how wood evolves: a new synthesis - sherwin carlquist · sherwin carlquist abstract: recent...

REVIEW / SYNTHÈSE

How wood evolves: a new synthesis

Sherwin Carlquist

Abstract: Recent advances in wood physiology, molecular phylogeny, and ultrastructure (chiefly scanning electron micro-scopy, SEM), as well as important new knowledge in traditional fields, provide the basis for a new vision of how woodevolves. Woody angiosperms have, in the main, shifted from conductive safety to conductive efficiency (with many varia-tions and modifications) and from ability to resist cavitation (low vulnerability) to ability to refill vessels. The invention ofthe vessel was a kind of dimorphism (vessel elements plus tracheids) that permitted division of labor and many kinds ofwood repatterning that suit conductive safety–efficiency trade-offs. Angiosperms were primarily adapted to mesic habitatsbut were not failures or “unstable.” They have survived to the present in such habitats well, along with older structural adap-tations (e.g., the scalariform perforation plate) that are still suited to such habitats. These “primitive” features are evident inearlier branchings of phylogenetic trees based on multiple genes. Older features may still be functional and thus persist,although newer formulations are overriding in effect. There are, however, numerous instances of “breakouts” in a number ofclades (ecological iterations and bursts of speciation and diversification related to new ways of dealing with water econ-omy), whereas in other branchings, other clades show ecological stasis over long periods of time. Newer physiological andanatomical mechanisms have permitted entry into habitats with marked fluctuation in moisture availability. Wood evolvesprogressively, and literal character state reversal may be unusual: genomic and developmental information holds answers tothese changes. Wood is a complex tissue, and each of the histological components shows polymorphism as an evolutionarymechanism. Cell types within wood evolve collaboratively. Shifts in wood features (e.g., simplification of the scalariformperforation plate) are commonly homoplastic. Manifold changes in habit and in leaf physiology, morphology, and anatomyaccompany wood evolution, and wood should be studied with relationship to real-world ecology, information that cannot begleaned from literature or other secondary sources. Heterochrony (protracted juvenilism, accelerated adulthood) characterizesangiosperm xylem extensively, far more so than in other vascular plants, and these mechanisms have resulted in many re-markable changes (e.g., monocots have permanently juvenile xylem, woody trees represent accelerated adulthood). Under-standing the many successful features of angiosperm wood evolution must ultimately rest on syntheses.

Key words: breakout theory, cell type polymorphism, collaborative cell type evolution, ecological iteration, embolism rever-sal, molecular phylogeny, wood physiology, xylem.

Résumé : Les progrès récents réalisés en physiologie du bois, en phylogénie moléculaire et en ultrastructure (notamment enmicroscopie électronique à balayage, MEB), ainsi que d’importantes connaissances nouvelles acquises des champs tradition-nels jettent la base d’une nouvelle façon de concevoir comment le bois évolue. Les angiospermes ligneuses ont principale-ment passé d’une conduction sécuritaire vers une conduction efficace (avec plusieurs variations et modifications), et d’unecapacité de résister à la cavitation (faible vulnérabilité) vers une capacité de remplir les vaisseaux. L’invention du vaisseauconstitue une sorte de dimorphisme (éléments des vaisseaux et les trachéides) qui permettait une division du travail et diffé-rents types de remodelage du bois qui conviennent aux compromis sécurité–efficacité de la conduction. Les angiospermesétaient d’abord adaptées aux habitats mésiques mais n’étaient pas des échecs ou « instables ». Elles ont bien survécu jusqu’àprésent dans de tels habitats, avec d’autres adaptations structurales plus anciennes (ex. plaque de perforation scalariforme)qui conviennent encore à ces habitats. Ces caractéristiques « primitives » sont évidentes dans les embranchements premiersdes arbres phylogéniques basés sur de multiples gènes. Des caractéristiques plus anciennes peuvent encore être fonctionnel-les et persistent ainsi, même si de nouvelles formules sont prédominantes en effet. Il y a cependant plusieurs exemples « d’é-vasion » dans plusieurs clades (itérations écologiques et poussées de spéciation et de diversification reliées à de nouvellesfaçons de composer avec l’économie d’eau), alors que d’autres embranchements, d’autres clades sont écologiquement plusstatiques pendant de longues périodes de temps. Les mécanismes physiologiques et anatomiques plus récents ont permis d’a-border des habitats caractérisés par d’importantes fluctuations au plan de l’humidité. Le bois évolue progressivement et unrenversement littéral d’un caractère peut être inhabituel : l’information génomique et développementale a réponse à ces chan-gements. Le bois est un tissu complexe, et chacune de ses composantes histologiques présente un polymorphisme commemécanisme évolutif. Les types de cellules à l’intérieur du bois évoluent en collaboration. Les changements des caractéristi-

Received 26 January 2012. Accepted 18 April 2012. Published at www.nrcresearchpress.com/cjb on 20 September 2012.

S. Carlquist. Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA.

E-mail for correspondence: [email protected].

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Botany 90: 901–940 (2012) doi:10.1139/B2012-048 Published by NRC Research Press

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ques du bois (ex. la simplification de la plaque de perforation scalariforme) sont habituellement homéoplastiques. Les diverschangements dans la physiologie, la morphologie et l’anatomie de la feuille et du port accompagnent l’évolution du bois etle bois doit être étudié en relation à l’écologie sur le terrain, une information qui ne peut être glanée de la littérature oud’autres sources secondaires. L’hétérochronie (juvénilisme prolongé, maturité accélérée) caractérise beaucoup le xylème desangiospermes, beaucoup plus que celui d’autres végétaux vasculaires, et ces mécanismes ont résulté en plusieurs change-ments remarquables (ex. les monocotylédones ont un xylème juvénile permanent, les arbres sont un exemple de maturité ac-célérée). La compréhension de plusieurs caractéristiques réussies de l’évolution du bois des angiospermes doit ultimements’appuyer sur les synthèses.

Mots‐clés : théorie de l’évasion, polymorphisme des types cellulaires, évolution collaboration des types cellulaires, itérationécologique, réversibilité de l’embolie, phylogénie moléculaire, physiologie du bois, xylème.

[Traduit par la Rédaction]

1. Introduction

What we know now but haven’t synthesizedAn enormous amount of new information relevant to

understanding wood function and structure — and thereforewood evolution — has appeared within the past 30 years.The fields in which this massive informational gain has oc-curred include wood physiology, scanning electron micro-scopy (SEM), transmission electron microscopy (TEM),ecological wood anatomy, comparative wood anatomy, woodmechanics, microfluidics, and molecular phylogenetics.Although many more details in these fields remain to be in-vestigated, the shortage that currently looms is the willing-ness to synthesize.

Wood physiology branches outWood physiology, like wood anatomy, was promoted in

earlier years within forestry institutes. The Harvard woodphysiologist Martin H. Zimmermann did endow his studentswith enough breadth in wood physiology so that they couldfit into botany and biology departments of universities, andZimmermann’s 1983 book Wood Structure and the Ascent ofSap did, as the title indicates, reach into structural matters.However, the nature of physiology is to proceed one experi-ment at a time, and the luxury of wide synthesis was not, andprobably could not, be extensively enjoyed fully during Zim-mermann’s time.

Wood anatomy as an indoor enterpriseThe strengths of systematic wood anatomy, from Solereder

(1885) onward through Metcalfe and Chalk (1950) to thepresent, have been accumulation of vast amounts of data,mostly based on dried specimens. The weaknesses of compa-rative wood anatomy lay in its separation from knowledge ofecology, habit, and other relevant information. Thus, Met-calfe and Chalk (1950) relegated “ecological anatomy” tosmall separate accounts in a handful of their familial summa-ries, a practice followed even by Gregory (1994). Twentiethcentury wood anatomy was defined, and limited, by the exis-tence of xylaria — wood collections, almost always in for-estry institutes, in which sample boards, from which smallbits could be removed for study, were kept in drawers. Bybeing thus separated from their living context, the xylariumsamples lost much of their significance. The species thatformed the nucleus of xylaria were trees that were useful orpossibly so, and the specimens of shrubs, woody herbs, and

lianas were less represented. Workers such as C.R. Metcalfe,I.W. Bailey, and others did not question this and chose studygroups that were “woody” and suited for sectioning by a slid-ing microtome. This resulted in conceptual shortfall. Baileyexulted in the fact that his trends of wood evolution were de-rived independently of systematics. Indeed, during almost allof the 20th century, angiosperm systematics and phylogenywere pursued in intuitive ways by collecting data that sug-gested relationship in the hope that a natural system wouldbe revealed. I.W. Bailey, whose knowledge of wood anatomywas encyclopedic, was aware that wood ecology was thedriving force in wood evolution (personal communication,1956) but avoided incorporating this in his work. Shifts inwood structure were, to him, an evolutionary verity on theirown terms. The trends that he proposed were progressivechanges that need not be compared with what plants weredoing in nature, or any physiological features (little woodphysiology had been done in that era). These methods wereadopted by his students Frost (1930a, 1930b, 1931), Kribs(1935, 1937), Barghoorn (1940, 1941a, 1941b), and Cheadle(1942, 1943; see also Carlquist 2012). Xylem was viewed aschanging inexorably from “primitive” to “specialized.” Allxylem data were considered referable to this progression.

Synthesis as reachable, even inevitableBooks that bridged lines in wood research (e.g., Braun 1970;

Carlquist 1975) were almost palpably resisted and did not reachtheir intended audience. In retrospect, we can see that the widerthe synthesis, the less prepared the reader and therefore thegreater the effort required for full comprehension. Today, wecan no longer postpone bridging the gaps between disciplinesthat never should have been separated. Detailed criticisms offailures in synthesis are unnecessary. We can use informationproduced by all workers, regardless of how narrowly it was ac-quired and described. The only constraint in a new synthesis ofthe wood form–function–development–phylogenetics contin-uum is that any new synthesis must be in accord with all ofthe available facts. Comparative data do not lie, but interpretingthem may be difficult.

2. From risk-averse to repair-capable:evolution of wood hydraulics

Vessels: a problematic invention?A pair of papers (Hacke et al. 2007; Sperry et al. 2007)

dealt with how certain wood conductive features may have

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evolved. The conclusion by Sperry et al. (2007) invites fur-ther comment: “vessel evolution was not driven by lowerflow resistance, and it may have been limited to wet habitatsby cavitation risk.” They also said that “truly efficient andsafe vessels evolved much later than vessels per se, perhapsin concordance with larger radiations among core angio-sperms.” Sperry et al. (2006) stated that “the evolution ofvessels in angiosperms may have required early angiospermsto survive a phase of mechanic and hydraulic instability.”These generalizations deserve re-examination.

What early angiosperm wood looks likeThe first five figures (Figs. 1–5) are designed to show the

characteristics of early angiosperm wood and to show thatthese apparently ancient features have survived in a numberof major different clades. This array of illustrations showswhat the prototypes of angiosperm wood were like. The con-clusion first: these woods did have moderately wide tracheids(Figs. 1A–1B) or narrow vessels (Figs. 2–5) with high resis-tivity but, therefore, great potential safety. The end walls oftracheids or vessels have scalariform pitting, like circular pitswidened out as the cells widen out (Figs. 1D, 1F), a likelyexplanation. Conifers retain the circular shape because it isrequired by the torus–margo system. The earliest angiospermwoods look juvenilistic (Carlquist 2009b) and have uprightray cells. Axial parenchyma is only occasional at first(Fig. 1E).In vessel-bearing angiosperms, the end walls are perfora-

tion plates and are scalariform and rather long (Fig. 2A), butwith lateral walls that are also scalariform, just with narrowerpits (Figs. 2C, 4E). The perforation plates in early angio-sperms retain various amounts of pit membrane remnants,from none (Figs. 2B, 5C–5F) to extensive sheets (Fig. 3B),variously interrupted by pores (Figs. 3C, 4A–4C, 5A–5B) orthreads or networks (Figs. 4D, 4F, 5E). These are bestviewed in thick sections and seen from inside a vessel (e.g.,Figs. 2E, 3D, 5A–5F) because no pit membrane is sectionedaway (Figs. 3A–3B) and we get an idea of how porous thedouble pit membrane is (Fig. 4A, above) compared with thesingle thickness of the primary wall in the perforations(Fig. 4B). Why are the pit membranes in perforations sowidespread and in so many orders of angiosperms? Theseare the structures that furnish not only resistance to flow, butalso, via a trade-off, confining of air bubbles when water col-umns are broken into single cells. This is the advantage oftracheids, so that vessels such as those in Figs. 2–5 are like“supertracheids,” better than tracheids in flow where diame-ter is concerned, but with end-wall impedance that providessafety.

Making comparisonsThe conclusions of Hacke et al. (2007) that early vessels

are of little advantage are acceptable as initial probes intothe early hydraulic history of angiosperms, but they are inneed of elaboration and modification. “Resistivity” to flowin woods can be measured, but a wood with higher resistivitymay merely be a wood with a construction biased in favor ofsafety. “Vulnerability” (to cavitation formation) can also bemeasured (Vogt 2001). Vogt (2001) selected for comparisontwo woody angiosperms with different strategies: Sorbus haslow vulnerability and has vessels that rarely cavitate, whereas

Sambucus has high vulnerability and its vessels cavitate fre-quently but refill readily. Are such differences gradually ac-quired? Probably not. Schisandraceae is a family thatqualifies as “early” (Illicium, which has plesiomorphic xylemfeatures, is now often put in the same family). Schisandra canhave wide vessels with simple perforation plates (Carlquist1999), surely hallmarks of low resistivity, whereas Illiciumwoods have the opposite hydraulic characteristics, high resis-tivity owing to long scalariform perforation plates and narrowvessels (Carlquist 1982).How does one compare the hydraulic features of an all-tra-

cheid wood with those of a vessel-bearing wood? Resistivityof a stem of either can readily be measured (Hacke et al.2007; Sperry et al. 2007), but if we are comparing how ves-sels conduct as compared with tracheids, shouldn’t we com-pare a wood composed wholly of vessels with an all-tracheidwood? There is no such thing as a wood composed wholly ofvessels, of course. Thus, the conductive effect of a limitednumber of vessels per square millimetre must really be con-sidered in contextual terms. On average, about 0.25 mm2 per1.00 mm2 transection is devoted to vessels (Carlquist 1975,p. 206). Thus, vessels could be said to be four times as effec-tive as tracheids in conduction. The proportion of woodtransection devoted to vessels is even smaller in some kindsof plants (succulents, desert shrubs) and greater in others (lia-nas). In some of these woods, vessels are combined with tra-cheids, which are conductive (Sano et al. 2011), whereas inothers, the vessels are combined with nonconductive cells(libriform fibers); there is no known way to measure the con-ductive capabilities of the ground tissue exclusive of the ves-sels. Certainly vessels are better designed for conductiveefficiency than an equivalent transectional area of tracheids.

Perforation plates: how much resistivity?Do scalariform perforation plates, characteristic of “primi-

tive” woods, contribute heavily to resistivity? Sperry et al.(2007) claimed that “primitive” vessels have a resistivity of57% ± 15%, whereas Ellerby and Ennos (1998) placed thefigure for scalariform plates much lower (between 0.6% and18.6%). The sample studied by Sperry et al. (2007) is quiteunusual: Ascarina, Hedyosmum, Illicium, and Trimenia haveprominent pit membrane remnants in the perforations (Carl-quist 1992), and these would certainly block flow. The vesselelements in such genera can be considered “semi-tracheids.”In fact, “ordinary” scalariform perforation plates without suchpit membrane remnants are quite common: they characterizegenera such as Alnus, Betula, Cornus, Ilex, and Magnoliaand must be counted as well adapted to their habitats. Thehabitats of these genera do tend to be mesic (Carlquist1975), so the point made by Sperry et al. (2007) that earlyangiosperms were not conductively efficient does carry someweight, but these genera are all large and conspicuous ones,not at all relictual.

Resistivity is not all bad: it’s part of a trade-off“Primitive” woods can be hypothesized to have higher resis-

tivity. In part, this is because of narrowness of vessels, whichincreases resistance inversely to the fourth power of the vesselradius according to the much-cited Hagen–Poiseuille equation(Zimmermann 1983). Narrow vessels can have scalariform per-foration plates (Illicium) or simple perforation plates (desert

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shrubs). One could generalize by saying that wood evolutionhas proceeded from high resistivity and low vulnerability tolow resistivity combined with high vulnerability. One can se-lect examples of such differences in strategy. For example,Acer (Taneda and Sperry 2008) and Sorbus (Vogt 2001) tendnot to develop vessel cavitations even on more stressful days,whereas Sambucus (Vogt 2001) and Quercus (Taneda andSperry 2008) do develop cavitations on a regular basis and re-fill cavitated vessels. The shift from low vulnerability – highresistivity to high vulnerability – low resistivity is not a linearprocess. There are “breakouts” represented by the clade thatincludes Asteraceae (Fig. 14), and many shifts (involving sev-

eral kinds of wood histology, not to mention foliage alteration)seem to have occurred. The early angiosperms do have woodswith high resistivity, but this is apparently not a disadvantagebecause they live in moist areas where transpiration is slow.Scalariform perforation plates can promote conductive

safety by compartmentalization of air bubbles (Slatyer 1967;Sperry 1986). If, as Ellerby and Ennos (1998) contend, vesselend walls add little friction (whereas vessel lateral walls addproportionately more, especially when narrow), scalariformperforation plates do not seem to be a strongly negative factorin vessel evolution. Available data do suggest that some pres-sure for simplification of perforation plates occurs in “primi-

Fig. 1. Wood of vesselless angiosperms. (A–E) Amborella trichopoda (Amborellaceae). (A) Transection showing lack of vessels (but varia-bility in tracheid diameter). (B) Tangential section. Rays and axial parenchyma are so abundant that no tracheid is isolated from some kind ofparenchyma cell. (C) Radial section. Section through a multiseriate ray to show that most cells are square to upright in shape. (D) Radialsection showing end walls of tracheids. Pitting is scalariform on end walls of wider tracheids. (E) Transection. Parenchyma is occasional inthe wood as a whole but sometimes occurs in bands (dot in each axial parenchyma cell). (F) Tetracentron sinense (Trochodendraceae). SEMphotograph of scalariform end-wall pitting showing small pores in the pit membranes.

