IAWA J 33 (2) 205-232

IAWA Journal, Vol. 33 (2), 2012: 205–232

WOOD ANATOMY OF CHENOPODIACEAE (AMARANTHACEAE s. l.)

Heike Heklau1, Peter Gasson2, Fritz Schweingruber3 and Pieter Baas4

SUMMARY

The wood anatomy of the Chenopodiaceae is distinctive and fairly uni-form. The secondary xylem is characterised by relatively narrow vessels (<100 µm) with mostly minute pits (<4 µm), and extremely narrow ves-sels (<10 µm intergrading with vascular tracheids in addition to “normal” vessels), short vessel elements (<270 µm), successive cambia, included phloem, thick-walled or very thick-walled fibres, which are short (<470 µm), and abundant calcium oxalate crystals. Rays are mainly observed in the tribes Atripliceae, Beteae, Camphorosmeae, Chenopodieae, Hab-litzieae and Salsoleae, while many Chenopodiaceae are rayless. The Chenopodiaceae differ from the more tropical and subtropical Amaran-thaceae 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, sub-shrubs, 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; Kühn 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: [email protected]].

2) Jodrell Laboratory, Royal Botanic Gardens Kew, TW9 3DS, Richmond, Surrey, United King-dom.

3) Swiss Federal Research Institute for Forest, Snow and Landscape, Zürcherstrasse 111, 8903 Birmensdorf, Switzerland.

4) NCB Naturalis - Nationaal Herbarium Nederland, P.O. Box 9514, 2300 RA Leiden, The Nether-lands.

IAWA Journal, Vol. 33 (2), 2012206

(Kühn et al. 1993). Amaranthaceae s.l., including Chenopodiaceae, number c. 2000 spe-cies (Mabberley 2008). Molecular studies by Cuénoud 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 cam-bia 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 anat-omy 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 re-corded 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 Cheno- podiaceae from the Middle East, and Schweingruber (1990) and Baas & Schwein-gruber (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; Il’in 1950; Butnik 1966, 1983; Vasilevskaja 1972; Novruzova & Chapari 1974; Lotova & Timonin 1985; Timonin 1987a & b, 1988) some of which are not included in Gregory’s 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 (Kühn et al. 1993) was investigated (Table 1). These samples represent different life forms and plant sizes (after Ellenberg & Mueller-Dombois 1967): phanerophytes: microphanerophytes (2–5 m), nanophanero-phytes (< 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 nanophan-erophytes 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

207Heklau et al. — Wood anatomy of Chenopodiaceae

(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 (humid-temperate 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® (dis- tilled 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 1–2 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 con-junctive 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


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. 2E, F) to clustered in bundles adaxial to cap-like parenchyma and phloem strands (Fig. 2A, C, D). Intermediates occur, especially where the conjunctive parenchyma is arc-like (Fig. 2B). Xylem rays may be absent (Fig. 2A, B) or present as 1- to 3-seriate rays (Fig. 2D, E, 3B, C, E). Less well-defined radial strips or wedges of axial parenchyma may also occur (Fig. 2E, 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 /µm).

Classification system adopted To put the anatomical characters in systematic context we followed recent phylo-genetic insights and recognised eight subfamilies (Betoideae, Camphorosmoideae, Chenopodioideae, Corispermoideae, Polycnemoideae, Salicornioideae, Salsoloideae and Suaedoideae) and the tribal subdivision of the Chenopodiaceae (in part after Kühn 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 (Cuénoud et al. 2002).

Subfamilies Tribes in subfamilies Chenopodioideae Chenopodieae, Atripliceae, Axyrideae, Dysphanieae Corispermoideae Corispermeae Camphorosmoideae Camphorosmeae (incl. Sclerolaeneae) Betoideae Beteae, Hablitzieae Salicornioideae Halopeplideae, Salicornieae Salsoloideae Salsoleae, Caroxyloneae Suaedoideae Suaedeae, Bienertieae Polycnemoideae 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 Cheno-podioideae plus Corispermoideae.


Chenopodioideae plus Corispermoideae are sisters to Betoideae as sister to Salsoloi-deae 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). Cuénod et al. (2002) differentiates between the core Caryophyllales (Caryo-phyllaceae, Amaranthaceae s.str., Chenopodiaceae, Molluginaceae, Aizoaceae, Phyto-laccaceae, Cactaceae, Portulacaceae, Didiereaceae, Nyctaginaceae, Basellaceae) and non-core Caryophyllales (Polygonaceae, Plumbaginaceae, Frankeniaceae, Droseraceae, Nepenthaceae, Tamaricaceae, Ancistrocladaceae, Dioncophyllaceae). The Achatocar-paceae, Caryophyllaceae, Amaranthaceae s.str., Chenopodiaceae plus Rhabdodendron and Simmondsia belong to the ‘Lower core Caryophyllales’ and the other core families to the more derived ‘Higher core Caryophyllales’.

Figure 1. Simplified phylogenetic tree of Chenopodiaceae, modified from the maximum likeli-hood 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.

(text continued on page 216)

Amaranthaceae s.str.(Up to 3–5, Rajput 2002)

Polycnemoideae(Mainly in roots

Corispermoideae(Up to 6)

Chenopodioideae(Up to >20)

Salicornioideae (Up to 10–16)

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 4–6, Krumbiegel 1998)

Achatocarpaceae(Without anomalous secondary thickening)

IAWA Journal, Vol. 33 (2), 2012210Ta

ble

1. C

heno

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d, a

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211Heklau et al. — Wood anatomy of Chenopodiaceae (A

trip

lex)

sagi

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sem

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2

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H

G

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any

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15

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4 B

vu

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bran

ch

H

Portu

gal

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c.

