IAWA Journal, Vol.

33 (2), 2012: 205232

WOOD ANATOMY OF CHENOPODIACEAE (AMARANTHACEAE s. l.)

Heike Heklau 1, Peter Gasson 2, Fritz Schweingruber 3 and Pieter Baas 4
SUMMARY

The wood anatomy of the Chenopodiaceae is distinctive and fairly uniform. The secondary xylem is characterised by relatively narrow vessels (<100 m) with mostly minute pits (<4 m), and extremely narrow vessels (<10 m intergrading with vascular tracheids in addition to normal vessels), short vessel elements (<270 m), successive cambia, included phloem, thick-walled or very thick-walled fibres, which are short (<470 m), and abundant calcium oxalate crystals. Rays are mainly observed in the tribes Atripliceae, Beteae, Camphorosmeae, Chenopodieae, Hablitzieae and Salsoleae, while many Chenopodiaceae are rayless. The Chenopodiaceae differ from the more tropical and subtropical Amaranthaceae s.str. especially in their shorter libriform fibres and narrower vessels. Contrary to the accepted view that the subfamily Polycnemoideae lacks anomalous thickening, we found irregular successive cambia and included phloem. They are limited to long-lived roots and stem borne roots of perennials (Nitrophila mohavensis) and to a hemicryptophyte (Polycnemum fontanesii). The Chenopodiaceae often grow in extreme habitats, and this is reflected by their wood anatomy. Among the annual species, halophytes have narrower vessels than xeric species of steppes and prairies, and than species of nitrophile ruderal sites. Key words: Chenopodiaceae, Amaranthaceae s.l., included phloem, successive cambia, anomalous secondary thickening, vessel diameter, vessel element length, ecological adaptations, xerophytes, halophytes.
INTRODUCTION

The Chenopodiaceae in the order Caryophyllales include annual or perennial herbs, subshrubs, shrubs, small trees (Haloxylon ammodendron, Suaeda monoica) and climbers (Hablitzia, Holmbergia). They are often found in deserts, semi-deserts, salt-marshes, coastal or inland saline and ruderal sites (Volkens 1893; Ulbrich 1934; Khn et al. 1993). The family is temperate and subtropical, traditionally with 98 genera and c. 1400 species
1) Institute of Biology, Department of Geobotany and Botanical Garden, Martin Luther University of Halle-Wittenberg, Neuwerk 21, 06108 Halle (Saale), Germany [E-mail: heike.heklau@botanik. uni-halle.de]. 2) Jodrell Laboratory, Royal Botanic Gardens Kew, TW9 3DS, Richmond, Surrey, United Kingdom. 3) Swiss Federal Research Institute for Forest, Snow and Landscape, Zrcherstrasse 111, 8903 Birmensdorf, Switzerland. 4) NCB Naturalis - Nationaal Herbarium Nederland, P.O. Box 9514, 2300 RA Leiden, The Netherlands.

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(Khn et al. 1993). Amaranthaceae s.l., including Chenopodiaceae, number c. 2000 species (Mabberley 2008). Molecular studies by Cunoud et al. (2002) and Kadereit et al. (2003) have shown that the Chenopodiaceae and Amaranthaceae form a monophyletic clade that has recently been united as Amaranthaceae s.l., based on the assumption that the Chenopodiaceae are paraphyletic to Amaranthaceae. However, Kadereit et al. (2003) noticed that the relationship between Amaranthaceae and Chenopodiaceae remains unclear. Branches at the base of the Amaranthaceae / Chenopodiaceae lineage are poorly resolved. The position of the monophyletic Polycnemoideae is still equivocal, and according to Kadereit et al. (2003) it is sister to Amaranthaceae s. str. The first wood anatomy studies of Chenopodiaceae describing their successive cambia were by Link (1807), Unger (1840), Gernet (1859), De Bary (1877), Gheorghieff (1887), Leisering (1899) and Pfeiffer (1926). In 1899 and 1908, in his systematic anatomy of dicotyledons, Solereder ascertained similarities in the stem structure between Chenopodiaceae, Amaranthaceae and Nyctaginaceae. Metcalfe and Chalk (1950) reviewed the wood anatomy of Chenopodiaceae and recorded data on vessel diameter and vessel element lengths in a few species and genera. Fahn et al. (1986) gave detailed accounts of the wood anatomy of 22 species of Chenopodiaceae from the Middle East, and Schweingruber (1990) and Baas & Schweingruber (1987) included 14 species in their analysis of European woody plants. Most of the literature on Chenopodiaceae wood anatomy from 1900 until 1993 is listed in the bibliography by Gregory (1994), but there are also numerous anatomical studies of individual Chenopodiaceae in Russian (Arcichovskij & Osipov 1934; Ilin 1950; Butnik 1966, 1983; Vasilevskaja 1972; Novruzova & Chapari 1974; Lotova & Timonin 1985; Timonin 1987a & b, 1988) some of which are not included in Gregorys bibliography. The wood anatomy of the more tropical and subtropical Amaranthaceae was the focus of attention of Rajput (2002) and Carlquist (2003). Until now a comparative analysis of wood characters of the Chenopodiaceae has not been made. This study examines the range of wood characters in the Chenopodiaceae, a family predominantly adapted to extreme habitats.
MATERIAL AND METHODS

The wood anatomy of 182 species from 86 genera (out of a total of 98) Chenopodiaceae genera (Khn et al. 1993) was investigated (Table 1). These samples represent different life forms and plant sizes (after Ellenberg & Mueller-Dombois 1967): phanerophytes: microphanerophytes (25 m), nanophanerophytes (< 2 m), and hemiphanerophytes ( 0.5 m), and herbs: chamaephytes, therophytes (annuals), and hemicryptophytes. In our samples of Chenopodiaceae the proportion of annuals and perennials is well balanced: 52% are annuals and 48% perennials. Hemiphanerophytes and nanophanerophytes make up a large proportion of perennials. Small trees (microphanerophytes) and perennial herbs (chamaephytes and hemicryptophytes) are very poorly represented. Most of our material was collected in natural sites. The sampling represents the main distribution areas of Chenopodiaceae: 14% from Australia, c. 26% from Asia

Heklau et al. Wood anatomy of Chenopodiaceae

207

(Mongolia, Russia, Kazakhstan, Iran, Iraq, Turkey), 10% from Africa (North Africa, Kenya, Somalia and South Africa), 41% from Europe (Central and South Europe), 8% from North America (USA and Mexico) and 1% from South America (Chile). The plant material was collected either by HH or FS from natural habitats or was taken from the herbaria in Halle (HAL), Jena (JE), Lisbon (LISU) or Kew (K). The herbarium material was very heterogeneous with regard to the part of the axial system of shrubs or sub-shrubs collected, and in the information on the herbarium labels. With annual plants we had no problems with the herbarium material and took the stem base or root collar. Ecological categories The samples were assigned to the following ecological categories on the basis of our field observations and the literature: Ruderal (i.e. disturbed habitats) Cultivated in gardens Littoral Halophytes: coastal halophytes and inland halophytes (humidtemperate halophytes; steppe halophytes; desert halophytes; tropical / subtropical halophytes) Steppe or prairie Semi-desert Desert Tropical /subtropical shrub-land. Anatomical preparations We used traditional botanical microtechnique as described in Gerlach (1984). Fresh, fixed (in FAA) or dry plant parts of stems, branches, shoots or of roots were used to prepare microscope slides. Before cutting transverse, tangential and radial sections with a Reichert sliding microtome, the dry plant material was put in 70 % alcohol or in glycerine overnight or for several days. Safranin was used to stain lignified tissue red and astrablue or alcian blue to stain non-lignified cell walls blue. The sections were placed in alcian blue or in astrablue for 5 minutes, washed in water, placed in safranin (1% safranin in 50 % alcohol) for two minutes and transferred to 50 % alcohol. After dehydration through an alcohol series, the sections were placed in Histo-Clear (distilled essential oils food grade) or xylene and mounted in Euparal or Canada balsam. For maceration wood splinters were boiled in 10 % HNO3 (nitric acid) for 12 minutes, washed in water and stained with safranin. The splinters were dehydrated in the same way as described above, and teased apart with needles. Microscopic features We have broadly followed the IAWA list (1989), but have considered anomalous secondary thickening (cambial variants) in more detail. The tangentially arranged apotracheal axial parenchyma can be described as conjunctive tissue (Carlquist 1988, 2001) and, together with the secondary phloem, as cap-like, arc-like and band-like. The shape of this complex of secondary phloem and tangential axial parenchyma in the secondary xylem changes from the base to the apex in most Chenopodiaceae. There is commonly a gradient in the stem from band-like in the hypocotyl and epicotyl to arc-like to cap-like axial parenchyma in the apical part. In branches and shoots there is less variability in conjunctive parenchyma and it is mostly cap-like or less often arc-like. These terms (cap-like, arc-like and band-like) indicate the

