901
REVIEW / SYNTHÈSE
How wood evolves: a new synthesis
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Sherwin Carlquist
Abstract: Recent advances in wood physiology, molecular phylogeny, and ultrastructure (chiefly scanning electron microscopy, SEM), as well as important new knowledge in traditional fields, provide the basis for a new vision of how wood
evolves. Woody angiosperms have, in the main, shifted from conductive safety to conductive efficiency (with many variations and modifications) and from ability to resist cavitation (low vulnerability) to ability to refill vessels. The invention of
the vessel was a kind of dimorphism (vessel elements plus tracheids) that permitted division of labor and many kinds of
wood repatterning that suit conductive safety–efficiency trade-offs. Angiosperms were primarily adapted to mesic habitats
but were not failures or “unstable.” They have survived to the present in such habitats well, along with older structural adaptations (e.g., the scalariform perforation plate) that are still suited to such habitats. These “primitive” features are evident in
earlier 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 of
clades (ecological iterations and bursts of speciation and diversification related to new ways of dealing with water economy), whereas in other branchings, other clades show ecological stasis over long periods of time. Newer physiological and
anatomical mechanisms have permitted entry into habitats with marked fluctuation in moisture availability. Wood evolves
progressively, and literal character state reversal may be unusual: genomic and developmental information holds answers to
these changes. Wood is a complex tissue, and each of the histological components shows polymorphism as an evolutionary
mechanism. Cell types within wood evolve collaboratively. Shifts in wood features (e.g., simplification of the scalariform
perforation plate) are commonly homoplastic. Manifold changes in habit and in leaf physiology, morphology, and anatomy
accompany wood evolution, and wood should be studied with relationship to real-world ecology, information that cannot be
gleaned from literature or other secondary sources. Heterochrony (protracted juvenilism, accelerated adulthood) characterizes
angiosperm xylem extensively, far more so than in other vascular plants, and these mechanisms have resulted in many remarkable changes (e.g., monocots have permanently juvenile xylem, woody trees represent accelerated adulthood). Understanding 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 reversal, molecular phylogeny, wood physiology, xylem.
Résumé : Les progrès récents réalisés en physiologie du bois, en phylogénie moléculaire et en ultrastructure (notamment en
microscopie électronique à balayage, MEB), ainsi que d’importantes connaissances nouvelles acquises des champs traditionnels jettent la base d’une nouvelle façon de concevoir comment le bois évolue. Les angiospermes ligneuses ont principalement passé d’une conduction sécuritaire vers une conduction efficace (avec plusieurs variations et modifications), et d’une
capacité de résister à la cavitation (faible vulnérabilité) vers une capacité de remplir les vaisseaux. L’invention du vaisseau
constitue une sorte de dimorphisme (éléments des vaisseaux et les trachéides) qui permettait une division du travail et différents types de remodelage du bois qui conviennent aux compromis sécurité–efficacité de la conduction. Les angiospermes
étaient d’abord adaptées aux habitats mésiques mais n’étaient pas des échecs ou « instables ». Elles ont bien survécu jusqu’à
présent 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 premiers
des arbres phylogéniques basés sur de multiples gènes. Des caractéristiques plus anciennes peuvent encore être fonctionnelles et persistent ainsi, même si de nouvelles formules sont prédominantes en effet. Il y a cependant plusieurs exemples « d’évasion » dans plusieurs clades (itérations écologiques et poussées de spéciation et de diversification reliées à de nouvelles
façons de composer avec l’économie d’eau), alors que d’autres embranchements, d’autres clades sont écologiquement plus
statiques pendant de longues périodes de temps. Les mécanismes physiologiques et anatomiques plus récents ont permis d’aborder des habitats caractérisés par d’importantes fluctuations au plan de l’humidité. Le bois évolue progressivement et un
renversement littéral d’un caractère peut être inhabituel : l’information génomique et développementale a réponse à ces changements. Le bois est un tissu complexe, et chacune de ses composantes histologiques présente un polymorphisme comme
mécanisme évolutif. Les types de cellules à l’intérieur du bois évoluent en collaboration. Les changements des caractéristiReceived 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].
Botany 90: 901–940 (2012)
doi:10.1139/B2012-048
Published by NRC Research Press
902
Botany, Vol. 90, 2012
ques du bois (ex. la simplification de la plaque de perforation scalariforme) sont habituellement homéoplastiques. Les divers
changements dans la physiologie, la morphologie et l’anatomie de la feuille et du port accompagnent l’évolution du bois et
le bois doit être étudié en relation à l’écologie sur le terrain, une information qui ne peut être glanée de la littérature ou
d’autres sources secondaires. L’hétérochronie (juvénilisme prolongé, maturité accélérée) caractérise beaucoup le xylème des
angiospermes, beaucoup plus que celui d’autres végétaux vasculaires, et ces mécanismes ont résulté en plusieurs changements remarquables (ex. les monocotylédones ont un xylème juvénile permanent, les arbres sont un exemple de maturité accélérée). La compréhension de plusieurs caractéristiques réussies de l’évolution du bois des angiospermes doit ultimement
s’appuyer sur les synthèses.
Mots‐clés : théorie de l’évasion, polymorphisme des types cellulaires, évolution collaboration des types cellulaires, itération
écologique, réversibilité de l’embolie, phylogénie moléculaire, physiologie du bois, xylème.
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
[Traduit par la Rédaction]
1. Introduction
What we know now but haven’t synthesized
An enormous amount of new information relevant to
understanding wood function and structure — and therefore
wood evolution — has appeared within the past 30 years.
The fields in which this massive informational gain has occurred include wood physiology, scanning electron microscopy (SEM), transmission electron microscopy (TEM),
ecological wood anatomy, comparative wood anatomy, wood
mechanics, microfluidics, and molecular phylogenetics.
Although many more details in these fields remain to be investigated, the shortage that currently looms is the willingness to synthesize.
Wood physiology branches out
Wood physiology, like wood anatomy, was promoted in
earlier years within forestry institutes. The Harvard wood
physiologist Martin H. Zimmermann did endow his students
with enough breadth in wood physiology so that they could
fit into botany and biology departments of universities, and
Zimmermann’s 1983 book Wood Structure and the Ascent of
Sap did, as the title indicates, reach into structural matters.
However, the nature of physiology is to proceed one experiment at a time, and the luxury of wide synthesis was not, and
probably could not, be extensively enjoyed fully during Zimmermann’s time.
Wood anatomy as an indoor enterprise
The strengths of systematic wood anatomy, from Solereder
(1885) onward through Metcalfe and Chalk (1950) to the
present, have been accumulation of vast amounts of data,
mostly based on dried specimens. The weaknesses of comparative wood anatomy lay in its separation from knowledge of
ecology, habit, and other relevant information. Thus, Metcalfe and Chalk (1950) relegated “ecological anatomy” to
small separate accounts in a handful of their familial summaries, a practice followed even by Gregory (1994). Twentieth
century wood anatomy was defined, and limited, by the existence of xylaria — wood collections, almost always in forestry institutes, in which sample boards, from which small
bits could be removed for study, were kept in drawers. By
being thus separated from their living context, the xylarium
samples lost much of their significance. The species that
formed the nucleus of xylaria were trees that were useful or
possibly 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 study
groups that were “woody” and suited for sectioning by a sliding microtome. This resulted in conceptual shortfall. Bailey
exulted in the fact that his trends of wood evolution were derived independently of systematics. Indeed, during almost all
of the 20th century, angiosperm systematics and phylogeny
were pursued in intuitive ways by collecting data that suggested relationship in the hope that a natural system would
be revealed. I.W. Bailey, whose knowledge of wood anatomy
was encyclopedic, was aware that wood ecology was the
driving force in wood evolution (personal communication,
1956) but avoided incorporating this in his work. Shifts in
wood structure were, to him, an evolutionary verity on their
own terms. The trends that he proposed were progressive
changes that need not be compared with what plants were
doing in nature, or any physiological features (little wood
physiology had been done in that era). These methods were
adopted 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 as
changing inexorably from “primitive” to “specialized.” All
xylem data were considered referable to this progression.
Synthesis as reachable, even inevitable
Books that bridged lines in wood research (e.g., Braun 1970;
Carlquist 1975) were almost palpably resisted and did not reach
their intended audience. In retrospect, we can see that the wider
the synthesis, the less prepared the reader and therefore the
greater the effort required for full comprehension. Today, we
can no longer postpone bridging the gaps between disciplines
that never should have been separated. Detailed criticisms of
failures in synthesis are unnecessary. We can use information
produced by all workers, regardless of how narrowly it was acquired and described. The only constraint in a new synthesis of
the wood form–function–development–phylogenetics continuum is that any new synthesis must be in accord with all of
the available facts. Comparative data do not lie, but interpreting
them 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
Published by NRC Research Press
Carlquist
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
evolved. The conclusion by Sperry et al. (2007) invites further comment: “vessel evolution was not driven by lower
flow resistance, and it may have been limited to wet habitats
by cavitation risk.” They also said that “truly efficient and
safe vessels evolved much later than vessels per se, perhaps
in concordance with larger radiations among core angiosperms.” Sperry et al. (2006) stated that “the evolution of
vessels in angiosperms may have required early angiosperms
to survive a phase of mechanic and hydraulic instability.”
These generalizations deserve re-examination.
What early angiosperm wood looks like
The first five figures (Figs. 1–5) are designed to show the
characteristics of early angiosperm wood and to show that
these apparently ancient features have survived in a number
of major different clades. This array of illustrations shows
what the prototypes of angiosperm wood were like. The conclusion first: these woods did have moderately wide tracheids
(Figs. 1A–1B) or narrow vessels (Figs. 2–5) with high resistivity but, therefore, great potential safety. The end walls of
tracheids or vessels have scalariform pitting, like circular pits
widened out as the cells widen out (Figs. 1D, 1F), a likely
explanation. Conifers retain the circular shape because it is
required by the torus–margo system. The earliest angiosperm
woods look juvenilistic (Carlquist 2009b) and have upright
ray cells. Axial parenchyma is only occasional at first
(Fig. 1E).
In vessel-bearing angiosperms, the end walls are perforation plates and are scalariform and rather long (Fig. 2A), but
with lateral walls that are also scalariform, just with narrower
pits (Figs. 2C, 4E). The perforation plates in early angiosperms 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) or
threads or networks (Figs. 4D, 4F, 5E). These are best
viewed in thick sections and seen from inside a vessel (e.g.,
Figs. 2E, 3D, 5A–5F) because no pit membrane is sectioned
away (Figs. 3A–3B) and we get an idea of how porous the
double pit membrane is (Fig. 4A, above) compared with the
single thickness of the primary wall in the perforations
(Fig. 4B). Why are the pit membranes in perforations so
widespread and in so many orders of angiosperms? These
are the structures that furnish not only resistance to flow, but
also, via a trade-off, confining of air bubbles when water columns are broken into single cells. This is the advantage of
tracheids, so that vessels such as those in Figs. 2–5 are like
“supertracheids,” better than tracheids in flow where diameter is concerned, but with end-wall impedance that provides
safety.
Making comparisons
The conclusions of Hacke et al. (2007) that early vessels
are of little advantage are acceptable as initial probes into
the early hydraulic history of angiosperms, but they are in
need of elaboration and modification. “Resistivity” to flow
in woods can be measured, but a wood with higher resistivity
may merely be a wood with a construction biased in favor of
safety. “Vulnerability” (to cavitation formation) can also be
measured (Vogt 2001). Vogt (2001) selected for comparison
two woody angiosperms with different strategies: Sorbus has
low vulnerability and has vessels that rarely cavitate, whereas
903
Sambucus has high vulnerability and its vessels cavitate frequently but refill readily. Are such differences gradually acquired? Probably not. Schisandraceae is a family that
qualifies as “early” (Illicium, which has plesiomorphic xylem
features, is now often put in the same family). Schisandra can
have wide vessels with simple perforation plates (Carlquist
1999), surely hallmarks of low resistivity, whereas Illicium
woods have the opposite hydraulic characteristics, high resistivity owing to long scalariform perforation plates and narrow
vessels (Carlquist 1982).
How does one compare the hydraulic features of an all-tracheid wood with those of a vessel-bearing wood? Resistivity
of a stem of either can readily be measured (Hacke et al.
2007; Sperry et al. 2007), but if we are comparing how vessels conduct as compared with tracheids, shouldn’t we compare a wood composed wholly of vessels with an all-tracheid
wood? There is no such thing as a wood composed wholly of
vessels, of course. Thus, the conductive effect of a limited
number of vessels per square millimetre must really be considered in contextual terms. On average, about 0.25 mm2 per
1.00 mm2 transection is devoted to vessels (Carlquist 1975,
p. 206). Thus, vessels could be said to be four times as effective as tracheids in conduction. The proportion of wood
transection devoted to vessels is even smaller in some kinds
of plants (succulents, desert shrubs) and greater in others (lianas). In some of these woods, vessels are combined with tracheids, which are conductive (Sano et al. 2011), whereas in
others, the vessels are combined with nonconductive cells
(libriform fibers); there is no known way to measure the conductive capabilities of the ground tissue exclusive of the vessels. Certainly vessels are better designed for conductive
efficiency than an equivalent transectional area of tracheids.
Perforation plates: how much resistivity?
Do scalariform perforation plates, characteristic of “primitive” woods, contribute heavily to resistivity? Sperry et al.
(2007) claimed that “primitive” vessels have a resistivity of
57% ± 15%, whereas Ellerby and Ennos (1998) placed the
figure for scalariform plates much lower (between 0.6% and
18.6%). The sample studied by Sperry et al. (2007) is quite
unusual: Ascarina, Hedyosmum, Illicium, and Trimenia have
prominent pit membrane remnants in the perforations (Carlquist 1992), and these would certainly block flow. The vessel
elements in such genera can be considered “semi-tracheids.”
In fact, “ordinary” scalariform perforation plates without such
pit membrane remnants are quite common: they characterize
genera such as Alnus, Betula, Cornus, Ilex, and Magnolia
and must be counted as well adapted to their habitats. The
habitats of these genera do tend to be mesic (Carlquist
1975), so the point made by Sperry et al. (2007) that early
angiosperms were not conductively efficient does carry some
weight, 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 resistivity. In part, this is because of narrowness of vessels, which
increases resistance inversely to the fourth power of the vessel
radius according to the much-cited Hagen–Poiseuille equation
(Zimmermann 1983). Narrow vessels can have scalariform perforation plates (Illicium) or simple perforation plates (desert
Published by NRC Research Press
904
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 1. Wood of vesselless angiosperms. (A–E) Amborella trichopoda (Amborellaceae). (A) Transection showing lack of vessels (but variability in tracheid diameter). (B) Tangential section. Rays and axial parenchyma are so abundant that no tracheid is isolated from some kind of
parenchyma cell. (C) Radial section. Section through a multiseriate ray to show that most cells are square to upright in shape. (D) Radial
section showing end walls of tracheids. Pitting is scalariform on end walls of wider tracheids. (E) Transection. Parenchyma is occasional in
the wood as a whole but sometimes occurs in bands (dot in each axial parenchyma cell). (F) Tetracentron sinense (Trochodendraceae). SEM
photograph of scalariform end-wall pitting showing small pores in the pit membranes.
shrubs). One could generalize by saying that wood evolution
has proceeded from high resistivity and low vulnerability to
low resistivity combined with high vulnerability. One can select examples of such differences in strategy. For example,
Acer (Taneda and Sperry 2008) and Sorbus (Vogt 2001) tend
not to develop vessel cavitations even on more stressful days,
whereas Sambucus (Vogt 2001) and Quercus (Taneda and
Sperry 2008) do develop cavitations on a regular basis and refill cavitated vessels. The shift from low vulnerability – high
resistivity to high vulnerability – low resistivity is not a linear
process. There are “breakouts” represented by the clade that
includes 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 woods
with high resistivity, but this is apparently not a disadvantage
because 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, vessel
end walls add little friction (whereas vessel lateral walls add
proportionately more, especially when narrow), scalariform
perforation plates do not seem to be a strongly negative factor
in vessel evolution. Available data do suggest that some pressure for simplification of perforation plates occurs in “primiPublished by NRC Research Press
Carlquist
905
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
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 perforation
plate plus a tracheid, below, showing four larger bordered pits. (C) Tip of vessel element showing portion of perforation plate, left, plus
scalariform vessel-tip-to-vessel-tip pitting. (D) Portion of a perforation plate that has retained pit membranes; membranes are absent in places
due to sectioning. (E) Portions of perforations that retain a network of pit membrane remnants. (F) Portion of transection. Axial parenchyma
is common and diffuse; axial parenchyma cells are indicated by dots in the central portion of the photo but are common throughout the wood.
tive” woods: the lianoid Dilleniaceae evidently abandoned the
scalariform condition rapidly (whereas the remainder of the
family did not) in accordance with a shift in the balance in
the trade-off in favor of high flow and low resistivity.
It’s not all about vessel elements
Cell types other than vessel elements may play decisive
roles in the conductive efficiency – conductive safety tradeoff. An appreciable number of woody angiosperms have vessels 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 tracheids
even 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 the
tracheids (as well as in the vessels), judging from the available data (Holbrook and Zwieniecki 1999; Wheeler and Holbrook 2007), perhaps maintaining osmotic pressures by
transferring sugars into the water columns (as with Acer;
Published by NRC Research Press
906
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 3. SEM micrographs of portions of radial sections to show degrees of pit membrane retention in perforation plates. (A, B) Carpodetus
serratus (Rousseaceae). (A) Entire length of a perforation plate. One-half has been sectioned away, and lack of pit membrane remnants in
most perforations may be due to sectioning. (B) Portion of a perforation plate. One cell mostly but not entirely sectioned away; pit membranes
are intact. Some perforation plates in this section naturally lack pit membrane remnants, but many have them. (C) Illicium floridanum (Illiciaceae). Portions of perforations as seen from inside a vessel element (the two halves of the perforation plate therefore intact). Pit membrane
remnants are present, but pores of various sizes are present.
Sauter et al. 1973). Root pressure is certainly a factor in removing embolisms (Fisher et al. 1997). Notice that the “less
woody” 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 root
pressure needed to reverse an embolism may be small (Yang
and Tyree 1992).
Published by NRC Research Press
Carlquist
907
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 4. SEM micrographs of vessel portions from radial wood sections of Paracryphiaceae. (A–E) Sphenostemon. (A) S. lobospora. Perforations 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 of
the double pit membranes is present; larger holes are due to sectioning, but the remainder of the pit membrane represents a natural condition
of porousness. (C–D) S. pachycladum. Portions of a perforation plate. (C) Near end of perforation plate showing a greater degree of pit
membrane presence. (D) Center of perforation plate’s only strandlike pit membrane remnants are present. (E) S. lobospora. Scalariform lateral
wall pitting. (F) Paracryphia alticola. Portion of perforation plate seen from inside vessel element; pit membrane remnants are mostly artifactfree and are extensive.
The emerging picture
Recent wood physiological literature emphasizes that much
angiosperm speciation has been attended by development of
vessels prone to embolism risk combined with mechanisms
for countering those risks. Vessel cavitation due to drought
is probably different from that due to freezing, if the examples shown by Langan et al. (1997) are more widely applica-
ble. We have an idea of the probable mechanisms for refilling
vessels (McCully et al. 1998; Holbrook and Zwieniecki 1999;
Wheeler and Holbrook 2007), as well as some of the mechanisms 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
Published by NRC Research Press
908
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
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 with
minimal 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 (Droseraceae). Perforation plate simple, but only half the diameter of the vessel.
the water columns are far more resistant to embolism formation (Sano et al. 2011). The state of our knowledge has been
succinctly summarized by Vogt (2001):
Several papers have shown refilling during the growing
season in different species, for example, in Plantago (Milburn and McLaughlin 1974), Zea mays (Tyree et al.
1986), and Rhapis excelsa (Sperry 1986). Refilling is explained by predawn water potentials rising to near zero
(Tyree et al. 1986), rainy periods (Sperry 1986), and root
pressure (Milburn and McLaughlin 1974; Pickard 1989).
Recent studies, however, indicate that embolism removal
may be concurrent with transpiration and with considerable 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 been
hypothesized that vessel embolism is a reversible phenomenon made possible by the interaction of xylem parenchyma, vessel wall chemistry, and the geometry of
intervessel pits (Holbrook and Zwieniecki 1999).