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http://www.nrcresearchpress.com/action/showImage?doi=10.1139/b2012-048&iName=master.img-000.jpg&w=336&h=450

tive” woods: the lianoid Dilleniaceae evidently abandoned thescalariform condition rapidly (whereas the remainder of thefamily did not) in accordance with a shift in the balance inthe trade-off in favor of high flow and low resistivity.

It’s not all about vessel elementsCell types other than vessel elements may play decisive

roles in the conductive efficiency – conductive safety trade-off. An appreciable number of woody angiosperms have ves-sels embedded among tracheids (Carlquist 1985a), which can

be shown to be conductive and to resist embolism formation(Sano et al. 2011). Vessels can be embedded among tracheidseven in a wood that also has libriform fibers, as in Ceanothus(Figs. 6A, 6B).Diffuse parenchyma is usually dispersed among tracheids

(Fig. 2E) and may serve to maintain water columns in thetracheids (as well as in the vessels), judging from the avail-able data (Holbrook and Zwieniecki 1999; Wheeler and Hol-brook 2007), perhaps maintaining osmotic pressures bytransferring sugars into the water columns (as with Acer;

Fig. 2. Wood features of Aextoxicon punctatum (Aextoxicaceae) showing features symplesiomorphic for a vessel-bearing angiosperm. (A–E) SEM pictures from radial section. (A) Entire perforation plate. Above the perforation plate are several tracheids. (B) Edge of perforationplate plus a tracheid, below, showing four larger bordered pits. (C) Tip of vessel element showing portion of perforation plate, left, plusscalariform vessel-tip-to-vessel-tip pitting. (D) Portion of a perforation plate that has retained pit membranes; membranes are absent in placesdue to sectioning. (E) Portions of perforations that retain a network of pit membrane remnants. (F) Portion of transection. Axial parenchymais common and diffuse; axial parenchyma cells are indicated by dots in the central portion of the photo but are common throughout the wood.

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Sauter et al. 1973). Root pressure is certainly a factor in re-moving embolisms (Fisher et al. 1997). Notice that the “lesswoody” angiosperms (perhaps the majority of angiosperms,certainly all of the monocots) could refill embolized vessels

at least partially by means of root pressure (Davis 1961),which is a parenchyma-generated phenomenon. The rootpressure needed to reverse an embolism may be small (Yangand Tyree 1992).

Fig. 3. SEM micrographs of portions of radial sections to show degrees of pit membrane retention in perforation plates. (A, B) Carpodetusserratus (Rousseaceae). (A) Entire length of a perforation plate. One-half has been sectioned away, and lack of pit membrane remnants inmost perforations may be due to sectioning. (B) Portion of a perforation plate. One cell mostly but not entirely sectioned away; pit membranesare intact. Some perforation plates in this section naturally lack pit membrane remnants, but many have them. (C) Illicium floridanum (Illi-ciaceae). Portions of perforations as seen from inside a vessel element (the two halves of the perforation plate therefore intact). Pit membraneremnants are present, but pores of various sizes are present.

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The emerging pictureRecent wood physiological literature emphasizes that much

angiosperm speciation has been attended by development ofvessels prone to embolism risk combined with mechanismsfor countering those risks. Vessel cavitation due to droughtis probably different from that due to freezing, if the exam-ples shown by Langan et al. (1997) are more widely applica-

ble. We have an idea of the probable mechanisms for refillingvessels (McCully et al. 1998; Holbrook and Zwieniecki 1999;Wheeler and Holbrook 2007), as well as some of the mecha-nisms that tend of prevent embolism formation (Hacke et al.2000, 2001). Vessels can evade embolisms by being narrow,whereas wider ones in the same plant are embolism-prone(Hargrave et al. 1994). This contrasts with tracheids in which

Fig. 4. SEM micrographs of vessel portions from radial wood sections of Paracryphiaceae. (A–E) Sphenostemon. (A) S. lobospora. Perfora-tions in which the double nature of the pit membrane is shown (compare center with top of photo); pit membrane of only one cell, below.Note that fewer and smaller pores are present in the intact portion of the pit membranes. (B) S. lobospora perforation portions. Only one ofthe double pit membranes is present; larger holes are due to sectioning, but the remainder of the pit membrane represents a natural conditionof porousness. (C–D) S. pachycladum. Portions of a perforation plate. (C) Near end of perforation plate showing a greater degree of pitmembrane presence. (D) Center of perforation plate’s only strandlike pit membrane remnants are present. (E) S. lobospora. Scalariform lateralwall pitting. (F) Paracryphia alticola. Portion of perforation plate seen from inside vessel element; pit membrane remnants are mostly artifact-free and are extensive.

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the water columns are far more resistant to embolism forma-tion (Sano et al. 2011). The state of our knowledge has beensuccinctly summarized by Vogt (2001):

Several papers have shown refilling during the growingseason in different species, for example, in Plantago (Mil-burn and McLaughlin 1974), Zea mays (Tyree et al.1986), and Rhapis excelsa (Sperry 1986). Refilling is ex-plained by predawn water potentials rising to near zero(Tyree et al. 1986), rainy periods (Sperry 1986), and rootpressure (Milburn and McLaughlin 1974; Pickard 1989).Recent studies, however, indicate that embolism removal

may be concurrent with transpiration and with consider-able negative water potentials in intact nearby vessels(Salleo et al. 1996; Borghetti et al. 1998; McCully 1999;Tyree et al. 1999; Melcher et al. 2001). It has also beenhypothesized that vessel embolism is a reversible phenom-enon made possible by the interaction of xylem parench-yma, vessel wall chemistry, and the geometry ofintervessel pits (Holbrook and Zwieniecki 1999).

The achievements in improving our understanding of howsome vascular plants resist embolisms whereas others experi-ence frequent events of cavitation followed by refilling are

Fig. 5. Diversity in perforation plates, seen in SEM micrographs of radial sections. (A–C) Heliamphora heterodoxa (Sarraceniaceae).(A) Pores present only in central portions of perforations. (B) Intermediate presence of pit membrane remnants. (C) Perforation plate withminimal presence of pit membrane remnants. (D) Darlingtonia californica (Sarraceniaceae). Perforation plates are small and have few bars.(E) Berzelia cordifolia (Bruniaceae). Bars are relatively few, but reticulate pit membrane remnants are present. (F) Drosera capensis (Droser-aceae). Perforation plate simple, but only half the diameter of the vessel.

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evident from the above studies. We know enough to see thatthere is a diversity of strategies that occur in wood structureof different species. There are obviously trade-offs betweenconductive efficiency and conductive safety. If the angio-

sperms began with wood that featured conductive safety,which therefore limited them to mesic habitats, there havebeen many shifts, as well as diversifications of mechanismsfor conductive safety, and therefore a complex picture has

Fig. 6. Wood sections showing presence of vasicentric tracheids, vascular tracheids, and degrees of vessel grouping. (A–B) Ceanothus thyrsi-florus. (A) Transection. The background tissue consists of narrow libriform fibers; several vessels are embedded, center, in a group of vasi-centric tracheids (narrower than the vessels, but wider than libriform fibers). (B) Radial section. A vessel is seen, center; to the left of it arevasicentric tracheids; to the right of the vessel are libriform fibers. (C–D) Artemisia filifolia. (C) Transection. The large vessels denote early-wood; the three or four terminal layers of latewood to the left of those are narrow vessels and vascular tracheids. (D) Tangential section. Theleft half of the photo consists of narrow vessels with simple perforation plates; in the right half are narrower tracheary elements of similarlength that lack perforation plates and are therefore vascular tracheids. (E–F) Portions of a transection of Artemisia tridentata wood. (E) Aportion of two growth rings from a period of active growth. A layer of interxylary cork delimits the latter half of a growth ring (left) fromearlywood (right). The latewood vessels are large, but very narrow vessels and vascular tracheids are formed just prior to the interxylary corklayer. The earlywood of the growth ring at right begins with rather narrow vessels, indicating growth in response to moisture availability butcold temperatures, and is followed by wider vessels formed during warmer months. (F) Terminal growth rings of the same section; as thegrowth of this stem declines, several rings of very narrow vessels are formed.

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Fig. 7. SEM images of types of vessel wall sculpturing that are claimed to prevent air embolisms or help in refilling of vessels. (A) Tiliaamericana (Tiliaceae or Malvaceae). Slender helical thickenings with tapered endings. (B) Poliomintha longiflora (Lamiaceae). Paired thick-enings alongside pits. (C) Prostanthera rotundifolia (Lamiaceae). Sparse, clearly defined thickenings that tend to be associated with pit aper-tures. (D) Olea cunninghamii (Oleaceae). Numerous but short and shallow thickenings on an unpitted wall surface. (E) Clematis vitalba(Ranunculaceae). Helical thickenings, prominent adjacent to the pits, plus grooves interconnecting pit apertures. (F) Metrosideros tomentosa(Myrtaceae). Inconspicuously warted vessel wall, plus a network of wall material covering two pit apertures. (G) Parkinsonia aculeata (Faba-ceae). Vessel wall seen from the outside; numerous vestures are seen in the pits; pit membranes are removed by sectioning except in the upperleft corner. (H) Cercidium floridum (Fabaceae). Vessel wall seen from inside vessel; no texturing is present on wall surface, but vestures maybe seen in the pit apertures. (I) Cercidium australe (Fabaceae). Coarse interconnected warty structures on the inside wall of a vessel; pits havecollarlike rims (“crateriform pits”).

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emerged. Do we know enough that we could predict theprobable efficiency–safety trade-offs for most angiosperms?The above results indicate that we are further along that path-way than might have been thought possible a few decadesago. We have reached a stage at which wood histology canbe predictive of probable physiological characteristics. If my(Carlquist 1975) book was dismissed as premature earlier(e.g., Zimmermann 1983), it might look foresighted, ifflawed, in the light of subsequent wood physiological work.The sections below attempt to promote understanding of

how we can couple knowledge of wood physiology and datafrom wood anatomy. In doing so, we must, however, takeinto account the fact that habit and foliar characteristics canbe of overriding importance or moderating influences, atleast where wood physiology is concerned. Therefore, thepredictive value of wood histology must be tempered bywhole-plant knowledge. A section below citing such fea-tures — which may range from endomycorrhizal roots tosunken stomata or crassulacean acid metabolism — can beincluded in our interpretations of wood anatomy and physiol-ogy of any particular plant.

3. Vessel repatterning as a way ofadaptation: woods of Asteraceae asexamples

Asteraceae as an experiment in wood anatomyAsteraceae (Compositae) are a family of at least 23 000

species (Funk et al. 2009). Commonly thought by NorthTemperate botanists to be nonwoody, an appreciable numberare shrubs or trees, especially in subtropical latitudes. Mostannuals in the family have some cambial activity.Wood anatomy in the first-departing branch; Barnadesieae

(Carlquist 1957), is essentially the same as that of the crowngroup, Madieae (Carlquist et al. 2003; phylogeny from Funket al. 2009), in qualitative characters. There is very little“evolutionary” range, meaning essentially that the differencesamong species are the result of rapidly and recently acquiredcharacter states that reflect ecology. Even the sister group of

Asteraceae, Calyceraceae, has the same basic qualitativewood features. Wood of the family can be likened to a natu-ral experiment designed to show how wood histologychanges in response to ecology and habit.

Ecology as the keyThe discovery that wood of Asteraceae was an ideal indi-

cator of ecology and that conclusions were applicable towoody angiosperms at large was fortuitous, a by-product ofmy early interest in the family. I monographed the wood ofthe family tribe by tribe and found no phylogenetic patterns(in those days, one expected phylogenetic dividends fromany comparative anatomical investigation). Only when sum-marizing the data from the family collectively (Carlquist1966) did I see that the patterns were quite precise ecologicalindicators. This is not surprising, considering that compositesrepresent a relatively recent, mostly post-Miocene explosion(Funk et al. 2009) into a very wide range of habitats: veryfew places in the world are free from them. An abbreviatedversion of my 1966 tabular summary (Table 1) tells the story.

How narrow must vessels be for safety?As mentioned above, narrow vessels tend to be safe (emb-

olize less often than wide vessels) in a particular wood (Har-grave et al. 1994), whereas wider vessels promote flow withless friction: the Hagen–Poiseuille equation (Zimmermann1983). In wet forest trees, an average vessel diameter of100 µm is not unusual (Metcalfe and Chalk 1950). Thus,even “mesic” Asteraceae (Table 1) are biased in favor ofsafety, probably because the family so characteristically occu-pies disturbed sites. One could pick a particular vessel diam-eter that seems to represent a midway point in the safety–efficiency trade-off, but we need to remember that withinany given wood sample, there is considerable deviation invessel diameter. However, the data in Table 1 suggest thatthe safety–efficiency threshold value might lie at around 55–60 µm. Note should be taken that wood does not operate onthe basis of an “average” cell, but on the basis of all of itsconductive cells.

Table 1. Quantitative wood features of Asteraceae.

n VD, µm V/G VEL, µm Helices, % Storied, %RainfallMesic 161 66 3.04 282 49 48Dry 129 39 5.20 198 57 37Desert 38 34 8.37 155 68 68LatitudeTemperate 191 51 5.68 191 61 53Tropical 137 65 2.64 300 46 36HabitAnnual or biennial 35 46 2.74 186 34 6Caudex perennial 29 39 4.45 152 77 48Shrub 173 45 6.26 240 63 50Tree 38 84 1.94 312 68 52Rosette tree or shrub 52 68 2.22 292 19 50All species 328 51 3.62 235 55 45

Note: VD, mean vessel diameter (outside diameter; lumen diameter would be 3–5 µm less); V/G, mean number of vessels pergroup; VEL, mean vessel element length; helices, %, percentage of species with some kind of helical sculpturing on vessel walls;storied, %, percentage of species with one or more types of storying.

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Why compromise?The growth ring is, of course, an ideal way of solving the

trade-off problem in vessel diameter (Figs. 6C–6F). There aremany kinds of growth rings (Carlquist 1980, 1988, 2001a),so the solutions are multiple. Ideally, one would design early-wood vessels that would be wide enough to supply activelytranspiring foliage while soil moisture is available. The early-wood vessels would either be subjected to few embolisms orbe able to repair them. The latewood vessels would be nar-row enough so as to deter embolism formation and wouldprovide water columns wide enough to conduct sufficientwater when the earlywood vessels permanently embolize.This curriculum probably is close to what particular plantsdo (e.g., Hargrave et al. 1994), but we do not have species-by-species knowledge of growth ring physiology — only afew species have been studied in this respect. Even for thosefew species, the physiological behavior of subsidiary con-ducting cells (vasicentric tracheids, tracheids, etc.) is un-known (with a few exceptions: Braun 1970; Sano et al.2011) because the physiology of nonvessel cells in vessel-bearing wood is more difficult to access.

More vessels or fewer?Vessel diameter and vessel density (number of vessels per

square millimetre of transection) are inversely proportional,within limits. When these two features are graphed (Carlquist1975, p. 163), there appears to be a “packing limit.” If onemakes calculations of vessel area per square millimetre oftransection (Carlquist 1975, p. 206), one finds that differentplant types differ quite markedly: trees have 0.24 mm2 vesselarea/mm2 of transection; lianas, 0.36; shrubs, 0.19; and stemsucculents, 0.09. Considerable wood volume is devoted tofunctions other than conduction. Mechanical strength, sheathingof wide vessels, water storage, starch storage, flexibility, andliving cells supporting the conductive system are some of thefunctions that come to mind. These functions cannot be meas-ured as readily as conduction, so they tend to be neglected.

Why group vessels?Some angiosperms have tracheids as a background tissue

or vasicentric tracheids near vessels (for criteria, see Carlquist1988, 2001a; Sano et al. 2011). Tracheids are conductive andhave wide-bordered pits, fiber-tracheids have vestigial borderson pits and are not conductive, and libriform fibers have sim-ple pits and are not conductive. When a wood with tracheidsor vasicentric tracheids experiences cavitations, tracheids canserve to maintain the conductive pathways until vessels arerefilled. Tracheids or vasicentric tracheids are much lessprone to cavitation than vessels. This has an interesting con-sequence. If libriform fibers are present, as they are in Aster-aceae, there is another mechanism that can maintainconductive pathways: grouping of vessels. If a larger vesselembolizes, an adjacent smaller vessel may not, so the smallervessel maintains the conductive pathway. Asteraceae havevessel grouping (Table 1), and its degree is proportional tothe likelihood of failure, based on the dryness or seasonalityof the habitat (Artemisia, with extensive vessel grouping,lives mostly in dry habitats; Figs. 6C–6F). Thus, vesselgrouping alone can be used as a way of detecting whetherthere are conductive imperforate tracheary elements presentin a wood. If vessel grouping is below about 1.3 vessels per

group in a vessel-bearing angiosperm, tracheids are probablypresent. Also, vessel grouping potentially offers more redun-dancy than ungrouped vessels.

How should vessels be grouped?Vessels may be grouped in various ways for various rea-

sons (for a review, see Carlquist 2009a). The most commontype of grouping, found in Asteraceae, is radial clusters orchains. This type of grouping provides a way in which therecan be a “relay,” newer vessels adjacent to the older ones.Such groupings can be extended in diagonal pathways also,so that if grouping is extensive, any vessel in a stem will beadjacent to some other vessel. Preservation of conductivepathways despite cavitations seems an important strategy. Ifthe pathways still contain water columns, even though somevessels are cavitated, reconstitution of the pathway can takeplace.

What is the significance of vessel element length?As Table 1 shows, vessel elements are markedly shorter in

species of dry environments. Although Zimmermann (1983)failed to find significance in this, Slatyer (1967) and Sperry(1986) have shown that there is a tendency for air embolismsto end at the ends of vessel elements. Thus, the shorter thevessel element, the more localized are the interruptions tothe conductive system. Smaller, more localized embolismsare more readily reversed (Holbrook and Zwieniecki 1999).Longer vessel elements offer less end-wall resistance and arethus of value in mesic habitats where conductive efficiency isfavored (Ellerby and Ennos 1998; Sperry et al. 2005).

