaller separate of assemblage an or styloid a either bears which

of each idioblasts contains cortex secondary the cortex, primary the Like outside. the

to cortex secondary of files radial produces meristem lateral cortex. The inner the in

forms top, arrows) 1, (Fig. meristem A lateral stem. the of age on the depends which

of extent the cortex, primary of remnants are there stem, the of exterior the At

anatomy and stem Wood

cambia. successive with Caryophyllales

of on woods work monographic of lack the for account and 1986), at., & Fahn

by (see illustrations workers best the even by experienced been have podiaceae)

Cheno (e.g., these like woods of staining and sectioning in difficulties

Extraordinary 3 4. and Figs. in pale so relatively is and applied methods staining

in variations despite readily stain not did tissue conjunctive the Moreover,

2000 FEBRUARY 49 TAXON 30 TAXON 49- FEBRUARY 2000 31

A 1 8

Figs. 5-9. SEM photos (5-8) and light photomicrograph (9) from tangential sections of stem of

Sarcobatus vermiculatus (5-7 show inside surfaces of vessels). — 5, surface showing grooves interconnecting pit apertures, a pair of ridges parallels most of the grooves; 6, surface showing grooves interconnecting pit apertures and more pronounced ridges paralleling the grooves; 7, surface of vessel with fewer, inconspicuous ridges, outside surface of vessel at right shows nonvestured nature of pits; 8, crystals from a broken phloem parenchyma cell, to show narrow shapes and small sizes; 9, rhomboidal crystal (upper left) in parenchyma of conjunctive tissue. — Figs. 5-8. magnification scales at lower left (bar = 10 jim); Fig. 9, scale same as below Fig. 3.

developed an autapomorphy, be may Sarcobatus in occurrence the 1994), (Gibson,

Chenopodiaceae as such Caryophyllales other in occurs also sculpturing wall

vessel Although 1966). ones (Carlquist, xenc in represented well and is of habitats

range wide a occupies which in Asteraceae, of xeromorphy an indicator is vessels,

in sculpturing helical of forms other with together This, groove. each accompanying

ridges of pairs with often apertures pit interconnecting grooves of form the

takes sculpturing This surfaces. vessel on sculpturing helical of presence and 1985)

(Carlquist, tracheids vasicentric of presence include wood vermiculatus S. in morphy

xero indicate that features Qualitative wood. xeromorphic very a of indicative

is also (7.3) S. vermiculatus in group per of vessels number high The salinity. soil

of because xeric physiologically are especially that areas in desert grows Sarcobatus

but , desert California southern the for value the below certainly is 4.5. This

of Ratio a Mesomorphy has S. vermiculatus whereas 1985), & Hoekman, (Carlquist

20.9 is shrubs desert Californian southern Ratio for Mesomorphy The safety.

conductive also but efficiency conductive not only reflects ratio This mm 2 ). per

vessels by divided length element vessel times diameter (vessel Ratio Mesomorphy

the of form the in combined be can data vessel quantitative of kinds Three

Phytolaccineae. in belong Sarcobataceae that idea (1997) Behnke’s with consonant

is Barbeuia in Sarcobatus and in meristem lateral of type same the of occurrence

The families. and genera of terms in distribution the show will series this in

papers further and Caryophyllales, in occur types these of Both inside. the to tissue

conjunctive plus cambia vascular and outside the to cortex secondary produces

that thickness in cell a single only meristem a lateral has Barbeuia whereas 1999c),

(Carlquist, formation cambium successive for a precursor as cortex) secondary

in cells of files (radial meristem lateral a diffuse exemplifies Ste gnosperma

Carvophyllales s.str. in occur cambia to successive leading meristems lateral of

types Two interest. unusual of is Sarcobatus in meristem lateral the of nature The

press). in 1998b,

(Carlquist s.l. Phytolaccaceae of stem tissues other and in bark occur Sarcobatus,

in seen in bark, Styloids unpubi.). (Cariquist, Santalales order 1998) (APG, adjacent

the in Santalum does as plates, perforation nonbordered s.l.) have (Caryophyllales

Tamaricaceae example, For 1998). (APG, Caryophyllales expanded recently

the as well as 1994) Mabry, & Behnke by defined (as s.str. Caryophyllales for

symplesiomorphic thus and distribution, in ordinal be to prove may it character, this

to respect with known better is Caryophyllales order the When unpubi.). Cariquist,

Chenopodiinae; and Didiereaceae, of the (Alluaudia Portulacineae of genera

in occurs it also but in press), 1999b-d, (Carlquist Phytolaccineae in occurs authors,

by most neglected feature, This plates. perforation nonbordered has Sarcobatus

suborder. latter to the Sarcobataceae

assigned (1997) Behnke Phytolaccineae). (suborder Nyctaginaceae and Aizoaceae

(= in but also Chenopodiineae), suborder the Chenopodiaceae and

in occurs raylessness (1994) to Gibson according rayless; is Sarcobatus

conclusions and Discussion

tracheids. vasicentric and the vessels by shared

2000 FEBRUARY 49- TAXON 32 TAXON 49 FEBRUARY 2000 33

independently of the feature in other Caryophyllales. The unusually xeromorphic nature of wood of Sarcobatus should not be interpreted as indicating close relationship to Chenopodiaceae or other Caryophyllales with similarly xeromorphic woods. The placement of Sarcobatus by Behnke (1997) in suborder Phytolaccineae is entirely conceivable on the basis of the stem and wood anatomy data above, even though these data do not decisively place it in that suborder as opposed to placement in the other suborders of Caryophyllales s.str.