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position in the axial system (root, basal stem, shoot or branch) where the cross section was taken. The occurrence and grouping of vessels varies with these positions in the stem and with the nature of the conjunctive parenchyma: from diffuse throughout the xylem when the parenchyma is banded (Fig. 2 E, F) to clustered in bundles adaxial to cap-like parenchyma and phloem strands (Fig. 2 A, C, D). Intermediates occur, especially where the conjunctive parenchyma is arc-like (Fig. 2 B). Xylem rays may be absent (Fig. 2 A, B) or present as 1- to 3-seriate rays (Fig. 2 D, E, 3 B, C, E). Less well-defined radial strips or wedges of axial parenchyma may also occur (Fig. 2 E, F). Diameter of vessel lumina Minimum, mean and maximum vessel lumen diameters are reported for each sample and species (Table 1). In these measurements we did not include the extremely narrow vessels, intergrading with vascular tracheids, which are present throughout the family when studied in longitudinal sections or macerations, but which are not always easy to identify in cross section, because there diameters are similar to those of the fibres and axial parenchyma cells (lumen diameters often <10 /m). Classification system adopted To put the anatomical characters in systematic context we followed recent phylogenetic insights and recognised eight subfamilies (Betoideae, Camphorosmoideae, Chenopodioideae, Corispermoideae, Polycnemoideae, Salicornioideae, Salsoloideae and Suaedoideae) and the tribal subdivision of the Chenopodiaceae (in part after Khn et al. 1993; Kadereit et al. 2003; Hohmann et al. 2006; Kadereit et al. 2010; Kadereit & Freitag 2011). As a result of molecular studies, the genera Sarcobatus and Halophytum were excluded as they are now established as separate families (Cunoud et al. 2002). Subfamilies Chenopodioideae Corispermoideae Camphorosmoideae Betoideae Salicornioideae Salsoloideae Suaedoideae Polycnemoideae Tribes in subfamilies Chenopodieae, Atripliceae, Axyrideae, Dysphanieae Corispermeae Camphorosmeae (incl. Sclerolaeneae) Beteae, Hablitzieae Halopeplideae, Salicornieae Salsoleae, Caroxyloneae Suaedeae, Bienertieae Polycnemeae

In the phylogenetic tree of the Chenopodiaceae (Hohmann et al. 2006 and modified by G. Kadereit (pers. comm.)) the Amaranthaceae s.str. and Polycnemoideae form a basal grade to Betoideae (Fig. 1). The Betoideae except Acroglochin are monophyletic. Acroglochin is sister to Corispermoideae. Polycnemoideae is sister to Amaranthaceae s. str. and these two are sisters to Chenopodioideae plus Corispermoideae.

Heklau et al. Wood anatomy of Chenopodiaceae

Amaranthaceae s.str.
(Up to 35, Rajput 2002)

209

Polycnemoideae
(Mainly in roots (Up to 6)

Corispermoideae

Chenopodioideae
(Up to > 20)

Salicornioideae (Up to 1016) Suaedoideae (Up to 9) Camphorosmoideae (Up to 18, Turki et al. 2008) Salsoloideae (Up to 12) Betoideae

(In the tap root and hypocotyl, up to 46, Krumbiegel 1998)

Achatocarpaceae

(Without anomalous secondary thickening)

Figure 1. Simplified phylogenetic tree of Chenopodiaceae, modified from the maximum likelihood tree based on 26 matK/trnK sequences by Hohmann et al. (2006). The maximum number of successive cambia recorded in annual species is shown between parentheses.

Chenopodioideae plus Corispermoideae are sisters to Betoideae as sister to Salsoloideae and Camphorosmoideae. The Salsoloideae are sister to Camphorosmoideae and these two are sister to Salicornioideae and Suaedoideae. At the base of this polytomy (Fig. 1) the Achatocarpaceae are separate. This family comprises two genera and about six species occurring from Texas, California and NW Mexico to Paraguay and Argentina with no anomalous secondary growth (Bittrich 1993). Cunod et al. (2002) differentiates between the core Caryophyllales (Caryophyllaceae, Amaranthaceae s.str., Chenopodiaceae, Molluginaceae, Aizoaceae, Phytolaccaceae, Cactaceae, Portulacaceae, Didiereaceae, Nyctaginaceae, Basellaceae) and non-core Caryophyllales (Polygonaceae, Plumbaginaceae, Frankeniaceae, Droseraceae, Nepenthaceae, Tamaricaceae, Ancistrocladaceae, Dioncophyllaceae). The Achatocarpaceae, Caryophyllaceae, Amaranthaceae s.str., Chenopodiaceae plus Rhabdodendron and Simmondsia belong to the Lower core Caryophyllales and the other core families (text continued on page 216) to the more derived Higher core Caryophyllales.

Table 1. Chenopodiaceae studied, and selected anatomical attributes.

210

Abbreviations (of Life form): C = Chamaephyte, F = Nanophanerophyte, H = Hemicryptophyte, M = Microphanerophyte, S = Hemiphanerophyte, T = Therophyte. 1 = Vessel diameter, range in m 2 = Vessel diameter, median value in m 3 = Vessel element length, range in m 4 = Intervessel pit size in m 5 = Rays: A, B, C = rays distinct (A = rays uniserate, B = rays 14-seriate, C = rays 510-seriate; * rays weakly differentiated); D = rays indistinct (rayless with distinct strips of radial (axial) parenchyma); N = wood rayless. ? = feature not observed or measured.
Origin Ecological category 1 2 3 4 5

Species

Plant part

Life form

IAWA Journal, Vol. 33 (2), 2012

Acroglochin persicarioides Agriophyllum minus pungens squarrosum Alexandra lehmannii lehmannii Allenrolfea occidentalis Anabasis articulata brevifolia Anthochlamys polygaloides Aphanisma blitoides Arthrocnemum fruticosum perenne Arthrophytum thomsonii Atriplex canescens cinerea deserticola glauca var. ifniensis glaucescens halimus holocarpa hortensis hortensis littoralis nummularia patula patula patula prostrata prostrata prostrata rosea sagittata

stem branch stem branch hypocotyl shoot basal branch hypocotyl rhizome branch root stem unknown branch stem branch branch unknown hypocotyl branch hypocotyl hypocotyl stem epicotyl branch hypocotyl hypocotyl stem hypocotyl stem stem stem, basal stem

T T T T T T F S S T T F F S F F F F/S S F T T T T F T T T T T T T T

Germany Uzbekistan Western Mongolia Ad lacu Indewuu Kazachstan Kazachstan Mexico Spain Mongolia Southwest Persia USA France Spain Pakistan USA South Australia Chile Spain Chile Algeria Australia Switzerland Switzerland Germany South Australia Switzerland Slovakia Germany Italy Austria Austria USA Germany

ruderal, garden culture semidesert steppe steppe steppe halophytes steppe halophytes coast halophytes desert steppe semidesert subtropical halophytes coast halophytes coast halophytes steppe prairie littoral desert steppe desert subtropical halophytes tropical/subtropical halophytes garden culture garden culture littoral semi-desert ruderal ruderal ruderal littoral ruderal ruderal ruderal ruderal

2232 3746 3343 2940 1723 1620 2940 1825 1822 2535 2133 1619 2227 1219 2939 2631 3242 3134 2332 1621 3142 3444 3336 2431 1316 2835 4049 2838 3554 3246 3147 2236 3053

27 42 38 35 20 18 35 22 20 30 27 17 24 16 34 44 37 32 28 18 37 39 34 28 14 31 45 33 44 39 39 29 41

100200 150200 50150 150200 50100 50100 50100 50100 50100 90160 100150 50100 100160 30100 50100 ? 50100 100150 <100 80180 50120 100120 80150 100150 50150 50100 100150 50100 50120 50100 50100 30130 50130

c. 2.5 c. 3.4 <4 c. 2.5 37 37 c. 4 <4 << 4 c. 3 2.72.9 4 c. 3.4 c. 2 <4 ? <4 <4 <4 <4 <4 2.73.4 <4 c. 3.7 c. 4 47 47 4 c. 2.5 c. 3 <4 c. 3 <4