What is the significance of vessel length?Long vessels (an uninterrupted file of vessel elements) can

extend the length of a plant, thereby being the ultimate inconductive efficiency (Zimmermann and Jeje 1981). How-ever, shorter vessels may be present in a wood as well as lon-ger vessels; there is commonly a variety of vessel lengths in agiven wood (Zimmermann and Jeje 1981). A narrower vesselis often shorter, often less than 4–10 cm. Shorter vessels rep-resent a conductive compromise: if vessels are better at con-ductive efficiency than tracheids because of diameter, longervessels are better at conduction, because they represent nearlyideal capillaries, a triumph of the woody dicot that has cam-bial activity the length of the plant. Monocots, which haveadventitious roots, lack this continuity and have other pat-terns (Carlquist 2012). Shorter vessels offer safety: confine-ment of air embolisms to a shorter vertical length of a watercolumn rather than the length of a plant. One can considerthem a sort of “megatracheid.” Not surprisingly, shorter ves-sels are found in latewood of growth rings, whereas longervessels occur in earlywood (Zimmermann and Jeje 1981).

Why is there sculpturing in vessel elements?The vessel elements of Asteraceae are often provided with

thickenings on the lumen surface, or grooves that intercon-nect pit apertures (“coalescent pit apertures”), or thickeningsthat parallel the grooves (Table 1). We have known for a longtime that helical sculpturing is more common in plants ofcolder or drier habitats (Table 1). It is also more pronouncedin latewood than in earlywood (Carlquist 1975). These factscounter the idea by Jeje and Zimmermann (1979) that helical

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thickenings accelerate flow, because helical sculpturing ismost prominent in precisely the vessels in which flow ischaracteristically slowest. Although an increase in surface re-lief on the vessel surface may be varied in shape and promi-nence, all manifestations probably represent an increase insurface area (Fig. 7). Such sculpturing has the effect of re-ducing air bubbles in vessels because it increases wettabilityand thus reverses (and well as presumably prevents) cavita-tions (Carlquist 1982, 1983; Kohonen and Helland 2009).Kohonen and Helland (2009) said that wettability is in-creased by surface relief of vessels: “wall sculpturing doesenhance wettability,” which tends to prevent cavitation andalso aids in “the removal of bubbles in microfluidic chan-nels.” Forms of helical sculpturing have evolved many timesindependently in woody angiosperms (homoplasy) and areprobably easily achieved because the pattern of these struc-tures seems to parallel the cyclosis of the cytoplasm that laiddown the secondary walls (Figs. 7A–7E).

Vestured pitsVestured pits (absent in Asteraceae, but characteristic of

some other groups, notably Myrtales) and vesturing on vesselsand tracheids (wart-like coverings of the wall facing the lumen)are an allied phenomenon. Vestured pits do not form a categoryseparate from vesturing, and both may be found in some genera(Metrosideros; Meylan and Butterfield 1978). Vesturing may bemore prominent in latewood (Parham and Baird 1974). Theidea that vestures form a flat-topped array that prevents the pitmembrane from excessive deflection (Zweypfenning 1978; Jan-sen et al. 2003) has been countered by the demonstration thatthese protuberances increase wall surface and thus have muchthe same function as helical sculpturing (Kohonen and Helland2009; Choat et al. 2004). Not only do vesturing patterns on lu-men surfaces run counter to the Zweypfenning explanation,there are instances of vestured pits in which the warts are clus-tered at the pit apertures and are not at all close to the pit mem-brane (Fig. 7) or are even on the pit cavity surface, as inconifers (Meylan and Butterfield 1978).

Are these vessel features reversible?Probably all of the vessel features described above can be

altered, which may not be the same thing as reversion. Cer-tainly a growth ring shows how readily wide and narrow ves-sels can be formed by the cambium at appropriate times and,accordingly, how vessel density or sparseness in a wood canbe achieved. As various clades of Asteraceae have adapted todesert conditions, narrowing of vessels has occurred, and thereverse pattern has occurred as a clade enters moister habitats(e.g., Dubautia; Carlquist et al. 2003). Change in vessel ele-ment length has a phylogenetic aspect in woody angiospermsas a whole (Bailey 1944), but in Asteraceae, a wide span ofthe gamut from permanent juvenilism to accelerated adult-hood is evident (Carlquist 2009b), perhaps because of thevalue of shorter vessel elements in xeric habitats and longerones in wet habitats, as cited above. Length of fusiform cam-bial initials is easily modified by increasing or decreasing thepace of vertical (or pseudotransverse) divisions in these ini-tials. Storying (Table 1) is also a reflection of this: the fewerthe vertical (or pseudotransverse) divisions in fusiform cam-bial divisions in a stem, the later the onset of storied histol-ogy in the wood. In Asteraceae, storying is thereby a

combination of length of fusiform cambial initials (whichgoverns the length of vessel elements, an adaptive feature re-lated to ecology) and the degree of juvenilism in the wood (afeature related to habit and, indirectly, to ecology).

4. Angiosperm vessels: the validity of being a“primitive” wood

Vessel origin: what do we know?Xylem evolution is often presented as a progression toward

an optimal condition. This is a fallacy, because there aremany optimal conditions, especially in wood as diverse asthat of angiosperms. More importantly, the idea of an optimalstructural condition does not take into account why “primi-tive” (plesiomorphic) conditions should be extant today. Infact, angiosperm woods with plesiomorphic features are rela-tively common. We need to account for why these types arealive today. Woods with scalariform perforation plates areabundant today, even forming whole forests (Betula, Cornus,Liquidambar).The idea that vessels represent a key innovation in angio-

sperms that has led to dominance and radiation of angio-sperms has often been held, if only implicitly. We now knowthat the earliest branches of the angiosperm tree are vessel-less (Amborella, Nymphaeales), although secondary vessel-lessness has occurred a few times (Winteraceae,Trochodendraceae; Chase et al. 1993; Soltis et al. 2000,2011). Obviously, invention of vessels took place early in an-giosperm evolution, according to these molecular phyloge-netic trees. Vessel origin may have occurred more than once:monocots might have begun in a vesselless condition,although the evidence for that is arguable (Carlquist 2012)and depends on the point at which perforations are suffi-ciently clear of pit membranes to qualify a cell as a vesselelement.In woody angiosperms, a division of labor (i.e., vessel ele-

ments vs. imperforate tracheary elements, with progressivelymore differences between these types) is inferred (Bailey andTupper 1918; Bailey 1944). If we look at particular woods,this idea can be supported, but the more we look at woodphysiology, the more complicated the situation becomes.“Primitive” angiosperm woods have high resistivity (i.e., con-duction efficiency lowered by friction) according to the dataof Sperry et al. (2007) and are thus not a structural formulathat is suited to a wide range of ecological sites. “Vessel evo-lution was not driven by lower flow resistance, and it mayhave been limited to wet habitats by cavitation risk” (Sperryet al. 2007). Is this literally true? Clearly, woods with morenumerous plesiomorphic features (scalariform perforationplates, tracheids as a ground tissue, and diffuse axial paren-chyma) are much more common in mesic habitats than indrier ones (Carlquist 1975), with some seeming exceptionssuch as Bruniaceae and Grubbiaceae. Certainly angiospermswith low wood resistivity and an abundance of apomorphicfeatures have invaded these same habitats, yet the specieswith ancient xylem formulae are still there. Certainly simpleperforation plates can be developed readily from ancestorswith scalariform perforation plates, as shown by Schisandra-ceae and by the various families of Ranunculales, as well asother basal branches of the angiosperm tree, as given by Sol-tis et al. (2011) and others. Why are woods that do not have

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“truly efficient and safe vessels” (phrase from Sperry et al.2007) in existence at all?As a working hypothesis, we might propose that the first

vessel-bearing angiosperms did feature lower cavitation risks,then later radiations in angiosperms added more efficientconductive capabilities, but that there are trade-offs involved,not an unalloyed series of advantages or inexorable progressto an optimal combination of character states. The hypothesisproposed here is that wood features evolve independently ofeach other and match ecological adaptations.

Reasons for perforation plate retention in “primitive” woodsZimmermann (1983) offered the intriguing idea that in

temperate areas with frost, scalariform perforation plates“sieve out” air bubbles that result from thawing of winter icein vessels. This “conductive safety” feature might account forwood of many cold temperate forest trees such as Betulaceae,Hamamelidaceae, and Nothofagaceae. These trees have broadleaves that are probably not compatible with fluctuation insoil moisture and therefore transpiration rates, but wet tem-perate forest trees with scalariform perforation plates live insoil that is either wet or frozen, and the latter condition oc-curs when leaves are shed. Thus high conductive resistivityin these trees is also high in conductive safety, a workabletrade-off.

How much resistivity does a scalariform perforation plateconfer?There are various estimates of how much resistance the ex-

istence of a scalariform perforation plate confers (Schulte andCastle 1993a, 1993b; Ellerby and Ennos 1998; Sperry et al.2005). These measurements disagree from one another be-cause different methods were used. Nevertheless, one cansay that the resistance of the scalariform perforation plate issufficient so that if selection favors maximizing conductive

flow, the number of bars will be reduced over evolutionarytime, a fact confirmed by the comparative data (Bailey andTupper 1918; Frost 1930a). Analysis of global phylogenies(e.g., Fig. 14) also confirms this. On the other hand, the re-sistance of the scalariform perforation plate may be low (es-pecially as it approaches the simple perforation platecondition) so that it is tolerable if it serves some other func-tion such as increasing conductive safety. It appears to dothat (Slatyer 1967; Sperry 1986). Thus, a trade-off interpreta-tion is viable, and the slow disappearance of the perforationplate in evolutionary terms becomes understandable.Scalariform perforation plates can be found in latewood of

some species that have simple perforation plates in adjacentearlywood (e.g., Styrax). This shows both the value of perfo-ration plate simplification and how rapidly it can occur. How-ever it also shows that higher resistivity in latewood isprobably not disadvantageous; if so, a slower rate of conduc-tive flow may be responsible.The resistance of the side walls of the vessel is proportion-

ate to vessel diameter, as well as to end-wall resistance(Sperry et al. 2005). There is a tendency for bars of the perfo-ration plate to become fewer as the vessel widens (a tendencyeasily seen in lianoid vs. tree Dilleniaceae). Not surprisingly,species with long scalariform perforation plates also have rel-atively narrow vessels (Bierhorst and Zamora 1965). Is extinc-tion of the last few bars of a plate slowed as the resistance ofthe plate lowers? As with many vestigial features, this is prob-ably the case, so persistence of few-barred scalariform perfo-ration plates phylogenetically is to be expected. This isconfirmed in clades such as that of Fig. 14. Vessel diameter,in a particular stem, tends to become wider for trees that arereaching a water table (Carlquist 1984), but vessel diametermay become narrower if a shrub is faced with a finite watersupply in competition with other shrubs (e.g., Artemisia;Figs. 6E–6F). Allometry is not involved.

Fig. 8. Two complementary drawings that represent how bordered pits function. (A) The bordered pit is seen as a structure maximizing flowwhile minimizing loss of wall strength (from Carlquist 2001a). (B) A drawing designed to show how water from a tracheary element with anintact water column, left, refills a cavitated tracheary element, right, via a bordered pit. “As water enters the bordered pit channel (1), it formsa concave meniscus such that the curvature of the meniscus pulls the water into the bordered pit. As the meniscus enters the pit chamber (2),it bows out, forming a convex shape...” (from Zwieniecki and Holbrook 2000, with permission).

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Resistance is also conferred by having many shorter ves-sels instead of a few long ones: a compromise in favor ofsafety. This is true of, for example, Ilex (Jeje and Zimmer-mann 1979), a wood that is in an early-branching clade ofCampanulidae, Aquifoliales (Fig. 14).

Pit membrane remnants: “semi-tracheids” and “neo-tracheids”A number of species with scalariform perforation plates

have pit membrane remnants in the form of cellulosic webs

or strands (Butterfield and Meylan 1972; Meylan and Butter-field 1978; Carlquist 1978, 1992). Aextoxicon (Fig. 2E), Car-podetus (Fig. 2A), Illicium (Fig. 2C), Paracryphia (Fig. 4F)and Sphenostemon (Figs. 4A–4E) are good examples. Arethese just historical remnants of a tracheid-like condition? Se-lective pressure is too common and too widespread in angio-sperms for such remnants to be considered merely persistenceof an ancient feature. Intact pit membranes in scalariform per-forations of a wood are always accompanied by perforationplates in which the perforations are clear or partially occluded.

Fig. 9. SEM photos showing the nature of imperforate tracheary elements (A–D) and parenchyma in wood. (A) Ilex anomala (Aquifoliaceae).Pits densely placed and with wide borders, as is characteristic of tracheids. (B) Sphenostemon lobospora (Paracryphiaceae). Smaller, lessprominent borders of pits, typical of fiber-tracheids. (C–E) Sambucus mexicana (Adoxaceae). (C) Outside of libriform fibers showing smallsimple pits. (D) Libriform fibers sliced open showing starch grains. (E) Ray cell sliced open showing starch grains. (F) Cuttsia viburnea(Rousseaceae). Scalariform perforation plate, two cells of an axial parenchyma strand, and tracheid, from tangential section.

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Fig. 10. Transections of woods to show distinctive tissue adaptations. (A) Cayratia clematidea (Vitaceae). Vessels are mostly wide (wv) andsheathed with fibers (fs); narrower vessels (nv) are also present. The background axial tissue is thin-walled axial parenchyma (ap); vascularrays (vr) are wide and few, with thin-walled cells. (B) Orphium frutescens (Gentianaceae). Strands of interxylary phloem (ip) are scattered ina wood that otherwise consists of narrow vessels (v), libriform fibers, and rays.

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Scalariform perforation plates (Fig. 3B) with intact pits occuroccasionally (Fig. 3C). Such vessels could be called “semi-tracheids” perhaps, or “neo-tracheids” if one wants to implysecondary acquisition of pit membranes in perforations. Suchpit membranes would offer more resistivity to flow but wouldalso give much better sequestration of air bubbles. However,the woods in which such vessels occur also contain perfora-tion plates in which pit membranes are absent. The intriguingidea of Holbrook et al. (2002) that shrinkage of pores in pitmembranes with increasing ion concentration in sap and

thereby shrinkage of hydrogels in the pit membranes (a rever-sible change enhancing flow) may be applicable here(although it needs more work; Van Ieperen 2007). In anycase, we find pit membrane remnants in perforation plates inearly-departing branches of clades in plants of very wet habi-tats (Fig. 14; Carlquist 1992). Feild et al. (2002) suggestedthat the secondary vessellessness of Winteraceae may putthem at an advantage where freezing occurs: this is possible,but Winteraceae are not “ecologically abundant” as those au-thors suggest, and Winteraceae is a relict family under most

Fig. 11. Details of pitting in parenchyma of woods. (A–D) Bordered pits on ray cells. (A) Bordered pits (seen in sectional view) of uprightray cells from radial sections. (B–D) Buddleja bullata (Buddlejaceae). (B) SEM photograph of sectioned wall of upright ray cell showingbordered pits. (C) Bordered pits seen on outer surface of upright ray cell from tangential section. (D) Bordered pits seen on outer surface ofprocumbent ray cells from tangential section. (E–F) Trigoniastrum hypoleucum (Trigoniaceae). Axial parenchyma cells (with adjacent fiber-tracheids) from radial section. (E) Cross wall of strand with bordered pits (bp); bordered pits are also present on the axial walls. (F) Crosswall of strand with a larger simple pit (lsp); inconspicuously bordered pits are also present on the axial walls.

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Fig. 12. Examples of successive cambia and their ontogeny. (A) Stegnosperma alimifolium (Stegnospermataceae). The master cambium (largepointers) produces several layers of secondary cortex (sc) externally; outside of that are primary cortex cells (c). Internal products of themaster cambium include successive bands of conjunctive tissue (ct) and vascular cambia (vc), each of which produces rays (r), secondaryxylem (sx), and secondary phloem (sp). (B) Operculina palmeri (Convolvulaceae). Tissues are produced by a single vascular cambium exceptfor a pith cambium (pc), which produces secondary phloem internally (extreme left edge) and a few vessels internally. The main vascularcylinder begins with primary xylem vessels in radial rows, separated by rows of axial parenchyma (pxv + ap), proceeds with a band of nar-row (fibriform vessels plus tracheids (nvtt), and then continues with wide vessels (wv) in a background of tracheids plus patches of axialparenchyma (ap). Occasional wide rays (owr) originate abruptly.

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definitions of that term. Areas close to where freezing is mod-erate are more likely to stay moist longer, and that probablyexplains winteraceous ecological preferences.

New uses for bars on perforation platesA surprising number of woody angiosperms have few, but

notably wide, bars on perforation plates. One can cite Aralia-ceae (Rodriguez 1957), Empetraceae (Carlquist 1989a), andEpacridaceae (Lens et al. 2003), as well as such well-knowngenera as Magnolia (Fig. 13D), Rhizophora, Ribes, andStyrax (Carlquist 2001a, p. 64). Are such perforation platesmechanical enhancement that offers support to vessels under

Fig. 13. Examples of heterochrony in wood as seen in (A) tangential and (B–F) radial sections. (A–B) Cyanea aculeatiflora (Campanulaceae).Permanently juvenile ray morphology. (A) Tangential section. All rays are multiseriate and consist mostly of prominently upright cells.(B) Ray cells are prominently upright (vertically elongate). (C) Brassaia actinophylla (Araliaceae). In metaxylem, perforations plates are sca-lariform (left), secondary xylem perforation plates (right) mostly simple, with some scalariform plates formed in early secondary xylem (someother Araliaceae have intermixed simple and scalariform perforation plates). (D) Magnolia grandiflora (Magnoliaceae). Scalariform perfora-tion plates are formed uniformly in the secondary xylem (more numerous bars per plate occur in metaxylem). (E) Eucommia ulmoides (Eu-commiaceae). Scalariform perforation plate in metaxylem (primary xylem at left); all secondary xylem vessels have simple perforation plates.(F) Kadsura japonica (Schisandraceae). At left, a narrow metaxylem vessel with a scalariform perforation plate; secondary xylem vessels arewide, with simple perforation plates (e.g., center).

