Caryophyllales: a Key Group for Understanding Wood

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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 characters 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

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’ or are they rayless? Do members of light microscopy as well as scanning electron micro-

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 344 S. CARLQUIST scopy (SEM). Comparative information on features The Results section of the present paper is devoted such as these can lead to a realization that bordered to patterns within Caryophyllales. Of necessity, these pits may occur in a variety of ways related to a wide presentations involve discussion of the problems pre- range of functions (the ‘tear-away’ helices of sented by the patterns and are not confined exclu- nepenthaceous helical idioblasts may have such a sively to descriptions. Original observations are novel function). Thus, we see a gene programme that incorporated, and thus ‘Results’ ranges between origi- has been modified in various unexpected ways. nal data and review, but within caryophyllalean The present essay is not a traditional overview of clades. Detailed descriptions have been furnished in wood of Caryophyllales, although it attempts expla- earlier books and papers, and the present essay does nations for why particular character states occur in not duplicate those, although illustrations are fur- given species. For example, Frankeniaceae and Tama- nished to make the textual information about Caryo- ricaceae are sister families. They both occupy saline phyllales more comprehensible. By contrast, the or alkaline habitats, but Frankeniaceae have narrow, Conclusions section presents the patterns of Caryo- markedly grouped vessels and rayless or near-rayless phyllales in relationship to angiosperms as a whole. woods, whereas Tamaricaceae have wide, solitary General phenomena such as habit, heterochrony, vessels and wide multiseriate rays. Such differences ecology, etc., are considered in that section. The Con- can be explained in terms of habit and ecology. By clusions section is also concerned with tenets about explaining such differences, we can hope to explain how we process information on wood anatomy in other differences in wood, and no longer categorize phylogenetic ways, and the validity of particular these as ‘systematic characters’, but as adaptive wood methods, concepts and definitions in wood anatomy as features. Too often, in the past, wood samples came a whole. from unknown provenance, and thus relating wood anatomy to ecology was considered unnecessary or MATERIAL AND METHODS speculative. It is neither. We may be unable fully to bridge the fields of wood anatomy and wood ecophysi- My own monographs on various families form a com- ology, but presentation of results in either field pilation basic to this study, but I have not attempted without references to the other should no longer be original research in Cactaceae because extensive data considered good science. have been offered by Gibson (1973 ff.), Mauseth (1999 Caryophyllales are a daunting group to review ff.) and by others. I have attempted to use new illus- because of the size: approximately 10 000 species are trations wherever possible. Data are not given for included within ‘core Caryophyllales’ (Behnke & illustrations that are the same as those in published Mabry, 1994). Molecular phylogenetic analyses have papers. For previously unpublished illustrations, sup- added another clade of perhaps 2000 species, termed porting data are given in captions that accompany ‘non-core Caryophyllales’ by Cuénoud et al. (2002), as them. Rivinaceae are recognized as a family separate shown in Figure 1. This annexation was the result of from Phytolaccaceae. Phytolaccaceae s.s. can be work by Williams, Albert & Chase (1994), Fay et al. defined by the presence of raphides and triaperturate (1997) and Applequist et al. (2006), among others. pollen grains (and are limited to the genera Anisome- Rhabdodendraceae, long misplaced, now become the ria D.Don, Ercilla A.Juss., and Phytolacca L.), sister to the remainder of Caryophyllales. Molecular whereas Rivinaceae have styloid-like crystals and studies have necessitated recognition of segregate polyaperturate pollen grains (data from Pax & families, especially in the groupings formerly consid- Harms, 1934; Erdtman, 1953). Petiveriaceae is con- ered as Phytolaccaceae and Portulacaceae. New sig- sidered a synonym of Rivinaceae for the purposes of nificance of particular wood features emerges when this essay. Recent phylogenetic analyses of Caryo- woods are considered on the basis of the recent work phyllaceae agree in uniting Amaranthaceae and Che- in molecular phylogeny. Of interest considering the nopodiaceae (as Amaranthaceae s.l.). That inclusive size of the assemblage, Caryophyllales are not mark- view is followed here, but ‘amaranths’ and ‘chenopods’ edly woody: only a small number are trees. We actu- are used as convenient names for the two subfamilies. ally have more to learn about wood anatomy and The sequence of photographic plates is intended to evolution from Caryophyllales than from such assem- conform to the sequence of features as they are dis- blages as Sapindales, because the non-arboreal cussed in the text. This sequence, happily, also corre- expressions of wood characters in Caryophyllales are sponds closely to systematic groupings, with the core more diverse than those in a ‘typically woody’ family. Caryophyllales presented first, followed by the non- One need only mention genera such as Beta L., Bou- core Caryophyllales. Because Rhabdodendron Gilg & gainvillea Comm. ex Juss. and Opuntia (L.) Mill. in Pilg. is the sister genus to the remainder of the order to see that wood anatomy serves in a wide Caryophyllales, it is presented first in the photo- range of growth forms and ecological programmes. graphic plates. Although Cuénoud et al. (2002) did not

Figure 1. Phylogenetic tree of Caryophyllales, including several outgroups, derived mainly from Cuénoud et al. (2002) and Applequist & Wallace (2001). Structure of the tree indicates only current ideas of relationship; no meaning is intended by branch lengths, which have been drawn to be of equal length. All families of Caryophyllales currently thought to be valid are included (see Material and Methods for further details). Note that some familial delimitations are still in ﬂux and Agdestidaceae and Rivinaceae, recognized here, are included in Phytolaccaceae in APG III (2009) pending further resolution. bracket Rhabdodendraceae within Caryophyllales, recently recognized. The present study does not the results of the present study clearly indicate that present any anatomical details concerning Corbi- they must be included within Caryophyllales rather chonia or Lophiocarpaceae, and therefore any com- than regarded as an outgroup of the order. The tree of ments regarding Molluginaceae do not refer to data Cuénoud et al. (2002) showed Molluginaceae as tra- from Corbichonia. Molluginaceae may prove to be ditionally constituted to be biphyletic. Corbichonia close to Caryophyllaceae, as suggested by Harbaugh Scop., usually placed in Molluginaceae, groups closely et al. (2010). Certainly, precise topology of the order is with Lophiocarpaceae, a caryophyllalean family only still in ﬂux (Brockington et al., 2009; Nyffeler & Eggli,

Figure 2. Phylogenetic tree of Caryophyllales, including most of the families shown in Figure 1. Those families shown in bold face contain species with successive cambia. Italic bold face indicates that all species of a family have successive cambia, as far as is known. ‘r’ indicates that raylessness occurs in at least one species of a family. Branch lengths are of standard length and no meaning is intended by this convention.

2010). However, agreement seems general that Steg- RESULTS nospermataceae and Simmondsiaceae are relatively SUCCESSIVE CAMBIA: PHYLOGENETIC REFINEMENTS early-diverging groups in the core Caryophyllales. AND COMPLEXITIES This essay is, in part, a critique of definitions: not so much of their existence as of how they are applied. Systematic distribution Definitions are essential to the student, but the If we look at successive cambial occurrence mapped on results of workers eventually transcend simple defi- the molecular tree of Figure 2, the distribution appears nitions. Modifications are inevitably needed. difficult to explain. If we make the assumption that

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 347 successive cambia are ancestrally absent in Caryo- Thus, a minimum of approximately 11 character phyllales, we have to hypothesize that this feature was state changes are required if we hypothesize the acquired independently in about eleven instances presence of successive cambia as a symplesiomorphy within the clade: (1) Rhabdodendraceae; (2) Dionco- in the caryophyllalean clade, and a minimum of phyllaceae; (3) Antigonon Endl. in Polygonaceae; (4) approximately 11 character state changes are Aegialitis R.Br. in Plumbaginaceae; (5) Simmondsi- required if we hypothesize the absence of successive aceae; (6) Caryophyllaceae; (7) Halophytaceae; (8) cambia as a symplesiomorphy (and thereby acquisi- Amaranthaceae s.l.; (9) Stegnospermataceae; (10) tion as an apomorphy). Basellaceae; (11) The Phytolaccaceae–Aizoaceae– Some observers might be tempted to ask which Nyctaginaceae clade. hypothesis is correct. The answer to that question Note should be taken that half of these families does not prove simple, perhaps not even possible. contain fewer than 10 species, and Aizoaceae, Ama- First, we do not have an exhaustive knowledge of ranthaceae and Nyctaginaceae are the only relatively successive cambial distribution within Caryophylla- large families in which successive cambia are perva- les. If we did, however, the results probably would sively present. If, however, we imagine absence of look similar to the above summary. Second, we do not successive cambia as symplesiomorphic, we also have have DNA-based trees for all of the clades in which to imagine that, in the ancestors of Caryophyllales, successive cambia are both present and absent. Third, successive cambia are an apomorphy in Nuytsia R.Br. there is a tendency for relatively short-lived or of Loranthaceae and Doliocarpus Rol. of Dilleniaceae, ephemeral growth forms to lack successive cambia families otherwise lacking in successive cambia. We because the ﬁrst vascular cambium produces suffi- also have to hypothesize secondary loss of successive cient secondary tissue for the duration of the plant. cambia within Gisekiaceae and within Hilleria Vell., One should note, however, that in some annual Ama- Ledenbergia Klotzsch ex Moq., Schindleria H.Walter, ranthaceae s.l. (Beta) successive cambia are present and Trichostigma A.Rich. of Rivinaceae, in which case in the root. Pfeiffer (1926) did not report successive the number of required character changes within cambia in Monococcus F.Muell. (Rivinaceae) or Steg- Caryophyllales could total 13. nosperma Benth. (Stegnospermataceae). His materi- If we look at the reverse hypothesis, that successive als were probably stems of insufficient diameter to cambia were ancestrally present in Caryophyllales, show successive cambia. Successive cambia were we have to hypothesize character change in at least since reported in Monococcus (Jansen, Ronse the following clades: loss of successive cambia in 1–8, Decraene & Smets, 2000) and in Stegnosperma secondary acquisition of successive cambia in 9–11. (Horak, 1981), based on specimens of larger diameter. If one compares presence of successive cambia to 1. The insectivorous clade (Nepenthaceae, Droser- diameter of stem or root, however, the correlation aceae, Drosophyllaceae, Ancistrocladaceae and within Caryophyllales is too weak to support either of most Dioncophyllaceae). the two hypotheses for origin of (or loss of) this 2. The Asteropeiaceae – Physenaceae clade. feature. For example, if stem diameter were the criti- 3. The salt-gland clade (Plumbaginaceae, Frankeni- cal factor, Achatocarpaceae, Ancistrocladaceae, Aster- aceae and Tamaricaceae) and Polygonaceae. opeiaceae and other families and genera that lack 4. Caryophyllaceae (successive cambia are absent in successive cambia should have them. In Caryophyl- stems of all but a few Caryophyllaceae, and laceae, however, there is a tendency for numerous absent in roots of most genera: Pax & Harms, genera to have successive cambia in perennial roots, 1934). but for only a few genera to have them in stems 5. Achatocarpaceae. (Cometes L., Corrigiola L and Pollichia Medik. Pfe- 6. The Molluginaceae–Limeaceae clade. iffer, 1926). This is similarly true in some Nyctagi- 7. The Portulacaceae–Didiereaceae–Cactaceae clade. naceae (Abronia Juss., Boerhaavia Mill.). 8. Four genera of Rivinaceae (Hilleria, Ledenbergia, Schindleria and Trichostigma). Successive cambia: basic plan 9. Aegialitis of Plumbaginaceae (successive cambia In a survey of successive cambia (Carlquist, 2007a), reacquired). stress was placed on the unity of how successive 10. Triphyophyllum of Dioncophyllaceae (successive cambia are formed. The ﬁrst vascular cambium, cambia reacquired). derived from procambium, forms secondary xylem 11. Antigonon of Polygonaceae (successive cambia and secondary phloem. Some time later, a meristem- reacquired). atic cylinder of cells forms in the cortex by periclinal If outgroups follow this pattern, autapomorphies (tangential) divisions in cortical parenchyma. This for successive cambia must be assumed for Nuytsia meristematic layer, termed the master cambium, (Loranthaceae) and Doliocarpus (Dilleniaceae). forms one to several layers of secondary cortex to the

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 348 S. CARLQUIST outside. (Failure to notice this abaxial activity, which The master cambium adaxially produces conjunctive can admittedly be inconspicuous, led Philipson & tissue, followed by differentiation of a vascular Ward, 1965 and others to think of this cambium as cambium; in turn, the vascular cambium produces unidirectional.) To the inside, the master cambium secondary xylem adaxially and secondary phloem forms radial rows of derivatives; these derivatives are abaxially. Alternating with these strips are rays the same in tangential diameter as the cells of the (Fig. 5B), some of which are not well defined, suggest- master cambium. The most adaxial of these cells ing a loss of differentiation between axial and radial mature into conjunctive tissue. At some point, a vas- systems. Can one say, as did Metcalfe & Chalk (1950), cular cambium forms outside of the cell layers des- that Bougainvillea has ‘radial bands of conjunctive tined to become conjunctive tissue. The origin of a tissue’? There is some merit in that designation in that vascular cambium is identifiable because anticlinal it stresses the loss of histological difference between divisions produce narrower meristematic cells, and radial and axial parenchyma. How does this occur these tangentially narrower cells do not widen (as ontogenetically? Are there still divisions that represent seen in longitudinal section, they do elongate by ray initials with a vascular cambium, or do all of the means of intrusive growth). This process is shown divisions leading to the radial strips of parenchyma here in Figures 4–6 and has been illustrated in Car- occur in the master cambium? If the former occurs, the lquist (2004, 2007a, c). The master cambium is not wood is rayless. I have carefully observed genera of always active, and may be dormant: continual mer- Amaranthaceae s.l and Nyctaginaceae, in search of ray istematic activity (as seen in Beta, for example) is the initials within the vascular cambium. The drawings in exception rather than the rule. More than one vascu- my paper (Carlquist, 2007a) show the concept of ray lar cambium can be active at a time, although inner cambium developing in the radial files of cells derived vascular cambia in a stem or root become progres- from master cambium. This drawing was based on sively less active than those at the periphery. Second- Stegnosperma, but can be applied to other Caryophyl- ary phloem is produced for a longer period than is lales. For ray cambia initials in the present paper, see secondary xylem. The master cambium can be Figure 4B. Ray cambia (in addition to master cambia) dormant for prolonged periods. can be found in the amaranths Amaranthus L., Bosea Ray initials are present within the vascular L. and Celosia L., and well as in some chenopods cambium (except in rayless species, as noted below). (Beta). Ray cambia in these genera are not as active as In genera such as Rhabdodendron (Fig. 3) and Steg- in Rhabdodendron, Simmondsia and Stegnosperma, nosperma (Fig. 4), the action of each vascular however. Thus, tangential divisions leading to ‘rays’ or cambium and its products are completely like those in radial strips of parenchyma that look like rays (but eudicots with a single cambium. One should therefore may not be as precisely defined) may be intermediate not make a distinction between a ‘normal cambium’ to raylessness in genera of Amaranthaceae and and an ‘anomalous cambium,’ as some have (Horak, Nyctaginaceae. 1981). This distinction has led to misinterpretations In fact, Bougainvillea seems to represent a stage of lateral growth in plants with successive cambia. well along in this transition and close to raylessness. The above is offered as a way of clarifying the nature Within certain genera of chenopods and amaranths, of successive cambia in Caryophyllales. One must now one can say that divisions leading to ray initials occur add some variations within the basic plan of Caryo- in certain genera, whereas, in others, there are no phyllales in terms of sequential evolutionary changes. bands of meristematic cells identifiable as ray initials The secondary xylem of Rhabdodendron, Simmond- intervening between master cambia and cells other sia Nutt. and Stegnosperma can be used as a basic than xylem and phloem. In the latter, raylessness type for purposes of discussion. In these, the wood occurs. Vascular cambia are produced by the master consists of tracheids and has both multiseriate and cambium in Bougainvillea, but only occasional ray uniseriate rays (the multiseriate rays are not notably cambial cells or rays (Fig. 5D). Thus, Bougainvillea large). The vascular cambia in these genera include may represent a transitional condition, and deserves ray initials, tangentially aligned with fusiform ini- more study as such. The ontogenetic interpretation of tials as in eudicots with single cambia. Note should be Esau & Cheadle (1969) is untenable. It claims a taken that these three genera from monogeneric fami- single cambium that produces conjunctive tissue and lies (Figs 1, 2) represent early-diverging branches of secondary phloem to the outside, as well as conjunc- the caryophyllalean clade. Similar examples may be tive tissue and secondary xylem to the inside. One found in Rivinaceae and Phytolaccaceae s.s. should be able to see the two increments in each band of conjunctive tissue, but such do not exist. Each Ray localization, widening, loss and shift in origin cambium would have to shift from producing wider The secondary xylem of Bougainvillea Comm. ex Juss. parenchyma cells to narrow conductive cells. More- (Fig. 5A) represents an example of these tendencies. over, the interpretation of Esau & Cheadle (1969)

Figure 3. Light and scanning electron microscopy (SEM) micrographs of wood of Rhabdodendron amazonicum (Spruce ex Benth.) Huber. A, transection, two strands of secondary phloem (sp), collapsed, at top. Location of vascular cambium indicated by arrow. B, tangential section. Uniseriate rays are composed of upright cells and multiseriate rays mostly have long wings. C, transection. Axial parenchyma is mostly scanty paratracheal, but with an occasional diffuse cell. D, transection of tracheids to illustrate the narrow lumina and the bordered nature of pits. E, SEM micrograph of inner vessel wall. Pit apertures are vestured. Scale bars, 50 mm (A, B); 20 mm (C); 5 mm (D); 3 mm (E).