3.5

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nert

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pter

a st

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T Ir

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step

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c. 3

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bran

ch

T K

azac

hsta

n st

eppe

hal

ophy

tes

29–3

8 34

35

–100

2

.8

B C

amph

oros

ma

annu

a hy

poco

tyl

T H

unga

ry

step

pe h

alop

hyte

s 14

–19

17

80–1

50

c. 3

A

, B

annu

a st

em

T H

unga

ry

step

pe h

alop

hyte

s 15

–22

18

50–1

00

c. 3

A

, B

mon

spel

iaca

br

anch

S

Gre

at B

ritai

n su

btro

pica

l hal

ophy

tes

19–4

1 30

?

< 4

B, C

m

onsp

elia

ca

bran

ch

F/S

Fran

ce

subt

ropi

cal h

alop

hyte

s 14

–18

16

50–1

00

2–2.

8 B

, C

soon

gori

cum

br

anch

T

Isra

el

step

pe h

alop

hyte

s 16

–22

19

100–

200

?

B C

erat

ocar

pus a

rena

rius

st

em

T K

azac

hsta

n st

eppe

19

–24

21

? ?

B

aren

ariu

s st

em

T R

ussi

a st

eppe

10

–13

12

? ?

N C

heno

leoi

des t

omen

tosa

br

anch

S

Spai

n lit

tora

l 13

–17

15

90–1

50

c. 2

.5

B

tom

ento

sa

bran

ch

S Sp

ain,

Can

arie

s lit

tora

l 16

–18

17

50–1

00

< 4

B C

heno

podi

um a

lbum

hy

poco

tyl

T Ita

ly

rude

ral

29–3

5 32

50

–150

<

4

B, C

am

bros

ioid

es

stem

T

Switz

erla

nd

gard

en c

ultu

re

37–5

7 47

50

–100

<

4

B

ambr

osio

ides

st

em

T Po

rtuga

l ga

rden

cul

ture

31

–43

37

100–

150

3.

4 B

bo

nus-

henr

icus

rh

izom

e H

Sw

itzer

land

ru

dera

l 36

–40

38

80–1

20

< 4

B

bo

nus-

henr

icus

rh

izom

e H

Ita

ly

rude

ral

21–3

1 26

?

< 4

B

botr

ys

stem

T

No

info

rmat

ion

rude

ral

27–3

7 32

50

–120

<

4

B*

ca

pita

tum

st

em

T Fr

ance

ru

dera

l 19

–24

22

50–1

50

c. 2

.5

B

ficifo

lium

st

em

T Po

rtuga

l ru

dera

l 35

–43

39

80–1

50

1.5–

2 B

(con

tinue

d)

IAWA Journal, Vol. 33 (2), 2012212 S

peci

es

Plan

t par

t Li

fe fo

rm

Orig

in

Ecol

ogic

al c

ateg

ory

1 2

3 4

5

(Che

nopo

dium

) fol

iosu

m

stem

T

Switz

erla

nd

rude

ral

27–3

6 32

50

–100

<

4 D

gi

gant

eum

st

em

T Sw

itzer

land

ga

rden

cul

ture

40

–49

45

50–1

10

c. 3

.5

B

glau

cum

hy

poco

tyl

T G

erm

any

rude

ral

20–2

5 22

50

–100

c.

3.5

B

gl

aucu

m

stem

T

Aus

tria

rude

ral

25–3

2 29

<1

00

c. 3

B

hy

brid

um

stem

T

Aus

tria

rude

ral

22–3

5 30

50

–150

3–

3.5

B

mur

ale

stem

T

Om

an

rude

ral

31–4

2 37

50

–200

≤

4 N

op

ulifo

lium

st

em

T Po

rtuga

l ru

dera

l 25

–32

29

50–1

00

2.8–

3 B

po

lysp

erm

um

stem

T

Switz

erla

nd

rude

ral

25–3

3 29

30

–130

c.

2.7

B

qu

inoa

hy

poco

tyl

T Sw

itzer

land

ga

rden

cul

ture

32

–39

36

100–

150

c.

3.3

B

ru

brum

ep

icot

yl

T G

erm

any

rude

ral

21–2

7 24

50

–100

c.

3

B, C

st

rict

um

stem

T

Switz

erla

nd

rude

ral

39–4

8 44

50

–150

≤

4 D

ur

bicu

m

stem

T

Ger

man

y ru

dera

l 41

–52

47

70–1

20

c. 4

B

ur

bicu

m

stem

T

Aus

tria

rude

ral

37–5

1 44

30

–100

c.

3

B

urbi

cum

st

em

T Sp

ain

rude

ral

42–5

7 50

50

–150

<

4 B

ur

bicu

m

stem

T

Switz

erla

nd

rude

ral

14–1

9 17

50

–100

c.

3.5

B

vu

lvar

ia

stem

T

Liby

a

rude

ral

44–5

4 49

<1

00

c. 3

B

Cor

ispe

rmum

pat

ellif

orm

e br

anch

T

Wes

t Mon

golia

st

eppe

31

–52

41

50–1

20

c. 2

A

, B C

ornu

laca

auc

heri

br

anch

T

Iraq

se

mi-d

eser

t 25

–31

28

50–1

50

c. 2

.4

D

mon

acan

tha

bran

ch

F/S

Liby

a de

sert

34–3

8 36

50

–110

<

4

A, B

Cyc

lolo

ma

atri

plic

ifoliu

m

stem

T

USA

pr

airie

25

–32

28

50–1

50

c. 4

B

at

ripl

icifo

lium

st

em

T G

erm

any

gard

en c

ultu

re

23–3

4 29

50

–100

c.