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Fig. 14. Molecular tree of the superorder Campanulidae, from Tank and Donoghue (2010). The curving line superimposed on their tree deli-mits species with simple perforation plates (to the right) from those with scalariform plates (placement of this line is inexact in some placesbecause of the large number of taxa). Note that species numbers in families (which have been added to the original tree) are, in general, muchlarger in families with simple perforation plates. “Branch lengths are proportional to the mean number of substitutions per site as measured bythe scale bar.” For other conventions, see Tank and Donoghue (2010). Modified and reproduced with permission of the authors.

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tension, thereby permitting the xylem in these species to havelowered vulnerability to deformation and embolism forma-tion? We need studies to find the answer.

Vessel element length as a factorThere is no question that vessel element length in spe-

cies with scalariform perforation plates is, on average,longer than tracheid length for any given species that hastracheids (Bailey and Tupper 1918; Frost 1930a; Carl-quist 1975). Fewer cross walls per unit of vessel offersless impedance, but the presence of bars on perforationsplates, especially if numerous, runs counter to any flowadvantage.

Vessel elements are better than tracheidsIf one performs experiments in which resistivity to flow is

measured by laboratory methods involving whole stems (asopposed to individual cells), one can find that vessel-bearingwoods with scalariform perforation plates have high resistiv-ity to flow (Sperry et al. 2007). However, what if one were toimagine comparing the conductivity of a vessel lumen 75 µmin diameter (a not uncommon vessel diameter in such woods)with a number of tracheids, the lumen diameter of whichwould total that of such a vessel? In terms of such individualcell comparisons, the vessel has a greater flow than theequivalent lumen area of tracheids. Unfortunately, experi-ments involving tubing cannot be applied to individual cells.The invention of vessels, when one compares vessels withtracheids in this way, was a good idea. The relative diameterand abundance of vessels in a wood (ca. one-quarter of thetransectional wood surface of a woody angiosperm; Carlquist1975, p. 206) can be varied, of course. More vessels meansmore volume of water flow, and more imperforate trachearyelements means more mechanical strength. There can be atrade-off. To be sure, a number of woods with vessels alsohave tracheids in them, and although a tracheid can be calcu-lated to have more resistance to flow (Sperry et al. 2007)than a vessel element, the addition of tracheids to vessels re-sults in a net gain in conductive capability. It also results ingreater safety, because tracheids in a woods such as Myricaor Eucalyptus are unlikely to embolize: their pit membranesresist that, whereas embolisms can spread readily from onevessel element to another.

5. The bordered pit: a structure with multiplemeanings

Wall strength vs. conductionThe bordered pit is a remarkable invention, common to all

groups of vascular plants, that balances conduction (a broadpit membrane) against wall strength (the pit aperture is a min-imal interruption in the wall, a fact involving the overarchingnature of the pit border). These features are summarized inFig. 8A. Bordered pits occur frequently on tangential walls ofray cells (Carlquist 2007b), so the strength–conductivity trade-offs of bordered pits are not limited to tracheary elements.

Pit membranes as passagewaysIn conifers, the bordered pit takes a circular shape, a fact

related to the torus–margo configuration. The closure (aspira-tion) of the pit can be accomplished by displacement of the

torus to one side or the other, but when conduction is active,the pit membrane stays in a midway position. The displace-ment of the margo to achieve closure is permitted not onlyby the margo threads, but also by the circular nature of thepit aperture, which is smaller than the torus, but whichmatches the pit aperture against which the torus becomes ap-pressed by aspiration. The margo threads offer relativelylarge passageways for water transfer (Pittermann et al. 2005).The conifers (including Gnetales) and ginkgophytes weregreatly advantaged by this invention (Pittermann et al. 2005),which was probably basic to the success and persistence ofthe group (a plesiomorphy in the ginkgophyte–conifer line-age). Woody angiosperms, by contrast, did not invent a truetorus–margo system: margo threads in the conifer sense areabsent (for a review, see Rabaey et al. 2006).Angiosperms very likely began with scalariform lateral

wall pitting of tracheids. Scalariform pitting is more abundantin earlier-branching angiosperm clades and in metaxylem(conifer tracheids do not have scalariform pitting). An unap-preciated correlation is a mechanical one: with a circulartorus–margo system, strain is equal on all sides of the margo,so that displacement of the torus is successful. If a scalari-form pit were to have a torus–margo system, strain would begreater in the center of the elliptical pit membrane, less at theends, so that closure of the elliptical pit aperture would notbe successful. Angiosperms, in essence, had to invent a seriesof mechanisms that gave scalariform pits hydraulic capabil-ities equivalent to (or superior to or more flexible than) thecircular pits of conifers. It was the angiosperms, not the coni-fers (as suggested by Pittermann et al. 2005), that were theunderdogs in this competition. Life cycle brevity was theoverriding advantage that the angiosperms held. The greatevolutionary flexibility of angiosperm woods (Carlquist2009b) also at some point permitted them to surpass conifers.

Pit membranes: flow and cavitationPores in pit membranes are small, much inferior to conifer

margo pores for flow, but with sufficient area; angiospermtracheary element pit membranes do have appreciable flowcapacity (Choat et al. 2003). Thinner pit membranes havelarger pores and thus are better at conducting, but offer morevulnerability (Jansen et al. 2009). Tracheids with thinner pitmembranes and visible pores include Amborella and Drimysand are figured by Hacke et al. (2007). This might representan early angiosperm condition.When pressure inequality between two adjacent tracheary

elements occurs, some deflection of pits membranes may re-sult, but probably not very much (Zwieniecki and Holbrook2000). Greater deflection of pit membranes can result in cre-ation of larger pores (Choat et al. 2004), but this risks irre-versible change and would not aid recovery. Interestingly, pitmembranes of monocot tracheids are often quite porose(when intact pit membranes are viewed; Carlquist 2012). Afascinating possibility with regard to pores in pit membraneswas offered by Holbrook et al. (2002): “With increasing con-centrations of ions, these [pit membrane] hydrogels are hy-pothesized to shrink, increasing the porosity of the pitmembrane and thus decreasing the resistance to water flow.These changes are both reversible and repeatable, suggestingthat plants could actively modulate their xylem resistance byaltering the ionic concentration of the fluid in the xylem.”

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Pit geometry and consequent meniscus formation (Fig. 8B)may be important to reversal of tracheary element cavitation(Holbrook and Zwieniecki 1999; Zwieniecki and Holbrook2000). However, in deterring or reversing cavitations, awhole-plant approach should be taken (Choat et al. 2008),and even fibers and the strength that they exert relative tovessels may be involved (Jacobsen et al. 2005).Zimmermann (1983) conceived the idea of pores in pit

membranes as “designed leaks,” a mechanism that permitsentry of air that cavitates vessels. This may be true, but pre-vention of cavitation and prevention of membrane deforma-tion may be the pervasive themes in angiosperms that needfurther investigation.

Types of bordered pits and their significanceViewed at a light microscope level, bordered pits are var-

ied in shape and in degree of border width in angiosperm tra-cheids and ray cells. Are scalariform lateral wall pitmembranes in angiosperm vessels a plesiomorphic condition,as Frost (1931) proposed? The presence of scalariform pittingon end walls of Amborella tracheids (Fig. 11D) and, for thatmatter, those of Nymphaeaceae and most monocots, could becited as possible evidence.Why is there scalariform lateral wall pitting in vessels of

Vitis, whereas alternate pitting characterizes vessels of someother Vitaceae? Scalariform pitting is common in vessels ofMagnoliaceae (Fig. 13D) and Piperaceae, as well as a num-ber of Araliaceae (Rodriguez 1957). An equivalent type ofpitting, pseudoscalariform pitting (Carlquist 1988, 2001a),has been derived phylogenetically from alternate pits by lat-eral widening — the tips of the pits do not coincide with ves-sel facets as they do in scalariform pits. Thus, there seems tobe some significance to laterally wider pits other than a merehistorical remnant of an ancient condition. Is there a trade-offbetween extensive intervessel contact and wall strength? Cer-tainly scalariform pitting is very common in angiospermmetaxylem (Bierhorst and Zamora 1965), but a functional ex-planation should be sought, even though metaxylem couldstill be expected, as Bailey (1944) suggested, to be a refugeof antique wood characteristics.Certainly, as Frost (1931) showed, alternate pitting is the

most common type in woody angiosperms. On a theoreticalbasis, circular to polygonal alternate pits theoretically offer amaximum strength configuration. There has been no experi-mental proof of this in plants, although engineering parallelsdo exist. Opposite pitting is so similar to alternate pitting thatmany students confuse the two types, and they are probablyclosely comparable in adaptive terms. There seems to be littleloss in conductive ability by subdivision of elongate pits intoalternate or opposite pitting. One interesting example is fur-nished by the pitting of the tracheids of Tasmannia (Carlquist1989b) and Zygogynum (Carlquist 1981a) of the Wintera-ceae. They often have scalariform pitting on end walls but al-ternate (albeit sparse) pitting on lateral walls. This suggests aselective value of enhanced conduction for scalariform pittingbut a value in mechanical strength for alternate (and sparse)circular pitting. Increase in wall thickening would providemore mechanical strength, but it would require more photo-synthate input and narrowing of the lumen, which wouldlower conductive capacity.

6. Polymorphism in conductive cells: a key toangiosperm success and radiation

Trade-offs againVirtually all angiosperms have the genetic information to

make bordered pits on lateral walls of vessels, tracheids,fiber-tracheids, and ray cells. More importantly, the locationof bordered pits in wood can be governed very precisely.Bordered pits are maximally conductive structures that lessenwall strength appreciably, whereas simple pits are minimallyconductive structures that offer minimal lessening of wallstrength. Thus, a trade-off is in effect. Mechanical strengthcan be enhanced by having narrower borders or no borderson pits of imperforate tracheary elements. It can also beachieved by having fewer pits, but a certain number of pitsis necessary for input of photosynthates during cell wall for-mation. Thus there is a gamut of possible cell types.

The tracheid as basicWe can assume that the basic conductive cell type of the

angiosperms was a tracheid with bordered pits: these pits arescalariform when a wider element is formed, circular when anarrower element is formed. Such tracheids can be seen inthe earliest extant angiosperms, Amborella and Nymphaeales.The first dimorphism in angiosperm xylem, phylogenetically,is the development of wide tracheids that have larger pores inpit membranes of end walls. If the pit membranes of the endwalls are thin, they are swept away by the conductive stream(perhaps with pit membrane remnants remaining), with a ves-sel element resulting. The other cells, in this dimorphism, aretracheids, but tracheids that tend to be narrower and longer(during early developmental stages, narrower cells have intru-sive capacity) and with circular pits in which pit membranesare retained. Tracheids of various specifications can be cre-ated, for example, thicker-walled tracheids. Lumen diametermust be sufficient for water conduction. That is, the conduc-tive capacity of the bordered pits, collectively, must bematched by the conductive capacity of the cell lumen. Bygreater length, fusiform cell shape, and thicker walls, trache-ids form mechanically strong tissue that forms the ground tis-sue of woods in early angiosperms. Illicium represents such adimorphism.

Tracheids, fiber-tracheids, and libriform fibersTracheids represent greater pit membrane area (as repre-

sented by the wide pit borders, membranes sectioned away asseen in Fig. 9A). Tracheids are viewed and defined as con-ductive cells (Carlquist 1988; Sano et al. 2011). Pits on tra-cheids are relatively densely placed (Fig. 9A). Fiber-tracheidsrepresent nonconductive imperforate tracheary elements inwhich pit borders are still present (Fig. 9B). Selective pressureto complete extinction of the pit border, like extinction ofother vestigial structures in plants and animals, is probablyminimal. Libriform fibers, the most common type of imperfo-rate tracheary element in woody angiosperms, have simplepits (Fig. 9C). Wall strength is minimally compromised, be-cause in libriform fibers, the pit is a slit without a border. Inmost imperforate tracheary elements, wall strength loss isminimized by the fact that pit apertures are elliptical to fusi-form (Figs. 9A–9C) and run parallel to the helical arrange-ment of cellulose microfibrils in cell walls.

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Polymorphism within a single year’s woodGrowth rings are a good example of trade-offs: conductively

efficient cells in earlywood (fewer, wider vessels), conduc-tively safer cells in latewood (narrower vessels). We must notforget the background cell type in this trade-off. In a vessel-bearing wood with tracheids (which presumably embolizerarely), there may be no vessels at all in latewood: the ultimatesafety (Myrica). Narrower vessels in latewood may retainwater columns when earlywood vessels in the same growthring embolize (Hargrave et al. 1994). The terms “ring-porous”and “diffuse-porous” do not delineate two distinct categoriesbut rather extremes in growth ring formations. There aremany types (Carlquist 1980, 1988, 2001a) that are not in-cluded in descriptions but that may key closely to the ecologyof a woody plant. Latewood vessel elements may be so narrowthat they have no perforation plates (yet have the same lengthas vessel elements) and are thus “vascular tracheids” (e.g., Ar-temisia; Figs. 6C–6D). These may resist embolism formationthroughout the most stressful months of the year, thereby pro-tecting the cambium.

Positioning polymorphismsPositioning of vessels within wood in ways other than

growth rings is often seen. In fact, a monograph on nonran-dom vessel positioning has been offered (Carlquist 2009a).For example, sheathing of vessels in libriform fibers is acommon strategy of lianas (Obaton 1960) and is shown here(Cayratia; Fig. 10A).

Vasicentric tracheids: tracheid dimorphism and fiber-tracheid dimorphismVasicentric tracheids are tracheids that co-occur with fiber-

tracheids or libriform fibers in particular woods. When thisco-occurrence takes place, the tracheids are always adjacentto vessels, whereas the mechanical elements (fiber-tracheidsor libriform fibers) are more distal. Vasicentric tracheids mayform massive sheaths of vessels, as in Eucalyptus or Quer-cus, or be only a few cells, as in Ceanothus (Figs. 6A, 6B)or Hedera. Wood macerations are necessary to identify vasi-centric tracheids in these latter cases. In Rosaceae, some spe-cies of Prunus have only tracheids, whereas in others,libriform fibers are present, the latter presumably a dimor-phism of tracheids (Carlquist 1988). Tracheids as a back-ground cell type are a plesiomorphy in Rosaceae. Vasicentrictracheids are common in Californian chaparral shrubs (Carl-quist 1985a). There is presumably a gain in mechanicalstrength in this dimorphism.Zygophyllaceae (Larrea) have fiber-tracheids as a back-

ground cell type but also have vasicentric tracheids (Carlquist1985a). The family Krameriaceae, a sister family of Zygo-phyllaceae (and sometimes merged with it), has only trache-ids (Carlquist 2005). One can think of these wood types asphylogenetic products of fiber-tracheid dimorphism.Vasicentric tracheids are occasional in Lamiaceae (Rosmar-

inus) and Solanaceae (Lycium), and because libriform fibersappear plesiomorphic in these families, vasicentric tracheidsmay have arisen phylogenetically by extending the formationof bordered pits (present, of course, in vessels) onto a scatter-ing of imperforate cells.

Fibrous cell walls as investments: wood densityThe walls of libriform fibers, fiber-tracheids, and tracheids

are sometimes thick and represent a considerable investmentof cellulose and other substances. This is mute testimony tothe strength function of imperforate tracheary elements. Fiberwalls are the chief mechanisms for dealing with the weight ofa plant and the stress produced by wind thrust and torque.Imperforate tracheary elements may also resist negative ten-sions that would lead to implosion (Carlquist 1975; Jacobsenet al. 2005). Vessel walls themselves have appreciable thick-ness that may represent, in part, a resistance to water columntensions. The roles that wood density (largely a product ofwall thickness) play are currently being examined by variousworkers.

Libriform fiber dimorphismThe work of Kribs (1937) assumes (if only by lack of com-

ment) that there has been only one phylogenetic origin of ax-ial parenchyma and that different rearrangements haveoccurred. However, a second type of origin has occurred: fi-ber dimorphism. This was observed early in helianthoid As-teraceae such as Dubautia (Carlquist 1958, 1961; Carlquistet al. 2003) and has been subsequently found in many Urtica-ceae (Bonsen and ter Welle 1984). Acer also has both living(nucleated) fibers and nonliving (libriform) fibers.

Fibers as storage devicesAlthough the main storage tissue within wood is rays

(Sauter 1966a, 1966b), libriform fibers can store considerablequantities of starch in some species (Fig. 9D). Extensivestarch storage in fibers seems related to more sudden flushesof growth and flowering (as in Araliaceae), but detailed corre-lations and physiological studies have not yet been presented.

Vessel dimorphismLianas often have both wide vessels and narrow ones

(Carlquist 1985b), illustrated here in Cayratia (Fig. 10A).When size classes are plotted out, smaller vessels are morenumerous, wider vessels fewer, so vessel dimorphism, as ingrowth rings, does not produce a “traditional” bimodal curve(this would be true in growth rings as well). A bimodal dis-tribution of size classes is not a necessary requisite for de-claring vessel dimorphism to be present: the point is that awider range of vessel widths is available to the conductivesystem, with the wider presumptively providing conductiveefficiency and the narrower providing conductive safety.Ewers et al. (1991) showed that vessel diameters form curvesintermediate between typical normal and typical bimodal,with narrower vessels somewhat more frequent than onewould expect.

Division of labor: a pervasive themeAll of the dimorphisms or polymorphisms cited above can

be said to exemplify division of labor. The term “trade-off” isalso applicable in many of these cases. The products show dif-ferentiation not merely in histology, but in function. Althoughthe co-occurrence of vessels and an imperforate tracheary ele-ment type (tracheids, fiber-tracheids, or libriform fibers), re-sulting in a vessel-bearing wood derived from an all-tracheidwood is the dramatic division of labor often cited; other typesof division of labor are often evident. Axial parenchyma cells

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that bear crystals are often different, in a particular wood, fromthose that do not contain crystals, and co-occur with them, in-dicating a division of labor. The amazingly polymorphic capa-bilities of wood cells of angiosperms are undoubtedly one keyto the evolutionary success of angiosperms.

