Monocot Xylem Revisited: New
Information, New Paradigms
Sherwin Carlquist
The Botanical Review
ISSN 0006-8101
Volume 78
Number 2
Bot. Rev. (2012) 78:87-153
DOI 10.1007/s12229-012-9096-1
1 23
Your article is protected by copyright and
all rights are held exclusively by The New
York Botanical Garden. This e-offprint is
for personal use only and shall not be selfarchived in electronic repositories. If you
wish to self-archive your work, please use the
accepted author’s version for posting to your
own website or your institution’s repository.
You may further deposit the accepted author’s
version on a funder’s repository at a funder’s
request, provided it is not made publicly
available until 12 months after publication.
1 23
Author's personal copy
Bot. Rev. (2012) 78:87–153
DOI 10.1007/s12229-012-9096-1
Monocot Xylem Revisited: New Information,
New Paradigms
Sherwin Carlquist1,2
1
2
Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA
Author for Correspondence; e-mail: [email protected]
Published online: 5 April 2012
# The New York Botanical Garden 2012
Abstract Five sources of data force extensive revision of ideas about the nature and
evolution of monocot xylem: scanning electron microscopy (SEM) studies of thick
sections; availability of molecular phylogenies covering a relatively large number of
families and genera; information on ecology and habitat; data concerning habit; and
observations from xylem physiology. These five new sources of data, absent from the
studies of Cheadle, plus added information from light microscopy, lead to a fresh
understanding of how xylem has evolved in monocots. Tracheary elements hitherto
recorded as vessel elements with scalariform end walls prove in a number of
instances, to retain pit membranes (often porous or reticulate) in the end walls. There
is not an inexorable progression from "primitive" to "specialized" xylem in monocots;
apparent accelerations or reversions are also possible. The latter include such changes
as the result of production of narrower vessel elements; or production of less
metaxylem, which is probably heterochronic in nature (an extreme form of juvenilism). Tracheary elements intermediate between vessel elements and tracheids must be
recognized for what they are, and not forced into mutually exclusive categories.
Original data on tracheids and various types of vessel elements is related here to
ecology and habit of groups such as Asteliaceae, Boryaceae, Cyclanthaceae, Orchidaceae, Pandanaceae, Taccaceae, Typhaceae, dracaenoid Asparagaceae, and Zingiberales. Data from palm xylem shows a nearly unique syndrome of features that can be
explained with the aid of information from physiology and ecology. Vessellessness of
stems and leaves characterizes a large number of monocot species; the physiological
and ecological significance of these is highlighted. An understanding of how nonpalm arborescent monocots combine an all-tracheid stem xylem with addition of
bundles and vegetative modifications is attempted. The effect of the disjunction
between xylems of adventitious roots and stems, providing a physiologically demonstrated valve ("rectifier") effect is discussed. "Ecological iteration" has occurred in
some monocot lineages, so that early-departing branches in some cases may have
more "specialized" xylem because of entry into xeric habitats, whereas nearby crown
groups, which may have retained "primitive" xylem, probably represent long occupation of mesic habitats. Cheadle's use of xylem for "negations" of phyletic pathways
can no longer be accepted. Symplesiomorphic mesomorphic xylem patterns do
characterize many of the earlier-departing branches in the monocots as a whole,
however. Cheadle's idea that monocots and non-monocot angiosperms attained
Author's personal copy
88
S. Carlquist
vessels independently is improbable in the light of molecular trees for angiosperms.
Vessels in roots seem an adaptation to major swings in moisture availability to
adventitious roots as compared to taproots. The commonness of all-tracheid plans
in stems and leaves in earlier-departing monocot clades is a feature that requires
further clarification but is primarily related to the xylem disjunction that adventitious
roots have. Secondary vessellessness or something very close to it can be hypothesized for Campynemataceae, Philesiaceae, Taccaceae, and some Orchidaceae. Eleven
salient shifts in our conceptual views of monocot xylem are proposed and conclude
the paper. Monocot xylem is not a collection of historical information, but a rigorously parsimonious system related to contemporary habits and habitats.
Keywords Ecological plant anatomy . Heterochrony . Microstructure . Monocot
cambium . Neotracheids . Vessellessness . Xylem evolution
Introduction
Evolutionary concepts in plant anatomy are limited by the fields of knowledge
available and taken into account. Certainly we have good descriptive accounts of
monocot anatomy in general, based mostly on light microscopy, from the Anatomy of
Monocotyledons series begun by C. R. Metcalfe (1960), and now extended by the
work of others (e.g., Tomlinson, 1961, 1969, 1983). Cheadle's work on monocots,
begun as data summaries (Cheadle, 1942, 1943a, b), was extended, with the collaboration of Hatsume Kosakai (e.g., Cheadle & Kosakai, 1971) to provide family by
family examinations of xylem. The end walls and lateral wall pitting of vessels are the
focuses of the Cheadle and Kosakai work. Work on monocot xylem has been
organized on the basis of systematic groupings, which is ideal for data retrieval
(e.g., Wagner, 1977). There is an implication, begun in the nineteenth century by
the work of Solereder, that anatomy will yield data useful for the construction of a
natural system.
Cheadle (1942) also offers some gradate phylogenetic progressions, based mostly
on the end walls of vessel elements: long scalariform perforation plates are considered indicative of "primitive" conditions, simple perforation plates are considered at
the opposite extreme, indicators of specialization. The organographic distribution of
vessels and their specialization levels were traced by Cheadle and associates. Cheadle's central phylogenetic thesis is that vessels originated in the roots of monocotyledons and advanced upward during evolution into stems, inflorescence axes, and
finally leaves (Cheadle, 1942). He also found (1943a, 1943b), not surprisingly, a
similar organographic sequence in vessel specialization (many bars to few to none on
perforation plates). He envisioned a sort of inexorable trend which could be tracked
by means of specialization index numbers. Cheadle's concepts, however, prove to be
rather more problematic than has been realized, for reasons that will be presented
below.
There are five main sources of new information that now change our ideas on how
monocot xylem evolved. The first of these is the construction of molecular trees.
Although certainly topologies of these trees are not certain, they have reached
sufficient stability and have sufficient levels of likelihood that they must be used as
Author's personal copy
Monocot Xylem Revisited
89
the framework on which we judge ideas of xylem evolution. Prior to Chase et al.
(1993), a natural system for the angiosperms was a goal that could only be dimly
reached, because anatomy and other indicators do not, as we see in retrospect, form
coherent and clearly directional patterns. The ideas of symplesiomorphy, apomorphy,
and homoplasy were not features of earlier attempts at a natural system: lists of
resemblances were the tool employed, and relationship was judged on the basis on
numbers of similarities rather than what character states they represented. The
taxonomic groups chosen for comparison sometimes did not even include the groups
that now prove, in the light of molecular phylogeny, to be most closely related. In any
case, molecular trees now drive the interpretation of xylem evolution, and xylem
configuration is no longer a tool in the construction of natural systems, although
distinctions of systematic value can still be yielded by xylem.
The second factor that has changed is the widespread use of scanning
electron microscopy (SEM). Until recently, use of SEM in studies of monocot
xylem was occasional, rather than frequent. SEM proves essential in revealing
the occurrence of pit membranes in end walls of tracheary elements, thereby
showing that such elements probably should be called tracheids, rather than
vessel elements. The production of porose or reticulate pit membranes in these
end wall pits, however, has implications not so much for terminology as for the
conductive physiology of the xylem. SEM studies, by showing that what
hitherto had been regarded as vessel elements are physiologically definable as
tracheids invite comparisons with systematics, organography, and ecology, and
give us a new understanding of monocot xylem evolution. SEM studies have
been changing in methodology (Carlquist & Schneider, 2006), and thickness of
pit membranes is now a concern (Jansen et al., 2009).
Earlier students of monocot xylem developed ideas on monocot xylem evolution
with little reference to ecology. Xylem is quite often a design for dealing with
ecological regimens (Carlquist, 1975). There are multiple plant designs within a
given habitat, but each design can be closely cued to xylem function. Ecological
information may seem imprecise or highly complex and not capable of analysis by
someone interested primarily in xylem, but knowledge of a plant's habitat can point
the way to development of focused physiological information. Two families that lie
next to each other in phylogenetic trees of monocots, Boryaceae and Asteliaceae,
have notably different xylem configurations (Carlquist et al., 2008; Carlquist &
Schneider, 2010b). Without knowing that Borya is a "resurrection plant" that grows
on briefly moist granite shelves, one would be unable to understand the distinctive
vessels and tracheids in its stems. The "primitive" xylem of Astelia, which lacks
vessels in stems and leaves but has, in its roots, variously tracheid-like vessels, could
not be understood without reference to its highly mesic habitat (often an understory
element in cloud forests).
Likewise, habit plays an important role in xylem configuration in monocots. We
cannot meaningfully understand why Petrosaviaceae and Triuridaceae lack vessels
throughout the plant until we realize that the two families have probably lost vessels
independently in response to the heteromycotrophic habit. Lack of vessels in shoots
of epiphytic orchids and epiphytic bromeliads relates to the habit, but the differences
in the epiphytic habits of the two groups must be taken into account. The succulence
of orchids and the tank habit of bromeliads are distinctive adaptations. Vessel
Author's personal copy
90
S. Carlquist
diameter in palms relates to whether a species is rhizomatous, erect, or climbing
(Klotz, 1977), not to its phylogenetic position within the family Arecaceae.
Ultimately, adaptations in xylem must be determined on the basis of physiological
function. Compendia that provide tests of physiological functions (e.g., Zimmermann,
1983; Tyree & Zimmermann, 2002) cannot always be detailed on the anatomy of the
plants they study, although plant physiologists are increasingly paying attention to
xylem anatomy. Plant physiologists have shown that high root pressure can provide
one explanation for the arboreal habit of palms (Davis, 1961) and other monocots
(Fisher et al., 1997a, b), and that the valve-like nature of the juncture between stems
and adventitious roots in Agave explains how Agave can occupy desert habitats
(Ewers et al., 1992). Woody plants are generally easier experimental subjects, so
we know much more about the conductive process in non-monocot woody angiosperms than in monocots. Therefore, the discussions of conductive physiology below
are less intensive that one could wish. The interesting data that do exist provide
motivation for expansion of our knowledge of monocot physiology.
The questions that can now be answered (albeit in a preliminary fashion in some
cases) validate the use of a multiple-prong approach to study of monocot xylem. Among
these questions discussed in this paper are the following. Were the ancestors to the
monocots aquatic? Were the ancestors of the monocots vesselless? What are the
advantages and limitations of sympodial stems with adventitious roots, and what role
does xylem play in the root/stem juncture? Is monocot xylem constructed for conductive
safety or conductive efficiency, or both (and in which species)? What are the advantages
of a vesselless stem and leaf xylem, as in so many monocots? What are the special
anatomical features of palms and how do they vary with habit and habitat? How do nonpalm arboreal monocots overcome the limitations of lack of a vascular cambium? What
are the advantages and disadvantages of the "monocot cambium" and which genera have
this kind of lateral meristem? Is progression towards greater vessel "specialization"
always progressive, as Cheadle claimed, or can there be reversions, and how can they
occur? What restructuring of our ideas on monocot xylem evolution is necessary in the
light of molecular phylogenies? What does SEM tell us about vessel elements and
tracheids in monocots, and how does that change our concept of what vessel elements
are and how they work? What is the syndrome of features associated with the scalariform pitting pattern of tracheary elements? Did vessels originate independently in
monocots and dicots? Which basal angiosperms are closest to the ancestral monocots,
and what symplesiomorphies might they share? Why do some early-departing clades
have more "specialized" xylem than "crown groups"?
Obviously, not all of these questions can be brought to a satisfactory resolution at
the present moment. However, original data and synthesis between available information of knowledge from other fields bring us to a new level of conceptual
awareness. Although there is much work about monocots recently published, the
absence of work on xylem is notable. In fact, data concerning xylem can play a key
role in our understanding of the monocots. Although once comparative anatomical
data were regarded as elements from which a fallible natural system would slowly be
built, the development of molecular systematics has reversed that procedure. DNAbased trees have such high degrees of probability compared to the earlier intuitive
natural systems that the newer trees become the framework and testing apparatus for
our ideas on how xylem evolves.
Author's personal copy
Monocot Xylem Revisited
91
Historical Perspective
The first significant contribution to understanding of xylem evolution was that of
Bailey and Tupper (1918), who hypothesized a phyletic shortening of fusiform
cambial initials. They did not include monocots in their data or in their conclusions,
presumably because monocots have no cambium. The Bailey and Tupper (1918)
concept was developed in the absence of a reliable phylogenetic tree of the angiosperms, a fact that Bailey (1944) considered a strength of his scheme because it was
not dependent on any outside data set. However, Bailey implicitly was aware, by
comparing tracheary element length in wood angiosperms with that of gymnosperms
and certain fossil groups, that phylogenetic comparison was in some way involved.
Lacking any clear phylogenetic tree of woody plants, Bailey and Tupper resorted to a
system of inexorable phylogenetic progression stages in xylem, from primitive to
specialized.
Bailey soon developed the idea of tracheary element length as a kind of phyletic
measuring stick usable for ranking degree of evolutionary departure from primitive
character expressions. He soon realized that other characters could be used as phyletic
indicators, since he sensed a statistical association among them (Bailey & Tupper,
1918, Table VI). Bailey recognized four categories, based on perforation plate
morphology and tracheary element pitting (scalariform perforation plates and bordered pits in tracheary elements defined the ancestral conditions). Bailey handed off
the task of elucidating stages in vessel evolution to Frost (1930a, b, 1931). All of
these studies were based on non-monocot woody angiosperms. Bailey handed the
task of elucidating ray parenchyma and axial parenchyma character state change to
Kribs (1935, 1937). Because the symplesiomorphic conditions of all of these were
considered statistically linked, Bailey and his co-workers considered that any one of
the symplesiomorphic character states (e.g., diffuse axial parenchyma, more numerous bars per perforation plate) could be substituted for vessel element length as a
"measuring stick" for phyletic advancement. The quantitative nature of vessel element length as a character made it an appealing first choice as a phyletic indicator,
however.
I. W. Bailey's knowledge of non-monocot woods was much more extensive than
his understanding of monocot xylem, owing to his forestry background. Bailey
handed to Vernon Cheadle the task of determining phyletic trends in monocot xylem.
At that time, the data base on monocot xylem was small (e.g., Solereder & Meyer,
1930), probably because the xylem of monocots does not have the commercial
importance that angiosperm wood has. Cheadle's five levels of advancement were
based mostly on perforation plate morphology. These categories were much like the
four categories of Bailey and Tupper (1918, Table VI), differing only in that Bailey
and Tupper did not include an all-tracheid condition as Cheadle did. Bailey (1944)
was certainly of the opinion that an all-tracheid (homoxylous) wood was ancestral in
angiosperms.
Cheadle's groupings, recognized from 1942 onward and even recently (e.g.,
Thorsch, 2000) were:
0 Tracheids only
1 Vessels with exclusively scalariform perforation plates
Author's personal copy
92
2
3
4
5
S. Carlquist
Vessels with
Vessels with
Vessels with
Vessels with
mostly scalariform perforation plates (a few simple plates present)
scalariform and simple perforation plates about equally common
mostly simple perforation plates
exclusively simple perforation plates
Any species or plant portion could be "scored" on this basis, and the scores
averaged for families as a whole, so that families could be compared in terms
of departure from a hypothetical ancestral condition (0). Protoxylem, early
metaxylem, and late metaxylem could also be given separate scores on this
basis. One notes that of all the vessel characters given phylogenetic status by
Frost (1930a, b, 1931) for woody angiosperms, Cheadle effectively used only
perforation plate morphology as the feature in monocots to be considered in detail
and consistently in any species or family.
Cheadle's conclusions were stated in a series of principles or dicta, beginning with
his first paper comparing a spectrum of monocots (Cheadle, 1942), and stated
unchanged years later (Cheadle & Tucker, 1961). These dicta are:
(1) There has been specialization in monocot vessels in the order listed in the above
(0–5) scheme.
(2) The organographic specialization of vessels has proceeded progressively from
roots (most specialized type of vessels in any given monocot)) to stems,
inflorescence axes, and leaves in that order. A few deviations in this sequence
(e.g., Dracaena) were noted by Cheadle (1942, 1943a, b).
(3) In any given organ of a vessel-bearing monocot, metaxylem vessels show more
"specialization" than those in protoxylem, and late metaxylem is more specialized than early metaxylem.
(4) Longer vessel elements are more "primitive" than shorter vessel elements in
monocots. Cheadle stated this principle in his early work (1943a) and retained
the idea (Cheadle & Tucker, 1961).
(5) The above trends are held by Cheadle and co-workers to be irreversible.
(6) A monocot group (i.e., family, genus) with more specialized xylem cannot have
given rise to a group with less specialized xylem.
(7) Origin of vessels in monocotyledons and in non-monocot angiosperms ("dicotyledons") was independent (Cheadle, 1953).
The above principles are reviewed in the text of the present paper. Cheadle, who
died in 1996, did not live to see the enormous impacts that global molecular-based
trees of angiosperms (e.g., Chase et al., 1993; Soltis et al., 2000) would have on
structural botany. Although Cheadle could not foresee those changes, he did not
pursue correlations between structure, physiology, and ecology which were available
to him. He and his co-workers worked almost exclusively with light microscopy.
Thus, the present account attempts not only to present new and original knowledge of
monocot xylem microstructure based on SEM studies, but to synthesize the knowledge gained with light microscopy with information from other fields in an effort to
present new ideas of how monocot xylem has evolved. Instead of imposing a scaffold
of generalized Baileyan ideas, we must now go in an entirely different direction and
use molecular trees as frameworks for organizing xylem patterns, and interpret those
patterns in terms of ecology, physiology, and habit.
Author's personal copy
Monocot Xylem Revisited
93
Materials, Methods, Procedures
The majority of the photographs presented here have not been previously published.