B B A, B D N D D B* B D B D B N D B N D B* B B B B B N B B B B B B A, B B

Heklau et al. Wood anatomy of Chenopodiaceae

(Atriplex) sagittata semibaccata vesicaria Axyris hybrida Bassia arabica eriophora eriophora hirsuta hirsuta laniflora muricata muricata prostrata prostrata scoparia scoparia scoparia sedoides sedoides sedoides stellaris Beta trigyna vulgaris Bienertia cycloptera Borszczowia aralocaspica Camphorosma annua annua monspeliaca monspeliaca soongoricum Ceratocarpus arenarius arenarius Chenoleoides tomentosa tomentosa Chenopodium album ambrosioides ambrosioides bonus-henricus bonus-henricus botrys capitatum ficifolium

hypocotyl hypocotyl branch hypocotyl branch stem branch branch branch stem stem branch root, hypocotyl root, hypocotyl branch hypocotyl stem, basal branch stem branch stem stem branch stem branch hypocotyl stem branch branch branch stem stem branch branch hypocotyl stem stem rhizome rhizome stem stem stem

T C S T S T T T T T T T F/S F/S T T T T T T T H H T T T T S F/S T T T S S T T T H H T T T

Germany Spain South Australia Russia Israel Turkmenistan Iran France France Poland Tunesia Iraq Russia Spain Portugal Germany USA Russia Russia Russia Iran Germany Portugal Iraq Kazachstan Hungary Hungary Great Britain France Israel Kazachstan Russia Spain Spain, Canaries Italy Switzerland Portugal Switzerland Italy No information France Portugal

ruderal ruderal tropical/subtropical shrub-land steppe semi-desert semi-desert semi-desert littoral littoral ruderal desert desert steppe steppe ruderal garden culture ruderal steppe halophytes steppe halophytes steppe halophytes semidesert garden culture littoral steppe halophytes steppe halophytes steppe halophytes steppe halophytes subtropical halophytes subtropical halophytes steppe halophytes steppe steppe littoral littoral ruderal garden culture garden culture ruderal ruderal ruderal ruderal ruderal

3241 3343 2026 2328 1520 1923 2125 2126 1320 1324 3343 2636 1323 911 1824 2942 2330 1522 1218 1316 1318 2933 2739 2225 2938 1419 1522 1941 1418 1622 1924 1013 1317 1618 2935 3757 3143 3640 2131 2737 1924 3543

36 38 23 26 18 21 23 23 17 19 38 31 18 10 21 36 27 19 15 14 15 31 34 23 34 17 18 30 16 19 21 12 15 17 32 47 37 38 26 32 22 39

100160 40100 50150 50120 100220 50120 100200 100150 50150 50150 80120 50100 50120 ? 100150 80120 50150 50120 >50>100 100150 50150 150200 50120 100150 35100 80150 50100 ? 50100 100200 ? ? 90150 50100 50150 50100 100150 80120 ? 50120 50150 80150

c. 3 c. 4 <4 <4 c. 2.5 c. 2.8 c. 2.5 c. 2.5 c. 2.8 <4 <4 c. 2.5 <4 <4 c. 3.8 <4 c. 3.5 c. 2.3 <4 3.74 c. 2 <4 c. 3.5 c. 3.5 2.8 c. 3 c. 3 <4 22.8 ? ? ? c. 2.5 <4 <4 <4 3.4 <4 <4 <4 c. 2.5 1.52

211

B N B B* D B B B B B B B B B B, C B, C B, C B B B B B B D B A, B A, B B, C B, C B B N B B B, C B B B B B* B B (continued)

Species

Plant part

Life form

Origin

Ecological category

212 IAWA Journal, Vol. 33 (2), 2012

(Chenopodium) foliosum giganteum glaucum glaucum hybridum murale opulifolium polyspermum quinoa rubrum strictum urbicum urbicum urbicum urbicum vulvaria Corispermum patelliforme Cornulaca aucheri monacantha Cycloloma atriplicifolium atriplicifolium atriplicifolium atriplicifolium atriplicifolium Dissocarpus paradoxus Einadia nutans Enchylaena tomentosa Eremophaea aggregata Exomis axyrioides Fadenia zygophylloides Gamanthus gamocarpus Girgensohnia oppositiflora Grayia spinosa Hablitzia tamnoides tamnoides Halanthium purpureum Halimione pedunculata pedunculata pedunculata portulacoides

stem stem hypocotyl stem stem stem stem stem hypocotyl epicotyl stem stem stem stem stem stem branch branch branch stem stem stem stem stem branch branch branch branch branch branch stem stem branch root annual shoots stem (liana) hypocotyl stem epicotyl stem

T T T T T T T T T T T T T T T T T T F/S T T T T T F/S C F S F S T T F/S H H T T T T C

Switzerland Switzerland Germany Austria Austria Oman Portugal Switzerland Switzerland Germany Switzerland Germany Austria Spain Switzerland Libya West Mongolia Iraq Libya USA Germany Germany Germany Italy Australia Spain South Australia Australia South Africa Somalia Turkmenistan Southwest Persia USA Germany Germany Southwest Persia Germany Germany Germany Cyprus

ruderal garden culture ruderal ruderal ruderal ruderal ruderal ruderal garden culture ruderal ruderal ruderal ruderal ruderal ruderal ruderal steppe semi-desert desert prairie garden culture garden culture garden culture ruderal tropical/subtropical shrubland ruderal tropical/subtropical shrubland tropical/subtropical shrubland littoral tropical/subtropical halophytes steppe semi-desert prairie garden culture garden culture desert humid temperate halophytes humid temperate halophytes humid temperate halophytes coast halophytes

2736 4049 2025 2532 2235 3142 2532 2533 3239 2127 3948 4152 3751 4257 1419 4454 3152 2531 3438 2532 2334 3342 2130 2531 2027 4660 2025 2026 2632 2027 1519 2327 2740 2832 3450 1214 1726 1728 1823 3037

32 45 22 29 30 37 29 29 36 24 44 47 44 50 17 49 41 28 36 28 29 37 25 28 23 53 22 23 29 23 17 25 33 30 42 13 21 22 21 33

50100 50110 50100 <100 50150 50200 50100 30130 100150 50100 50150 70120 30100 50150 50100 <100 50120 50150 50110 50150 50100 100250 100250 100200 50130 ? 60100 50120 50120 5090 50150 50150 50120 100150 100150 100150 c. 100 50120 100200 50150

<4 c. 3.5 c. 3.5 c. 3 33.5 4 2.83 c. 2.7 c. 3.3 c. 3 4 c. 4 c. 3 <4 c. 3.5 c. 3 c. 2 c. 2.4 <4 c. 4 c. 3 c. 3 c. 3 c. 3.6 c. 3 ? c. 2 <4 c. 3 2.62.9 c. 3 c. 3 4 <4 <4 c. 2.5 c. 3 c. 3.5 3.54.5 <4

D B B B B N B B B B, C D B B B B B A, B D A, B B B B B B A, B D A, B A, B B* D D B N.A. B N.A. B D D D D

Heklau et al. Wood anatomy of Chenopodiaceae

(Halimione) portulacoides portulacoides verrucifera verrucifera verrucifera Halimocnemis mollissima Halocharis sulphura Halocnemum strobilaceum Halogeton alopecuroides Halopeplis amplexicaulis perfoliata Halosarcia auriculata bulbosa calyptrata halocnemoides subsp. caudata Halostachys caspica caspica caspica Halothamnus glaucus subaphyllus Halotis pilosa Haloxylon ammodendron ammodendron griffithii persicum salicornicum tamariscifolium Hammada articulata scoparia scoparia Horaninovia anomala Iljinia regelii Kalidium arabicum foliatum foliatum gracile Kirilowia eriantha Krascheninnikovia ceratoides subsp. ceratoides subsp. ceratoides subsp. ceratoides Mongolia Spain Russia steppe steppe steppe 2738 2635 2229 32 31 25 60100 60100 60100 <4 <4 <4 N N N (continued)

branch branch branch branch branch stem stem stem, basal stem stem stem branch branch branch branch branch? branch branch branch branch branch stem branch branch branch branch branch branch branch branch stem branch branch branch branch branch root, hypocotyl