7. Axial parenchyma: what does it do?

Finding patternsAxial parenchyma is elusive to students — it is visible

clearly only in radial sections of wood where the direction ofthe strands of cells contrasts with that of ray cells and itsfunctions have not been the subject of extensive research.Thus, the evolutionary significance of these cells and howthey might figure phylogenetically has been neglected. Kribs(1937) presented a number of topographic types of axial pa-renchyma, as seen in wood transections, but he did not corre-late these types with any other wood anatomical phenomenaor offer any functional interpretations. He did attempt to lineup the types in putatively phylogenetic sequences, beginningwith diffuse (or absent) and proceeding with types in whichaxial parenchyma cells (as seen in transections) aggregateinto tangential rows (diffuse-in-aggregates) or tangentialbands two or more cells thick (apotracheal banded). Like-wise, progressive grouping around vessels (paratracheal) isanother trend. However, multiple types may be found insuch genera as Metrosideros (Meylan and Butterfield 1978)or Corynocarpus (Carlquist and Miller 2001).

Finding functionsAxial parenchyma strands or bands intersect with rays and

touch rays and vessels, and these contacts create interlink-ages between the vertical and radial parenchyma systems.The interlinkages of the two systems seem phylogeneticallyto change from smaller and more numerous to fewer andmore massive, but exceptions could be cited. Diffuse axialparenchyma has a high correlation with tracheid occurrence,and this and the abundance of paratracheal types (the mostcommon in woody angiosperms) suggest that there is a rela-tionship to conduction. This makes sense, because some kindof mediation between the cohesion–tension sequence initiatedby leaf transpiration and the water intake system of roots isa presumptive physiological necessity. Sauter et al. (1973)found sugar release into vessels at the beginning of thegrowth season in the sugar maple (Acer), a way of osmoti-cally “jump-starting” the conduction in vessels. Axial paren-chyma cells and living fibers are vertically oriented livingsystems that contain sugar or starch and that could accom-plish this activity, together with carbohydrate storage in rays(Sauter 1966a, 1966b). We do not know how widely appli-cable this phenomenon is and whether or not it occurs tosome degree in all angiosperms. We do know that the pres-ence of starch in axial parenchyma is almost universallyseen, provided that woods are liquid-preserved (drying ofwoods as in the preparation of xylarium samples, results inloss of starch, so that the vital functioning of the axial pa-renchyma system goes unnoticed all too often). The occur-rence of living fibers in angiosperm woods is thusunderreported.

Reversing embolismsHolbrook and Zwieniecki (1999) made a compelling case

for removal of embolisms by transfer of solutes into vesselsfrom axial parenchyma. They elaborate these ideas in termsof ion concentration in a later paper (Holbrook et al. 2002).Such activity would result in a kind of “stem pressure” thatwould work similarly to root pressure. This hypothesis needsfurther work. A hint at axial parenchyma as an agent con-trolling conduction is signaled by the existence of diffuseparenchyma. If axial parenchyma were primarily a storagetissue, dispersion of the cells (diffuse parenchyma) amongnonconductive (libriform) fibers would make no sense. How-ever, diffuse parenchyma cells (or similar types) are relatedto the occurrence of conductive tracheids in woods (Figs. 1E,2F). At least a few diffuse parenchyma cells may be seen ad-jacent to vessels even in the other types. Thus all conductingcells have close contact with living parenchyma cells whenviewed three-dimensionally. One is reminded of the occur-rence, seen occasionally, of starch grains in companion cellsin phloem, adjacent to sieve tube elements, which are, ofcourse, enucleate.

What about “absent” or “scarce” axial parenchyma?Absence or scarcity of axial parenchyma is reported in a

number of woods (it is sparse in conifer woods). In many ofthe angiosperm woods in which axial parenchyma is absentor very sparse, e.g., Burseraceae, one finds that the imperfo-rate tracheary elements are living fibers (for systematic occur-rence of living fibers, see Carlquist 1988, 2001a). Woodstudies based on xylarium specimens cannot reveal this be-cause drying of woods is often accompanied by decomposi-tion of starch.In vesselless angiosperms, there is another story. Axial pa-

renchyma is scarce in some Winteraceae, somewhat morecommon in some; it is also scarce in Amborellaceae(Fig. 1A) and Trochodendraceae. One reason for the scarcitymay be that in these families, upright ray cells are commonand rays are close to each other (Fig. 1B), so upright raycells may serve as a kind of substitute for axial parenchyma.Axial parenchyma, where present in Tetracentron and Tro-chodendron, is in latewood, which is compatible with theidea of axial parenchyma as a stress-countering conductivesupport cell type. Presumably, under this assumption, early-wood is not embolism-prone and functions under conditionsthat are free from drought and frost (which would accordwith the ecology of these genera).

A bigger story?In conifers, the margo–torus structure of pits may be so ef-

fective at minimizing cavitation that axial parenchyma be-comes nearly irrelevant as a mechanism for “osmoticallyguarding” tracheids. An interesting corollary of this possibil-ity would be that development of relatively abundant axialparenchyma (or living fibers) in vessel-bearing angiospermswas a requisite of their coping with the cavitation risks thatvessels present when compared with an all-tracheid system.Vessels that are prominently sheathed by axial parenchyma(e.g., many Fabaceae) may similarly serve as photosynthatestorage related to flushes of growth and flowering, as wellas transfer of ions or sugars into vessels.

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Other functionsAlthough axial parenchyma cells rarely have bordered pits

(which would indicate active flow), pits on end walls of astrand are denser than on the lateral walls, according withaxial flow within the strand. Bordered pits may be seen in afew cases (Fig. 11E). Pits on transverse walls of an axial pa-renchyma strand tend to be denser than those on the sidewalls (Fig. 11F). Axial parenchyma is an ideal site for depo-sition of herbivore-deterrent substances such as silica, crys-tals, and terpenoids. Axial parenchyma, when strategicallyplaced, offers tissue that can yield to torsion, a feature espe-cially important in lianas such as Cayratia (Fig. 10A) andOperculina (Fig. 12B). Axial parenchyma is especiallyprominent in the secondary xylem of some succulents suchas Crassula.

8. Rays: diversity in histology, diversefunctionsAs seen in radial sections of wood, rays are composed of

upright cells and procumbent cells (Kribs 1935; Barghoorn1940, 1941a). Procumbent cells are common in the centersof rays (“isolation cells” of Braun 1970), whereas uprightcells (“contact cells”) are common in ray tips and sheathingcells of the central portions of multiseriate rays. The propor-tion of each type varies with species and with ray ontogeny.What is the function of the two ray cell types, and why dotheir proportions vary?

Functions that interrelateThe simplest answer is that procumbent cells conduct pho-

tosynthates radially (Sauter 1966a, 1966b) and store photo-synthates (Fig. 9E). Procumbent cells are horizontallyelongated. Most cells that conduct water or photosynthatesare elongated in the direction of conduction: fewer impedan-ces (end walls) per unit length of a strand of conducting tis-sue (Sperry et al. 2005; Tyree and Ewers 1991). Notsurprisingly, the older the stem is, the more abundant are theprocumbent cells, presumably because there is a progres-sively greater volume of photosynthates to be conducted hor-izontally. Note also that rays may be living and functioningfor many years, so that the volume of living cells that storesphotosynthates gradually increases. Rays also widen duringenlargement of a stem, becoming more numerous cells widein the central portions (Barghoorn 1941a). The idea thatwood is a storage tissue may seem novel, but the ray and ax-ial parenchyma cells in wood offer most of the storage tissuein a woody plant, and starch can be observed in them, oftenabundantly. Upright cells in rays conduct vertically and pro-vide good linkage to axial parenchyma strands, thereby form-ing a network of living cells in wood that can conductphotosynthates both vertically and horizontally.

Mechanical and conductive aspects combineAlthough almost always overlooked in wood descriptions,

bordered pits occur on ray cells (Figs. 11A–11D). These areespecially common on tangential (periclinal) walls of pro-cumbent ray cells (Carlquist 1988, 2007b; see also microcastimage in Fujii 1993, fig. 59). Bordered pits on these wallsare best observed in sectional view with light microscopy(Fig. 11A) or SEM (Fig. 11B) or on tangential walls of ray

cells exposed by sectioning (Figs. 11C, 11D). They occur(along with some simple pits) in about half of the woody an-giosperms that I have examined, so this is not a rare phenom-enon. The overarching of the pit membrane by wall material,so that the size of the pit aperture minimally weakens thewall strength while maintaining a broad pit membrane forconduction, is basic to the strategy of the bordered pit. Thisapplies to the bordered pits of ray cells, as well as to the bor-dered pits of tracheary elements. Ray cells usually have sec-ondary walls in woody angiosperms, and these walls aremoderately thick (very thin walls are much less likely tohave pit borders). The fact that woody plants expend photo-synthates in forming lignified walls for ray cells shows thatan appreciable mechanical role (a fact not mentioned in text-books) is played by ray cell walls: they contribute to thestrength of a woody stem. Ray cells may be thin-walled instems of lianas (where they offer flexible partitions betweenthe strands of fibrous tissue) or succulents (where they offerwater storage tissue).

Changing ontogenies, changing histologyOne of the major events in the development of the

cambium of a woody plant is the horizontal subdivision ofray initials, so that vertically shorter (but horizontally longer)ray cells are produced. This may relate to the conductive na-ture of rays, as noted above. However, such subdivisions arefewer in stems of secondarily woody plants such as rosettetrees (woody lobelioids, for example). In secondarily woodyplants, ray cells are predominantly upright. The fact that up-right ray cells predominate in the rays of stems for the dura-tion of secondary growth can be cited as evidence ofjuvenilism, a departure from an herbaceous ancestry ratherthan a strongly woody one. This condition characterizes lobe-lioids (Carlquist 1969) but also can be found in a diversity ofother families such as Empetraceae (Carlquist 1989a) andEpacridaceae (Lens et al. 2003). Is the predominance of up-right ray cells an indication of a balance tilted toward verticalflow and away from horizontal flow in such species? Thatwould be a logical conclusion, related to the more limitedwood accumulation of secondarily woody species.

RaylessnessOnly a few woody angiosperms form wood that lacks rays

(notable for this, Hebe; Meylan and Butterfield 1978). This isbest explained as an overriding selection for mechanicalstrength. In fact, rays do eventually appear (Barghoorn1941b) in stems of some species that are initially rayless (Ar-temisia, Cyrtandra, Plantago). In rayless woods, fusiformcambial initials are very short, so that the length differencebetween a potential fiber and a potential ray cell when de-rived from the cambium is minimal. Raylessness does not oc-cur in plants with long fusiform cambial initials.

Other functionsDeposition of tannins, terpenoids, crystals, and silica in ray

cells probably deters chewing beetles and even mammalianherbivores. Ray cells, along with axial parenchyma cells, canserve in the regeneration of a cambium following damage toa stem by drought, frost, or fire. Ray-to-vessel pits are usu-ally larger than vessel-to-vessel pits. This may indicate, aswith axial parenchyma, an osmotic activity by the living

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cells, transferring ions or photosynthates into the hydrosys-tem and thereby preventing cavitations or refilling them (Hol-brook and Zwieniecki 1999).

9. Collaborative cell type evolution: adistinctive feature of angiosperm woods

Division of labor: one kind of fusiform cambial initialproduces many different productsThe invention of the vessel element marked not just a ma-

jor division of labor creation for angiosperms, but the begin-ning of further modifications for both of the resulting celltypes. With vessel origin, there is a change in diameter andcell length. Vessel elements within any given wood are widerand shorter than the imperforate tracheary elements that theyaccompany. Vessel elements do not elongate appreciablycompared with the fusiform cambial initial from which theywere derived, but imperforate tracheary elements, which areable to undergo intrusive growth due to their slenderness,do. There also tends to be a dimorphism between vessel ele-ments and accompanying imperforate tracheary elements inwall thickness. With the invention of vessel elements, thereis also a change to greater abundance of axial parenchyma,which serves in regulating “stem pressure” and thereby main-taining water columns. Holbrook et al. (2002) showed thatliving cells (axial parenchyma) mediate flow in the vessel el-ements and imperforate tracheary elements, which are deadcells. The patterns of rays are indirectly affected by thechanges in axial parenchyma distribution. Vessel elementsfrequently become distributed in nonrandom ways (Carlquist2009a). Thus, the origin of vessels, seemingly a singlechange, involves changes, directly or indirectly, in all woodcell types.

Vessels distributed with relation to different trachearyelement typesWoods with tracheids as the background fibrous cell type

(Sorbus and most other Rosaceae), or with abundant vasicen-tric tracheids surrounding vessels (Quercus), have solitaryvessels. As the imperforate tracheary element type shifts tofiber-tracheids or libriform fibers, grouping in vessels occurs(Carlquist 1984). Tracheids are conductive imperforate tra-cheary elements (Carlquist 1985a; Sano et al. 2011) thathelp to maintain the conductive pathways of vessels shouldvessels embolize and are evidently superior as a device formaintaining conductive pathways compared with grouping ofvessels. With the diminution or loss of borders on the imper-forate tracheary elements, grouping of vessels becomes an ef-fective way of maintaining the pathways: redundancy isachieved, but also variation in diameter of vessels occurs,with smaller vessels embolizing less readily (Hargrave et al.1994). These groupings are often radial sequences, remindingone of a “relay” in which newer vessels can take over asolder ones embolize and no longer are conductively active.Extensive vessel groupings occur, often in diagonal pat-

terns (Carlquist 1987) but sometimes in tangential patches.The diagonal groupings, seen three-dimensionally, intersectwith each other, thereby potentially interconnecting all of thevessels in the stem into a network. The diagonal bands arenot simply vessels, but are complexes that include vasicentrictracheids and axial parenchyma cells as well (Carlquist

1987). When diagonal bands occur, the intervening platesand strands of libriform fibers are consolidated into largergroupings, with attendant mechanical consequences.

Metaxylem — secondary xylem progressionsMetaxylem differs from secondary xylem in significant

ways. Metaxylem vessels are often narrower and associatedwith parenchyma (often in radial bands between vesselbands) instead of with mechanical cells. The onset of secon-dary growth usually features wider vessels, as well as me-chanical cells (“fibers”).In Convolvulaceae, the lianoid habit leads to shifts in his-

tology as the stem grows (Carlquist and Hanson 1991). Thesechanges are dramatically shown in Operculina (Fig. 12B).This may represent, first, some vessels to supply elongatenew shoots, then, mechanically stronger tissue to support ayoung elongate stem, and finally, large vessels with greatconductive efficiency plus parenchyma patches to enhanceflexibility.

Cell types shift within growth ringsGrowth rings are commonly thought to involve merely a

shift from wider vessels in earlywood to narrower ones in la-tewood. However, growth rings can involve shifts in vesselabundance and vessel grouping (Ulmus). Placement of paren-chyma may be involved: some growth rings end or beginwith parenchyma bands (marginal parenchyma). In someplants that have tracheids as a background cell type, produc-tion of vessels may be discontinued in latewood (Bruniaceae,Myricaceae; this feature is also common in Ephedra). Late-wood vessels (not to be confused with vessel elements) aretypically shorter than earlywood vessels (Zimmermann andJeje 1981). For a more complete survey of growth ring phe-nomena, see chapter 2 in Carlquist (1988, 2001a).

Interactions and parenchyma typesAxial parenchyma and ray parenchyma are not independ-

ent of each other. The lack of axial parenchyma in Ambor-ella (Figs. 1A, 1E) must be viewed conjunctively with theabundance of rays and the abundance of upright cells inthose rays (Fig. 1B). “Diffuse” parenchyma, when viewedthree-dimensionally, forms a network, albeit one withsmaller and more numerous contact points that in woodswith massive axial parenchyma sheaths around vessels andprominent rays, as in Fabaceae (Carlquist 1988, 2001a).Diffuse-in-aggregates axial parenchyma forms tangentialbridges between rays (as does paratracheal banded axial pa-renchyma).

Living fibers versus parenchymaScarcity or absence of axial parenchyma is quite frequently

accompanied by conversion of the background tissue of awood into living fibers (some of which are septate, whereasothers are nucleate, a condition not observable in dried woodsamples).

Broader significanceThe simultaneous evolutionary changes in several cell

types of a wood have an interesting implication: can true re-version occur? Reversion, of course, is defined at present interms of character states, not genomic changes. However

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defined, it seems as though changes in several cell types con-junctively are not so much likely to be reversed as to prog-ress toward new combinations and norms. This explains thefact that not all clades have the same sequence of wood ana-tomical changes (see section 14) rather than inexorable gra-dations from plesiomorphic to apomorphic. A wood withlong scalariform perforation plates, long vessel elements,solitary vessels, tracheids, and diffuse axial parenchyma (i.e.,features found in Paracryphia, Escallonia, and Ilex amongthe campanulids; Fig. 14) may change, phylogenetically, to awood such as that of Asteraceae, with vessel elements withsimple perforation plates, grouped vessels, libriform fibers,and paratracheal axial parenchyma. But can such a sequencerun backwards? These cell type expressions are functionallyrelated to each other, and shifting the entirety of their adapta-tions backwards is unlikely. These characters are not geneti-cally linked to each other, and synchronicity can dissolve. Ifthere were an inexorable progression of all characters to-gether instead of some degree of independence, the Bailey–Frost–Kribs trends would not have been evident, becausethey saw that different clades tended in similar directions butindependently and with varied rates of evolution. The totalityof cell type expressions of wood of Asteraceae cannot changeback to the cell complexes of Ilex or Paracryphia. A fewquantitative changes in vessel diameter, vessel length, vesselelement length, and growth ring formation in a clade of As-teraceae could shift it from a conductively efficient wood to aconductively safe wood. These quantitative changes are rap-idly achieved, whereas the Bailey–Frost–Kribs trends areslow-evolving features. We can consider heterochrony andvessel changes related to ecology as overlays on the Bailey–Frost–Kribs patterns, rather than as part of them.