3

B

atri

plic

ifoliu

m

stem

T

Ger

man

y ga

rden

cul

ture

33

–42

37

100–

250

c. 3

B

at

ripl

icifo

lium

st

em

T G

erm

any

gard

en c

ultu

re

21–3

0 25

10

0–25

0 c.

3

B

atri

plic

ifoliu

m

stem

T

Italy

ru

dera

l 25

–31

28

100–

200

c.

3.6

B

Dis

soca

rpus

par

adox

us

bran

ch

F/S

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

land

20

–27

23

50–1

30

c. 3

A

, B E

inad

ia n

utan

s br

anch

C

Sp

ain

rude

ral

46–6

0 53

?

? D

Enc

hyla

ena

tom

ento

sa

bran

ch

F So

uth

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

land

20

–25

22

60–1

00

c. 2

A

, B E

rem

opha

ea a

ggre

gata

br

anch

S

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

land

20

–26

23

50–1

20

< 4

A, B

Exo

mis

axy

rioi

des

bran

ch

F So

uth

Afr

ica

litto

ral

26–3

2 29

50

–120

c.

3

B*

Fad

enia

zygo

phyl

loid

es

bran

ch

S So

mal

ia

tropi

cal/s

ubtro

pica

l hal

ophy

tes

20–2

7 23

50

–90

2.6–

2.9

D G

aman

thus

gam

ocar

pus

stem

T

Turk

men

ista

n st

eppe

15

–19

17

50–1

50

c. 3

D

Girg

enso

hnia

opp

ositi

flora

st

em

T So

uthw

est P

ersi

a se

mi-d

eser

t 23

–27

25

50–1

50

c. 3

B

Gra

yia

spin

osa

bran

ch

F/S

USA

pr

airie

27

–40

33

50–1

20

≤ 4

N.A

. H

ablit

zia

tam

noid

es

root

H

G

erm

any

gard

en c

ultu

re

28–3

2 30

10

0–15

0

< 4

B

tam

noid

es

annu

al sh

oots

H

G

erm

any

gard

en c

ultu

re

34–5

0 42

10

0–15

0 <

4 N

.A.

Hal

anth

ium

pur

pure

um

stem

(lia

na)

T

Sout

hwes

t Per

sia

dese

rt 12

–14

13

100–

150

c.

2.5

B

Hal

imio

ne p

edun

cula

ta

hypo

coty

l T

Ger

man

y hu

mid

tem

pera

te h

alop

hyte

s 17

–26

21

c. 1

00

c. 3

D

pe

dunc

ulat

a st

em

T G

erm

any

hum

id te

mpe

rate

hal

ophy

tes

17–2

8 22

50

–120

c.

3.5

D

pe

dunc

ulat

a ep

icot

yl

T G

erm

any

hum

id te

mpe

rate

hal

ophy

tes

18–2

3 21

10

0–20

0 3.

5–4.

5 D

po

rtul

acoi

des

stem

C

C

ypru

s co

ast h

alop

hyte

s 30

–37

33

50–1

50

< 4

D

213Heklau et al. — Wood anatomy of Chenopodiaceae (H

alim

ione

) por

tula

coid

es

bran

ch

C

Sout

heas

t Spa

in

coas

t hal

ophy

tes

29–3

4 32

20

–100

c.

2

D

port

ulac

oide

s br

anch

C

C

ypru

s co

ast h

alop

hyte

s 26

–32

29

50–1

00

c. 2

.4

D

verr

ucife

ra

bran

ch

F/S

Iran

st

eppe

hal

ophy

tes

18–2

2 20

c.

50

c.

3

D

verr

ucife

ra

bran

ch

F/S

Pers

ia

step

pe h

alop

hyte

s 12

–18

15

50–1

00

c. 2

.5

D

verr

ucife

ra

bran

ch

F/S

Pers

ia

step

pe h

alop

hyte

s 15

–20

18

50–1

00

c. 2

D

Hal

imoc

nem

is m

ollis

sim

a st

em

T Tu

rkm

enis

tan

dese

rt 19

–24

21

80–1

20

c. 3

D

Hal

ocha

ris s

ulph

ura

stem

T

Iran

se

mi–

dese

rt 16

–21

19

90–1

60

c. 3

A

, B H

aloc

nem

um st

robi

lace

um

stem

, bas

al

F Tu

rkey

co

ast h

alop

hyte

s 18

–24

21

80–1

50

c. 3

D

Hal

oget

on a

lope

curo

ides

st

em

T A

lger

ia

dese

rt 12

–17

14

<100

c.

3

N H

alop

eplis

am

plex

icau

lis

stem

T

Italy

su

btro

pica

l hal

ophy

tes

15–1

8 16

50

–100

c.

2.5

D

perf

olia

ta

stem

T

Om

an

coas

t hal

ophy

tes

16–2

0 18

<1

50

<< 4

N

Hal

osar

cia

auri

cula

ta

bran

ch

F/S

Aus

tralia

su

btro

pica

l hal

ophy

tes

10–1

4 12

90

–120

2.

5–3.

4 N

bu

lbos

a br

anch

F/

S A

ustra

lia

tropi

cal/s

ubtro

pica

l shr

ub-la

nd

13–1

6 15

40

–150

c.

1.7

N

ca

lypt

rata

br

anch

F

Aus

tralia

su

btro

pica

l hal

ophy

tes

12–1

7 14

50

–130

2.