Figure 4. Sections of Stegnosperma alimifolium Benth. stem. A, transection, showing two vascular increments. Pointer indicates master cambium, arrows indicate the vascular cambia. B, transection, higher power, to show the histology of the outer stem. Pointer indicates master cambium and arrows indicate vascular cambium; sc, secondary cortex; sp, secondary phloem, sx, secondary xylem. C, tangential section, to show bordered pits on vessel (centre) and tracheids (at right and left). There are narrow slits interconnecting some pit apertures. D, tangential section; both multiseriate and uniseriate rays are present. Scale bars, 20 mm (A, B, D); 10 mm (C).

Figure 5. Sections of stems of Nyctaginaceae. A–B, Bougainvillea spectabilis Willd. A, transection to show successive cambia. Pointers indicate master cambium, arrows indicate vascular cambia. B, tangential section. Several multiseriate rays may be seen at the centre; fct, ﬁbrous conjunctive tissue; pct, parenchymatous conjunctive tissue. C–D, Heimerlio- dendron brunonianum (Endl.) Skottsberg. C, transection, showing several vascular increments. Arrow indicates a vascular cambium; pct, parenchymatous conjunctive tissue (ﬁbrous bands of conjunctive tissue are dark grey); sp, secondary phloem; sx, secondary xylem. D, tangential section. Fibres occupy most of photo; no rays are present; vessel to left of centre. Scale bars, 50 mm (A–D).

Figure 6. Sections of stems of Nyctaginaceae and Aizoaceae. A–B, Pisonia rotundata Griseb. A, transection, showing several vascular increments embedded in a background of ﬁbrous conjunctive tissue (fct); thick-walled parenchymatous conjunctive tissue (pct) is adjacent to secondary phloem (crushed phloem is dark grey); arrow indicates a vascular cambium. B, tangential section of ﬁbrous conjunctive tissue to show that it contains uniseriate and biseriate rays; three two-celled strands of axial parenchyma are adjacent of the vessel at right. C–D, Trichodiadema bulbosum Schwantes. C, transection of outer stem, showing numerous vascular increments embedded in a parenchymatous background of conjunctive tissue. Location of master cambium is indicated by pointers. D, transection of portion of outer stem to indicate location of vascular cambium (arrow) in a vascular increment and the rayless nature of the vascular increments. Pointers indicate location of master cambium. Scale bars, 50 mm (A, B, D); 20 mm (C).

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 353 required continual production of new cambia abaxi- closely related genera Calpidia Thouars, Guapira ally, but did not explain how such cambia could be Aubl. and Neea Ruiz & Pav. show the same pattern. produced without using up the cortical tissues (the These genera are distinctive in having vascular incre- idea of a secondary cortex did not occur to them). ments in a fibrous background of cells (= conjunctive Their hypothesized ontogenetic plan does not agree tissue), but they also have rays, which run through with observed histological reality, a flaw also found in the conjunctive tissue but are absent from the vascu- studies by other workers. lar increments. This pattern was pictured by Sol- ereder (1908), whose figure was reproduced by Metcalfe & Chalk (1950), but not explained for Rayless genera and species approximately a century. The Pisonia clade seems to Rayless Caryophyllales may appear to have vascular have arrived at a rayless condition (Heimerlioden- strands scattered within a background of non- dron, in that clade, is rayless), but then rays, distinc- conductive cells, either parenchyma, as in Trichodi- tively uniseriate or biseriate, have originated de novo adema Schwantes of Aizoaceae (Fig. 6C), or fibres in the master cambium (Fig. 6B). The vascular (Stayneria L.Bolus of Aizoaceae) or both fibres and cambia (Fig. 6A) do not produce rays, but apparently thin-walled parenchyma, as in Heimerliodendron they produce secondary xylem and secondary phloem, Skottsb. (Fig. 5D). The background tissue is a plus a few fibres that merge with those produced by product of the master cambium. When seen in tan- the master cambium. The background to the vascular gential section, there are no rays in these species increments does not consist wholly of fibres in Cal- (Fig. 5D). The vascular strands are randomly distrib- pidia, Guapira, Neea and Pisonia; parenchyma caps uted (Figs 5C, 6D); there are no radially continuous or strands surround the phloem of each vascular strips of parenchyma as in Bougainvillea (Fig. 5A). increment. These parenchymatous caps may allow for What might be mistaken for rays in the fibrous expansion of the secondary phloem, which conceivably strands in transections of Heimerliodendron (Fig. 5C) is produced over a period of years by each vascular are, in fact, merely the wider portions of fibres, which cambium (each cambium adds little secondary xylem, are storied. In rayless Caryophyllaceae, the master probably because the dense fibre background allows cambium produces vascular cambia at various sites for no addition of any more hard-walled cells). and, from each of these cambia, strands of secondary xylem and secondary phloem are produced. Second- Lianoid modifications ary growth is evident in them more in terms of Anredera A.Juss. (Basellaceae), a liana, has succes- secondary phloem, because arcs of dark-staining sive cambia in roots and stems, but not in tubers crushed phloem appear abaxially to newly formed (Carlquist, 1999d). The number of successive cambia phloem, as in Bougainvillea (Fig. 5C), Pisonia L. is small, perhaps only one cylinder outside the origi- (Fig. 6A) or Trichodiadema (Fig. 6D). nal vascular cylinder. Because the successive cambia Examples of rayless Caryophyllales with successive action is so limited, no master cambium forms; vas- cambia occur in many Nyctaginaceae (Carlquist, cular cambium occurs in the original cylinder and a 2004) and most Aizoaceae (Carlquist, 2007c). The second vascular cambium originates in the cortex, but chenopods Atriplex L., Eurotia Adans. and Grayia no master cambium may become a permanent Hook. & Arn. are rayless (Carlquist & Hoekman, feature. This pattern is shared by the lianas Anti- 1985), as are species of Hammada Iljin and Salsola L. gonon of Polygonaceae (Carlquist, 2003b) and Agdes- (Fahn, Werker & Baas, 1986). More are likely to be tis Moc. & Sessé ex DC. of Agdestidaceae (Carlquist, added to this list, which is in need of refinement. 1999b), differing only in their having somewhat wider Raylessness is correlated to some extent with gross rays. Bosea and Deeringia R.Br. (= Dendroportulaca appearance in transection: the vascular increments Eggli p.p.) of Amaranthaceae are upright but scan- are more likely to appear as scattered strands in dent when supporting branches of neighbouring trees rayless species, and more likely to appear in concen- are available; this is also true of Barbeuia Thou. of tric arcs in ray-bearing species with successive Barbeuiaceae (Carlquist, 1999c). These three genera cambia, as seen in transections. Aizoaceae may have more than three cylinders of vascular incre- contain more rayless species with successive cambia ments; they have master cambia and they have than the remainder of the list, although chenopods ray initials in the second and subsequent vascular would be second. Heimerliodendron is a tree, and may increments. be the largest plant with rayless secondary xylem. These lianoid members of Caryophyllales are not unusual except in having a somewhat elevated degree Reinvention of rays: Nyctaginaceae tribe Pisonieae of parenchymatization, although thickness of conjunc- The nature of secondary growth in Pisonia was exam- tive tissue bands is not notable in these genera. They ined in detail earlier (Carlquist, 2004, 2007a). The do exemplify, however, the tendency for lianas to have

fibre-sheathed cylinders containing vessels, a mecha- is important, because consistent presence of vestigial nism for protecting the integrity of vessels in case of scalariform perforation plates could be an important torsion (Carlquist, 1985a, 2009a). The successive character state in Caryophyllales. cambial plan, in fact, pre-adapts stems of Caryophyl- lales for the lianoid habit in many ways. Borders on perforation plates The commentary by Olson (2005) on wood features Storage and succulence modifications included an intriguing diagram, an idea which forms The number of Caryophyllaceae that have successive the basis for Figure 7. The concept that Olson cambia in roots (and thus rings of conjunctive tissue explored is character transformation, but he does not available for storage) is relatively large (Pfeiffer, use a specific plant group as an example. The clade in 1926), one indication that successive cambia form Figure 7 might include four lineages (other branch- successful plans in storage roots. Gypsophila L. and ings are omitted). Caryophyllales represent an ideal Silene L., however, lack successive cambia in roots, group, except for lack of scalariform perforation but have pervasive parenchyma (and thus an alter- plates (which presumably occurred in a family often native storage tissue) as a secondary xylem back- thought ancestral to Caryophyllales, Dilleniaceae: ground tissue in which the vessels are embedded. Cuénoud et al. (2002). The feature of special interest Scopulophila M.E.Jones (Caryophyllaceae) does have in the imaginary clade of Olson (2005), recreated here successive cambia, but vascular increments are few, in terms of Caryophyllales (Fig. 7), is the transforma- and no ongoing master cambia are formed (Carlquist, tion from bordered simple perforation plates to non- 1995). bordered simple perforation plates. In the chenopods, Beta has rays (and ray cambial The occurrence of non-bordered perforation plates, initials aligned with fusiform initials in vascular although visible with both light microscopy and SEM cambia); storage roots of the chenopod Atriplex semi- (Fig. 8), has not been generally appreciated by wood baccata R.Br. are similar (S. Carlquist, pers. observ.). anatomists. Non-bordered perforation plates are not Caryophyllales with storage roots that have succes- mentioned by Metcalfe & Chalk (1950) or the IAWA sive cambia and tend to show greater thickness of Committee (1989). There has been no baseline list of conjunctive tissue bands than do the stems. families with non-bordered perforation plates other than that of Carlquist (2001b). In Caryophyllales, Meylan & Butterfield (1978) presented an SEM pho- VESSEL ELEMENTS tograph of a non-bordered plate in Heimerliodendron Perforation plate types (Nyctaginaceae). A transmission electron micrograph Caryophyllales have exclusively simple perforation of such a plate was given by Fahn (1990: 112) for plates, with only the most minor exceptions. In Dianthus L. (Caryophyllaceae). Although I have primary xylem of Nepenthes, gyre tips that fringe the called attention to non-bordered perforation plates in perforation plate like teeth may be found (Fig. 8A). various families of Caryophyllales, no listing has been Multiple perforation plates (Fig. 8B) occur in second- compiled. Any such compilation is uncertain, because ary xylem of Nepenthes. Do these represent vestiges expressions of this character are more varied than of scalariform perforation plates? Multiple perforation one might at first expect. These expressions demon- plates also occur in Dionaea Ellis (Fig. 16A). Multiple strate the problem, illustrated in Figure 7, of perforation plates are not restricted to the non-core mapping successive character state changes (or even Caryophyllales. They have been reported in vessels of mapping any information onto a phylogenetic tree secondary xylem of Didiereaceae by Rauh & Dittmar based on molecular data. (1970). A rough approximation of the occurrence of this What is the difference between a scalariform per- character within Caryophyllales can be given, foration plate with one or two bars and a multiple however. Non-bordered perforation plates have been perforation plate? This question is not answered by reported in Achatocarpaceae (Carlquist, 2000b), the traditional literature of wood anatomy. The fol- Agdestidaceae (Carlquist, 1999b), Amaranthaceae lowing definition is offered. Scalariform perforation (Carlquist, 2003a), Barbeuiaceae (Carlquist, 1999c; plates with few bars tend to have perforations of Fig. 8D here), Basellaceae (Carlquist, 1999d), Dionco- similar size, separated by bars similar to each other phyllaceae (S. Carlquist, data original), Frankeniaceae in width. Multiple perforation plates have randomly (Fig. 8E, S. Carlquist, data original), Rhabdoden- placed perforations on an end wall; the perforations draceae (Carlquist, 2001a), Phytolaccaceae (Carlquist, are spaced so that they do not group as a ‘perforation 2000a), Polygonaceae (Carlquist, 2003b), Rivinaceae plate.’ Using this definition, the end walls of vessel (Monococcus), Jansen, et al., 2000; Trichostigma, Car- elements in Dionaea, Nepenthes and Didiereaceae lquist 2000b; Fig. 8F), Sarcobataceae (Carlquist, qualify as multiple perforation plates. This distinction 2000c), Simmondsiaceae (Carlquist, 2002; Fig. 8C) and

Figure 7. Generalized phylogenetic tree of selected Caryophyllales and a putative outgroup (Dilleniaceae) to indicate possible character state transformations in perforation plate morphology. Shaded areas indicate character states that are intermediate, ultimately emerging (non-shaded lines) as clearly deﬁned character states. Acquisition of simple perforation plates in Davilla has probably been accelerated because of the lianoid habit of that genus; Dillenia is non-lianoid and retains scalariform perforation plates. Modiﬁed from a drawing in Olson (2005).

Tamaricaceae (S. Carlquist, data original). The genus ration plates. In Figure 9D, one sees a non-bordered Portulacaria Jacq., which may be referable to perforation plate, but in Figure 9E, the perforation Didiereaceae rather than to Portulacaceae (Applequist plate is deﬁnitely bordered (curving double structure & Wallace, 2001) has non-bordered perforation plates. at the top of the photograph). Whether or not a perforation plate has borders can Original observations based on SEM include the usually be seen readily with light microscopy, although following. Lithops N.E.Br. (Aizoaceae) has bordered SEM gives more accurate images. perforation plates with rounded borders (Fig. 10A, Given that the above listing is incomplete, some taxa centre). As seen in face view, perforation plates of not listed might be expected to have bordered perfora- Dionaea of Droseraceae (Fig. 16A) have clearly delim- tion plates, at least to some degree. The borders of ited borders. Drosophyllum Link (Drosophyllaceae) Gypsophila plates are fused, but are blunt rather than has variously prominent borders (Fig. 16D–F). Nepen- sharp (Fig. 9A). The plate shown for Celosia (Fig. 9B) thes (Nepenthaceae) has bordered perforation plates, has a nearly non-bordered condition that becomes but the borders are rounded rather than sharp-edged clearly non-bordered at the top of the photograph. The (Fig. 17D). Asteropeia micrograph (Fig. 9C) shows a condition that New records for bordered plates based on light might be viewed as non-bordered with a light micro- microscopy include the families Anacampserotaceae scope, but which is vestigially bordered as seen with (bordered), Cactaceae (bordered, borders rounded in SEM. Two vessels from the same section of Eriogonum sectional view; vestigial in Rathbunia alamosensis giganteum S.Watson wood differ with respect to perfo- (J.M.Coult.) Britton & Rose), Portulacaceae (bor-

Figure 8. Perforation plate morphology in stems of Caryophyllales. A–B, Nepenthes rajah Hook. f. ¥ N. villosa Hook. f. (Nepenthaceae). A, protoxylem vessel element from maceration; perforation plate is oval, with two tooth-like intrusions of secondary wall material. B, vessel from tangential section of secondary xylem, showing multiple perforations. C, Simmondsia chinensis C.K.Schneid. (Simmondsiaceae); scanning electron microscopy (SEM) micrograph from tangential section, showing non-bordered perforation plate, above; helical thickenings present on vessel wall. D, Barbeuia mada- gascariensis Steud. (Barbeuiaceae); SEM of vessel from tangential section; two non-bordered perforation plates are seen in sectional view. E, Frankenia grandifolia Cham. & Schlect. (Frankeniaceae), SEM of non-bordered perforation plate from vessel. element, tangential section. F, Triplaris melanodendron (Bertol.) Standl. & Steyerm. (Polygonaceae), SEM of non-bordered perforation plate from tangential section. Scale bars, 5 mm (A–C); 5 mm (D–F).

Figure 9. Scanning electron microscopy (SEM) micrographs of perforation plates and adjacent wall portions, from tangential sections of secondary xylem. A, Gypsophila patrini Ser. (Caryophyllaceae), non-bordered perforation plates; vessel walls with pseudoscalariform pitting. B, Celosia ﬂoribunda A.Gray (Amaranthaceae), perforation plate non- bordered at top of photo, vestigially bordered below. C, Asteropeia micraster Hallier f. (Asteropeiaceae), vestigially bordered perforation plate. D–E, Eriogonum giganteum S.Watson (Polygonaceae). D, non-bordered perforation plate from wider vessel; ﬁne helical thickenings on wall. E, bordered perforation plate (top) from narrower vessel; arrows indicate borders on the helical thickenings. Scale bars, 10 mm (A); 5 mm (B–E).

Figure 10. Scanning electron microscopy (SEM) micrographs of secondary wall patterns in Caryophyllales. A, Lithops sp. (Aizoaceae). Pseudoscalariform pitting; bordered perforation plate with rounded edges at centre. B, portion of tangential section of Mammillaria mystax Mart. (Cactaceae) stem secondary xylem. The vessel, centre, has narrower helices than the vascular tracheids, left and right. C–E, Anacampseros marlothii Poelln. (Anacampserotaceae) stem. C, transection of secondary xylem portion, with relatively narrow helices on vessels, above, and a wide-helix idioblast, below. D, longisection of a primary xylem vessel, with narrow-band bordered helices. E, longisection of a wide-band idioblast with non-bordered gyres. Scale bars, 10 mm.