10. Successive cambia and other cambialvariants: correcting misinterpretations,finding significance

Why successive cambia matterAlthough in terms of species, successive cambia are not

common in angiosperms at large, they are characteristic of anumber of plants, ranging from beets (Beta) to Bougainvilleaand including many shrubs of salty and desert areas (cheno-pods) and many succulents (Aizoaceae). Successive cambiaform a radical departure from the single-cambium system,and because of that, they demand functional explanation. Ifwe cannot explain successive cambia, our explanations forfunctioning of single-cambium stems are in doubt. In fact,stems with successive cambia illuminate, by contrast, thefunctioning of single-cambium stems.

First, let’s understand the phenomenonDifficult to section (obscuring their developmental nature),

unsatisfactorily preserved when dried (as in wood collec-tions — xylaria), and not studied because no commercialtimbers have successive cambium, this phenomenon hasbeen remarkably misunderstood.After a series of studies on plants with successive cambia,

I produced a summary (Carlquist 2007a) and also an interpre-tive study of Caryophyllales (Carlquist 2010) in which themajority of families and genera with successive cambia are lo-cated. From these studies, I was able to draw the conclusions

below. The first vascular cambium in a stem with successivecambia is just an ordinary vascular cambium, producing sec-ondary xylem inwardly and secondary phloem outwardly.

The master cambiumAt a certain point, a new cambium-like layer appears in the

cortex. This layer is indicated by the pointers in the transec-tion of a Stegnosperma stem in Fig. 11A. The mastercambium encircles the stem (or root) and is, like a vascularcambium, functionally a single cell layer thick. It is not avascular cambium. Like a vascular cambium, it functions in-definitely. To the outside, the master cambium produces alayer or two of secondary cortex cells. To the inside, it pro-duces conjunctive tissue (usually a kind of parenchyma) andthen another vascular cambium. The initiation of each vascu-lar cambium is signaled by anticlinal (radial) divisions, sothat the cambia initials are narrower tangentially than theconjunctive tissue cells (or the master cambium cells). Thenit repeats this action indefinitely. Each of the vascular cambiaproduces secondary phloem to the outside and secondary xy-lem to the inside, so a series of vascular cambia and theirproducts, separated from each other by conjunctive tissue, re-sult. These are the “rings” of a beet.

Different, permanent, and nonseasonalThe master cambium is different from vascular cambia.

The vascular cambia in a plant such as Beta are perfectly nor-mal vascular cambia. The cylinder around the stem or rootthat acts as the master cambium is permanent and usuallycontinues for the life of the stem or root. Thus, there is onlya single master cambium at the periphery of a beet. The vas-cular cambia are produced without regard to season. In abeet, one can see that numerous vascular cambia are pro-duced per season.In a beet, which grows actively for a single season, the

master cambia and the vascular cambia are active. In manyspecies with vascular cambia, the master cambium goes intodormancy until the time for initiation of a new vascularcambium comes, in which case active periclinal (tangential)divisions can be seen. How much secondary xylem doeseach of the vascular cambia produce? The amount is prob-ably limited by spatial considerations: the more numerousthe vascular cambia, the less secondary xylem each produces.However, the amount of secondary phloem is not so limited,because secondary phloem produced by each vascularcambium collapses with age, so that more secondary phloemcan be accommodated. Vascular rays (sometimes termed “ra-dial sheets of conjunctive tissue”), as well as axial xylem,may be produced by the vascular cambia. Axial parenchyma,which is not to be confused with conjunctive tissue, canoften be found adjacent to the vessels.

Conductive longevityIf new secondary phloem is continually produced by each

of the vascular cambia in a stem, surely that new phloem isactive in photosynthate conduction. The vessels in specieswith successive cambia are probably functional in vascularincrements that continue to produce secondary phloem.

ComparisonsThose who try to think of the master cambium as a kind of

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vascular cambium will be making a mistake. The parallel iswith a monocot cambium, found in genera such as Dracaenaand Yucca. The monocot cambium is like the mastercambium in that it produces secondary cortex outwardly. In-wardly, the monocot cambium produces cells that mature intoparenchyma, as well as strands of procambium, each ofwhich matures into a bundle containing xylem and phloem.No vascular cambial activity is present in monocots (Carl-quist 2012). The monocot cambium and its products havebeen generally interpreted correctly, perhaps because there isno cambial activity in the secondary bundles. The monocotcambium (“secondary thickening meristem”) is the only lat-eral meristem in monocots with secondary bundles.

Functional value of successive cambiaThe occurrence of successive cambia in a number of fami-

lies (Carlquist 2001a, 2007a) is testimony to the validity ofthis type of structure. If one looks at the nature of the plantswith this structural scheme, one finds the following.

a. Wide vessels maximize conduction. Examples are too nu-merous to cite here but include such well-known exam-ples as Bougainvillea as compared with nonlianoidNyctaginaceae. In conifers, one notes that the two treespecies of Gnetum have virtually no successive cambialactivity, whereas the approximately 30 lianoid species ofGnetum have wider vessels than the tree species. All ofthe lianoid species have prominent successive cambial ac-tivity. The flexibility provided by the increased abun-dance of parenchyma (mostly that of conjunctive tissue)and the spatial separation of vascular increments into con-centric cylinders separated by parenchyma are ideal forthe “cable construction” modes of lianas (Pfeiffer 1926;Obaton 1960; Carlquist 1985b).

b. Storage. Storage of sugar by Beta is obvious from its do-mestication. Water storage (often concurrent with photo-synthate storage) is evident in roots of Agdestis andBasellaceae and, to some extent, stems and roots of Ai-zoaceae (tuberous roots of Trichodiadema).

c. Salt sequestration. Amaranthaceae (amaranths, chenopods)are especially common in highly saline areas, and highsalt concentrations can be found in roots, stems, and leafparenchyma of this family (Atriplex, Salicornia, and Tetra-gonia), permitting them to thrive in osmotically challen-ging situations (Khan et al. 2000). Salt sequestration isclaimed for Avicennia (Robert et al. 2011). Other probableinstances may occur in Aizoaceae (Carpobrotus) and Nyc-taginaceae (Abronia).

d. Three-dimensionalization and longevity of vascular tissues.Successive cambia provide inner, as well as outer, portionsof the stem with active phloem cells. Thereby, a muchgreater volume of a stem (or root) can be used for storageand retrieval over a longer period of time, and the distribu-tion of conductive within storage tissue is ideal.

Other cambial variantsInterxylary phloem produced by a single cambium (certain

Combretaceae, Gentianaceae, Loganiaceae, Onagraceae, etc.)have strands of phloem (usually sheathed by parenchyma)within the secondary xylem. This can easily be distinguishedfrom successive cambia because the pairing of phloemstrands or bands with vessels (“vascular increments”) found

in successive cambia is absent with interxylary phloem(Fig. 10B), in which vessels do not contact the phloemstrands. Thus, even the most cursory examination of sectionscan permit differentiation between interxylary phloem (froma single cambium) and successive cambia: ontogenetic stud-ies are not needed to establish the condition.

11. Heterochrony I: a road map to juvenilism,paedomorphosis, and secondary woodiness

Pre- and post-molecular conceptsFor most of the twentieth century, the concept that woody

forms (especially the “woody Ranales”) were ancestral in an-giosperms was prevalent. The revelations of molecular phy-logeny (Chase et al. 1993) revealed a more complexsituation, but premolecular thinking tended to hold thatwoodiness was ancestral within angiosperms, herbaceousnesssecondary, and that this was accompanied by a radiation fromtropical into temperate zones. Studies of evolution of woodcharacters (Bailey and Tupper 1918; Frost 1930a, 1930b,1931; Kribs 1935, 1937) did not even include less woodyspecies, and the implied assumption was that minimally orless woody angiosperms had wood essentially like that ofmore woody species, just less of it. The idea that there couldbe secondary woodiness (particularly visible in island floras)and that anatomical features could pinpoint such instanceshad to wait until my 1962 paper (Carlquist 1962). Althoughthe ideas in that paper were soon accepted, the obvious cor-ollary idea was left unexplored for many years: how preva-lent was secondary woodiness in angiosperms, what kinds ofjuvenilism in wood were there, and can one see shifts to-wards (or away from) woodiness? I attempted answers in arecent paper (Carlquist 2009b) by using the premise that thehypotheses should be consonant with more recent global mo-lecular trees of angiosperms (e.g., Soltis et al. 2000; Angio-sperm Phylogeny Group (APG) 2009).

Types of juvenilismThe term “paedomorphosis” was imported from zoology to

denote plants that flowered (i.e., reached sexual maturity)while still in an early developmental stage. Where xylem isconcerned, this logically could include monocots, whichhave no secondary growth (but have protoxylem and metaxy-lem), as permanently juvenile. And I believe that monocotsshould be so considered (Carlquist 2012). Monocots thathave little or no metaxylem, and only protoxylem, could beconsidered the logical extreme in this series (e.g., Elodea). Itook the position that within nonmonocot angiosperms, therecould be degrees of juvenilism from very little secondarygrowth (Saururaceae) to rapid accumulation of large quanti-ties of wood (most well-known trees) and that there could beshifts in both directions within particular clades (Carlquist2009b). This section deals with woodiness that shows juve-nile features protracted to various extents into secondary xy-lem. Section 12 deals with angiosperms in which ontogeneticchange to “adult” (“typically woody”) wood features is rapidand in which development of flowers (sexual maturity) is de-layed (not infrequently for years, as in numerous trees).

Criteria for paedomorphosis or protracted juvenilismOne can readily understand the strategy of a nonmonocot

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flowering with the development of a minimal amount of sec-ondary xylem: a plant can succeed reproductively whiledrawing on a relatively ephemeral water source. Monocots,which have other strategies (Carlquist 2012) are not consid-ered here. However, in the secondary xylem of woods withpaedomorphosis, one can find some indicators, but the phylo-genetic shifting nature of heterochrony is evident in suchgroups (Lens et al. 2012).

a. Once a cambium is formed in a plant, subdivisions leadingto vertically shorter cambial initials usually are formed(Cumbie 1969). Such subdivisions are fewer in plants withpaedomorphic xylem. The fusiform cambial initials thusstay longer, although they do decrease in length as second-ary growth proceeds.

b. Horizontal subdivision occurs in ray initials at a slower pacealso. Thus, ray cells are relatively vertically longer in raysof species with paedomorphosis (Figs. 13A, 13B). Suchray cells are seen not just in woody lobelioids and rosette-tree composites, but also in a wide range of woods thatare suspiciously plesiomorphic: Amborellaceae, Austrobai-leyaceae, and Chloranthaceae, for example.

c. Intrusive growth is characteristic of derivatives of slenderfusiform cambial initials. Those destined to be imperforatetracheary elements (“fibers”) are more capable of intrusivegrowth; those destined to become vessels are not so intru-sive, because their greater width retards intrusiveness.This process takes place more slowly, and thus to a lesserdegree, in woods with paedomorphosis than in “typicallywoody” species. Thus, fusiform cambial initials in juve-nilistic woods tend to decrease in length over time orstay the same (the latter is especially true in storiedwoods). Examples can be found in rosette trees and inglobular cacti (Carlquist 1975, pp. 218–219).

d. Wide primary rays are characteristic of a number of lesswoody eudicots. A vascular cambium can add to suchrays, but instead of subdividing them actively into acomplex of smaller rays (e.g., Barghoorn 1941a), theymay change little over time. Subdivision of rays typi-cally occurs through intrusive growth of fusiform cam-bial initials, and this occurs slowly or not at all inpaedomorphic woods.

e. In some woody angiosperms, rays are narrower at first,mostly uniseriate, with the multiseriate portion of raysonly one or two cells wide. Although in “typicallywoody” species (e.g., Bursera simaruba), rays tend towiden rapidly; some woody species tend to retain nar-rower rays for a longer period of time (Empetraceae).Epacridaceae could be said to exemplify lack of onto-genetic change in both narrow and wide rays, whereas“typically woody” Ericaceae (into which Epacridaceaecan be placed) develop “adult” ray systems rapidly.

f. In a species with short fusiform cambial initials, absence ofhorizontal subdivision in ray initials may result in ray cellsabout the same vertical length as libriform fibers. If the“potential ray cells” become intrusive and thereby are fusi-form in shape, they have all of the characteristics of fibers,and thus a rayless wood results (Hebe, insular species ofPlantago). Ray formation may eventually occur in a raylessspecies depending on how prolonged the juvenility of thewood is in a paedomorphic species (Barghoorn 1941b).

g. Metaxylem pitting patterns of vessels may continue into sec-

ondary xylem with little change, or with delayed changes.These are signals of protracted juvenilism. Piperaceae, whichhave scalariform lateral wall pitting in metaxylem and thenindefinitely thereafter, may be an example of this.

h. The above characteristics are not always found together ina paedomorphic species and very likely have multiple ge-netic causes and multiple phylogenetic origins.

Causes of protracted juvenilismShorter life cycles usually correlate with shortages in water

or extremes in moisture availability or by annual occurrence offreezing. Although there are various other ways of counteringthese conditions, the short life cycle is certainly one. When aplant with a short life cycle enters a new habitat where milderconditions prevail, prolonging the vegetative body of the plantbecomes a positive selective value (stem tissue can be retainedrather than die annually), and secondary woodiness can result(e.g., rosette trees and rosette shrubs in Asteraceae).

a. Oceanic islands provide an excellent example of conditionsfavoring secondary woodiness. Long-distance dispersal of aplant adapted to highly seasonal climate to an oceanic islandwhere the flora is unsaturated and where milder climaticconditions prevail results in selection for prolonged vegeta-tive growth. Not all areas of oceanic islands provide theseconditions, but secondary woodiness is common in lower tomid elevations of the Canary Islands and mid to subalpineelevations of the Hawaiian Islands. Oceanic islands tend tohave broad zones of moderated climate. Frost is minimizedat subalpine elevations because of the temperature-insulatingeffect of broad areas of ocean. Evaporation is thereby low-ered, and increased rainfall may be present (depending onthe geographical location of the island).

b. Mid elevations of mountains in the central Andes or of theeast African volcanoes offer climatic moderation similar tooceanic islands. These “sky islands” also tend to be geolo-gically less stable, thereby offering large tracts of recentlydisturbed rock and soil. These floras therefore tend to beunsaturated, like those of oceanic islands. Because theyare temperate areas surrounded by tropical lowland forestthat lacks adaptation to cold, “sky islands” acquire a largenumber of immigrant species via long-distance dispersalfrom temperate areas such as oceanic islands.

c. Continental islands, as in islands with volcanic activity andrecent glaciation such as New Zealand, may offer nichessuitable for colonization by long-distance dispersal, asshown by woodiness in such genera as Olearia.

d. Coastal Mediterranean-type continental areas offer nichesfor secondary woodiness (e.g., shrubby Lamiaceae incoastal southern California and along some Mediterra-nean coasts).

e. In many instances, less woody (“herbaceous” to various ex-tents) species have excellent capabilities for long-distancedispersal and thus reach islands and island-like areas prefer-entially. As a generalization, forest trees have larger andless dispersible seeds.

f. If one looks at growth forms native to islands and island-like areas (Canary Islands; Carlquist 1974), one findssuch floras relatively poor in annuals, but relatively richin species woody to various degrees. These growth-formspectra represent selective ecological regimens to whichrecently arrived species are likely to respond.

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12. Heterochrony II: rapid ontogeneticchange to adult wood patterns

The opposite of paedomorphosisAccelerated adulthood may be considered the opposite of

paedomorphosis, or protracted vegetative juvenilism. Wehave not noticed this phenomenon because it is the well-known norm in “typically woody” plants, but to understandwood evolution, we have to understand all expressions of it.In fact, early woody angiosperms were most likely paedomor-phic (Carlquist 2009b). Characteristics of “typically woody”angiosperm woods are cited below.

a. Fusiform cambial initials actively subdivide so as to shortensoon after the onset of secondary growth.

b. Ray initials actively subdivide so as to provide verticallyshorter ray cells. The ray initials also soon begin to di-vide tangentially at relatively infrequent intervals in thecentral portions of rays, so that radially elongated raycells are produced.

c. Fusiform cambial initial derivatives rapidly become intru-sive, thereby resulting in vertically longer derivatives.Thus, the “fibrous” wood cells (imperforate tracheary ele-ments) can become much longer than the vessel elements.

d. Ontogenetic changes in ray histology take place rapidly afterthe onset of secondary growth: wide “herbaceous” rays aresubdivided by intrusion of fusiform cambial initials, andnarrow rays widen by vertical radial divisions of cambial in-itials (Barghoorn 1941a). “Adult” ray configuration isthereby rapidly achieved.

e. Accelerated adulthood, once thought to have been univer-sally primitive in angiosperm groups, may have been de-rived as a homoplasy from less woody ancestors on anumber of occasions, and woods with little secondary xy-lem and with protracted juvenilism may have been de-rived from woody ancestors. Woody ancestors may havegiven rise to less woody ones in a number of clades(e.g., Dipsacaceae, some Caprifoliaceae, Adoxa, Apia-ceae, Asteraceae, and Eremosyne in Fig. 14). Angios-perms are unique in being able to shift between moreadult and more juvenilistic expressions readily in someclades (Carlquist 2009b). Conifers, which are a good ex-ample of accelerated adulthood, seem to be incapable ofjuvenilism in the angiosperm senses of the word, and allhave “adult” wood. An exception, so minor that it provesthe rule, can be found in New Zealand conifers that pro-duce juvenile (“heteroblastic”) foliage (Rumball 1963).

f. If scalariform perforation plates occur in primary xylem,there is a rapid shift to simple perforation plates in sec-ondary xylem. This is shown here for Brassaia(Fig. 13C), Eucommia (Fig. 13E), and Kadsura(Fig. 13F) and has been reported for Crossosoma (Carl-quist 2007c). If a woody species characteristically hasscalariform perforation plates in secondary xylem suchas Magnolia (Fig. 13D), there are more numerous barsper perforation plate in metaxylem. Bailey (1944) andBierhorst and Zamora (1965) noted these tendencies fora more “primitive” perforation plate type to be presentearlier in ontogeny and thus thought of primary xylemas a “refuge” for ancestral features. Bierhorst and Za-mora (1965) found that narrower vessels are more likelyto have scalariform perforation plates.

g. “Adult” wood features as a complex, described above, mayall be present in a particular wood, or only some of themmay be. For example, abundance of upright ray cells canbe found in some woody groups (e.g., Epacridaceae, Win-teraceae, Chloranthaceae). Epacridaceae also have raysthat seem “less adult” (section 11). However, the charac-teristics of the tracheary elements in Epacridaceae seemtypical of adult groups. The “Paedomorphic type III” rays(Carlquist 1988) are found in such groups.

h. Groups in which wood is “adult” have a characteristic typi-cal of nonjuvenilistic plants and animals: delay of sexualmaturity. The onset of flowering (sexual maturity) is de-layed in woody angiosperms, often for several years, justas it is in conifers.