5–2.

9 N

ha

locn

emoi

des s

ubsp

. cau

data

br

anch

S

Aus

tralia

su

btro

pica

l hal

ophy

tes

11–1

4 12

40

–100

c.

2.5

D

Hal

osta

chys

cas

pica

br

anch

? F/

M

Cau

casu

s se

mi-d

eser

t 34

–50

42

50–2

00

< 4

D

casp

ica

bran

ch

F/M

Tu

rkm

enis

tan

sem

i-des

ert

33–5

0 42

80

–160

c.

2

D

casp

ica

bran

ch

F G

eorg

ia

sem

i-des

ert

10–1

9 15

20

–80

3–

3.5

D H

alot

ham

nus g

lauc

us

bran

ch

F/S

Iran

se

mi-d

eser

t 18

–21

20

50–1

00

2–2.

5 B

su

baph

yllu

s br

anch

F

Turk

men

ista

n se

mi-d

eser

t 20

–26

23

50–1

50

c. 2

.2

N H

alot

is p

ilosa

br

anch

T

Turk

men

ista

n se

mi-d

eser

t 13

.–17

15

?

? B

Hal

oxyl

on a

mm

oden

dron

st

em

F/M

M

ongo

lia

dese

rt 61

–71

66

100

< 4

?

amm

oden

dron

br

anch

F/

M

Iran

de

sert

22–2

7 25

50

–90

c.

3.2

N

gr

iffith

ii br

anch

F/

S A

fgha

nist

an

dese

rt 21

–28

25

80–1

30

c. 2

.5

B

pers

icum

br

anch

F/

M

Iran

de

sert

36–4

7 42

?

? A

*

sa

licor

nicu

m

bran

ch

S O

man

se

mi-d

eser

t 16

–20

18

<150

<

4 A

, B

tam

aris

cifo

lium

br

anch

F/

S A

lger

ia

dese

rt 19

–25

22

50–8

0 c.

2.5

N

Ham

mad

a ar

ticul

ata

bran

ch

F Sp

ain

dese

rt 15

–18

17

50–1

00

c. 3

N

sc

opar

ia

bran

ch

F M

oroc

co

dese

rt 19

–28

23

50–1

00

< 4

N

scop

aria

br

anch

F

Alg

eria

de

sert

24–3

3 29

50

–<10

0 <

4 N

Hor

anin

ovia

ano

mal

a st

em

T ‘T

rans

casp

ica’

se

mi-d

eser

t 21

–25

23

50–1

50

c. 3

B

Iljin

ia re

gelii

br

anch

S

Tja

n Sh

an

sem

i-des

ert

12–1

5 13

50

–100

c.

1.8

N

Kal

idiu

m a

rabi

cum

br

anch

F

Arm

enia

st

eppe

hal

ophy

tes

21–2

7 24

80

–150

?

?

folia

tum

br

anch

F/

S M

ongo

lia

step

pe h

alop

hyte

s 20

–29

25

<50–

100

<

4 N

fo

liatu

m

bran

ch

F R

ussi

a st

eppe

hal

ophy

tes

23–2

8 25

50

–100

c.

3.5

?

gr

acile

br

anch

S

Sout

h M

ongo

lia

dese

rt ha

loph

yte

21–2

8 25

>5

0–12

0

c. 2

N

Kir

ilow

ia e

rian

tha

root

, hyp

ocot

yl

T K

azac

hsta

n se

mi-d

eser

t 16

–22

19

50–1

40

2.6–

2.8

B K

rasc

heni

nnik

ovia

cer

atoi

des

su

bsp.

cer

atoi

des

hypo

coty

l F

Mon

golia

st

eppe

27

–38

32

60–1

00

< 4

N

subs

p. c

erat

oide

s hy

poco

tyl

F Sp

ain

step

pe

26–3

5 31

60

–100

<

4 N

su

bsp.

cer

atoi

des

hypo

coty

l F

Rus

sia

step

pe

22–2

9 25

60

–100

<

4 N

(con

tinue

d)

IAWA Journal, Vol. 33 (2), 2012214 S

peci

es

Plan

t par

t Li

fe fo

rm

Orig

in

Ecol

ogic

al c

ateg

ory

1 2

3 4

5 L

agen

anth

a cy

clop

tera

br

anch

S

Som

alia

tro

pica

l/sub

tropi

cal s

hrub

-land

14

–19

17

40–8

0

2.0–

2.9

N

gille

ttii

bran

ch

S K

enya

tro

pica

l/sub

tropi

cal s

hrub

-land

20

–26

23

50–1

20

c. 2

N

Mai

rean

a py

ram

idat

a br

anch

F

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

-land

19

–27

23

50–1

30

c. 3

B

se

difo

lia

bran

ch

F A

ustra

lia

tropi

cal/s

ubtro

pica

l shr

ub-la

nd

13–1

9 16

50

–100

c.

2

A, B

Mic

rogy

noec

ium

tibe

ticum

hy

poco

tyl

T C

hina

ru

dera

l 10

–20.

15

40

–80

1.

8–2.

2 A

, B M

icro

nem

um c

oral

loid

es

stem

T

Spai

n su

btro

pica

l hal

ophy

tes

10–1

4 12

c.

50

c.