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 359 dered, some with rounded edges) and Talinaceae (bor- character is, and one is willing to deal with a char- dered with rounded edges). Hectorella (now included acter that may be variously expressed. in Portulacaceae: Applequist et al., 2006) has bor- There seems little question that Caryophyllales as dered plates. a whole have perforation plates less prominently bor- Although most families of Caryophyllales seem to dered than are the simple perforation plates of other be categorizable, two are heterogeneous with respect major eudicot families and orders that one could cite. to the character (observations based on light micros- The genetic basis for this character is unknown, and copy). For Caryophyllaceae, I record: Arenaria L. what its selective value might be is not apparent. (non-bordered, blunt), Dianthus (non-bordered, There are other wood characters such as this in their blunt), Gymnocarpos Forssk. (bordered), Polycarpaea variability of expression. Limiting wood anatomy only Lam. (bordered, rounded), and Schiedea A.Rich. (bor- to characters that are easily seen and can be given dered, vestigial, blunt). The species studied are the binary designations, and which can therefore be con- same as those listed in Carlquist (1995). For Plum- fidently presented in a glossary, does not seem advis- baginaceae, I observed: Aegialitis (bordered, but not able. Other characters, discussed below, form prominently), Armeria Willd. (vestigially bordered to patterns other than 0/1 types of expression, and must non-bordered), Ceratostigma Bunge (bordered and be considered before we can develop ways of recording non-bordered) Limonium Mill. (bordered to non- wood anatomy that conform to new definitions. bordered); Plumbago L. (non-bordered) (species as in Carlquist & Boggs, 1996). One can see in Cera- Constricted perforation plates tostigma that bordered perforation plates character- This somewhat awkward term is used here to ize the perforations of a particular vessel, whereas describe vessel element end walls in which a perfo- non-bordered perforation plates can characterize ration plate occupies only part of an end wall. In such nearby similar vessels. a vessel, a marked constriction in the vessel contour If one looks at Santalales, often thought to be close appears in a longisection where the end wall is. to the origin of Caryophyllales (Fig. 1), materials Dionaea of Droseraceae (Fig. 16A) has this condition. viewed by light microscopy include Loranthaceae A similar end wall is figured by Gregory (1998) for [Amyema Tiegh. (bordered); Lasionema D.Don (non- Drosera slackii Cheek. Perforation plates of Droso- bordered); Nuytsia (bordered, rounded); Psittacan- phyllum are typically much narrower than the diam- thus Mart. (bordered, sharp)], Olacaceae (Olax L.) eter of the vessel in which they occur (Fig. 16D–F). non-bordered; Opiliaceae (Opilia Roxb., non- This feature is not unique to Droseraceae and Droso- bordered), Santalaceae [Acanthosyris Griseb. (non- phyllaceae, in both of which it is characteristic, and it bordered); Exocarpos Labill. (bordered, vestigial), may occasionally be seen in various vessel-bearing Iodesia Chiov. (bordered, vestigial), Phoradendron families. Unfortunately, no comparative data for this Nutt. (bordered, vestigial), Santalum L. (bordered)]. condition has been accumulated. Constricted perfora- All simple perforation plates in Dilleniaceae are tion plates are not equivalent to fibriform vessel bordered. elements. The latter have fusiform shape and The inconstancy of this character may seem strik- perforations plates borne laterally rather than termi- ing, but large taxonomic groups seem uniform (e.g. in nally. Constricted perforation plates might be a way Cactaceae, all species examined have bordered perfo- of restricting air bubbles to a particular vessel ration plates). In some large families outside Caryo- element or series of vessel elements, disabling shorter phyllales, bordered simple perforation plates may be distances within vessels (see Carlquist, 2001b, Figs 3, universal: in members of Asteraceae, in which I have 11, 12). In this construct, constricted perforation examined longitudinal sections of vessels, I have plates could have a selective value where flow rates noted only bordered perforation plates. If one com- are not rapid. Scalariform perforation plates, espe- pares the distribution of bordered and non-bordered cially those with pit membrane remnants, have a perforation plate presence to the phylogenetic tree of restrictive effect on flow rates: more bars decrease Figure 1, and takes a binary viewpoint, one might flow rates (Ellerby & Ennos, 1993), and marked con- posit a reversion to bordered perforations from non- strictions of perforation plates, which also decrease bordered ones in such groups as the Cactaceae– end wall area, doubtless act similarly. Multiple per- Portulacaceae clade. In this interpretation, the foration plates and fibriform vessel elements have not early-diverging clades of Caryophyllales (Rhabdoden- yet been subjected to experimental studies. Likewise, draceae, Ancistrocladaceae–Dioncophyllaceae, Sim- the effect of bars on perforation plates to reduce flow mondsiaceae and Stegnospermataceae) would have rates can increase with increased flow velocity (A. C. non-bordered perforation plates as a symplesiomor- Gibson, pers. comm.), but models that incorporate phy. This is a possible interpretation, but only if one various flow rates for various types of angiosperm is not demanding about how clearly definable the vessels are not yet at hand.

Figure 11. Scanning electron microscopy (SEM) micrographs of vesturing related to pits in vessels of Polygonaceae, from wood longisections. A, Atraphaxis frutescens (L.) K.Koch. Vesturing in centres of pit cavities, seen from outside of a vessel (pit membranes removed). B–C, Rumex frutescens Thouars. Vesturing in pseudoscalariform pits. B, View from inner surface of vessel. C, view from outside of vessel. D, Ruprechtia sp. Vesturing extends to a moderate degree from pit aperture onto inside surface of vessel. E, Triplaris surinamensis Cham. Vesturing extends extensively from pit aperture onto inner surface of vessel. Scale bars, 5 mm.

Figure 12. Wood sections of Caryophyllales. A, Cereus peruvianus (L.) Mill. (Cactaceae). Tangential section to show cell types as seen in a tangential section (nsf, narrow septate fibres; wst, wide septate fibres; urc, upright ray cell). B, Trichocereus spachianus Riccob. (Cactaceae). Radial section. Procumbent cells (left) and upright cells) occur in the same file, the shape difference related to degree of radial elongation during growth cycles. C, Asteropeia rhopaloides Baill. (Asteropeiaceae). Transection, illustrating axial parenchyma patterns (abax, abaxial; d, diffuse). D, Achatocarpus praecox Griseb. (Achatocarpaceae). Tangential section. Rays have mostly procumbent cells; axial parenchyma strands near vessels are composed of three cells each. Scale bars, 20 mm (A–C); 50 mm (D).

LATERAL WALLS OF VESSELS fers that are moist throughout the year, although soil surfaces where Tamaricaceae grow are often dry. Helical sculpture Similar considerations apply to the clade that ‘Helical thickenings’ in vessels are a structural char- includes Basellaceae, Cactaceae, Didiereaceae, Portu- acteristic common in angiosperm wood. In fact, the lacaceae and allied families. These are all succulent term as currently applied can be misleading, because to some degree and thus have relatively mesophytic it covers only a part of what can, more inclusively, be wood features. All of the families in this clade lack termed helical sculpturing. helical sculpture in secondary xylem vessels. Helical Helical thickenings are indeed present on the inner thickenings are one form of wall sculpturing that has surfaces of vessel walls of some Caryophyllales been shown to be related to wettability by Kohonen & illustrated here, such as Simmondsia (Fig. 8C) and Helland (2009). Presence of such forms of relief in Eriogonum (Fig. 9D–E). There are many other wood of non-succulent plants, and absence in succu- examplies, such as Muehlenbeckia Meisn. (Carlquist, lent plants, is therefore to be expected. 2003b), Sarcobatus Nees (Carlquist, 2000c) and The inner surfaces of vessels of Scopulophila several Plumbaginaceae (Carlquist & Boggs, 1996). M.E.Jones of Caryophyllaceae (Fig. 9A) or Lithops of Bordered helical thickenings (Fig. 9E) are a phenom- Aizoaceae (Fig. 10A) are not related to helical sclup- enon reported here for the first time. ture, but represent a phenomenon called pseudosca- Grooves interconnecting or widening pit apertures lariform pitting (Carlquist, 2001b). Scalariform are another form of helical sculpturing. They are pitting, as seen in fern tracheids or in metaxylem of well illustrated by Trichostigma (Carlquist, 2000a), a many species of angiosperms, consists of laterally genus which should probably now be placed in Rivi- wide pits, the lengths of which are confined to, and naceae, and by Rhabdodendraceae (Carlquist, correspond to, a cell facet Pseudoscalariform pitting 2001a). These grooves are sometimes termed coales- consists of laterally wide pits, some of which may cent pit apertures, but such grooves are often found extend from one cell facet onto another. Pseudosca- on isolated pits and therefore the pit apertures do lariform pits may be regarded as a modification of not coalesce. They are illustrated here for Stegno- alternate pitting, or an extreme expression of it. Pseu- sperma (Fig. 4C) and Trichostigma (Fig. 8F). Species doscalariform pits are common in vessels of succulent with grooves adjacent to pit apertures may also Caryophyllales. Vessels with pseudoscalariform simultaneously have thickenings on the margins of pitting usually do not form in groups, but are com- the grooves, as in Sarcobatus (Carlquist, 2000c) and monly separated from each other by parenchyma some species of Eriogonum (Carlquist, 2003b). This cells, as in Dianthus and Silene of Caryophyllaceae feature, first mentioned many years ago (Carlquist, (Carlquist, 1995), a possible compromise between wall 1958a, b) is common in woods of Asteraceae and strength and flexibility discussed in the Conclusions other families (Clematis L. of Ranunculaceae: But- section. terfield & Meylan, 1980). It has not yet entered lexi- Cacti such as Acanthocereus (Engelm. ex A.Berger) cons of terms used to describe woods, however. So Britton & Rose and Mediocactus Britton & Rose have far, no comprehensive terminology has been pro- wide, ‘gaping’ pit apertures. Such pits can also be posed for types of helical sculpture, perhaps because found in other succulent genera from this clade, such the kinds encountered are so manifold and seem in as Cistanthe Spach (Carlquist, 1998a). The wide-band some species to intergrade. Vessel wall sculpturing annular and helical vascular tracheids of globular can be accurately characterized in most species with cacti (Fig. 10B) represent an ultimate compromise a few words. between wall strength (sufficient to maintain the cell There is, however, a correlation between helical shape) and ability to contract and expand with chang- sculpture on vessel walls and ecology in eudicots at ing water availability. Such cells also occur as idio- large (Carlquist, 1975; Carlquist & Hoekman, 1985). blasts in rays of certain Anacampserotaceae ‘Ecology’ cannot be interpreted in terms of rainfall, (Fig. 10C, top; Fig. 10D). Wall configurations of but in terms of the water economy within individual vessels in cacti may be similar, but with narrower species. Shrubs that survive long dry seasons (Polygo- bands (Fig. 10B; see also Metcalfe & Chalk, 1950: naceae, Sarcobataceae, chenopods) obviously qualify. fig. 161). Such vessels are common in Hectorella Shrubby Plumbaginaceae, which grow in places that Hook. f. and Lewisia Pursh of Portulacaceae (Car- are both salty and seasonally dry, have helical sculp- lquist, 1998a). In cacti, such vessels are considered to turing. However, Tamaricaceae, which grow in ‘desert’ be paedomorphic, because all cacti have them in locations, do not have helical thickenings (Fahn et al., earlier formed xylem, but they are also present in 1986). This fact is explainable by the characteristic later-formed secondary xylem in globular cacti, and habitat of Tamaricaceae: these shrubs or trees tap intermediate degrees of distribution occur (Mauseth subsurface aquifers that are saline or brackish, aqui- & Plemons, 1995; Mauseth, 1999, 2004).

Distinctive wall bands are present in the metaxy- (Nepenthaceae, etc.) and the branch leading to ‘core lem of Dionaea Ellis of Droseraceae (Fig. 16C). These Caryophyllales.’ bands are approximately half the width and twice as numerous as protoxylem helices (also present in the Vessel grouping same sections). Metaxylem vessels with these bands In a phylogenetic sense, vessel grouping is deterred have simple perforation plates surrounded by a non- by presence in a wood of a ground tissue composed of banded secondary wall, and thus are unlike perfora- tracheids (Carlquist, 1984). A tracheid background tion plates usually seen in primary xylem vessels. occurs in Barbeuiaceae (Carlquist, 1999c), Caryophyl- These bands need further study. laceae tribe Paronychieae Dumort., Nepenthaceae (Carlquist, 1981), Rhabdodendraceae (Fig. 3), Sim- mondsiaceae (Carlquist, 2002) and Stegnospermata- Vestured pits and vesturing ceae (Fig. 4). In all of these, vessels are solitary or The systematic occurrence and diverse appearances of nearly so, validating that hypothesis. A similar con- vesturing in Caryophyllales make this feature prob- sideration may apply to the solitary vessels of Aster- lematic. Vestured pits in vessel walls have been opeiaceae and Physenaceae (Carlquist, 2006), the reported for Rhabdodendraceae (Fig. 3; Carlquist, vessels of which are associated with vasicentric 2001a) and Polygonaceae (Fig. 11; Carlquist, 2003b). tracheids. In Polygonaceae, ‘typical’ vestured pits have wart-like In other families of Caryophyllales, various degrees or coralloid complexes in the centre of a pit cavity, as of vessel grouping may be found. These degrees in Atraphaxis L. (Fig. 11A) and Coccoloba P.Browne acquire significance when put into an ecological (Carlquist, 2003b). The pit cavities of these two context and when compared with vessel grouping in genera are circular to polygonal in outline. The pits other families of eudicots. in Rumex L. (Fig. 11B, C), Ruprechtia C.A.Mey. (Fig. 11D), and Triplaris Loefl. (Fig. 11E) are moder- Vesssel localization ately (Fig. 11D) to markedly (Fig. 11B–E) laterally Distinctive patterns of vessel localization have been elongate (the latter an example of a pseudoscalari- noted for particular eudicot woods (Carlquist, 2009a). form pattern). The vesturing of vessels of Ruprechtia Vessels that are surrounded by fibres, and thus do not and Triplaris is much more abundant than in the abut directly on any ray cells, may be found in Anti- other genera, extending well onto the inner surfaces. gonon Endl., Muehlenbeckia Meisn and Polygonum L. Vesturing of this type has not often been reported, of Polygonaceae (Carlquist, 2003b); Aegialitis R.Br. of because it is not visible with light microscopy, Plumbaginaceae (Carlquist & Boggs, 1996); Anredera although the type of vestured pits seen in Atraphaxis Juss. of Basellaceae (Carlquist, 1999d); an amaranth, can be detected with light microscopy. Vesturing is Charpentiera Gaudich. (Carlquist, 2003a); the cheno- probably much more widespread in Polygonaceae pods Beta L and Chenopodium L.; and Triphyophyl- than has been hitherto reported. Polygonaceae are a lum Airy Shaw of Dioncophyllaceae (Fig. 21A). large family and, because most species are not mark- In contrast, more nearly random patterns of vessel edly woody, they remain uninvestigated with respect grouping (some vessels in contact with ray cells) may to any wood features. be seen here in the case of cacti; Fig. 13A, D). Pat- Vesturing on vessel walls and in vessel pits of terns such as those shown here for cacti, in fact, Caryophyllales has mostly been reported now, at least characterize the majority of Caryophyllales. at the familial levels, thanks to the surveys of Jansen, Smets & Baas (1989) and Jansen, Baas & Smets IMPERFORATE TRACHEARY ELEMENTS (2001). The pattern of systematic distribution within Tracheids Caryophyllales might suggest that vestured pits are a The tracheid is the background wood cell type in symplesiomorphy in the order, because of their pres- Barbeuia Thou. (Carlquist, 1999c), Dioncophyllaceae ence in Rhabdodendraceae, sister to the remainder of (Fig. 21B), Nepenthes L. (Fig. 17B), Rhabdodendron Caryophyllales. However, vesturing is not reported Gilg & Pilg. (Fig. 3D), Simmondsia Nutt. (Carlquist, from any of the families of Santalales (Jansen et al., 2002) and Stegnosperma Benth. (Fig. 4C, lower right). 1989) or Dilleniales, which appear to be early Paronychioid Caryophyllaceae such as Gymnocarpos branches in the clade leading to Caryophyllales Forssk. have tracheids (Carlquist, 1995), but other according to the hypothesis of Cuénoud et al. (2002), tribes of Caryophyllaceae have libriform fibres or whose phylogenetic trees form the primary basis for pervasive parenchyma as a background tissue. Figure 1. If vesturing is a symplesiomorphy for Caryophyllales, one must imagine loss of vesturing in Vasicentric tracheids the Plumbaginaceae clade, the Tamaricaceae– Fibre-tracheids, together with vasicentric tra- Frankeniaceae clade, the insectivorous clade cheids, characterize Ancistrocladaceae (Fig. 19B, C),

Figure 13. Wood sections of Cactaceae. A, Pereskia aculeata Mill. Transection to show growth ring (ew, earlywood; lw, latewood); axial parenchyma is paratracheal. B, Rathbunia alamosensis Britton & Rose. Tangential section to show that rays are multiseriate only, composed of upright, square and procumbent cells in approximately equal numbers. C, Pereskia aculeata. Radial section. Ray cells contain starch, evidence by black hila (= air spaces attributable to microtechnical dehydration). D, Opuntia kleiniae DC. Transection of base of plant to show growth ring; vessels are in prominent groupings, narrow in latewood, associated with paratracheal parenchyma. Scale bars, 50 mm (A, B, D); 20 mm (C).