Citations in captions document those that have previously appeared in papers.
Collection data is cited in captions for figures. Authors of binomials are given in
either in captions or in the running text.
The method mostly employed for SEM photographs newly presented here is that
described for Orchidaceae (Carlquist & Schneider, 2006). Thick sections of roots,
stems, inflorescence axes, and leaves were prepared for SEM study. Thin sections,
such as those produced by rotary microtome, prove unsatisfactory because they
present limited portions of perforations plates, etc., whereas thick sections can capture
the entirety of a perforation plate. In addition, thick sections reveal cell contexts of
xylem and the three-dimensional shapes of vessel elements much better than thin
sections do. Thick sections also have the advantage of minimizing torsion, which
would damage delicate walls, during the handling process. Sections that show end
walls of tracheary elements from the inside of an element are more likely to represent
unaltered conditions, and are much preferable to sections that show outside of end
walls, which have been subject to scraping away of the primary wall by the sectioning
process.
Maceration was the technique typically used by Cheadle and associates for study
of monocot vessels. It has been used here in a several cases (a few Asteliaceae,
Boryaceae, Orchidaceae, and Taccaceae). Maceration is excellent for revealing cell
shape and dimensions with light microscopy. Probably Cheadle, having begun with
this method, continued it in order to provide data comparable to those he acquired
earlier. Macerated cells can also be studied with SEM, and in some families such as
Araceae (Carlquist & Schneider, 1998; Schneider & Carlquist, 1998) primary and
secondary walls seem relatively unaffected by the maceration process. However,
primary walls may experience degradation if the maceration process is prolonged,
as is required by material of some other families. Longer maceration times are often
necessary with Jeffrey's fluid or any other oxidative reagent capable of dissolving
middle lamellae and thereby separating cells. Longer macerating times may be
necessary when vascular bundles are sheathed with fibers that separate from each
other tardily. Numerous primary wall details have been observed only since Edward
L. Schneider and I began using SEM in conjunction with thick sections (Carlquist &
Schneider, 2006). Especially important in this regard are the primary walls in pits of
end walls of tracheary elements. These are delicate, and can be preserved with
reasonable certainty only by means of methods that involve no oxidative or acidic
reagents. Materials from macerations are deliberately illustrated here to contrast their
probable degrees of loss of pit membrane portions with the appearances obtained
from sections of alcohol-fixed material.
Materials to be studied were fixed in 50 % aqueous ethanol. Sections (about 1–2 mm
in thickness) were cut manually with a single-edged razor blade. Sections were then
subjected to three changes of distilled water at 50 °C in order to remove extraneous
substances. Sections were then placed between pairs of glass slides and pressure applied
with a clip in order to assure flatness of the dried section. Drying was accomplished by
placing the glass slides so assembled on a warming table at 50 °C until drying has
occurred. Dried sections were then examined according to the usual techniques.
Author's personal copy
94
S. Carlquist
The thick sections offer the advantage not merely of revealing large portions of or
the entirety of a perforation plate, but in being able to reveal it as seen from the inside
of a cell, or in the form of oblique sections. These views reveal with greater certainty
the presence of pit membranes in end walls of tracheary element. Some perforation
plates may be separated by the sectioning process into halves representing the two
component cells, but such split or scraped perforation plates reveal portions of the
primary wall to various degrees, and are. Sections that reveal intact perforations (as
opposed to split) perforation plates are the most valuable because they show, relatively free from artifacts, what the conductive stream in xylem encounters when
traversing an end wall. Intact perforation plates are visible, from the inside of a vessel
element, and thus a longisection that exposes the lumen is required.
New Data, New Contexts
What is a Vessel?
Anatomical Considerations
Vessel elements are defined on the basis of presence of perforation plates on end
walls, composed of one or more perforations. This classical definition is, ironically, a
statement of what is not present: primary walls are absent in the perforations. But is
our knowledge of this reliable? The definition is based on light microscopy, which in
the case of macerated cells (or perforations plates as seen in face view in sections)
rarely can show presence of pit membranes in the perforations, even with particular
staining methods. The inference of absence of pit membranes in these cases has been
made on the basis that perforations are larger than the pits on lateral walls of a
particular vessel element (Fig. 1a, b; Fig. 4f). If the perforations are larger, and a
perforation plate can thereby be declared to be present, the absence of pit membranes
can be inferred with reasonable certainty (but pit membrane remnants may be present
in some scalariform perforation plates: viz, Carlquist, 1992a). The oversimplified
drawings of Kosakai (e.g., Cheadle & Kosakai, 1971) tend to suggest that perforation
plates can be delimited clearly. When long scalariform perforation plates are examined with SEM, however, the distinctions between end walls and lateral walls may
prove elusive.
Interestingly, in one supposed vessel element (Anigozanthos rufus Labill., Haemodoraceae), Cheadle (1968) superimposed a pattern on the perforation plate, indicating his uncertainty that pit membranes actually were lacking. This indication is,
however, a unique instance. Uncertainty about whether a tracheary element is actually
a vessel element or a tracheid led Fahn (1954), who used light microscopy, and
Wagner (1977) to employ the term "vessel tracheid" to call attention to apparent
intermediacy. This usage calls attention to the problem, but does not add new
information. The term is also misleading, because vessel element, not vessel, would
be the counterpart to tracheid. The nature of instances of apparent intermediacy could
not be elucidated in the era when light microscopy was the sole tool for viewing
xylem. Pit membranes in Astelia (Fig. 1c–g) demonstrated with SEM cannot be seen
with light microscopy. Transmission electron microscopy is also a valid tool for
Author's personal copy
Monocot Xylem Revisited
95
Fig. 1 SEM micrographs of tracheary elements from roots (a–e) and stems (f–g) of Astelia (Asteliaceae).
a, b. A. chathamica (Skottsb.) L. B. Moore. Perforation plates from macerations. a. membrane remnants are
absent. b. Perforations are wider, separated by narrower bars, than are the lateral wall pits (upper right). c.
A. menziesiana Sm.. End wall of tracheary element from section, showing variously porose membranes in
the pits (or perforations), viewed from inside of tracheary element. d. A. chathamica tracheary element end
wall from section, showing intact pit membranes in the end wall pits. e. A. argyrocoma A. Heller, oblique
view of end wall from section, part of the end wall sectioned away. Pit membranes are present. f. A.
chathamica. Tracheary element end wall (right) and lateral wall (left) portions; threadlike pit membrane
remnants are present in end wall. g. A. menziesiana, portion of end wall from section, viewed from outer
surface of tracheary element; less wall material is scraped away at top and bottom than in the middle two
pits. Collection data given in Carlquist and Schneider (2010b)
revealing presence of pit membranes in tracheary elements, but it has been used only
rarely in monocots (e.g., Thorsch, 2000), probably because lack of commercial
importance of monocot xylem. SEM has also been relatively little used to date in
the study of monocot xylem.
Cheadle (1942) referred to passage of India ink particles through perforation plates
of monocots as a criterion for discrimination between vessel elements and tracheids.
By doing this, Cheadle implicitly recognized that pit membranes in some form might
be present in "perforations." India ink particles are about 1 μm in diameter. By
Author's personal copy
96
S. Carlquist
extension, one could also use colloidal latex microspheres, which are now commercially available in uniform-diameter populations. Such microspheres would best be
detected by study of vessels with SEM after the latex had been taken up by a plant or
injected—a complicated and prolonged procedure. We now know that size of porosities with end-wall pit membranes varies considerably (e.g., Fig. 3). What is the
porosity size that relates to a physiological distinction? Passage or non-passage of air
bubbles within a transpiration stream might represent an example of such a
distinction.
Fahn (1954) rejected the passage of India ink particles through a perforation plate
as an aid in deciding whether a cell is a vessel element or a tracheid. Instead, he
entertained the idea that by pressing a needle on a cover slip of a maceration
preparation, one can perform a test. If this action displaces some of the bars, he
believes that no pit membranes interconnect the bars; if the action results in equal
spacing of the bars, he thought that lack of pit membranes was indicated. This test
may have been appropriate in its time, but it has been supplanted by SEM studies.
Some large monocot families have long scalariform end walls on tracheary
elements (Bromeliaceae, Orchidaceae, and Pandanaceae, for example). In these
families, SEM is the only reliable method to decide both whether pit membranes
are present in end wall pits and what the membrane microstructure is (porous,
reticulate, etc.). Thus, the only secure method for deciding whether tracheary elements or vessel elements are present in particular species becomes an elaborate
procedure, available to few. This will appeal to some workers as an untenable
situation in terms of terminology, but development of mutually exclusive terms is
not a realistic or even desirable goal in this instance. Instead, demonstration of the
structural continuum and thereby the evolutionary and physiological status of tracheary elements in monocots becomes a much more important goal. Fahn (1954) offers
the term "vessel tracheid" for intermediate tracheary elements. Such a proposal may
well be a better choice that attempting to reinstate definitions that had their origin in
light microscopy and are not applicable when microstructure is taken into account.
Astelia (Asteliaceae, formerly a subfamily of Liliaceae) has been regarded as
having vessels only in roots (Cheadle & Kosakai, 1971). On the basis of Fig. 1a
and b, one could judge vessel elements to indeed be present. However, these two
figures are based upon macerations, and delicate primary wall material might have
been removed from the perforation plates by that process. One can find, within a
single root, perforation plates that vary in terms of presence and size of porosities in
the pit membranes or pit membrane remnants of perforations (Fig. 1a–e). In Fig. 1d
and e, the end wall membranes are entirely intact. Possibly these could be immature,
but they were not taken from apical portions of the roots, and such plates may be
found here and there in Astelia root xylem. Figure 1a–e all show narrow bars
characteristic of perforation plates.
End walls in stem tracheary elements of Astelia show little difference between end
walls and lateral walls in the secondary wall patterns that delimit pits. There are,
however, threadlike remnants of primary wall material to a greater (Fig. 1f) or lesser
(Fig. 1g) extent.
Can pit membranes be either present or absent within a given root portion of
Astelia? Presumably so, although some caution should be observed. The perforations
of Fig. 1a–b are from macerations, and the oxidative properties of macerating fluid
Author's personal copy
Monocot Xylem Revisited
97
can result in loss of primary wall material not only from end walls, but from lateral
wall pits as well (see Fig. 5a–d). This happens when xylem is enclosed within fibers,
because the prolonged treatment needed to macerate the fibers also can damage
primary walls of xylem elements.
The possibility remains that tracheid-like vessels can be intermixed with vessels
with perforations lacking pit membranes. SEM study of sectioned material is ideal at
revealing pit membranes in perforation plates, but it can sample only a small number
of perforation plates, leaving uncertain what a large population of vessel elements
might show. Sections in which one can view perforation plates from the inside of a
tracheary element (Fig. 1c) are ideal. Of equal value are oblique sections of end walls
(Fig. 1f: compare the threads of the perforation plate at right to the solid sheets of wall
material to the left).
Frequently in sectioning, tracheary elements are split apart, rather than
sectioned down through a lumen. This may result in "scrape away" effects, in
which various amounts of primary wall material are removed, depending on
how deeply the blade edge cuts into any given pit membrane. Cellulosic fibrils
are often revealed well (Fig. 1g), but one is uncertain how much wall material has
been removed. For accurate information about intact pit membranes, views from the
lumen sides of tracheary elements or oblique sections of end walls are much more
reliable.
Given these considerations, natural patterns of pit membrane retention can differ
from one monocot to another. The inflorescence axis of Canna (Fig. 2a–e) represents
conditions somewhat different from those of Astelia. The perforation plate of Fig. 2a
is viewed from the inside of the tracheary element, and has not been affected by the
sectioning process. Rather coarse microfibrillar pit membrane remnants are present.
In Fig. 2b, the wall between two adjacent vessel elements has been split, indicating
that the fibrils belong not just to one of the two adjacent tracheary elements, but to
both, as one would expect. Figure 2c–e are sections that show most of the fibrils in a
perforation (or pit) of end walls. The fibrils are intercontinuous from one perforation
to another (Fig. 1d). Larger holes in the network (Fig. 1c, e) may be indicative of
removal of a few strands by sectioning.
In the root perforation plate of Canna, no primary wall material is present in most
of the perforations (Fig. 2f, far right), although pits transitional between lateral wall
pitting and perforation plates (Fig. 2f, bottom center) may retain pit membranes
(which are fractured in this micrograph, the fracturing presumably an artifact).
Scalariform perforation plates are not perfectly delimited from lateral wall pitting,
although drawings of perforation plates often suggest that they are.
Orchidaceae offer additional examples of transitions between vessel elements and
tracheids. In Phalaenopsis (Fig. 2a–d), one can se a progressively diminished degree
of poroussness of end wall pit membranes, beginning with roots (Fig. 3a), then stems
(Fig. 3b), and finally inflorescence axes (Fig. 3c). Lateral walls of vessels (or vessellike tracheids) in Phalaenopsis (Fig. 3d) show no pores in the pit membranes. Roots
of Vanilla have only small pores in pit membranes (Fig. 3e: the fracturing should be
disregarded). Vessels illustrated for Stenoglossa (Fig. 3f) are from sectioned material,
and this appearance, common in sectioned material, must be considered in the light of
the "scrape away" effect (for an example of this in woody material, see Jansen et al.,
2009, Fig. 2).
Author's personal copy
98
S. Carlquist
Fig. 2 SEM micrographs of tracheary elements portions from sections of inflorescence axes (a–e) and
roots (f) of Canna indica L.. a. Portions of two pits (or perforations) of an end wall as seen from the inside
of the element; longitudinally-oriented strands of pit membrane remnants are present. b. Portions of end
walls from two adjacent tracheary elements, torn apart by the sectioning process, to show the presence of pit
membrane remnants in pits of both of the two cells; not contrast with the lateral walls (at left, and at above
right) in which pit membranes are laminar. c. Outer surface of end wall, the adjacent tracheary element
removed by sectioning; the longitudinal strands have been retained in this portion. d. An end wall (similar
to that of c) at higher magnification, to show that the pit membrane strands extend from one pit to another,
and are not separated from each other by a primary wall with a different texture. e. Two pits from a
tracheary element end wall, showing pit membrane remnants that form reticulate rather than longitudinallyoriented portions. f. Portion of a vessel from a root. In the upper half are lateral wall pits with intact pit
membranes. In the lower half are pits (delicate pit membranes torn) that are transitional to a perforation plate
(which would be at right), showing degrees of transition. Further data in Carlquist and Schneider (2010a)
Epidendrum roots (Fig. 4a–c) have abundant longitudinally-oriented strands in
perforations. Stems from the same Epidendrum plant (Fig. 4d–e) have more nearly
intact but prose membranes. In Odontoglossum (Fig. 4f), one can see a "classical"
perforation plate, although some pit membrane remnants might have been removed
Author's personal copy
Monocot Xylem Revisited
99
Fig. 3 SEM micrographs of portions of tracheary elements of Orchidaceae, from sections. a–d, Phalaenopsis amabilis Blume. a. End wall from root, as seen from inside the tracheary element. Porose pit
membranes are present. b. End wall from stem, a portion split away from an adjacent tracheary element by
the sectioning. Pit membranes are less porose than those in a. c. End wall from inflorescence axis, seen from
inside the tracheary element. Pores on pit membranes are mostly small and inconspicuous. d. Lateral wall
from inflorescence axis; pit membranes are non-porose (fracture in one of the pit membranes is an artifact).
e. Vanilla fragrans (Salisb.) Ames, end wall of tracheary element from root, seen from inside. Porose pit
membranes are present, but are fractured by handling. f. Stenoglossa longifolia Hook f., portion of end wall
of stem tracheary element, separated from adjacent tracheary element by sectioning; various degrees of
porousness represent a "scrape away" effect, with the larger holes representing greater removal of primary
wall material by the sectioning process. Collection data in Carlquist & Schneider (2006)
by the macerating process. Sections of Odontoglossum stems (Fig. 4g) have pores in
pit membranes only where pit membranes are scraped away by the sectioning
process; the pit membranes are otherwise intact.
By contrast, roots of Orchidaceae subfamily Apostasioideae (sometimes cited as
Apostasiaceae) can have circular perforation plates that do not occupy the entirety of
an end wall (Fig. 5b–c). Tracheids may also be encountered (Fig. 5a). There is little
Author's personal copy
100
S. Carlquist
Fig. 4 SEM micrographs of end walls tracheary elements of Orchidaceae. a–e. Epidendrum radicans Pav.
ex Lindl. a–c. Sections of tracheary elements from roots. a. View from inside element, showing
longitudinally-oriented pit membrane remnant strands. b. View of a "perforation" from inside the tracheary
element; the pit membrane remnants are intermediate between linear and reticulate. c. Oblique view of
"perforation" showing pit membrane remnant threads. d–e. Sections of tracheary elements from stems. d.
An end wall in which more pit membrane material has been retained (above) but some has been scraped
away (below) by the sectioning process. e. An end wall in which sectioning has resulted in extensive
scraping away of pit membranes, the pit membranes thus fragmentary instead of intact, as they are in, for
example, a–b. e–f. Odontoglossum grande Lindl. e. Perforation plate from maceration of root; pit
membrane remnants have very likely been removed by the macerating process. f. End wall of tracheary
element from section of stem, showing small and inconspicuous pores in pit membranes. Collection data in
Carlquist and Schneider (2006)
difference between roots and stems with respect to tracheary end wall structure. One
must remember, however, as noted by Wagner (1977), that little of the family has
been sampled.
Ophiopogon (Asparagaceae, subfamily Dracaenoideae) roots sometimes have only
a small number of pores in tracheary element end wall pit membranes (Fig. 5e, f).