The achievements in improving our understanding of how
some vascular plants resist embolisms whereas others experience frequent events of cavitation followed by refilling are
Published by NRC Research Press
Carlquist
909
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 6. Wood sections showing presence of vasicentric tracheids, vascular tracheids, and degrees of vessel grouping. (A–B) Ceanothus thyrsiflorus. (A) Transection. The background tissue consists of narrow libriform fibers; several vessels are embedded, center, in a group of vasicentric tracheids (narrower than the vessels, but wider than libriform fibers). (B) Radial section. A vessel is seen, center; to the left of it are
vasicentric tracheids; to the right of the vessel are libriform fibers. (C–D) Artemisia filifolia. (C) Transection. The large vessels denote earlywood; the three or four terminal layers of latewood to the left of those are narrow vessels and vascular tracheids. (D) Tangential section. The
left half of the photo consists of narrow vessels with simple perforation plates; in the right half are narrower tracheary elements of similar
length that lack perforation plates and are therefore vascular tracheids. (E–F) Portions of a transection of Artemisia tridentata wood. (E) A
portion of two growth rings from a period of active growth. A layer of interxylary cork delimits the latter half of a growth ring (left) from
earlywood (right). The latewood vessels are large, but very narrow vessels and vascular tracheids are formed just prior to the interxylary cork
layer. The earlywood of the growth ring at right begins with rather narrow vessels, indicating growth in response to moisture availability but
cold temperatures, and is followed by wider vessels formed during warmer months. (F) Terminal growth rings of the same section; as the
growth of this stem declines, several rings of very narrow vessels are formed.
evident from the above studies. We know enough to see that
there is a diversity of strategies that occur in wood structure
of different species. There are obviously trade-offs between
conductive efficiency and conductive safety. If the angio-
sperms began with wood that featured conductive safety,
which therefore limited them to mesic habitats, there have
been many shifts, as well as diversifications of mechanisms
for conductive safety, and therefore a complex picture has
Published by NRC Research Press
910
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 7. SEM images of types of vessel wall sculpturing that are claimed to prevent air embolisms or help in refilling of vessels. (A) Tilia
americana (Tiliaceae or Malvaceae). Slender helical thickenings with tapered endings. (B) Poliomintha longiflora (Lamiaceae). Paired thickenings alongside pits. (C) Prostanthera rotundifolia (Lamiaceae). Sparse, clearly defined thickenings that tend to be associated with pit apertures. (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 (Fabaceae). Vessel wall seen from the outside; numerous vestures are seen in the pits; pit membranes are removed by sectioning except in the upper
left corner. (H) Cercidium floridum (Fabaceae). Vessel wall seen from inside vessel; no texturing is present on wall surface, but vestures may
be seen in the pit apertures. (I) Cercidium australe (Fabaceae). Coarse interconnected warty structures on the inside wall of a vessel; pits have
collarlike rims (“crateriform pits”).
Published by NRC Research Press
Carlquist
911
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Table 1. Quantitative wood features of Asteraceae.
Rainfall
Mesic
Dry
Desert
Latitude
Temperate
Tropical
Habit
Annual or biennial
Caudex perennial
Shrub
Tree
Rosette tree or shrub
All species
n
VD, µm
V/G
VEL, µm
Helices, %
Storied, %
161
129
38
66
39
34
3.04
5.20
8.37
282
198
155
49
57
68
48
37
68
191
137
51
65
5.68
2.64
191
300
61
46
53
36
35
29
173
38
52
328
46
39
45
84
68
51
2.74
4.45
6.26
1.94
2.22
3.62
186
152
240
312
292
235
34
77
63
68
19
55
6
48
50
52
50
45
Note: VD, mean vessel diameter (outside diameter; lumen diameter would be 3–5 µm less); V/G, mean number of vessels per
group; 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.
emerged. Do we know enough that we could predict the
probable efficiency–safety trade-offs for most angiosperms?
The above results indicate that we are further along that pathway than might have been thought possible a few decades
ago. We have reached a stage at which wood histology can
be predictive of probable physiological characteristics. If my
(Carlquist 1975) book was dismissed as premature earlier
(e.g., Zimmermann 1983), it might look foresighted, if
flawed, 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 data
from wood anatomy. In doing so, we must, however, take
into account the fact that habit and foliar characteristics can
be of overriding importance or moderating influences, at
least where wood physiology is concerned. Therefore, the
predictive value of wood histology must be tempered by
whole-plant knowledge. A section below citing such features — which may range from endomycorrhizal roots to
sunken stomata or crassulacean acid metabolism — can be
included in our interpretations of wood anatomy and physiology of any particular plant.
3. Vessel repatterning as a way of
adaptation: woods of Asteraceae as
examples
Asteraceae as an experiment in wood anatomy
Asteraceae (Compositae) are a family of at least 23 000
species (Funk et al. 2009). Commonly thought by North
Temperate botanists to be nonwoody, an appreciable number
are shrubs or trees, especially in subtropical latitudes. Most
annuals 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 crown
group, Madieae (Carlquist et al. 2003; phylogeny from Funk
et al. 2009), in qualitative characters. There is very little
“evolutionary” range, meaning essentially that the differences
among species are the result of rapidly and recently acquired
character states that reflect ecology. Even the sister group of
Asteraceae, Calyceraceae, has the same basic qualitative
wood features. Wood of the family can be likened to a natural experiment designed to show how wood histology
changes in response to ecology and habit.
Ecology as the key
The discovery that wood of Asteraceae was an ideal indicator of ecology and that conclusions were applicable to
woody angiosperms at large was fortuitous, a by-product of
my early interest in the family. I monographed the wood of
the family tribe by tribe and found no phylogenetic patterns
(in those days, one expected phylogenetic dividends from
any comparative anatomical investigation). Only when summarizing the data from the family collectively (Carlquist
1966) did I see that the patterns were quite precise ecological
indicators. This is not surprising, considering that composites
represent a relatively recent, mostly post-Miocene explosion
(Funk et al. 2009) into a very wide range of habitats: very
few places in the world are free from them. An abbreviated
version 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 (embolize less often than wide vessels) in a particular wood (Hargrave et al. 1994), whereas wider vessels promote flow with
less friction: the Hagen–Poiseuille equation (Zimmermann
1983). In wet forest trees, an average vessel diameter of
100 µm is not unusual (Metcalfe and Chalk 1950). Thus,
even “mesic” Asteraceae (Table 1) are biased in favor of
safety, probably because the family so characteristically occupies disturbed sites. One could pick a particular vessel diameter that seems to represent a midway point in the safety–
efficiency trade-off, but we need to remember that within
any given wood sample, there is considerable deviation in
vessel diameter. However, the data in Table 1 suggest that
the safety–efficiency threshold value might lie at around 55–
60 µm. Note should be taken that wood does not operate on
the basis of an “average” cell, but on the basis of all of its
conductive cells.
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
912
Why compromise?
The growth ring is, of course, an ideal way of solving the
trade-off problem in vessel diameter (Figs. 6C–6F). There are
many kinds of growth rings (Carlquist 1980, 1988, 2001a),
so the solutions are multiple. Ideally, one would design earlywood vessels that would be wide enough to supply actively
transpiring foliage while soil moisture is available. The earlywood vessels would either be subjected to few embolisms or
be able to repair them. The latewood vessels would be narrow enough so as to deter embolism formation and would
provide water columns wide enough to conduct sufficient
water when the earlywood vessels permanently embolize.
This curriculum probably is close to what particular plants
do (e.g., Hargrave et al. 1994), but we do not have speciesby-species knowledge of growth ring physiology — only a
few species have been studied in this respect. Even for those
few species, the physiological behavior of subsidiary conducting cells (vasicentric tracheids, tracheids, etc.) is unknown (with a few exceptions: Braun 1970; Sano et al.
2011) because the physiology of nonvessel cells in vesselbearing 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 (Carlquist
1975, p. 163), there appears to be a “packing limit.” If one
makes calculations of vessel area per square millimetre of
transection (Carlquist 1975, p. 206), one finds that different
plant types differ quite markedly: trees have 0.24 mm2 vessel
area/mm2 of transection; lianas, 0.36; shrubs, 0.19; and stem
succulents, 0.09. Considerable wood volume is devoted to
functions other than conduction. Mechanical strength, sheathing
of wide vessels, water storage, starch storage, flexibility, and
living cells supporting the conductive system are some of the
functions that come to mind. These functions cannot be measured 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 Carlquist
1988, 2001a; Sano et al. 2011). Tracheids are conductive and
have wide-bordered pits, fiber-tracheids have vestigial borders
on pits and are not conductive, and libriform fibers have simple pits and are not conductive. When a wood with tracheids
or vasicentric tracheids experiences cavitations, tracheids can
serve to maintain the conductive pathways until vessels are
refilled. Tracheids or vasicentric tracheids are much less
prone to cavitation than vessels. This has an interesting consequence. If libriform fibers are present, as they are in Asteraceae, there is another mechanism that can maintain
conductive pathways: grouping of vessels. If a larger vessel
embolizes, an adjacent smaller vessel may not, so the smaller
vessel maintains the conductive pathway. Asteraceae have
vessel grouping (Table 1), and its degree is proportional to
the likelihood of failure, based on the dryness or seasonality
of the habitat (Artemisia, with extensive vessel grouping,
lives mostly in dry habitats; Figs. 6C–6F). Thus, vessel
grouping alone can be used as a way of detecting whether
there are conductive imperforate tracheary elements present
in a wood. If vessel grouping is below about 1.3 vessels per
Botany, Vol. 90, 2012
group in a vessel-bearing angiosperm, tracheids are probably
present. Also, vessel grouping potentially offers more redundancy than ungrouped vessels.
How should vessels be grouped?
Vessels may be grouped in various ways for various reasons (for a review, see Carlquist 2009a). The most common
type of grouping, found in Asteraceae, is radial clusters or
chains. This type of grouping provides a way in which there
can 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 be
adjacent to some other vessel. Preservation of conductive
pathways despite cavitations seems an important strategy. If
the pathways still contain water columns, even though some
vessels are cavitated, reconstitution of the pathway can take
place.
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 embolisms
to end at the ends of vessel elements. Thus, the shorter the
vessel element, the more localized are the interruptions to
the conductive system. Smaller, more localized embolisms
are more readily reversed (Holbrook and Zwieniecki 1999).
Longer vessel elements offer less end-wall resistance and are
thus of value in mesic habitats where conductive efficiency is
favored (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 in
conductive efficiency (Zimmermann and Jeje 1981). However, shorter vessels may be present in a wood as well as longer vessels; there is commonly a variety of vessel lengths in a
given wood (Zimmermann and Jeje 1981). A narrower vessel
is often shorter, often less than 4–10 cm. Shorter vessels represent a conductive compromise: if vessels are better at conductive efficiency than tracheids because of diameter, longer
vessels are better at conduction, because they represent nearly
ideal capillaries, a triumph of the woody dicot that has cambial activity the length of the plant. Monocots, which have
adventitious roots, lack this continuity and have other patterns (Carlquist 2012). Shorter vessels offer safety: confinement of air embolisms to a shorter vertical length of a water
column rather than the length of a plant. One can consider
them a sort of “megatracheid.” Not surprisingly, shorter vessels are found in latewood of growth rings, whereas longer
vessels 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 interconnect pit apertures (“coalescent pit apertures”), or thickenings
that parallel the grooves (Table 1). We have known for a long
time that helical sculpturing is more common in plants of
colder or drier habitats (Table 1). It is also more pronounced
in latewood than in earlywood (Carlquist 1975). These facts
counter the idea by Jeje and Zimmermann (1979) that helical
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
thickenings accelerate flow, because helical sculpturing is
most prominent in precisely the vessels in which flow is
characteristically slowest. Although an increase in surface relief on the vessel surface may be varied in shape and prominence, all manifestations probably represent an increase in
surface area (Fig. 7). Such sculpturing has the effect of reducing air bubbles in vessels because it increases wettability
and thus reverses (and well as presumably prevents) cavitations (Carlquist 1982, 1983; Kohonen and Helland 2009).
Kohonen and Helland (2009) said that wettability is increased by surface relief of vessels: “wall sculpturing does
enhance wettability,” which tends to prevent cavitation and
also aids in “the removal of bubbles in microfluidic channels.” Forms of helical sculpturing have evolved many times
independently in woody angiosperms (homoplasy) and are
probably easily achieved because the pattern of these structures seems to parallel the cyclosis of the cytoplasm that laid
down the secondary walls (Figs. 7A–7E).
Vestured pits
Vestured pits (absent in Asteraceae, but characteristic of
some other groups, notably Myrtales) and vesturing on vessels
and tracheids (wart-like coverings of the wall facing the lumen)
are an allied phenomenon. Vestured pits do not form a category
separate from vesturing, and both may be found in some genera
(Metrosideros; Meylan and Butterfield 1978). Vesturing may be
more prominent in latewood (Parham and Baird 1974). The
idea that vestures form a flat-topped array that prevents the pit
membrane from excessive deflection (Zweypfenning 1978; Jansen et al. 2003) has been countered by the demonstration that
these protuberances increase wall surface and thus have much
the same function as helical sculpturing (Kohonen and Helland
2009; Choat et al. 2004). Not only do vesturing patterns on lumen surfaces run counter to the Zweypfenning explanation,
there are instances of vestured pits in which the warts are clustered at the pit apertures and are not at all close to the pit membrane (Fig. 7) or are even on the pit cavity surface, as in
conifers (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. Certainly a growth ring shows how readily wide and narrow vessels can be formed by the cambium at appropriate times and,
accordingly, how vessel density or sparseness in a wood can
be achieved. As various clades of Asteraceae have adapted to
desert conditions, narrowing of vessels has occurred, and the
reverse pattern has occurred as a clade enters moister habitats
(e.g., Dubautia; Carlquist et al. 2003). Change in vessel element length has a phylogenetic aspect in woody angiosperms
as a whole (Bailey 1944), but in Asteraceae, a wide span of
the gamut from permanent juvenilism to accelerated adulthood is evident (Carlquist 2009b), perhaps because of the
value of shorter vessel elements in xeric habitats and longer
ones in wet habitats, as cited above. Length of fusiform cambial initials is easily modified by increasing or decreasing the
pace of vertical (or pseudotransverse) divisions in these initials. Storying (Table 1) is also a reflection of this: the fewer
the vertical (or pseudotransverse) divisions in fusiform cambial divisions in a stem, the later the onset of storied histology in the wood. In Asteraceae, storying is thereby a
913
combination of length of fusiform cambial initials (which
governs the length of vessel elements, an adaptive feature related to ecology) and the degree of juvenilism in the wood (a
feature 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 are
many optimal conditions, especially in wood as diverse as
that of angiosperms. More importantly, the idea of an optimal
structural condition does not take into account why “primitive” (plesiomorphic) conditions should be extant today. In
fact, angiosperm woods with plesiomorphic features are relatively common. We need to account for why these types are
alive today. Woods with scalariform perforation plates are
abundant today, even forming whole forests (Betula, Cornus,
Liquidambar).
The idea that vessels represent a key innovation in angiosperms that has led to dominance and radiation of angiosperms has often been held, if only implicitly. We now know
that the earliest branches of the angiosperm tree are vesselless (Amborella, Nymphaeales), although secondary vessellessness has occurred a few times (Winteraceae,
Trochodendraceae; Chase et al. 1993; Soltis et al. 2000,
2011). Obviously, invention of vessels took place early in angiosperm evolution, according to these molecular phylogenetic 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 sufficiently clear of pit membranes to qualify a cell as a vessel
element.
In woody angiosperms, a division of labor (i.e., vessel elements vs. imperforate tracheary elements, with progressively
more differences between these types) is inferred (Bailey and
Tupper 1918; Bailey 1944). If we look at particular woods,
this idea can be supported, but the more we look at wood
physiology, the more complicated the situation becomes.
“Primitive” angiosperm woods have high resistivity (i.e., conduction efficiency lowered by friction) according to the data
of Sperry et al. (2007) and are thus not a structural formula
that is suited to a wide range of ecological sites. “Vessel evolution was not driven by lower flow resistance, and it may
have been limited to wet habitats by cavitation risk” (Sperry
et al. 2007). Is this literally true? Clearly, woods with more
numerous plesiomorphic features (scalariform perforation
plates, tracheids as a ground tissue, and diffuse axial parenchyma) are much more common in mesic habitats than in
drier ones (Carlquist 1975), with some seeming exceptions
such as Bruniaceae and Grubbiaceae. Certainly angiosperms
with low wood resistivity and an abundance of apomorphic
features have invaded these same habitats, yet the species
with ancient xylem formulae are still there. Certainly simple
perforation plates can be developed readily from ancestors
with scalariform perforation plates, as shown by Schisandraceae and by the various families of Ranunculales, as well as
other basal branches of the angiosperm tree, as given by Soltis et al. (2011) and others. Why are woods that do not have
Published by NRC Research Press
914
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 8. Two complementary drawings that represent how bordered pits function. (A) The bordered pit is seen as a structure maximizing flow
while minimizing loss of wall strength (from Carlquist 2001a). (B) A drawing designed to show how water from a tracheary element with an
intact water column, left, refills a cavitated tracheary element, right, via a bordered pit. “As water enters the bordered pit channel (1), it forms
a 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).
“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 efficient
conductive capabilities, but that there are trade-offs involved,
not an unalloyed series of advantages or inexorable progress
to an optimal combination of character states. The hypothesis
proposed here is that wood features evolve independently of
each other and match ecological adaptations.
Reasons for perforation plate retention in “primitive” woods
Zimmermann (1983) offered the intriguing idea that in
temperate areas with frost, scalariform perforation plates
“sieve out” air bubbles that result from thawing of winter ice
in vessels. This “conductive safety” feature might account for
wood of many cold temperate forest trees such as Betulaceae,
Hamamelidaceae, and Nothofagaceae. These trees have broad
leaves that are probably not compatible with fluctuation in
soil moisture and therefore transpiration rates, but wet temperate forest trees with scalariform perforation plates live in
soil that is either wet or frozen, and the latter condition occurs when leaves are shed. Thus high conductive resistivity
in these trees is also high in conductive safety, a workable
trade-off.
How much resistivity does a scalariform perforation plate
confer?
There are various estimates of how much resistance the existence of a scalariform perforation plate confers (Schulte and
Castle 1993a, 1993b; Ellerby and Ennos 1998; Sperry et al.
2005). These measurements disagree from one another because different methods were used. Nevertheless, one can
say that the resistance of the scalariform perforation plate is
sufficient so that if selection favors maximizing conductive
flow, the number of bars will be reduced over evolutionary
time, a fact confirmed by the comparative data (Bailey and
Tupper 1918; Frost 1930a). Analysis of global phylogenies
(e.g., Fig. 14) also confirms this. On the other hand, the resistance of the scalariform perforation plate may be low (especially as it approaches the simple perforation plate
condition) so that it is tolerable if it serves some other function such as increasing conductive safety. It appears to do
that (Slatyer 1967; Sperry 1986). Thus, a trade-off interpretation is viable, and the slow disappearance of the perforation
plate in evolutionary terms becomes understandable.
Scalariform perforation plates can be found in latewood of
some species that have simple perforation plates in adjacent
earlywood (e.g., Styrax). This shows both the value of perforation plate simplification and how rapidly it can occur. However it also shows that higher resistivity in latewood is
probably not disadvantageous; if so, a slower rate of conductive flow may be responsible.
The resistance of the side walls of the vessel is proportionate to vessel diameter, as well as to end-wall resistance
(Sperry et al. 2005). There is a tendency for bars of the perforation plate to become fewer as the vessel widens (a tendency
easily seen in lianoid vs. tree Dilleniaceae). Not surprisingly,
species with long scalariform perforation plates also have relatively narrow vessels (Bierhorst and Zamora 1965). Is extinction of the last few bars of a plate slowed as the resistance of
the plate lowers? As with many vestigial features, this is probably the case, so persistence of few-barred scalariform perforation plates phylogenetically is to be expected. This is
confirmed in clades such as that of Fig. 14. Vessel diameter,
in a particular stem, tends to become wider for trees that are
reaching a water table (Carlquist 1984), but vessel diameter
may become narrower if a shrub is faced with a finite water
supply in competition with other shrubs (e.g., Artemisia;
Figs. 6E–6F). Allometry is not involved.
Published by NRC Research Press
Carlquist
915
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
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, less
prominent borders of pits, typical of fiber-tracheids. (C–E) Sambucus mexicana (Adoxaceae). (C) Outside of libriform fibers showing small
simple 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.
Resistance is also conferred by having many shorter vessels instead of a few long ones: a compromise in favor of
safety. This is true of, for example, Ilex (Jeje and Zimmermann 1979), a wood that is in an early-branching clade of
Campanulidae, Aquifoliales (Fig. 14).
Pit membrane remnants: “semi-tracheids” and “neotracheids”
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 Butterfield 1978; Carlquist 1978, 1992). Aextoxicon (Fig. 2E), Carpodetus (Fig. 2A), Illicium (Fig. 2C), Paracryphia (Fig. 4F)
and Sphenostemon (Figs. 4A–4E) are good examples. Are
these just historical remnants of a tracheid-like condition? Selective pressure is too common and too widespread in angiosperms for such remnants to be considered merely persistence
of an ancient feature. Intact pit membranes in scalariform perforations of a wood are always accompanied by perforation
plates in which the perforations are clear or partially occluded.
Published by NRC Research Press
916
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 10. Transections of woods to show distinctive tissue adaptations. (A) Cayratia clematidea (Vitaceae). Vessels are mostly wide (wv) and
sheathed with fibers (fs); narrower vessels (nv) are also present. The background axial tissue is thin-walled axial parenchyma (ap); vascular
rays (vr) are wide and few, with thin-walled cells. (B) Orphium frutescens (Gentianaceae). Strands of interxylary phloem (ip) are scattered in
a wood that otherwise consists of narrow vessels (v), libriform fibers, and rays.