Asteropeiaceae, Frankeniaceae and Physenaceae. like and fibre-like cells in Bougainvillea takes the Although most Frankeniaceae have libriform fibres form of bands, patches and other types of groupings. (along with narrow vessels, Fig. 15). Hypericopsis Heimerliodendron (Fig. 5C, D) has conjunctive Boiss. has a few vasicentric tracheids in addition to tissue differentiated into fibrous bands (which contain libriform fibres (Olson, Gaskin & Ghahremani-nejad, strands of vascular increments) alternating with 2003). parenchyma. In Pisonia, prosenchymatous conjuctive More instances in Caryophyllales of imperforate tissue forms sheaths (‘caps’ in transectional view) tracheary elements with bordered pits are likely to be around the phloem poles of the vascular increments found, but the preponderance of the order has libri- (Fig. 6A, 6B, left), whereas the remainder of the conform fibres in secondary xylem. Libriform fibres, junctive tissue in which the vascular increments are however, are diverse. Vestigial borders may be found embedded is fibrous (Fig. 6A, B). This is also true in on pits of imperforate tracheary elements. One must other genera of tribe Pisonieae (Neea, Guapira, etc.). keep in mind that fibres may be derived either from Some Caryophyllales have conjunctive tissue com- a vascular cambium as in Bougainvillea (Fig. 5B), or posed wholly of parenchyma, as in Trichodiadema of a master cambium, as in Heimerliodendron, or both, Aizoaceae (Fig. 6C, D). Some have conjunctive tissue as in Pisonieae other than Heimerliodendron. This composed wholly of fibres, as in Stayneria (Carlquist, seeming paradox is the only logical way to explain the 2007b). Some Aizoaceae have alternating concentric origins of fibrous tissue in the stems of tribe Pisonieae fibre and parenchyma bands, as in Aptenia N.E.Br. (Carlquist, 2004). These various conjunctive tissue plans relate to succulence, mechanical strength and flexibility. Fibre dimorphism The Cactaceae–Portulacaceae clade illustrates diver- AXIAL PARENCHYMA sification of libriform fibres within Caryophyllales. Fibre dimorphism and conjunctive tissue form two The most obvious shift is to living fibres, which are sources of parenchymatization in stems of roots of probably common in families of this clade (although Caryophyllales. However, axial parenchyma in the sampling is still limited). Cereus peruvianus (L.) Mill. ordinary sense (strands of cells, horizontally subdi- (Fig. 12A) has narrow septate fibres and wide, living vided) is also present in the order. In the early- septate fibres. Upright ray cells, common in cacti, are diverging branches of the clade, diffuse parenchyma sometimes difficult to distinguish from wider living is present, as in Rhabdodendron (Fig. 3C, D), Sim- fibres (Figs 12A, 13B) and suggest continuity in func- mondsia (Carlquist, 2002), Stegnosperma (Carlquist, tion and morphology between fibres and ray cells in 1999a), Nepenthaceae (Carlquist, 1981) and parony- cacti (both are unusually rich in starch in cacti: chioid Carophyllaceae such as Gymnocarpos (Car- Fig. 13C). This has also been reported in Didiereaceae lquist, 1995). All of these except for Simmondsia have (Rauh & Dittmar, 1970). some other type of axial parenchyma distribution as In addition, Portulacaceae and cacti exhibit what well: scanty vasicentric in Rhabdodendron (Fig. 3C); can be called a form of fibre dimorphism, a concept marginal and vasicentric in Gymnocarpos; abaxial or which originated long ago (Carlquist, 1958a, b, 1961: abaxial–confluent in Asteropeia (Fig. 12C); tangential 50). In this phenomenon, patches of fibres have wider bands of a few cells in Nepenthes (Carlquist, 1981); diameter, shorter length, living contents and thinner and in short strands (two to four cells) in Stegno- (but not always non-lignified) walls. Such a combina- sperma (Horak, 1981). Short radial chains, although tion of the two cell types has been reported in certain an unusual axial parenchyma distribution, were con- cacti (Gibson, 1977b; Mauseth, 1999; Melo-de-Pinna, firmed in my material because of the presence of 2009). starch and the two-celled nature of axial parenchyma In some cacti, the polymorphism is even greater, strands as seen in radial sections (S. Carlquist, origi- attributable to the inclusion of wide-banded tracheids nal observations). The predominant type of axial instead of ordinary vessels (Mauseth & Plemons, parenchyma distribution in woods of Caryophyl- 1995). The wide-band tracheids have been termed laceae, however, is scanty vasicentric (scanty paratra- vascular tracheids. In cacti, the vessels have appre- cheal), as shown for Rhabdodendron (Fig. 3C, D). ciably narrower bands than the tracheids (Fig. 10B). Tamaricaceae have abundant paratracheal (Fahn et al., 1986; Carlquist, 2001b) and is shown here Conjunctive tissue dimorphism (Fig. 14A, C). Banded apotracheal characterises Fibre dimorphism can be seen readily in Bougainvil- Ancistrocladaceae (Fig. 19A). lea (Fig. 5A, D). In the roots of Bougainvillea, starch- As seen in longitudinal sections, axial parenchyma rich fibriform cells are more common than in the ranges from a single cells in Frankenia (Fig. 13C, E) stems (Carlquist, 2004). The mixture of parenchyma- and one or two cells in Tamaricaceae (Fig. 14B, C)

Figure 14. Wood sections of Tamaricaceae. A, Tamarix articulata Wall. Transection. Vessels are mostly solitary, axial parenchyma is paratracheal abundant (r, ray). B, T. aphylla (L.) H.Karst. Tangential section. Rays are all multiseriate, Homogeneous Type II. Axial parenchyma cells (ap) are in strands of two or not subdivided. C, T. aphylla. Tangential section to show ray (r) with crystals (arrows, c) at lateral ray margins. Axial parenchyma (not subdivided) at right. D, T. aphylla. Radial section, showing rhomboidal crystals (some black, some grey) in the sheathing cells. E, Reaumuria hirtella Jaub. & Spach. Tangential section of juvenile stem; one biseriate ray, cells mostly upright. Scale bars, 50 mm (A,B); 20 mm (C–E).

Figure 15. Wood sections of Frankeniaceae. A–C, Frankenia palmeri S.Watson. A, transection. Latewood in lower third of picture, earlywood above, vessels in extensive groups. B, latewood (lower half) contains narrow vessels and a few vasicentric tracheids; earlywood (above) contains vessels and libriform ﬁbres. C, tangential section; wood is rayless; some axial parenchyma cells contain chains of rhomboidal crystals. D–E, Frankenia grandifolia Cham. & Schlecht. D, transection. A pair of rays runs the vertical length of the photo, each between the letter ‘r’ at the top and the ‘r’ at the bottom; rays are indistinct because cell diameter and staining are similar in transection to the libriform ﬁbres. E, tangential section. A ray, top and bottom approximately indicated by arrows, at left. Scale bars, 60 mm (A, C, D, F); 20 mm (B).

Figure 16. Scanning electron microscopy (SEM) photographs of stem vessel elements of Droseraceae and Drosophyl- laceae. A–C, Dionaea muscipula J.Ellis, hand sections of liquid-preserved material. A, tip of vessel element. Double perforation, showing borders. B, tips of two vessel elements. Pits are pseudoscalariform, narrowly bordered. C, pseudoscalariform pitting, seen from inside of vessel elements. A ﬁne reticulum is seen on the pit membranes. D–F, Drosophyllum lusitanicum (L.) Kink, perforation plates from microtomed sections. D, bordered simple perforation plate. E, vestigially bordered simple perforation plate. F, bordered perforation plate that occupies only a small portion of the end-wall contact area (‘constricted perforation plate’). Scale bars, 10 mm (A, B, D, E); 5 mm (C, F).

Figure 17. Wood of stem secondary xylem of Nepenthes alata Blanco (Nepenthaceae). A, scanning electron microscopy (SEM) micrograph of transection. A patch of axial parenchyma (ap) at upper right; another similar patch near centre. A multiseriate ray abrupt in origin is at top, centre; the remainder of the ground tissue is composed of ﬁbriform cells (tracheids, fx). B–D, SEM micrographs. B, outer surface of tracheid, pits are large and bordered. C, inner surface of vessel element in transection, viewed obliquely; wall microstructure shows helical pattern. D, bordered perforation plate from tangential section. Scale bars, 100 mm (A); 5 mm (B); 10 mm (C, D).

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 370 S. CARLQUIST and Plumbaginaceae (Carlquist & Boggs, 1996) to of their using twig material from herbarium speci- three to six cells in Ancistrocladaceae and five to ten mens for their studies instead of more mature cells in Dioncophyllaceae (S. Carlquist, original data). samples. Uniseriate to triseriate rays (Paedomorphic The predominant length of axial parenchyma strands Type I) occur in Dioncophyllaceae (Gottwald & in Caryophyllales is two cells. Parameswaran, 1968; S. Carlquist, original data). Drosophyllaceae have uniseriate rays only, Paedomor- phic Type III (Carlquist & Wilson, 1995). VASCULAR RAYS The salt-gland families, Frankeniaceae and Tama- Caryophyllales are unusual in the diversity of ray ricaceae, are markedly different in ray histology. anatomy represented (for illustrations of ray types Reaumeria hirtella Jaub. & Spach (Tamaricaceae) has mentioned here, see Carlquist, 2001b, or Carlquist, uniseriate and biseriate rays composed of upright, 2009a). The type claimed to be primitive for procumbent and square cells (Fahn et al., 1986), but angiospermous wood by Kribs (1935), Heterogeneous in immature specimens, only upright cells are present Type I, has not been reported in the order. However, (Fig. 14E). Tamarix is radically different from Heterogeneous Type IIA, seen in Rhabdodendron Reaumeria in having multiseriate rays composed (Fig. 4B), is close to Type I. Achatocarpaceae wholly of procumbent cells (Fig. 14A–D) in all species (Fig. 12D) have Heterogeneous Type IIB (Carlquist, (Fahn et al., 1986). 2000b). Asteropeia and Physena have Homogeneous Shifts in radial outlines of ray cells related to Type III rays (Carlquist, 2006), in which rays are seasonality can be seen in Cactaceae. At the ends of uniseriate and are composed of procumbent cells. growth rings, cell elongation in a radial direction may Those who think in terms of the Kribs ray types slow, resulting in more upright cells (Fig. 12B). Ray will be surprised to find that in most Caryophyllales, cells in cacti are often filled with starch, as are the rays are paedomorphic: upright cells outnumber proc- living fibres (Fig. 13C). The abundant storage of umbent cells or are present exclusively. Simmondsia starch in these tissues is doubtless for seasonal mobi- has Paedomorphic Type I rays, as does Stegnosperma lization for flowering and growth. However, there is (Carlquist, 1999b). In the ‘core Caryophyllales,’ espe- no evidence for rapid mobilization of sugars from cially in the Portulacaceae–Cactaceae clade, one can starch, as in deciduous woody trees. Rather, both identify a trend toward loss of uniseriate rays com- water and starch storage may be suspected in the bined with presence of wide multiseriate rays particularly massive rays of cacti. (Fig. 13B). Uniseriate rays are common in Rivinaceae Frankeniaceae are reported to be rayless (Whalen, and one genus (Anisomeria) of Phytolaccaceae s.s. 1987). Olson et al. (2003) claim rayless woods for (Jansen et al., 2000; Carlquist, 2000a). The rays of all Hypericopsis persica Boiss. (= Frankenia persica Phytolaccaceae and Rivinaceae are paedomorphic Jaub. & Spach), but illustrated ‘ray-like plates of (Type I, because both uniseriate and multiseriate rays axial parenchyma’. I have been able to examine are present). The rays of Gymnocarpos and Polycar- Olson’s slides of roots of this species and would term paea of the paronychioid Caryophyllaceae are the ‘plates’ rays. Likewise, rays that extend from pith uniseriate and composed of upright ray cells to cambium can be found in Frankenia grandifolia (Paedomorphic Type III), whereas alsinoid and caryo- Cham. & Schltdl. (Fig. 15C, D), but not in other phylloid (silenoid) Caryophyllaceae (Harbaugh et al., species. The fact that these apparent rays are com- 2010) exhibit raylessness. Raylessness, an expression posed of upright cells similar in vertical length to of juvenilism, is common in the core Caryophyllales axial parenchyma cells makes them difficult to iden- (Fig. 2). tify in tangential section (Fig. 15E; limits of ray as In the other (‘non-core’) clade of Caryophyllales, indicated by arrows are arguable). Such transitions the ray type seen in Rhabdodendraceae (Heteroge- between raylessness and vaguely definable rays com- neous Type IIA) is probably a symplesiomorphy. posed of upright cells are exactly what one would Such rays occur in an old stem of Nepenthes alata expect as a stem or root grows in diameter and shifts Blanco (S. Carlquist, original data); earlier reports from a rayless condition to a ray-bearing condition, a on Nepenthes wood dealt with somewhat narrower transition noted by Barghoorn (1941b) in cases of stems; the narrowness of multiseriate rays and raylessness in other angiosperm families. greater abundance of upright cells are indicative of The diversity of rays in Polygonaceae is great (Car- prolonged juvenilism. lquist, 2003b). All ray types except for Heterogeneous Rays similar to those reported for Nepenthes (Car- I and Homogeneous II have been reported, suggesting lquist, 1981) can be found in Ancistrocladus tectorius that this family is a plexus for diversification in ray (Lour.) Merr. (S. Carlquist, original data). Paucity of types, a pattern often associated with diversification multiseriate rays, claimed for Ancistrocladus by Got- in habit and degree of juvenilism within a family twald & Parameswaran (1968), is probably the result (Carlquist, 2009b).

Amaranths and chenopods have offered difficulties tissue, showing hard and soft tissues equally well) with respect to definition of rays (Carlquist, 2003a). now permit us to make distinctions that were not Rajput (2002) reported raylessness in Amaran- possible when dried samples involving successive thaceae. However, ray initials in vascular cambia are cambia, often sectioned with only moderate success, tangentially in line with fusiform initials (the normal were the basis for studies. condition for ray-bearing species) in Amaranthaceae, given appropriate stem transections. My observations indicate that, with respect to ontogeny, rays in Ama- ‘NEORAYS’ ranthaceae are not markedly different from those in The ‘reinvention’ of rays, narrow and produced from a Stegnospermataceae (Fig. 4A, B), although rays in master cambium, in tribe Pisonieae is a special phe- Stegnosperma are not as wide. Amaranths can be said nomenon that is confined to that tribe as far as is to have wider, more localized rays (or ray-like sheets known. This phenomenon, shown here for Pisonia of parenchyma). Some have used the term ‘radial (Fig. 6A, B), has been described in detail earlier (Car- plates of conjunctive tissue’ for rays in Bougainvillea lquist, 2004, 2007a) for Pisonia and allied genera. (Metcalfe & Chalk, 1950). In chenopods, Fahn et al. These ‘neorays’ originate clearly from the master (1986) described rays of particular species in diverse cambium, whereas secondary phloem and secondary terms: ‘rays typically absent, but some narrow to xylem (both rayless in Pisonieae) develop from vas- broad (up to ten cells wide), radial parts of conjunc- cular cambia. The fibrous conjunctive tissue of Piso- tive parenchyma tending to have ray-like structure’ nieae develops from the master cambium, although a (Atriplex halimus L.); ‘rays absent or indistinguish- few fibres close to vessels may be traced to vascular able from strips of conjunctive parenchyma’ (Salsola cambia also. baryosma (Roem. & Schult.) Dandy); ‘rays uncommon, 1–3 seriate’ (S. tetrandra Forsk.); ‘rays vaguely delim- ited from radial strips of conjunctive parenchyma, RAYLESSNESS 1–10 seriate (Seidlitzia rosmarinum Bge.); ‘rays Although Figure 2 is devoted primarily to showing absent’ (Halogeton alopecuroides Del.) Moq., Haloge- instances of the occurrence of successive cambia in ton persicum Bge., Hammada negevensis Iljin & Zoh., Caryophyllales, the lettering also indicates occur- H. salicornia (Moq.) Iljin, H. scoparia (Ponel) Iljin, rences of raylessness. The abundance of both trends is and Noaea mucronata (Forsk.) Aschers & Schweinf. unparalleled elsewhere in eudicots, but raylessness The above observations are accurate descriptions of has not hitherto been appreciated. The difficulty in what these workers saw. They underline the uncer- defining rays cannot be equated with instances of tainties of categorizing rays in the Amaranthaceae s.l. successive cambial occurrence. For example, Metcalfe based on mature structure. I suggest that when one & Chalk (1950) reported raylessness for all Amaran- can find ray initials tangentially aligned with other thaceae except Charpentiera, whereas Rajput (2002) vascular cambium cells in a vascular cambium in considered all amaranths rayless. In fact, there are amaranths or chenopods, a ray, even if wide, can be parenchymatous radial bands between vascular incre- said to be present. This assumes that, in addition to ment segments in Charpentiera, but some portions of the successive vascular cambia, there is a master those bands bear secondary walls (Carlquist, 2003a) cambium to the outside. (Fig. 1 in Carlquist, 2009b, a The amaranth Bosea has stem structure similar to figure based on Stegnosperma, Fig. 4A, B here). If that of Charpentiera, differing merely in the lack of only a master cambium can be found, and no ray sclerenchyma in the rays or radial parenchyma initials are present alongside fusiform cambium ini- bands. Correlations with habit and ecology are to be tials in the vascular cambia, then rays can be said to sought, as indicated below. In fact, ray initials may be be absent and vascular increments are then embed- found in vascular cambia of Amaranthus caudatus L. ded in a background of conjunctive tissue, as in Tri- (Carlquist, 2003a), just as clearly visible as those of chodiadema (Fig. 6C, D). Establishing ray presence Stegnosperma (Fig. 4A, B). on what may seem subtle ontogenetic grounds may The phenomenon of raylessness occurs when fusi- seem impracticable, but the differences between form cambial initials are short, but when ray initials perisperm and endosperm or other structural distinc- are vertically long, an indication of a juvenile conditions one could cite are no less important or more tion, paedomorphosis (Carlquist, 1970), one form of elusive. The distinction between rays and radial heterochrony (Carlquist, 2009b). Thus, ray initials plates of conjunctive tissue should not be based solely are approximately the same vertical length as fusi- on assessment of mature tissues. In fact, ontogeny is form initials and fibres are formed in ‘potential’ ray revealed by sequence and placement of products as areas. Horizontal subdivision, over time, of initials in well as by developmental stages. Certainly, better the cambium of ‘potential’ ray areas leads to vertically methods of preparation (sections of liquid-preserved shorter initials that can be termed ray initials; rays