C C F/S F/S F/S T T F T T T F/S F/S F S F/M F/M F F/S F T F/M F/M F/S F/M S F/S F F F T S F F/S F S T

Southeast Spain Cyprus Iran Persia Persia Turkmenistan Iran Turkey Algeria Italy Oman Australia Australia Australia Australia Caucasus Turkmenistan Georgia Iran Turkmenistan Turkmenistan Mongolia Iran Afghanistan Iran Oman Algeria Spain Morocco Algeria Transcaspica Tjan Shan Armenia Mongolia Russia South Mongolia Kazachstan

coast halophytes coast halophytes steppe halophytes steppe halophytes steppe halophytes desert semidesert coast halophytes desert subtropical halophytes coast halophytes subtropical halophytes tropical/subtropical shrub-land subtropical halophytes subtropical halophytes semi-desert semi-desert semi-desert semi-desert semi-desert semi-desert desert desert desert desert semi-desert desert desert desert desert semi-desert semi-desert steppe halophytes steppe halophytes steppe halophytes desert halophyte semi-desert

2934 2632 1822 1218 1520 1924 1621 1824 1217 1518 1620 1014 1316 1217 1114 3450 3350 1019 1821 2026 13.17 6171 2227 2128 3647 1620 1925 1518 1928 2433 2125 1215 2127 2029 2328 2128 1622

32 29 20 15 18 21 19 21 14 16 18 12 15 14 12 42 42 15 20 23 15 66 25 25 42 18 22 17 23 29 23 13 24 25 25 25 19

20100 50100 c. 50 50100 50100 80120 90160 80150 <100 50100 <150 90120 40150 50130 40100 50200 80160 2080 50100 50150 ? 100 5090 80130 ? <150 5080 50100 50100 50<100 50150 50100 80150 <50100 50100 >50120 50140

c. 2 c. 2.4 c. 3 c. 2.5 c. 2 c. 3 c. 3 c. 3 c. 3 c. 2.5 << 4 2.53.4 c. 1.7 2.52.9 c. 2.5 <4 c. 2 33.5 22.5 c. 2.2 ? <4 c. 3.2 c. 2.5 ? <4 c. 2.5 c. 3 <4 <4 c. 3 c. 1.8 ? <4 c. 3.5 c. 2 2.62.8

D D D D D D A, B D N D N N N N D D D D B N B ? N B A* A, B N N N N B N ? N ? N B

hypocotyl hypocotyl hypocotyl

F F F

213

Species

Plant part

Life form

Origin

Ecological category

214 IAWA Journal, Vol. 33 (2), 2012

Lagenantha cycloptera gillettii Maireana pyramidata sedifolia Microgynoecium tibeticum Micronemum coralloides Micropeplis arachnoidea Monolepis asiatica nuttalliana nuttalliana Nanophyton erinaceum erinaceum Neobassia proceriflora proceriflora Nitrophila mohavensis mohavensis Noaea major mucronata Nucularia perrini Ofaiston monandrum Oreobliton thesioides Pachycornia triandra triandra Panderia pilosa Patellifolia patellaris procumbens Petrosimonia glauca monandra oppositifolia Piptoptera turkestana Polycnemum arvense arvense fontanesii fontanesii majus majus Rhagodia baccata preisii spec. Roycea divaricata

branch branch branch branch hypocotyl stem stem stem stem hypocotyl hypocotyl unknown branch branch stem born root root stem branch branch hypocotyl hypocotyl branch branch hypocotyl stem stem stem hypocotyl stem stem hypocotyl hypocotyl root branch hypocotyl root branch branch branch branch

S S F F T T T T T T S S S S C C T F/S S T H S S T H H T T T T T T C C T T F F F F

Somalia Kenya Australia Australia China Spain East Mongolia Germany Germany USA Mongolia Kirgizia Australia Australia USA USA Turkmenistan Southeast Anatolia Algeria Russia Algeria Australia Australia Armenia Spain Spain Turkmenistan No information Southwest Persia Buchara France Italy Algeria Algeria Germany Germany South Australia South Australia South Australia Australia

tropical/subtropical shrub-land tropical/subtropical shrub-land tropical/subtropical shrub-land tropical/subtropical shrub-land ruderal subtropical halophytes steppe ruderal garden culture prairie steppe steppe tropical/subtropical shrub-land tropical/subtropical shrub-land desert desert semidesert semidesert desert steppe halophytes desert subtropical halophytes subtropical halophytes ruderal? littoral littoral steppe halophytes steppe halophytes steppe ruderal? temperate sand soils temperate sand soils desert desert garden culture ruderal tropical/subtropical shrub-land tropical/subtropical shrub-land tropical/subtropical shrub-land tropical/subtropical shrub-land

1419 2026 1927 1319 1020. 1014 2028 1722 1829 2638 1621 1518 1925 2129 2631 2431 2326 1621 2128 1623 1419 2125 1722 1926 3548 4664 1622 1824 1934 2124 1417 1418 1117 1113 1012 1621 1923 3036 2434 1115

17 23 23 16 15 12 24 19 23 32 18 17 22 25 28 28 25 18 25 19 17 23 20 22 41 55 19 21 26 23 15 16 14 12 11 19 21 33 29 13

4080 50120 50130 50100 4080 c. 50 50150 50100 50150 50100 <50 50100 50100 100200 50100 50110 50120 50120 100200 100130 100120 70120 70130 50100 50150 100200 100220 50100 100150 50150 50150 50150 C. 120 50110 ? 100200 60120 80120 50160 110160

2.02.9 c. 2 c. 3 c. 2 1.82.2 c. 2 c. 2 <3 c. 3 c. 3 <4 2.7 c. 2 2.0 2.6 c. 2 c. 2.4 c. 3 c. 3 c. 2.5 +/- 4 c. 2.5 3.73.9 c. 2.5 c. 2.5 <4 <4 c. 3 c. 3.5 3.33.5 3.03.5 <4 c. 3.5 3.54.5 c. 3.7 ? c. 2.3 ? <4 <4 c. 3

N N B A, B A, B B B A, B B B N N A, B B B B B D D B A, B N N B B B D D B D A, B A, B B A A, B A, B N D D A, B

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Salicornia europeea europeea subsp. brachystachya fragilis nitens patula ramosissima Salsola arbuscula genistoides kali kali kali kali subsp. tragus oppositifolia passerina soda vermiculata vermiculata Sclerolaena convexula densiflora glabra oliquicuspis Seidlitzia florida florida rosmarinus Sevada schimperi Spinacia turkestanica Suaeda aegyptiaca albescens maritima spicata splendens splendens vera vera Suckleya suckleyanum Sympegma regelii Tegicornia uniflora Threlkeldia diffusa inchoata Traganum nudatum nudatum Zuckia brandegeei

hypocotyl basal stem hypocotyl stem stem epicotyl branch stem hypocotyl stem stem stem branch branch hypocotyl/root branch branch root, hypocotyl branch branch branch hypocotyl branch stem, basal branch branch stem epicotyl hypocotyl hypocotyl stem? stem branch stem branch branch branch branch stem branch branch branch

T T T T T T F/S F T T T T F S T F F C C S S T T F S T T T T T T T F S T S C C C S S S

Germany Germany South Portugal Portugal Portugal Portugal West Mongolia Spain Italy USA Spain Portugal Spain West Mongolia Portugal Spain Spain Australia Australia South Australia Australia Baku Armenia Iraq Oman Turkmenistan Egypt Portugal Germany Portugal Portugal Portugal Libya Portugal USA Mongolia Australia Australia Australia Egypt Algeria USA

humid temperate halophytes humid temperate halophytes coast halophytes coast halophytes coast halophytes coast halophytes steppe steppe littoral prairie steppe littoral littoral steppe littoral steppe steppe semidesert semidesert tropical/subtropical halophytes tropical/subtropical shrub-land steppe halophytes steppe halophytes desert desert steppe subtropical halophytes coast halophytes humid temperate halophytes subtropical halophytes coast halophytes coast halophytes subtropical halophytes subtropical halophytes prairie desert tropical/subtropical halophytes subtropical halophytes tropical/subtropical halophytes desert desert prairie

1218 1215 1317 1316 1214 1418 3540 1721 3241 3146 2533 3239 2023 920 2127 2128 2637 1620 1725 2026 1520 1624 2027 2328 1519 2840 3137 1519 1827 1518 1524 2230 1927 2326 1923 3140 1619 1318 1520 2735 2127 2227

15 14 15 14 13 16 38 19 36 38 29 35 22 15 24 24 31 18 21 23 18 20 24 26 17 34 34 17 22 16 19 26 23 25 21 36 17 15 17 31 24 25

40100 50100 80150 50120 50120 100200 50100 50100 50100 50120 50110 100200 50130 >50120 50130 50100 50150 50120 40100 80140 50100 50130 100200 50150 3070 70200 80150 50100 50100 30100 100130 100160 50100 ? 100200 50110 70120 50100 100180 100120 80120 50100

3.53.8 2.02.4 c. 3.8 3.33.6 c. 2.7 c. 3.5 <4 ? <4 <4 c. 3 3.84.0 c. 3 <4 3.84.0 <4 c. 2.4 c. 3 2.42.9 <4 <4 2.54 c. 2.7 c. 2.8 c. 2 47 <4 c. 3.5 47 c. 3 c. 3 c. 3.5 <4 ? c. 2.5 <4 2.4 c. 2 3.23.3 c. 3.5 c. 2 c. 3

B B B B B B B A, B B B B B B D A, B B B B B A, B A, B D B A, B A B A, B B D B B B N N ? B* N A, B A, B N N N

215

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Statistical methods Anatomical characters were analysed by simple correlations. To test for differences among the regions we used ANOVAs and Tukey post-hoc tests. All statistical analyses and plotting were made using the R software (R Development Core Team 2009).