Literature cited APG (ANGIOSPERM PHYLOGENY GROUP). 1998. An ordinal classification for the families of flowering plants. Ann. Missouri Bot. Gard. 85: 53 1-553.

Behnke, H.-D. 1997. Sarcobataceae — a new family of CaryophyUales. Taxon 46: 495-507. — & Mabry, T. J. (eds.). 1994. Caryophyllales. Systeniatics and evolution. Berlin & Heidelberg. Carlquist, S. 1966. Wood anatomy of Compositae: a summary, with comments on factors influencing wood evolution. Aliso 6(2): 25-44. — 1985. Vasicentric tracheids as a drought survival mechanism in the woody flora of southern California and similar regions; review of vasicentric tracheids. Aliso II: 37-68. — 1995. Wood anatomy of Caryophyllaceae: ecological, habitat, systematic, and phylogenetic implications. Aliso 14: 1-17.

— 1998a. Wood anatomy of Porrulacaceae and Hectorellaceae: ecological, habital, and systematic implications. Aliso 16: 137-153.

— L998b. Wood and stem anatomy of Petiveria and Rivina (Caryophyllales): systematic implications. tnt. Assoc. WoodAnat. J. 19: 383-391. — 1 999a. Wood, stem, and root anatomy of Basellaceae, with relation to systematics and cambial variants. Flora 194: 1-12. 1999b. Wood anatomy of Agdestis (Caryophyllales): systematic position and nature of the successive cambia. Aliso 18: 35-43.

— 1999c. Wood and stem anatomy of Stegnosperma (Caryophyllales): phylogenetic relationships; nature of lateral meristems and successive cambial activity. tnt. Assoc. Wood Anal. J. 20: 149- 163.

— 1999d. Wood anatomy, stem anatomy, and cambial activity of Barbeuia (Carvophyllales). tnt. Assoc. Wood Anal. J. 20: 431-440.

— in press. Wood and stem anatomy of phytolaccoid and rivinoid Phyiolaccaceae (Caryophyllales): ecology, systematics, nature of successive cambia. Aliso. — & Hoekman, D. A. 1985. Ecological wood anatomy of the woody southern California flora. tnt. Assoc. WoodAnat. Bull., N. S. 6: 319-347. Clement, J. S. & Mabry, T. J. 1996. Chloroplast DNA evidence and family-level relationships in the Caryophyllales. Amer. J. Bot. 83(6, suppl.): 143. Cronquist, A. & Thorne, R. F. 1994. Nomenclatural and taxonomic history. Pp. 5-25 in: Behnke, H.-D. & Mabry, T. J. (eds.), Caryophyllales. Evolution and systematics. Berlin, Heidelberg & New York. Downie, S. R., Katz-Downie, D. S., & Cho, K-i. 1995. Structural and sequence variation in the highly conserved cpDNA inverted repeat region: implication for higher level taxonomic studies. Amer. J. Bot. 82(6, suppl.): 126.

— & — 1997. Relationships in the Caryophyllales as suggested by phylogenetic analyses of partial chloroplast DNA 0RF2280 homolog sequences. Amer. i. Bot. 84: 253-273. Fahn, A., Werker, E. & Baas P. 1986. Wood anatomy and identWcation of trees and shrubs from tsrael and adjacent regions. Jerusalem. Gibson, A. C. 1994. Vascular tissues. Pp. 45-74 in: Behnke, H.-D. & Mabry, T. J. (eds.), Caryophyllales. Evolution and systematics. Berlin, Heidelberg & New York. 34 TAXON 49- FEBRUARY 2000

— Heimerl, A. 1934. Phytolaccaceae. Pp. 135-164 in: Engler, A. & Prantl, K. (eds.), Die natUrlichen Pflanzenfamilien, ed. 2, I 6C. Leipzig. IAWA Commitee on Nomenclature. 1964. Multilingual glossary of terms used in wood anatomy. Winterthur. Metcalfe, C. R. & Chalk, L. 1950. Anatomy of the dicotyledons. Oxford. Williams, S. E., Albert, V. A. & Chase, M. W. 1994. Relationships of Droseraceae: a cladistic analysis of rbcL sequence and morphological data. Amer. .1. Bot. 81: 1027-1037.