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 372 S. CARLQUIST thus can be said to be present (Barghoorn, 1941b). (e.g. Trichodiadema Fig. 6C, D) instead of concentric Although Caryophyllales may well contain more rings of vascular increments (as in Beta) is possible rayless species than any other order of eudicots, no when there is no continuity of vascular cambia species belonging to the order are mentioned in Barg- around the stem. If rays do not exist, as in Trichodi- hoorn’s (1941b) account. The field of wood anatomy adema, vascular increments can take the form of was, at that time, still so skewed in favour of ‘truly strands that are be dispersed in various ways. This woody’ species that modes of xylary structure charac- does not mean, however, that concentric rings are teristic of non-woody or less woody eudicots made few lost in all rayless species. In fact, Heimerliodendron appearances in the literature. Certainly Caryophylla- (Fig. 5C), which is rayless, does have vascular incre- les expand our ideas of raylessness in that rayless- ments in concentric rings or, in older stems, arcs of ness can be combined with successive cambia (Gibson, indefinite tangential extent. In Heimerliodendron, 1978a; Fahn et al., 1986; Carlquist, 1998b). The ray- there is a marked succession between fibrous and lessness of Aizoaceae, a species-rich family, has been parenchymatous rings in the conjunctive tissue. The evident for many years, but perhaps went unmen- explanation for these rings is to be sought in tioned because few Aizoaceae are ‘woody’ and few strength configurations. A number of amaranths and samples from the family are to be found in xylaria. chenopods have a succession of fibrous and non- Stayneria certainly has relatively large stems (for the fibrous rings in their conjunctive tissue. In some family) and stems with a dense fibrous texture (Car- rayless species, conjunctive tissue consists of a lquist, 2007b). Nyctaginaceae can be considered fibrous background: Pisonieae of Nyctaginaceae, rayless, except for the ‘neo-rays’ in Pisonia, produced Figure 6A; Stayneria of Aizoaceae (Carlquist, 2007c) by the master cambium (Fig. 6A, B). Bougainvillea and the rayless chenopods Haloxylon Bunge ex may be considered nearly rayless, but a few multise- E.Fenzl and Hammada (Fahn et al., 1986). This riate rays composed of upright cells can be seen in fibrous matrix is related to random dispersion of the tangential sections (Fig. 5B). vascular increments which are, in the genera named, Within the Cactaceae–Portulacaceae clade (see circular in transectional outline rather than arc-like Fig. 1), Portulaca has some rayless woods (Carlquist, or ring-like. 1998a; Melo-de-Pinna, 2009). The wood of Talinopsis A.Gray begins rayless but then develops rays; Tali- nopsis now belongs in Anacampserotaceae (Appleq- CELL CONTENTS uist et al., 2006; Nyffeler & Eggli, 2010). Talinum Rhabdodendron has both silica bodies and sphaeroc- paniculatum (Jacq.) Gaertn., now in Talinaceae, is rystals (Carlquist, 2001a), but the two types of rayless (Carlquist 1998a: Figs 11–14 in that paper are inclusions do not occur within a single cell. T. paniculatum but were erroneously labelled T. tri- Sphaerocrystals are compound crystals that take a angulare (Jacq.) Willd.). globular form but have a smooth outer surface (Car- A phylogenetic pattern in raylessness can be lquist, 2001b), and in that respect differ from druses, traced in Caryophyllaceae. The tribe Paronychieae, in which the angular tips and edges of the crystals considered a ‘primitive’ tribe in the sequence of Pax project from the surface of the crystal grouping. & Harms (1934) and also an early-diverging group in Sphaerocrystals are found in some other Caryophyl- Harbaugh et al. (2010) has rays, but Alsinoideae and lales (notably cacti). Sphaerocrystals were not men- Caryophylloideae do not (Carlquist, 1995). The tioned by the IAWA Committee (1989). family has been little sampled with respect to xylem, Silica bodies occur in only a few families of the because few species have a pronounced degree of order, all of which belong to ‘non-core’ Caryophyllales woodiness, although secondary xylem does occur in such as Polygonaceae (Carlquist, 2003b). In Plum- most of the family. The same can be said for Polygo- baginaceae, the silica bodies tend to be elongate and naceae, in which one species of Eriogonum appears relatively large (Carlquist & Boggs, 1996). Silica rayless (Carlquist, 2003b). As more species are bodies occur in ray cells of Ancistrocladaceae (Got- known with respect to secondary xylem, other twald & Parameswaran, 1968) and in the ray cells of examples of raylessness in Polygonaceae are likely a family close to Ancistrocladaceae, Nepenthaceae (S. to be found. In Plumbaginaceae, there are two Carlquist, original observations based on N. alata,a instances of raylessness (Aegialitis and Armeria), but new record for the family). their woods are rather different and these are not Druses and sphaerocrystals are common in the sister genera (Carlquist & Boggs, 1996; Lledó et al., Cacataceae–Portulacaceae clade (Gibson, 1973, 2001). 1978b, 1994; Carlquist, 1998a). Raphides are common Raylessness can be related to production of a stem in Nyctaginaceae. ‘Coarse raphides’ occur in familes of ‘ground tissue’ in which vascular increments are what may be termed the phytolaccoid clade. Styloids located. Presence of scattered vascular increments are present in Rivinaceae, whereas raphides charac-

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 373 terize the three genera of Phytolaccaceae s.s., Ani- ing were selected for illustration. In these, the helices someria. Ercilla and Phytolacca (Carlquist, 1998b, lie side by side in close proximity (Fig. 18F) and any 2000a). appreciable separation between the helices (Fig. 18E) In Tamaricaceae, rhomboidal crystals occur in may be considered an artefact. The bordered nature of sheathing cells of rays (Fig. 14C, D) of a few species of the helices and the occurrence of these idioblasts in Tamarix. In Frankeniaceae, rhomboidal crystals are xylem rays, pith and cortex of roots of Nepenthes are present, but as a line of crystals within the undivided newly reported and, probably, material of older roots axial parenchyma cells, as in Frankenia palmeri (and stems) of Nepenthes has not been available S.Watson (Fig. 15B; first report of rhomboidal crystals before. I had access to unusually large plants of for the family). N. alata. Idioblasts such as those of Nepenthes (but with ‘wide lumina’) were reported in the ‘strongly devel- IDIOBLASTS AND DISTINCTIVE CELL TYPES oped cortical parenchyma’ of roots of Drosera macra- In Anacampseros L., idioblasts with wide annular or ntha Endl. and D. trinervia Spreng. by Oels (1879), helical bands of secondary wall material are present in and this was cited by Solereder (1908) and Gregory interfascicular areas (Fig. 10D–F). Vessels in Ana- (1998). campseros have wide bands that are annular The helically banded idioblasts of Nepenthes were (Fig. 10E) or helical (Fig. 10D, top) and are narrower considered by Metcalfe & Chalk (1950) to perform a than the idioblasts (Carlquist, 1998a). The wide-band water storage function. However, the fact that the idioblasts of Anacampseros are similar to other ray helices do not expand and contract calls this inter- cells in their dimensions (Carlquist, 1998a). The idio- pretation into question. The helical bands of Nepen- blasts in Anancampseros rays should probably not be thes idioblasts provide extreme difficulties for termed tracheids, as Landrum (2006) did, even sectioning, because the bands catch on cutting edges although they are similar to the tracheids of fascicular and unwind, providing a dense tangle (Fig. 18A–C). areas of globular cacti (Fig. 10B, left and right). The This suggests that the bands could retard foraging by wide-band helical (vascular) tracheids of both globular turning into an entanglement whenever insects or cacti and the ray idioblasts of Anacampseros suggest a other predators attempt to chew the structures in maximal strength configuration that allows the col- which they exist. In terms of degree of abundance lapse of cells, like pleats in an accordion, as water is within the root of N. alata, the density is greatest withdrawn during periods of drought. The wide-band close to the surface of the root cortex; in secondary vascular tracheids of globular cacti (Fig. 10B) are in xylem, the idioblasts occur in ray portions nearer to contact with each other, so they expand and contract the cambium. Helical idioblasts in older portions of conjunctively, and their helices, not surprisingly, touch root rays of N. alata are often inconspicuous because each other. With SEM, I have been unable to see they tend to be crushed over time. borders on the wide bands of ray idioblasts of Ana- The occurrence of helical patterns in walls of par- campseros, although borders are present on wide-band ticular tracheary elements of Droseraceae and (vascular) tracheids of fascicular xylem in globular Nepenthaceae may be allied expressions of helical cacti (S. Carlquist, original data). patterns of wall structure. The curious fine banding A distinctive type of ‘spiral’ (term from Metcalfe & on walls of vessels of Dionaea has been mentioned Chalk, 1950) idioblast has been reported from leaves above. When seen obliquely, the vessel walls in of Nepenthes by Solereder (1908) and Metcalfe & Nepenthes show a distinct helical pattern (Fig. 17C). Chalk (1950). The tracheids that terminate in diges- This is also evident in walls of Nepenthes tracheids tive glands in Nepenthes appear similar in wall char- (Fig. 21D). Likewise, the vessel walls of Triphyophyl- acteristics to the helically banded idioblasts. The lum (Dioncophyllaceae), a genus close to Nepenthes helically banded idioblasts have hitherto only been phylogenetically, have pseudoscalariform pitting in studied by light microscopy and have been reported which the pits are laterally wide, so that intervening only in leaves. I prepared sections of roots and stems wall portions tend to appear as helices (Fig. 21C: S. from an old plant of N. alata Blanco and was able to Carlquist, new report). show that these idioblasts are abundant in rays of Perhaps the most amazing phenomenon related to roots (Fig. 18A–C). These idioblasts are also found at wall structure in the non-core Caryophyllales is to be the periphery of the pith and are especially common found in Ancistrocladus (Fig. 20). There are groupings in the inner cortex of roots in N. alata. The helices are of peculiar axial parenchyma cells reported by Got- secondary wall bands that are prominently bordered twald & Parameswaran (1968) as ‘spiral cells.’ The when one views idioblasts from which primary walls nature of the walls was not discussed by them, (seen in Fig. 18D) have been removed by sectioning although a vaguely helical pattern could be seen in (Fig. 18E–F), The idioblasts least damaged by section- the light photomicrographs they presented. When

Figure 18. Scanning electron microscopy (SEM) micrographs of helical idioblasts from root of Nepenthes alata Blanco. A, portion of transection of secondary xylem; multiseriate ray (r), centre, oriented horizontally in photo. Fascicular xylem (fx) at top and bottom edges of photo. Thread-like portions of helical idioblasts in ray torn away by sectioning. Starch grains present in many ray cells. B, oblique view into helical idioblast from transection of ray. C–F, views of helical idioblasts from inner cortex. C, numerous helical idioblasts, from transection of inner cortex. D, helical idioblast in inner cortex, from radial section. Primary wall covers the idioblast. Idioblast is nearly intact except for a few cracks in the primary wall induced by sectioning. E, edge of outside of idioblast, the primary wall of which has been removed by sectioning; two openings in the otherwise tight helices induced by sectioning. F, idioblast, the primary wall of which has been removed by sectioning; the helices are in a natural position. Scale bars, 50 mm (A, D); 8 mm (B); 10 mm (C); 5 mm (E, F).

Figure 19. Secondary xylem of Ancistrocladus tectorius (Lour.) Merr. (Ancistrocladaceae). A, transection, showing solitary vessels and banded axial parenchyma (ap); a few diffuse axial parenchyma cells are also present. B–C, scanning electron microscopy (SEM) micrographs of outside surfaces of imperforate tracheary elements. B, ﬁbre-tracheid, with relatively small bordered pits. C, vasicentric tracheid, with relatively large bordered pits. D, radial section of ray, showing secondary walls with pits, most of which are bordered (indicated by dumbell shapes in secondary wall as seen in sectional view); none of the ray cells in this area have the banded patterns shown in Figure 20. E, SEM of ray cells from a tangential section, showing the consistently bordered nature of the pits. Scale bars, 50 mm (A); 5 mm (B, E); 20 mm (C).

Figure 20. Scanning electron microscopy (SEM) micrographs of ‘ancistrocladan cells’ in axial parenchyma from the radial section of secondary xylem of Ancistrocladus tectorius (Lour.) Merr. A, cell seen from inside, showing the distinct banded pattern of inner secondary wall, with pit apertures intercalated into the bands; portion of ﬁbre-tracheid at right. B, view of banding with intercalated pit apertures; inner wall, at right, is torn away from outer wall. C, view of cell from inner surface; inner wall is torn away from upper portion, revealing pit cavities in outer wall. D, inner surface of cell, showing elongate openings in the wall; three pit cavities in the outer wall, such as those shown in C are visible within the openings. E, view of outer surface of torn-away portion of inner wall corresponding to the torn-away portion at right in (B), showing prominent borders on the openings in the secondary wall. Scale bars, 10 mm (A–C, E); 5 mm (D).

Figure 21. Wood sections of Triphyophyllum peltatum (Hutch. & Dalziel) Airy Shaw (Dioncophyllaceae) (A–C) and Nepenthes alata (D). A, portion of transection, showing portions of two vascular increments, with conjunctive tissue (ct) between them; wide solitary vessels; patches of axial parenchyma, as well as paratracheal and a few diffuse cells, are present within the secondary xylem (sx); an area of secondary phloem (sp.) containing ray cells which contain dark-staining tannins at upper left. B, portions of outer surfaces of adjacent tracheids from tangential section; large, densely placed bordered pits are present. C, inner surface of vessel from tangential section (long axis of vessel oriented horizontally), showing the helical pattern of the pseudoscalariform pits. D, tracheids from secondary xylem transection, showing helical microstructure. Scale bars, 50 mm (A); 10 mm (B–D).

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 378 S. CARLQUIST studied by SEM (Fig. 20A–E), these cells prove to be challenges. The prevalence of successive cambia in a distinctive cell type, described fully here for the first the order has proved problematic, because successive time. I am terming these ancistrocladan cells. Accord- cambia have been so variously (and mostly incor- ing to Gottwald & Parameswaran (1968), all species rectly) interpreted in the literature. Thus, there has of Ancistrocladus they studied have some of these been no secure baseline on which workers dealing cells in axial parenchyma, but ordinary axial paren- with species in the order could rely. Successive chyma cells are always present too. In fact, in my cambia are related to some aspects of juvenilism, and material of A. tectorius, ordinary axial parenchyma thus heterochrony becomes a pervasive and unappre- cells are approximately three times as common as the ciated theme throughout the order. Juvenilism in ancistrocladan type. These peculiar cells do not occur woods of the order is by no means limited to those idioblastically, but in various groupings. This peculiar that have successive cambia. Woodiness in the ordi- cell type does not appear to occur in rays of Ancistro- nary sense characterizes only a small minority of cladus wood, nor in the pith or cortex of stems. These Caryophyllales, and woodiness in the numerous ancistrocladan cells do not occur in the paratracheal species with successive cambia demands a new view (= vasicentric) axial parenchyma of Ancistrocladus, of how ‘woodiness’ can be achieved, just as monocots only in the banded apotracheal parenchyma. do not meet ordinary criteria of woodiness. Successive The ancistrocladan axial parenchyma cells have cambia and their products are not uniform within two wall layers, both approximately equally thick and Caryophyllales, but rather show a fascinating series both apparently composed of lignified wall material, of stages in wood evolution that has not been hitherto judging from staining reactions in my material of A. appreciated. tectorius. The two layers separate from each other to Caryophyllales do not show a complete range of various extents during sectioning (liquid-preserved what earlier workers would have termed ‘primitive’ to material was studied). The outer layer bears circular ‘specialized’ features. Symplesiomorphies in wood fea- pits, well revealed where large portions of the inner tures present in the majority of major angiosperm wall layer are torn away (Fig. 20C). Viewed from the clades are notably missing in Caryophyllales, as cur- lumen-facing surface, the inner wall layer displays rently defined. (This situation would change if Dille- long elliptical openings as well as some oval ones niaceae were added, Fig. 7.) Nevertheless, the (Fig. 20A, B). Some oval areas correspond to the near- character states represented in Caryophyllales are circular pits in the outer layer (Fig. 20C, top). often not congruent with what current terminology However, some of the circular outer-layer pits lie might lead us to expect, and thus wood in order is of beneath markedly elongate openings in the inner special interest and of special difficulty. Construction layer (Fig. 20D). In a torn-away portion of the inner of data matrices, mapping of character states on layer (Fig. 20E), one sees that all of the openings in DNA-based phylogenetic trees and application of the inner layer are prominently bordered. The section ontogenetic concepts all offer problems in Caryophyl- shown in Figure 20B illustrates, at right, separation lales, problems rarely discussed explicitly. These new between the inner layer and the outer layer. The perspectives are highlighted in the topics below. Are grooving on the inner layer does not correspond to the terms designed for wood identification (e.g. IAWA helical sculpture types depicted by Carlquist (2001b). Committee, 1989) suitable for use in describing woods Bordered pits are remarkably common in ray cells of of Caryophyllales? In many cases, the nature of vas- many woody angiosperms and of Gnetales, and are cular rays in Caryophyllales lies outside of what a less common, but also present, in axial parenchyma wood anatomical glossary offers. The discussions cells (Carlquist, 2007b). Both bordered and simple below attempt to place Caryophyllales in wider pits may be found in ray and axial parenchyma cells contexts. with secondary walls in angiosperms at large. The pits of the ancistrocladan cells are, however, much larger than bordered pits encountered in angiosperm SUCCESSIVE CAMBIA axial parenchyma cells that have bordered pitting. Symplesiomorphic or apomorphic? As we have seen, the number of character state changes required for either interpretation of the phy- CONCLUSION: CARYOPHYLLALEAN WOOD logenetic status of successive cambia within Caryo- phyllales is approximately the same (c. 11). The ANATOMY IN ITS WIDER CONTEXT presence of successive cambia in early-diverging lin- OVERVIEW eages (Rhabdodendraceae, Polygonaceae, Simmondsi- While each family and order of angiosperms has dis- aceae, Stegnospermataceae) might tip the balance in tinctive features, Caryophyllales present a series of favour of a symplesiomorphy hypothesis for succes- wood anatomical features with serious interpretive sive cambial occurrence within the order. However,