Figure 2. A: Krascheninnikovia ceratoides (Axyrideae), branch with cap- and arc-like, unlignified conjunctive parenchyma and without radial parenchyma. B: Krascheninnikovia ceratoides (Axyrideae), basal stem with band-like, unlignified tangential parenchyma and without radial parenchyma. C: Noaea mucronata (Salsoleae), branch with cap- and arc-like, unlignified tangential parenchyma; black arrow shows a growth ring boundary. D: Seidlitzia rosmarinus (Salsoleae), branch with two distinct vessel diameters, cap-like tangential parenchyma and xylem rays; black arrow shows a growth ring boundary. E: Sclerolaena densiflora (Sclerolaeneae), basal stem with discontinuous radial parenchyma strips. F: Atriplex prostrata (Atripliceae), basal stem with rays; the axial and ray parenchyma is in an irregular net-like pattern. Scale bars = 200 m in A, B, C, E, F; 100 m in D.

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RESULTS

Number of Successive cambia (Fig. 1) Anomalous secondary thickening has developed to different extents in Amaranthaceae s. str., Polycnemoideae and Chenopodiaceae. In the Polycnemoideae it is limited to the older tap root or stem borne roots (Fig. 3). In the basal lineage of Chenopodiaceae it occurs in the fleshy tap root and hypocotyl (Betoideae). From the tap root and hypocotyl anomalous secondary thickening has arisen in the axis (all other sub-families of the Chenopodiaceae). In the Salsoloideae, Suaedoideae, Salicornioideae, Camphorosmoideae, Chenopodioideae, Corispermoideae and Amaranthaceae s.str. successive cambia are present in the root, hypocotyl, in stems, in branches and in the terminal shoots. Amaranthaceae s.str. have successive cambia in roots and all the above-ground axes. In Polycnemoideae anomalous growth seems to be restricted mainly to older roots and then in a rather irregular form (Fig. 3 B and F ). Successive cambia and included secondary phloem are typical in Chenopodiaceae. The largest number of successive cambia (Fig. 1) was found in the basal stem of annuals of the following tribes: Atripliceae (Atriplex prostrata up to 19), Halopeplideae (Halopeplis perfoliata up to 16), Chenopodieae (up to 14), Salicornieae (Salicornia europaea up to 9), Salsoleae (Seidlitzia florida up to 9), Suaedeae (Suaeda maritima up to 9), Camphorosmeae (Bassia scoparia up to 6), Bienertieae (Borszczowia aralocaspica up to 9) and Corispermeae (Agriophyllum minus up to 6). The annual species of Atriplex (Atripliceae) have the highest number of successive cambia. In the autumn of 2010 we found samples of Atriplex sagittata with 24 successive cambia in ruderal sites in central Europe. Successive cambia were only absent in the root and stem of the monotypic annual genus Aphanisma (Hablitzieae, Betoideae), but we investigated only one sample. Hablitzia (Hablitzieae, Betoideae) from the Caucasus Mountains possesses twining short-lived shoots and a perennial pleiocormus with up to four successive cambia, while the short-lived shoots are without secondary thickening (according to Meusel 1968, a pleiocormus is a herb with a main root and few or numerous basal stocky stems). In some samples of the Sclerolaeneae (Australian Camphorosmeae, for example Roycea divaricata) we were also unable to find successive cambia, but we only investigated young shoots or branches of these sub-shrubs and more samples are needed. Successive cambia in the Polycnemeae (Fig. 3) Successive cambia do not occur in roots or short stems of the short-lived species Polycnemum arvensis and P. majus. However, in the North African sub-shrub Polycnemum fontanesii we found irregularly arranged successive cambia in the root (Fig. 3 B). After more than 10, 11 and 12 growth periods, the next successive cambium started and produced secondary xylem in five or more growth periods. In the branches of P. fontanesii successive cambia are absent, but the branches we examined may have been too young (6 years) or are only short-lived in this species. It seems that the anomalous secondary thickening in Polycnemum is limited to very long-living roots. In the roots and in the stem borne roots of the perennial herb Nitrophila mohavensis (Fig. 3 F), also belonging to the Polycnemeae, successive cambia do exist, but are absent in the stem.

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Figure 3. Polycnemoideae. A: Polycnemum fontanesii, a chamaephyte, Herbarium Jena (JE). B: Polycnemum fontanesii, cross section of root with irregular successive cambia. C: Polycnemum fontanesii, cross section of a branch without successive cambia. D: Nitrophila mohavensis, a chamaephyte, Herbarium Kew (K). E: Polycnemum arvense, cross section of a short-lived root without successive cambia, but with growth rings. F: Nitrophila mohavensis, cross section of stem borne root with irregular successive cambia. Scale bars = 200 m in B, F; 50 m in C; 100 m in E.

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However, anomalous thickening has been observed by R. Masson & G. Kadereit (pers. comm.) in the axis of Polycnemoideae, but they did not specify which species and genera. Incidentally, growth rings are recognisable (Fig. 3 E) in the cross sections of roots in Polycnemum majus and P. arvense, so these species can also be perennial herbs and not only annuals as stated by Tutin et al. (1993). Activity of successive cambia The activity (duration of cell divisions) of successive cambia varies in Chenopodiaceae: very short in annuals; a relatively short or long time (several growth periods) in perennials or sub-shrubs. In annuals the activity of each successive cambium ends when the respective secondary xylem and secondary phloem have developed, not before the next cambium starts cell divisions. In longer lived plants the growth rings are not always distinct. At the end of the growth period fibres in the secondary xylem are narrower and radially flattened (Fig. 2 C), provided that the climate is truly seasonal. These fibres at the end of the growth period are different in size and shape from the other fibres. The fibre wall thickness changes very little over the growth period in longer lived plants. In annuals, e.g. Atriplex and Chenopodium, each successive cambium is active for only a few weeks (Heklau 1992), much longer in sub-shrubs. In sub-shrubs only a few successive cambia (14) are active in one growth period. In the basal stem of the subshrub Bassia prostrata (Camphorosmeae) from northeast Spain, we found one growth ring in the wide secondary xylem arising from the first successive cambium. In contrast, there were four narrow growth rings in the secondary xylem of the first cambium in the basal stem of the sample from eastern Russia. In Bassia prostrata the duration of cell divisions of a single cambium is interrupted by a dry or cold period, after which the cambium continues. This activity seems to be related to the quantity of the secondary xylem produced. The activity of a single successive cambium covers several growth periods not only in Bassia prostrata, but also in Maireana, Sclerolaena, Threlkeldia, Eremophaea aggregata (Australian Camphorosmeae), Lagenantha (Salsoleae) and in Polycnemum fontanesii and Nitrophila mohavensis (Polycnemeae). Growth ring boundaries are frequently indistinct or absent in sub-shrubs. The distinctness of growth ring boundaries can be variable in a climate with irregular cold or dry periods: for instance in the Mediterranean (Atriplex halimus, Salsola vermiculata, Hamada scoparia, Krascheninnikovia ceratoides in Spain) or in semi-deserts in Australia (Halosarcia species in Salicornieae and Rhagodia in Chenopodieae). Vessel diameter In the Chenopodiaceae studied here the mean diameter of vessel lumina is always less than 70 m (Table 1). The widest vessels are in the small tree Haloxylon ammodendron. Wide vessels were found in the hypocotyl of some annual Atriplex and Chenopodium species, in the perennial herb Patellifolia procumbens (basal part), and in the pleiocormus of Hablitzia tamnoides. The narrowest vessels (913 m) occur in some small annuals or short-lived plants such as Ceratocarpus arenarius (Atripliceae), Halanthium purpureum (Suaedeae) and in sub-shrubs in extreme locations (saline soils, gypsaceous soils) such as Halosarcia