Author's personal copy
Monocot Xylem Revisited
101
Fig. 5 a–d. SEM micrographs of end walls of tracheary elements of Apostasia roots (a–b) and Neuwiedia
stems (c–d), genera of apostasioid Orchidaceae. Preparations are from macerations, and are thus lacking in
pit membranes in lateral walls. a. Tracheary element with no perforation plate at end. b. Oval perforation
plate and end of a vessel element. c. Pair of tracheary elements separating due to maceration; the central
oval perforation plate occupies part of the end wall, but smaller pits surround it on each cell. d. isolated
vessel element tip, showing the oval simple perforation plate that occupies a central place on, but not the
entirety of, the end wall. Collection data located in Judd et al. (1993). e–f. End wall portions of tracheary
elements of roots of Ophiopogon jabaran Lodd. (dracaenoid Asparagaceae). d. Longisection of end wall
showing displacement of some bars, with consequent tearing.. e. Longisection of end wall, bars intact; pit
membranes are laminar with only a few small pores in central portions. (cultivated, Lotusland Horticultural
Foundation)
This is true whether the end wall has experienced some sectioning (Fig. 5e) or is
intact (Fig. 5f).
Narrow tracheary elements of Typha (Typhaceae) roots should be called tracheids
because they retain a primary wall meshwork in the end wall pits (Fig. 6a–b, e–f).
Wider tracheary elements of Typha roots (Fig. 6c–d) can be called vessel elements
Author's personal copy
102
S. Carlquist
Fig. 6 SEM micrographs of sections of tracheary elements in roots (a–e) and stems (f) of Typha
angustifolia L. (Las Positas Road at Elings Park, Santa Barbara, CA). All of these are views from the
inside of an element, and thus are maximally intact (compared to an element cut away from neighboring
cells). a. Portion of early metaxylem tracheary element, the end wall cut lengthwise. b. Enlarged portion of
a section of early metaxylem tracheary element, to show microfibrillar webs in the "perforations." c. About
half of a late metaxylem vessel element (tip at left), to show nature of perforation plate. d. Perforations (plus
two lateral wall pits, upper left) of a late metaxylem vessel; a few pit membrane shreds are present in the
perforations. e. Metaxylem end wall with microfibrillar reticulum in the pits, with comparison to lateral
wall pits (bottom), which have solid pit membranes. f. End wall of a stem tracheary element, showing dense
microfibrillar webs in the pits
because the end walls lack pit membranes in most perforations. At the end of the
perforation plate (Fig. 6c–d) where there is a transition to lateral wall pitting, pit
membrane remnants are present to various degrees, however. In stems of Typha, end
walls of tracheary elements have reticulate pit membranes (Fig. 6e–f). This contradicts the data of Cheadle (1942) and Wagner (1977) to the effect that vessels occur
throughout the plant in Typhaceae.
Author's personal copy
Monocot Xylem Revisited
103
Similar considerations apply to Cyclanthaceae (Fig. 7a–c) and Pandanaceae
(Fig. 7d–i), families that apparently are closely related to each other (Chase, 2004)
In Carludovica of the Cyclanthaceae, roots have long vessels with many-barred
scalariform perforation plates (Fig. 7a, b). In these, perforations can be said to be
Fig. 7 SEM photomicrographs of sections of tracheary elements from Cyclanthaceae (a–c) and Pandanaceae (d–i). a–c. Carludovica palmata Griseb.(David Lorence 10224, NTBG), longisections of roots. a. The
end wall of a probable vessel element, above, and part of such an end wall, below. b. Perforations lacking
pit membranes, seen from inside a tracheary element. b. Portion of a perforation, seen from outer surface of
a tracheary element, that has a porose pit membrane. d–g. Freycinetia novocaledonica Warb.(David
Lorence 10223, NTBG). d–e. Longisections from roots. d, A perforation plate, showing the numerous
bars. e. Ends of some perforations; seen from inside a tracheary element; pit membrane remnants are
lacking. f–g. Portions of pits from end walls of stem tracheary elements. f. Oblique view, parts of bars cut
away; reticulate networks present. g. Portions of two perforations, seen from inside the tracheary element;
pit membranes are meshlike to laminar and porose. h–i. Pandanus amaryllifolius Roxb.(David Lorence
10222, NTBG), pits from end walls of longisections of stem tracheary elements, seen from inside the
tracheary element. h. Variously porose pit membranes. i. Networklike pit membrane
Author's personal copy
104
S. Carlquist
present on the basis that most of their area is devoid of pit membranes, but pit
membrane remnants can be found at the lateral ends of perforation plates (Fig. 7c).
Wagner (1977) records vessel presence in roots of Cyclanthaceae, but only tracheids
in stems. That view can be maintained on the basis of the present study (if one takes
the viewpoint that a reticulate pit membrane characterizes a vessel element rather than
a tracheid).
The pattern seen in Typha is present in Freycinetia of the Pandanaceae also. Roots
of Freycinetia have long scalariform perforation plates (Fig. 7d) with some pit
membrane remnants at lateral ends of perforations (e.g., Fig. 7e, extreme left). In
stems of the same Freycinetia, there are clearly porose pit membranes in end walls of
tracheary elements, whether seen where an adjacent vessel has been sectioned away
(Fig. 7f) or whether one is seeing an intact pit membrane from the inside of a
tracheary element (Fig. 7g). This is also true of a stem of Pandanus studied
(Fig. 7h–i). Cheadle (1942) and Wagner (1977) claim presence of vessels throughout
the plant in Pandanaceae, but that is not confirmed on the basis of the present SEM
studies.
Lapageria (Philesiaceae) adds further dimensions to this pattern. SEM micrographs reveal that in the roots of Lapageria, pit membranes are present in presumptive end walls of tracheary elements, whether viewed from inside of the element or
from the outside surfaces in which adjacent tracheary elements have been sectioned
away (Fig. 8a–b). The pattern of the pit membranes in Fig. 8a–b) suggests a dense
reticulum, with some pores present. The number of bars on the end walls of
Lapageria root tracheary elements is quite high (150–700 according to Fahn, 1954,
who calls the elements "vessel tracheids"). Loss of pit membranes in such narrow pits
of an end wall is highly improbable, based on SEM studies of such long plates.
Consequently, end walls of Lapageria are virtually indistinguishable from lateral
walls in terms of pit morphology. The criterion for identifying end walls used in the
SEM studies reported here is that end walls traverse an element diagonally as seen in
a longitudinal section. On the basis of the present study, Lapageria can be called a
non-aquatic vesselless angiosperm (it grows in moist forests, but in soil that is never
inundated).
Roots of Taccaceae have very long perforation plates. Fahn (1954) reports 30–200
bars on end walls of "vessel tracheids" of roots of Schizocapsa plantaginea Hance,
80–100 on those of Tacca paxiana W. Limpricht, and 90–300 on those of T. palmata
Blume. I have found about 40–100 bars on root tracheary element end walls of T.
leontopetaloides (Fig. 8c) and T. chantrieri André, and at least 200 on those of T.
integrifolia W. M. Curtis (original data). Such a large number of bars, combined with
such narrow perforations, is incompatible with complete hydrolysis of pit membranes
from the end wall pits, so various kinds of pit membrane remnants occur. Material of
T. leontopetaloides from macerations (Fig. 8c) does not show such remnants: a result
of the chemical removal of primary wall material by the acidic and oxidative qualities
of the macerative fluid. However, thick sections of liquid-preserved material of T.
chantrieri, T. integrifolia, and T. leontopetaloides show a range of appearances, from
intact but somewhat porose membranes (Fig. 8d, e) to pit membranes with both large
and small pores (Fig. 8f, g). All of the micrographs of T. leontopetaloides are from
portions of a single plant. Even in older root portions, pit membrane remnants are
retained. No end walls of sectioned roots lack pit membranes or pit membrane
Author's personal copy
Monocot Xylem Revisited
105
Fig. 8 SEM micrographs of tracheary elements of Philesiaceae (a–b) and Taccaceae (c–g). a–b, Lapageria
rosea Ruiz & Pav. (cultivated in Santa Barbara, California), portions of end walls of root tracheary
elements. a. End wall seen from outside of element, portions of the membranes at the lateral ends of the
pits scraped away by the sectioning process. b. Portions of pit membranes such as those seen in a, at high
magnification to show fine pores in pit membranes. c–f. Tacca leontopetaloides (L.) Kuntze (Fairchild
Tropical Garden). c. maceration, showing portions of two tracheary elements. The front tracheary element
shows an end wall, the rear element shows lateral wall pitting. Because of the maceration process, pit
membranes are mostly absent from end wall and lateral walls. d–f. Portions of end walls of tracheary
elements from longisections of tracheary elements, seen from inside of those elements. d. Pit membrane
from root, showing the laminar nature, with a few small pores (tears at top due to handling). e. Portion of
tracheary element from tuberous stem, showing laminar membranes with a scattering of very small pores.
f–g. Pit membranes from tracheary elements of inflorescence axis base. f. Pit membrane mostly broken, due
to handling. g. Pit membranes mostly intact
Author's personal copy
106
S. Carlquist
remnants of some kind, so on a functional as well as a morphological basis, the
tracheary elements of roots are closer to the tracheid end of the gamut than to the
vessel element end.
The lateral walls of vessel elements in T. integrifolia roots are notable for consisting of scattered circular bordered pits. These connect to fibriform tracheids that bear
circular pits with prominent borders.
The difference between vessel end walls and tracheid end walls is not very great in
a number of monocot species. It is merely a matter of persistence of pit membranes
that are sometimes so networklike (as in Typha) that the holes in the meshes occupy
much more area than do the strands of the network. In monocots, scalariform pitting
on end walls of tracheids closely resembles the scalariform perforation plates on end
walls of "less specialized" vessel elements. Varied thicknesses of pit membranes in
vessel element have been reported by Jansen et al. (2009), who find that larger pores
may be found in thinner pit membranes.
If one envisions a "primitive" vessel in developmental terms, a nonporose pit
membrane (but traversed by micropores of the plasmodesmata) is present at maturity
of the cell. As the protoplast vanishes, dissolution of soluble (presumably mostly
pectic) portions of the end wall occurs. This leaves a remnant reticulum of cellulosic
fibrils in some end wall pits. These reticula can be swept away by the conductive
stream to various extents. The wider the tracheary element, the lower the likelihood
that the pit membrane reticulum will remain intact, because stresses on an elongate pit
membrane are greater than those on a short pit membrane. The wider the tracheary
element, the less conductive resistance it has and the greater the likelihood that the pit
membranes in its end wall pits will be swept away, producing a vessel element, by a
form of hydrolysis (Butterfield & Meylan, 1982).
Physiological Considerations
Evidence from comparative anatomy has justifiably been taken as indicating that
vessels confer an advantage to conduction. However, Hacke et al. (2007) and Sperry
et al. (2007) issue a caution, claiming that removal of pit membranes from an end wall
does not by itself confer much conductive advantage, although vessel widening and
simplification of the perforation can be still be considered appreciably advantageous.
Sperry et al. (2007) say, "primitive scalariform plates were major obstructions to flow,
accounting for 50 % of the total flow resistivity on average." Ellerby and Ennos
(1998), on the other hand, reported that vessel element end walls, whether scalariform
or simple, confer a small portion of resistivity to conduction (0.6–18.6 %) when
compared to the resistivity caused by the lateral walls. However, what has not and
cannot be measured is the conductive capabilities of a vessel element and an
equivalent transectional area of tracheids in a given species. If such a measurement
were possible, it would undoubtedly show that the vessel holds an advantage over an
equivalent transectional area of tracheids. Long scalariform perforation plates do
provide resistance to flow, but they may have the advantage of decreasing likelihood
of air embolism formation and of promoting recovery from embolisms and aiding
refilling, based on the ideas of Kohonen and Helland (2009). Ellerby and Ennos
(1998) indicate that perforation plates do not confer nearly as much resistance (0.6–
8.6 % of the resistance offered by the vessel), and are much less important in this
Author's personal copy
Monocot Xylem Revisited
107
respect than the vessel walls. Widening of the lumen confers a major advantage (the
fourth power of the diameter increase) to vessels (Tyree & Zimmermann, 2002), a
fact that is easily reflected in the wide diameter of earlywood vessels.
The function of perforation plates with a limited number of bars, which are found
in a number of palms (Klotz, 1977), is not clear. They may be sites for resistance to
high positive or negative pressures in vessels (Carlquist, 1975) or may even confer
mechanical strength of some other sort.
Wider vessels with simple perforation plates offer potentially increased vulnerability to the conductive system. Air bubbles involved in embolisms can spread from
one vessel element to another. Perforation plates, even simple ones, may tend to
restrict air bubbles, as compared to an ideal continuous smooth capillary (Slatyer,
1976; Sperry, 1985, 1986; Ewers, 1985; Kohonen & Helland, 2009). Scalariform
perforation plates would be expected in this scenario to confine embolisms to
individual vessel elements, especially if they have pit membranes in the end walls.
Removal of air embolisms and mechanisms for recovery of the water columns in
vessels have received considerable attention in recent years (Clearwater & Goldstein,
2005; Pickard & Melcher, 2005; Holbrook & Zwieniecki, 1999), and clearly is
widely operative. Root pressure is pronounced in some monocots (Davis, 1961)
and is a widespread phenomenon in monocots as well as certain non-monocots
(Ewers et al., 1997; Fisher et al. 1997a, b). Most monocots are within the height
range where root pressure would be effective. Information on refilling of cavitated
vessels in grasses is offered by McCully et al., (1998) and Stiller et al. (2005).
Hacke et al. (2007) refer to "cryptic vessels," which have greater porousness of end
walls than typical tracheids, but do not clarify this concept. Feild et al. (2000) figure
tracheids with pit membranes lacking in Amborella, but these are artifacts, because
intact porose pits in end walls of Amborella can be found (Carlquist & Schneider,
2001; Hacke et al., 2007). The pit membranes of Amborella are very delicate and
break easily. This is also true in Bubbia, a genus of the vesselless Winteraceae
(Carlquist, 1983). Pit membrane thickness may be important in study of conduction
of vessels, but data from monocots is lacking. Our ideas about the physiology of
conduction are based largely on woody angiosperms and conifers. Presumably these
concepts can also be demonstrated with monocots (e.g., Sperry, 1985, 1986), but all
monocots are not alike in xylem anatomical formulae or in quantitative characteristics
(e.g., Fisher et al., 1997a, b).
A null hypothesis (that scalariform perforation plates have no function, but are a
feature that has persisted from ancestral species) does not seem likely, because
structural evolution is too efficient for mass persistence of a functionless character
state. No functionality, however, is implied by the work of Cheadle (1942 et seq.),
who presents vessel evolution in monocots as an inexorable process of perforation
plate simplification. Structures such as scalariform perforation plates, which represent
considerable expenditure of photosynthates, are not likely to be present for relictual
reasons.
Vessellessness in Monocots: A Pervasive and Important Theme
How common is vessellessness in monocots, systematically and organographically?
What relationships exist between vessellessness and ecology and conductive
Author's personal copy
108
S. Carlquist
physiology? What relationships exist between characteristics of plants and organs
(e.g., succulence) an vessellessness? Are there monocots in which primary xylem and
early metaxylem are vesselless but metaxylem contains vessels? Cheadle (1942,
1943a, b) stressed evolutionary development of vessels within monocots systematically and organographically. However, should one not stress, instead, the inverse: the
retention of all-tracheid systems in many monocot organs, and try to establish why
this retention has occurred? Vesselless woody angiosperms are few and geographically restricted, but if one looks at a landscape and knows which monocots lack
vessels one may be surprised at how much vesselless vegetation one is seeing. This is
true even in a grocery store: the edible parts of onions, garlic, and asparagus, for
example.
Vessellessness is very common at the organ level in monocots. There are many
monocot species in which all tracheary elements of stems and leaves have pit
membranes on all pits. Such elements fit the traditional definition of a tracheid, but
that is a problem if SEM is required to establish pit membrane presence in end walls.
Any other definition (e.g., degree of porousness of the pit membrane) is equally
problematic, also relying on SEM data that would take decades to accumulate. The
traditional light microscope definition—a scalariform end wall in which the perforations are wider (and the bars between them are narrower) than the pits of lateral
walls of tracheary elements— will probably continue to be used because it can be
applied so easily in light microscopy and can be demonstrated in many species.
Examples of intermediacy will, in this case, not be stressed. SEM data now available
suggest that in most cases in which there is little difference between end walls and
lateral walls of tracheary elements, pit membranes are likely to be present on end
walls. If this is true, vessellessness is much more common in monocot stems and
leaves than the listings of Cheadle (1942 et seq.) and Wagner (1977) would lead one
to believe.
Examples are presented above for Asteliaceae (Fig. 1), Cannaceae (Fig. 2),
Orchidaceae (Figs. 3, 4), dracaenoid Asparagaceae (Fig. 5e–f), Pandanaceae
(Fig. 7d–f), Philesiaceae (Fig. 8a–b) and Taccaceae (Fig. 8c–g) These represent just
a small sampling of species I regard as likely to have pit membranes in end wall pits
rather than having perforations, as reported (Wagner, 1977). To be sure, there is
progressively less porousness within an end wall pit membrane of a single plant as
one goes from root to inflorescence axis in Epidendrum and Phalaenopsis, suggesting
a decrease in conductive ability as one goes from root to inflorescence axis, but in the
form of a minor gradation of tracheid microstructure. To be sure, the root of
Odontoglossum (Fig. 3f) seems to have perforation plates, but the illustration is from
a maceration, a technique that could remove pit membrane remnants.
The pattern of vessel presence in roots combined with tracheids elsewhere in the
plant is common in monocots, and one needs to account for the significance of this
pattern. No monocots are reported by Wagner (1977) to lack vessels in roots except
for a few families in ecologically special circumstances. These include families of
submersed aquatics (e.g., Aponogetonaceae, Ruppiaceae, Zosteraceae). Also notable
in this regard are families which are heteromycotrophic, such as Petrosaviaceae,
Triuridaceae, and achlorophyllous Burmanniaceae and Orchidaceae (Carlquist,
1975; Wagner, 1977). These families are denoted by small circles to the left of family
names in Fig. 15.