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 379 the story is probably not that simple. Even a hypoth- A transition from secondary xylem with wide rays esis involving ‘character reversion’ does not help us composed of upright cells to raylessness can be seen explain the systematic distribution of this feature in in some families. Barbeuiaceae, Bougainvillea of Caryophyllales. One can ‘declare’ a character state Nyctaginaceae and Phytolaccaceae are examples. reversion to have taken place on a drawing of a A final stage in this evolutionary sequence is ‘rein- phylogenetic tree, but what does that mean in genetic vention’ of rays (mostly uniseriate rays) in Nyctagi- terms? Is a drawing that ‘maps’ a character onto a naceae tribe Pisonieae. In Pisonieae, rays are phylogenetic tree a device that equates to under- produced by the master cambium, whereas the vas- standing of gene action? We can probably agree that cular cambia produce axial secondary xylem and sec- a genetic basis for development of successive cambia ondary phloem. The master cambium also produces is widely present in Caryophyllales, but what does the fibrous background in which the vascular incre- that mean in actual molecular terms? Modifier genes ments are located, and thus Pisonieae do not have that change timing or alter the kind of successive ‘wood’ in the ordinary sense. Because this has not cambial activity can be hypothesized, but any such been understood until recently (Carlquist, 2007a), the hypothesis is probably premature. A similar situation terminological challenges posed by Pisonieae, and by obtains in monocots, in which presence of a ‘monocot other diverse expressions in ray expression men- cambium’ (common in Asparagales, but probably tioned above, are new. homoplasious within that order), or loss of it, is dif- Is there a linear progression in structural modes ficult to explain. Monocot cambia occur in stems of within Caryophyllales? Probably not, so no simple some genera, but in both roots and stems of others categorization or sequence is proposed here. However, (e.g. Dracaena Vand.exL.). the examples cited do represent real evolutionary changes, and hopefully the comments provided here, and in my earlier monograph (Carlquist, 2007a), will Evolutionary change of successive cambia provide a basis for detailed studies on how the within Caryophyllales various structural modes have evolved. The successive cambia of Rhadodendraceae, sister to the remainder of Caryophyllales, are not at all the Scattered vascular increments same as, for example, those of Nyctaginaceae or Ama- When ray cambial activity is not present in a vascular ranthaceae, which are later-diverging clades within cambium, there is a disconnect between the master the order (Fig. 1). There is apparently a sequence cambium and the vascular cambium: they act sepa- from production of wood with a normal system of rays rately to provide tissues, but their activities must be (corresponding to Heterogeneous Type IIA of Kribs, coordinated. For example, the background paren- 1935) to a system of rays in which some are markedly chyma in Trichodiadema (Aizoaceae) is produced by larger and wider, with uniseriates or biseriates scarce the master cambium, whereas small strips of vascular to non-existent. This condition can be seen in Ama- cambia (which do not include rays) produce secondary ranthaceae, which have successive cambia, and in xylem and secondary phloem. Because of this depar- some families that do not: Cactaceae and allied portu- ture from the pattern of forming arcs (Bougainvillea) lacoid families; Tamaricaceae. One can see ray initials or concentric cylinders (Beta) of vascular increments, that produce the wide rays and the fusiform cambial the vascular increments, which occur as strands initials in the vascular cambia of Bougainvillea and within the (conjunctive tissue) parenchyma can be some amaranths and chenopods. However, in other distributed in a scattered fashion in Trichodiadema. amaranths and chenopods, wide rays (‘radial plates of This is evident in other genera also (Stayneria of conjunctive tissue’ of some authors) are produced Aizoaceae, rayless chenopods and pisonioid Nyctagi- directly from the master cambium. Not unexpectedly, naceae). All of these have vascular cambia that intermediate cambial conditions with respect to ray produce no rays. origin are lacking: ray production from both master A similar situation obtains in monocots with vas- cambium and from vascular cambium simultaneously cular bundles added secondarily by a ‘monocot is not likely to be a histologically successful scheme. cambium’ (e.g. Dracaena, Yucca L.). A scattered dis- Bosea (Amaranthaceae), claimed to have ‘radial position of bundles is permitted by absence of ray plates of conjunctive tissue’ can be demonstrated, in cambial activity, because the background tissue good preparations, to have meristematic cells in the serves in lieu of rays. Scattered bundles have the wide ‘ray’ areas, meristematic cells tangentially advantage of being potentially equidistant, and there- aligned with the fusiform initials in the ‘fascicular fore providing shorter pathways for water and photo- areas. Metcalfe & Chalk (1950) reported ‘radial plates synthate movement. This scattered bundle pattern is of conjunctive tissue’ for Bosea, but recognized rays in not ontogenetically possible when rays are formed in the amaranth Charpentiera. vascular cambia, a fascinating correlation that has

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 380 S. CARLQUIST eluded mention in the anatomical literature. Perhaps often have successive cambia in roots than in stems the surprising aspect of this concept is that so few (Pfeiffer, 1926), a fact explainable by the fact that the angiosperms other than monocots have developed the roots are perennial and bear annual or short-lived scattered bundle pattern. There are some non- stems. monocot angiosperm families in which pith bundles Some genera of Caryophyllales, such as Anredera are common (e.g. Piperaceae), but that condition is (Basellaceae), Monococcus (Rivinaceae) and Stegno- not as pervasive as it is in monocots. The reason is sperma (Stegnospermataceae), were not reported to that, in an appreciable number of Piperaceae, a vas- have successive cambia by Pfeiffer (1926), a circum- cular cambium (complete with ray initials) does stance explainable by the relatively small diameter of develop. The fact that pith bundles are common and stems available to him. When larger stems of these little or no vascular cambial activity occurs in species species were studied (Horak, 1981; Jansen et al., of Peperomia Ruiz & Pav. and Piper L. serves to show 2000; Carlquist, 1999a, d), successive cambia were a selective advantage for a scattered bundle system reported. This suggests one basis for believing that in particular situations. To be sure, non-monocot more genera and species of Caryophyllales will be angiosperm storage organs may have three- reported to have successive cambial activity. The dimensional displacement of bundles (e.g. Ipomoea L., anatomy of only a small proportion of the order has Solanum L.), which shows the advantage of this been studied at present. More importantly, increased structural type. In those storage organs, little or no organ diameter may be correlated with increased secondary growth occurs within the bundles. The successive cambial occurrence. Successive cambia scattered pattern of bundle-like vascular increments may well be lacking in Gisekiaceae, Limeaceae, in Caryophyllales illustrates a novel way of achieving Lophiocarpaceae and Molluginaceae, but studies are this structural pattern, based on invention of a needed: annuals and small perennials are relatively master cambium rather than occurrence of a monocot little known anatomically. Organ diameter is only one cambium or (in non-monocot angiosperms) dispersion factor in successive cambial occurrence, however: of procambial strands. Cactaceae and Didiereaceae have notably large Although the scattered vascular increments of Piso- stems, but lack successive cambia. Cacti have a nieae are striking, arc-like vascular increments, seen number of unique structural plant features. in a number of Caryophyllales (e.g. many Amaran- Didiereaceae resemble the unrelated family Burser- thaceae s.l.), represent a structural mode similar to aceae in having a succulent cortex but with a well- that of scattered bundle-like vascular increments and developed woody cylinder. doubtless have similar physiological significance. The Our incomplete knowledge of systematic distribu- concentric alternation of cylinders of vascular incre- tion of successive cambia suggests that mapping a ments with cylinders of conjunctive tissue (Beta)is character can be misleading. The presence of succes- certainly a successful photosynthate and water sive cambia in Anredera (Carlquist, 1999d) would storage/retrieval plan and should not be considered not have been discovered except for the fact that an less effective than the strand or arc system. Each unusually large specimen was available. The second system must obviously be studied as a whole. The vascular increment in the oldest stem studied was older the stem or root of a species with successive clearly present, but it was relatively small in extent cambia, the more likely that the pattern consists of compared with the mass of tissue produced by the arcs rather than concentric cylinders: integrity of an first cambium. Because of this single instance, unbroken master cambium around the periphery of a mapping of successive cambia onto a phylogenetic stem or root lessens over time (this may even be seen tree (Fig. 2) requires that one say that successive in roots of old plants of Beta). cambia are present in the clade that includes Portu- lacaceae and Cactaceae. Obviously, mapping a char- Successive cambial occurrence and absence: acter onto a tree cannot be interpreted as indicating possible explanations how common a character is in a particular clade, or The examples just cited suggest a correlation between what the significance of character presence or organ thickness and disposition of vascular incre- absence may be. One might conclude from Figure 2 ments. There is no question that the older and larger that raylessness bears a relatively high degree of the structure, the more likely it is to have more correlation with successive cambia, but that conclu- numerous vascular increments. A corollary is that sion would not be justified. Raylessness is more presence or absence of successive cambia may depend common in groups with a higher degree of paedo- on the longevity of the plant or organ. For example, morphosis (or juvenilism; Carlquist, 2009b). Caryo- absence of successive cambia in ephemeral Caryo- phyllales as a whole have a relatively high phyllaceae such as Stellaria L. is understandable in proportion of species with juvenilistic modes of this connection. Perennial Caryophyllaceae more structure.

Physiological and ecological implications of common in lianas and shrubs than in trees. The trees successive cambia in which successive cambia do occur are worthy of If successive cambia are a successful structural attention precisely because they represent an alter- system, why are they not more widespread in native method of managing optimal mechanical angiosperms? They are limited to a relatively small strength while also fulfilling other physiological number of angiosperm families (Pfeiffer, 1926; Car- requirements. Pisonieae are especially interesting in lquist, 2001b, 2007a, 2009b). They occur in Welwits- this regard (Carlquist, 2004). chia Hook. f. and in lianoid Gnetales (Martens, 1971; Conjunctive tissue may be entirely parenchyma, Carlquist, 1996). The differences in successive entirely fibres or alternating concentric bands of cambia, fascinating although they are (particularly in parenchyma and fibres, thereby matching axial Pisonieae of Nyctaginaceae and in the contorted parenchyma in diversity and potential function. stems of lianoid species of Bauhinia L. and other There can even be fibre dimorphism in conjunctive lianas) are perhaps not so striking as the similarity in tissue, in which some fibriform cells are starch-rich their ontogenetic nature. The various types of succes- and thin-walled, whereas others are starch-poor and sive cambia (Carlquist, 2007a) are more similar in thick-walled, as in Bougainvillea (Carlquist, 2004). ontogeny than descriptions in the literature might Species with successive cambia can have stems that indicate. are light, because of thin-walled conjunctive tissue, or Plants with successive cambia have a relatively low they can be dense. Atriplex and other chenopods vessel area per mm2 of stem transection (Carlquist, (Amaranthaceae s.l.) can be difficult to section 1975). This figure may be misleading, in fact, because because of their extreme hardness and density. Thus, in an ‘ordinary’ stem, active conduction may be successive cambia do not limit the strength of stems. limited to the periphery of the secondary xylem Juvenilistic although some species with successive (Braun, 1970), although not always. Secondary cambia may be, that may or may not correlated phloem in many woody species is short-lived, often with mechanical strength. only lasting a single year (Esau, 1965), so a compa- Conjunctive tissue by its very existence is respon- rably limited quantity of secondary xylem may also be sible for non-random distribution of vessels in stems functioning. Tests need to be conducted, but second- and roots of Caryophyllales (as compared with diffuse ary xylem in species with successive cambia may be vessel distribution in woods produced by a single active for an indefinite period of time. The reason for cambium). The possibilities inherent in non-random saying this is that secondary phloem is continually distribution of vessels are many (Carlquist, 2009a). produced by many of the vascular cambia in a stem. Amount and positioning of conjunctive tissue and of In species with successive cambia, crushed secondary the vascular increments are both readily varied. This phloem and apparently functional phloem in most of makes the successive cambial plan suitable for lianas, the vascular increments are routinely observed. If and lianas do appear prominently within the order: secondary phloem is present and functioning in so Agdestis (Agdestidaceae), Anredera (Basellaceae), many of the vascular increments (in itself a physi- Barbeuia (Barbeuiaceae), Bosea (Amaranthaceae), ological phenomenon that has been overlooked), one Bougainvillea (Nyctaginaceae) and Seguiera Rchb. ex suspects that these numerous functional secondary Oliv. (Rivinaceae) are among the more prominent phloem strands may be associated with functioning examples that can be cited. Successive cambia also secondary xylem cells. Progressively less secondary occur prominently in non-caryophyllalean lianas (e.g. xylem appears added to each vascular increment over Gnetum L.). The flexibility of parenchyma that sur- time, but secondary phloem production appears con- rounds vascular increments offers the possibility of stant for extended periods. What possible correlations twisting and of changing the transectional outline of can be found between this histological/physiological the stem. Conjunctive tissue also offers the possibility phenomenon in Caryophyllales and other seed plants of compartmentalization of vascular increments. The and other aspects, such as habit and ecology? distribution of parenchyma in stems offers many Extended function of the vascular increments more sites for development of lateral buds, as con- would be a prerequisite for extended function of conjunctive tissue is often meristematic, as pruning junctive tissue. Water and photosynthate storage and a tree of Heimerliodendron or Phytolacca readily retrieval could therefore be more extensive, three- demonstrates. dimensionally, in species with successive cambia than in species with a single vascular cylinder per stem or root. A larger portion of an organ with successive HETEROCHRONY cambia could function in these respects, and the dura- Although the idea of paedomorphosis in woods was tion over time of these functions could theoretically be proposed many years ago (Carlquist, 1962), decades greater. Successive cambia are relatively more passed before the full variety of expressions and the

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 382 S. CARLQUIST limits of the phenomenon were examined (Carlquist, tions are studied (Carlquist, 2007a). This fact may 2009b). All species of angiosperms fall somewhere seem only mildly interesting until one realizes that on a continuum from permanent juvenilism to accel- vascular cambia in species with successive cambia erated adulthood. The concept that heterochrony is are, in the case of the second vascular increment and pervasive in angiosperms, and one of their distinc- thereafter, the product of the master cambium, tive features (heterochrony is little developed in which in turn is formed not from procambium but conifers) was needed to counter the default concept from cortical cells. Bailey & Tupper (1918) and Car- that all woods are equally adult and that woodiness lquist (1962) found changes in length of fusiform is, ipso facto, an adult condition. We now realize cambial initials over time in species with a single that numerous families and orders of angiosperms cambium. In species with a single cambium, lengths have shifted between juvenilism and adulthood in of vessel elements indicate cambial changes faith- their secondary xylem structural modes, and that fully. In species with successive cambia, fusiform ini- sheer volume of secondary xylem volume produced tials derived from the master cambium are relatively is not a reliable indicator of juvenilism or adulthood shorter than procambial cells, because the master in wood. Caryophyllales, when compared with other cambium originates in cortical parenchyma rather orders of angiosperms, are mostly skewed toward than procambium. Each vascular cambium has a juvenilism. finite duration and this fact alone would make change in fusiform cambial initial length less likely. Adult patterns The template of the master cambium seems rela- Only a few families of Caryophyllales have truly adult tively unchanged compared with that of the vascular wood patterns. An arborescent habit is shown in cambium in single-cambium species with respect to Asteropeia (Asteropeiaceae), Coccoloba (Polygo- fusiform cambial initial length. These circumstances naceae), Ledenburgia (Rivinaceae), Tamarix (Tamari- would explain the unvaried length of vessel elements caceae) and most Didiereaceae, although other as reported by Horak (1981) in Stegnosperma alimi- examples may be cited. Achatocarpaceae form a good folium. They would also explain the relatively short example of a shrubby family of the order with an vessel element length of species with successive adult wood pattern. In these examples, the presence cambia in angiosperms in general (Carlquist, 1975). of procumbent cells and their proportion in rays as Short fusiform cambial initials can be found in a compared with upright cells is roughly in proportion range of angiosperm woods derived from a single to the conditions typical of ‘woody’ families generally. cambium, but one can find decrease in initial length Cactaceae depart from the ‘woody’ norm by having over time, especially early in the history of the mostly upright cells and are thereby a family that can cambium (Carlquist, 2009b). be described as arborescent but with some juvenile Ray structure has been stressed as the second cri- features. The large multiseriate rays of cacti are terion indicative of juvenilism in woods (Carlquist, infrequently broken into smaller rays over time. 1962, 2009b). In Caryophyllales with successive The main criterion of adult structure other than ray cambia, ray cells are predominantly upright, and histology is the ontogenetic change of vessel element therefore juvenile. This seems correlated with lack of length in a particular stem (Carlquist, 1962, 2009b). change in fusiform cambial initial length in species We do not have information in this respect for most with successive cambia. Wide rays, composed mostly species of Caryophyllales, but examination of radial of upright cells, characterize the Cactaceae– sections of Achatocarpaceae, Ancistrocladaceae, Aster- Portulacaceae clade. Wide rays usually change little opeiaceae, woody Polygonaceae and Tamaricaceae in histology and dimensions, no matter how old the indicates rapid acquisition of adult vessel element plant (e.g. old pereskioid trees, old cereoid cacti). This lengths and rays. last change is indicative of protracted juvenilism, but it may also have an ecological dimension, succulence, Are woods with successive cambia juvenile? as discussed below. Vessel element length is a good indicator of changes Raylessness has been construed as a juvenile in fusiform cambial initial length over time, because feature (Carlquist, 1970, 2009b) and is more abun- vessel elements undergo little intrusive growth dant in Caryophyllales than in any other order of during maturation compared with imperforate trac- angiosperms (Fig. 2). Some rayless woods eventually heary elements. Horak (1981) studied change in develop rays with age (e.g. Talinopsis). However, Hei- vessel element length over time in Stegnosperma merliodendron brunonianum (Endl.) Skottsb. alimifolium Benth. and demonstrated that a flat-line (Nyctaginaceae), perhaps the largest rayless woody plot, rather than an ascending or descending one, is angiosperm, does not. present. This pattern can be found in other Caryo- Secondary woodiness is a distinctive feature of a phyllales with successive cambia when radial sec- number of Caryophyllales. Secondary woodiness and