Published by NRC Research Press
Carlquist
917
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 11. Details of pitting in parenchyma of woods. (A–D) Bordered pits on ray cells. (A) Bordered pits (seen in sectional view) of upright
ray cells from radial sections. (B–D) Buddleja bullata (Buddlejaceae). (B) SEM photograph of sectioned wall of upright ray cell showing
bordered pits. (C) Bordered pits seen on outer surface of upright ray cell from tangential section. (D) Bordered pits seen on outer surface of
procumbent ray cells from tangential section. (E–F) Trigoniastrum hypoleucum (Trigoniaceae). Axial parenchyma cells (with adjacent fibertracheids) from radial section. (E) Cross wall of strand with bordered pits (bp); bordered pits are also present on the axial walls. (F) Cross
wall of strand with a larger simple pit (lsp); inconspicuously bordered pits are also present on the axial walls.
Scalariform perforation plates (Fig. 3B) with intact pits occur
occasionally (Fig. 3C). Such vessels could be called “semitracheids” perhaps, or “neo-tracheids” if one wants to imply
secondary acquisition of pit membranes in perforations. Such
pit membranes would offer more resistivity to flow but would
also give much better sequestration of air bubbles. However,
the woods in which such vessels occur also contain perforation plates in which pit membranes are absent. The intriguing
idea of Holbrook et al. (2002) that shrinkage of pores in pit
membranes with increasing ion concentration in sap and
thereby shrinkage of hydrogels in the pit membranes (a reversible change enhancing flow) may be applicable here
(although it needs more work; Van Ieperen 2007). In any
case, we find pit membrane remnants in perforation plates in
early-departing branches of clades in plants of very wet habitats (Fig. 14; Carlquist 1992). Feild et al. (2002) suggested
that the secondary vessellessness of Winteraceae may put
them at an advantage where freezing occurs: this is possible,
but Winteraceae are not “ecologically abundant” as those authors suggest, and Winteraceae is a relict family under most
Published by NRC Research Press
918
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 12. Examples of successive cambia and their ontogeny. (A) Stegnosperma alimifolium (Stegnospermataceae). The master cambium (large
pointers) produces several layers of secondary cortex (sc) externally; outside of that are primary cortex cells (c). Internal products of the
master cambium include successive bands of conjunctive tissue (ct) and vascular cambia (vc), each of which produces rays (r), secondary
xylem (sx), and secondary phloem (sp). (B) Operculina palmeri (Convolvulaceae). Tissues are produced by a single vascular cambium except
for a pith cambium (pc), which produces secondary phloem internally (extreme left edge) and a few vessels internally. The main vascular
cylinder begins with primary xylem vessels in radial rows, separated by rows of axial parenchyma (pxv + ap), proceeds with a band of narrow (fibriform vessels plus tracheids (nvtt), and then continues with wide vessels (wv) in a background of tracheids plus patches of axial
parenchyma (ap). Occasional wide rays (owr) originate abruptly.
Published by NRC Research Press
Carlquist
919
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
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 scalariform (left), secondary xylem perforation plates (right) mostly simple, with some scalariform plates formed in early secondary xylem (some
other Araliaceae have intermixed simple and scalariform perforation plates). (D) Magnolia grandiflora (Magnoliaceae). Scalariform perforation plates are formed uniformly in the secondary xylem (more numerous bars per plate occur in metaxylem). (E) Eucommia ulmoides (Eucommiaceae). 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 are
wide, with simple perforation plates (e.g., center).
definitions of that term. Areas close to where freezing is moderate are more likely to stay moist longer, and that probably
explains winteraceous ecological preferences.
New uses for bars on perforation plates
A surprising number of woody angiosperms have few, but
notably wide, bars on perforation plates. One can cite Araliaceae (Rodriguez 1957), Empetraceae (Carlquist 1989a), and
Epacridaceae (Lens et al. 2003), as well as such well-known
genera as Magnolia (Fig. 13D), Rhizophora, Ribes, and
Styrax (Carlquist 2001a, p. 64). Are such perforation plates
mechanical enhancement that offers support to vessels under
Published by NRC Research Press
920
Botany, Vol. 90, 2012
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Fig. 14. Molecular tree of the superorder Campanulidae, from Tank and Donoghue (2010). The curving line superimposed on their tree delimits species with simple perforation plates (to the right) from those with scalariform plates (placement of this line is inexact in some places
because of the large number of taxa). Note that species numbers in families (which have been added to the original tree) are, in general, much
larger in families with simple perforation plates. “Branch lengths are proportional to the mean number of substitutions per site as measured by
the scale bar.” For other conventions, see Tank and Donoghue (2010). Modified and reproduced with permission of the authors.
Published by NRC Research Press
Carlquist
tension, thereby permitting the xylem in these species to have
lowered vulnerability to deformation and embolism formation? We need studies to find the answer.
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Vessel element length as a factor
There is no question that vessel element length in species with scalariform perforation plates is, on average,
longer than tracheid length for any given species that has
tracheids (Bailey and Tupper 1918; Frost 1930a; Carlquist 1975). Fewer cross walls per unit of vessel offers
less impedance, but the presence of bars on perforations
plates, especially if numerous, runs counter to any flow
advantage.
Vessel elements are better than tracheids
If one performs experiments in which resistivity to flow is
measured by laboratory methods involving whole stems (as
opposed to individual cells), one can find that vessel-bearing
woods with scalariform perforation plates have high resistivity to flow (Sperry et al. 2007). However, what if one were to
imagine comparing the conductivity of a vessel lumen 75 µm
in diameter (a not uncommon vessel diameter in such woods)
with a number of tracheids, the lumen diameter of which
would total that of such a vessel? In terms of such individual
cell comparisons, the vessel has a greater flow than the
equivalent lumen area of tracheids. Unfortunately, experiments involving tubing cannot be applied to individual cells.
The invention of vessels, when one compares vessels with
tracheids in this way, was a good idea. The relative diameter
and abundance of vessels in a wood (ca. one-quarter of the
transectional wood surface of a woody angiosperm; Carlquist
1975, p. 206) can be varied, of course. More vessels means
more volume of water flow, and more imperforate tracheary
elements means more mechanical strength. There can be a
trade-off. To be sure, a number of woods with vessels also
have tracheids in them, and although a tracheid can be calculated to have more resistance to flow (Sperry et al. 2007)
than a vessel element, the addition of tracheids to vessels results in a net gain in conductive capability. It also results in
greater safety, because tracheids in a woods such as Myrica
or Eucalyptus are unlikely to embolize: their pit membranes
resist that, whereas embolisms can spread readily from one
vessel element to another.
5. The bordered pit: a structure with multiple
meanings
Wall strength vs. conduction
The bordered pit is a remarkable invention, common to all
groups of vascular plants, that balances conduction (a broad
pit membrane) against wall strength (the pit aperture is a minimal interruption in the wall, a fact involving the overarching
nature of the pit border). These features are summarized in
Fig. 8A. Bordered pits occur frequently on tangential walls of
ray cells (Carlquist 2007b), so the strength–conductivity tradeoffs of bordered pits are not limited to tracheary elements.
Pit membranes as passageways
In conifers, the bordered pit takes a circular shape, a fact
related to the torus–margo configuration. The closure (aspiration) of the pit can be accomplished by displacement of the
921
torus to one side or the other, but when conduction is active,
the pit membrane stays in a midway position. The displacement of the margo to achieve closure is permitted not only
by the margo threads, but also by the circular nature of the
pit aperture, which is smaller than the torus, but which
matches the pit aperture against which the torus becomes appressed by aspiration. The margo threads offer relatively
large passageways for water transfer (Pittermann et al. 2005).
The conifers (including Gnetales) and ginkgophytes were
greatly advantaged by this invention (Pittermann et al. 2005),
which was probably basic to the success and persistence of
the group (a plesiomorphy in the ginkgophyte–conifer lineage). Woody angiosperms, by contrast, did not invent a true
torus–margo system: margo threads in the conifer sense are
absent (for a review, see Rabaey et al. 2006).
Angiosperms very likely began with scalariform lateral
wall pitting of tracheids. Scalariform pitting is more abundant
in earlier-branching angiosperm clades and in metaxylem
(conifer tracheids do not have scalariform pitting). An unappreciated correlation is a mechanical one: with a circular
torus–margo system, strain is equal on all sides of the margo,
so that displacement of the torus is successful. If a scalariform pit were to have a torus–margo system, strain would be
greater in the center of the elliptical pit membrane, less at the
ends, so that closure of the elliptical pit aperture would not
be successful. Angiosperms, in essence, had to invent a series
of mechanisms that gave scalariform pits hydraulic capabilities equivalent to (or superior to or more flexible than) the
circular pits of conifers. It was the angiosperms, not the conifers (as suggested by Pittermann et al. 2005), that were the
underdogs in this competition. Life cycle brevity was the
overriding advantage that the angiosperms held. The great
evolutionary flexibility of angiosperm woods (Carlquist
2009b) also at some point permitted them to surpass conifers.
Pit membranes: flow and cavitation
Pores in pit membranes are small, much inferior to conifer
margo pores for flow, but with sufficient area; angiosperm
tracheary element pit membranes do have appreciable flow
capacity (Choat et al. 2003). Thinner pit membranes have
larger pores and thus are better at conducting, but offer more
vulnerability (Jansen et al. 2009). Tracheids with thinner pit
membranes and visible pores include Amborella and Drimys
and are figured by Hacke et al. (2007). This might represent
an early angiosperm condition.
When pressure inequality between two adjacent tracheary
elements occurs, some deflection of pits membranes may result, but probably not very much (Zwieniecki and Holbrook
2000). Greater deflection of pit membranes can result in creation of larger pores (Choat et al. 2004), but this risks irreversible change and would not aid recovery. Interestingly, pit
membranes of monocot tracheids are often quite porose
(when intact pit membranes are viewed; Carlquist 2012). A
fascinating possibility with regard to pores in pit membranes
was offered by Holbrook et al. (2002): “With increasing concentrations of ions, these [pit membrane] hydrogels are hypothesized to shrink, increasing the porosity of the pit
membrane and thus decreasing the resistance to water flow.
These changes are both reversible and repeatable, suggesting
that plants could actively modulate their xylem resistance by
altering the ionic concentration of the fluid in the xylem.”
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
922
Pit geometry and consequent meniscus formation (Fig. 8B)
may be important to reversal of tracheary element cavitation
(Holbrook and Zwieniecki 1999; Zwieniecki and Holbrook
2000). However, in deterring or reversing cavitations, a
whole-plant approach should be taken (Choat et al. 2008),
and even fibers and the strength that they exert relative to
vessels may be involved (Jacobsen et al. 2005).
Zimmermann (1983) conceived the idea of pores in pit
membranes as “designed leaks,” a mechanism that permits
entry of air that cavitates vessels. This may be true, but prevention of cavitation and prevention of membrane deformation may be the pervasive themes in angiosperms that need
further investigation.
Types of bordered pits and their significance
Viewed at a light microscope level, bordered pits are varied in shape and in degree of border width in angiosperm tracheids and ray cells. Are scalariform lateral wall pit
membranes in angiosperm vessels a plesiomorphic condition,
as Frost (1931) proposed? The presence of scalariform pitting
on end walls of Amborella tracheids (Fig. 11D) and, for that
matter, those of Nymphaeaceae and most monocots, could be
cited as possible evidence.
Why is there scalariform lateral wall pitting in vessels of
Vitis, whereas alternate pitting characterizes vessels of some
other Vitaceae? Scalariform pitting is common in vessels of
Magnoliaceae (Fig. 13D) and Piperaceae, as well as a number of Araliaceae (Rodriguez 1957). An equivalent type of
pitting, pseudoscalariform pitting (Carlquist 1988, 2001a),
has been derived phylogenetically from alternate pits by lateral widening — the tips of the pits do not coincide with vessel facets as they do in scalariform pits. Thus, there seems to
be some significance to laterally wider pits other than a mere
historical remnant of an ancient condition. Is there a trade-off
between extensive intervessel contact and wall strength? Certainly scalariform pitting is very common in angiosperm
metaxylem (Bierhorst and Zamora 1965), but a functional explanation should be sought, even though metaxylem could
still be expected, as Bailey (1944) suggested, to be a refuge
of antique wood characteristics.
Certainly, as Frost (1931) showed, alternate pitting is the
most common type in woody angiosperms. On a theoretical
basis, circular to polygonal alternate pits theoretically offer a
maximum strength configuration. There has been no experimental proof of this in plants, although engineering parallels
do exist. Opposite pitting is so similar to alternate pitting that
many students confuse the two types, and they are probably
closely comparable in adaptive terms. There seems to be little
loss in conductive ability by subdivision of elongate pits into
alternate or opposite pitting. One interesting example is furnished by the pitting of the tracheids of Tasmannia (Carlquist
1989b) and Zygogynum (Carlquist 1981a) of the Winteraceae. They often have scalariform pitting on end walls but alternate (albeit sparse) pitting on lateral walls. This suggests a
selective value of enhanced conduction for scalariform pitting
but a value in mechanical strength for alternate (and sparse)
circular pitting. Increase in wall thickening would provide
more mechanical strength, but it would require more photosynthate input and narrowing of the lumen, which would
lower conductive capacity.
Botany, Vol. 90, 2012
6. Polymorphism in conductive cells: a key to
angiosperm success and radiation
Trade-offs again
Virtually all angiosperms have the genetic information to
make bordered pits on lateral walls of vessels, tracheids,
fiber-tracheids, and ray cells. More importantly, the location
of bordered pits in wood can be governed very precisely.
Bordered pits are maximally conductive structures that lessen
wall strength appreciably, whereas simple pits are minimally
conductive structures that offer minimal lessening of wall
strength. Thus, a trade-off is in effect. Mechanical strength
can be enhanced by having narrower borders or no borders
on pits of imperforate tracheary elements. It can also be
achieved by having fewer pits, but a certain number of pits
is necessary for input of photosynthates during cell wall formation. Thus there is a gamut of possible cell types.
The tracheid as basic
We can assume that the basic conductive cell type of the
angiosperms was a tracheid with bordered pits: these pits are
scalariform when a wider element is formed, circular when a
narrower element is formed. Such tracheids can be seen in
the earliest extant angiosperms, Amborella and Nymphaeales.
The first dimorphism in angiosperm xylem, phylogenetically,
is the development of wide tracheids that have larger pores in
pit membranes of end walls. If the pit membranes of the end
walls are thin, they are swept away by the conductive stream
(perhaps with pit membrane remnants remaining), with a vessel element resulting. The other cells, in this dimorphism, are
tracheids, but tracheids that tend to be narrower and longer
(during early developmental stages, narrower cells have intrusive capacity) and with circular pits in which pit membranes
are retained. Tracheids of various specifications can be created, for example, thicker-walled tracheids. Lumen diameter
must be sufficient for water conduction. That is, the conductive capacity of the bordered pits, collectively, must be
matched by the conductive capacity of the cell lumen. By
greater length, fusiform cell shape, and thicker walls, tracheids form mechanically strong tissue that forms the ground tissue of woods in early angiosperms. Illicium represents such a
dimorphism.
Tracheids, fiber-tracheids, and libriform fibers
Tracheids represent greater pit membrane area (as represented by the wide pit borders, membranes sectioned away as
seen in Fig. 9A). Tracheids are viewed and defined as conductive cells (Carlquist 1988; Sano et al. 2011). Pits on tracheids are relatively densely placed (Fig. 9A). Fiber-tracheids
represent nonconductive imperforate tracheary elements in
which pit borders are still present (Fig. 9B). Selective pressure
to complete extinction of the pit border, like extinction of
other vestigial structures in plants and animals, is probably
minimal. Libriform fibers, the most common type of imperforate tracheary element in woody angiosperms, have simple
pits (Fig. 9C). Wall strength is minimally compromised, because in libriform fibers, the pit is a slit without a border. In
most imperforate tracheary elements, wall strength loss is
minimized by the fact that pit apertures are elliptical to fusiform (Figs. 9A–9C) and run parallel to the helical arrangement of cellulose microfibrils in cell walls.
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
Polymorphism within a single year’s wood
Growth rings are a good example of trade-offs: conductively
efficient cells in earlywood (fewer, wider vessels), conductively safer cells in latewood (narrower vessels). We must not
forget the background cell type in this trade-off. In a vesselbearing wood with tracheids (which presumably embolize
rarely), there may be no vessels at all in latewood: the ultimate
safety (Myrica). Narrower vessels in latewood may retain
water columns when earlywood vessels in the same growth
ring embolize (Hargrave et al. 1994). The terms “ring-porous”
and “diffuse-porous” do not delineate two distinct categories
but rather extremes in growth ring formations. There are
many types (Carlquist 1980, 1988, 2001a) that are not included in descriptions but that may key closely to the ecology
of a woody plant. Latewood vessel elements may be so narrow
that they have no perforation plates (yet have the same length
as vessel elements) and are thus “vascular tracheids” (e.g., Artemisia; Figs. 6C–6D). These may resist embolism formation
throughout the most stressful months of the year, thereby protecting the cambium.
Positioning polymorphisms
Positioning of vessels within wood in ways other than
growth rings is often seen. In fact, a monograph on nonrandom vessel positioning has been offered (Carlquist 2009a).
For example, sheathing of vessels in libriform fibers is a
common strategy of lianas (Obaton 1960) and is shown here
(Cayratia; Fig. 10A).
Vasicentric tracheids: tracheid dimorphism and fibertracheid dimorphism
Vasicentric tracheids are tracheids that co-occur with fibertracheids or libriform fibers in particular woods. When this
co-occurrence takes place, the tracheids are always adjacent
to vessels, whereas the mechanical elements (fiber-tracheids
or libriform fibers) are more distal. Vasicentric tracheids may
form massive sheaths of vessels, as in Eucalyptus or Quercus, or be only a few cells, as in Ceanothus (Figs. 6A, 6B)
or Hedera. Wood macerations are necessary to identify vasicentric tracheids in these latter cases. In Rosaceae, some species of Prunus have only tracheids, whereas in others,
libriform fibers are present, the latter presumably a dimorphism of tracheids (Carlquist 1988). Tracheids as a background cell type are a plesiomorphy in Rosaceae. Vasicentric
tracheids are common in Californian chaparral shrubs (Carlquist 1985a). There is presumably a gain in mechanical
strength in this dimorphism.
Zygophyllaceae (Larrea) have fiber-tracheids as a background cell type but also have vasicentric tracheids (Carlquist
1985a). The family Krameriaceae, a sister family of Zygophyllaceae (and sometimes merged with it), has only tracheids (Carlquist 2005). One can think of these wood types as
phylogenetic products of fiber-tracheid dimorphism.
Vasicentric tracheids are occasional in Lamiaceae (Rosmarinus) and Solanaceae (Lycium), and because libriform fibers
appear plesiomorphic in these families, vasicentric tracheids
may have arisen phylogenetically by extending the formation
of bordered pits (present, of course, in vessels) onto a scattering of imperforate cells.
923
Fibrous cell walls as investments: wood density
The walls of libriform fibers, fiber-tracheids, and tracheids
are sometimes thick and represent a considerable investment
of cellulose and other substances. This is mute testimony to
the strength function of imperforate tracheary elements. Fiber
walls are the chief mechanisms for dealing with the weight of
a plant and the stress produced by wind thrust and torque.
Imperforate tracheary elements may also resist negative tensions that would lead to implosion (Carlquist 1975; Jacobsen
et al. 2005). Vessel walls themselves have appreciable thickness that may represent, in part, a resistance to water column
tensions. The roles that wood density (largely a product of
wall thickness) play are currently being examined by various
workers.
Libriform fiber dimorphism
The work of Kribs (1937) assumes (if only by lack of comment) that there has been only one phylogenetic origin of axial parenchyma and that different rearrangements have
occurred. However, a second type of origin has occurred: fiber dimorphism. This was observed early in helianthoid Asteraceae such as Dubautia (Carlquist 1958, 1961; Carlquist
et al. 2003) and has been subsequently found in many Urticaceae (Bonsen and ter Welle 1984). Acer also has both living
(nucleated) fibers and nonliving (libriform) fibers.
Fibers as storage devices
Although the main storage tissue within wood is rays
(Sauter 1966a, 1966b), libriform fibers can store considerable
quantities of starch in some species (Fig. 9D). Extensive
starch storage in fibers seems related to more sudden flushes
of growth and flowering (as in Araliaceae), but detailed correlations and physiological studies have not yet been presented.
Vessel dimorphism
Lianas 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 more
numerous, wider vessels fewer, so vessel dimorphism, as in
growth rings, does not produce a “traditional” bimodal curve
(this would be true in growth rings as well). A bimodal distribution of size classes is not a necessary requisite for declaring vessel dimorphism to be present: the point is that a
wider range of vessel widths is available to the conductive
system, with the wider presumptively providing conductive
efficiency and the narrower providing conductive safety.