2

B M

icro

pepl

is a

rach

noid

ea

stem

T

East

Mon

golia

st

eppe

20

–28

24

50–1

50

c. 2

B

Mon

olep

is a

siat

ica

stem

T

Ger

man

y ru

dera

l 17

–22

19

50–1

00

< 3

A, B

nu

ttalli

ana

stem

T

Ger

man

y ga

rden

cul

ture

18

–29

23

50–1

50

c. 3

B

nu

ttalli

ana

hypo

coty

l T

USA

pr

airie

26

–38

32

50–1

00

c. 3

B

Nan

ophy

ton

erin

aceu

m

hypo

coty

l S

Mon

golia

st

eppe

16

–21

18

<50

<

4 N

er

inac

eum

un

know

n S

Kirg

izia

st

eppe

15

–18

17

50–1

00

2.7

N

Neo

bass

ia p

roce

riflo

ra

bran

ch

S A

ustra

lia

tropi

cal/s

ubtro

pica

l shr

ub-la

nd

19–2

5 22

50

–100

c.

2

A, B

pr

ocer

iflor

a br

anch

S

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

-land

21

–29

25

100–

200

2.

0– 2

.6

B N

itrop

hila

moh

aven

sis

stem

bor

n ro

ot

C

USA

de

sert

26–3

1 28

50

–100

c.

2

B

moh

aven

sis

root

C

U

SA

dese

rt 24

–31

28

50–1

10

c. 2

.4

B N

oaea

maj

or

stem

T

Turk

men

ista

n se

mi–

dese

rt 23

–26

25

50–1

20

c. 3

B

m

ucro

nata

br

anch

F/

S So

uthe

ast A

nato

lia

sem

i–de

sert

16–2

1 18

50

–120

c.

3

D N

ucul

aria

per

rini

br

anch

S

Alg

eria

de

sert

21–2

8 25

10

0–20

0 c.

2.5

D

Ofa

isto

n m

onan

drum

hy

poco

tyl

T R

ussi

a st

eppe

hal

ophy

tes

16–2

3 19

10

0–13

0

+/- 4

B

Ore

oblit

on th

esio

ides

hy

poco

tyl

H

Alg

eria

de

sert

14–1

9 17

10

0–12

0

c. 2

.5

A, B

Pac

hyco

rnia

tria

ndra

br

anch

S

Aus

tralia

su

btro

pica

l hal

ophy

tes

21–2

5 23

70

–120

3.

7–3.

9 N

tr

iand

ra

bran

ch

S A

ustra

lia

subt

ropi

cal h

alop

hyte

s 17

–22

20

70–1

30

c. 2

.5

N P

ande

ria

pilo

sa

hypo

coty

l T

Arm

enia

ru

dera

l?

19–2

6 22

50

–100

c.

2.5

B

Pat

ellif

olia

pat

ella

ris

stem

H

Sp

ain

litto

ral

35–4

8 41

50

–150

<

4 B

pr

ocum

bens

st

em

H

Spai

n lit

tora

l 46

–64

55

100–

200

<

4 B

Pet

rosi

mon

ia g

lauc

a st

em

T Tu

rkm

enis

tan

step

pe h

alop

hyte

s 16

–22

19

100–

220

c.

3

D

mon

andr

a hy

poco

tyl

T N

o in

form

atio

n st

eppe

hal

ophy

tes

18–2

4 21

50

–100

c.

3.5

D

op

posi

tifol

ia

stem

T

Sout

hwes

t Per

sia

step

pe

19–3

4 26

10

0–15

0 3.

3–3.

5 B

Pip

topt

era

turk

esta

na

stem

T

‘Buc

hara

’ ru

dera

l?

21–2

4 23

50

–150

3.

0–3.

5 D

Pol

ycne

mum

arv

ense

hy

poco

tyl

T Fr

ance

te

mpe

rate

sand

soils

14

–17

15

50–1

50

< 4

A, B

ar

vens

e hy

poco

tyl

T Ita

ly

tem

pera

te sa

nd so

ils

14–1

8 16

50

–150

c.

3.5

A

, B

font

anes

ii ro

ot

C

Alg

eria

de

sert

11–1

7 14

C

. 120

3.

5–4.

5 B

fo

ntan

esii

bran

ch

C

Alg

eria

de

sert

11–1

3 12

50

–110

c.

3.7

A

m

ajus

hy

poco

tyl

T G

erm

any

gard

en c

ultu

re

10–1

2 11

?

? A

, B

maj

us

root

T

Ger

man

y ru

dera

l 16

–21

19

100–

200

c.

2.3

A

, B R

hago

dia

bacc

ata

bran

ch

F So

uth

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

-land

19

–23

21

60–1

20

? N

pr

eisi

i br

anch

F

Sout

h A

ustra

lia

tropi

cal/s

ubtro

pica

l shr

ub-la

nd

30–3

6 33

80

–120

<

4 D

sp

ec.

bran

ch

F So

uth

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

-land

24

–34

29

50–1

60

< 4

D R

oyce

a di

vari

cata

br

anch

F

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

-land

11

–15

13

110–

160

c.

3

A, B

215Heklau et al. — Wood anatomy of Chenopodiaceae S

alic

orni

a e

urop

eea

hypo

coty

l T

Ger

man

y hu

mid

tem

pera

te h

alop

hyte

s 12

–18

15

40–1

00

3.5–

3.8

B

eu

rope

ea su

bsp.

bra

chys

tach

ya

basa

l ste

m

T G

erm

any

hum

id te

mpe

rate

hal

ophy

tes

12–1

5 14

50

–100

2.

0–2.

4 B

fr

agili

s hy

poco

tyl

T So

uth

Portu

gal

coas

t hal

ophy

tes

13–1

7 15

80

–150

c.

3.8

B

ni

tens

st

em

T Po

rtuga

l co

ast h

alop

hyte

s 13

–16

14

50–1

20

3.3–

3.6

B

patu

la

stem

T

Portu

gal

coas

t hal

ophy

tes

12–1

4 13

50

–120

c.

