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, suc- cessive 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: heike.heklau@botanik. uni-halle.de]. 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. Downloaded from Brill.com09/25/2021 11:45:20PM via free access 206 IAWA Journal, Vol. 33 (2), 2012 (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 Downloaded from Brill.com09/25/2021 11:45:20PM via free access 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 (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 min- utes, 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 Downloaded from Brill.com09/25/2021 11:45:20PM via free access 208 IAWA Journal, Vol. 33 (2), 2012 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.