Ewers et al. (1991) showed that vessel diameters form curves
intermediate between typical normal and typical bimodal,
with narrower vessels somewhat more frequent than one
would expect.
Division of labor: a pervasive theme
All of the dimorphisms or polymorphisms cited above can
be said to exemplify division of labor. The term “trade-off” is
also applicable in many of these cases. The products show differentiation not merely in histology, but in function. Although
the co-occurrence of vessels and an imperforate tracheary element type (tracheids, fiber-tracheids, or libriform fibers), resulting in a vessel-bearing wood derived from an all-tracheid
wood is the dramatic division of labor often cited; other types
of division of labor are often evident. Axial parenchyma cells
Published by NRC Research Press
924
that bear crystals are often different, in a particular wood, from
those that do not contain crystals, and co-occur with them, indicating a division of labor. The amazingly polymorphic capabilities of wood cells of angiosperms are undoubtedly one key
to the evolutionary success of angiosperms.
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
7. Axial parenchyma: what does it do?
Finding patterns
Axial parenchyma is elusive to students — it is visible
clearly only in radial sections of wood where the direction of
the strands of cells contrasts with that of ray cells and its
functions have not been the subject of extensive research.
Thus, the evolutionary significance of these cells and how
they might figure phylogenetically has been neglected. Kribs
(1937) presented a number of topographic types of axial parenchyma, as seen in wood transections, but he did not correlate these types with any other wood anatomical phenomena
or offer any functional interpretations. He did attempt to line
up the types in putatively phylogenetic sequences, beginning
with diffuse (or absent) and proceeding with types in which
axial parenchyma cells (as seen in transections) aggregate
into tangential rows (diffuse-in-aggregates) or tangential
bands two or more cells thick (apotracheal banded). Likewise, progressive grouping around vessels (paratracheal) is
another trend. However, multiple types may be found in
such genera as Metrosideros (Meylan and Butterfield 1978)
or Corynocarpus (Carlquist and Miller 2001).
Finding functions
Axial parenchyma strands or bands intersect with rays and
touch rays and vessels, and these contacts create interlinkages between the vertical and radial parenchyma systems.
The interlinkages of the two systems seem phylogenetically
to change from smaller and more numerous to fewer and
more massive, but exceptions could be cited. Diffuse axial
parenchyma has a high correlation with tracheid occurrence,
and this and the abundance of paratracheal types (the most
common in woody angiosperms) suggest that there is a relationship to conduction. This makes sense, because some kind
of mediation between the cohesion–tension sequence initiated
by leaf transpiration and the water intake system of roots is
a presumptive physiological necessity. Sauter et al. (1973)
found sugar release into vessels at the beginning of the
growth season in the sugar maple (Acer), a way of osmotically “jump-starting” the conduction in vessels. Axial parenchyma cells and living fibers are vertically oriented living
systems that contain sugar or starch and that could accomplish this activity, together with carbohydrate storage in rays
(Sauter 1966a, 1966b). We do not know how widely applicable this phenomenon is and whether or not it occurs to
some degree in all angiosperms. We do know that the presence of starch in axial parenchyma is almost universally
seen, provided that woods are liquid-preserved (drying of
woods as in the preparation of xylarium samples, results in
loss of starch, so that the vital functioning of the axial parenchyma system goes unnoticed all too often). The occurrence of living fibers in angiosperm woods is thus
underreported.
Botany, Vol. 90, 2012
Reversing embolisms
Holbrook and Zwieniecki (1999) made a compelling case
for removal of embolisms by transfer of solutes into vessels
from axial parenchyma. They elaborate these ideas in terms
of ion concentration in a later paper (Holbrook et al. 2002).
Such activity would result in a kind of “stem pressure” that
would work similarly to root pressure. This hypothesis needs
further work. A hint at axial parenchyma as an agent controlling conduction is signaled by the existence of diffuse
parenchyma. If axial parenchyma were primarily a storage
tissue, dispersion of the cells (diffuse parenchyma) among
nonconductive (libriform) fibers would make no sense. However, diffuse parenchyma cells (or similar types) are related
to the occurrence of conductive tracheids in woods (Figs. 1E,
2F). At least a few diffuse parenchyma cells may be seen adjacent to vessels even in the other types. Thus all conducting
cells have close contact with living parenchyma cells when
viewed three-dimensionally. One is reminded of the occurrence, seen occasionally, of starch grains in companion cells
in phloem, adjacent to sieve tube elements, which are, of
course, 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 of
the angiosperm woods in which axial parenchyma is absent
or very sparse, e.g., Burseraceae, one finds that the imperforate tracheary elements are living fibers (for systematic occurrence of living fibers, see Carlquist 1988, 2001a). Wood
studies based on xylarium specimens cannot reveal this because drying of woods is often accompanied by decomposition of starch.
In vesselless angiosperms, there is another story. Axial parenchyma is scarce in some Winteraceae, somewhat more
common in some; it is also scarce in Amborellaceae
(Fig. 1A) and Trochodendraceae. One reason for the scarcity
may be that in these families, upright ray cells are common
and rays are close to each other (Fig. 1B), so upright ray
cells may serve as a kind of substitute for axial parenchyma.
Axial parenchyma, where present in Tetracentron and Trochodendron, is in latewood, which is compatible with the
idea of axial parenchyma as a stress-countering conductive
support cell type. Presumably, under this assumption, earlywood is not embolism-prone and functions under conditions
that are free from drought and frost (which would accord
with the ecology of these genera).
A bigger story?
In conifers, the margo–torus structure of pits may be so effective at minimizing cavitation that axial parenchyma becomes nearly irrelevant as a mechanism for “osmotically
guarding” tracheids. An interesting corollary of this possibility would be that development of relatively abundant axial
parenchyma (or living fibers) in vessel-bearing angiosperms
was a requisite of their coping with the cavitation risks that
vessels present when compared with an all-tracheid system.
Vessels that are prominently sheathed by axial parenchyma
(e.g., many Fabaceae) may similarly serve as photosynthate
storage related to flushes of growth and flowering, as well
as transfer of ions or sugars into vessels.
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
Other functions
Although axial parenchyma cells rarely have bordered pits
(which would indicate active flow), pits on end walls of a
strand are denser than on the lateral walls, according with
axial flow within the strand. Bordered pits may be seen in a
few cases (Fig. 11E). Pits on transverse walls of an axial parenchyma strand tend to be denser than those on the side
walls (Fig. 11F). Axial parenchyma is an ideal site for deposition of herbivore-deterrent substances such as silica, crystals, and terpenoids. Axial parenchyma, when strategically
placed, offers tissue that can yield to torsion, a feature especially important in lianas such as Cayratia (Fig. 10A) and
Operculina (Fig. 12B). Axial parenchyma is especially
prominent in the secondary xylem of some succulents such
as Crassula.
8. Rays: diversity in histology, diverse
functions
As seen in radial sections of wood, rays are composed of
upright cells and procumbent cells (Kribs 1935; Barghoorn
1940, 1941a). Procumbent cells are common in the centers
of rays (“isolation cells” of Braun 1970), whereas upright
cells (“contact cells”) are common in ray tips and sheathing
cells of the central portions of multiseriate rays. The proportion of each type varies with species and with ray ontogeny.
What is the function of the two ray cell types, and why do
their proportions vary?
Functions that interrelate
The simplest answer is that procumbent cells conduct photosynthates radially (Sauter 1966a, 1966b) and store photosynthates (Fig. 9E). Procumbent cells are horizontally
elongated. Most cells that conduct water or photosynthates
are elongated in the direction of conduction: fewer impedances (end walls) per unit length of a strand of conducting tissue (Sperry et al. 2005; Tyree and Ewers 1991). Not
surprisingly, the older the stem is, the more abundant are the
procumbent cells, presumably because there is a progressively greater volume of photosynthates to be conducted horizontally. Note also that rays may be living and functioning
for many years, so that the volume of living cells that stores
photosynthates gradually increases. Rays also widen during
enlargement of a stem, becoming more numerous cells wide
in the central portions (Barghoorn 1941a). The idea that
wood is a storage tissue may seem novel, but the ray and axial parenchyma cells in wood offer most of the storage tissue
in a woody plant, and starch can be observed in them, often
abundantly. Upright cells in rays conduct vertically and provide good linkage to axial parenchyma strands, thereby forming a network of living cells in wood that can conduct
photosynthates both vertically and horizontally.
Mechanical and conductive aspects combine
Although almost always overlooked in wood descriptions,
bordered pits occur on ray cells (Figs. 11A–11D). These are
especially common on tangential (periclinal) walls of procumbent ray cells (Carlquist 1988, 2007b; see also microcast
image in Fujii 1993, fig. 59). Bordered pits on these walls
are best observed in sectional view with light microscopy
(Fig. 11A) or SEM (Fig. 11B) or on tangential walls of ray
925
cells exposed by sectioning (Figs. 11C, 11D). They occur
(along with some simple pits) in about half of the woody angiosperms that I have examined, so this is not a rare phenomenon. The overarching of the pit membrane by wall material,
so that the size of the pit aperture minimally weakens the
wall strength while maintaining a broad pit membrane for
conduction, is basic to the strategy of the bordered pit. This
applies to the bordered pits of ray cells, as well as to the bordered pits of tracheary elements. Ray cells usually have secondary walls in woody angiosperms, and these walls are
moderately thick (very thin walls are much less likely to
have pit borders). The fact that woody plants expend photosynthates in forming lignified walls for ray cells shows that
an appreciable mechanical role (a fact not mentioned in textbooks) is played by ray cell walls: they contribute to the
strength of a woody stem. Ray cells may be thin-walled in
stems of lianas (where they offer flexible partitions between
the strands of fibrous tissue) or succulents (where they offer
water storage tissue).
Changing ontogenies, changing histology
One of the major events in the development of the
cambium of a woody plant is the horizontal subdivision of
ray initials, so that vertically shorter (but horizontally longer)
ray cells are produced. This may relate to the conductive nature of rays, as noted above. However, such subdivisions are
fewer in stems of secondarily woody plants such as rosette
trees (woody lobelioids, for example). In secondarily woody
plants, ray cells are predominantly upright. The fact that upright ray cells predominate in the rays of stems for the duration of secondary growth can be cited as evidence of
juvenilism, a departure from an herbaceous ancestry rather
than a strongly woody one. This condition characterizes lobelioids (Carlquist 1969) but also can be found in a diversity of
other families such as Empetraceae (Carlquist 1989a) and
Epacridaceae (Lens et al. 2003). Is the predominance of upright ray cells an indication of a balance tilted toward vertical
flow and away from horizontal flow in such species? That
would be a logical conclusion, related to the more limited
wood accumulation of secondarily woody species.
Raylessness
Only a few woody angiosperms form wood that lacks rays
(notable for this, Hebe; Meylan and Butterfield 1978). This is
best explained as an overriding selection for mechanical
strength. In fact, rays do eventually appear (Barghoorn
1941b) in stems of some species that are initially rayless (Artemisia, Cyrtandra, Plantago). In rayless woods, fusiform
cambial initials are very short, so that the length difference
between a potential fiber and a potential ray cell when derived from the cambium is minimal. Raylessness does not occur in plants with long fusiform cambial initials.
Other functions
Deposition of tannins, terpenoids, crystals, and silica in ray
cells probably deters chewing beetles and even mammalian
herbivores. Ray cells, along with axial parenchyma cells, can
serve in the regeneration of a cambium following damage to
a stem by drought, frost, or fire. Ray-to-vessel pits are usually larger than vessel-to-vessel pits. This may indicate, as
with axial parenchyma, an osmotic activity by the living
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
926
Botany, Vol. 90, 2012
cells, transferring ions or photosynthates into the hydrosystem and thereby preventing cavitations or refilling them (Holbrook and Zwieniecki 1999).
1987). When diagonal bands occur, the intervening plates
and strands of libriform fibers are consolidated into larger
groupings, with attendant mechanical consequences.
9. Collaborative cell type evolution: a
distinctive feature of angiosperm woods
Metaxylem — secondary xylem progressions
Metaxylem differs from secondary xylem in significant
ways. Metaxylem vessels are often narrower and associated
with parenchyma (often in radial bands between vessel
bands) instead of with mechanical cells. The onset of secondary growth usually features wider vessels, as well as mechanical cells (“fibers”).
In Convolvulaceae, the lianoid habit leads to shifts in histology as the stem grows (Carlquist and Hanson 1991). These
changes are dramatically shown in Operculina (Fig. 12B).
This may represent, first, some vessels to supply elongate
new shoots, then, mechanically stronger tissue to support a
young elongate stem, and finally, large vessels with great
conductive efficiency plus parenchyma patches to enhance
flexibility.
Division of labor: one kind of fusiform cambial initial
produces many different products
The invention of the vessel element marked not just a major division of labor creation for angiosperms, but the beginning of further modifications for both of the resulting cell
types. With vessel origin, there is a change in diameter and
cell length. Vessel elements within any given wood are wider
and shorter than the imperforate tracheary elements that they
accompany. Vessel elements do not elongate appreciably
compared with the fusiform cambial initial from which they
were derived, but imperforate tracheary elements, which are
able to undergo intrusive growth due to their slenderness,
do. There also tends to be a dimorphism between vessel elements and accompanying imperforate tracheary elements in
wall thickness. With the invention of vessel elements, there
is also a change to greater abundance of axial parenchyma,
which serves in regulating “stem pressure” and thereby maintaining water columns. Holbrook et al. (2002) showed that
living cells (axial parenchyma) mediate flow in the vessel elements and imperforate tracheary elements, which are dead
cells. The patterns of rays are indirectly affected by the
changes in axial parenchyma distribution. Vessel elements
frequently become distributed in nonrandom ways (Carlquist
2009a). Thus, the origin of vessels, seemingly a single
change, involves changes, directly or indirectly, in all wood
cell types.
Vessels distributed with relation to different tracheary
element types
Woods with tracheids as the background fibrous cell type
(Sorbus and most other Rosaceae), or with abundant vasicentric tracheids surrounding vessels (Quercus), have solitary
vessels. As the imperforate tracheary element type shifts to
fiber-tracheids or libriform fibers, grouping in vessels occurs
(Carlquist 1984). Tracheids are conductive imperforate tracheary elements (Carlquist 1985a; Sano et al. 2011) that
help to maintain the conductive pathways of vessels should
vessels embolize and are evidently superior as a device for
maintaining conductive pathways compared with grouping of
vessels. With the diminution or loss of borders on the imperforate tracheary elements, grouping of vessels becomes an effective way of maintaining the pathways: redundancy is
achieved, but also variation in diameter of vessels occurs,
with smaller vessels embolizing less readily (Hargrave et al.
1994). These groupings are often radial sequences, reminding
one of a “relay” in which newer vessels can take over as
older ones embolize and no longer are conductively active.
Extensive vessel groupings occur, often in diagonal patterns (Carlquist 1987) but sometimes in tangential patches.
The diagonal groupings, seen three-dimensionally, intersect
with each other, thereby potentially interconnecting all of the
vessels in the stem into a network. The diagonal bands are
not simply vessels, but are complexes that include vasicentric
tracheids and axial parenchyma cells as well (Carlquist
Cell types shift within growth rings
Growth rings are commonly thought to involve merely a
shift from wider vessels in earlywood to narrower ones in latewood. However, growth rings can involve shifts in vessel
abundance and vessel grouping (Ulmus). Placement of parenchyma may be involved: some growth rings end or begin
with parenchyma bands (marginal parenchyma). In some
plants that have tracheids as a background cell type, production of vessels may be discontinued in latewood (Bruniaceae,
Myricaceae; this feature is also common in Ephedra). Latewood vessels (not to be confused with vessel elements) are
typically shorter than earlywood vessels (Zimmermann and
Jeje 1981). For a more complete survey of growth ring phenomena, see chapter 2 in Carlquist (1988, 2001a).
Interactions and parenchyma types
Axial parenchyma and ray parenchyma are not independent of each other. The lack of axial parenchyma in Amborella (Figs. 1A, 1E) must be viewed conjunctively with the
abundance of rays and the abundance of upright cells in
those rays (Fig. 1B). “Diffuse” parenchyma, when viewed
three-dimensionally, forms a network, albeit one with
smaller and more numerous contact points that in woods
with massive axial parenchyma sheaths around vessels and
prominent rays, as in Fabaceae (Carlquist 1988, 2001a).
Diffuse-in-aggregates axial parenchyma forms tangential
bridges between rays (as does paratracheal banded axial parenchyma).
Living fibers versus parenchyma
Scarcity or absence of axial parenchyma is quite frequently
accompanied by conversion of the background tissue of a
wood into living fibers (some of which are septate, whereas
others are nucleate, a condition not observable in dried wood
samples).
Broader significance
The simultaneous evolutionary changes in several cell
types of a wood have an interesting implication: can true reversion occur? Reversion, of course, is defined at present in
terms of character states, not genomic changes. However
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
defined, it seems as though changes in several cell types conjunctively are not so much likely to be reversed as to progress toward new combinations and norms. This explains the
fact that not all clades have the same sequence of wood anatomical changes (see section 14) rather than inexorable gradations from plesiomorphic to apomorphic. A wood with
long scalariform perforation plates, long vessel elements,
solitary vessels, tracheids, and diffuse axial parenchyma (i.e.,
features found in Paracryphia, Escallonia, and Ilex among
the campanulids; Fig. 14) may change, phylogenetically, to a
wood such as that of Asteraceae, with vessel elements with
simple perforation plates, grouped vessels, libriform fibers,
and paratracheal axial parenchyma. But can such a sequence
run backwards? These cell type expressions are functionally
related to each other, and shifting the entirety of their adaptations backwards is unlikely. These characters are not genetically linked to each other, and synchronicity can dissolve. If
there were an inexorable progression of all characters together instead of some degree of independence, the Bailey–
Frost–Kribs trends would not have been evident, because
they saw that different clades tended in similar directions but
independently and with varied rates of evolution. The totality
of cell type expressions of wood of Asteraceae cannot change
back to the cell complexes of Ilex or Paracryphia. A few
quantitative changes in vessel diameter, vessel length, vessel
element length, and growth ring formation in a clade of Asteraceae could shift it from a conductively efficient wood to a
conductively safe wood. These quantitative changes are rapidly achieved, whereas the Bailey–Frost–Kribs trends are
slow-evolving features. We can consider heterochrony and
vessel changes related to ecology as overlays on the Bailey–
Frost–Kribs patterns, rather than as part of them.
10. Successive cambia and other cambial
variants: correcting misinterpretations,
finding significance
Why successive cambia matter
Although in terms of species, successive cambia are not
common in angiosperms at large, they are characteristic of a
number of plants, ranging from beets (Beta) to Bougainvillea
and including many shrubs of salty and desert areas (chenopods) and many succulents (Aizoaceae). Successive cambia
form a radical departure from the single-cambium system,
and because of that, they demand functional explanation. If
we cannot explain successive cambia, our explanations for
functioning of single-cambium stems are in doubt. In fact,
stems with successive cambia illuminate, by contrast, the
functioning of single-cambium stems.
First, let’s understand the phenomenon
Difficult to section (obscuring their developmental nature),
unsatisfactorily preserved when dried (as in wood collections — xylaria), and not studied because no commercial
timbers have successive cambium, this phenomenon has
been remarkably misunderstood.
After a series of studies on plants with successive cambia,
I produced a summary (Carlquist 2007a) and also an interpretive study of Caryophyllales (Carlquist 2010) in which the
majority of families and genera with successive cambia are located. From these studies, I was able to draw the conclusions
927
below. The first vascular cambium in a stem with successive
cambia is just an ordinary vascular cambium, producing secondary xylem inwardly and secondary phloem outwardly.
The master cambium
At a certain point, a new cambium-like layer appears in the
cortex. This layer is indicated by the pointers in the transection of a Stegnosperma stem in Fig. 11A. The master
cambium encircles the stem (or root) and is, like a vascular
cambium, functionally a single cell layer thick. It is not a
vascular cambium. Like a vascular cambium, it functions indefinitely. To the outside, the master cambium produces a
layer or two of secondary cortex cells. To the inside, it produces conjunctive tissue (usually a kind of parenchyma) and
then another vascular cambium. The initiation of each vascular cambium is signaled by anticlinal (radial) divisions, so
that the cambia initials are narrower tangentially than the
conjunctive tissue cells (or the master cambium cells). Then
it repeats this action indefinitely. Each of the vascular cambia
produces secondary phloem to the outside and secondary xylem to the inside, so a series of vascular cambia and their
products, separated from each other by conjunctive tissue, result. These are the “rings” of a beet.
Different, permanent, and nonseasonal
The master cambium is different from vascular cambia.
The vascular cambia in a plant such as Beta are perfectly normal vascular cambia. The cylinder around the stem or root
that acts as the master cambium is permanent and usually
continues for the life of the stem or root. Thus, there is only
a single master cambium at the periphery of a beet. The vascular cambia are produced without regard to season. In a
beet, one can see that numerous vascular cambia are produced per season.
