Botanical Journal of the Linnean Society, 2010, 164, 342–393. With 21 figures Caryophyllales: a key group for understanding wood anatomy character states and their evolutionboj_1095 342..393 SHERWIN CARLQUIST FLS* Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93110, USA Received 13 May 2010; accepted for publication 28 September 2010 Definitions of character states in woods are softer than generally assumed, and more complex for workers to interpret. Only by a constant effort to transcend the limitations of glossaries can a more than partial understanding of wood anatomy and its evolution be achieved. The need for such an effort is most evident in a major group with sufficient wood diversity to demonstrate numerous problems in wood anatomical features. Caryophyllales s.l., with approximately 12 000 species, are such a group. Paradoxically, Caryophyllales offer many more interpretive problems than other ‘typically woody’ eudicot clades of comparable size: a wider range of wood structural patterns is represented in the order. An account of character expression diversity is presented for major wood characters of Caryophyllales. These characters include successive cambia (more extensively represented in Caryophyllales than elsewhere in angiosperms); vessel element perforation plates (non-bordered and bordered, with and without constrictions); lateral wall pitting of vessels (notably pseudoscalariform patterns); vesturing and sculpturing on vessel walls; grouping of vessels; nature of tracheids and fibre-tracheids, storying in libriform fibres, types of axial parenchyma, ray anatomy and shifts in ray ontogeny; juvenilism in rays; raylessness; occurrence of idioblasts; occurrence of a new cell type (ancistrocladan cells); correlations of raylessness with scattered bundle occurrence and other anatomical discoveries newly described and/or understood through the use of scanning electron microscopy and light microscopy. This study goes beyond summarizing or reportage and attempts interpretations in terms of shifts in degrees of juvenilism, diversification in habit, ecological occupancy strategies (with special attention to succulence) and phylogenetic change. Phylogenetic change in wood anatomy is held to be best interpreted when accompanied by an understanding of wood ontogeny, species ecology, species habit and taxonomic context. Wood anatomy of Caryophyllales demonstrates problems inherent in binary character definitions, mapping of morphological characters onto DNA-based trees and attempts to analyse wood structure without taking into account ecological and habital features. The difficulties of bridging wood anatomy with physiology and ecology are briefly reviewed. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393. ADDITIONAL KEYWORDS: constricted perforation plates – ecophysiology – idioblasts – juvenilism – paedomorphosis – raylessness – scattered bundles – successive cambia – vestured pits – wood evolution. ‘. words are scary and inadequate, things named being keys to identify plants. They currently enjoy popular- compromised thereby, and changed.’ Guy Davenport, A Table ity in data matrices and thereby lend themselves to of Green Fields computerized (0/1) manipulations. Where wood char- acters are concerned, do binary characters express anatomical features accurately? We know that char- INTRODUCTION acter transformation in wood features involves Binary definitions (present/absent, long/short) have changes in gene presence, gene expression timing, been used for centuries in the form of dichotomous modifier genes and hormonal pathways (Nilsson et al., 2008), features not yet integrated by wood anatomists into their work. In the wood anatomy of *Corresponding author. E-mail: [email protected] Caryophyllales and some other clades, however, we 342 © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 343 find complex character expressions, the nuances, mul- tribe Pisonieae Meisn. of Nyctaginaceae have ‘rays’ or tiplicity and lability of which defy ordinary definitions ‘neorays’? Phylogenetic trees based on DNA sequences and glossary treatment. This diversity may not be have now plotted out the entirety of Caryophyllales stressed by workers interested primarily in wood well (e.g. Cuénoud et al., 2002) and some areas of the identification and in mapping wood characters onto order have been subjected to more detailed DNA- phylogenetic trees. Caryophyllales show how morpho- based phylogenetic study (further refinements in logical patterns often elude earlier definitions, and topology are to be expected). However, these trees do therefore evolutionary patterns can be misinterpreted not provide the answer to those questions; ontoge- or neglected. The focus