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 383 juvenilism are closely related, because departure from are relatively common in Caryophyllales (Gibson, non-woodiness includes degrees of ‘typical woodiness.’ 1973, 1977a, b, 1978b; Carlquist, 1999a, b). The problem with interpretation of secondary woodi- Paedomorphic Type III rays are found in small ness is one of direction. At any given moment in time, shrubs of limited growth, such as Myrothamnaceae some groups are becoming less woody and some (Carlquist, 1976) and Ericaceae (Wallace, 1986; Car- becoming woodier. Brassicaceae and Caryophyllaceae lquist, 1989). If secondary growth is limited, multise- are families that probably contain examples of both riate rays are narrower or may not even be present trends. (Barghoorn, 1941a): wider rays occur later in ontog- One cannot map these changes onto a DNA-based eny. Upright cells are characteristic of Heterogeneous phylogenetic tree of families with any degree of mean- Type IIA rays. Thus, Paedomorphic Type III rays are ingful conclusions that clarify rather than conceal essentially juvenilistic versions of Heterogeneous what is happening. Only detailed study of individual Type IIA rays and occur in clades that have relatively smaller clades with respect to secondary xylem devel- primitive (Heterogeneous Type I and Heterogeneous opment (and use of data from molecular phylogenet- Type IIA of Kribs, 1935) rays. Heterogeneous Type ics) can tell us about directionality of wood evolution. IIA rays do occur in some Caryophyllales, such as Juvenilistic features should be found in examples of Rhabdodendraceae (Carlquist, 2001a), Simmondsi- both phylogenetic decrease and phylogenetic increase aceae (Carlquist, 2002) and Stegnospermataceae in woodiness. (Carlquist, 1999a), so a juvenilistic form (Paedomor- phic Type III) of that ray type, with uniseriate rays Storying only, is not unexpected. The other paedomorphic ray Storying is usually an indicator of reaching stasis in types are relatively common in Caryophyllales. fusiform cambial initial length. Bailey (1923) clearly Clearly, ray histology in Caryophyllales is indicative showed that storying is a product of vertical, rather of paedomorphy, or juvenilism, in woods. than pseudotransverse, radial divisions in fusiform cambial initials to multiply the number of initials. In histological terms, this means that shortening of fusi- WALL STRUCTURES, IDIOBLASTS, ETC. form cambial initials has progressed to a point at Ancistrocladan cells are a kind of tracheid in most which further shortening is unlikely because deriva- characteristics (nuclei absent, bordered pits promi- tives from such shorter fusiform cambial initials nent), but they occur in axial parenchyma of Ancis- would not be more adaptive. This is demonstrated by trocladus. They are newly described above. These the tendency for flat age-on-length curves for vessel cells are of special interest in showing how bordered element length in species with storied cambia. Such pits can occur in a novel way. The two-layered nature curves descend at first and then become flat [e.g. in of the wall, with the outer layer pits non-bordered Macropiper excelsum (G.Forst.) Miq., Carlquist 1962, and the inner layer pits bordered, is highly distinc- 2009b]. In such species, a juvenile pattern is tive. The patterning of the inner wall suggests helical expressed early and then the length changes little arrangement of the pits. They might be considered a over time. kind of transfusion cell, like the ray tracheids of Extremely short vessel elements in species with Pinaceae. storied woods are likely to be accompanied by short ‘Helical idioblasts’ were described (as ‘spiral cells’) libriform fibres (or sometimes fibre-tracheids). A few for the leaves of Nepenthaceae (Solereder, 1908; Met- examples could be cited, such as Lactoridaceae (Car- calfe & Chalk, 1950) and also roots of two species of lquist, 1990) and Misodendraceae (Carlquist, 1985a). Drosera (see Solereder, 1908). They are reported here These are ‘miniature shrubs’ and therefore short lib- for wood for the first time and studied for the first riform fibres or fibre-tracheids are probably not of time with SEM. The helical idioblasts of Nepenthes negative selective value (longer fibriform cells corre- appear to be the ultimate iteration of bordered pits late with greater arborescence: Carlquist, 1975). and helical wall sculpture in Caryophyllales. Metcalfe & Chalk (1950) claim a water storage function for Explanation for the occurrence of Paedomorphic these cells. However, the density of the helical idio- Type III rays blasts in root cortex, the lack of spaces between Paedomorphic Type III rays are uniseriate and adjacent helices (and, thereby, lack of expansion and consist wholly of upright cells. This ray type is contraction) and the tendency for the helices to dis- present, within Caryophyllales, in Harfordia Greene integrate into a tangled mass when physically dis- & Parry of Polygonaceae (Carlquist, 2003b), Droso- turbed suggest otherwise. The idioblasts might be a phyllum of Drosophyllaceae (Carlquist & Wilson, deterrent for chewing herbivores. 1995) and Gymnocarpos of the Caryophyllaceae (Fahn The above two cell types are illustrative of pro- et al., 1986). Paedomorphic Type I and Type II rays nounced helical wall patterns, as seen in the non-core

Caryophyllales. For example, the vessel walls and Banks ex Gaertn. (Myrtaceae): Meylan & Butter- tracheids of Nepenthes show helical fine structure field, 1978; also tracheids of that genus] and is not when studied with SEM and the pseudoscalariform restricted to pits. Wart-like structures occur on pitting of vessel walls in Nepenthaceae and Dionco- conifer tracheids as well (Butterfield & Meylan, phyllaceae is suggestive of it. The vessel walls of 1980), not merely on the lumen surfaces, but on pit Triphyophyllum (Dioncophyllaceae) almost take the cavity surfaces, where they are minute and evenly form of helical strips, because there is a tendency for spaced, and they do not resemble at all the large the pseudoscalariform pits to be markedly elongate. coralloid protuberances often depicted as exemplify- The patterning of vessel walls of Dionaea (Droser- ing vestured pits in angiosperms. The distribution of aceae) and of vessel wall microcontouring in vessels warts and vesturing renders the hypothesis of and tracheids of Nepenthes are also suggestive of a Zweypfenning (1978) and the implications for ves- pervasive tendency toward types of helical micro- tured pit function discussed by Choat et al. (2004) structure in tracheary elements of the non-core as a device for preventing deflection of pit mem- Caryophyllales. branes and widening of pores in pit membranes untenable for vesturing as a whole. Other instances, including wart presence inside vessels and trache- WOOD CHARACTERS: ECOLOGICAL OR PHYLOGENETIC? ids, are unexplained by those authors. Ecological All wood features are presumed to have functional correlations have been sought (Jansen et al., 2004), value; one cannot categorize some characters as ‘taxo- but the trends stated by those authors are vague nomic’ and others as ‘ecological’ in significance. Inter- and may reflect radiation of a few families such pretation of this continuum is daunting and has been as Myrtaceae. Jansen et al. (2004) claimed that frequently avoided in work on wood anatomy. Met- warm tropical or lowland groups tend to have calfe & Chalk (1950) undertook the enormous task of vesturing. compiling wood character expressions in a systematic One might equally well hypothesize the reverse – context. The unintended consequence of this useful that groups possessing vesturing have radiated in compilation has been to advance the use of wood warm, dry climates, in the case of Myrtaceae in features for ‘identification,’ while marginalizing eco- Australia. That would not explain, however, why logical, physiological and evolutionary interpreta- Brassicaceae and Polygonaceae, which are commonly tions. The application of wood anatomical data to herbaceous and which are commonest in cool temper- identification has remained robust, as is evidenced by ate areas, characteristically have vesturing, a largely the IAWA Committee (1989) and the publication of unappreciated fact, because wood anatomy is much numerous wood atlases. Interpretation of wood struc- better known for woodier species. ture is a much more complex task than describing The most plausible explanation for vesturing (and and cataloguing it. Wood anatomy interpretation other kinds of wall sculpturing, such as grooves or requires synthesis, which in turn is based on detailed helical thickenings) has been offered by Kohonen information from a variety of fields usually kept & Helland (2009). These authors show that wall separate. sculpturing of all kinds, including vesturing, increases wettability, and thus can serve to remove Vesturing bubbles from vessels, hastening recovery from In Caryophyllales, the phenomenon of vesturing pro- embolisms and perhaps also preventing embolism vides a salient example of interpretive difficulties. formation. Vestured pits have been reported within Caryophyl- Vesturing is surely functional, but equally effective lales only in Rhabdodendraceae, sister to the remain- mechanisms are more common in species without der of Caryophyllales, and in Polygonaceae. Vesturing vesturing in drier areas, because only a fraction of the is not present in any of the outgroups (Fig. 1) except woods in any floristic area have vesturing. If vestur- Brassicales. Conceivably, one could interpret this as ing represents an adaptation to drought, perhaps it indicating that vesturing is an apomorphy in Caryo- may persist when a group radiates into a wetter phyllales, but has been lost except in Polygonaceae. If habitat, as with individuals of Metrosideros in stand- so, why has vesturing survived in Polygonaceae? ing water of bogs in the Hawaiian Islands. Various hypotheses have been offered on the signifi- Certainly simple perforation plates, thought to cance of vesturing. For example, Jansen et al. (2003) have evolved in relation to seasonality (Carlquist, discussed numerous hypotheses. 1975), may be found in some species of highly mesic Experimental work on such microstructures is areas. Although scalariform perforation plates tend to extraordinarily difficult. In addition, commentaries be more common in mesic areas and be absent in have all but forgotten that vesturing is common on favour of simple plates in dry areas, simple perfora- vessel lumen walls in some genera [Metrosideros tion plates are not disadvantageous in mesic areas.

Persistence of these features as clades radiate into contrast, the sister family, Frankeniaceae, have more mesic sites seems likely. Vesturing and simple grouped narrow vessels, growth rings and even infre- perforation plates do not seem to have a negative quent vasicentric tracheids. Frankeniaceae grow in value in mesic areas. Such persistence of a feature as saline places, but have relatively shallow root a clade radiates from a dry area into a wet one would systems, which are likely to experience fluctuation in mask the ecophysiological significance of a character. water availability. Although species vary a little However, ‘trends’ are less relevant here than experi- within the family with respect to vessel diameter and mental work. If ‘trends’ were operative, the gnetalean vessel grouping, these features are present in all genus least likely to have vestured pits would be the species and offer conductive safety mechanisms char- only one that does have them: Gnetum (Carlquist, acteristic of drought-resistant species that have libri- 1996). Ellerby & Ennos (1993) claimed that vessel form fibres rather than tracheids (Carlquist & surfaces act to slow conductive rates. In this case, Hoekman, 1985). structures such as vesturing or warts would slow conductive rates, not a function of positive value per se for the conductive process. However, the reason HABIT that conductive rates are slowed, presumably by Aizoaceae are succulents that have shown amazing increasing friction, also suggests heightened bonding radiation, especially in the arid regions of southern of wall with water, an idea validated by Kohonen & Africa. Do they have features that explain this? The Helland (2009). sprawling stems of Aptenia, Carpobrotus N.E.Br. and Tetragonia L., which can shift in response to drifting Vessel grouping and tracheids: contexts of the sand dunes where they grow, are highly flex- and complexities ible. This flexibility appears to be clearly related to Grouping of vessels is not one character, but many the presence of concentric cylinders of vascular incre- (Carlquist, 2009a). Presence of tracheids is clearly ments well separated from each other by conjunctive related to minimal grouping of vessels (Carlquist, tissue. Other Aizoaceae, with more upright stems 1984). Tracheids are present in a relatively small (Stayneria) or more abbreviated rhizomes, do not number of Caryophyllales, notably Ancistrocladaceae, show a clear relationship between habit and pattern Dioncophyllaceae, Drosophyllaceae, Nepenthaceae, of successive cambial distribution within stems. In all Simmmondsiaceae and Stegnospermataceae, which Aizoaceae, the presence and distribution of vascular are, as a generalization, early-diverging families in increments undoubtedly do provide advantageous the clade (see Fig. 1). This pattern of occurrence rati- three-dimensional distributions of conductive tissues fies the contention that tracheids are a symplesiomor- relative to storage tissues. These patterns have been phy, ‘primitive’ for angiosperms as a whole (Carlquist, little studied. Likewise, the succulent roots of Ama- 1962: 50). It also ratifies the concept that, as a way of ranthaceae (Beta), Basellaceae, Cactaceae, Caryo- maximizing conductive safety, tracheid presence is phyllaceae and other caryophyllalean families are more important than vessel grouping, and provides worth comparison with similar structures in other an effective second system for conduction (Carlquist, orders with respect to vascular patterning. 1984). Vessel grouping is notably low in the families The main wood anatomical correlation between listed above as having tracheids, validating that idea. anatomical structure and succulence in cylindrical or Most families of Caryophyllales do not have trac- flat-stemmed cacti is the presence of rays that are heids as the imperforate tracheary element type, and wide, tall and relatively unchanged during ontogeny. have vessel grouping. Vessel grouping prevails even To some extent, these ray characteristics may be in those families with succulence (Aizoaceae, Cacta- found throughout the Cactaceae–Portulacaceae clade, ceae) and with successive cambia. Vessel grouping is, but they are represented in their most extreme form in angiosperms as a whole, a way in which conductive by arborescent cereoid and opuntioid cacti. This con- pathways are safeguarded (Carlquist, 2009a). figuration represents a compromise between cylindri- Wide non-grouped vessels are characteristic of cal disposition of fibre-rich wood positions (such as Tamaricaceae. Are they an exception to the above? steel rods and beams that reinforce a concrete build- Tamaricaceae have libriform fibres and therefore no ing) with parenchymatous pith, cortex and rays that background of tracheids as a potential subsidiary are capable of a wide range of expansion and con- conductive system. However, Tamarix grows in areas traction. These parenchyma tissues, when studied in where its roots tap saline or brackish water. Tamari- living plants, also prove to be sites for abundant caceae can be termed halohydrophytes, plants that storage of starch. The structural system of stems of experience no shortage of water and are capable of cacti does not contain successive cambia. Parallels in dealing with the high ion levels in the abundant disposition of vascular tissue within a ribbed paren- underground water available where they grow. In chymatous stem may be found in succulent Euphor-

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 386 S. CARLQUIST biaceae. Although the similarities between these naceae). Notable is the fact that all of these, except two families with respect to external appearance has for Pereskia, have successive cambia. Successive long been noted, anatomical plan parallels need cambia provide a template close to the roster of exploration. lianoid anatomical features mentioned above. Espe- Caryophyllales as a whole are not regarded by most cially notable is the fact that, by virtue of immersion botanists as a woody group. That impression is of vascular increments within a background of con- largely correct, and trees such as Phytolacca dioica L. junctive tissue and wide rays, the successive cambial (Phytolaccaceae) and Heimerliodendron (and other plan provides an ideal prefiguration of the fibrous pisonioid Nyctaginaceae) are thus unexpected (these vessel-bearing strand plan common in lianas. The have successive cambia). However, some Caryophyl- possibility that successive cambia have longevity in lales are trees with dense woods, notably Asteropeia the function of vascular increments (as indicated by (Asteropeiaceae), which does not have successive continued phloem production from older as well as cambia, and Rhabdodendron (Rhabdodendraceae), younger successive cambia in a stem or root) needs which does have successive cambia, for example. further study. Longevity of vascular tissues, such as When confronted with these and other tree examples longevity of bundles in some monocots, would lend (Polygonaceae, Didiereaceae), one may wonder why itself to habits in which mechanical strength is sub- arborescence is not more common in the order, espe- ordinated in volume to conductive tissue presence: cially in the core Caryophyllales. The reason for this this combination is certainly what one sees in lianoid seeming paradox may be that non-tree Caryophyllales angiosperms as a whole. have, in fact, radiated more abundantly because of special advantages that they have. The presence of successive cambia is one probable reason, but INTERPRETING WOOD EVOLUTION the presence of succulence in the Cactaceae– Character definition Portulacaceae clade is another. The woody chenopods Defining wood anatomical features seems basic to have radiated amazingly well in south-western North understanding direction and extent of evolution and America, drier parts of Australia and across vast Caryophyllales are rich in features that demand areas of arid Eurasia and North Africa. Aizoaceae better definition. Better definitions are achieved not form a huge assemblage of genera and species in so much from an emphasis on precision as inclusive- southern Africa, whereas Cactaceae are conspicuous ness. Vasicentric tracheids are defined precisely by in the Americas. Although both Aizoaceae and Cacta- the IAWA Committee (1989), but in a way that ceae are best represented in summer-wet deserts, excludes most instances of the phenomenon, as rec- they have also been able to adapt to winter-wet desert ognized by Metcalfe & Chalk (1950) and Carlquist areas. Parenchyma patterns are certainly one (1985c, 2001b). If one excludes these instances, the element in adaptation to these habitats. functional and ecological importance of vasicentric tracheids is dismissed and misunderstood. Lianas Caryophyllales show all known variations of suc- Lianas are characterized by wide vessels. When cessive cambia. At one end of the spectrum are those vessel diameters are plotted, the distribution shows a which produce secondary xylem much like that larger number of narrower vessels and a larger derived from a single cambium, as in Stegnosperma number of exceptionally wide vessels than in the and Rhabdodendron. At the other end, are those with wood of a tree or shrub (Carlquist, 1985b; Ewers, localized rays or rays produced from a master Fisher & Fichtner, 1991). Lianas also have notably cambium and those without rays. We can use the wide rays. These often begin abruptly, as seen in term ‘rays’, ‘radial plates of conjunctive tissue’ or transection, rather than as widening of narrow mul- ‘neorays’ (the latter in Pisonieae) to call attention to tiseriate rays, as mentioned above for Nepenthes. some distinctive types, but what matters more is that Lianas also have a high proportion of conductive structures termed rays and agreeing with all defini- tissue per mm2 of transection (Carlquist, 1975). Other tions of rays can have more than one ontogenetic distinctive features include sheathing of the wide origin. We also should take into account that the vessels in fibrous tissue (Carlquist, 1985b, 2009a). ‘monocot cambium’ in monocots with secondary These features are all well represented in the growth, such as Dracaena, is much like the master scandent caryophyllalean families Agdestidaceae, cambium of Trichodiadema (which is rayless, like Barbeuiaceae, Basellaceae, Diocophyllaceae and monocots) in the tissues it produces and their Nepenthaceae and in scandent genera of other fami- disposition. lies (Pereskia Mill. of Cactaceae; Bosea and Chamis- The definitions of the IAWA Committee (1989) for soa Kunth of Amaranthaceae; Seguiera of Rivinaceae; cambial variants claim to depend merely on ‘appear- Antigonon of Polygonaceae; Bougainvillea of Nyctagi- ance of the wood.’ to define successive cambia and