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auriculata (Salicornieae), Bassia prostrata (Camphorosmeae), Roycea divaricata (Sclerolaeneae) and in Illjinia regelii (Salsoleae). In the tribe Salsoleae, the mean vessel diameter varies greatly between 13 and 66 m. This large tribe, traditionally with 32 genera includes different growth forms, with a similar number of annuals and perennials (perennial herbs, sub-shrubs, shrubs and small trees). The range of vessel diameters is narrower in the tribes Corispermeae and Sclerolaeneae, which are either annuals or sub-shrubs. Mean vessel diameter, ecology and life forms The strong influence of macroclimatic and soil factors on mean vessel diameter is shown in the different life forms combined (Table 2, Fig. 4 and 5). In annual Chenopodiaceae the vessels are especially narrow in individuals of deserts, semi-deserts and in halophytes. The differences in mean vessel diameter between annual halophytes of different climate zones are small. Coastal halophytes have the narrowest vessels followed by steppe halophytes, humid temperate halophytes, and tropical/subtropical halophytes (Fig. 4). The annuals in deserts and semi-deserts also have relatively narrow vessels. Salt and drought clearly are associated with a low mean vessel diameter in annuals. The annuals of ruderal places and gardens, prairies, steppes and near the coasts (littoral) without high levels of salt and higher humidity have wider vessels (mean diameter 29 to 33 m). The statistical tests show highly significant difTable 2. Tukey multiple comparisons of mean values for vessel diameter in different ecological categories.
2.1. Annuals Comparison of ecological categories
Garden culture ~ coast halophytes Ruderal ~ coast halophytes Steppe halophytes ~ garden culture Steppe halophytes ~ ruderal Humid temperate halophytes ~ ruderal

Differences between ecological categories (m)

16 15 -13 -12 -13

Significance level of differences

** ** ** ** *

2.2. Annuals Comparison of ecological categories (All halophytes combined into one ecological category)
Halophytes ~ garden culture Ruderal ~ halophytes Steppe / prairie ~ halophytes
*** = p < 0.001; ** = p < 0.01; * = p < 0.05.

Differences between ecological categories (m)

-13 12 8

Significance level of differences

*** *** *

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50

221

Mean vessel diameter in m

40

* * *

30

20

10
Desert plants Semi-desert Steppe/ prairie Tropical / subtropical halophytes Coast halophytes Garden culture Humid temperate halophytes Tropical / subtropical shrub-land Littoral Steppe halophytes Ruderal

Figure 4. Range of mean vessel diameters in m in therophytes (annual herbs) of Chenopodiaceae in different ecological categories. Each box-plot with bars shows the range of values or observations. The range is divided into four quartiles. The distance from lower bar to rectangle shows the first quartile (25 % of the values). The rectangle contains the second and third quartile. The distance from rectangle to the upper bar shows the fourth quartile. In the rectangle the band marks the median. The median (not mean value) is a numerical value separating the lower half of a sample from the upper half. Any data not included between the box-plot are plotted as an outlier with an asterisk.

*
60

Mean vessel diameter in m

50 40 30 20 10
Coast halophytes Desert Desert halophytes Tropical / subtropical halophytes Semi-desert Steppe/ prairie Steppe halophytes Littoral Ruderal

* *

Figure 5. Range of mean vessel diameters in m in sub-shrubs (microphanerophytes, nanophanerophytes, hemiphanerophytes) in Chenopodiaceae in different ecological categories. See caption of Fig. 4 for an explanation of the box-plot.

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ferences between the mean vessel diameter of coastal halophytes and plants in gardens, between coastal halophytes and ruderal plants, between steppe-halophytes and ruderal plants, between steppe-halophytes and plants in gardens and between humid temperate halophytes and ruderal plants (Table 2.1). When the categories of different halophytes are combined into one, the differences of mean vessel diameter are highly significant between halophytes and plants of the steppes and prairies, and also between halophytes and ruderal plants and halophytes and plants in gardens (Table 2.2). In sub-shrubs the vessels in branches are mostly narrow, while the main stems have slightly wider vessels (data not shown). There are only very minor, statistically nonsignificant differences between the various ecological categories of perennial plants. Only the single value for a ruderal species with relatively wide vessels stands out (Fig. 5). Vessel element length Mean vessel element length does not exceed 250 m. In some species of the tribe Camphorosmeae, e.g. Camphorosma soongoricum, Cycloloma atriplicifolium, Bassia eriophora, relatively long vessel elements (>200 m) are frequent. In the tribe Corispermeae, that only comprises annual species, the mean vessel element length is frequently 150200 m, especially in Agriophyllum and Anthochlamys. Also in the Betoideae, in Hablitzia, Patellifolia and Acroglochin, the mean vessel element length can vary between 100 and 200 m. Extremely short vessel elements (30 or 40100 m) are frequent in Salicornieae, Salsoleae and Suaedeae. The range of vessel element lengths is quite small in some species, e.g. in the branches of the small tree Haloxylon ammodendron (5090 m), whereas the range is much larger in the axis of the annual herb Chenopodium murale (50200 m) and in the branches of the sub-shrub Halostachys caspica (80160 m). Overall, the vessel elements are very short. Intervessel pits Intervessel pits are often alternate. In about 40% of the samples they were exclusively alternate. Only in 11% of the species alternate intervessel pits are entirely absent. In about 49% the intervessel pitting is mixed: alternate/opposite, or occasionally alternate/scalariform or alternate, opposite and scalariform. Exclusively opposite intervessel pitting occurred only in Alexandra lehmannii (Suaedeae), Bassia stellaris and in Halosarcia auriculata. Scalariform intervessel pits occurred mostly together with opposite and/or alternate pits. Scalariform pits in combination with the other types were frequent in Salsoleae (Girgensohnia oppositiflora, Halothamnus subaphyllus, Haloxylon griffithii, Horaninovia anomala, Lagenantha cycloptera, Micropeplis arachnoidea, Seidlitzia rosmarinus), Chenopodieae (Chenopodium capitatum, C. hybridum, C. polyspermum, C. strictum) and Betoideae (Acroglochin persicarioides). Only in Chenopodium bonus-henricus, Beta trigyna, Patellifolia procumbens (Fig. 6 D) and Hablitzia tamnoides (Fig. 6 C) are the pits mostly scalariform. Intervessel pits are mostly < 4 m. However, in Allenrolfea occidentalis, Atriplex patula, Arthrocnemum fruticosum, Polycnemum fontanesii, Spinacia turkestanica and Suaeda maritima they were slightly larger than 4 m, and Atriplex patula and Suaeda

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Figure 6. A: Nucularia perinii (Salsoleae) from northwest Africa. Sclerified pith cells in branch. B: Tegicornia uniflora (Salicornieae), cross section of a branch. Aerenchyma in the primary cortex. C: Hablitzia tamnoides (Hablitzieae): scalariform to reticulate intervessel pits. D: Patellifolia procumbens (Hablitzieae): scalariform intervessel pits. Scale bars = 50 m in A; 100 m in B; 20 m in C, D.

maritima have pit sizes between 4 and 7 m. Only in the vessels of roots of Polycnemum fontanesii were a few pits larger than 4 m. Anabasis brevifolia, Halopeplis perfoliata, Iljinia regelii, Microgynoecium tibeticum and Suckleya suckleanum have minute pits (<< 4 m). Helical thickenings on vessel walls Vessels with helical thickenings were found only in Arthrocnemum fruticosum (Salicornieae) from the Mediterranean, and in Maireana pyramidata and Roycea divaricata (Sclerolaeneae) from Western and Southern Australia.