In a beet, which grows actively for a single season, the
master cambia and the vascular cambia are active. In many
species with vascular cambia, the master cambium goes into
dormancy until the time for initiation of a new vascular
cambium comes, in which case active periclinal (tangential)
divisions can be seen. How much secondary xylem does
each of the vascular cambia produce? The amount is probably limited by spatial considerations: the more numerous
the vascular cambia, the less secondary xylem each produces.
However, the amount of secondary phloem is not so limited,
because secondary phloem produced by each vascular
cambium collapses with age, so that more secondary phloem
can be accommodated. Vascular rays (sometimes termed “radial 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, can
often be found adjacent to the vessels.
Conductive longevity
If new secondary phloem is continually produced by each
of the vascular cambia in a stem, surely that new phloem is
active in photosynthate conduction. The vessels in species
with successive cambia are probably functional in vascular
increments that continue to produce secondary phloem.
Comparisons
Those who try to think of the master cambium as a kind of
Published by NRC Research Press
928
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
vascular cambium will be making a mistake. The parallel is
with a monocot cambium, found in genera such as Dracaena
and Yucca. The monocot cambium is like the master
cambium in that it produces secondary cortex outwardly. Inwardly, the monocot cambium produces cells that mature into
parenchyma, as well as strands of procambium, each of
which matures into a bundle containing xylem and phloem.
No vascular cambial activity is present in monocots (Carlquist 2012). The monocot cambium and its products have
been generally interpreted correctly, perhaps because there is
no cambial activity in the secondary bundles. The monocot
cambium (“secondary thickening meristem”) is the only lateral meristem in monocots with secondary bundles.
Functional value of successive cambia
The occurrence of successive cambia in a number of families (Carlquist 2001a, 2007a) is testimony to the validity of
this type of structure. If one looks at the nature of the plants
with this structural scheme, one finds the following.
a. Wide vessels maximize conduction. Examples are too numerous to cite here but include such well-known examples as Bougainvillea as compared with nonlianoid
Nyctaginaceae. In conifers, one notes that the two tree
species of Gnetum have virtually no successive cambial
activity, whereas the approximately 30 lianoid species of
Gnetum have wider vessels than the tree species. All of
the lianoid species have prominent successive cambial activity. The flexibility provided by the increased abundance of parenchyma (mostly that of conjunctive tissue)
and the spatial separation of vascular increments into concentric cylinders separated by parenchyma are ideal for
the “cable construction” modes of lianas (Pfeiffer 1926;
Obaton 1960; Carlquist 1985b).
b. Storage. Storage of sugar by Beta is obvious from its domestication. Water storage (often concurrent with photosynthate storage) is evident in roots of Agdestis and
Basellaceae and, to some extent, stems and roots of Aizoaceae (tuberous roots of Trichodiadema).
c. Salt sequestration. Amaranthaceae (amaranths, chenopods)
are especially common in highly saline areas, and high
salt concentrations can be found in roots, stems, and leaf
parenchyma of this family (Atriplex, Salicornia, and Tetragonia), permitting them to thrive in osmotically challenging situations (Khan et al. 2000). Salt sequestration is
claimed for Avicennia (Robert et al. 2011). Other probable
instances may occur in Aizoaceae (Carpobrotus) and Nyctaginaceae (Abronia).
d. Three-dimensionalization and longevity of vascular tissues.
Successive cambia provide inner, as well as outer, portions
of the stem with active phloem cells. Thereby, a much
greater volume of a stem (or root) can be used for storage
and retrieval over a longer period of time, and the distribution of conductive within storage tissue is ideal.
Other cambial variants
Interxylary 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 distinguished
from successive cambia because the pairing of phloem
strands or bands with vessels (“vascular increments”) found
Botany, Vol. 90, 2012
in successive cambia is absent with interxylary phloem
(Fig. 10B), in which vessels do not contact the phloem
strands. Thus, even the most cursory examination of sections
can permit differentiation between interxylary phloem (from
a single cambium) and successive cambia: ontogenetic studies are not needed to establish the condition.
11. Heterochrony I: a road map to juvenilism,
paedomorphosis, and secondary woodiness
Pre- and post-molecular concepts
For most of the twentieth century, the concept that woody
forms (especially the “woody Ranales”) were ancestral in angiosperms was prevalent. The revelations of molecular phylogeny (Chase et al. 1993) revealed a more complex
situation, but premolecular thinking tended to hold that
woodiness was ancestral within angiosperms, herbaceousness
secondary, and that this was accompanied by a radiation from
tropical into temperate zones. Studies of evolution of wood
characters (Bailey and Tupper 1918; Frost 1930a, 1930b,
1931; Kribs 1935, 1937) did not even include less woody
species, and the implied assumption was that minimally or
less woody angiosperms had wood essentially like that of
more woody species, just less of it. The idea that there could
be secondary woodiness (particularly visible in island floras)
and that anatomical features could pinpoint such instances
had to wait until my 1962 paper (Carlquist 1962). Although
the ideas in that paper were soon accepted, the obvious corollary idea was left unexplored for many years: how prevalent was secondary woodiness in angiosperms, what kinds of
juvenilism in wood were there, and can one see shifts towards (or away from) woodiness? I attempted answers in a
recent paper (Carlquist 2009b) by using the premise that the
hypotheses should be consonant with more recent global molecular trees of angiosperms (e.g., Soltis et al. 2000; Angiosperm Phylogeny Group (APG) 2009).
Types of juvenilism
The 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 is
concerned, this logically could include monocots, which
have no secondary growth (but have protoxylem and metaxylem), as permanently juvenile. And I believe that monocots
should be so considered (Carlquist 2012). Monocots that
have little or no metaxylem, and only protoxylem, could be
considered the logical extreme in this series (e.g., Elodea). I
took the position that within nonmonocot angiosperms, there
could be degrees of juvenilism from very little secondary
growth (Saururaceae) to rapid accumulation of large quantities of wood (most well-known trees) and that there could be
shifts in both directions within particular clades (Carlquist
2009b). This section deals with woodiness that shows juvenile features protracted to various extents into secondary xylem. Section 12 deals with angiosperms in which ontogenetic
change to “adult” (“typically woody”) wood features is rapid
and in which development of flowers (sexual maturity) is delayed (not infrequently for years, as in numerous trees).
Criteria for paedomorphosis or protracted juvenilism
One can readily understand the strategy of a nonmonocot
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
929
flowering with the development of a minimal amount of secondary xylem: a plant can succeed reproductively while
drawing on a relatively ephemeral water source. Monocots,
which have other strategies (Carlquist 2012) are not considered here. However, in the secondary xylem of woods with
paedomorphosis, one can find some indicators, but the phylogenetic shifting nature of heterochrony is evident in such
groups (Lens et al. 2012).
ondary xylem with little change, or with delayed changes.
These are signals of protracted juvenilism. Piperaceae, which
have scalariform lateral wall pitting in metaxylem and then
indefinitely thereafter, may be an example of this.
h. The above characteristics are not always found together in
a paedomorphic species and very likely have multiple genetic causes and multiple phylogenetic origins.
a. Once a cambium is formed in a plant, subdivisions leading
to vertically shorter cambial initials usually are formed
(Cumbie 1969). Such subdivisions are fewer in plants with
paedomorphic xylem. The fusiform cambial initials thus
stay longer, although they do decrease in length as secondary growth proceeds.
b. Horizontal subdivision occurs in ray initials at a slower pace
also. Thus, ray cells are relatively vertically longer in rays
of species with paedomorphosis (Figs. 13A, 13B). Such
ray cells are seen not just in woody lobelioids and rosettetree composites, but also in a wide range of woods that
are suspiciously plesiomorphic: Amborellaceae, Austrobaileyaceae, and Chloranthaceae, for example.
c. Intrusive growth is characteristic of derivatives of slender
fusiform cambial initials. Those destined to be imperforate
tracheary elements (“fibers”) are more capable of intrusive
growth; those destined to become vessels are not so intrusive, because their greater width retards intrusiveness.
This process takes place more slowly, and thus to a lesser
degree, in woods with paedomorphosis than in “typically
woody” species. Thus, fusiform cambial initials in juvenilistic woods tend to decrease in length over time or
stay the same (the latter is especially true in storied
woods). Examples can be found in rosette trees and in
globular cacti (Carlquist 1975, pp. 218–219).
d. Wide primary rays are characteristic of a number of less
woody eudicots. A vascular cambium can add to such
rays, but instead of subdividing them actively into a
complex of smaller rays (e.g., Barghoorn 1941a), they
may change little over time. Subdivision of rays typically occurs through intrusive growth of fusiform cambial initials, and this occurs slowly or not at all in
paedomorphic woods.
e. In some woody angiosperms, rays are narrower at first,
mostly uniseriate, with the multiseriate portion of rays
only one or two cells wide. Although in “typically
woody” species (e.g., Bursera simaruba), rays tend to
widen rapidly; some woody species tend to retain narrower rays for a longer period of time (Empetraceae).
Epacridaceae could be said to exemplify lack of ontogenetic change in both narrow and wide rays, whereas
“typically woody” Ericaceae (into which Epacridaceae
can be placed) develop “adult” ray systems rapidly.
f. In a species with short fusiform cambial initials, absence of
horizontal subdivision in ray initials may result in ray cells
about the same vertical length as libriform fibers. If the
“potential ray cells” become intrusive and thereby are fusiform in shape, they have all of the characteristics of fibers,
and thus a rayless wood results (Hebe, insular species of
Plantago). Ray formation may eventually occur in a rayless
species depending on how prolonged the juvenility of the
wood is in a paedomorphic species (Barghoorn 1941b).
g. Metaxylem pitting patterns of vessels may continue into sec-
Causes of protracted juvenilism
Shorter life cycles usually correlate with shortages in water
or extremes in moisture availability or by annual occurrence of
freezing. Although there are various other ways of countering
these conditions, the short life cycle is certainly one. When a
plant with a short life cycle enters a new habitat where milder
conditions prevail, prolonging the vegetative body of the plant
becomes a positive selective value (stem tissue can be retained
rather 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 conditions
favoring secondary woodiness. Long-distance dispersal of a
plant adapted to highly seasonal climate to an oceanic island
where the flora is unsaturated and where milder climatic
conditions prevail results in selection for prolonged vegetative growth. Not all areas of oceanic islands provide these
conditions, but secondary woodiness is common in lower to
mid elevations of the Canary Islands and mid to subalpine
elevations of the Hawaiian Islands. Oceanic islands tend to
have broad zones of moderated climate. Frost is minimized
at subalpine elevations because of the temperature-insulating
effect of broad areas of ocean. Evaporation is thereby lowered, and increased rainfall may be present (depending on
the geographical location of the island).
b. Mid elevations of mountains in the central Andes or of the
east African volcanoes offer climatic moderation similar to
oceanic islands. These “sky islands” also tend to be geologically less stable, thereby offering large tracts of recently
disturbed rock and soil. These floras therefore tend to be
unsaturated, like those of oceanic islands. Because they
are temperate areas surrounded by tropical lowland forest
that lacks adaptation to cold, “sky islands” acquire a large
number of immigrant species via long-distance dispersal
from temperate areas such as oceanic islands.
c. Continental islands, as in islands with volcanic activity and
recent glaciation such as New Zealand, may offer niches
suitable for colonization by long-distance dispersal, as
shown by woodiness in such genera as Olearia.
d. Coastal Mediterranean-type continental areas offer niches
for secondary woodiness (e.g., shrubby Lamiaceae in
coastal southern California and along some Mediterranean coasts).
e. In many instances, less woody (“herbaceous” to various extents) species have excellent capabilities for long-distance
dispersal and thus reach islands and island-like areas preferentially. As a generalization, forest trees have larger and
less dispersible seeds.
f. If one looks at growth forms native to islands and islandlike areas (Canary Islands; Carlquist 1974), one finds
such floras relatively poor in annuals, but relatively rich
in species woody to various degrees. These growth-form
spectra represent selective ecological regimens to which
recently arrived species are likely to respond.
Published by NRC Research Press
930
12. Heterochrony II: rapid ontogenetic
change to adult wood patterns
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
The opposite of paedomorphosis
Accelerated adulthood may be considered the opposite of
paedomorphosis, or protracted vegetative juvenilism. We
have not noticed this phenomenon because it is the wellknown norm in “typically woody” plants, but to understand
wood evolution, we have to understand all expressions of it.
In fact, early woody angiosperms were most likely paedomorphic (Carlquist 2009b). Characteristics of “typically woody”
angiosperm woods are cited below.
a. Fusiform cambial initials actively subdivide so as to shorten
soon after the onset of secondary growth.
b. Ray initials actively subdivide so as to provide vertically
shorter ray cells. The ray initials also soon begin to divide tangentially at relatively infrequent intervals in the
central portions of rays, so that radially elongated ray
cells are produced.
c. Fusiform cambial initial derivatives rapidly become intrusive, thereby resulting in vertically longer derivatives.
Thus, the “fibrous” wood cells (imperforate tracheary elements) can become much longer than the vessel elements.
d. Ontogenetic changes in ray histology take place rapidly after
the onset of secondary growth: wide “herbaceous” rays are
subdivided by intrusion of fusiform cambial initials, and
narrow rays widen by vertical radial divisions of cambial initials (Barghoorn 1941a). “Adult” ray configuration is
thereby rapidly achieved.
e. Accelerated adulthood, once thought to have been universally primitive in angiosperm groups, may have been derived as a homoplasy from less woody ancestors on a
number of occasions, and woods with little secondary xylem and with protracted juvenilism may have been derived from woody ancestors. Woody ancestors may have
given rise to less woody ones in a number of clades
(e.g., Dipsacaceae, some Caprifoliaceae, Adoxa, Apiaceae, Asteraceae, and Eremosyne in Fig. 14). Angiosperms are unique in being able to shift between more
adult and more juvenilistic expressions readily in some
clades (Carlquist 2009b). Conifers, which are a good example of accelerated adulthood, seem to be incapable of
juvenilism in the angiosperm senses of the word, and all
have “adult” wood. An exception, so minor that it proves
the rule, can be found in New Zealand conifers that produce juvenile (“heteroblastic”) foliage (Rumball 1963).
f. If scalariform perforation plates occur in primary xylem,
there is a rapid shift to simple perforation plates in secondary xylem. This is shown here for Brassaia
(Fig. 13C), Eucommia (Fig. 13E), and Kadsura
(Fig. 13F) and has been reported for Crossosoma (Carlquist 2007c). If a woody species characteristically has
scalariform perforation plates in secondary xylem such
as Magnolia (Fig. 13D), there are more numerous bars
per perforation plate in metaxylem. Bailey (1944) and
Bierhorst and Zamora (1965) noted these tendencies for
a more “primitive” perforation plate type to be present
earlier in ontogeny and thus thought of primary xylem
as a “refuge” for ancestral features. Bierhorst and Zamora (1965) found that narrower vessels are more likely
to have scalariform perforation plates.
Botany, Vol. 90, 2012
g. “Adult” wood features as a complex, described above, may
all be present in a particular wood, or only some of them
may be. For example, abundance of upright ray cells can
be found in some woody groups (e.g., Epacridaceae, Winteraceae, Chloranthaceae). Epacridaceae also have rays
that seem “less adult” (section 11). However, the characteristics of the tracheary elements in Epacridaceae seem
typical 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 typical of nonjuvenilistic plants and animals: delay of sexual
maturity. The onset of flowering (sexual maturity) is delayed in woody angiosperms, often for several years, just
as it is in conifers.
The value of accelerated development of adult wood
patterns
The idea of looking at woody plants after considering juvenilistic ones may seem ironic (we often think of woody
plants as the “norm”), but the sequence is intentional to
present woodiness in contrast to nonwoody or less woody
conditions in angiosperms. Accelerated change in the
cambium and its products, producing adult wood rapidly, is
associated with a series of characteristics. The early angiosperms may have been only moderately woody, as reflected
in the present-day wood of Amborellaceae, Chloranthaceae,
Illiciaceae, and others.
a. Development of more numerous procumbent cells in rays
correlates with larger plant size. Procumbent wood cells
are active in translocating photosynthates to and from
storage sites within the wood. The larger the stem diameter, the more radial photosynthate activity is likely to
occur, and therefore, the greater the abundance of procumbent cells.
b. Development of more intrusive growth in derivatives of fusiform cambial initials correlates with greater mechanical
strength, which in turn permits taller growth forms. Ratios
between imperforate tracheary element lengths and vessel
element length (“F/V” ratios) are relatively high in “truly
woody” species (1.5 to 4.0 most commonly; Bailey and
Tupper 1918). Ratios are lower in woods of basal angiosperms such as Chloranthaceae and Illiciaceae, as well as in
species with secondary woodiness mentioned in section 11.
Taller trees tend to have libriform fibers, whereas woods
with tracheids in addition to vessels (e.g., Sorbus) are often
medium-sized. Libriform fibers usually represent the strongest of the imperforate tracheary elements, although wall
thickness rather than pitting type is an important criterion.
c. The selective value of a rapid shift from scalariform to simple perforation plates (or a shift from longer scalariform
plates to plates with fewer bars) is probably less about
maintenance of the ancient condition in primary xylem
than production of conductively more efficient vessels in
secondary xylem. Woody species tend to occur in sunny
areas or reach canopy status more rapidly than less woody
early angiosperms, so less impedance in perforation plates
makes sense. This is clearly demonstrated in lianoid genera
such as Kadsura of the Schisandraceae (Fig. 13F) or Tetracera of the Dilleniaceae.
d. The size of trees and shrubs is roughly proportional to their
water supply on an annual and a seasonal basis. More
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
“adult” wood is therefore to be expected in woodier species
of more mesic habitats. Competing in these habitats requires considerable investment of photosynthates into mechanically 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 reinforce the arboreal syndrome where water permits.
e. A shortcut to the canopy habit is found in lianas. Lianas
show accelerated change to adult ray conditions (Carlquist 2009b), and this is often accompanied by shortening in fusiform cambial initials as well. Mechanically
strong imperforate tracheary elements are not of high value in lianas (although ones that sheathe vessels are advantageous). Lianas often have wide rays, extensions of
the wide primary rays: these are of value in torque-prone
stems. The lianoid habit appears to have been a shortcut
for a number of basal angiosperms (Piptocalyx of Trimeniaceae, Schisandra, Austrobaileya, and some species of
Piper). The shift to lianoid habit is accompanied by accelerated acquisition of some adult features.
13. Ecological stasis and iteration: stability
and breakouts in wood evolution
Campanulidae as an example
If we look at a phylogenetic tree of Campanulidae
(Fig. 14), we see a number of fascinating revelations about
wood anatomy, provided that we know relevant data sets.
One data set that seems obvious has been added to the Tank
and Donoghue (2010) tree: species numbers. However, species numbers are only an indirect indication of change in
habitat-occupancy capabilities within a clade. Even without
detailed knowledge of the habitats of the various campanulid
families and genera, one can see that the short early branchings of the Tank and Donoghue tree are associated with
small species per family numbers, and these short branches
have a very high degree of correlation with scalariform perforation plates (indicated by the curving line superimposed on
the tree in Fig. 14).
Unbroken histories of mesic occupancy
Some 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, Rousseaceae, Argophyllaceae, Bruniaceae, Columelliaceae, Griseliniaceae, and Paracryphiaceae can be cited as examples. The
evidence is not merely in retention of scalariform perforation
plates in all of these families. They also all have tracheids as
the imperforate tracheary element type, mostly diffuse parenchyma, and heterocellular (heterogeneous) rays. They exhibit
no juvenilistic features that suggest phylesis toward or away
from herbaceousness. And today, they all occur in mesic habitats. The hypothesis consonant with all available information
about these families is that they have had unbroken histories
in mesic habitats. Any departures have been relatively minor,
as in the case of Bruniaceae, which show xeromorphy in
growth form (shrubs of variously limited size) and in foliar
characteristics.
The obvious conclusion is that wood anatomy is entirely
congruent with habitat, when we take into account probable
931
occupancy history, wood physiology, foliar apparatus, habit,
the nature of microclimates, and how plants occur in the
field. Ecological stasis and ecological iteration are fully validated when one combines this information with information
on 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. There
are few opportunities for radiation within such habitats, and
they tend to be floristically saturated with species. Such habitats are rich in species with unbroken occupancy of such
habitats, if one can judge by their retention of woods with
high safety characteristics and low vulnerability. These
groups include Paracryphiaceae, Escalloniaceae, Bruniaceae,
and many of the Aquifoliales. Some of their adaptations that
probably account for the success of these groups are striking.
Bruniaceae, for example, are microphyllous shrubs, most of
which grow on south-facing slopes (= the cooler, moister
slopes in the Southern Hemisphere) and on cool mountaintops. Aquifoliaceae may owe speciation in part to good dispersal (Ilex occurs on Hawaii, Tahiti, the Bonin Islands, and
on several Atlantic Islands). Many Aquifoliaceae are able to
withstand frost, and some have drought-resistant leaves. Ilex
has short vessels (Zimmermann and Jeje 1981), which give
its wood conductive safety.