Author's personal copy
Monocot Xylem Revisited
109
The species studied here present some interesting examples. Typha does have
wider metaxylem vessels that lack pit membranes in roots but also narrower metaxylem vessels in which end wall pits still have pit membranes (Fig. 6). Similar
situations occur in Cyclanthaceae and Pandanaceae (Fig. 7) when microstructure is
studied. This suggests a relationship between tracheary element diameter and degree
of end wall primary wall retention. In woody dicots, vessels tend to be wider in roots
than in stems (Patel, 1965), so a similar trend is not unexpected in monocots. Thus
widening of tracheary elements could account, in part, for presence of vessels in roots
of monocots which lack vessels in stems and leaves. It might also account for the
apparent lack of vessels in the roots (Fig. 8a–d) of Lapageria (Philesiaceae), and the
lack of vessels in stems of the palm Phytelephas (Klotz, 1977), and the apparent lack
of vessels throughout the plant in most Taccaceae (see original data above).
We are still confronted by the question of why tracheids or tracheid-like vessels
should occur in these plants. There are two prime questions: can there be secondary
vessellessness within particular organs? And what ecological circumstances favor the
presence of vesselless conditions in particular organs or the occurrence of vessels in
others? These questions have been sidelined in earlier studies. Cheadle (1942 et seq.)
merely believed in progressive inexorable acquisition of vessels, and thought that
acquisition of vessels was an irreversible trend. Cheadle also averred that links
between xylem and ecology and between xylem and habit in monocots should be
sought "after the data on xylem in monocots is in" (V. I. Cheadle, personal communication, 1994), and regarded attempts to find such correlations (Carlquist, 1975) as
premature.
The heteromycotrophic monocots use a network of fungi instead of root hairs as a
method of absorbing water, and all grow in notably mesic forest floor locations rich in
leaf litter and have limited aboveground stature. Under these circumstances, tracheids
suffice quite well for conduction and, in fact, in all of these taxa, the tracheids are
narrow (Carlquist, 1975). The systematic distribution of the heteromycotrophic
monocots (Fig. 14) suggests that there has been vessel loss and that autotrophic
ancestors probably had vessels in roots.
In some other monocots mentioned above in which tracheids are more
pervasive, and vessels less common than had been thought by Cheadle (1942)
and Wagner (1977), highly mesic habitats are a common denominator. This is true in
Asteliaceae, Cyclanthaceae, many Pandanacaeae, and terrestrial Orchidaceae, for
example.
Aquatic habitats are, of course, the ultimate in making minimal transpiration
demands on a plant. Therefore, the many families and genera that are vesselless
among aquatics, are, not surprisingly, vesselless. These occur in Alismatales (or
Alismatidae) mostly. For these plants, vessels have little or no selective value except
in relation to fluctuating levels of moisture, as is the case in pond or stream margins
(e.g., Sagittaria), where brief periods of lowered water availability may correlate with
the increased conductive rates, which may rapidly reverse any embolisms that form
on hot, dry days. Although Alismatales are an early branch in the monocot tree
(Fig. 14), they may not be ancestrally vesselless. Some vesselless monocots, such as
Zosteraceae, may solve the low-oxygen content problem of an underwater habitat by
living in areas subject to wave action, and thereby maximal water oxygenation. Other
submersed aquatics have solved the problem of low oxygen availability in standing
Author's personal copy
110
S. Carlquist
water by developing air circulation patterns within the plant body, as is known for
non-monocots such as Nymphaeaceae and Menyanthaceae. The complexity of these
specializations correlates with the rather small number of families and genera that
have adapted to the submersed aquatic habitat. We should consider the possibility that
the xylem and the air circulation systems of these plants represent some apomorphic
features, and are not wholly symplesiomorphic, even though they may retain antique
DNA sequence patterns.
Succulence and lowering of transpiration by thick cuticles, sunken stomata,
drought deciduousness of aerial portions of leaves (e.g., Allieae) and C4 photosynthesis (e.g., Silvera et al., 2010) are mechanisms that should be studied in conjunction
with vessellessness of particular organs in monocots. "Protection from transpiration"
(0 high diffusive resistance of leaf surfaces; condensed leaf forms) and "internal
mesomorphy" (0 succulence) are themes that should be studied in relation to vessellessness in stems and leaves of monocots.
Tracheids Coexisting with Vessel Elements
Tracheids that form the background of vessel bearing woods (e.g., Cornaceae,
Hamamelidaceae, many Rosaceae) are a commonly encountered phenomenon in
the woods of many woody angiosperms. Xylem in which tracheids as well as vessel
elements occur alongside each other in a single vascular bundle occurs in monocots,
but has not been sufficiently appreciated. Certainly co-occurrence of tracheids and
vessels together has been reported (Cheadle, 1942; Fahn, 1954; Klotz, 1977; Wagner,
1977). When both are present together, a kind of intergradation between the two cell
types may be characteristic.
A strong division of labor between co-occurring tracheids and vessel elements is
present, however in Borya (Carlquist et al., 2008). The stems of Borya have scalariform perforation plates (Fig. 9a–c). The bars are thin to extremely tenuous, and often
collapse in cell macerations. In vessels, the perforation plates are well differentiated
from lateral wall pitting, which consists of alternate circular pits (Fig. 9b, upper right).
Most xylem cells are narrow tracheids with one to three rows of prominently bordered
alternate circular pits (Fig. 9d–f). The tracheids are fusiform, in contrast to the vessel
elements. In fact, the xylem of Borya stems in a maceration looks much like the
xylem of a woody angiosperm.
To understand the co-occurrence of two such contrasted cell types in stems, one
must know that Borya is an Australian "resurrection plant" that grows on granite
shelves which may be wet and dripping during rains, but which are dry for most of
the year. The vessel elements offer the potential of rapid supply of water to the foliage
with the initiation of the rainy season. The tracheids are thick-walled, and can
probably maintain water columns even under water tension during the dry season.
The xylem of Borya is not what one would expect from an early-departing, near-basal
branch of Asparagales if one thinks in terms of gradual phylogenetic progressions as
Cheadle did. Instead, the xylem design shows radical design suited for a special
ecological situation.
The lateral walls of wide, vessel-like tracheary elements (which possess pit
membranes or pit membrane remnants) in roots of Tacca integrifolia have scattered
circular lateral wall pits. These circular pits connect to fibriform tracheids with
Author's personal copy
Monocot Xylem Revisited
111
Fig. 9 SEM photographs of vessel elements (a–c) and tracheids (d–f) from macerations of stems of Borya
sphaerocephala R. Br. (a, b, f) and B. subulata C. A. Gardner (c–e). a. Perforation plate with thin bars. b.
Perforation plate with very tenuous bars. c. Pit membrane remnants (right) at one end of a perforation plate.
d. Portions of several tracheids to show circular bordered pits. e. Wide tip of a tracheid. f. Slender tip of a
tracheid. From Carlquist et al. (2008)
circular bordered pits (unpublished data). Thus, more than one kind of functionally
imperforate tracheary element can co-occur in T. integrifolia roots. Tacca integrifolia
is an understory plant of moist tropical forests, and clearly unlike Borya. The root
xylem of Tacca integrifolia may have counterparts in other wet forest monocots, such
as Lapageria. Our knowledge of such monocots using SEM is as yet rudimentary.
Arecaceae is an interesting family with respect to co-occurrence of vessels and
tracheids. Klotz (1977) indicates imperforate tracheary elements (0 tracheids) present
in early metaxylem of roots, stems, and leaves of all of the palms he studied. In most
species, late metaxylem in these species has vessels. This is an interesting kind of cooccurrence that has, like the quite different xylems of Borya and Dracaena, implications for retaining conductive safety (tracheids resist spread of embolisms) with
conductive efficiency (the metaxylem vessels of palms are few per bundle and
notably wide).
Author's personal copy
112
S. Carlquist
Lateral Meristem Activity in Monocots and Its Implications
Lateral meristems in monocots (called "monocot cambia" here so as not to be
confused with types of cambial activity in non-monocots) have been studied by
various workers, notably Cheadle (1937), Tomlinson and Zimmermann (1969), and
Rudall (1991). The genera in which monocot cambia have been recorded include the
following (taxonomy according to APG III, 2009, and the tree of Fig. 15). The term
"monocot cambium" is equivalent to "secondary thickening meristem" as used by
Rudall (1991). Rudall is doubtful that the monocot cambium is equivalent to secondary thickening meristematic activity in non-monocot angiosperms and Gnetales,
and indeed, it is not. The process by which a "master cambium" arises and gives rise
to conjunctive tissue and to vascular cambia, which in turn, produce xylem and
phloem, is quite a different process (Carlquist, 2007), and thus the contrasting terms
"monocot cambium" and "master cambium: are used here. Monocots either have no
cambium or a cambium-like layer in bundles that, in fact, is permanently dormant and
produces no vascular tissue (Carlquist, 2007). According to the most recent compilation of Rudall (1995), monocot cambia are found in:
Asparagales
Iridaceae
Aristeoideae
Aristea
Nivenioideae
Klattia
Nivenia
Schizostylis
Witsenia
Xanthorrhoeaceae
Xanthorrhoeoideae
Xanthorrhoea
Asphodeloideae
Aloë
Gasteria
Haworthia
Trachyandra
Asparagaceae
Aphyllanthoideae
Aphyllanthes
Agavoideae
Agave
Beaucarnea
Calibanus
Chlorophytum
Dasylirion
Dracaena
Furcraea
Hesperaloë
Author's personal copy
Monocot Xylem Revisited
113
Hesperoyucca
Nolina
Pleomele
Thysanotus
Yucca
Lomandroideae
Cordyline
Lomandra
The above listing is not as simple as it may seem. Monocot cambia produce relatively
few if any secondary bundles in the genera of Dasypogonaceae; Baxteria, Calectasia,
and Kingia may not belong on this list and are not so included in the survey of Rudall
(1995). Formation of tracheids, either by differentiation of pre-existing parenchyma
cells, or preceded by a few divisions that could be considered rudimentary meristematic activity, has been reported in root-stem junctions in some Bromeliaceae,
Commelinaceae, and Zingiberales, for example (Tomlinson & Zimmermann, 1969;
Rudall, 1991). These latter instances need further study.
The admirable essays by Tomlinson and Zimmermann (1969) and Rudall (1991)
make the point that monocot cambium is a continuation of the primary thickening
meristematic activity which enlarges the meristematic zone at the shoot tip. The
primary bundles may still be maturing at the same level where lateral meristematic
of the monocot cambium is already in progress; however, there may be a discontinuity between the two processes. Stevenson (1980) shows that the two processes can
be intercontinuous in seedlings of Beaucarnea, but discontinuous in the adult plant.
Tomlinson and Zimmermann (1969) make the interesting, if minor, point that addition of more numerous bundles on the lower surface than on the upper surface of a
slanting stem serves the purpose of reaction wood. They report that the monocot
cambium can originate both inside and outside of the endodermis in roots of
Dracaena, even within a single section.
The ontogeny and mature stems of Yucca brevifolia exemplify secondary bundle
formation (Fig. 10). A meristematic layer forms in the cortex of a stem (Fig. 10a,
pointers). Products of this meristem are radially aligned, and therefore can easily be
distinguished from the primary cortex (Fig. 10a, right) and the primary part of the
stem internal to the cortex. Primary cortex cells are not radially aligned. In younger
stems of Yucca brevifolia, periderm develops from periclinal divisions in the outer
primary cortex. As the stem increases in size, the periderm and primary cortex
become broken into functionless segments but are retained on the stem. As this
happens, new periderms are initiated within secondary cortex.
The monocot cambium produces radial files of meristematic cells internally
(Fig. 10a–b). Vascular bundles are initiated (Fig. 10b, vbi) by means of divisions
within these radial files. Two early stages are indicated in Fig. 10b, and one of these is
shown enlarged in Fig. 10c. Divisions continue (left half of Fig. 10b) until an optimal
strand of procambium-like cells is achieved (Fig. 10a, left). These then differentiate
into collateral bundles, with phloem external (Fig. 10d, p). The xylem (Fig. 10d, x)
part of each bundle is much larger than the phloem and consists wholly of tracheids.
The Yucca brevifolia pattern, with variations, occurs in other monocots with
secondary growth. In Dracaena deremensis (Fig. 11), an early stage in secondary
Author's personal copy
114
S. Carlquist
Fig. 10 The monocot cambium in Yucca brevifolia Schott ex Torr. (cultivated at Rancho Santa Ana b
Botanic Garden) and its products, as seen in transection. a. Low-magnification portion to show the monocot
cambium (pointers) and its products, plus a portion of the primary (1 °) cortex, to show the arrangement of
the tissues. The primary bundles of the stem (not shown) would be to the left of the area photographed. b.
Higher magnification portion of the monocot cambium (pointers) and its products: secondary cortex (far
right) and secondary stem. The vascular bundles shown are all immature; the earliest stages in origin of the
bundles (vbi 0 vascular bundle initials) are indicated. c. A strand of cells destined to become a vascular
bundles, in an early stage of development. d. Two secondary vascular bundles (p 0 phloem, x 0 xylem); the
bundles are collateral, with phloem on the side of the bundle facing the outer surface of the stem
activity is depicted. The monocot cambium has produced only about two layers of
secondary cortex at this stage. Toward the inside, a single series of secondary bundles
has been produced. These bundles are amphivasal rather than collateral. Phloem (p)
and a tracheid (t) are shown for one of the secondary bundles in Fig. 11a. Only a few
tracheids are mature in these secondary bundles, so that the amphivasal nature is not
conspicuous. The primary bundles (Fig. 1a, left half) are collateral, with phloem (p)
external) to two or more tracheids (t). In addition, the external face of the primary
bundles consists of extraxylary fibers (f).
The features of Dracaena stem bundles are illustrated more conspicuously by the
bundles of Cordyline (Fig. 11b–c). Primary bundles (Fig. 11b) tend to be collateral,
with protoxylem (px) internal to the central phloem strand, but metaxylem (mx)
external to it. All xylem cells are tracheids. The secondary bundles (Fig. 11c) are
clearly amphivasal, with tracheids surrounding a central strand of phloem. Note that
because secondary bundles are derived from meristematic (procambium-like) cells
that do not elongate, as do those in primary stems, the tracheids can all be considered
to resemble metaxylem tracheids, and the elements formed in secondary bundles are
pitted rather than with annular or helical thickenings.
In the dracaenoid genera, Cheadle (1942) reported vessels only in the roots, with
an all-tracheid nature for bundles of the stem. This is confirmed here (Figs. 11, 12b–
c). As seen with SEM, the tracheids of Dracaena stems prove to have porose
membranes in the scalariform pits on tracheid end walls (Fig. 11d). Cheadle (1942)
reported scalariform perforation plates in leaves of Dracaena, and cited this as an
exception to the root‐stem—leaf sequence of vessel progression within a plant.
However, the supposed vessel elements of Dracaena actually have porose pit membranes (Fig. 11e) and should probably be called tracheids.
Roots of monocots mostly do not develop secondary bundles. Widened stem bases
do occur in Aloe, Beaucarnea, Cordyline, and Yucca, but roots are continually
initiated on these stem bases as they widen. As plants of these genera increase in
size, the diameter of the roots may widen, however, but they still, as far as is known,
consist only of primary tissues. This is also true in roots of such non-asparagalean
groups as palms (Iriartea) and Pandanaceae, both of which form conspicuous prop
roots. Roots of large diameter have more numerous alternating xylem and phloem
poles surrounding a central pith.
Dracaena is an exception in that its roots produce secondary bundles, as noted by
Tomlinson and Zimmermann (1969). Dracaena draco, the dragon tree, bears thick
roots at the bases of stems, roots which increase in thickness over time. These roots
contain secondary bundles (Fig. 12a). The limits of the primary root and the beginning of the zone of secondary bundles are indicated in Fig. 12a (top). At left in
Author's personal copy
Monocot Xylem Revisited
115
Fig. 12a are alternating xylem and phloem poles (two of each are labeled; they
continue around the root in a cylinder). The larger the root, the more numerous the
alternating xylem and phloem poles. These xylem and phloem poles, as shown in
Author's personal copy
116
S. Carlquist
Fig. 11 a. Beginning of monocot cambium activity in Dracaena deremensis Engl. as seen in a transection of the
stem; the monocot cambium is indicated by pointers. a small portion of the primary cortex (1 °C) and some of the primary
stem (1 ° stem) are shown, together with the secondary cortex (2 °C) and secondary stem internal to the cambium (2 °
stem) formed at this point are indicated (f 0 fibers, p 0 phloem; t 0 tracheid; v 0 vessel). b, c. Bundles from a stem of
Cordyline australis (G. Forst.) Endl.. b. Bundle from primary stem (px 0 protoxylem; mx 0 metaxylem;
phloem is in center of bundle). c. A secondary bundle, consisting of tracheids that encircle a strand of
phloem ("amphivasal bundles"). d, e. SEM micrographs of pits from end walls of tracheary elements in
Dracaena deremensis. d. Pit membrane laminar, but with small pores, from stem. e. Pit membrane
reticulate, from leaf. Material cultivated in and accessioned by Lotusland Foundation, Santa Barbara
Author's personal copy
Monocot Xylem Revisited
117
Fig. 12 SEM micrographs of tissues from roots of Dracaena draco L. (a, b, d, e) and Pleomele
(Dracaena) aurea N. E. Brown (c). a.Transection of root showing the primary (1 °) and secondary (2 °)
tissues. In the primary root portion alternating poles of xylem (which consists wholly of vessels) and
phloem occur in a fibrous background. In the secondary tissues, only tracheids—notably large in diameter–
are present in the xylem (p 0 phloem, x 0 xylem). b. Simple perforation plate, in oblique view, from
longisection of primary bundle. c. Simple perforation plate in sectional view; lateral wall pitting in face
view. d. Prominently bordered pits on surface of tracheid, secondary portion of root. e. Transection of
tracheid portions from secondary portion of root, to illustrate thick wall and (upper left), a bordered pit in
sectional view. Material cultivated and accessioned by Lotusland Foundation
Author's personal copy
118
S. Carlquist
Fig. 12a, are embedded in extraxylary fibers (dense area of light gray). Special note
should be taken that the xylem in the primary roots of Dracaena draco (and other
species of Dracaena) consists of vessels (Fig. 12b–c) rather than tracheids. The
secondary bundles (Fig. 12a, right) consist, on the contrary, wholly of tracheids,
and are collateral, with phloem (p) facing toward the outer surface of the root.