of the present paper is on netic studies have been required. these characters and why they defy simplistic binary The ray question just cited is part of the story of capture. successive cambia in Caryophyllales. Ontogenetic The case of the placement of Gnetales offers a studies, in this paper and earlier (Carlquist, 2007a; critical example of how definitions drive evolutionary Rajput, Patil & Shah, 2008), permit us to recognize interpretations, to the detriment of those interpreta- modes of successive cambial action throughout Caryo- tions. The vessels of Gnetales were claimed by phyllales and other angiosperms: once we know which Thompson (1918) to be different from those of ontogenies create which patterns, we do not need to angiosperms, and therefore not referable to them. A carry out the developmental studies for each species. challenge to that concept (Muhammad & Sattler, However, the IAWA Committee (1989) advised ‘The 1982), although widely cited, was unsupportable. The features for included phloem types are based on the idea that gnetalean vessels were homologous to those appearance of the wood, and do not have developmen- of angiosperms, and could therefore be referred to a tal inferences – they are not defined on whether there unitary concept of ‘vessels’, was revived (Doyle, 1996), is a single permanent cambium, or successive cambia, although contemporary evidence (Carlquist, 1996) to or whether the tissue surrounding the phloem the contrary was demonstrated. The use of binary strands is xylem or conjunctive tissue’. Now that we definitions and thereby the claim that both Gnetales have ontogenetic information, newer definitions less and angiosperms had comparable (‘homologous’) likely to mislead are possible. vessels (Doyle, 1996) was one of the keystones that Caryophyllales invite us to look anew at bordered led to the ‘anthophyte hypothesis’. This now- pits, because the order contains numerous iterations abandoned hypothesis claimed that Gnetales were of this feature, some hitherto undescribed. Bordered an early-diverging branch of flower-bearing plants. pits are a symplesiomorphy of vascular plants as a Soon, DNA-based work showed that Gnetales are whole, a fact often unappreciated. Although often probably nested within conifers. Had two categories, depicted in textbooks, their function is rarely ‘angiospermous vessels absent/present, and ‘gneta- described (or described fully), thereby inviting stu- lean vessels absent/present’ (along with similar inter- dents to regard them as some sort of xylary ornament pretations for other characters, such as strobilar rather than as a precisely designed compromise structure and gametophyte nature), been invoked for between conduction and wall strength. Bordered pits a data matrix, an anthophyte hypothesis placing are common on ray cells of angiosperms, especially on Gnetales as sister to the angiosperms might not have tangentially oriented walls (Carlquist, 2007b), a been advanced. feature that is routinely avoided or omitted in One can say that if one starts with molecular evi- descriptions of woods. Borders are present on second- dence, definitions (and phylogenetic interpretations) ary wall annuli and helices of primary xylem and on are more likely to be correct than if one starts merely scalariform pits of metaxylem, although textbook with morphology. One could wish that were true, but figures often omit them. Not surprisingly, then, the such a simple procedure is, in fact, not always avail- occurrence of non-bordered perforation plates in able or applicable. DNA-based trees cannot be con- Caryophyllales and a scattering of families from other structed for fossil groups, and fitting fossil groups into orders (Carlquist, 2001b) has attracted notice from trees that include extant groups forces us to stress only a few authors. Consequently, that feature is morphological characters that can be found in both more fully discussed here. Secondary wall helices of fossil and extant groups. The problems of definition tracheary elements of globular cacti have attracted creation and application do not end there, however. As attention, but the fact that the helices are bordered we will see, ray types and origins in Caryophyllales has not been stressed. Idioblasts with borders in do not, in some respects, conform to classical defini- Nepenthaceae have not been accurately described tions of these structures. Do amaranths and chenop- before, nor have peculiar axial parenchyma cells with ods (together, Amaranthaceae s.l. sensu APG III, large bordered pits in Ancistrocladaceae. Ray cells 2009) have ‘wide rays’ or do they have ‘radial plates of often have small bordered pits, easily identified with conjunctive tissue’