The least speciose of the early branches (short-branch)
families of Campanulidae have extraordinarily narrow ecological adaptations. Paracryphia has a single species, confined to the highest and wettest mountains (also geologically
old) of New Caledonia. Not surprisingly, it has a wood rich
in features symplesiomorphic for woody angiosperms
(Fig. 4F). The only species of Pittosporaceae with scalariform
perforation 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 Asterales, have few genera per family and few species per family.
Moderate departures
Among the campanulid families, Araliaceae have moderate
degrees of departure from the mesomorphic symplesiomorphic wood plans of early woody angiosperms. Araliads have
scalariform and simple perforations plates (sometimes both in
a single wood), with simple perforation plates tending to
characterize genera in seasonal habitats where frost occurs
(Aralia, Hedera, and Kalopanax). Scalariform lateral wall
pitting also characterizes some genera: the functional value
of this seemingly symplesiomorphic feature needs further
study. However, one notes that Araliaceae have living fibers
in the wood in which starch is stored and retrieved, and vessels can be ray-adjacent in some Araliaceae. Storage of starch
in libriform fibers may relate to the “flushes” of sudden foliation and flowering in many Araliaceae. Araliaceae clearly
furnish examples inviting ecological interpretation.
Ecological breakouts
Branches of the campanulid tree that have simple perforation plates can be considered breakouts, as indicated in species numbers but, more importantly, in a shift to a diversity of
ecological sites, including some that offer extreme conditions
Published by NRC Research Press
932
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
(such as nightly freezing: the Asteraceae Stoebe on Mt. Kilimanjaro and Loricaria in the Andean superpáramo). Asteraceae can also enter warm, moist lowland sites if they are
not saturated (oceanic islands). Asteraceae represent the
most explosive (and recent) speciation in woody angiosperms (Funk et al. 2009) but certainly also the most diverse family of all angiosperms with regard to ecology
(Carlquist 1966). Xylem configuration correlates with this
(see section 3).
Vessel changes and ecological breakouts
Ecological breakouts are accompanied by changes in vessel
element size and not always vessel widening. Woods of Asteraceae show that desert Asteraceae, which are probably
mostly recent in their occupancy of xeric sites, have narrower
and shorter vessel elements, a configuration that features
safety over conductive efficiency. The ability to shift vessel
dimensions radically is one of the reasons for success of Asteraceae (see section 3). The ancestors of the family probably
lost scalariform perforation plates (there are none even in the
primary xylem). The same nearly holds true for Apiaceae:
Solereder (1906) listed a few exceptions, which, considering
the size of Apiaceae, prove the rule. In such families, can
scalariform perforation plates be regained phylogenetically?
Has the genetic information for them been lost, or have genes
just been silenced? In lianoid Dilleniaceae, simple perforation
plates are present, although scalariform ones are present elsewhere in the family. If selection favors conductive efficiency,
clearly the scalariform condition can be lost readily.
The answer concerning reversibility of the scalariform perforation plate appears to be a functional one: Whatever the
value of the scalariform perforation plate in earlier angiosperms as a mechanism for promoting conductive safety, that
value has been replaced in most clades by a multiplicity of
other features that prevent embolism formation or permit vessel refilling, mechanisms such as those discussed by Holbrook and Zwieniecki (1999). The presence of odd,
malformed perforation plates in certain Asteraceae (Carlquist
1960) can be taken as evidence that genetic information for
the plates is so modified that even if a less conductive vessel
element end wall has some value, its conformation is disorganized. Such plates in Asteraceae are very rare, in any case,
and alter the conductive characteristics so little that by frequency alone, they are not true reversions. Production of scalariform perforation plates along with simple ones side by
side within a wood can be found in a number of genera such
as Nothofagus (Meylan and Butterfield 1978). This illustrates
that “extinction” of an apparently plesiomorphic feature is
gradual, rather than abrupt, and may relate to developmental
factors. Clearly, the present-or-absent coding of wood characters for cladistic purposes is fraught with difficulty (Carlquist
2010).
Radical ecological breakouts and diverse occupancy
histories can occur in basal clades: Papaveraceae
Ranunculales is the sister order to the remaining eudicots
(Chase et al. 1993; Soltis et al. 2000, 2011). The basal-most
family of the order, the monogeneric Eupteleaceae, has long
scalariform perforation plates that even retain pit membrane
remnants (Carlquist 1992). The next branch of the clade is
Papaveraceae, and the branch after that is Lardizabalaceae.
Botany, Vol. 90, 2012
The shrubby genus of Lardizabalaceae (Decaisnea) has scalariform perforation plates, although other Lardizabalaceae
are lianoid and have only vestiges of the scalariform plate
condition. One might expect that Papaveraceae, departing
from the Ranunculales clade after Euptelea but before Lardizabalaceae, would have some retention of scalariform perforation plates. A survey of the family (Carlquist and Zona
1988) revealed no such perforation plates. I conveyed this information to Joachim W. Kadereit, who had studied the phylogeny of Papaveraceae. He suggested that I should look at
the genus Pteridophyllum, which he considered the basalmost genus of Papaveraceae, and he sent me some liquidpreserved material. Perhaps the primary xylem would retain
scalariform perforation plates, in accord with Bailey’s
(1944) refuge idea? In fact, careful study of Pteridophyllum
revealed that both primary and secondary xylem contain
only simple perforation plates.
The explanation for this seeming exception to phylogenetic
trends probably lies in ecological occupancy theory. Papaveraceae in this scenario adapted early in their radiation to
highly seasonal conditions that favored conductive efficiency
(simple perforation plates) over conductive safety, with other
means existing for conductive safety within the family. Papaveraceae, as a whole, may be secondarily woody (Carlquist
and Zona 1988). Dendromecon and Romneya are shrubs
with multiple stems and occur in coastal and insular southern
California. Bocconia occurs in the central Andean cloud forest. In these areas, Papaveraceae often occur in disturbed
habitats such as slides or burns. Other less woody genera occur in zones of climatic moderation, whereas most species
are annuals or biennials. We can hypothesize that Papaveraceae have had an unbroken history of occupancy of seasonal
sites, with minor secondary forays into areas where secondary woodiness has been possible, areas with relatively unsaturated floras. At the very least, any early steps from
mesomorphy to xeromorphy in Papaveraceae have not survived.
In the campanulid clade (Fig. 14), Eremosyne represents a
spectacular “breakout” from woody Escalloniales: it has little
if any secondary xylem and simple perforation plates. Breakouts like this can occur anywhere in a clade, either in basal
groups such as Eascalloniales or in crown groups such as Asterales.
14. Phylogenetic principles of wood anatomy:
what DNA-based trees do and do not tell us
The value of global molecular trees to comparative wood
anatomy
In earlier years, studies in comparative wood anatomy required that one select families for comparison with the one
under study. One had to rely on the natural systems then
available. Unfortunately, those trees, compiled by intuitive
conclusions based on collection of data, were not reliable.
The case of the sister families Asteropeiaceae and Physenaceae is an interesting instance. These Madagascar families
were of uncertain position. The wood studies of Dickison
and Miller (1993) compared these two families in tabular
form with no fewer than 12 families (none of which later
proved to be a member of the order Caryophyllales) in which
Asteropeiaceae and Physenaceae are located according to
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
molecular-based phylogenies (e.g., Soltis et al. 2000). The
number of potential families for wood comparisons is so
great that this situation happened routinely during the premolecular era. The lesson is not that wood anatomists were
wrong, rather that the natural systems on which they relied
were faulty. By being unable to compare wood of one family
with that of families highly likely, on a DNA basis, to be
closely 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 often
quite different (e.g., Caricaceae compared with Tropaeolaceae; Tamaricaceae compared with Frankeniaceae). The appreciation of this has been slow, because the idea that wood
anatomy must be an indicator of relationship persists and
with some reason (e.g., the presence of vestured pits in vessels is common to all families of Myrtales). However, the
role of shifts in habit and ecology on wood evolution and
the fact that some groups represented rapid change in wood
anatomy, whereas others remained stable for long periods,
went unappreciated. In short, we lacked a framework that
could guide our interpretations of wood evolution.
Caution in use of molecular trees
Molecular trees, becoming ever more precise as more
genes are sequenced (e.g., Soltis et al. 2011), are based on
genes that do not code for wood anatomical features. Molecular trees have to be based on gene sites with a rate of substitution suitable for large-scale comparison to recover
relationships (e.g., Fig. 14). Wood features evolve at diverse
rates, different from the genes used in molecular tree construction. Some wood features represent infrequent inventions
(vestured pits, tile cells, etc.), and some represent much more
common homoplasious innovations. Some wood features
have evolved slowly, and some have evolved more rapidly.
Intervention of heterochrony during the evolution of a clade
has produced some surprising results. Wood anatomy must
not be studied as a historical archive, even though it does
contain much evidence of evolutionary change. Molecular
trees can be used as a basis for showing progression of a
character (e.g., scalariform perforation plates in Fig. 14).
However, the fact that molecular trees are not constructed using gene site substitutions related to wood anatomy means
that we cannot read out “reversion” of characters (as done
by, for example, Baas and Wheeler 1996). Rather, genomic
change in woods is likely progressive, and reversion of genes
to earlier states is not a likely scenario. For example, secondary vessellessness in Winteraceae and Trochodendraceae
does not rely on restoration of genetic states of ancient stem
angiosperms. Rather, it probably results from simple modifications that result in nonhydrolysis of pit membranes in end
walls. Transitional stages such as seen in Aextoxicon (Fig. 2),
Carpodetus (Figs. 3A, 3B), Illicium (Fig. 3B), and Sarraceniaceae (Fig. 5), among others, could shift to either more hydrolysis of pit membranes or less hydrolysis. The alteration
of the degree of hydrolysis, probably controlled by modifying
genes, should not be considered a character state reversion,
but rather a shift in a developmental process.
The search for plesiomorphy
I.W. Bailey was somewhat disingenuous when he said that
his “major trends of xylem evolution” were developed inde-
933
pendently of natural systems of classification. In fact, several
of these systems featured the “woody Ranales” (= woody
basal angiosperms of APG (2009)) as a source group from
which major groupings of angiosperms might have radiated.
Bailey’s interest in the wood anatomy (and other features) of
woody Ranales is shown by his numerous monographs on
this group. Bailey must have been interested in the phylogenetic starting point of his “major trends.” Study of these families reveals that the traits thought by Bailey and his students
to be beginning points (e.g., long scalariform perforation
plates, tracheids as the imperforate tracheary element type,
heterogeneous type I rays, and diffuse axial parenchyma)
were common in these families. However, the wood anatomy
of the basal angiosperms is by no means uniform (Metcalfe
1987). Some of the unspecialized character states just cited
may be found in early branches of various eudicot clades
(e.g., Paracryphia of Campanulidae, Euptelea of Ranunculales, Aextoxicon of Berberidopsidales, Dillenia of Dilleniales, etc.). Extant angiosperms are present because they are
adapted to where they live today, and we should not be surprised to find that their wood features relate to particular conditions of ecology and habit. However, the features that
Bailey, Frost, Kribs, and Barghoorn regarded as “primitive”
in perforation plates, imperforate tracheary elements, axial
parenchyma, and rays do look valid as unspecialized character states, by and large, when one compares these character
states with molecular trees (Soltis et al. 2011, used for comparisons in this section). Bailey’s methods can be questioned,
but his conclusions were surprisingly acute. They are best
read in retrospect, however, not as starting points for research.
Multiplicity of apomorphies
The Bailey–Frost–Kribs changes in wood character states
would not be valid unless they occurred numerous times independently as homoplasies. For example, the change from
diffuse to grouped axial parenchyma cells has occurred
within many different clades. The significance may be formation and enhancement of a support system for vessels, as
Holbrook and Zwieniecki (1999) claimed. There may be
other explanations (interconnection of axial parenchyma with
rays, etc.). If the apomorphies were not multiple, but only a
few, they would coincide with a few major branches in the
tree of woody angiosperms, but they do not. Once acquired,
the advantages of new axial parenchyma distributions do not
seem to be abandoned in favor of the early diffuse system; if
they change, they progress on to varied expressions. The evolution of ray histology results in increasing procumbency of
cells in the multiseriate rays. The selective value for this is
presumably increased radial conduction of photosynthates, a
requisite of the woody habit (Apiaceae are somewhat exceptional in this regard, reflecting the pattern in the related family Araliaceae). An increasing proportion of upright cells in
rays may also be found, a feature of paedomorphosis (Carlquist 1964, 2009b). The Bailey group (except for Cheadle,
who studied monocots) worked with “truly woody” species
and thus lost an important dimension in their picture of how
woods evolve.
Character synchrony dissolution
In many interesting instances, there is marked change in
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
934
one or more characters in order concomitant with evolutionary changes, often those of habit. Tropaeolaceae have wood
(admittedly not much) that has libriform fibers in the secondary xylem and is self-supporting, but they have no phloem
fibers. The sister family Caricaceae have large accumulations
of phloem fibers, but fiber-free secondary xylem in which
vessels are embedded in thin-walled parenchyma. Eremosyne
is a long-branch derivative of Escalloniales (Fig. 14) that has
little if any secondary xylem and vessels with simple perforation plates, unlike the remainder of the escallonioid genera.
Gornall and Al-Shammary (1998) did find one resemblance
to escallonioids: the unusual glandular trichomes. The scalariform lateral wall pitting in Piperaceae represents a disconnect from the perforation plate type (simple), thereby
differing from the related family Saururaceae.
Different clades, different fates
When we study wood features and compare them with the
major clades, we see that some wood features such as vestured pits are common in some clades but infrequent or absent
in others. For example, vestured pits occur in Brassicales and
Myrtales but not in Caryophyllales or the campanulid families. Rosid families have differentially retained tracheids (Rosaceae), sometimes adding libriform fibers (Quercus) so that
vasicentric tracheids are present, whereas vasicentric tracheids
are almost entirely absent in campanulids (present in Hedera
of Araliaceae and in a few Asteraceae). Different clades have
different degrees of heterochrony: secondary woodiness is
well represented in the Lamiidae.
Different characters, different rates
One is not surprised at the acceleration of perforation plate
simplification with a change in habit, as with Adoxaceae
compared with Viburnum (Fig. 14), or Crossosomataceae
(shrubs of arid Mexico and adjacent California) compared
with other Crossosomatales, which grow in much wetter situations (Carlquist 2007c). One is more surprised when close
sister orders, both apparently woody at the outset, differ in
this respect: Berberidopsidales (scalariform perforation
plates) and Caryophyllales (perforation plates all simple, perhaps a single bar in a few Droseraceae and Nepenthaceae;
Carlquist 2010).
Early diversification versus recent diversification
Using the same character (scalariform perforation plates),
one can see that early (short-branch) diversification in Campanulidae tends to be correlated with retention of scalariform
perforation plates (Fig. 14). Aquifoliales, Escalloniales (except
for Eremosyne), Bruniaceae + Columelliaceae, and Paracryphiaceae exemplify this. “Breakouts” characterize branches
with more site substitutions in the Tank and Donoghue construction (e.g., Asteraceae, Calyceraceae, and Goodeniaceae).
These latter families can be hypothesized to have speciated
because of their capability of maintaining active conductive
systems in wood of species in highly seasonal climates.
Character reinforcement strategy
Wood physiology experiments that measure resistivity are,
by definition, unifactorial. In terms of wood anatomy, however,
conductive characteristics often depend on several features
working in conjunction. Conductive safety exemplifies this phe-
Botany, Vol. 90, 2012
nomenon well. Narrow vessels, vessel grouping, short vessels,
growth ring formation, helical vessel sculpturing, and axial parenchyma configurations that may confer resistance to embolism 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 coexist
Lianas in early-departing (“basal”) clades are wonderful
examples of how changes to individual characters may accompany plesiomorphic features. If one assumes that tracheids (as opposed to fiber-tracheids) are plesiomorphic in basal
angiosperms, they have been retained in the genera Schisandra and Kadsura of Schisandraceae, Piptocalyx of Trimeniaceae, and Aristolochia of Aristolochiaceae. In all three of
these instances, simple perforation plates may be found. Similar examples can be found in lianoid genera of families with
numerous wood plesiomorphies such as Dilleniaceae, Lardizabalaceae, and Menispermaceae. As a side note, the retention of tracheids in stems of so many monocots is
noteworthy (Carlquist 2012).
Bruniaceae and Sarraceniaceae have tracheids and vessels
with scalariform perforation plates, but bars are relatively few
in number (Carlquist 1978; DeBuhr 1977). In both of these
families, pit membrane remnants are present (Carlquist 1992),
so that vessel elements are more tracheid-like, compartmentalizing the vessel to a greater extent. These remnants may have
the effect of conferring greater safety and, in developmental
terms, are readily produced simply by lack of hydrolysis of
the membranes in perforations (Butterfield and Meylan 1982).
Retention of the pit membrane remnants in genera of these
two families is noteworthy. Sweeping away of the pit membrane remnants in the conductive stream is, in theory, less
readily accomplished if bars are many and the perforations are
accordingly narrow, as in Aextoxicaceae, Atherospermataceae,
Illiciaceae, and Paracryphiaceae. Pit membranes are lacking in
a number of families with numerous bars per perforation plate
such as Cornaceae and Hamamelidaceae.
Reversibility in other cell types
Does true and full reversibility ever occur in wood evolution, or do woods merely progress to new expressions, using
some older genetic information as well as some newer information? If various character states have value during the ecological shifts that occur within a clade, reversibility is
possible to that extent. Krameria is sister to the family Zygophyllaceae in which fiber-tracheids and vasicentric tracheids
occur. Krameriaceae and Zygophyllaceae thus retain the capability to form bordered pits on imperforate tracheary elements. The point stressed here is that the bordered pits may
be of various size and density. The developmental changes
required to make them larger or smaller are best regarded as
varied expressions, a “repertoire” that is always latent, and
reversibility in the Hennigian sense is not involved. Krameria, characteristic of dry to desert localities, has wood composed of vessels with simple perforation plates plus tracheids
with fully bordered pits (Carlquist 2005). Is this a reversion
to an ancestral tracheid expression, or is it within the range
of expression for genetic information present in the zygophyll
clade? The latter seems the correct interpretation. Baas and
Wheeler (1996) cited “reversions” when they compared character states with placement of taxa in phylogenetic trees.
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
935
However, characters and character states are designated by
humans and may bear no resemblance to gene content of a
plant or the way in which genes act. In the collision between
Hennigian cladistics (using designated character states) and
genomics (which follows changes at gene sites), we must
choose genomics. The genes used to construct phylogenetic
trees (e.g., Soltis et al. 2011) are not genes related to wood
development.
of a plant and how that plant interacts with the environment.
Precise physiological information? No, but one has the beginnings of learning about how the vegetative nature of the plant
and its wood anatomy might be related. A surprising number
of botanists are misled by the word “herb,” the inadequacy of
which should be obvious. Most eudicots that are termed
“herbs” do, in fact, have cambia and produce enough wood
for study of wood anatomy (e.g., annual Asteraceae).
15. Not wood alone: the relationship between
foliage, habit, and wood anatomy
Simple beginnings
Correlations of leaf form and size with climate show the
importance of knowing about foliage (Bailey and Sinnott
1916; Givnish 1979; Halloy and Mark 1996). These studies
point the way to what could be measured and how, important
ingredients for a wood student wanting to integrate foliage
knowledge into wood studies. More complex integration is
shown by Brodribb et al. (2003), as well as by Vilagrosa et
al. (2003), who join together knowledge of stomatal closure,
leaf turgor, and xylem vulnerability. Ideally, one would like
such studies done on genera that show a great deal of adaptive radiation. In fact, in Dubautia, “the differences in leaf
turgor maintenance capacities among the species are related,
in turn, to differences in tissue elastic and osmotic properties” (Purugganan et al. 2003). Species from dry habitats
such as D. ciliolata, D. linearis, D. menziesii, and D. platyphylla “have much greater capacities for maintaining high
turgor pressures as tissue water content decreases than species from mesic and wet habitats, such as D. knudseni,
D. plantaginea, and D. raillardioides” (Purugganan et al.
2003). These marked differences among species have happened in a rather short period of time (probably 5 million
years or less) on the Hawaiian Islands and correlate very
well with data from wood anatomy (Carlquist 1998). Studies
in Dubautia leaf physiology, leaf anatomy (Carlquist et al.
2003), and wood anatomy are merely in a stage at which significant differences are evident (Robichaux and Canfield
1985; Robichaux et al. 1986). More detailed studies, which
could involve wood physiology, could still be done. The Canarian species of Sonchus offer similar opportunities.
Role of leaves
Plants demand considerable water from the environment
and lose much water to it (Holbrook et al. 2002). Plants “respond physiologically to water stress, with the dominant
mechanism being to reduce rates of water loss by closing
their stomatal pores” (Holbrook et al. 2002). Brodribb et al.