Special note should also be taken of the comparative diameter of the vessels in the
primary root and the tracheids in the secondary bundles. The tracheids in the
secondary bundles are notably wide in diameter but also may be thick-walled
(Fig. 12d–c). In other words, there is a compensation, by means of wide tracheids,
for the fact that vessels are absent in secondary bundles. This correlation has not been
noticed earlier, but is essential to understanding the physiology of conduction in
dracaenoid roots. The stems in the monocots listed above are vesselless, so that there
is no way in which vessels of roots could be connected to tracheids in stems: the
adventitious nature of monocots prevents that. Dracaena is highly distinctive among
monocots in that secondary growth in roots of Dracaena can be intercontinuous with
monocot cambia in stems, and therefore formation of vessels than extend from stems
into roots is a theoretical possibility, but one that has not been realized in the
dracaenoids or any other monocots. The intercontinuity of wide tracheids formed in
secondary stem and root bundles may be considered a reasonable substitute. The
advantages of adventitious roots in monocots (Carlquist, 2009; see also the "valve"
hypothesis below) are sufficiently great that adoption of vessels that extend from
roots into stems as in woody angiosperms would be of marginal value.
The addition of secondary bundles to stems by means of a monocot cambium is a
way of achieving greater stature; palms, which do not have a monocot cambium, have
an alternative series of adaptations, considered later. Most of the non-palm arborescent monocots have addition of secondary bundles as a way of achieving taller
stature. Ravenala and similar strelitzioid genera may be considered arborescent by
some, or may be excluded from the arborescent category; they do not have monocot
cambia.
Protoxylem Wall Microstructure
In most primary walls of monocot metaxylem, networks of primary wall cellulosic
fibrils can be seen in preparations in which amorphous wall portions are sectioned
away (e.g., Figs. 1g, 2c–e) or in which amorphous material is characteristically
hydrolyzed (e.g., Figs. 1f, 2a–b, 11d, e). In most monocots, however, there is
probably no cellulosic network in the primary walls of protoxylem (Carlquist &
Schneider, 2011), as illustrated by grasses. This may be correlated with rapid elongation and expansion of protoxylem tracheary elements. However, in protoxylem of
some monocots, such as Zingiberales (Carlquist & Schneider, 2010a), cellulosic
strands are revealed by SEM (Fig. 13). These fibrillar strands are best illustrated in
sections that have cut tracheary elements open, leaving the fibrils intact, rather than in
tracheary element surfaces that have been split apart by sectioning.
If limited amounts of wall material are cut away, as in Fig. 13a, a few strands may
persist. It the primary wall is not sectioned, thick strands running perpendicularly to
the helical bars of secondary wall material are visible (Fig. 13b–f). These strands are
presumably primary wall material, but this has not been demonstrated conclusively.
Author's personal copy
Monocot Xylem Revisited
119
Fig. 13 SEM micrographs of surfaces of helical protoxylem tracheids from inflorescence axes of Canna
indica (a–d) and Strelitzia reginae Banks (e–f). a. Tracheid seen from outer surface, part of wall cut away
by sectioning, showing the cellulosic longitudinal strands. b–f. Tracheids seen from inside, showing the
inner surfaces between secondary wall gyre or helix portions. c. Wall surface, showing longitudinallyoriented unbranched strands. d. Cellulosic strands with some reticulate interconnections. e. Helical band,
(center), showing points of attachments of the cellulosic strands. f. Cellulosic strands, with prominent
reticulate patterns' attachments to secondary wall helical band at extreme left. (Material cultivated by the
author)
The major strands that extend across primary walls of protoxylem tracheary elements
in Zingiberales often fade into a reticulate pattern. This is noticeable in Fig. 13b, d, e,
and f, but not evident in Fig. 13c.
Microstructure of protoxylem is a topic that has as yet been little explored in any
group of angiosperms. The significance of cellulosic fibrils in primary walls of
zingiberalean protoxylem elements may relate to nature of expansion. In genera
and families of this order, expansion of protoxylem may be slow and limited
compared with rapid and extensive elongation of protoxylem in, say, grasses. The
Author's personal copy
120
S. Carlquist
presence of a cellulosic network could delay indefinitely the collapse of protoxylem
primary walls. Ideas such as these can be tested by comparative investigations.
Monocot Xylem in the Context of Phylogeny
Early workers in xylem evolution took pride in the fact that their ideas were
developed independently of a phylogenetic tree of angiosperms (Bailey & Tupper,
1918; Turrill, 1942; Cheadle, 1942; Bailey, 1944; Tippo, 1946; Cheadle & Tucker,
1961). This attitude was defensible only because DNA-based trees, such as the one in
Fig. 15, were not available to them. Indeed, if such trees had been in existence,
working on xylem evolution with reference to molecular phylogeny would have been
considered mandatory.
In fact, Bailey was disingenuous in downplaying the role of the natural system in
the development of wood phylogeny. In a long series of papers (with such workers as
Nast and Swamy), he avidly studied the "woody Ranales" (0 woody basal angiosperms in current phylogenies, such as APG III, 2009). By studying such suspiciously "primitive families", he was aware of phylogenetic thinking, but curiously wished
to distance himself from it, perhaps because the efforts to construct a natural system at
that time (e.g., Bessey, 1915) involved so much guesswork and the arbitrary use of
"dicta." Also, the natural systems proposed in much of the 20th century were diverse
in many key details, and the lack of consensus made them less than useful to those
interested in evolution of structural features.
What criteria did Bailey and his students use for phylogenetic purposes under
these circumstances? Bailey and Tupper (1918) identified an evolutionary trend,
visible in vascular plants as a whole, for shortening of fusiform cambial initials
(monocots were not included in the survey, however). In vesselless woody groups,
tracheid length could be employed as a way of approximating the length of fusiform
cambial initials. In vessel-bearing woody groups, vessel element length is an accurate
indicator for fusiform cambial initial length (vessel elements do not increase in length
appreciably compared to the length of the fusiform cambial initial from which they
were derived).
Bailey and Tupper (1918) must have realized that tracheary element length by
itself is not an indicator of phylogenetic progression away from a hypothetical
ancestor. Table VI in Bailey and Tupper (1918) divides woody angiosperms into four
groups based on character state changes in wood anatomical features: lateral wall
pitting (beginning with scalariform, ending with alternate); and degree of border
presence on pits of imperforate tracheary elements (fully bordered, ending with
absence of borders). Bailey seems to be saying that morphological features can be
used interchangeably with tracheary element length as phyletic indicators (see Tippo,
1946). Indeed, Bailey handed off these features to graduate students. Frost (1930a, b,
1931) detailed angularity of vessels as seen in transection; end wall angle of vessel
elements; number of bars per perforation plate; and lateral wall pitting of vessels.
Kribs analyzed degrees and kinds of aggregation of axial parenchyma (1935) and
change in ray histology (1937).
To Vernon Cheadle fell the task of determining how xylem evolved in monocots.
Cheadle (1942) considered that longer vessel elements should be considered a
symplesiomorphic ("primitive") character state, and retained that view (Cheadle &
Author's personal copy
Monocot Xylem Revisited
121
Tucker, 1961) and never questioned it. In fact, this assumption is fallacious, because
monocots do not have vascular cambia, and therefore do not have fusiform cambial
initials. In monocots, vessel element length is governed by other factors, such as
degree of organ elongation, activity of basal meristems, size of plant, etc. The data of
Klotz (1977) show that climbing palms with long internodes have longer vessel
elements than do upright palms, for example.
Now that we have molecular-based trees inclusive of many families for monocots
(Fig. 14), we can see that other assumptions made by Cheadle (1942; Cheadle &
Tucker, 1961) are unfounded. Cheadle thought that vessels originated independently
Fig. 14 SEM micrographs of Acorus tracheary elements, showing the inner surfaces of tracheids. a–d, A.
calamus L.. Lower magnification of root tracheary element, to show the diagonal nature of the end wall,
which tapers to a tip at right. b. End wall of root tracheary element, showing the pit membrane, showing
both reticulate patches and nonporose areas. c. Lateral wall of root tracheary element, showing two pit
membranes which are virtually non-textured and show no porosities. d. End wall of stem tracheary element,
illustrating reticulate pattern of pit membranes, with fewer porosities at lateral ends of the pits (left). e–f. A.
gramineus Soland., root tracheary elements. e. End wall of tracheary element at lower magnification,
showing tapering to tip of element at right. f. Pit membranes from tracheary element end wall, showing a
delicate reticulate pit membrane in each of three pit portions. (Material cultivated by the author)
Author's personal copy
122
S. Carlquist
in monocotyledons and dicotyledons, but that was at a time when monocots and
dicots were thought to represent the products of the first forking of the angiosperm
tree. That idea was abandoned with the first global tree of angiosperms (Chase et al.,
1993) and all subsequent trees. "Basal angiosperms" are now regarded as the ancestral group in which monocots are nested. All of the basal angiosperms have vessels
except for Amborellaceae, Ceratophyllaceae, Nymphaeales, and Winteraceae. These
groups are probably not the direct ancestors of monocots, which seem rooted more
closely to the vessel-bearing groups Chloranthales and Piperales (Carlquist, 1992a, b,
2009) where structural resemblances are concerned. Winteraceae are basal angiosperms, but not close to the origin of monocots, and very likely are secondarily
vesselless (Young, 1981; Chase et al., 1993; Soltis et al., 2000).
One should mention that woody non-monocot angiosperms all have vascular
cambia, and that cambial loss is one of the earliest character state changes, if not
the earliest, that led to monocots. The loss of cambium is well illustrated in Houttuynia of the Saururaceae (Carlquist, 2009), although that genus is not ancestral to
monocots.
The studies of Bierhorst and Zamora (1965) show that in families and species
from 165 angiosperms (including basal angiosperms, sensu APG III, 2009), primary
xylem contains vessels in all of the species they studied. Bierhorst and Zamora (1965)
report tracheids as well as vessels in protoxylem of many of the species they studied,
and note a trend of specialization, expressing itself in the earlier ontogenetic appearance of advanced features and the elimination of primitive ones. The only families
in which Bierhorst and Zamora note some tracheids (along with vessel elements
with scalariform perforation plates) in metaxylem are Aquifoliaceae (Ilex),
Buxaceae (Pachysandra), Caprifoliaceae (Weigela), Cornaceae (Cornus), Cunoniaceae (Spiraeanthemum), and Ericaceae (Gaultheria). The omission of Chloranthaceae
from these studies is regrettable, because one might have found that primary xylem of
Sarcandra stems lacks vessels, as suggested by the results of Bailey and Swamy
(1950). Sarcandra develops discernable vessels only in secondary xylem of roots or
caudices (Carlquist, 1987). The primary xylem in Winteraceae and Trochodendraceae
is evidently vesselless, also (Carlquist, 2009). Some of the species studied by
Bierhorst and Zamora (1965) might have proved to have pit membranes in end walls
of vessel elements, if they had been able to undertake SEM studies of sections instead
of light microscope studies of macerations. Primary xylem is mentioned here because
it was alleged by Bailey (1944) to be a sort of refuge for primitive features, so that if
monocots and non-monocot angiosperms independently acquired vessels, we might
expect to see all-tracheid primary xylem with vessel-bearing secondary xylem. That
is evidently not always the case.
The available data and molecular trees now produced suggest that Cheadle's
contention (Cheadle, 1942; Cheadle & Tucker, 1961) that monocotyledons are
primitively vesselless and that vessels originated independently in monocotyledons
and non-monocot angiosperms should be questioned. We can no longer accept the
dictum of Bailey (1944): "The independent origins and specializations of vessels in
monocotyledons and dicotyledons clearly indicate that if the angiosperms are monophyletic, the monocotyledons must have diverged from the dicotyledons before the
acquisition of vessels by their common ancestors. This renders untenable all suggestions for deriving monocotyledons from vessel-bearing dicotyledons or vice versa."
Author's personal copy
Monocot Xylem Revisited
123
Bailey's statement is incorrect now that we have information from DNA-based
phylogenetic trees. He also fails to take into account the profound differences related
to growth form. Sympodial angiosperms with adventitious roots inevitably have
patterns of vessel evolution different from those seen in monopodial woody angiosperms with taproots.
Symplesiomorphy in Monocot Xylem: Can we Find It?
If we compare the molecular-based tree of Fig. 15 to what is known about the xylem
of these families, do we find concordance or discordance? If we find discordance,
why?
Heteromycotrophic monocots are apparently vesselless, although we do not have
complete information on all of them (notably heteromycotrophic Burmanniaceae and
Orchidaceae). The heteromycotrophic families (signified by circles at tips of branches
in Fig. 15) do not group closely. Rather, they are homoplasic, as the tree in Fig. 15
suggests (this would be even more evident if heteromycotrophic orchids were
plotted). Although one family (Petrosaviaceae) is an early-diverging branch of
monocots, one genus (Japanolirion) is autotrophic. We can safely conclude that
vessellessness in heteromycotrophic monocots (still insufficiently studied) is secondary. This is instructive, in that these monocots can serve as an example of how
secondary vessellessness can occur.
After Acorales (0 the genus Acorus),which is the sister to the remaining monocots
and is discussed separately below, the next node leads to Alismatales. Araceae do
have vessels in roots (Carlquist & Schneider, 1998; Schneider & Carlquist, 1998),
although some pit membrane remnants can be found in some perforation plates. No
convincing evidence for presence of vessels in stems of Araceae has been presented.
The clade that contains Alismatales (Fig. 15) can be characterized as consisting
mostly of aquatics. Notable is the fact that the submersed aquatics in the order
(Aponogetonaceae, Hydrocharitaceae, Najadaceae, Ruppiaceae, Zannichelliaceae,
Zosteraceae) lack vessels throughout the plant. Submersed aquatics may have adapted
to that habit/habitat recently, but the likelihood is that the earliest monocots were not
submersed aquatics and that vessels may have been present in the roots. One notes
that in Fig. 15, the family Tofieldiaceae is the sister to the remaining Alismatales. To
be sure, this sampling is less than optimal. However, Tofieldiaceae and Alismataceae,
although characteristic of marshy habitats (ranging from savannah seeps to ponds),
have vessels in roots. To be sure, one must always keep in mind that the xylem of
plants is likely to relate to the present-day ecology of the plant, and not represent
relictual conditions. Imagining a symplesiomorphic status for vessellessness in the
submersed families of Alismatales would require nonparsimonious character state
reversions. Much more likely is the idea that presence of vessels in roots of aquatic
monocots is symplesiomorphic, and is related to occupancy of habitats in which roots
experience some degree of fluctuation of moisture availability, making vessels
advantageous. Submersed aquatics have developed intricate (and diverse) means of
coping with low oxygen levels in water, mechanisms that would have to be developed
and then lost again if submersed aquatics were to represent the ancient monocot
habitat. Absence of vessels in roots, of the submersed aquatic monocots is, therefore,
probably apomorphic, representing secondary vessellessness.
Author's personal copy
124
Fig. 15 A phylogenetic tree of
the monocots, prepared by
Thomas J. Givnish and associates (e.g., Givnish et al., 2010)
from the multigene data in Chase
et al. (2006) and other sources.
This tree has not been previously
published and is reproduced
from the internet site, "Assembling the Phylogeny of the
Monocotyledons" with the permission of Thomas J. Givnish. In
order to conserve space, some
taxa have been omitted by the
authors. Typhaceae (including
Sparganiaceae) constitutes
Typhales, and Araceae is the sole
family of Arales. Taccaceae
belong to Dioscoreales (possibly
included within Dioscoreaceae).
The families Aponogetonaceae,
Najadaceae, Scheuchzeriaceae
and Zannichelliaceae belong to
Alismatales. Circles at tips of
branches indicate heteromycotrophic occurrences; some Burmanniaceae and Petrosaviaceae
are autotrophic, and some
Orchidaceae are
heteromycotrophic
S. Carlquist
Author's personal copy
Monocot Xylem Revisited
125
Autotrophic habits and nonaquatic habitats are characteristic of the monocots near
early nodes of the tree in Fig. 15 and other trees that have been proposed (Davis et al.,
2004; APG III, 2009). Such habitats are characteristic of monocots, in which one
sees, with few exceptions, presence of vessels in roots, but lack of vessels in stems
and leaves (Fahn, 1954; Cheadle, 1963, 1968; Cheadle & Kosakai, 1971; Wagner,
1977; see also original data above). According to Cheadle (1968), Campynemataceae
are possibly totally devoid of vessels. Original data on Lapageria (Philesiaceae)
given above (Fig. 8a–b) suggests that it may fall in that category also. A few other
instances may be found in Liliales when they have been more intensively investigated. The SEM data on Asteliaceae (Carlquist & Schneider, 2010b) and Orchidaceae
(Carlquist & Schneider, 2006; see also Fig. 3) are persuasive that some Asparagales
have no vessels. In Dioscoreales, vessel presence has not yet been clearly established
throughout Taccaceae (Fahn, 1954; Cheadle, 1968; Wagner, 1977). All of the Liliales
and Dioscoreales listed occur in highly mesic habitats, but that does not necessarily
indicate that the genera and families just cited are relictual in lacking vessels in roots
(as well as in stems and leaves). Secondary vessellessness has been claimed for
Winteraceae and Trochodendraceae (Young, 1981, and subsequent authors), and
those two families are limited, as are the monocots just mentioned, to highly mesic
localities in which there is little fluctuation in water availability.