2.7

B

ra

mos

issi

ma

epic

otyl

T

Portu

gal

coas

t hal

ophy

tes

14–1

8 16

10

0–20

0

c. 3

.5

B S

also

la a

rbus

cula

br

anch

F/

S W

est M

ongo

lia

step

pe

35–4

0 38

50

–100

<

4 B

ge

nist

oide

s st

em

F Sp

ain

step

pe

17–2

1 19

50

–100

?

A, B

ka

li hy

poco

tyl

T Ita

ly

litto

ral

32–4

1 36

50

–100

<

4 B

ka

li st

em

T U

SA

prai

rie

31–4

6 38

50

–120

<

4

B

kali

stem

T

Spai

n st

eppe

25

–33

29

50–1

10

c. 3

B

ka

li su

bsp.

trag

us

stem

T

Portu

gal

litto

ral

32–3

9 35

10

0–20

0

3.8–

4.0

B

oppo

sitif

olia

br

anch

F

Spai

n lit

tora

l 20

–23

22

50–1

30

c. 3

B

pa

sser

ina

bran

ch

S W

est M

ongo

lia

step

pe

9–20

15

>5

0–12

0

< 4

D

soda

hy

poco

tyl/r

oot

T Po

rtuga

l lit

tora

l 21

–27

24

50–1

30

3.8–

4.0

A, B

ve

rmic

ulat

a br

anch

F

Spai

n st

eppe

21

–28

24

50–1

00

< 4

B

verm

icul

ata

bran

ch

F Sp

ain

step

pe

26–3

7 31

50

–150

c.

2.4

B

Scl

erol

aena

con

vexu

la

root

, hyp

ocot

yl

C

Aus

tralia

se

mi–

dese

rt 16

–20

18

50–1

20

c. 3

B

de

nsifl

ora

bran

ch

C

Aus

tralia

se

mi–

dese

rt 17

–25

21

40–1

00

2.4

–2.9

B

gl

abra

br

anch

S

Sout

h A

ustra

lia

tropi

cal/s

ubtro

pica

l hal

ophy

tes

20–2

6 23

80

–140

<

4 A

, B

oliq

uicu

spis

br

anch

S

Aus

tralia

tro

pica

l/sub

tropi

cal s

hrub

-land

15

–20

18

50–1

00

< 4

A, B

Sei

dlitz

ia fl

orid

a hy

poco

tyl

T ‘B

aku’

st

eppe

hal

ophy

tes

16–2

4 20

50

–130

2.

5–4

D

flori

da

bran

ch

T A

rmen

ia

step

pe h

alop

hyte

s 20

–27

24

100–

200

c. 2

.7

B

rosm

arin

us

stem

, bas

al

F Ir

aq

dese

rt 23

–28

26

50–1

50

c. 2

.8

A, B

Sev

ada

schi

mpe

ri

bran

ch

S O

man

de

sert

15–1

9 17

30

–70

c.

2

A S

pina

cia

turk

esta

nica

br

anch

T

Turk

men

ista

n st

eppe

28

–40

34

70–2

00

4–7

B S

uaed

a ae

gypt

iaca

st

em

T Eg

ypt

subt

ropi

cal h

alop

hyte

s 31

–37

34

80–1

50

< 4

A

, B

albe

scen

s ep

icot

yl

T Po

rtuga

l co

ast h

alop

hyte

s 15

–19

17

50–1

00

c. 3

.5

B

mar

itim

a hy

poco

tyl

T G

erm

any

hum

id te

mpe

rate

hal

ophy

tes

18–2

7 22

50

–100

4–

7 D

sp

icat

a hy

poco

tyl

T Po

rtuga

l su

btro

pica

l hal

ophy

tes

15–1

8 16

30

–100

c.

3

B

sple

nden

s st

em?

T Po

rtuga

l co

ast h

alop

hyte

s 15

–24

19

100–

130

c.

3

B

sple

nden

s st

em

T Po

rtuga

l co

ast h

alop

hyte

s 22

–30

26

100–

160

c.

3.5

B

ve

ra

bran

ch

F Li

bya

subt

ropi

cal h

alop

hyte

s 19

–27

23

50–1

00

< 4

N

vera

st

em

S Po

rtuga

l su

btro

pica

l hal

ophy

tes

23–2

6 25

?

? N

Suc

kley

a su

ckle

yanu

m

bran

ch

T U

SA

prai

rie

19–2

3 21

10

0–20

0 c.

2.5

?

Sym

pegm

a re

gelii

br

anch

S

Mon

golia

de

sert

31–4

0 36

50

–110

<

4 B

* T

egic

orni

a un

iflor

a br

anch

C

A

ustra

lia

tropi

cal/s

ubtro

pica

l hal

ophy

tes

16–1

9 17

70

–120

2

.4

N T

hrel

keld

ia d

iffus

a br

anch

C

A

ustra

lia

subt

ropi

cal h

alop

hyte

s 13

–18

15

50–1

00

c. 2

A

, B

inch

oata

st

em

C

Aus

tralia

tro

pica

l/sub

tropi

cal h

alop

hyte

s 15

–20

17

100–

180

3.

2–3.

3 A

, B T

raga

num

nud

atum

br

anch

S

Egyp

t de

sert

27–3

5 31

10

0–12

0 c.

3.5

N

nu

datu

m

bran

ch

S A

lger

ia

dese

rt 21

–27

24

80–1

20

c. 2

N

Zuc

kia

bran

dege

ei

bran

ch

S U

SA

prai

rie

22–2

7 25

50

–100

c.