(2003) agreed: “Assuming stomata guard cells directly translate physical water potential signals in the leaf and epidermis
into changes in pore aperture, and that the transduction of
these signals are governed by physical attributes of the guard
and epidermal cells, it seems probable that these traits might
co-evolve with traits governing xylem vulnerability.” Holbrook et al. (2002) add, “However, stomatal closure has the
cost of reduced CO2 uptake. The ability to refill a cavitated
vessel would allow plants to regain their original transport
capacity, and without the delays and costs of having to construct additional wood.” The fact that vessels refill (even
under conditions of negative water pressure in the xylem)
after cavitation by water stress and the mechanisms for doing
that have been stressed in section 2. In the water economy of
the plant, the less frequent the cavitations and the shorter
their duration, the better it is for plant survival and reproduction. If we know about foliage and habit, can we better
understand wood anatomy in a species? The answer clearly
seems to be yes.
Disconnected wood
Unfortunately, those who study wood anatomy often begin
with portions cut from small sample boards stored in xylarium drawers, samples often connected by accession numbers
to a minimum of information. In fact, even if those specimens are related to known herbarium specimens, such specimens are, in fact, probably rarely consulted. Even if
consulted, herbarium specimens do not reveal vital features
relating to ecology. Likewise, studies of leaf anatomy and
leaf physiology very rarely take into account wood anatomy
and wood physiology. Correlations between leaf area and
vessel characteristics for Dubautia (Carlquist 1974, p. 153)
are simple and easy to make.
The tree bias
The woodier a plant, the more likely it is to be included in
a wood collection. Large families with less woodiness such
as Apiaceae, Asteraceae, and Brassicaceae are woefully
underrepresented. Anyone attempting wood studies in such
families must do his own collecting and rely minimally on
xylaria. However, the reward of collecting plants in the field
(rather than using samples from machined microboards in xylaria) is that one learns much about the vegetative apparatus
Losing leaves
Everyone 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 in
the case of drought deciduousness along the coastal strip of
southern California, where “coastal sage” species occur. During the driest times of the year, Artemisia californica has few
functioning leaves on its stems. Coreopsis gigantea has no
functioning leaves at all during dry months and persists as
green succulent stems for the duration of the dry period.
Less conspicuously, Salvia mellifera, Malacothrix saxatilis,
and Mimulus aurantiacus reduce their leaf area markedly
and have only a few, narrow leaves in play at the tips of
branches at the end of a dry season.
Perhaps the most dramatic examples of woody droughtdeciduous shrubs and trees are represented by the family
Fouquieriaceae. Fouquieria leafs out after a rain shower (or
a moderate watering), but leaves crisp and fall soon thereafter unless more rainfall arrives. Only leaves on short
shoots are produced; long shoots are produced only during
the wet season and may not be produced at all if rains are
Published by NRC Research Press
936
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
insufficient in a particular year. The wood features of Fouquieria do not look especially xeromorphic and would, in
most species, match those of an average shrub or tree with
respect to vessel characteristics (Carlquist 2001b). The same
can be said for the wood of a Madagascar analogue of Fouquieriaceae, the drought-deciduous family Didiereaceae
(Rauh and Dittmar 1970).
Leaves that compensate and complement
Leaves may have characteristics that lessen stress on xylem. The most obvious are succulent leaves or stems. C4
photosynthesis and crassulacean acid metabolism are photosynthetic pathways that have the effect of lessening stress on
the conductive system of a plant. Microphylly and other
forms of leaf condensation characterize whole floras such as
the 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) are
fynbos shrubs that have the xylem that one would expect in
mesic shrubs of early-departing members of a clade, and indeed, Bruniaceae appear in such a position in Fig. 14. The
wood features scalariform perforation plates, relatively long
vessel elements, and tracheids. The leaves are clearly compensatory, ranging from small and needle-like to even
scale-like, with notably thick cuticles (Carlquist 1991). The
ecological sites occupied by Bruniaceae include south-facing
mountaintops (the cooler exposure in the Southern Hemisphere), as well as nonmontane sites where underground
water sources are more likely to prevail.
Phylogeny toward leaf xeromorphy and xylem
xeromorphy
Ackerly (1999, 2004) used phylogenetic trees of particular
chaparral elements and their relatives in more mesic areas to
show that adaptation to the chaparral has involved decreasing
leaf area as a criterion for entry into and success in chaparral.
Chaparral habitats feature rainfall confined to a few cool winter months. Chaparral shrubs are mostly evergreen, which
puts special constraints on leaf size and anatomy. Woods are
appropriately xeromorphic. The fibrous background of many
chaparral woods is tracheids (Adenostoma, Cercocarpus, Heteromeles) or vasicentric tracheids (Arcostaphylos, Ceanothus,
Dendromecon, Prunus, shrubby Quercus species), and quantitative characteristics of vessels are notably xeromorphic
(Carlquist and Hoekman 1985).
Reliance and cooperation
A surprising number of woody plants have hemiparasitic
interconnections with other plants (Kuijt 1969), including
Krameria and Nuytsia. The nature and degree of hemiparasitism and parasitism in these species needs to be taken into
account in any understanding of wood anatomy and physiology. Also, a surprising number of plants in southwestern
Australia form ectomycorrhizal and vesicular–arbuscular mycorrhizal associations (Bell and Pate 1996; Brundrett 2008).
Mycorrhizae have a mediating effect, increasing safety and
water-gathering capabilities. These associations explain the
occurrence of shrubs in what appear to be arid and hot areas,
especially those of acid sands. Such associations occur in
some Californian chaparral genera such as Arctostaphylos
(Brundrett 2008).
Botany, Vol. 90, 2012
Habit
Correlations of wood anatomy and physiology are very important. For instance, the relatively short stature of many
woody plants permits root pressures to be operative in refilling cavitated vessels. Succulence definitely plays a role in
wood structure, and wood of succulents is particularly poorly
known, because of its lack of inclusion in wood collections.
Cacti are an exception (Gibson 1973, 1977, 1978), and cacti
offer many fascinating structure–function correlations in their
wood (Mauseth 1993). Unusual plant shapes such as that of
Fouquieria (Idria) columnaris involve special meristematic
occurrences to expand parenchyma within the secondary xylem (Carlquist 2001b).
Summing up
Wood anatomy, wood physiology, leaf anatomy, leaf physiology, and other features are all important in the study of
woody angiosperms and their evolution. We all realize that
the ultimate desired synthesis and bridge among these fields
tends not to be realized because all workers are limited to
some degree in training or access to equipment or to the
field. Awareness of the contexts of findings in any one of
these fields may be indispensable to understanding these
findings. Synthesis in wood studies, if not easy and if not always ideally performed, is nevertheless essential to understanding wood evolution.
Acknowledgements
Special thanks go to two individuals who encouraged me
and provided facilities and supplies: Thomas S. Elias, when
he was Director at Rancho Santa Ana Botanic Garden, was
crucial in helping me begin scanning electron microscopy;
and Edward L. Schneider, during his tenure as President of
Santa Barbara Botanic Garden, proved equally helpful in similar ways, permitting me to transfer my research from Claremont to Santa Barbara. Those who provided me with
materials for study were very important: Regis B. Miller during his years with the Forest Products Laboratory, Madison,
Wisconsin, was notable in this regard. Scott Zona provided a
careful and helpful review of the manuscript. Christian Lacroix kindly invited me to submit this paper to the journal
Botany and provided editorial support.
References
Ackerly, D.D. 1999. Phylogeny and the comparative method in plant
functional ecology. In Physiological plant ecology. Edited by
M. Press, J. Scholes, and M.G. Barker. Blackwell Scientific,
Oxford, UK. pp. 391–413.
Ackerly, D.D. 2004. Adaptation, niche conservation, and convergence: comparative studies of leaf evolution in the California
chaparral. Am. Nat. 163(5): 654–671. doi:10.1086/383062. PMID:
15122485.
Angiosperm Phylogeny Group. 2009. An update of the Angiosperm
Phylogeny Group classification for the orders and families of
flowering plants: APG III. Bot. J. Linn. Soc. 161(2): 105–121.
doi:10.1111/j.1095-8339.2009.00996.x.
Baas, P., and Wheeler, E.A. 1996. Parallelism and reversibility in
xylem evolution: a review. IAWA J. 17: 351–364.
Bailey, I.W. 1944. The development of vessels in angiosperms in
morphological research. Am. J. Bot. 31(7): 421–428. doi:10.2307/
2437302.
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
Bailey, I.W., and Sinnott, E.W. 1916. The climatic distribution of
certain types of angiosperm leaves. Am. J. Bot. 3(1): 24–29.
doi:10.2307/2435109.
Bailey, I.W., and Tupper, W.W. 1918. Size variation in tracheary
cells. I. A comparison between the secondary xylems of vascular
cryptograms, gymnosperms, and angiosperms. Proc. Am. Acad.
Arts Sci. 54(2): 149–204. doi:10.2307/20025747.
Barghoorn, E.S. 1940. The ontogenetic development and phylogenetic specialization of rays in the xylem of dicotyledons. I.
Primitive ray structure. Am. J. Bot. 27(10): 918–928. doi:10.2307/
2436561.
Barghoorn, E.S. 1941a. The ontogenetic development and phylogenetic specialization of rays in the xylem of dicotyledons. II.
Modification of the multiseriate and uniseriate rays. Am. J. Bot.
28(4): 273–282. doi:10.2307/2436785.
Barghoorn, E.S. 1941b. The ontogenetic development and phylogenetic specialization of rays in the xylem of dicotyledons. III. The
elimination of rays. Bull. Torrey Bot. Club, 68(5): 317–325.
doi:10.2307/2481604.
Bell, T.L., and Pate, J.S. 1996. Nitrogen and phosphorus nutrition in
mycorrhizal Epacridaceae of south-west Australia. Ann. Bot.
(Lond.), 77(4): 389–398. doi:10.1006/anbo.1996.0047.
Bierhorst, D.W., and Zamora, P.M. 1965. Primary xylem elements
and element associations of angiosperms. Am. J. Bot. 52(7): 657–
710. doi:10.2307/2446590.
Bonsen, K.J., and ter Welle, B.J.H. 1984. Systematic wood anatomy
and affinities of the Urticaceae. Bot. Jahrb. Syst. 105: 49–71.
Borghetti, M., Cinnirella, S., Magnani, F., and Saracino, A. 1998.
Impact of long-term drought on xylem embolism and growth in
Pinus halepensis Mill. Trees, 12: 187–195. doi:10.1007/
PL00009709 .
Braun, H.J. 1970. Funktionelle Histologie der sekundären Sprossachse. I. Das Holz. In Handbuch der Pflanzenanatomie. Vol. 9,
Part 1. Gebrüder Borntraeger, Berlin, Germany.
Brodribb, T.J., Holbrook, N.M., Edwards, E.J., and Gutierrez, M.V.
2003. Relations between stomatal closure, leaf turgor, and xylem
vulnerability in eight tropical dry forest trees. Plant Cell Environ.
26(3): 443–450. doi:10.1046/j.1365-3040.2003.00975.x.
Brundrett, M.C. 2008. Mycorrhizal associations: the Web resource.
Available at http://mycorrhizas.info [accessed December 2011].
Butterfield, B.G., and Meylan, B.A. 1972. Scalariform perforation
plate development in Laurelia novae-zelandiae A. Cunn.: a
scanning electron microscope study. Aust. J. Bot. 20(3): 253–
259. doi:10.1071/BT9720253.
Butterfield, B.G., and Meylan, B.A. 1982. Cell wall hydrolysis in the
tracheary elements of the secondary xylem. In New perspectives in
wood anatomy. Edited by P. Baas. Martinus Nijhoff Publishers, the
Hague, Netherlands. pp. 71–81.
Carlquist, S. 1957. Wood anatomy of Mutisieae (Compositae). Trop.
Woods, 106: 29–45.
Carlquist, S. 1958. Wood anatomy of Heliantheae (Compositae).
Trop. Woods, 108: 1–30.
Carlquist, S. 1960. Wood anatomy of Cichorieae (Compositae). Trop.
Woods, 112: 65–91.
Carlquist, S. 1961. Comparative plant anatomy. Holt, Rinehart &
Winston, New York.
Carlquist, S. 1962. A theory of paedomorphosis in dicotyledonous
woods. Phytomorphology, 12: 30–45.
Carlquist, S. 1966. Wood anatomy of Compositae: a summary, with
comments on factors controlling wood evolution. Aliso, 6(2): 25–44.
Carlquist, S. 1969. Wood anatomy of Lobelioideae (Campanulaceae).
Biotropica, 1(2): 47–72. doi:10.2307/2989761.
Carlquist, S. 1974. Island biology. Columbia University Press, New
York.
937
Carlquist, S. 1975. Ecological strategies of xylem evolution.
University of California Press, Berkeley, California.
Carlquist, S. 1977. Wood anatomy of Grubbiaceae. J. S. African Bot.
43: 129–144.
Carlquist, S. 1978. Wood anatomy of Bruniaceae: correlations with
ecology, phylogeny, and organography. Aliso, 9: 323–364.
Carlquist, S. 1980. Further concepts in ecological wood anatomy,
with comments on recent work in wood anatomy and evolution.
Aliso, 9: 499–553.
Carlquist, S. 1981a. Wood anatomy of Zygogynum (Winteraceae):
field observations. Bull. Mus. Nat. Hist. Nat. Ser. 4, Sect. B
Adansonia, 3: 281–292.
Carlquist, S. 1981b. Wood anatomy of Pittosporaceae. Allertonia, 7:
355–391.
Carlquist, S. 1982. Wood anatomy of Illicium (Illiciaceae):
phylogenetic, ecological, and functional interpretations. Am. J.
Bot. 69(10): 1587–1598. doi:10.2307/2442914.
Carlquist, S. 1983. Wood anatomy of Onagraceae: further species;
root anatomy; significance of vestured pits and allied structures in
dicotyledons. Ann. Mo. Bot. Gard. 69(4): 755–769. doi:10.2307/
2398995.
Carlquist, S. 1984. Vessel grouping in dicotyledon woods: significance and relationship to imperforate tracheary elements. Aliso,
10: 505–525.
Carlquist, S. 1985a. Vasicentric tracheids as a drought survival
mechanism in the woody flora of southern California and similar
regions: review of vasicentric tracheids. Aliso, 11: 37–68.
Carlquist, S. 1985b. Observations on functional wood histology of
vines and lianas: vessel dimorphism, tracheids, vasicentric
tracheids, narrow tracheids, and parenchyma. Aliso, 11: 139–157.
Carlquist, S. 1987. Diagonal and tangential vessel aggregations in
wood: function and relationship to vasicentric tracheids. Aliso, 11:
451–462.
Carlquist, S. 1988. Comparative wood anatomy. Springer-Verlag,
Heidelberg, Germany.
Carlquist, S. 1989a. Wood and bark anatomy of Empetraceae:
comments on paedomorphosis in woods of certain small shrubs.
Aliso, 12: 487–515.
Carlquist, S. 1989b. Wood anatomy of Tasmannia: summary of wood
anatomy of Winteraceae. Aliso, 12: 257–275.
Carlquist, S. 1991. Leaf anatomy of Bruniaceae: ecological,
systematic, and phylogenetic aspects. Bot. J. Linn. Soc. 107(1):
1–34. doi:10.1111/j.1095-8339.1991.tb00212.x.
Carlquist, S. 1992. Pit membrane remnants in perforation plates of
primitive dicotyledons and their significance. Am. J. Bot. 79(6):
660–672. doi:10.2307/2444882.
Carlquist, S. 1998. Wood anatomy of Dubautia (Asteraceae:
Madiinae) in relation to adaptive radiation. Pac. Sci. 52: 356–368.
Carlquist, S. 1999. Wood anatomy of Schisandraceae: implications
for phylogeny, habit, and vessel evolution. Aliso, 18: 45–55.
Carlquist, S. 2001a. Comparative wood anatomy. 2nd ed. SpringerVerlag, Heidelberg, Germany.
Carlquist, S. 2001b. Wood anatomy of Fouquieriaceae in relation to
habit, ecology, and systematics: nature of meristems in wood and
bark. Aliso, 19: 137–163.
Carlquist, S. 2005. Wood anatomy of Krameriaceae with comparisons
with Zygophyllaceae: phylesis, ecology, and systematics. Bot. J.
Linn. Soc. 149(3): 257–270. doi:10.1111/j.1095-8339.2005.
00451.x.
Carlquist, S. 2007a. Successive cambia revisited: ontogeny, histology,
diversity, and functional significance. J. Torrey Bot. Soc. 134(2):
301–332. doi:10.3159/1095-5674(2007)134[301:SCROHD]2.0.
CO;2.
Carlquist, S. 2007b. Bordered pits in ray cells and axial parenchyma:
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
938
the histology of conduction, storage, and strength in living wood
cells. Bot. J. Linn. Soc. 153(2): 157–168. doi:10.1111/j.10958339.2006.00608.x.
Carlquist, S. 2007c. Wood anatomy of Crossosomatales: patterns of
wood evolution with relation to phylogeny and ecology. Aliso, 24:
1–18.
Carlquist, S. 2009a. Non-random vessel distribution in woods:
patterns, modes, diversity, correlations. Aliso, 27: 39–58.
Carlquist, S. 2009b. Xylem heterochrony: an unappreciated key to
angiosperm origins and diversifications. Bot. J. Linn. Soc. 161(1):
26–65. doi:10.1111/j.1095-8339.2009.00991.x.
Carlquist, S. 2010. Caryophyllales: a key group for understanding
wood anatomy character states and their evolution. Bot. J. Linn.
Soc. 164(4): 342–393. doi:10.1111/j.1095-8339.2010.01095.x.
Carlquist, S. 2012. Monocot xylem revisited: new information, new
paradigms. Bot. Rev. 78(2): 87–153. doi:10.1007/s12229-0129096-1.
Carlquist, S., and Hanson, M.A. 1991. Wood and stem anatomy of
Convolvulaceae: a survey. Aliso, 13: 51–94.
Carlquist, S., and Hoekman, D.A. 1985. Ecological wood anatomy of
the woody southern Californian flora. IAWA Bull. (n.s.), 6: 319–
347.
Carlquist, S., and Miller, R.B. 2001. Wood anatomy of Corynocarpaceae is consistent with placement in Cucurbitales. Syst. Bot. 26:
54–65.
Carlquist, S., and Zona, S. 1988. Wood anatomy of Papaveraceae,
with comments on vessel restriction patterns. IAWA Bull. (n.s.), 9:
253–267.
Carlquist, S., Carr, G.D., and Baldwin, B.G. 2003. Tarweeds and
silverswords. Evolution of the Madiinae (Asteraceae). Missouri
Botanical Garden Press, St. Louis, Missouri.
Chase, M.W., Soltis, D.E., Olmstead, R.G., Morgan, D., Les, D.H.,
Mishler, B.D., Duvall, M.R., Price, R.A., Hills, H.G., Qiu, Y.-L.,
Kron, K.A., Rettig, J.H., et al. 1993. Phylogenetics of seed plants:
an analysis of nucleotide sequences from the plastid gene rbcL.
Ann. Mo. Bot. Gard. 80(3): 528–580. doi:10.2307/2399846.
Cheadle, V.I. 1942. The occurrence and types of vessels in the
various organs of the plant in the Monocotyledoneae. Am. J. Bot.
29(6): 441–450. doi:10.2307/2437308.
Cheadle, V.I. 1943. The origin and certain trends of specialization of
the vessel in the Monocotyledoneae. Am. J. Bot. 30(1): 11–17.
doi:10.2307/2437386.
Choat, B., Ball, M., Luly, N., and Holtum, J. 2003. Pit membrane
porosity and water stress-induced cavitation in four co-existing
rainforest tree species. Plant Physiol. 131(1): 41–48. doi:10.1104/
pp.014100. PMID:12529513.
Choat, B., Jansen, S., Zwieniecki, M.A., Smets, E., and Holbrook,
N.M. 2004. Changes in pit membrane porosity due to deflection
and stretching: the role of vestured pits. J. Exp. Bot. 55(402):
1569–1575. doi:10.1093/jxb/erh173. PMID:15181107.
Choat, B., Cobb, A., and Jansen, S. 2008. Structure and function of
bordered pits: new discoveries and impacts on whole plant
hydraulic function. New Phytol. 177(3): 608–626. doi:10.1111/j.
1469-8137.2007.02317.x. PMID:18086228.
Cumbie, B.G. 1969. Developmental changes in the vascular cambium
of Poligonum lapathifolium. Am. J. Bot. 56(2): 139–146. doi:10.
2307/2440699.
Davis, T.A. 1961. High root-pressures in palms. Nature, 192(4799):
277–278. doi:10.1038/192277a0.
DeBuhr, L.E. 1977. Wood anatomy of Sarraceniaceae: ecological and
evolutionary implications. Plant Syst. Evol. 128(3–4): 159–169.
doi:10.1007/BF00984552.