However, to the above, one can add families and genera that lack vessels in stems
and roots and have very "primitive" vessels (long scalariform perforation plates) in
roots. Cyclanthaceae, Pandanaceae, and Typhaceae have been highlighted above in
this regard because earlier reports suggested that these three families have vessels
throughout the plant. Families in which vessels with long scalariform perforation
plates occur in roots whereas stems and leaves have only tracheids include Araceae
(Keating, 2003), Costaceae, Hanguanaceae, Heliconiaceae, Hypoxidaceae, Melanthiaceae, Petermanniaceae, Ruscaceae, Trilliaceae, Zingiberaceae, and a number of
genera of hyacinthoid Liliaceae (Wagner, 1977).. Numerous genera from Orchidaceae
and various other families could be added to this list. In other words, this appears to
be a widespread condition in the earlier-departing clades of monocots (as schematized
in Fig. 15: orders from Acorales upward to Asparagales). If one views the distribution
of vesselless or near vesselless genera, they do not appear to be the earliest branches
in their respective clades in Fig. 15. If one were to hypothesize vessellessness as
symplesiomorphic for monocots, one would have to account for multiple instances of
vessel acquisition, if the tree of Fig. 15 is tenable.
One can hypothesize that the presence of long scalariform perforation plates in
roots combined with only tracheids in stems and leaves is not only symplesiomorphic
for monocots as a whole, but also that it has adaptive significance. Roots tend to have
wider vessels than stems in woody dicots (Patel, 1965), and if this is true for
monocots as well, then vessels are more likely to occur in roots than in stems of
monocots. Adventitious roots by their very nature experience more fluctuation in
water availability than do taproots, so the presence of vessels in roots of monocots is
understandable.
If one views the ecology of the monocots with this xylem formula (vessels with
scalariform perforation plates in roots, only tracheids in stems), one sees that they
mostly inhabit highly mesic localities. Some genera on this list have mitigating
conditions, such as succulence, that permit them to function as "temporary
Author's personal copy
126
S. Carlquist
mesophytes" (e.g., many orchids; Hyacinthaceae). The hypothesis most in line with
molecular trees of monocots, knowledge of tracheary element morphology, and
ecology is twofold. Genera with this formula have a symplesiomorphic xylem
condition, and they have had unbroken occupation of mesic habitats. Departures
from this formula must have taken place homoplasically, and such divergences
represent numerous clades that have adapted to progressively more seasonal conditions. These departures represent tradeoffs between conductive efficiency (vessels
with simple perforation plates) and safety (an all-tracheid condition). The patterns of
xylary apomorphies in monocot xylem are numerous and should be traced on a
family-by-family basis. Commelinales and Poales are not covered to any appreciable
extent in the present paper, because they are crown groups that have already attained
extensive vessel presence throughout the plant—a feature deserving of ecophysiological study, notably different from the presence of all-tracheid systems in monocots.
The Role of Ontogeny and Cell Size in Vessel Presence
The simplest explanation for presence or absence of pit membranes in a vessel end
wall is a developmental one. The pit membranes are swept away by the conductive
stream because they have an insufficient cellulosic network to resist the effects of the
flow. The nature of the cellulosic network is, presumably a feature embedded in the
genetics and development of the vessel elements. As yet, we do not have comparative
tracking of cellulosic network presence in pit membranes or stages in its loss as vessel
elements mature. Secondary vessellessness may be achieved by relatively minor
changes in the cellulosic components of the pit membrane. If cellulosic fibrils are
present in pit membranes of tracheid end walls, pit membranes may be retained as a
result of gene action, resulting in absence of lysis of the pit membrane, rather than (as
is typical for perforations in vessel elements), swept away in the flow of xylem sap.
Such possibilities are developmentally simple and plausible causes of retention of the
tracheidlike characteristics of a xylem cell, and should be considered before other
possibilities are entertained.
There are, however, other ways in which secondary vessellessness may occur.
Klotz (1977) showed that in palms, imperforate tracheary elements are present in all
species in early metaxylem, whereas vessels occur in late metaxylem. Could this lead,
phylogenetically, to an all-tracheid system if production of late metaxylem was
suppressed? Theoretically, yes, but definitive demonstrations of such shifts may be
difficult. Nevertheless, some examples are suggestive, and are worthy of discussion.
The clearest examples of this trend are in the submersed aquatics of the Alismatales such as Aponogetonaceae or Zosteraceae, in which vessels may have been lost
simply because so little xylem is produced. Something like this may have happened
in commelinalean family of submersed aquatics, Mayacaceae, also. Mayacaceae have
long scalariform perforation plates in roots, tracheids only in stems and leaves.
Mayacaceae are nested within Commelinales that have more "specialized" xylem
(see Fig. 15), a contradiction of a dictum by Cheadle (see next section). Mayacaceae
may merely be forming protoxylem and early metaxylem, in which tracheids and
scalariform perforation plates are to be expected.
Also possible examples of this may be found in Philesiaceae (Lapageria), Taccaceae, and Campynemataceae. They may be forming no "late" metaxylem as defined
Author's personal copy
Monocot Xylem Revisited
127
by the presence of wider tracheary elements. This could also be true in the palm
Phytelephas and its close relative Ammandra, which lack vessels in stems, and have
relatively narrow metaxylem elements (Klotz, 1977). Perhaps we should think in
terms of narrowing of tracheary elements rather than disappearance of vessels.
Narrrower tracheary elements in protoxylem and earlier formed metaxylem are more
likely to be tracheids than vessels, and more likely to have scalariform perforation
plates than simple ones as compared to metaxylem. This idea was enunciated by
Bailey (1944) who thought of the primary xylem as a refuge for "primitive" xylem
characteristics in woody angiosperms. Bierhorst and Zamora (1965) found evidence
to support this idea in their study of primary xylem, as did Cheadle (1968) in
Haemodoraceae.
Monocot bundles may be considered juvenile in comparison with those of angiosperms capable of vascular cambial activity. The developmental sequence can therefore be regarded as foreshortened, or juvenilistic. Monocot bundles have been so
regarded in a study that places xylems of angiosperms within a developmental
framework (Carlquist, 2009). That study was conceived in terms of activity of the
vascular cambium. However, one may, by extension, add ontogenetic changes within
a bundle that has no vascular cambium. Monocot bundles that do not proceed all the
way to typical late metaxylem patterns can thus be called juvenilistic. Typhaceae are
mentioned above as an example of how early metaxylem tracheary elements of roots
have scalariform end walls that retain pit membranes, whereas late metaxylem
tracheary elements are genuine vessel elements that lack pit membranes (except as
fragmentary remnants) in perforation plates. Evolutionary deletion of late metaxylem
in such a clade could result in secondary vessellessness.
In another perspective, one may consider that vascular bundles of monocots can
exhibit various degrees of dimorphism. In palms, for example, the late metaxylem
vessels are much larger (and more likely to have fewer bars on perforation plates)
than the early metaxylem, and early metaxylem apparently always contains tracheids
whereas late metaxylem lacks tracheids (Klotz, 1977). Dimorphism between late
metaxylem vessels and protoxylem + early metaxylem vessels is also familiar in
the transectional configurations one sees in grass vascular bundles (Metcalfe, 1960).
In this perspective, abrupt differences between early and late metaxylem are undoubtedly mediated by hormonal action.
Although both of the above perspectives seem valid, one is still left with the
question as to why these ontogenetic progressions occur, and are foreshortened or
abruptly changed. Morphological goals are reached not as fulfillments of inexorable
changes, but in response to functional value in the environment. There seems little
doubt that wide vessels, as in palms, are formed in response to the increase in
conductive capability by the fourth power of the increase in vessel diameter (the
Hagen-Poiseuille equation, Tyree & Zimmermann, 2002). Such wide vessels are,
however, potentially vulnerable, because wider vessels embolize more readily than
narrower ones, as indicated by vessel diameter changes in growth rings (Carlquist,
1980), and as can be proved experimentally (Hargrave et al., 1994). The sheathing of
wide vessels in palms by parenchyma (Tyree & Zimmermann, 2002) suggests that
parenchyma may form a system that counteracts vulnerability to some extent. Root
pressure (which is controlled by parenchyma in ways not fully demonstrated yet) may
also play a rote in countering vulnerability in wide vessels such as those of palms
Author's personal copy
128
S. Carlquist
(Davis, 1961). Angiosperm tracheids, on the other hand, are quite resistant to spread
of embolisms from one cell to the next by having pit membranes that resist air bubble
transfer by having small pore size. Increasing thickness of pit membranes reinforces
this capability (Jansen et al., 2009). Tracheids also generally have small diameter, and
thus, as the Hagen-Poiseuille equation tells us, are less efficient in conduction
(conifer tracheids do not conform to this, for reasons stated by Pitterman et al.,
2005), but we are dealing here with angiosperms, in which coniferous kinds of
margo-torus pit membrane structure has never evolved in tracheids. There are instances of tori or pseudotori, which may seal off bordered pits when pressure differences
among cells develop, in woody dicots such as Oleaceae, Ericaceae, Thymeleaceae,
and Ulmaceae (e.g., Dute & Rushing, 1987; Rabaey et al., 2006). These do not have
the conductive advantage possessed by the margo in conifer tracheid pit membranes.
In any case, monocots are not known to have tori or pseudotori.
The shift from protoxylem tracheary elements to late metaxylem elements has
usually been seen in structural terms, from extensible wall patterns (annular, helical)
to non-extensible pitted patterns. This common textbook story does not take into
account a shift from low conductive abilities combined with conductive safety
(protoxylem, early metaxylem) to high conductive abilities combined with increased
vulnerability (late metaxylem). The ways in which such xylem patterns relate to the
physiology and ecology of a species are left unexplored in favor of the more easily
described wall patterns, readily shown with light microscopy. Monocots show an
organographic balance between conductive efficiency and conductive safety. This
balance is not possible in woody angiosperms because the vascular cambium produces continuity from root to shoot. This resulting vascular continuity lacks the valve
(or "rectifier") feature that adventitious roots supply (see below). The conductive
safety/conductive efficiency balance can be regulated in monocots by production of
roots of finite (often very short) duration on stems of longer duration. It can also be
accomplished by curtailment of or sudden shifts in the protoxylem/metaxylem progression. Thus, terrestrial monocots with very narrow tracheary elements, such as
Lapageria or Campynema, can manage without vessels or with very tracheidlike
vessels because they have mesic ecology matched with low transpiration rates, and
can satisfy their water economy requirements with xylem low in conductive efficiency. Xylem formulations should always be viewed within ecological and physiological
contexts. To view them merely as externalizations of degrees of evolutionary progress
eliminates consideration of the forces that drive change in anatomical patterns and
robs them of their significance.
Ecological Iterations: A Key to Paradoxical Distributions of Xylem Character States
Cheadle (1942) thought of xylem formulas in monocots as representing levels or
grades of specialization, and he developed numerical ratings to record degree of
advancement for any taxonomic group. His five-point scale is given above under
Historical Perspectives. Rating evolutionary advancement is a data sink: it is condensed from real and valid data, but because it produces generalizations, it cannot
be used to yield new perceptions or conclusions about particular species: it cannot
tell anything about how these species and clades evolved, in relationship to
what factors.
Author's personal copy
Monocot Xylem Revisited
129
Symplesiomorphic xylem characters should be expected for monocots that have
had unbroken histories of occupancy of mesic habitats, and which therefore exhibit
no "ecological iteration" (shift in habitat preference). Long scalariform perforation
plates in vessels of roots, combined with only tracheids elsewhere in the plant body,
characterize such diverse groups as Campynemataceae (moist rock outcrops in New
Caledonia and Tasmania); Lapageria (moist forest in southern Chile), Petermannia
(moist forest in Queensland and New South Wales), and Cyclanthaceae (understory
of wet neotropical forests). These would correlate with their position as early
branchings within clades of monocots (Fig. 14). There is no reason to believe that
scalariform perforation plates have been secondarily derived from simple plates by
some kind of morphological reversion. Clades with simple perforation plates in
xylem can radiate into less seasonal habitats. For example, grasses can occupy
extremely wet areas, despite the fact that their xylem (vessels with simple perforation
plates, throughout the plant body) probably evolved in response to highly seasonal
conditions, drawing water from shallow soil depths. Thus, scalariform perforation
plates in roots often do represent a symplesiomorphic feature—but with numerous
cautions mentioned above. The genera and families just cited have distribution
patterns that correspond to ancient land areas.
However, good dispersal may permit a monocot with such an antique xylem
formulation to reach geologically new and highly disjunct land areas—as long as
they are ecologically suitable. This is true of Astelia, for example, which has
apparently dispersed from areas like New Zealand and Australia to Islands as distant
as Reunion in the Indian Ocean and Tahiti and the Hawaiian Islands in the Pacific.
Astelia has baccate fruits with small seeds suited to bird dispersal. Corresponding to
its symplesiomorphic xylem features, it occupies consistently moist forests or similarly mesic areas. Typha, which has preferences for sunny ditches and muddy
depressions and has a xylem configuration similar to that of Astelia, has a very wide
boreal distribution because of its tiny windborne seeds. Thus, one should not
expect symplesiomorphic xylem to correlate with extent of ancient geological
areas, although in some instances it does.
Rapid evolution into highly seasonal habitats is certainly characteristic of many
monocot clades: there are always more evolutionary opportunities in environments
with more fluctuation in temperature and precipitation, because extinction is likely to
be greater in more extreme habitats and therefore, niches are more readily available.
This triggers the question: can monocot clades that in their contemporary species
have more "specialized" (0 vessels in stems and/or leaves in those in roots; perforation plates with few bars or simple) xylem branch off early, while "crown groups"
retain more "primitive" configurations? The answer is yes, but Cheadle negates this
possibility. He argued that xylem specialization was identical to phylogenetic specialization, and that therefore a group with "specialized" xylem could not be ancestral
to one with "primitive xylem." One example is the apostasioid orchids (Apostasiaceae
of some authors), which molecular trees uniformly show branching off at the base of
the clade leading to the other orchid subfamilies (Davis et al., 2004; Fig. 14). Cheadle
and Tucker (1961) say, "Apostasiaceae......cannot have been the origin of Orchidales". Cheadle consistently negated the possibility that plants with simple perforation
plates might be the survivors of a line with numerous symplesiomorphic characters.
Today, we would say the "breakouts" favoring rapid evolution of simple perforation
Author's personal copy
130
S. Carlquist
plates can occur in any clade. In fact, xylem designed for water economy in more
extreme habitats would favor long-term survivorship in a line in which, say, floral
characters are symplesiomorphic, as they are in the apostasioids (Judd et al., 1993;
Kocyan et al., 2004) Aspostasioids have carried along symplesiomorphic DNA
sequences in plants that have evolved to cope with marked fluctuation in moisture
availability.
An even more striking example can be found in Borya (Boryaceae), mentioned
above (Fig. 9) is Borya, in which vessels with few bars on perforation plates occur in
stems. This xylem formulation correlates with the "resurrection plant" habit of Borya,
which lives on granite outcrops that dry quickly after winter rains. Borya is near-basal
in the Asparagales clade, nearly all of the genera of which lack vessels in stems.
Interestingly, one of the few exceptions to that description of Asparagales is Sisyrhynchium (Iridaceae), which has vessels in stems and leaves (Cheadle, 1963) and
maintains foliage in summer-dry habitats of the southwestern U.S. Boryaceae probably belong to a group that once included genera with symplesiomorphic xylem
features, genera that are now extinct. This is not an improbable scenario, and other
examples can be cited within monocots. In the tree of Fig. 15, Arecaceae (vessels
throughout the plant, except in a few non-basal genera) is a sister family to Zingiberales (vessels in roots only except for Cannaceae, Marantaceae) plus Commelinales
(vessels various). Velloziaceae (vessels with simple perforation plates in roots) plus
Triuridaceae (a vesselless heteromycotroph) bear a sister relationship to the remaining
Pandanales (Fig. 14). All of the remaining Pandanales have more symplesiomorphic
xylem configurations (vessels with long scalariform perforation plates in roots, but
probably no vessels in stems or leaves). Velloziaceae have adapted to tropical
savannah-like habitats with seasonal fluctuation in water availability that corresponds
to presence of simple perforation plates in root vessels. Rhizogonaceae, with simple
perforation plates in roots (Fahn, 1954), is probably a sister group to Philesiaceae
(either tracheids only, or possibly very long scalariform perforation plates in roots).
The pairs of close families just cited show how one family of a pair may have adapted
to highly seasonal habitats while its sister group continued an unbroken occupancy of
mesic habitats.
Probable loss of metaxylem vessels phylogenetically in submersed aquatics make
some "crown groups" seem to have more "primitive" xylem than they do. For
example, Mayacaceae, with vessels with long scalariform perforation plates in roots
and stems, is a "crown group" nested among non-aquatic commelinalean groups that
have vessels with fewer bars per perforation plates, according to the data of Tomlinson (1969). Likewise, the submersed aquatics of Alismatales lack vessels, although
Araceae, with vessels in roots, are sister to the Alismatales. All of these examples
underline the principle that xylem designs are adaptive in contemporary situations,
and we should not look to them as reliable sources of phylogenetic history.
Thus, there are at least two possible scenarios for why "specialized" xylem may
appear in groups basal in particular clades. One can find these scenarios in nonmonocot angiosperms also. Within Ranunculales, Papaveraceae (vessels with simple
perforation plates throughout the plant, even in primary xylem: Bierhorst & Zamora,
1965; Carlquist & Zona, 1988) is sister to a group of families that includes Lardizabalaceae and Ranunculaceae. Decaisnea of the Lardizabalaceae has long scalariform
perforation plates (Carlquist, 1984b). Papaveraceae have probably radiated into
Author's personal copy
Monocot Xylem Revisited
131
highly seasonal habitats, and surviving Papaveraceae show no traces of earlier stages
of this radiation.