3

N


Statistical methods Anatomical characters were analysed by simple correlations. To test for differences among the regions we used ANOVA’s 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, unligni-fied 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 µm in A, B, C, E, F; 100 µm in D.


RESULTS

Number of Successive cambia (Fig. 1) Anomalous secondary thickening has developed to different extents in Amarantha-ceae 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 hypo-cotyl anomalous secondary thickening has arisen in the axis (all other sub-families of the Chenopodiaceae). In the Salsoloideae, Suaedoideae, Salicornioideae, Camphor-osmoideae, 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. 3B 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), Halopepli- deae (Halopeplis perfoliata up to 16), Chenopodieae (up to 14), Salicornieae (Salicor- nia 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 inves-tigated 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 Poly- cnemum fontanesii we found irregularly arranged successive cambia in the root (Fig. 3B). 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. 3F), also belonging to the Polycnemeae, successive cambia do exist, but are absent in the stem.


Figure 3. Polycnemoideae. – A: Polycnemum fontanesii, a chamaephyte, Herbarium Jena (JE). – B: Polycnemum fontanesii, cross section of root with irregular successive cambia. – C: Poly- cnemum 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 µm in B, F; 50 µm in C; 100 µm in E.


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. 3E) 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 Chenopodia-ceae: 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. 2C), 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 (1–4) are active in one growth period. In the basal stem of the sub-shrub 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 in-stance 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 µm (Table 1). The widest vessels are in the small tree Haloxylon am-modendron. 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 (9–13 µm) 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


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 µm. 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 Sclero- laeneae, 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 µm). The statistical tests show highly significant dif-

Table 2. Tukey multiple comparisons of mean values for vessel diameter in different eco-logical categories.

2.1. Annuals

Comparison of ecological Differences between Significance level categories ecological categories (µm) of differences

Garden culture ~ coast halophytes 16 **

Ruderal ~ coast halophytes 15 **

Steppe halophytes ~ garden culture -13 **

Steppe halophytes ~ ruderal -12 **

Humid temperate halophytes ~ ruderal -13 *

2.2. Annuals

Comparison of ecological Differences between Significance level categories (All halophytes ecological categories (µm) of differences combined into one ecological category)

Halophytes ~ garden culture -13 ***

Ruderal ~ halophytes 12 ***

Steppe /prairie ~ halophytes 8 *

*** = p < 0.001; ** = p < 0.01; * = p < 0.05.


Figure 4. Range of mean vessel diameters in µm in therophytes (annual herbs) of Chenopo-diaceae 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.

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

Coa

st

halo

phyt

es

Des

ert p

lant

s

Gar

den

cultu

re

Litto

ral

Rud

eral

Sem

i-des

ert

Ste

ppe/

prai

rie

Ste

ppe

halo

phyt

es

Hum

idte

mpe

rate

halo

phyt

es

Trop

ical

/su

btro

pica

lha

loph

ytes

50

40

30

20

10

Mea

n ve

ssel

dia

met

er in

µm

*

*

*

Coa

st

halo

phyt

es

Des

ert

Des

ert

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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 non-significant 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 µm. In some species of the tribe Camphorosmeae, e.g. Camphorosma soongoricum, Cycloloma atriplicifolium, Bassia eriophora, relatively long vessel elements (>200 µm) are frequent. In the tribe Cori-spermeae, that only comprises annual species, the mean vessel element length is frequently 150–200 µm, 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 µm. Extremely short vessel elements (30 or 40–100 µm) 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 (50–90 µm), whereas the range is much larger in the axis of the annual herb Chenopodium murale (50–200 µm) and in the branches of the sub-shrub Halostachys caspica (80–160 µm). Overall, the vessel elements are very short.

Intervessel pits Intervessel pits are often alternate. In about 40% of the samples they were exclu-sively alternate. Only in 11% of the species alternate intervessel pits are entirely absent. In about 49% the intervessel pitting is mixed: alternate/opposite, or occasion-ally 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 subaphyl-lus, Haloxylon griffithii, Horaninovia anomala, Lagenantha cycloptera, Micropeplis arachnoidea, Seidlitzia rosmarinus), Chenopodieae (Chenopodium capitatum, C. hybri-dum, C. polyspermum, C. strictum) and Betoideae (Acroglochin persicarioides). Only in Chenopodium bonus-henricus, Beta trigyna, Patellifolia procumbens (Fig. 6D) and Hablitzia tamnoides (Fig. 6C) are the pits mostly scalariform. Intervessel pits are mostly < 4 µm. However, in Allenrolfea occidentalis, Atriplex patula, Arthrocnemum fruticosum, Polycnemum fontanesii, Spinacia turkestanica and Suaeda maritima they were slightly larger than 4 µm, and Atriplex patula and Suaeda


maritima have pit sizes between 4 and 7 µm. Only in the vessels of roots of Poly-cnemum fontanesii were a few pits larger than 4 µm. Anabasis brevifolia, Halopeplis perfoliata, Iljinia regelii, Microgynoecium tibeticum and Suckleya suckleanum have minute pits (<< 4 µm).

Helical thickenings on vessel walls Vessels with helical thickenings were found only in Arthrocnemum fruticosum (Sali- cornieae) from the Mediterranean, and in Maireana pyramidata and Roycea divaricata (Sclerolaeneae) from Western and Southern Australia.

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 µm in A; 100 µm in B; 20 µm in C, D.