The value of accelerated development of adult woodpatternsThe idea of looking at woody plants after considering ju-

venilistic ones may seem ironic (we often think of woodyplants as the “norm”), but the sequence is intentional topresent woodiness in contrast to nonwoody or less woodyconditions in angiosperms. Accelerated change in thecambium and its products, producing adult wood rapidly, isassociated with a series of characteristics. The early angio-sperms may have been only moderately woody, as reflectedin the present-day wood of Amborellaceae, Chloranthaceae,Illiciaceae, and others.

a. Development of more numerous procumbent cells in rayscorrelates with larger plant size. Procumbent wood cellsare active in translocating photosynthates to and fromstorage sites within the wood. The larger the stem dia-meter, the more radial photosynthate activity is likely tooccur, and therefore, the greater the abundance of pro-cumbent cells.

b. Development of more intrusive growth in derivatives of fu-siform cambial initials correlates with greater mechanicalstrength, which in turn permits taller growth forms. Ratiosbetween imperforate tracheary element lengths and vesselelement length (“F/V” ratios) are relatively high in “trulywoody” species (1.5 to 4.0 most commonly; Bailey andTupper 1918). Ratios are lower in woods of basal angios-perms such as Chloranthaceae and Illiciaceae, as well as inspecies with secondary woodiness mentioned in section 11.Taller trees tend to have libriform fibers, whereas woodswith tracheids in addition to vessels (e.g., Sorbus) are oftenmedium-sized. Libriform fibers usually represent the stron-gest of the imperforate tracheary elements, although wallthickness rather than pitting type is an important criterion.

c. The selective value of a rapid shift from scalariform to sim-ple perforation plates (or a shift from longer scalariformplates to plates with fewer bars) is probably less aboutmaintenance of the ancient condition in primary xylemthan production of conductively more efficient vessels insecondary xylem. Woody species tend to occur in sunnyareas or reach canopy status more rapidly than less woodyearly angiosperms, so less impedance in perforation platesmakes sense. This is clearly demonstrated in lianoid generasuch as Kadsura of the Schisandraceae (Fig. 13F) or Tetra-cera of the Dilleniaceae.

d. The size of trees and shrubs is roughly proportional to theirwater supply on an annual and a seasonal basis. More

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“adult” wood is therefore to be expected in woodier speciesof more mesic habitats. Competing in these habitats re-quires considerable investment of photosynthates into me-chanically strong wood cells (and long-lasting leaves).These habitats are often “saturated” forest habitats in which“adult” woods were long ago the established condition.Competition for sunlight, moisture, and pollinators all re-inforce the arboreal syndrome where water permits.

e. A shortcut to the canopy habit is found in lianas. Lianasshow accelerated change to adult ray conditions (Carl-quist 2009b), and this is often accompanied by shorten-ing in fusiform cambial initials as well. Mechanicallystrong imperforate tracheary elements are not of high va-lue in lianas (although ones that sheathe vessels are ad-vantageous). Lianas often have wide rays, extensions ofthe wide primary rays: these are of value in torque-pronestems. The lianoid habit appears to have been a shortcutfor a number of basal angiosperms (Piptocalyx of Trime-niaceae, Schisandra, Austrobaileya, and some species ofPiper). The shift to lianoid habit is accompanied by ac-celerated acquisition of some adult features.

13. Ecological stasis and iteration: stabilityand breakouts in wood evolution

Campanulidae as an exampleIf we look at a phylogenetic tree of Campanulidae

(Fig. 14), we see a number of fascinating revelations aboutwood anatomy, provided that we know relevant data sets.One data set that seems obvious has been added to the Tankand Donoghue (2010) tree: species numbers. However, spe-cies numbers are only an indirect indication of change inhabitat-occupancy capabilities within a clade. Even withoutdetailed knowledge of the habitats of the various campanulidfamilies and genera, one can see that the short early branch-ings of the Tank and Donoghue tree are associated withsmall species per family numbers, and these short brancheshave a very high degree of correlation with scalariform perfo-ration plates (indicated by the curving line superimposed onthe tree in Fig. 14).

Unbroken histories of mesic occupancySome clades appear, by virtue of their wood features, to

have had unbroken histories of occupation of mesic habitats.Within the campanulid clade (Fig. 14), Aquifoliaceae, Rous-seaceae, Argophyllaceae, Bruniaceae, Columelliaceae, Grise-liniaceae, and Paracryphiaceae can be cited as examples. Theevidence is not merely in retention of scalariform perforationplates in all of these families. They also all have tracheids asthe imperforate tracheary element type, mostly diffuse paren-chyma, and heterocellular (heterogeneous) rays. They exhibitno juvenilistic features that suggest phylesis toward or awayfrom herbaceousness. And today, they all occur in mesic hab-itats. The hypothesis consonant with all available informationabout these families is that they have had unbroken historiesin mesic habitats. Any departures have been relatively minor,as in the case of Bruniaceae, which show xeromorphy ingrowth form (shrubs of variously limited size) and in foliarcharacteristics.The obvious conclusion is that wood anatomy is entirely

congruent with habitat, when we take into account probable

occupancy history, wood physiology, foliar apparatus, habit,the nature of microclimates, and how plants occur in thefield. Ecological stasis and ecological iteration are fully vali-dated when one combines this information with informationon ecologically responsive wood characteristics.

Why stay in mesic habitats?The species with scalariform perforation plates in Fig. 14

are woody plants characteristic of moist stable habitats. Thereare few opportunities for radiation within such habitats, andthey tend to be floristically saturated with species. Such hab-itats are rich in species with unbroken occupancy of suchhabitats, if one can judge by their retention of woods withhigh safety characteristics and low vulnerability. Thesegroups include Paracryphiaceae, Escalloniaceae, Bruniaceae,and many of the Aquifoliales. Some of their adaptations thatprobably account for the success of these groups are striking.Bruniaceae, for example, are microphyllous shrubs, most ofwhich grow on south-facing slopes (= the cooler, moisterslopes in the Southern Hemisphere) and on cool mountain-tops. Aquifoliaceae may owe speciation in part to good dis-persal (Ilex occurs on Hawaii, Tahiti, the Bonin Islands, andon several Atlantic Islands). Many Aquifoliaceae are able towithstand frost, and some have drought-resistant leaves. Ilexhas short vessels (Zimmermann and Jeje 1981), which giveits wood conductive safety.The least speciose of the early branches (short-branch)

families of Campanulidae have extraordinarily narrow eco-logical adaptations. Paracryphia has a single species, con-fined to the highest and wettest mountains (also geologicallyold) of New Caledonia. Not surprisingly, it has a wood richin features symplesiomorphic for woody angiosperms(Fig. 4F). The only species of Pittosporaceae with scalariformperforation plates, Pittosporum paniense (Carlquist 1981b),grows in the same area. The other genera of Paracryphiaceae,as well as the short branch families of Aquifoliales and As-terales, have few genera per family and few species per fam-ily.

Moderate departuresAmong the campanulid families, Araliaceae have moderate

degrees of departure from the mesomorphic symplesiomor-phic wood plans of early woody angiosperms. Araliads havescalariform and simple perforations plates (sometimes both ina single wood), with simple perforation plates tending tocharacterize genera in seasonal habitats where frost occurs(Aralia, Hedera, and Kalopanax). Scalariform lateral wallpitting also characterizes some genera: the functional valueof this seemingly symplesiomorphic feature needs furtherstudy. However, one notes that Araliaceae have living fibersin the wood in which starch is stored and retrieved, and ves-sels can be ray-adjacent in some Araliaceae. Storage of starchin libriform fibers may relate to the “flushes” of sudden foli-ation and flowering in many Araliaceae. Araliaceae clearlyfurnish examples inviting ecological interpretation.

Ecological breakoutsBranches of the campanulid tree that have simple perfora-

tion plates can be considered breakouts, as indicated in spe-cies numbers but, more importantly, in a shift to a diversity ofecological sites, including some that offer extreme conditions

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(such as nightly freezing: the Asteraceae Stoebe on Mt. Ki-limanjaro and Loricaria in the Andean superpáramo). Aster-aceae can also enter warm, moist lowland sites if they arenot saturated (oceanic islands). Asteraceae represent themost explosive (and recent) speciation in woody angio-sperms (Funk et al. 2009) but certainly also the most di-verse family of all angiosperms with regard to ecology(Carlquist 1966). Xylem configuration correlates with this(see section 3).

Vessel changes and ecological breakoutsEcological breakouts are accompanied by changes in vessel

element size and not always vessel widening. Woods of As-teraceae show that desert Asteraceae, which are probablymostly recent in their occupancy of xeric sites, have narrowerand shorter vessel elements, a configuration that featuressafety over conductive efficiency. The ability to shift vesseldimensions radically is one of the reasons for success of As-teraceae (see section 3). The ancestors of the family probablylost scalariform perforation plates (there are none even in theprimary xylem). The same nearly holds true for Apiaceae:Solereder (1906) listed a few exceptions, which, consideringthe size of Apiaceae, prove the rule. In such families, canscalariform perforation plates be regained phylogenetically?Has the genetic information for them been lost, or have genesjust been silenced? In lianoid Dilleniaceae, simple perforationplates are present, although scalariform ones are present else-where in the family. If selection favors conductive efficiency,clearly the scalariform condition can be lost readily.The answer concerning reversibility of the scalariform per-

foration plate appears to be a functional one: Whatever thevalue of the scalariform perforation plate in earlier angio-sperms as a mechanism for promoting conductive safety, thatvalue has been replaced in most clades by a multiplicity ofother features that prevent embolism formation or permit ves-sel refilling, mechanisms such as those discussed by Hol-brook and Zwieniecki (1999). The presence of odd,malformed perforation plates in certain Asteraceae (Carlquist1960) can be taken as evidence that genetic information forthe plates is so modified that even if a less conductive vesselelement end wall has some value, its conformation is disor-ganized. Such plates in Asteraceae are very rare, in any case,and alter the conductive characteristics so little that by fre-quency alone, they are not true reversions. Production of sca-lariform perforation plates along with simple ones side byside within a wood can be found in a number of genera suchas Nothofagus (Meylan and Butterfield 1978). This illustratesthat “extinction” of an apparently plesiomorphic feature isgradual, rather than abrupt, and may relate to developmentalfactors. Clearly, the present-or-absent coding of wood charac-ters for cladistic purposes is fraught with difficulty (Carlquist2010).

Radical ecological breakouts and diverse occupancyhistories can occur in basal clades: PapaveraceaeRanunculales is the sister order to the remaining eudicots

(Chase et al. 1993; Soltis et al. 2000, 2011). The basal-mostfamily of the order, the monogeneric Eupteleaceae, has longscalariform perforation plates that even retain pit membraneremnants (Carlquist 1992). The next branch of the clade isPapaveraceae, and the branch after that is Lardizabalaceae.

The shrubby genus of Lardizabalaceae (Decaisnea) has sca-lariform perforation plates, although other Lardizabalaceaeare lianoid and have only vestiges of the scalariform platecondition. One might expect that Papaveraceae, departingfrom the Ranunculales clade after Euptelea but before Lardi-zabalaceae, would have some retention of scalariform perfo-ration plates. A survey of the family (Carlquist and Zona1988) revealed no such perforation plates. I conveyed this in-formation to Joachim W. Kadereit, who had studied the phy-logeny of Papaveraceae. He suggested that I should look atthe genus Pteridophyllum, which he considered the basal-most genus of Papaveraceae, and he sent me some liquid-preserved material. Perhaps the primary xylem would retainscalariform perforation plates, in accord with Bailey’s(1944) refuge idea? In fact, careful study of Pteridophyllumrevealed that both primary and secondary xylem containonly simple perforation plates.The explanation for this seeming exception to phylogenetic

trends probably lies in ecological occupancy theory. Papaver-aceae in this scenario adapted early in their radiation tohighly seasonal conditions that favored conductive efficiency(simple perforation plates) over conductive safety, with othermeans existing for conductive safety within the family. Papa-veraceae, as a whole, may be secondarily woody (Carlquistand Zona 1988). Dendromecon and Romneya are shrubswith multiple stems and occur in coastal and insular southernCalifornia. Bocconia occurs in the central Andean cloud for-est. In these areas, Papaveraceae often occur in disturbedhabitats such as slides or burns. Other less woody genera oc-cur in zones of climatic moderation, whereas most speciesare annuals or biennials. We can hypothesize that Papavera-ceae have had an unbroken history of occupancy of seasonalsites, with minor secondary forays into areas where secon-dary woodiness has been possible, areas with relatively unsa-turated floras. At the very least, any early steps frommesomorphy to xeromorphy in Papaveraceae have not sur-vived.In the campanulid clade (Fig. 14), Eremosyne represents a

spectacular “breakout” from woody Escalloniales: it has littleif any secondary xylem and simple perforation plates. Break-outs like this can occur anywhere in a clade, either in basalgroups such as Eascalloniales or in crown groups such as As-terales.

14. Phylogenetic principles of wood anatomy:what DNA-based trees do and do not tell us

The value of global molecular trees to comparative woodanatomyIn earlier years, studies in comparative wood anatomy re-

quired that one select families for comparison with the oneunder study. One had to rely on the natural systems thenavailable. Unfortunately, those trees, compiled by intuitiveconclusions based on collection of data, were not reliable.The case of the sister families Asteropeiaceae and Physena-ceae is an interesting instance. These Madagascar familieswere of uncertain position. The wood studies of Dickisonand Miller (1993) compared these two families in tabularform with no fewer than 12 families (none of which laterproved to be a member of the order Caryophyllales) in whichAsteropeiaceae and Physenaceae are located according to

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molecular-based phylogenies (e.g., Soltis et al. 2000). Thenumber of potential families for wood comparisons is sogreat that this situation happened routinely during the premo-lecular era. The lesson is not that wood anatomists werewrong, rather that the natural systems on which they reliedwere faulty. By being unable to compare wood of one familywith that of families highly likely, on a DNA basis, to beclosely related, we could not see how wood has evolved.The introduction of global molecular trees showed, in fact,that woods of pairs of closely related families were oftenquite different (e.g., Caricaceae compared with Tropaeola-ceae; Tamaricaceae compared with Frankeniaceae). The ap-preciation of this has been slow, because the idea that woodanatomy must be an indicator of relationship persists andwith some reason (e.g., the presence of vestured pits in ves-sels is common to all families of Myrtales). However, therole of shifts in habit and ecology on wood evolution andthe fact that some groups represented rapid change in woodanatomy, whereas others remained stable for long periods,went unappreciated. In short, we lacked a framework thatcould guide our interpretations of wood evolution.

Caution in use of molecular treesMolecular trees, becoming ever more precise as more

genes are sequenced (e.g., Soltis et al. 2011), are based ongenes that do not code for wood anatomical features. Molec-ular trees have to be based on gene sites with a rate of sub-stitution suitable for large-scale comparison to recoverrelationships (e.g., Fig. 14). Wood features evolve at diverserates, different from the genes used in molecular tree con-struction. Some wood features represent infrequent inventions(vestured pits, tile cells, etc.), and some represent much morecommon homoplasious innovations. Some wood featureshave evolved slowly, and some have evolved more rapidly.Intervention of heterochrony during the evolution of a cladehas produced some surprising results. Wood anatomy mustnot be studied as a historical archive, even though it doescontain much evidence of evolutionary change. Moleculartrees can be used as a basis for showing progression of acharacter (e.g., scalariform perforation plates in Fig. 14).However, the fact that molecular trees are not constructed us-ing gene site substitutions related to wood anatomy meansthat we cannot read out “reversion” of characters (as doneby, for example, Baas and Wheeler 1996). Rather, genomicchange in woods is likely progressive, and reversion of genesto earlier states is not a likely scenario. For example, secon-dary vessellessness in Winteraceae and Trochodendraceaedoes not rely on restoration of genetic states of ancient stemangiosperms. Rather, it probably results from simple modifi-cations that result in nonhydrolysis of pit membranes in endwalls. Transitional stages such as seen in Aextoxicon (Fig. 2),Carpodetus (Figs. 3A, 3B), Illicium (Fig. 3B), and Sarrace-niaceae (Fig. 5), among others, could shift to either more hy-drolysis of pit membranes or less hydrolysis. The alterationof the degree of hydrolysis, probably controlled by modifyinggenes, should not be considered a character state reversion,but rather a shift in a developmental process.

The search for plesiomorphyI.W. Bailey was somewhat disingenuous when he said that

his “major trends of xylem evolution” were developed inde-

pendently of natural systems of classification. In fact, severalof these systems featured the “woody Ranales” (= woodybasal angiosperms of APG (2009)) as a source group fromwhich major groupings of angiosperms might have radiated.Bailey’s interest in the wood anatomy (and other features) ofwoody Ranales is shown by his numerous monographs onthis group. Bailey must have been interested in the phyloge-netic starting point of his “major trends.” Study of these fam-ilies reveals that the traits thought by Bailey and his studentsto be beginning points (e.g., long scalariform perforationplates, tracheids as the imperforate tracheary element type,heterogeneous type I rays, and diffuse axial parenchyma)were common in these families. However, the wood anatomyof the basal angiosperms is by no means uniform (Metcalfe1987). Some of the unspecialized character states just citedmay be found in early branches of various eudicot clades(e.g., Paracryphia of Campanulidae, Euptelea of Ranuncu-lales, Aextoxicon of Berberidopsidales, Dillenia of Dille-niales, etc.). Extant angiosperms are present because they areadapted to where they live today, and we should not be sur-prised to find that their wood features relate to particular con-ditions of ecology and habit. However, the features thatBailey, Frost, Kribs, and Barghoorn regarded as “primitive”in perforation plates, imperforate tracheary elements, axialparenchyma, and rays do look valid as unspecialized charac-ter states, by and large, when one compares these characterstates with molecular trees (Soltis et al. 2011, used for com-parisons in this section). Bailey’s methods can be questioned,but his conclusions were surprisingly acute. They are bestread in retrospect, however, not as starting points for re-search.