In general, the more symplesiomorphic xylem configurations are more abundant in
more basal positions within clades. This would verify Cheadle's generalization, with
exceptions like the above. However, there is one major caveat. The most symplesiomorphic xylem condition in monocots, according to Cheadle, is an all-tracheid
condition. According to modern phylogenies (e.g., APG III, 2009), monocots represent a clade branching from basal angiosperms close to the departure point of
Chloranthales. Earlier branchings in the basal angiosperms include the outgroups
shown at the bottom of Fig. 14, according to all modern molecular trees.
A quotation from Bailey (1944) is appropriate to show how far we have
advanced in our thinking, and how much paradigms of monocot xylem must be
changed:
"The independent origins and specialization of vessels in monocotyledons and
dicotyledons clearly indicate that if the angiosperms are monophyletic, the monocotyledons must have diverged from the dicotyledons before the acquisition of
vessels by their common ancestors. This renders untenable all suggestions for
deriving monocotyledons from vessel-bearing dicotyledons or vice versa. Furthermore, the highly specialized structure of the xylem throughout both stems and roots
of herbaceous dicotyledons, not only affords conclusive supplementary evidence of
the derivation of herbaceous from arboreal or fruticose dicotyledons, but also is an
insuperable barrier to the derivation of monocotyledons from herbaceous
dicotyledons."
Newer information has made Bailey's statement untenable. Evidence from DNAbased phylogenies refutes Bailey's thinking, as all of the global angiosperm trees
produced since Chase et al. (1993) show. In that respect, Bailey was a victim of his
time. However, the understandings of Bailey and of Cheadle were seriously limited
by methodological procedures. They never related xylem structure to ecology of
species, which is especially curious considering that Cheadle field-collected much of
his material. Both viewed xylem as an inexorable progression (the stages of which
could be given numerical ratings). They did not correlate xylem with habit. They did
not consider relevant work in conductive physiology. They did not study developmental sequences and changes in tracheary element diameter within a xylem sample.
And they did not consider the role of hormonal changes and translocation which were
beginning to be appreciated in their time. Ultimately, of course, the governance of
hormonal change by gene action must be included in the evolutionary picture.
However, the central point is that in order to understand evolution of xylem structure,
we cannot exclude information from habit, ecology and physiology.
Evidence for Terrestrial Versus Aquatic Origin of Monocots
Are monocots as a whole ancestrally aquatic or terrestrial? Current interpretations
indicate that angiosperms as a whole are ancestrally sympodial, a growth form that is
very frequently associated with adventitious roots, and that taproots and monopodial
structures are probably apomorphies within angiosperms (Carlquist, 2009). To be
sure, monopodial growth forms appear to have originated early in angiosperms
(Carlquist, 2009).
Author's personal copy
132
S. Carlquist
Certainly monocots are better adapted to habitats that are wet for prolonged
periods, because taproots, characteristics of woody angiosperms, are not effective
in inundated habitats low in oxygen. The prostrate sympodial habit common in most
monocot clades has the advantage of being able to spread laterally over territory,
whereas a monopodial eudicot is limited to a narrowly limited piece of ground.
Lateral spreading, accompanied by development of adventitious roots, is certainly
adaptive in moist habitats, but more lateral spread implies capability of dealing with
various degrees of moisture availability close to the ground surface, and therefore
presence of vessels in roots can be hypothesized as advantageous.
If one were to hypothesize a submersed aquatic, or an aquatic with submersed
stems but leaves emergent above the water surface as an ancestral habit/.habitat in
monocots, non-parsimonious probabilities emerge. One has to imagine that somehow
such submersed aquatics acquired methods for ventilating roots and stems in low
oxygen habitats, then lost these mechanisms as most of the descendents moved onto
terrestrial or occasionally inundated habitats. Because of the limitations imposed by
low oxygen (and often low nitrogen or other nutrients) in standing water, the number
of species adapted to such habitats is necessarily small. The number and area of
habitats with a range of moisture availability ranging from seasonally inundated to
sometimes dry is relatively large, on the contrary. To imagine a submersed aquatic
origin for monocots, one would have to imagine them entering a very difficult,
limited habitat first, then spreading to habitats for which varied xylem and parenchyma histology is suitable. To be sure, there are some apparently ancient groups that
lack clearly defined vessels, such as Nymphaeales and Acorales, but these may have
survived precisely because they long ago entered minimally contested habitats.
In addition, if one hypothesizes aquatic origin for monocots, one must imagine
multiple origins of vessels, and multiple events in which vessels specialized in terms
of organography and morphology. These multiple events would have to be imagined
as having parallel outcomes instead of diverse ones. One would have to imagine that
vessels originated from tracheids, always yielding the same scalariform end wall
pattern, always simplifying the perforation plate in the same way.
Vesselless Stems and Leaves: Why so Common in Monocots?
Cheadle (1942, 1943a, b) posited that vessels originated first in roots and then spread,
in the course of evolution to stems, inflorescence axes, and leaves successively.
Accepting that this is true as a generalization, one could look at it in the reverse
perspective: progressive loss of all-tracheid conditions. Monocot species with stems
and leaves that lack vessels are perhaps as numerous as monocot species with vesselbearing stems and leaves, although some conspicuous and speciose families, such as
Cyperaceae and Poaceae do fall in the latter group (see Carlquist, 1975, p. 106). In
fact, acquisition of vessels in Cyperaceae and Poaceae may well have helped accelerate their evolution. They deal with the environment in ways quite different from
those of, say, the asparagalean families. Vessels throughout a plant body characterize
most non-monocot angiosperms. so the physiology of all-tracheid systems has been
neglected.
One explanation for maintenance of an all-tracheid xylem in stems and leaves has
to do with the sympodial habit of most monocots, in which roots are adventitious.
Author's personal copy
Monocot Xylem Revisited
133
Developmentally, vessels in adventitious roots cannot connect with vessels in a stem.
This disjunction between stem and root xylem necessarily produces differential
opportunities for roots and stems. The numerous species of bulbous monocots have
exploited this disjunction. Roots are rather ephemeral, and have xylem with (mostly)
simple perforation plates in vessels suited for rapid conduction during seasons when
moisture is available and frost does not exist. This formula is combined with alltracheid xylem in leaf bases and stems, which are perennial. The leaf bases and stems
can thereby persist through the dry season, the water columns of the tracheids
unlikely to embolize, the parenchyma of the leaves serving for water and photosynthate storage. In many bulbous monocots, the upper photosynthetic portions of the
leaves are succulent, and can persist well into the dry season (Calochortus, for
example), attenuating the growing and flowering season.
Similarly, orchid stems are different from orchid roots in the way they deal with
water economy—a fact that is doubtless basic to the amazing speciation of epiphytic
orchids with their succulent pseudobulbs and leaves. Orchids also have mechanisms
such as C4 photosynthesis (Silvera et al., 2010) and thick cuticles that provide ways
of dealing with the special water and light economy in the epiphytic mode of
existence.
Succulence and a suite of other features (Nobel & Hartsock, 1978, Woodhouse et
al., 1980; Nobel, 1988) permit Agave to combine large leaf size with an all-tracheid
xylem configuration in desert environments. Similar considerations apply to Yucca
(Smith et al., 1983).
Some monocots with vesselless stems and leaves can become trees. Aloë dichotoma, Beaucarnea recurvata, Cordyline australis, Dracaena draco, and Yucca brevifolia are among a number of species that could be mentioned in this regard. The
degree of arborescence of these species is not unlimited. All of them except Dracaena
have adventitious roots that apparently lack monocot cambia and are formed on a
widened base, or in some other fashion (Yucca brevifolia can form underground
stolons). Adventitious vessel-bearing roots can in these be continually formed to
supply the vesselless xylem of stems. The monocot cambium characterizes stems of
all of these arborescent forms, and thereby provides a way of increasing the stem
vasculature. There is, at the same time, an increase in either diameter or
number of the adventitious roots. All of the arborescent monocots may be said
to have succulent stems, and some of them have succulent leaves (Aloë most
obviously). The leaf boundary layers of arborescent monocots should be investigated
more fully, because they, like the transpiration reduction methods of orchids, can very
likely be correlated with the advantages and limitations of a vesselless system. In fact,
the work of Smith et al. (1983) provides considerable illumination on the ecophysiology of Yucca brevifolia and how it survives with an all-tracheid system in a desert
environment. .
Dracaena draco and other species of Dracaena have monocot cambium in roots,
as well as in stems. This means that except for the metaxylem that functions near the
tips of roots, Dracaena has a vesselless conductive system. As shown above, the
large diameter of tracheids formed from monocot cambia in roots of D. draco
probably compensates for the lack of vessels in the secondary bundles of stems and
roots. Monocot cambia always produce only tracheids in the secondary bundles. We
need more studies on arborescent monocots that link anatomy with function, because
Author's personal copy
134
S. Carlquist
arborescent monocots are, in fact, relatively little known. Lack of such studies is
probably the result of lack of commercial importance of arborescent monocots, and
the fact that most of them do not grow near major academic institutions.
Habit and habitat correlate very closely with xylem anatomy, and xylem anatomy
should be studied in this regard. The above observations, which may be regarded
merely as obvious, are illustrative of opportunities for study of all-tracheid systems in
stems and leaves of monocots in relation to habit and habitat. The all-tracheid xylem
found in stems and leaves of so many monocots is compatible with management of
moderate fluctuations in conductive rates, but there are many physiological mechanisms for maintaining lower conductive flux while maintaining plant size and variety
in leaf construction.
Is the vesselless condition in stems and leaves of the vast majority of Arales,
Alismatales, and Asparagales primitive or secondary? Parsimony would dictate that
multiple instances of loss of vessel-bearing metaxylem in these orders are unlikely to
have happened, and that if trees such as those of Davis et al. (2004) and that of Fig. 15
are valid, vessellessness in monocot stems and leaves is a symplesiomorphy.
Palms: Unique in Habit and Xylem
Palms do not have a monocot cambium, a salient fact that separates them from other
arboreal monocots. The widened bases of palm trunks are not the result of lateral
meristem activity, they are masses of accumulated roots. The fact that palms do not
have monocot cambia means that they have developed a series of xylem strategies
different from those of the arboreal monocots with monocot cambia (Kingia of the
Dasypogonaceae has very little if any monocot cambium activity, and offers some
comparisons with palms).
Palms often have vessels with simple perforation plates in roots, scalariform or
simple perforation plates in stem vessels with scalariform perforation plates in leaves
(Tomlinson, 1961; Klotz, 1977; Wagner, 1977). There are a few exceptions to this
pattern, and these exceptions prove unusually interesting.
Nypa is a prostrate palm of estuarine margins. Its stems are dichotomously
branched and prostrate. The root vessels have long scalariform perforation plates in
roots and stems (Klotz, 1977). Leaves have tracheids only. This xylem might be
expected if Nypa (one species, N. fruticans) were phylogenetically a basal branch of
Arecaceae, but it is not. In fact, the calamoid palms appear to be sister to the
remaining Arecaceae (Baker et al., 2009). Calamoids (the genus Calamus) have
simple perforation plates in roots and stems, and a mix of simple and scalariform
perforation plates in leaves (Tomlinson, 1961; Klotz, 1977)—a xylem conformation
one would call apomorphic within the family. This paradox may be explainable if we
take into account habit and ecology. Lianas tend to have wide vessels, in almost any
angiosperm group (Carlquist, 1975). Calamus is lianoid and has wide vessels (those
of Calamus stems 100–460 μm, with simple perforation plates: Klotz, 1977) in
almost any angiosperm group, and wider vessels tend to have simple perforation
plates (Carlquist, 1975). There are also nonlianoid calamoid palms, so that we need
not postulate the lianoid habit as symplesiomorphic in palms. The Cheadle dicta
(Cheadle & Tucker, 1961) would claim that nypoid and chamaedoroid palms could
not have been derived from calamoid palms. Cheadle did not take into account such
Author's personal copy
Monocot Xylem Revisited
135
factors as habit and vessel diameter, merely perforation plate morphology, in attempting to establish status of a particular group on a sort of phylogenetic ladder.
Nypa has comparatively narrow late metaxylem vessels in roots (120–130 μm in
diameter) and stems (80–120 μm in diameter). Klotz (1977) somewhat whimsically
wonders whether or not we should consider Nypa as a xerophyte because it grows
along estuaries which may vary in saltiness. The answer is no, because availability of
water, even if saline, is more important than mineral concentration. In Caryophyllales, Frankeniaceae have xeromorphic xylem. Frankeniaceae have relatively
shallow root systems that draw from soil depths that are not only salty but
often dry. In Frankeniaceae narrow vessels are in groups, an indication of
xeromorphy (Carlquist 1984a, 2010). The neighboring family Tamaricaceae taps
deeper levels that are perpetually moist, if saline, and thus has relatively mesomorphic xylem (vessels wide, solitary). Tamaricaceae are therefore "hydrohalophytes"
(Carlquist, 2010).
The phytelephoid ('vegetable ivory") palms have some pertinent tracheary element
details. In Ammandra roots, perforation plates are simple, 230–270 μm in diameter,
but in stems, only imperforate tracheary elements, 50–90 μm in diameter are reported
(Klotz, 1977). In Phytelephas. vessels of roots have simple perforation plates 170–
220 μm in diameter. Klotz (1977) reports stem vessels with scalariform perforation
plates in late metaxylem, 50–100 μm in diameter in one collection of Phytelephas,
but only imperforate tracheary elements, 30–70 μm in diameter in another. Although
the difference may seem slight, the occurrence of wider late metaxylem elements in
the collection observed to have vessels is suggestive. Phytelephas and Ammandra are
palms of wet tropical understory habitats (Dransfield et al., 2008).
Chamaedorea is an especially interesting palm genus where analysis of habit and
habitat and their relationship (or nonrelationship) to molecular trees are involved.
Both Cheadle (1942) and Klotz (1977) placed Chamaedorea as a "primitive" genus in
palms because it has scalariform perforation plates in vessels both in roots and stems.
The root late metaxylem vessels mostly range from 30–80 μm in diameter, whereas
those of stems are a little wider (50–100 μm). Baker et al. (2009) give Chamaedorea
a "crown group" rather than an early-diverging placement within palms. Chamaedorea is usually a palm of wet understory habitats, with some species relatively small
in stature. These habit/habitat features explain why late metaxylem of Chamaedorea
should have narrower vessels (lower and steadier transpiration and conduction rates).
If narrower vessels are more likely to have scalariform perforation plates, one can see
why Chamaedorea was thought by workers who were using conceptions prior to
those generated by molecular phylogenies to show more ancestral features. The role
of habit and habitat as well as vessel diameter cannot be neglected in assessing the
significance of perforation plate type. Chamaedorea may have had an unbroken
history of occupancy of mesic habitats.
As noted above, palms do not have monocot cambia and cannot produce secondary bundles. Therefore, one would hypothesize that palms have sieve-tube elements
with great longevity, and that has, in fact, been demonstrated (Parthasarathy &
Tomlinson, 1967; Parthasarathy, 1980). It has also been demonstrated in Kingia of
the Dasypogonaceae, (Lamont, 1980) which produces very few if any secondary
bundles. If phloem in palms has such great longevity, the xylem should also have
great longevity. Davis (1961) showed that root pressure in palms could exceed 10 m,
Author's personal copy
136
S. Carlquist
thus accounting for conductive characteristics of palms—perhaps most notably, how
embolisms could be reduced and cleared should they form.
The data of Klotz (1977) reveal a strong dimorphism between early metaxylem
tracheary elements of palms (frequently imperforate) and late metaxylem tracheary
elements (usually vessels, much wider than early metaxylem elements). This dimorphism is suggested in transectional views (e.g., Tomlinson, 1961). This dimorphism
is an ideal way of combining the conductive safety that tracheids have with the great
conductive effectiveness of metaxylem vessels. Tracheids have end walls that bear pit
membranes which do not permit passage of air bubbles from one tracheid to the next
in a vertical series. Tyree and Zimmermann (2002) figure parenchyma surrounding
large metaxylem palm vessels, a configuration that may support conduction by
regulating osmotic pressure of xylem through release of photosynthates into the
conductive stream, much like the concept of Sauter et al. (1973) in woody
angiosperms.
Some palm leaves thought to have long scalariform perforation plates in petioles
may actually have tracheids. SEM images of petiole tracheary elements of Actinokentia and Hyphorbe reveal that intact, though highly porose, pit membranes occur in
the end walls of petiole tracheary elements, which are therefore arguably tracheids
(Klotz, 1977).
Combined with these conductive features, palms offer mechanical division of
labor that lends itself to a variety of structural types—most notably the erect unbranched stem. Vessels and tracheids in palms do not have appreciable mechanical
strength compared with the bundle fibers. Fibers in bundles may be various in
quantity and pattern of distribution. Palms also demonstrate various degrees of wall
thickness and lignification of ground tissue, thereby also adding to mechanical
strength and stem hardness (Tomlinson, 1961, 1990).
Acorus: Tracheary Elements in a Pivotal Genus
Molecular-based phylogenetic reconstructions of the monocots (e.g., Fig. 15, Davis et
al., 2004) agree in placing Acorus, sole genus of Acoraceae, as the sister to the
remaining monocots. This basal position makes Acorus of special interest. Does
Acorus represent a xylem configuration symplesiomorphic within monocots? Does
it show xylem adapted to a particular habitat? The answers to these questions are
extraordinarily important because of the precedent they may set for interpretation of
other monocots.
Carlquist and Schneider (1997) examined Acorus gramineus Soland. roots and
found that pit membranes in end walls of tracheids have pores of various sizes. The
method used, that of cutting paraffin longisections of roots, and then removing
paraffin so that sections could be examined under SEM, has limitations, however.