Fibre wall thickness In the stem and basal branch wood of most Chenopodiaceae fibres dominate. How-ever, in taxa with a succulent hypocotyl and roots (Beta, Patellifolia) or a pleiocormus (Hablitzia tamnoides, Chenopodium bonus-henricus) axial parenchyma is more abun-dant. 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 µm (Chenopodium rubrum), 271 µm (Atriplex sagittata), 246 µm (Atriplex prostrata) and 317 µm (Bassia scoparia). In the stem of the small tree Haloxylon ammodendron the fibres were on average 286 µm long. In the stems of hemiphanerophytes or nanophanerophytes (Kraschenin-nikovia ceratoides, Anabasis brevifolia, Salsola vermiculata, Maireana pyramidata, Atriplex lindleyi) the fibres were 193–357 µm long. In comparison to dicotyledons as a whole the Chenopodiaceae have short fibres.

Axial parenchyma Paratracheal parenchyma — In most Chenopodiaceae paratracheal axial parenchy-ma 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 conjunc-tive axial parenchyma is consistent within stems, for instance in annual Atriplex or Chenopodium species and in the sub-shrub Krascheninnikovia ceratoides (Fig. 2A, 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


as a network, as in the annual Atriplex species A. sagittata, A. prostata (Fig. 2F) 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. 2D–F) Medullary rays extending from the pith to the primary cortex hardly exist in Chenopo-diaceae stems because continuity to the primary cortex may be interrupted by the first “master cambium” (sensu Carlquist 2007a) and later successive cambia. In cross sec-tions 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, Camphoros-meae, 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. 2E, 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 tempo-rarily 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 Poly-cnemum majus, P. arvensis (Fig. 3E) and in the stem of Polycnemum fontanesii (Fig. 3C). The rays in Chenopodiaceae consist mostly of upright cells. Their shape (oval, round, rectangular) and ray width vary between genera and species. In Atriplex hort-ensis 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 (1–3-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


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 Mi-crocnemum 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 inclu-sions 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. 6A).

Aerenchyma Tegicornia uniflora (Salicornieae) stems from saline habitats in Western Australia have aerenchyma in the primary cortex (Fig. 6B).

DISCUSSION

Successive cambia (Anomalous thickening) Successive cambia are widespread in the Caryophyllales (Carlquist 2001). The inter-pretation of anomalous secondary thickening is summarised in Fahn & Zimmermann (1982), Heklau (1992) and Kühn 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 develop-ment of successive cambia. The radiation of the Chenopodiaceae probably was associated with the develop-ment of arid regions in the world (Kühn 1993). In the late Tertiary a large arid zone


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–)40–300 (–700) µm (Lösch 2003). Nearly 41% of dicotyledons have vessel diameters between 40 and 79 µm (Metcalfe & Chalk 1985; Wheeler et al. 2007), and the vessels of Cheno-podiaceae 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 µm in stems of Atriplex halimus and 90 µm in Haloxylon persicum. Their results extend the range of maximum tangential vessel diameter in Chenopo-diaceae, 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), ecologi-cal investigations need to compare material from the same organ and cambial age. In Krascheninnikovia ceratoides, the vessel diameter in the stem was nearly 10–15 µm wider than in the shoots, and 5–10 µm wider than in basal branches of the same sample (Heklau & Von Wehrden 2011). The range of mean vessel diameters in Chenopodiaceae (9–66 µm) is similar in the close relatives of Amaranthaceae. In Amaranthaceae from the tropics and subtropical deserts, Carlquist (2003) recorded a range of 15–52 µm. Rajput (2002) found that short-lived tropical Amaranthaceae had vessel diameters of 49–69 µm. Baas et al. (1983), Fahn et al. (1986), Baas & Schweingruber (1987) and Schwein-gruber (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/µm, also in species where the clearly recognisable narrow vessels in transverse section had diameters >>10/µm, cf. Table 1) were not easily recognisable as such in transverse sec-


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 µm, whereas our sample was only 160 µm.

Mean fibre length The Chenopodiaceae has some of the shortest fibres in the dicotyledons. Metcalfe and Chalk (1950) gave a range of 200–400 µm in Chenopodiaceae, in good overall agreement with our range of 190–360 µm for average fibre lengths. In dicotyledons as a whole 44% of the species have a range of means of 900–1499 µm and only 0.5% up to 299 µm (Metcalfe & Chalk 1950). According to Fahn et al. (1986) the mean fibre length of sub-shrubs reaches 400 µm in Anabasis articulata. In a few species the maximum fibre length far exceeds this: 600 µm in Haloxylon persicum, 540 µm in Anabasis articulata and 580 µm 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 600–900 µm and in the Cactaceae 400–900 µm (Metcalfe & Chalk 1950). In Amaranthaceae the range of fibre lengths is larger, from 347–1528 µm (Carlquist 2003). For the common tropical weed Trianthema monogyna (Aizoaceae) Rao and Rajput (1998) noted a fibre length of 380–460 µm.

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). Medul-lary 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


secondary woodiness – that is the evolution of woodiness from herbaceous ancestors in some chiefly herbaceous clades of the Chenopodiaceae – might have occurred. How-ever, 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, Lev-Yadun 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 succes-sive cambia in Chenopodioideae, Salicornioideae, Salsoloideae, Suaedoideae; fewer in Betoideae, Corispermoidae and Camphorosmoideae and even fewer in Polycnemoi-deae. The present study confirms and enlarges upon observations described in the literature, e.g. successive cambia, narrow vessels (<100 µm), short vessel elements (< 270 µm), mostly minute intervessel pits (< 4 µm) and short fibres (< 470 µm). 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. Zündorf (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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