Multiplicity of apomorphiesThe Bailey–Frost–Kribs changes in wood character states

would not be valid unless they occurred numerous times in-dependently as homoplasies. For example, the change fromdiffuse to grouped axial parenchyma cells has occurredwithin many different clades. The significance may be forma-tion and enhancement of a support system for vessels, asHolbrook and Zwieniecki (1999) claimed. There may beother explanations (interconnection of axial parenchyma withrays, etc.). If the apomorphies were not multiple, but only afew, they would coincide with a few major branches in thetree of woody angiosperms, but they do not. Once acquired,the advantages of new axial parenchyma distributions do notseem to be abandoned in favor of the early diffuse system; ifthey change, they progress on to varied expressions. The evo-lution of ray histology results in increasing procumbency ofcells in the multiseriate rays. The selective value for this ispresumably increased radial conduction of photosynthates, arequisite of the woody habit (Apiaceae are somewhat excep-tional in this regard, reflecting the pattern in the related fam-ily Araliaceae). An increasing proportion of upright cells inrays may also be found, a feature of paedomorphosis (Carl-quist 1964, 2009b). The Bailey group (except for Cheadle,who studied monocots) worked with “truly woody” speciesand thus lost an important dimension in their picture of howwoods evolve.

Character synchrony dissolutionIn many interesting instances, there is marked change in

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one or more characters in order concomitant with evolution-ary changes, often those of habit. Tropaeolaceae have wood(admittedly not much) that has libriform fibers in the secon-dary xylem and is self-supporting, but they have no phloemfibers. The sister family Caricaceae have large accumulationsof phloem fibers, but fiber-free secondary xylem in whichvessels are embedded in thin-walled parenchyma. Eremosyneis a long-branch derivative of Escalloniales (Fig. 14) that haslittle if any secondary xylem and vessels with simple perfora-tion plates, unlike the remainder of the escallonioid genera.Gornall and Al-Shammary (1998) did find one resemblanceto escallonioids: the unusual glandular trichomes. The sca-lariform lateral wall pitting in Piperaceae represents a discon-nect from the perforation plate type (simple), therebydiffering from the related family Saururaceae.

Different clades, different fatesWhen we study wood features and compare them with the

major clades, we see that some wood features such as ves-tured pits are common in some clades but infrequent or absentin others. For example, vestured pits occur in Brassicales andMyrtales but not in Caryophyllales or the campanulid fami-lies. Rosid families have differentially retained tracheids (Ro-saceae), sometimes adding libriform fibers (Quercus) so thatvasicentric tracheids are present, whereas vasicentric tracheidsare almost entirely absent in campanulids (present in Hederaof Araliaceae and in a few Asteraceae). Different clades havedifferent degrees of heterochrony: secondary woodiness iswell represented in the Lamiidae.

Different characters, different ratesOne is not surprised at the acceleration of perforation plate

simplification with a change in habit, as with Adoxaceaecompared with Viburnum (Fig. 14), or Crossosomataceae(shrubs of arid Mexico and adjacent California) comparedwith other Crossosomatales, which grow in much wetter sit-uations (Carlquist 2007c). One is more surprised when closesister orders, both apparently woody at the outset, differ inthis respect: Berberidopsidales (scalariform perforationplates) and Caryophyllales (perforation plates all simple, per-haps a single bar in a few Droseraceae and Nepenthaceae;Carlquist 2010).

Early diversification versus recent diversificationUsing the same character (scalariform perforation plates),

one can see that early (short-branch) diversification in Campa-nulidae tends to be correlated with retention of scalariformperforation plates (Fig. 14). Aquifoliales, Escalloniales (exceptfor Eremosyne), Bruniaceae + Columelliaceae, and Paracry-phiaceae exemplify this. “Breakouts” characterize brancheswith more site substitutions in the Tank and Donoghue con-struction (e.g., Asteraceae, Calyceraceae, and Goodeniaceae).These latter families can be hypothesized to have speciatedbecause of their capability of maintaining active conductivesystems in wood of species in highly seasonal climates.

Character reinforcement strategyWood physiology experiments that measure resistivity are,

by definition, unifactorial. In terms of wood anatomy, however,conductive characteristics often depend on several featuresworking in conjunction. Conductive safety exemplifies this phe-

nomenon well. Narrow vessels, vessel grouping, short vessels,growth ring formation, helical vessel sculpturing, and axial pa-renchyma configurations that may confer resistance to embo-lism formation (or recovery from it) may coexist in a family(they all can be found together in woods of some Asteraceae).

Old and new adaptations coexistLianas in early-departing (“basal”) clades are wonderful

examples of how changes to individual characters may ac-company plesiomorphic features. If one assumes that trache-ids (as opposed to fiber-tracheids) are plesiomorphic in basalangiosperms, they have been retained in the genera Schisan-dra and Kadsura of Schisandraceae, Piptocalyx of Trimenia-ceae, and Aristolochia of Aristolochiaceae. In all three ofthese instances, simple perforation plates may be found. Sim-ilar examples can be found in lianoid genera of families withnumerous wood plesiomorphies such as Dilleniaceae, Lardi-zabalaceae, and Menispermaceae. As a side note, the reten-tion of tracheids in stems of so many monocots isnoteworthy (Carlquist 2012).Bruniaceae and Sarraceniaceae have tracheids and vessels

with scalariform perforation plates, but bars are relatively fewin number (Carlquist 1978; DeBuhr 1977). In both of thesefamilies, pit membrane remnants are present (Carlquist 1992),so that vessel elements are more tracheid-like, compartmental-izing the vessel to a greater extent. These remnants may havethe effect of conferring greater safety and, in developmentalterms, are readily produced simply by lack of hydrolysis ofthe membranes in perforations (Butterfield and Meylan 1982).Retention of the pit membrane remnants in genera of thesetwo families is noteworthy. Sweeping away of the pit mem-brane remnants in the conductive stream is, in theory, lessreadily accomplished if bars are many and the perforations areaccordingly narrow, as in Aextoxicaceae, Atherospermataceae,Illiciaceae, and Paracryphiaceae. Pit membranes are lacking ina number of families with numerous bars per perforation platesuch as Cornaceae and Hamamelidaceae.

Reversibility in other cell typesDoes true and full reversibility ever occur in wood evolu-

tion, or do woods merely progress to new expressions, usingsome older genetic information as well as some newer infor-mation? If various character states have value during the eco-logical shifts that occur within a clade, reversibility ispossible to that extent. Krameria is sister to the family Zygo-phyllaceae in which fiber-tracheids and vasicentric tracheidsoccur. Krameriaceae and Zygophyllaceae thus retain the ca-pability to form bordered pits on imperforate tracheary ele-ments. The point stressed here is that the bordered pits maybe of various size and density. The developmental changesrequired to make them larger or smaller are best regarded asvaried expressions, a “repertoire” that is always latent, andreversibility in the Hennigian sense is not involved. Krame-ria, characteristic of dry to desert localities, has wood com-posed of vessels with simple perforation plates plus tracheidswith fully bordered pits (Carlquist 2005). Is this a reversionto an ancestral tracheid expression, or is it within the rangeof expression for genetic information present in the zygophyllclade? The latter seems the correct interpretation. Baas andWheeler (1996) cited “reversions” when they compared char-acter states with placement of taxa in phylogenetic trees.

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However, characters and character states are designated byhumans and may bear no resemblance to gene content of aplant or the way in which genes act. In the collision betweenHennigian cladistics (using designated character states) andgenomics (which follows changes at gene sites), we mustchoose genomics. The genes used to construct phylogenetictrees (e.g., Soltis et al. 2011) are not genes related to wooddevelopment.

15. Not wood alone: the relationship betweenfoliage, habit, and wood anatomy

Role of leavesPlants demand considerable water from the environment

and lose much water to it (Holbrook et al. 2002). Plants “re-spond physiologically to water stress, with the dominantmechanism being to reduce rates of water loss by closingtheir stomatal pores” (Holbrook et al. 2002). Brodribb et al.(2003) agreed: “Assuming stomata guard cells directly trans-late physical water potential signals in the leaf and epidermisinto changes in pore aperture, and that the transduction ofthese signals are governed by physical attributes of the guardand epidermal cells, it seems probable that these traits mightco-evolve with traits governing xylem vulnerability.” Hol-brook et al. (2002) add, “However, stomatal closure has thecost of reduced CO2 uptake. The ability to refill a cavitatedvessel would allow plants to regain their original transportcapacity, and without the delays and costs of having to con-struct additional wood.” The fact that vessels refill (evenunder conditions of negative water pressure in the xylem)after cavitation by water stress and the mechanisms for doingthat have been stressed in section 2. In the water economy ofthe plant, the less frequent the cavitations and the shortertheir duration, the better it is for plant survival and reproduc-tion. If we know about foliage and habit, can we betterunderstand wood anatomy in a species? The answer clearlyseems to be yes.

Disconnected woodUnfortunately, those who study wood anatomy often begin

with portions cut from small sample boards stored in xyla-rium drawers, samples often connected by accession numbersto a minimum of information. In fact, even if those speci-mens are related to known herbarium specimens, such speci-mens are, in fact, probably rarely consulted. Even ifconsulted, herbarium specimens do not reveal vital featuresrelating to ecology. Likewise, studies of leaf anatomy andleaf physiology very rarely take into account wood anatomyand wood physiology. Correlations between leaf area andvessel characteristics for Dubautia (Carlquist 1974, p. 153)are simple and easy to make.

The tree biasThe woodier a plant, the more likely it is to be included in

a wood collection. Large families with less woodiness suchas Apiaceae, Asteraceae, and Brassicaceae are woefullyunderrepresented. Anyone attempting wood studies in suchfamilies must do his own collecting and rely minimally onxylaria. However, the reward of collecting plants in the field(rather than using samples from machined microboards in xy-laria) is that one learns much about the vegetative apparatus

of a plant and how that plant interacts with the environment.Precise physiological information? No, but one has the begin-nings of learning about how the vegetative nature of the plantand its wood anatomy might be related. A surprising numberof botanists are misled by the word “herb,” the inadequacy ofwhich should be obvious. Most eudicots that are termed“herbs” do, in fact, have cambia and produce enough woodfor study of wood anatomy (e.g., annual Asteraceae).

Simple beginningsCorrelations of leaf form and size with climate show the

importance of knowing about foliage (Bailey and Sinnott1916; Givnish 1979; Halloy and Mark 1996). These studiespoint the way to what could be measured and how, importantingredients for a wood student wanting to integrate foliageknowledge into wood studies. More complex integration isshown by Brodribb et al. (2003), as well as by Vilagrosa etal. (2003), who join together knowledge of stomatal closure,leaf turgor, and xylem vulnerability. Ideally, one would likesuch studies done on genera that show a great deal of adap-tive radiation. In fact, in Dubautia, “the differences in leafturgor maintenance capacities among the species are related,in turn, to differences in tissue elastic and osmotic proper-ties” (Purugganan et al. 2003). Species from dry habitatssuch as D. ciliolata, D. linearis, D. menziesii, and D. platy-phylla “have much greater capacities for maintaining highturgor pressures as tissue water content decreases than spe-cies from mesic and wet habitats, such as D. knudseni,D. plantaginea, and D. raillardioides” (Purugganan et al.2003). These marked differences among species have hap-pened in a rather short period of time (probably 5 millionyears or less) on the Hawaiian Islands and correlate verywell with data from wood anatomy (Carlquist 1998). Studiesin Dubautia leaf physiology, leaf anatomy (Carlquist et al.2003), and wood anatomy are merely in a stage at which sig-nificant differences are evident (Robichaux and Canfield1985; Robichaux et al. 1986). More detailed studies, whichcould involve wood physiology, could still be done. The Can-arian species of Sonchus offer similar opportunities.

Losing leavesEveryone is familiar with deciduousness related to cold,

but drought deciduousness is very common in some floras.The most obvious example of this tendency may be seen inthe case of drought deciduousness along the coastal strip ofsouthern California, where “coastal sage” species occur. Dur-ing the driest times of the year, Artemisia californica has fewfunctioning leaves on its stems. Coreopsis gigantea has nofunctioning leaves at all during dry months and persists asgreen succulent stems for the duration of the dry period.Less conspicuously, Salvia mellifera, Malacothrix saxatilis,and Mimulus aurantiacus reduce their leaf area markedlyand have only a few, narrow leaves in play at the tips ofbranches at the end of a dry season.Perhaps the most dramatic examples of woody drought-

deciduous shrubs and trees are represented by the familyFouquieriaceae. Fouquieria leafs out after a rain shower (ora moderate watering), but leaves crisp and fall soon there-after unless more rainfall arrives. Only leaves on shortshoots are produced; long shoots are produced only duringthe wet season and may not be produced at all if rains are

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insufficient in a particular year. The wood features of Fou-quieria do not look especially xeromorphic and would, inmost species, match those of an average shrub or tree withrespect to vessel characteristics (Carlquist 2001b). The samecan be said for the wood of a Madagascar analogue of Fou-quieriaceae, the drought-deciduous family Didiereaceae(Rauh and Dittmar 1970).

Leaves that compensate and complementLeaves may have characteristics that lessen stress on xy-

lem. The most obvious are succulent leaves or stems. C4photosynthesis and crassulacean acid metabolism are photo-synthetic pathways that have the effect of lessening stress onthe conductive system of a plant. Microphylly and otherforms of leaf condensation characterize whole floras such asthe fynbos (literally “fine bush,” referring to the small leaves)that one sees in Cape Province, South Africa. Bruniaceae(Carlquist 1978, 1991) and Grubbiaceae (Carlquist 1977) arefynbos shrubs that have the xylem that one would expect inmesic shrubs of early-departing members of a clade, and in-deed, Bruniaceae appear in such a position in Fig. 14. Thewood features scalariform perforation plates, relatively longvessel elements, and tracheids. The leaves are clearly com-pensatory, ranging from small and needle-like to evenscale-like, with notably thick cuticles (Carlquist 1991). Theecological sites occupied by Bruniaceae include south-facingmountaintops (the cooler exposure in the Southern Hemi-sphere), as well as nonmontane sites where undergroundwater sources are more likely to prevail.

Phylogeny toward leaf xeromorphy and xylemxeromorphyAckerly (1999, 2004) used phylogenetic trees of particular

chaparral elements and their relatives in more mesic areas toshow that adaptation to the chaparral has involved decreasingleaf area as a criterion for entry into and success in chaparral.Chaparral habitats feature rainfall confined to a few cool win-ter months. Chaparral shrubs are mostly evergreen, whichputs special constraints on leaf size and anatomy. Woods areappropriately xeromorphic. The fibrous background of manychaparral woods is tracheids (Adenostoma, Cercocarpus, Het-eromeles) or vasicentric tracheids (Arcostaphylos, Ceanothus,Dendromecon, Prunus, shrubby Quercus species), and quan-titative characteristics of vessels are notably xeromorphic(Carlquist and Hoekman 1985).

Reliance and cooperationA surprising number of woody plants have hemiparasitic

interconnections with other plants (Kuijt 1969), includingKrameria and Nuytsia. The nature and degree of hemiparasi-tism and parasitism in these species needs to be taken intoaccount in any understanding of wood anatomy and physiol-ogy. Also, a surprising number of plants in southwesternAustralia form ectomycorrhizal and vesicular–arbuscular my-corrhizal associations (Bell and Pate 1996; Brundrett 2008).Mycorrhizae have a mediating effect, increasing safety andwater-gathering capabilities. These associations explain theoccurrence of shrubs in what appear to be arid and hot areas,especially those of acid sands. Such associations occur insome Californian chaparral genera such as Arctostaphylos(Brundrett 2008).

HabitCorrelations of wood anatomy and physiology are very im-

portant. For instance, the relatively short stature of manywoody plants permits root pressures to be operative in refill-ing cavitated vessels. Succulence definitely plays a role inwood structure, and wood of succulents is particularly poorlyknown, because of its lack of inclusion in wood collections.Cacti are an exception (Gibson 1973, 1977, 1978), and cactioffer many fascinating structure–function correlations in theirwood (Mauseth 1993). Unusual plant shapes such as that ofFouquieria (Idria) columnaris involve special meristematicoccurrences to expand parenchyma within the secondary xy-lem (Carlquist 2001b).

Summing upWood anatomy, wood physiology, leaf anatomy, leaf phys-

iology, and other features are all important in the study ofwoody angiosperms and their evolution. We all realize thatthe ultimate desired synthesis and bridge among these fieldstends not to be realized because all workers are limited tosome degree in training or access to equipment or to thefield. Awareness of the contexts of findings in any one ofthese fields may be indispensable to understanding thesefindings. Synthesis in wood studies, if not easy and if not al-ways ideally performed, is nevertheless essential to under-standing wood evolution.

AcknowledgementsSpecial thanks go to two individuals who encouraged me

and provided facilities and supplies: Thomas S. Elias, whenhe was Director at Rancho Santa Ana Botanic Garden, wascrucial in helping me begin scanning electron microscopy;and Edward L. Schneider, during his tenure as President ofSanta Barbara Botanic Garden, proved equally helpful in sim-ilar ways, permitting me to transfer my research from Clare-mont to Santa Barbara. Those who provided me withmaterials for study were very important: Regis B. Miller dur-ing his years with the Forest Products Laboratory, Madison,Wisconsin, was notable in this regard. Scott Zona provided acareful and helpful review of the manuscript. Christian La-croix kindly invited me to submit this paper to the journalBotany and provided editorial support.

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