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Fibre wall thickness In the stem and basal branch wood of most Chenopodiaceae fibres dominate. However, in taxa with a succulent hypocotyl and roots (Beta, Patellifolia) or a pleiocormus (Hablitzia tamnoides, Chenopodium bonus-henricus) axial parenchyma is more abundant. Fibre wall thickness is variable. In the tribes Atripliceae and Chenopodieae fibres are mostly thin- to thick-walled. The tribes Halopeplideae and Sclerolaeneae have mostly thick- to very thick-walled fibres. Very thick-walled fibres are prominent in 66% of the tribe Salsoleae; e.g. Anabasis brevifolium, Haloxylon ammodendron, Nanophyton erinaceum of high arid Mongolian steppes and deserts, Hammada scoparia in the Sahara, and Lagenantha species from East Africa. In Salsoleae, thin-walled fibres were never observed. Annuals and sub-shrubs clearly differ in fibre wall thickness. The proportions of very thick-walled or thick- to very thick-walled fibres are very high in sub-shrubs. In annuals only 6.4% of the species have very thick-walled fibres, and these are from semi-deserts, deserts or saline habitats. Annual ruderal plants are fast-growing and have mostly thin- to thick- or thick-walled fibres, but overall, thin-walled fibres are very rare throughout the family. Fibre length We measured the fibres in a small selection of species in different life forms. In the basal stem of annuals the mean fibre lengths were 251 m (Chenopodium rubrum), 271 m (Atriplex sagittata), 246 m (Atriplex prostrata) and 317 m (Bassia scoparia). In the stem of the small tree Haloxylon ammodendron the fibres were on average 286 m long. In the stems of hemiphanerophytes or nanophanerophytes (Krascheninnikovia ceratoides, Anabasis brevifolia, Salsola vermiculata, Maireana pyramidata, Atriplex lindleyi) the fibres were 193357 m long. In comparison to dicotyledons as a whole the Chenopodiaceae have short fibres. Axial parenchyma Paratracheal parenchyma In most Chenopodiaceae paratracheal axial parenchyma is present, even if scanty. It was absent in a few species, e.g. Kalidium gracile and Suckleya suckleyanum. Conjunctive axial parenchyma (Fig. 2) In most species the form of conjunctive axial parenchyma is consistent within stems, for instance in annual Atriplex or Chenopodium species and in the sub-shrub Krascheninnikovia ceratoides (Fig. 2 A, B): the conjunctive parenchyma is mostly band-like in the basal stem and mostly cap- or arc-like in the apical part of stem and in branches. Only in Salicornieae we found cap-like or sometimes arc-like, but never band-like unlignified conjunctive parenchyma in the hypocotyl of annuals, for instance in Salicornia europaea, S. fragilis, S. ramosissima. In this tribe there is less variation in conjunctive axial parenchyma within individual plants. Irregular net-like parenchyma If both unlignified radial parenchyma or rays and unlignified banded conjuctive parenchyma are present, then the parenchyma appears

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as a network, as in the annual Atriplex species A. sagittata, A. prostata (Fig. 2 F) and, A. hortensis, Bassia species (Camphorosmeae), Betoideae and Chenopodium species, such as C. bonus-henricus, C. hybridum, C. urbicum, and C. glaucum. Xylem rays and radial parenchyma (Fig. 2 DF ) Medullary rays extending from the pith to the primary cortex hardly exist in Chenopodiaceae stems because continuity to the primary cortex may be interrupted by the first master cambium (sensu Carlquist 2007a) and later successive cambia. In cross sections of seedlings a meristematic zone around the central cylinder is always present. However, c. 64% of the samples investigated (Table 1) have distinct secondary rays (wood rays or xylem rays), especially annuals in the tribes Atripliceae, Camphorosmeae, Chenopodieae, Beteae, Hablitzieae and Salsoleae. Rays in typical dicotyledon wood develop from one single cambium. In Chenopodiaceae rays can arise from each successive cambium. The preceding cambium stops dividing and the xylem rays are discontinuous over the whole cross section. This is the case in roots or basal stems with banded conjunctive tissue, including the secondary phloem strands and abaxial to the vessel-bearing secondary xylem. The respective rays are frequently restricted to this part of the secondary tissue that has arisen from the respective successive cambium (Fig. 2 E, F ). In shoots or branches without bands, where the diffuse vascular bundles possess only cap-like or arc-like tangential parenchyma connected with secondary phloem and a cambium, the rays can be longer. If the rays extend over two or more bands of secondary xylem and conjunctive parenchyma, they may vary in width. In these cases each successive cambium is involved in the development of the rays. In species where a successive cambium is active for longer than one growth period (especially in Camphorosmeae, Sclerolaeneae) and the first cambium exists temporarily as a single cambium, the radial parenchyma is more clearly ray-like (Roycea divaricata, Bassia prostrata, B. sedoides). In other Bassia and Camphorosma species, Chenoleoides tomentosa, Oreobliton thesioides, Maireana pyramidatum, Enchylaena tomentosa and Sclerolaena glabra, rays are present. Rays also exist in stems and roots without successive cambia, for instance in Polycnemum majus, P. arvensis (Fig. 3 E) and in the stem of Polycnemum fontanesii (Fig. 3 C). The rays in Chenopodiaceae consist mostly of upright cells. Their shape (oval, round, rectangular) and ray width vary between genera and species. In Atriplex hortensis the rays are more than 5-seriate and the cells are upright, rectangular and rarely square. In Polycnemum fontanesii the rays are uniseriate and the ray cells are upright, very narrow and oval. Camphorosma monspeliaca has oval, round or rectangular ray cells and the rays are mostly 4- to 5-seriate. Radial parenchyma In most Chenopodiaceae clearly delimited rays are absent, but radial strips of axial parenchyma (referred to as radial parenchyma) traverse the secondary xylem. The radial strips vary from narrow (13-seriate) to broad (>3-seriate) and may be unlignified or lignified. In our samples radial parenchyma was rarely absent: especially in the tribe Salsoleae (e.g. Iljinia regelii, Lagenantha species, Nanophyton erinaceum, Traganum nudatum). In some Salicornieae, for instance in Allenrolfea

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occidentalis and Halosarcia species, there is no radial parenchyma. In 15.7% of our samples radial axial parenchyma was totally absent, especially in sub-shrubs, rare in annuals or perennial herbs. Sub-shrubs in deserts and subtropical halophytes have the highest proportion of species without radial parenchyma. Mineral inclusions In Chenopodiaceae the accumulation of oxalic acid (C2H2O4) and its importance in the neutralisation of salt cations (K+, Ca2+, Mg2+) is well known (Hegnauer 1964). In saline habitats, especially inland, the salt water with NaCl, MgCl2, KCl, MgSO4 is frequently mixed with Ca(HCO3)2 from other inflows and additional carbonates develop. Calcium oxalate crystals are prominent in the Chenopodiaceae. Species with many mineral inclusions are Bassia sedoides (Camphorosmeae), and some species of the tribe Salsoleae (e.g. Halimocnemis mollissima, Nanophytum erinaceum, Salsola genistoides, Sevada schimperi) and Patellifolia procumbens (Hablitzieae, Betoideae). Threlkeldia diffusa (Sclerolaeneae) from the Australian coast and inland salt lakes is conspicuous for its numerous and large crystals in parenchyma cells and fibres. In Microcnemum coralloides (Salicornieae) different forms of crystals (round and triangular) were found. Druses are more frequent than prismatic crystals. Mineral inclusions in vessels were common in Alexandra lehmannii, Halanthium purpureum (Suaedeae), Beta vulgaris, Patellifolia procumbens (Betoideae), Bassia sedoides (Camphorosmeae) and Nucularia perrini (Salsoleae). In the tribe Salicornieae with true eu-halophytes the frequency of mineral inclusions in the stem was usually moderate. No mineral inclusions were found in a fifth of our samples. Sclerified pith Nucularia perinii (Salsoleae) from northwest Africa has strongly sclerified cell walls in the pith (Fig. 6 A). Aerenchyma Tegicornia uniflora (Salicornieae) stems from saline habitats in Western Australia have aerenchyma in the primary cortex (Fig. 6 B).
DISCUSSION

Successive cambia (Anomalous thickening) Successive cambia are widespread in the Caryophyllales (Carlquist 2001). The interpretation of anomalous secondary thickening is summarised in Fahn & Zimmermann (1982), Heklau (1992) and Khn et al. (1993). Timonin (1987b) proposed the theory of aromorphosis (Greek: change of form) for the origin of successive cambia. This was developed in zoology to describe a change of organisation and function in animals with a common importance (Sewertzoff 1931). Carlquist (1988, 2001) used the term cambial variant for all types of anomalous secondary growth, including the development of successive cambia. The radiation of the Chenopodiaceae probably was associated with the development of arid regions in the world (Khn 1993). In the late Tertiary a large arid zone