Dickison, W.C., and Miller, R.B. 1993. Morphology and anatomy of
the Malagasy genus Physena (Physenaceae), with a discussion of
Botany, Vol. 90, 2012
the relationships of the genus. Bull. Mus. Nat. Hist. Nat. Paris, Ser.
14, Sect. B, Adansonia, 15: 85–106.
Ellerby, D.J., and Ennos, A.R. 1998. Resistances to fluid flow of
model xylem vessels with simple and scalariform perforation
plates. J. Exp. Bot. 49: 979–985.
Ewers, F.W., Fisher, J.B., and Fichtner, K. 1991. Water flux and
xylem structure in vines. In The biology of vines. Edited by F.E.
Putz and H.A. Mooney. Cambridge University Press, Cambridge,
UK. pp. 127–160.
Feild, T.S., Brodribb, T., and Holbrook, N.M. 2002. Hardly a relict:
freezing and the evolution of vesselless wood in Winteraceae.
Evolution, 56(3): 464–478. PMID:11989678.
Fisher, J.B., Angeles A., G., Ewers, F.W., and Lopez-Portillo, J. 1997.
Survey of root pressure in tropical vines and woody species. Int. J.
Plant Sci. 158(1): 44–50. doi:10.1086/297412.
Frost, F.H. 1930a. Specialization in secondary xylem in dicotyledons.
I. Origin of vessels. Bot. Gaz. 89(1): 67–94. doi:10.1086/334026.
Frost, F.H. 1930b. Specialization in secondary xylem in dicotyledons.
II. Evolution of end wall of vessel segment. Bot. Gaz. 90(2): 198–
212. doi:10.1086/334094.
Frost, F.H. 1931. Specialization in secondary xylem in dicotyledons.
III. Specialization of lateral wall of vessel segment. Bot. Gaz.
91(1): 88–96. doi:10.1086/334128.
Fujii, T. 1993. Application of a resin casting method in wood anatomy
of some Japanese Fagaceae species. IAWA J. 14: 273–288.
Funk, V.A., Susanna, A., Stuessy, T.F., and Bayer, R.J. (Editors).
2009. Systematics, evolution, and biogeography of Compositae.
International Association for Plant Taxonomy, Vienna, Austria.
Gibson, A.C. 1973. Comparative anatomy of secondary xylem in
Cactoideae (Cactaceae). Biotropica, 5(1): 29–65. doi:10.2307/
2989678.
Gibson, A.C. 1977. Wood anatomy of Opuntias with cylindrical to
globular stems. Bot. Gaz. 138(3): 334–351. doi:10.1086/336933.
Gibson, A.C. 1978. Wood anatomy of platyopuntias. Aliso, 9: 279–
307.
Givnish, T. 1979. On the adaptive significance of leaf form. In Topics
in plant population biology. Edited by O.T. Solbrig, S. Jain, G.B.
Johnson, and P.H. Raven. Columbia University Press, New York.
pp. 375–407.
Gornall, R.J., and Al-Shammary, K.I.A. 1998. Eremosynaceae. In
Anatomy of the dicotyledons. 2nd ed. Vol. 4. Edited by D.F. Cutler
and M. Gregory. Clarendon Press, Oxford, UK. pp. 236–237.
Gregory, M. 1994. Bibliography of systematic wood anatomy of
dicotyledons. IAWA Journal, Suppl. 1 – 1994. International
Association of Wood Anatomists, Heidelberglann, Netherlands.
Hacke, U.G., Sperry, J.S., and Pittermann, J. 2000. Drought
experience and cavitation resistance in six desert shrubs from
the Great Basin, Utah. Basic Appl. Ecol. 1(1): 31–41. doi:10.1078/
1439-1791-00006.
Hacke, U.G., Sperry, J.S., Pockman, W.T., Davis, S.D., and
McCulloh, K.A. 2001. Trends in wood density and structure are
linked to prevention of xylem implosion by negative pressure.
Oecologia (Berl.), 126(4): 457–461. doi:10.1007/s004420100628.
Hacke, U.G., Sperry, J.S., Feild, T.S., Sano, Y., Sikkema, E.H., and
Pittermann, J. 2007. Water transport in vesselless angiosperms:
conducting efficiency and cavitation safety. Int. J. Plant Sci.
168(8): 1113–1126. doi:10.1086/520724.
Halloy, S.R.P., and Mark, A.F. 1996. Comparative leaf morphology
spectra of plant communities in New Zealand, the Andes, and the
European Alps. J. R. Soc. N.Z. 26(1): 41–78. doi:10.1080/
03014223.1996.9517504.
Hargrave, K.R., Kolb, K.J., Ewers, F.W., and Davis, S.D. 1994.
Conduit diameter and drought-induced embolisms in Salvia
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
Carlquist
mellifera Greene (Labiatae). New Phytol. 126(4): 695–705. doi:10.
1111/j.1469-8137.1994.tb02964.x.
Holbrook, N.M., and Zwieniecki, M.A. 1999. Embolism repair and
xylem tension: do we need a miracle? Plant Physiol. 120(1): 7–10.
doi:10.1104/pp.120.1.7. PMID:10318678.
Holbrook, N.M., Zwieniecki, M.A., and Melcher, P.J. 2002. The
dynamics of “dead wood”: maintenance of water transport through
plant stems. Integr. Comp. Biol. 42(3): 492–496. doi:10.1093/icb/
42.3.492. PMID:21708743.
Jacobsen, A.L., Ewers, F.W., Pratt, R.B., Paddock, W.A., III, and
Davis, S.D. 2005. Do xylem fibers affect vessel cavitation
resistance? Plant Physiol. 139(1): 546–556. doi:10.1104/pp.104.
058404. PMID:16100359.
Jansen, S., Baas, P., Gasson, P., and Smets, E. 2003. Vestured pits: do
they promote safer water transport? Int. J. Plant Sci. 164(3): 405–
413. doi:10.1086/374369.
Jansen, S., Choat, B., and Pletsers, A. 2009. Morphological variation
of intervessel pit membranes and implications to xylem function in
angiosperms. Am. J. Bot. 96(2): 409–419. doi:10.3732/ajb.
0800248. PMID:21628196.
Jeje, A.A., and Zimmermann, M.H. 1979. Resistance to flow in
vessels. J. Exp. Bot. 30(4): 817–827. doi:10.1093/jxb/30.4.817.
Khan, M.A., Ungar, I.A., and Showalter, A.M. 2000. Effects of
salinity on growth, water relations, and ion accumulation of the
subtropical perennial halophyte, Atriplex griffithi var. stockii. Ann.
Bot. (Lond.), 85(2): 225–232. doi:10.1006/anbo.1999.1022.
Kohonen, M.M., and Helland, A. 2009. On the function of wall
sculpturing in xylem conduits. J. Basic Engin. 6: 324–329.
Kribs, D.A. 1935. Salient lines of structural specialization in the
wood rays of dicotyledons. Bot. Gaz. 96(3): 547–557. doi:10.
1086/334500.
Kribs, D.A. 1937. Salient lines of structural specialization in the
wood parenchyma of dicotyledons. Bull. Torrey Bot. Club, 64(4):
177–186. doi:10.2307/2481141.
Kuijt, J. 1969. The biology of parasitic flowering plants. University of
California Press, Berkeley, California.
Langan, S.J., Ewers, F.W., and Davis, S.D. 1997. Xylem dysfunction
caused by water stress and freezing in two species of co-occurring
chaparral shrubs. Plant Cell. Environ. 20: 425–437.
Lens, F., Gasson, P., Smets, E., and Jansen, S. 2003. Comparative
wood anatomy of epacrids (Styphelioideae, Ericaceae s.l.). Ann.
Bot. (Lond.), 91(7): 835–856. doi:10.1093/aob/mcg089. PMID:
12770843.
Lens, F., Eeckhout, S., Zwartjes, R., Smets, E., and Janssens, S.B.
2012. The multiple fuzzy origins of woodiness within Balsaminaceae using an integrated approach: where do we draw the line?
Ann. Bot. (Lond.), 109(4): 783–799. doi:10.1093/aob/mcr310.
PMID:22190560.
Mauseth, J.D. 1993. Water-storing and cavitation-preventing adaptations in wood of cacti. Ann. Bot. (Lond.), 72(1): 81–89. doi:10.
1006/anbo.1993.1083.
McCully, M.E. 1999. Root xylem embolism and refilling. Relation to
water potentials of soil, roots, and leaves, and osmotic potentials of
root xylem sap. Plant Physiol. 119(3): 1001–1008. doi:10.1104/
pp.119.3.1001.
McCully, M.E., Huang, J.C.X., and Ling, L.E.C. 1998. Daily
embolism and refilling of xylem vessels in the roots of fieldgrown maize. New Phytol. 138(2): 327–342. doi:10.1046/j.14698137.1998.00101.x.
Melcher, P.J., Goldstein, G., Meinzer, F.C., Yount, D.E., Jones, T.J.,
Holbrook, N.M., and Huang, C.X. 2001. Water relations of coastal
and estuarine Rhizophora mangle: xylem pressure potential and
dynamics of embolism formation and repair. Oecologia (Berl.),
126(2): 182–192. doi:10.1007/s004420000519.
939
Metcalfe, C.R. 1987. Anatomy of the diecotyledons. 2nd ed. Vol. III.
Magnoiliales, Illiciales, and Laurales. Clarendon Press, Oxford, UK.
Metcalfe, C.R., and Chalk, L. 1950. Anatomy of the dicotyledons.
Clarendon Press, Oxford, UK.
Meylan, B.A., and Butterfield, B.G. 1978. The structure of New
Zealand woods. DSIR Bulletin 222, New Zealand Department of
Scientific and Industrial Research, Wellington, New Zealand.
Milburn, J.A., and McLaughlin, M.E. 1974. Studies of cavitation in
isolated vascular bundles and whole leaves of Plantago major L.
New Phytol. 73(5): 861–871. doi:10.1111/j.1469-8137.1974.
tb01315.x.
Obaton, M. 1960. Les lianes ligneuses à structure anomales des forêts
dense d’Afrique occidentale. Ann. Sci. Nat. Bot. 12, Ser. 1.
Parham, R.A., and Baird, W.M. 1974. Warts in the evolution of
angiosperm wood. Wood Sci. Technol. 8: 1–10.
Pfeiffer, H. 1926. Das abnorme Dickenwachstum.In Handbuch der
Pflanzenanatomie. Vol. 9, Part 1. Gebrüder Borntraeger, Berlin,
Germany.
Pickard, W.F. 1989. How might a tracheary element which is
embolized by day be healed by night? J. Theor. Biol. 141(2): 259–
279. doi:10.1016/S0022-5193(89)80021-9.
Pittermann, J., Sperry, J.S., Hacke, U.G., Wheeler, J.K., and Sikkema,
E.H. 2005. Torus-Margo pits help conifers compete with
angiosperms. Science, 310(5756): 1924. doi:10.1126/science.
1120479. PMID:16373568.
Purugganan, M.D., Remington, D., and Robichaux, R.H. 2003.
Molecular evolution of regulatory genes in the silversword
alliance. In Evolution of the Madiinae (Asteraceae). Tarweeds
and silverswords. Edited by S. Carlquist, B.G. Baldwin, and G.
Carr. Missouri Botanical Garden Press, St. Louis, Missouri.
pp. 171–182.
Rabaey, D., Lens, F., Smets, E., and Jansen, S. 2006. The
micromorphology of pit membranes in tracheary elements of
Ericales: new records of tori or pseudotori? Ann. Bot. (Lond.),
98(5): 943–951. doi:10.1093/aob/mcl183.
Rauh, W., and Dittmar, K. 1970. Weitere Untersuchungen an
Didieraceen: Teil III: Vergleichend-Anatomische Untersuchungen
an den Sprossachsen und den Dornen der Didiereaceen.
Sitzungsber. Heidelberg Akad. Wiss., Math.-Nat. Kl. 4: 1–88.
Robert, E.M.R., Schmitz, N., Boeren, I., Driesens, T., Herremans, K.,
De Mey, J., Van der Casteele, E., Beeckman, H., and Koedam, N.
2011. Successive cambia: a developmental oddity or an adaptive
structure. PLoS ONE, 6(1): e16558. doi:10.1371/journal.pone.
0016558. PMID:21304983.
Robichaux, R.H., and Canfield, J.E. 1985. Tissue elastic properties of
eight Hawaiian Dubautia species that differ in habitat and diploid
chromosome number. Oecologia (Berl.), 66(1): 77–80. doi:10.
1007/BF00378555.
Robichaux, R.H., Holsinger, K.E., and Morse, S.R. 1986. Turgor
maintenance in Hawaiian Dubautia species: the role of variation in
tissue osmotic and elastic properties. In On the economy of plant
form and function. Edited by T.J. Givnish. Cambridge University
Press, Cambridge, UK. pp. 353–380.
Rodriguez, R.L. 1957. Systematic anatomical studies on Myrrhidendron and other woody Umbellales. Univ. Calif. Publ. Bot. 29:
145–318.
Rumball, W. 1963. Wood structure in relation to heteroblastism.
Phytomorphology, 11: 206–214.
Salleo, S., Lo Gullo, M.A., De Paoli, D., and Zippo, M. 1996. Xylem
recovery from cavitation-induced embolism in young plants of
Laurus nobilis: a possible mechanism. New Phytol. 132(1): 47–56.
doi:10.1111/j.1469-8137.1996.tb04507.x.
Sano, Y., Morris, H., Shimada, H., Ronse De Craene, L.P., and
Jansen, S. 2011. Anatomical features associated with water
Published by NRC Research Press
Botany Downloaded from www.nrcresearchpress.com by Dr Christian Lacroix on 11/01/12
For personal use only.
940
transport in imperforate tracheary elements of vessel-bearing
angiosperms. Ann. Bot. (Lond.), 107(6): 953–964. doi:10.1093/
aob/mcr042. PMID:21385773.
Sauter, J.J. 1966a. Untersuchungen zur Physiologie der Pappelholzstrahlen. I. Jahresperiodischer Verlaug der Stärkesspeicherung im
Holztrahlparenchym. Zeitschr. Pflanzenphys. 55: 246–258.
Sauter, J.J. 1966b. Undersuchungen zur Physiologie der Pappelholzstrahlen. II. Jahresperiodischen Änderungen der PhosphotaseAktivität im Holzstrahlparenchym und ihre mögliche Bedeutung
für den Kohlhydratstoffwechsel und den acktiven Assimilattransport. Zeitschr. Pflanzenphys. 55: 349–382.
Sauter, J.J., Iten, W.I., and Zimmermann, M.H. 1973. Studies on the
release of sugar into the vessels of the sugar maple (Acer
saccharum). Can. J. Bot. 51(1): 1–8. doi:10.1139/b73-001.
Schulte, P.J., and Castle, A.L. 1993a. Water flow through vessel
perforation plates — a fluid mechanical approach. J. Exp. Bot.
44(7): 1135–1142. doi:10.1093/jxb/44.7.1135.
Schulte, P.J., and Castle, A.L. 1993b. Water flow through vessel
perforation plates — the effects of plate angle and thickness in
Liriodendron tulipifera. J. Exp. Bot. 44(7): 1143–1148. doi:10.
1093/jxb/44.7.1143.
Slatyer, R.O. 1967. Plant–water relationships. Academic Press, New
York.
Solereder, H. 1885.Über den systematischen Wert der Holzstruktur
bei den Dikotyledonen. R. Oldenbourg, München.
Solereder, H. 1906. Systematic anatomy of the dicotyledons (trans.
Boodle and Frit6sch). Clarendon Press, Oxford, UK.
Soltis, D.E., Soltis, P.S., Chase, M.W., Mort, M.E., Albach, D.C.,
Zanis, M., Savolainen, V., et al. 2000. Angiosperm phylogeny
inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn.
Soc. 133: 381–461.
Soltis, D.E.W., Smith, S.A., Cellinese, N., Wurdack, K.J., Tank, D.C.,
Brockington, S.F., Refulio-Rodgriguez, N.F., Walker, J.B., Moore,
M.J., Carlsward, B.S., Bell, C.D., Latvis, M., Crawley, S., Black,
C., Diouf, D., Xi, S., Rushworth, C.A., Gitzendanner, M.A.,
Sytsma, K.J., Qiu, Y.-L., Hilu, K.W., Davis, C.C., Sanderson, M.J.,
Beaman, R.S., Olmstead, R.G., Judd, W.S., Donoghue, M.J., and
Soltis, P.S. 2011. Angiosperm phylogeny: 17 genes, 640 taxa. Am.
J. Bot. 98(4): 704–730. doi:10.3732/ajb.1000404. PMID:
21613169.
Sperry, J.S. 1986. Relationship of xylem embolism to xylem pressure
potential, stomatal closure, and shoot morphology in the palm
Rhapis excelsa. Plant Physiol. 80(1): 110–116. doi:10.1104/pp.80.
1.110. PMID:16664563.
Sperry, J.S., Hacke, U.G., and Wheeler, J.K. 2005. Comparative
analysis of end wall resistivity in xylem conduits. Plant Cell
Environ. 28(4): 456–465. doi:10.1111/j.1365-3040.2005.01287.x.
Sperry, J.S., Hacke, U.G., and Pittermann, J. 2006. Size and function
in conifer tracheids and angiosperm vessels. Am. J. Bot. 93(10):
1490–1500. doi:10.3732/ajb.93.10.1490. PMID:21642096.
Sperry, J.S., Hacke, U.G., Feild, T.S., Sano, Y., and Sikkema, E.H.
Botany, Vol. 90, 2012
2007. Hydraulic consequences of vessel evolution in angiosperms.
Int. J. Plant Sci. 168(8): 1127–1139. doi:10.1086/520726.
Taneda, H., and Sperry, J.S. 2008. A case-study of water transport in
co-occurring ring- versus diffuse-porous trees: contrasts in waterstatus, conducting capacity, cavitation and vessel refilling. Tree
Physiol. 28(11): 1641–1651. doi:10.1093/treephys/28.11.1641.
PMID:18765369.
Tank, D.C., and Donoghue, M.J. 2010. Phylogeny and phylogenetic
nomenclature of the Campanulidae based on an extended sample
of genes and taxa. Syst. Bot. 35(2): 425–441. doi:10.1600/
036364410791638306.
Tyree, M.T., and Ewers, F.W. 1991. The hydraulic architecture of
trees and other woody plants. New Phytol. 119(3): 345–360.
doi:10.1111/j.1469-8137.1991.tb00035.x.
Tyree, M.T., Fiscus, E.L., Wullschleger, S.D., and Dixon, M.A. 1986.
Detection of xylem cavitation in corn under field conditions. Plant
Physiol. 82: 597–599. doi:10.1104/pp.82.2.597.
Tyree, M.T., Salleo, S., Nardini, A., Lo Gullo, M.A., and Mosca, R.
1999. Refilling of embolized vessels in young stems of laurel. Do
we need a new paradigm? Plant Physiol. 120(1): 11–21. doi:10.
1104/pp.120.1.11.
van Ieperen, W. 2007. Ion-mediated changes of xylem hydraulic
resistance in plants: fact or fiction? Trends Plant Sci. 12(4): 137–
142. doi:10.1016/j.tplants.2007.03.001. PMID:17368079.
Vilagrosa, A., Bellot, J., Vallejo, V.R., and Gil-Pelegrin, E. 2003.
Cavitation, stomata conductance, and leaf dieback in seedlings of
two co-occurring Mediterranean shrubs during an intense drought.
J. Exp. Bot. 54(390): 2015–2024. doi:10.1093/jxb/erg221. PMID:
12885857.
Vogt, U.K. 2001. Hydraulic vulnerability, vessel refilling, and
seasonal courses of stem water potential of Sorbus aucuparia
L. and Sambucus nigra L. J. Exp. Bot. 52(360): 1527–1536.
doi:10.1093/jexbot/52.360.1527. PMID:11457913.
Wheeler, J.K., and Holbrook, N.M. 2007. Cavitation and refilling. In
A companion to plant physiology. 5th ed. Edited by L. Taiz and
E. Zeiger. Available at http://5e.plantphys.net/ [accessed July 2011].
Yang, Y., and Tyree, M.T. 1992. A theoretical model of hydraulic
conductivity recovery from embolism with comparison to
experimental data on Acer saccharum. Plant Cell Environ. 15(6):
633–643. doi:10.1111/j.1365-3040.1992.tb01005.x.
Zimmermann, M.H. 1983. Xylem structure and the ascent of sap.
Springer-Verlag, Heidelberg, Germany.
Zimmermann, M.H., and Jeje, A.A. 1981. Vessel-length distribution
in stems of some American woody plants. Can. J. Bot. 59(10):
1882–1892. doi:10.1139/b81-248.
Zweypfenning, R.C.V.J. 1978. A hypothesis on the function of
vestured pits. IAWA Bull. 1978(1): 13–15.
Zwieniecki, M.A., and Holbrook, N.M. 2000. Bordered pit structure
and vessel wall surface properties. Implications for embolism
repair. Plant Physiol. 123(3): 1015–1020. doi:10.1104/pp.123.3.
1015. PMID:10889250.
Published by NRC Research Press