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 CARYOPHYLLALES WOOD ANATOMY 387 other cambial variants. However, species with succes- group is not advisable. We have been willing to sive cambia cannot be said to have ‘wood’ in the include diverse variations of vessel elements (e.g. ordinary sense. The ‘appearance’ in transection of how fibriform, gnetalean, with multiple perforations, etc.) phloem is distributed, regardless of its ontogenetic within the definition of vessel elements, but such origin, invites misunderstanding of anatomical struc- inclusiveness has been denied the terminology for ture. Using ‘appearance’ in transection without taking tracheids in angiosperms. The wide-helix tracheids of into account ontogenetic origin invites us to use expe- globular cacti can be called vascular tracheids. diency in preference to understanding, with a subtext Similar cells in rays of Anacampserotaceae occur idio- that inexperienced workers should be able to make blastically, apparently lack borders and thus perhaps judgements as competently as those with a more are best not termed tracheids. In the secondary xylem informed understanding. The IAWA Committee (1989) of Asteropeiaceae, Frankeniaceae and Physenaceae, definitions build on the fact that successive cambia tracheids are in contact with vessels and are thus (and other cambial variants) have been poorly studied best termed vasicentric tracheids, in accordance with and are often misinterpreted, for reasons considered predominant use of that term (Metcalfe & Chalk, elsewhere (Carlquist, 2007a). Misinterpretation is not 1950; Carlquist, 1985b, 2001b). The idea that vasi- a sufficient reason for oversimplified and uninforma- centric tracheids should be defined by distorted shape tive definitions. Mature appearances are, in fact, the (IAWA Committee, 1989) is not supported by known result of particular ontogenies and, now that we occurrences of this cell type. That idea was based on understand those ontogenies better, we can base defi- occurrence of distorted cells with bordered pits adja- nitions and descriptions on mature appearances in a cent to earlywood vessels of Quercus L and some more accurate and informed way. Caryophyllales are Myrtaceae (mostly Eucalyptus). Tracheids adjacent to clearly the most important group for understanding latewood vessels in both of these groups would, in how successive cambia function. that definition, not qualify as vasicentric tracheids Caryophyllales illustrate the numerous transitions because they are not distorted enough in shape. The between bordered and non-bordered perforation central theme of vasicentric tracheids, which should plates. This character (not mentioned by the IAWA be consonant with their definition, is that they Committee, 1989) is a neglected phenomenon that is provide sheaths of conducting cells around vessels; if best approached by the use of a modifying adjective vessels embolize, water columns of the conductively (see Fig. 7). safe vasicentric tracheids remain intact and therefore The presence of borders on pits of wood cells with safeguard the pathways of the vessels. secondary walls shows that our tendency to contrast A somewhat more difficult instance is represented cells with bordered pits with those with simple pits is by the tracheids that provide the ground tissue of often based on incomplete observations. A large woods in a large number of angiosperms. Many of number of angiosperm and gnetalean woods have these cells are identical to what would be termed bordered pits on ray cells (Carlquist, 2007b), especially vasicentric or vascular tracheids by the IAWA Com- on tangential walls (Fig. 19D, E), and even axial mittee (1989), but are denied recognition as ‘trache- parenchyma cells, but this has not been acknowledged, ids’ because that glossary arbitrarily decides that, in despite the fact that such borders can readily be seen angiosperms, ‘tracheid’ must be confined to vesselless in sectional view with light microscopy and, more angiosperms excluding monocots and the term ‘fibre- dramatically, with SEM. To omit this feature from tracheid’ applied. In Gnetales, Esau (1965), correctly glossaries, as is currently the case, is to condone poor recognized both tracheids and fibre-tracheids as observation. Caryophyllales contain some fascinating present in woods of Ephedra. instances of borders that occur in unusual places in Tracheids that form a ground tissue in angiosperm wood cells, such as on the helical thickenings of woods offer an ideal subsidiary conductive system, Eriogonum giganteum S.Watson, on the helices of much as described for vasicentric tracheids above. Nepenthes helical idioblasts, on the ancistrocladan That function surely should be the focus of how tra- axial parenchyma cells and on the wide-band tracheids cheids are defined, even if some morphological diver- of cacti and the vessels of Anacampserotaceae. We tend sity must be admitted, as must be carried out with to think that the presence of bordered pits qualifies vessel elements. The fact that, in woods with a trac- cells as tracheids, but that is clearly not true. Bordered heid background, or with abundant vasicentric trac- pits in epidermal cells of cacti were depicted long ago heids (Quercus), vessels are essentially solitary (Solereder, 1908; Metcalfe & Chalk, 1950). Stylidium (Carlquist, 1984) provides a visible criterion for rec- streptocarpum Sond. (Stylidiaceae) has epidermal cells ognition of tracheids. The more widely used criterion with bordered pits that have tori (Burns, 1900). traditionally applied (e.g. IAWA Committee on Tracheids are surely not uniform. To define trache- Nomenclature, 1964; Esau, 1965) is that of densely ids on the basis of how they appear in one particular placed bordered pits. That criterion is still definitely

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 388 S. CARLQUIST applicable, but one should recognize some variability Character analysis: mapping, expression, reversion in that pitting. The central focus of the definition Characters are more nuanced in real life than in should be that a tracheid is a conductive cell, whereas glossary definitions, they are more complex and fibre-tracheids and libriform fibres are not. diverse. Conceding this, and conceding that we do not Tracheids in Stegnospermataceae and in Gymno- know the genetic basis or biochemical pathways for carpos (Caryophyllaceae) have relatively small bor- formation of character states, can we meaningfully dered pits, but they are densely placed. Tracheids are analyse them? Hennigian definitions demand a wide in lumen diameter and the lack of vessel group- binary system of definition or some methodology ing is a good indicator that they are conductively equally capable of being expressed without equivoca- competent. Nepenthes and Simmondsia have ‘typical’ tion. This is less difficult when analysing molecular tracheids, with large bordered pits; these easily results, but it is intrinsically much less reliable for qualify as tracheids. In Rhabdodendron, bordered pit phylogenetic purposes where morphology is con- cavity areas are a little smaller than those in Nepen- cerned. In fact, construction of phylogenetic hypoth- thes or Simmondsia, but the small lumen volume of eses based on morphology has waned in favour of tracheids in Rhabdodendron is proportional to the using DNA-based phylogenetic trees. probable conductive capacity of the tracheid. The Phylogenetic trees based on DNA data are poten- small lumen diameter is related to the thick-walled tially immensely useful to wood anatomy, as they nature of tracheids. Obviously, less pit cavity volume have been for plant phylogeny, in pointing the way per cell can serve adequately for conduction in a toward how wood evolves. When compared with a tracheid if the lumen diameter is small, although this DNA-based phylogeny, such as shown in Figure 1, for correlation is not mentioned in discussions of tracheid example, early-diverging clades (Rhabdodendraceae, morphology and function. Trying to impose numerical Simmondsiaceae, Stegnospermataceae) have trache- values on pit diameter or number of pits per unit ids rather than fibre-tracheids or libriform fibres. length of a tracheid does not seem useful in differen- Other characters that tend to occur in early- tiating tracheids from fibre-tracheids. Definitions that branching positions within Caryophyllales include avoid the physiological nature of a cell (which can be ray type (Heterogeneous Type IIA rather than Type readily be deduced by anatomical signals from light IIB, or paedomorphic versions of these types; ray microscopy) do not seem advisable, appealing though presence rather than raylessness). The same is true they may be in terms of simplicity. with axial parenchyma; diffuse axial parenchyma is Axial parenchyma should seem simple to define, considered a primitive character state by Kribs (1937) but in fact, there are two major kinds: strands of cells and it is confined to early-diverging clades within that are disposed in various patterns (Kribs, 1935) Caryophyllales. Imperforate tracheary elements also and apotracheal bands of cells not subdivided into follow this pattern. Successive cambia (of a less strands to any appreciable extent, the bands resulting derived type) occur in the families with tracheids. from fibre dimorphism. Parenchyma that has resulted This could be cited as indicating that occurrence of from fibre dimorphism can be distinguished from successive cambia in Caryophyllales is a symplesio- ordinary axial parenchyma easily in Asteraceae (Car- morphy rather than a synapomorphy, but the situa- lquist, 1958a, b, 2003a) and in Cactaceae and Portu- tion is not as simple as that. lacaceae (Melo-de-Pinna, 2009), because all of these Caryophyllales offer a nice example of how molecu- families are characterized by scanty paratracheal lar trees can tell us about, and offer confirmation of, axial parenchyma in strands which is easily differen- wood anatomical trait evolution. Caryophyllales do tiated from the bands, in which cells are not sub- not show the full range of features seen in some other divided into strands. In addition, apotracheal families, or comprehended in the schemes of Frost parenchyma cells in instances of fibre dimorphism are (1930) and Kribs (1935, 1937). For example, there are consistently shorter than the libriform fibres they only the most vestigial hints of scalariform perfora- accompany and they have thinner walls. tion plate structure in Caryophyllales. The above examples comparing Caryophyllales Correlated with the above trends, storied vessel with other families of angiosperms are only a partial elements and imperforate tracheary elements are account of discrepancies one can find between terms rather common in Caryophyllales. As Bailey (1923) as found in glossaries and morphological conditions as showed, storying characterizes species with fusiform seen through the microscope. Glossaries may deter cambial initials shorter than those of non-storied exploration by omitting diversity within characters. wood (Bailey & Tupper, 1918). Caryophyllales as a The omission of characters in glossaries tends to whole do show relatively short fusiform cambial ini- oversimplify wood anatomy, thereby resulting in tials, as judged by the length of vessel elements. continued lack of observation of extant anatomical Storying is not, however, a character than can be conditions. expressed in a simple binary (present or absent) way.

Storying becomes more evident with greater woodi- this a character reversion or progression? How can ness (i.e. less juvenilistic woods, sensu Carlquist, the ontogenetic origin of rays be shifted to a different 2009b) and often it is more conspicuous as a stem meristem? The venue for the solution of morphologi- grows in diameter. The overlay of juvenilism onto cal questions now changes from microscopes to several character sets in Caryophyllales, such as ray genomic laboratories (Farquharson, 2008; Nilsson histology and progression to storying, provides diffi- et al., 2008), but knowledge of morphology still culty in applying the strategy of mapping characters remains essential. If anything, detailed knowledge of onto DNA-based phylogenetic trees. Our understand- variations in structure becomes more important, ing of wood characters has been based on ‘typically because the applicability of genetic information from woody’ (= adult in terms of ontogenetic change in one plant to wider areas of phylogenetic relationships wood cells, notably in the age-on-length curves for or unappreciated structural diversity becomes an vessel element length). Woods with one or more juve- issue. nilistic features (Carlquist, 2009b) were excluded, to a large extent, from the earlier schemes (e.g. Bailey & Tupper, 1918) that attempted to show wood evolution. THE BRIDGE: CONNECTING WOOD ANATOMY WITH The easy access to milled wood samples in xylaria, OTHER DISCIPLINES combined with the reluctance of wood anatomists to Anatomical structures, as seen with a microscope, can engage in collection of their own wood samples, are in be described as visual phenomena, but such descrip- no small measure responsible for this bias. tions are poor substitutes for understanding the full Some will claim that a number of families such as structure–function relationship and the developmen- Betulaceae or Dipterocarpaceae are truly woody, and tal and genetic bases for structures. Wood anatomists one can therefore neglect the possibilities of overlay of are faced with a wide range of appearances. The protracted juvenilism on wood patterns when study- temptation is to react to these within the limits of a ing them. Caryophyllales, however, are composed single discipline, a single glossary, a single method- mostly of families that show various degrees of juve- ology. That may be the best way to gain a particular nilism, and thereby character states rather different piece of information, but is it the best way to under- from those found in those families with little wood stand wood evolution? juvenilism. One can, reductively, contrast those who have col- Some character states may represent collections of lected woods in the field, and who therefore under- phenomena that should not be reduced to a single stand ecology, with those who section the woods and expression. Is raylessness in one species of Eri- study their microscopic characteristics. All too often, ogonum (Polygonaceae) or the annual Halophytum these activities have been performed separately from (Halophytaceae: Gibson, 1978a) the same as rayless- each other. There is the implication that ‘systematic’ ness in some large chenopods such as Hammada characters can be divorced from ‘ecological’ characters (Fahn et al., 1986) or Heimerliodendron (Nyctagi- and that physiological studies can be carried out naceae)? The phylogenetic and ontogenetic pathways without reference to structural understanding of any through which raylessness has been achieved in given wood in its entirety. various menbers of Caryophyllaceae may be diverse. In Caryophyllales, and other orders, can one find Raylessness is, after all, one type of juvenilism, and characters that relate to systematic study and differ- juvenilism is a sliding scale, with expressions ranging entiate them from those that relate to ecology and between permanent juvenilism and accelerated adult- physiology, or is the implied polarity instead part of a hood (Carlquist, 2009b). continuum? Silica bodies, for example, occur only in Alleged character state reversion is equally difficult ‘non-core’ Caryophyllales, whereas various types of to establish on the basis of morphology. Successive calcium oxalate crystals (some characteristic of par- cambia in Caryophyllales (Fig. 2) offer a bewildering ticular families) occur in both core and non-core pattern of seeming appearances and disappearances. Caryophyllales. Such a distribution is often consid- But are these shifts reversions or are they the effect ered to involve a ‘systematic feature.’ of modifier genes that can repress successive cambia This tends to imply that crystals and silica bodies at some times, although the genetic information for are not functional, whereas ‘ecological features’ such the formation of successive cambia is present? The as quantitative vessel element characters are directly occurrence of rays in Pisonieae (Nyctaginaceae) is a related to the environment. In fact, there is no reason case in point. In other menbers of Caryophyllales, to believe that any anatomical feature has a zero rays, if present, are formed from ray initials in vas- selective value with respect to existence of a plant in cular cambia; in Pisonieae rays are derived from the its native environment. Herbivore-deterrent features master cambium, whereas vascular cambia produce such as calcium oxalate crystals and silica bodies rayless secondary phloem and secondary xylem. Is work conjunctively with a range of chemicals and wall

© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164, 342–393 390 S. CARLQUIST structures to reduce predation. All of them are prob- find my way to plants in the wild, I am grateful to ably not of equal value. Wendy Applequist, John Bleck, Pierre Detienne, In fact, wood anatomy has all too often been Steven Jansen, David H. Lorence, Regis Miller, Mark regarded, by default, as a collection of structures E. Olson, Peter H. Raven, Baron Rugge, Ann Sakai, which are ‘useful for identification’ and thus ‘of taxo- Edward L. Schneider, William L. Stern, Benjamin C. nomic importance’. Enormously useful as the works of Stone, John Trager, Gary M. Wallace, Steven Weller Solereder (1908) and Metcalfe & Chalk (1950) are as and Scott Zona. The microscope slides of cactus woods compendia of comparative information, they offer few of Arthur C. Gibson were available and important to vistas of ecological and physiological significance. me; his work, as well as the work of James D. Trying to bridge these two fields does pose consid- Mauseth and his students on Cactaceae proved erable difficulty. Few if any individuals have equal valuable. comprehension of both fields or carry with them knowledge of both fields. Wood is the most compli- REFERENCES cated tissue in plants and therefore the least well understood; for example, specialists in wood of APG III. 2009. An update of the angiosperm phylogeny group African trees of Fabaceae are not likely to be aware of classification for the orders and families of flowering plants: the complexities within Caryophyllales (nor have any APG III. Botanical Journal of the Linnean Society 161: motivation to learn about wood of numerous groups in 105–121. depth). Comparative wood anatomy grows by amass- Applequist WL, Wallace RS. 2001. 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