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existed from Central Asia and East China to North Africa and Spain. According to Takhtajan (1973) the region of Central Asia to northwestern China has significance for the evolution of many xeromorphic angiosperm groups. These regions are also a centre of biodiversity of Chenopodiaceae. Fossil records are scarce. The oldest fossil records for Chenopodiaceae are pollen grains recovered from Maastrichtian sediments (Late Cretaceous) of Canada (Srivastava 1969). There appear to be no fossil records for wood (Gregory et al. 2009; InsideWood 2004 onwards). Vessel diameter and vessel element length In angiosperms vessels vary considerably in diameter, ranging from (20)40300 (700) m (Lsch 2003). Nearly 41% of dicotyledons have vessel diameters between 40 and 79 m (Metcalfe & Chalk 1985; Wheeler et al. 2007), and the vessels of Chenopodiaceae are mostly at the lower end of this range. Fahn et al. (1986) described the wood anatomy of 21 species (mostly sub-shrubs) of Chenopodiaceae and the tangential vessel diameter of their species was higher than in the branches of our samples. They recorded tangential vessel diameters (including the walls) up to 100 m in stems of Atriplex halimus and 90 m in Haloxylon persicum. Their results extend the range of maximum tangential vessel diameter in Chenopodiaceae, and in most cases, our measurements of the same species were in their reported range. It should be noted, however, that Fahn et al. (1986) measured vessel diameter including the vessel walls, while we measured vessel lumen diameter in accordance with recommendations of the IAWA Committee (1989). In Krascheninnikovia ceratoides (a half-shrub of steppe, prairie and semi-deserts widely distributed in the holarctic, covering a large climatic range) Heklau and Von Wehrden (2011) found that the plants from temperate sites with a semi-humid climate have the widest vessels in basal branches and flowering shoots. In contrast, the vessels of plants from an arid temperate climate in Central Asia are narrowest. As a result of vessel diameters being different in the axial system (stem, branch and shoot), ecological investigations need to compare material from the same organ and cambial age. In Krascheninnikovia ceratoides, the vessel diameter in the stem was nearly 1015 m wider than in the shoots, and 510 m wider than in basal branches of the same sample (Heklau & Von Wehrden 2011). The range of mean vessel diameters in Chenopodiaceae (966 m) is similar in the close relatives of Amaranthaceae. In Amaranthaceae from the tropics and subtropical deserts, Carlquist (2003) recorded a range of 1552 m. Rajput (2002) found that short-lived tropical Amaranthaceae had vessel diameters of 4969 m. Baas et al. (1983), Fahn et al. (1986), Baas & Schweingruber (1987) and Schweingruber (1990) emphasised the occurrence of two vessel size classes in all woody Chenopodiaceae from the Middle East and Europe studied by them: in addition to the typical and distinct vessels, they reported narrow vessels, intergrading with imperforate vascular tracheids. We also noted the occurrence of two vessel size classes in most of our material, but when the very narrow vessels (in lumen diameter often <10/m, also in species where the clearly recognisable narrow vessels in transverse section had diameters >>10/m, cf. Table 1) were not easily recognisable as such in transverse sec-

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tion, we did not include them in our measurements of vessel lumen diameter, assuming that their contribution to hydraulic conductance must be very small indeed. However, the role of these very narrow, cavitation resistant vessels and vascular tracheids may be important to survive long and extreme droughts. The vessel elements in Chenopodiaceae were similar in length to those recorded by Fahn et al. (1986). However, in the shrub of Arthrocnemum perenne their maximum vessel element length was 270 m, whereas our sample was only 160 m. Mean fibre length The Chenopodiaceae has some of the shortest fibres in the dicotyledons. Metcalfe and Chalk (1950) gave a range of 200400 m in Chenopodiaceae, in good overall agreement with our range of 190360 m for average fibre lengths. In dicotyledons as a whole 44% of the species have a range of means of 9001499 m and only 0.5% up to 299 m (Metcalfe & Chalk 1950). According to Fahn et al. (1986) the mean fibre length of sub-shrubs reaches 400 m in Anabasis articulata. In a few species the maximum fibre length far exceeds this: 600 m in Haloxylon persicum, 540 m in Anabasis articulata and 580 m in Noaea mucronata. The relatively short fibres must be linked to the low stature of most Chenopodiaceae; sub-shrubs ranging from < 0.5 m to 2 m. The ecological trend for fibres is mostly weak. Heklau and Von Wehrden (2011) showed that the length of the fibres in the always low main axis of Krascheninnikovia ceratoides (Chenopodioideae, Axyridineae) is constant and independent of macroclimate. In other Caryophyllales the fibre lengths can be clearly different. In Phytolaccaceae the fibres reach lengths of 600900 m and in the Cactaceae 400900 m (Metcalfe & Chalk 1950). In Amaranthaceae the range of fibre lengths is larger, from 3471528 m (Carlquist 2003). For the common tropical weed Trianthema monogyna (Aizoaceae) Rao and Rajput (1998) noted a fibre length of 380460 m. Rays in Chenopodiaceae In plant families with successive cambia conceptual problems exist with rays. In traditional anatomy two terms exist: medullary rays with as synonyms pith rays or early primary rays (Braun 1970), and xylem rays or early secondary rays, sensu Braun (1970). In normal dicotyledonous wood both types of rays are common, but in mature wood medullary rays cannot be traced or are fully replaced by secondary rays, so that the term medullary ray has hardly any or no significance in the wood anatomy of trees. In species with successive cambia the situation is different (Carlquist 2007). Medullary rays do not exist in Chenopodiaceae, only xylem rays or secondary rays, largely composed of upright cells. These true rays do, however, intergrade with the rayless condition, where rays may be replaced by radial strips of axial parenchyma (loosely referred to as radial parenchyma) occurring in many Chenopodiaceae. The entire range of ray types and rayless conditions could be interpreted as variations on the paedomorphic ray types recognised by Carlquist (2001) and others, implying that

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secondary woodiness that is the evolution of woodiness from herbaceous ancestors in some chiefly herbaceous clades of the Chenopodiaceae might have occurred. However, a further analysis of our data in relation to secondary woodiness is beyond the scope of this paper. In Suaeda monoica, a large shrub up to 4 m high in the eastern Mediterranean, LevYadun and Aloni (1991) described the vascular ray system as a flexible radial system. Initially the wood is rayless, but in mature secondary xylem ray initiation begins. In this case the description of wood would also depend on the developmental stage of wood: immature wood without rays, mature wood with rays. Ecological trends in the wood anatomy of Chenopodiaceae The narrow vessels and short vessel elements are strongly associated with extreme habitats. Fahn et al. (1986) found the narrowest vessels in species on stony soils and in xerohalophytic shrubs. Species from the driest habitats also tend to have the shortest vessel elements (Fahn et al. 1986; Carlquist 1988; our study). Thick- to very thick-walled fibres are very common in trees and shrubs in both the desert flora and the Mediterranean flora (Fahn et al. 1986). This trait is also very common in the Chenopodiaceae in sub-shrubs from Australia, the Asian and North American deserts and semi-deserts, and in the Mediterranean.
CONCLUSION

The wood anatomy of the entire family Chenopodiaceae shows consistent adaptations to extreme arid temperate and arid subtropical environments. The narrow vessels, short vessel elements, minute intervessel pits, and the short fibres frequently with thick walls in most Chenopodiaceae reflect general ecological trends in woody plants (xerophytes, halophytes) from extreme habitats. The only anatomical feature providing a strong phylogenetic and systematic signal is anomalous secondary thickening with numerous successive cambia, common throughout the Caryophyllales. This feature is expressed to different degrees in the eight sub-families of Chenopodiaceae: with many successive cambia in Chenopodioideae, Salicornioideae, Salsoloideae, Suaedoideae; fewer in Betoideae, Corispermoidae and Camphorosmoideae and even fewer in Polycnemoideae. The present study confirms and enlarges upon observations described in the literature, e.g. successive cambia, narrow vessels (<100 m), short vessel elements (< 270 m), mostly minute intervessel pits (< 4 m) and short fibres (< 470 m). Contrary to the accepted view, successive cambia were found in roots and stem borne roots in the Polycnemoideae and help support its inclusion in Amaranthaceae s.l.
ACKNOWLEDGEMENTS We thank U. Braun (Halle), D. Goyder (Kew), H.J. Zndorf (Jena), for giving access to herbarium material. We are grateful to G. Kadereit for molecular-systematic comments and H. Wilkinson (Kew) for technical advice in the laboratory.

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