Paraffin sections are relatively thin, so that only a few fragments of end walls are
available for study, and the context of these fragments is not always clear. A method
that we used subsequently (Carlquist & Schneider, 2010a), is much better. It involves
cutting longisections of liquid-preserved roots (or stems, etc.) with a single-edged
razor blade, followed by changes of distilled water and drying between slides under
pressure on a warming table. That method (used in original work in the present paper)
has the advantage of giving thick sections, in which large portions of vessels
Author's personal copy
Monocot Xylem Revisited
137
(sometimes entire end walls) are present. Because of the thickness of the sections, one
can view intact walls that have not been scraped by the blade (as well as some
surfaces that have been). The thickness also results in fewer fractures (as compared to
microtome sections) in pit membranes.
Using this new method, two species of Acorus are shown to have porose pit
membranes in root tracheary elements (Fig. 14a–c, e–f), and material of A. calamus
L. stems (Fig. 14d) had similar pit membranes. The pit membranes shown in Fig. 14
are somewhat different from those figured earlier (Carlquist & Schneider, 1997) in
having pit membranes that are more network-like than porose, but the effect is very
similar in both instances. Pit membranes are consistently present in end walls of
tracheary elements of Acorus roots and stems. Although earlier (Schneider & Carlquist, 1998), the porousness of these pit membranes was emphasized, leading to the
possibility that vessels could be said to be present, subsequent experience with
SEM studies of monocots suggests that pit membrane presence of any kind in
tracheary end walls is better considered under the rubric of "tracheid" or
possibly "pre-vessel." Physiologically, the presence of porous or meshworklike
pit membranes would likely confine air bubbles to a single tracheary element,
and this has been considered in the past to be a significant characteristic of
tracheids as opposed to vessel elements.
The end walls in pit membranes in Acorus tracheids (Fig. 14) are paralleled by the
conditions observed in Typha (Fig. 6), which occupies a very similar habitat. The endwall pits in Typha roots (Fig. 6 Both genera typically grow with submersed stems and
roots, but stems can also extend onto non-submerged ground provided that the soil
remains moist. Acorus leaf tips turn brown readily if soil moisture falls below
saturation levels. The presence of porose pit membranes in stem tracheary elements
of both genera could correlate with an active conductive stream, in turn related to the
sunny localities in which both grow combined with their access to abundant soil
moisture.
The lateral walls of Acorus tracheary elements have pits with non-porose pit
membranes (Fig. 14c), so there is differentiation between lateral walls and end walls
in this respect. There are differences between end walls and lateral walls with respect
to secondary wall structure: the bars between pits are slightly thinner on end walls
than on lateral walls, and the end wall pits slightly wider than those of lateral walls
(Fig. 14c), but the differences are not great. Such differences can be seen in tracheids
of Amborellaceae and Winteraceae also.
If we are to entertain the idea that Acorus xylem represents a symplesiomorphic
condition for monocots, we are forced to think that the habitat of Acorus is that of
ancestral monocots, and that there has been no change over time in the ecological
adaptations of Acoraceae. On the other hand, we may take a more inclusive view to
the effect that Acorus, with "pre-vessel" tracheids, may be considered vesselless but
with xylem expressions that correspond to occupancy of the aquatic—terrestrial
interface that characterizes Acorus habitats. This more inclusive view permits us to
consider monocots ancestrally vesselless, but recognizes some possibilities of diversity within the vesselless condition. Vessellessness is thus not a uniform condition,
but one that is subject to variations, if not to the extent that the vessel-bearing
condition is. Such an interpretation permits us to retain the concept that xylem does
correspond to ecology (taking into account other water economy adaptations such as
Author's personal copy
138
S. Carlquist
leaf shape, leaf surface moisture gradients, leaf anatomy, photosynthetic pathways,
etc.).
New Paradigms
Molecular phylogenies are now guidelines for how to interpret xylem evolution.
When data from habit, ecology, and physiology, xylem ontogeny, quantitative xylem
features, and SEM studies are incorporated, we reach quite new perspectives from
those reached by earlier workers. These should not be regarded as trends and certainly
not as dicta. Each example examined in the light of such a synthesis can help us in
assembling a larger picture and in exploring patterns.
What Controls Monocot Xylem Evolution?
Monocot xylem has evolved with response to ecology, but there is a wide range of
ways in which clades have shown adaptation. There is not an inexorable progression
of xylem specialization, as Cheadle's work (1942 et seq.) might seem to infer. For
example, most bulbs have only tracheids in leaves and stems, but vessels with simple
perforation plates in roots: an abrupt disjunction. Short duration of roots, persistence
of succulent leaf bases, drought deciduousness of leaf blades (sometimes with
attenuated longevity of leaf blades by means of succulence), and other features of
this growth form must be taken into account. To say that the xylem of leaves and
stems of bulbs remains "primitive" whereas that of the roots has "accelerated specialization" hides many important facts at best and may be misleading.
Although claimed to show irreversible progressions, evolution in monocot xylem
can feature apparent reversions. For example, the lack of vessels in submersed
aquatics such as Aponogetonaceae and Zosteraceae is an apomorphic condition, not
a primitive one, and probably involves an ontogenetic foreshortening, by forming no
late metaxylem.
Multiplicity of Expressions and Heterochrony as Factors in "Primitive" Xylem
Symplesiomorphic monocot xylem is a "porous" concept in that there is no single
xylem formulation one can cite in contemporary monocots that represents exactly
what the conductive tissue of the earliest monocotyledons was like. Monocots with
numerous symplesiomorphic features in xylem have probably had long and perhaps
unbroken histories of occupancy of mesic sites, but there are various ways in which
mesic sites can be exploited. Modification of foliage is certainly a persistent theme,
and one must take into account the multiplicity of linear/lanceolate leaf forms and
their modifications. One can trace changes in DNA sequences leading away from
symplesiomorphic monocots, but ancient DNA sequences do not necessarily correlate with ancient xylem structure. The global tree of monocots does permit us,
however, to identify key groups that will show us some important xylem transformations. For example, the calamoid palms, identified as an early branch of the
palm clade in molecular trees, have xylem adapted to particular niches, such as
lianoid growth forms, that relate to major reconfiguration of their xylem. Lianas as
Author's personal copy
Monocot Xylem Revisited
139
a whole have wide stem vessels and the wider the vessel, the more the likelihood of a
simple perforation plate. The lianoid calamoids have vessels that would not have been
identified as "primitive" by earlier workers. Chamaedoroid palms are a crown group,
but narrowness of vessels and a mesic understory habitat have favored retention in
that group of xylem with long scalariform perforations that in the past have been
interpreted as unqualified indicators of primitiveness. Phytelephoid palms have loss
of late metaxylem patterns and therefore can have a vesselless xylem that looks more
symplesiomorphic than it really is. Palms have tracheids in early metaxylem, but
prominent vessels in late metaxylem. By foreshortening this developmental sequence,
a kind of juvenilism, the phytelephoid palms have heterochronically attained this
condition, which is compatible with their wet forest habitats.
The Paradox of "Specialized" Xylem in Early-Departing Branches of Clades
Ecological interations must be taken into account in analyzing xylem; an earlydeparting brach of a clades may have adapted to highly seasonal conditions and have
apomorphic xylem (simple perforation plates in vessels) as have the apostasioid
orchids, may retain ancient DNA sequences. Apostasioids (a small, relictual group
compared to other orchids) may once have had species with long scalariform perforation plates in roots, species likely to be ancestral to orchids, but if so, those
apostasioids have apparently disappeared. One can also envision a rapid ecological
shift that coincided with departure of the apostasioid branch. The crown groups of
orchids may have changed little in xylem, while speciating extensively. At any rate,
the molecular tree of monocots must now be a guideline as to what changes in
monocot xylem took place. Apostasioids are sister to the remainder of orchids
(Kocyan et al., 2004). Cheadle and Tucker (1961) claimed that the apostasioids could
not possibly be ancestral to other orchids, based on xylem. The possibility that living
members of an early-departing clade might not represent all of the expressions that
once existed in that clade should have been considered by them. As a generalization,
Cheadle and Tucker (1961) claimed that "Because of its unidirectional course, vessel
specialization can be used primarily in negations; that is, a taxon with a certain level
(or levels) of vessel specialization cannot have been involved in the origin of another
with less specialized xylem in the same organs." Other examples that may seem
paradoxical until one takes a broader viewpoint include Boryaceae, Velloziaceae, and
Rhipogonaceae, as noted above. There is no reason why an early-departing branch of
a clade should not be, in fact, ecologically more exploitive and the remainder of the
clade rather conservative in preferences.
SEM has Changed Our Ideas About Monocot Tracheary Elements
Microstructure of the end walls of tracheary elements reveals pit membranes in end
walls of what appear, on the basis of light microscopy, to be vessel elements. These
SEM studies show that tracheids are more widespread in monocots than the listings of
Cheadle (1942); Fahn (1954) and Wagner (1977) would indicate. Among examples
are a number of orchids (Carlquist & Schneider, 2006) as well as Acoraceae,
Cyclanthaceae, Pandanaceae, and Philesiaceae, SEM studies of which appear in the
present paper. Klotz (1977) illustrates presence of pit membranes in scalariform end
Author's personal copy
140
S. Carlquist
walls in some palms previously thought to have scalariform perforation plates
(Actinokentia, Hyphorbe). Pit membranes in end walls of tracheary elements may
have various degrees of porousness, from being an open strand system to being
laminar with few holes. There is no way, other than an arbitrary (and therefore
probably meaningless) one, to place a boundary across this continuum.
Reports of vessel elements that have, say, 30 or more bars on the basis of light
microscopy need re-examination to see whether pit membranes may be retained in the
alleged perforations. End walls of longer tracheary elements are often poorly defined
and may grade into lateral wall pitting, contrary to the broad-lined ovals designating
end walls in the drawings in the Cheadle and Kosakai papers. .
The construction of data matrices for phylogenetic purposes and other uses for
anatomical data all too often demand categorization of tracheary elements as either
"tracheids" or vessel elements." Vessel elements with fewer than 30 bars on end walls
may be confidently recognized on the basis of light microscopy. The development of
SEM in relation to tracheary element type assignment has, however, made the
definitions very difficult. This is definitely a gain for understanding of the physiological nature of the conductive system. The presence of pit membranes and of pit
membrane remnants in end walls makes understanding xylem evolution by relating it
to ecological factors a more insightful process, because the intermediate conditions
are "non-missing links." The search for definitions should not drive or distort our
understanding of the evolution of structure.
Tracheary Element Length: Not an Indicator of Xylem Phylogeny in Monocots
Vessel element length and tracheid length are not phylogenetic indicators in monocots. The idea that longer tracheids and vessel elements are "more primitive" in
monocots has been repeatedly promulgated (Cheadle, 1942; Cheadle & Tucker,
1961), but in fact, neither Cheadle nor any other worker really attempted to demonstrate this. Very likely, Cheadle and others found that tracheary element length is not
really correlated with phylogenetic position or degree of departure from an ancestral
type in monocots, and simply did not present data on this feature for that reason.
Essentially, Cheadle based all of his intepretations of degree of phyletic advancement
in monocots on one feature, the number of bars on a scalariform perforation plate,
and, as a corollary, the distribution of various types of perforation plates systematically and organographically.
The idea that long tracheary elements are symplesiomorphic derives from the work
of Bailey and Tupper (1918), who did not, in fact, study monocots at all. In woody
angiosperms, Bailey and Tupper (1918) did obtain statistical correlations, but such
correlations cannot be carried over to monocots. They are inapplicable in monocots
because cambium is absent. The factors governing the length of fusiform cambial
initials in plants with vascular cambia and the factors governing length of procambium in monocots, which lack vascular cambia, are quite different. Degree of
elongation of tracheary elements in monocots is probably related to factors such as
internode length, rapidity of growth, organ size, and other factors. All of these, in
turn, undoubtedly have hormonal components. Research on what controls tracheary
element length in monocots is needed, and can very likely be obtained by quite
simple experiments and observations.
Author's personal copy
Monocot Xylem Revisited
141
Tracheary Element End Wall Pit Membranes: Diversity, Ontogeny, and Functional
Significance
Pit membranes in end walls of tracheary elements, as SEM studies show, are not all
alike. If they were, we could make a clear distinction between vessel elements and
tracheids, and such a distinction would probably be discernible even with light microscopy (perforation plates would be more clearly delimited than end walls of tracheids).
In fact, many tracheary elements of monocots, such as those in Orchidaceae, show
all degrees of transition between laminar and non-porose pit membranes versus and
presence of only a few threads as pit membrane remnants in pits of tracheary elements
of end walls (Carlquist & Schneider, 2006). In genera such as Cymbidium and
Phalaenopsis, pit membranes on tracheary element end walls of roots have a more
open end-wall meshwork, whereas those of stems show a smaller area devoted to
porosities. These is no clear delimitation between tracheids and vessel elements in
such genera.
The development of vessel elements features a hydrolysis of pit membranes in the
end wall (Butterfield & Meylan, 1982). Some end walls have more extensive microfibrillar networks in pit membranes than others, so when hydrolysis of the end walls
occurs, some become more porose than others. A cellulosic network is not evident in
the pit membranes of the end walls of maturing grass vessels (Carlquist & Schneider,
2011), but amorphous material is abundant. Microfibrillar networks in vessel element
perforations, when swept away by the conductive stream, may be present in lateral
ends of the perforations, probably because the center of the conductive stream exerts
more pressure, whereas the microfibrils at the lateral ends are under less tension from
the pressure of the stream. Different degrees of end wall hydrolysis and loss of the
microfibrillar network are characteristic of different species and, in monocots, the
various organs of the species. This has been demonstrated in woody angiosperms, in
which even perforation plates with relatively few bars/perforations (e.g., Bruniaceae)
may retain extensive pit membrane remnants (Carlquist 1992a, b).
"Neotracheids" may be a genuine phenomenon in some monocots: the tendency
for pit membranes to remain intact or nearly so in pit membranes of what on the basis
of having well-defined perforation plates might appear to be vessel elements. This
was figured above for Ophiopogon (Fig. 5e–f) and in Orchidaceae for stems of
Vanilla (Carlquist & Schneider, 2006). This phenomenon has been found in woody
angiosperms such as Myrothamnaceae (Carlquist, 1988) and cannot be ascribed to
lack of maturity of vessels, since it can be found repeatedly in particular species. This
may be a mechanism for phylogenetic return to the conductive safety of tracheid end
walls. Delimiting this phenomenon precisely from instances of pit membrane preservation in end walls of tracheary elements may not always be easy, but if pit
membranes are present in apparent perforation plates that are well differentiated from
lateral wall pitting, one could say that neotracheids may be present.
Adventitious Roots and the Root-Stem Juncture as a Valve
With regard to conduction in Agave deserti Engel., Ewers et al. (1992) say:
"During soil drying, the hydraulic conductance per unit pressure (Kh) declined
dramatically in the [root-stem] junctions and to a lesser extent in the roots, but not in
Author's personal copy
142
S. Carlquist
the stems. The decline in junction Kh was particularly important for A. deserti, which
lacks vessels in its stems, because even under wet conditions, its Kh was lower in
stems and junctions than in roots....The decline in Kh was due to embolism in the
connective tracheary elements at the junction. Such connective elements may be
particularly vulnerable ro embolism due to the large amount of unlignified primary
cell wall. Because the embolism is reversible, the junctions act as rectifiers. The high
Kh under wet conditions allows for rapid water uptake following rainfall, and low Kh
during drought helps limit water loss from the succulent shoots to a dry soil."
Vessels cannot be continuous from adventitious roots into stems, because of their
discontinuous ontogeny. The idea by Ewers et al. (1992) that the juncture between
root tracheary elements and stem tracheary elements is a valve that can insure oneway flow is logical and intriguing. Agave roots have much greater duration than those
of bulbs, in which functionality of roots is compressed between winter cold and
summer drought. Agave is, in fact, characteristic of summer-rainfall areas in which
winters are dry but without severe frost. Roots and leaves with long duration thus are
correlated with the advantages and limitations of the xylem in Agavaceae. The
ephemeral nature of roots in bulbs may be more important than the valve function
with respect to their short growth and flowering season.
The Ewers et al. (1992) concepts do explain why monocots have been able to
occupy such a wide range of habitats despite the limitations of adventitious roots. The
nature of adventitious roots requires them to draw from shallower soil levels than can
deep taproots in woody angiosperms. The idea that roots could lose water to dry soil
is probably not a function of the nature of xylem, but based on other facts.
There is broader significance in the Ewers et al. (1992) paper in that it joins data
from physiology with information about xylem anatomy. Most of our data on
conductive physiology are based on woody angiosperms, and the applicability of
physiological data from woody growth forms with high transpiration rates to monocots needs to be considered.
Vessellessness in Monocots: Conductive Safety, Structural Necessity, or
Relictualism?
Cheadle (1942, 1943a, b) envisioned the upward evolutionary progression of vessels
within the organs of monocotyledons: first roots, then stems, then inflorescence axes,
and then leaves. Such progression is not as inexorable as this scheme might suggest,
and Cheadle himself (1942) calls attention to some genera in which the progression is
not so simple (e.g., Dracaena).
Much attention has been focused on vesselless woody angiosperms, but little
attention has been paid to why vessellessness is so pervasive in monocots. The safety
of the all-tracheid system and the physiological limitations that early vessel-bearing
angiosperms may have encountered have been noted earlier (Carlquist, 1975, 1984a,
1985, 1988, 2012; Hacke et al., 2007; Sperry et al., 2007). There is a trade-off in the
ability of tracheids to resist formation and cell-to-cell transmission of embolisms on
the one hand and the inability of tracheids to be ideal capillaries that can deal with
peak flow and conduction speed on the other. Succulence, boundary layers (epidermis, cuticle) highly resistant to high transpiration rates, narrowness of leaves, crassulacean acid metabolism, and C4 photosynthesis, as noted earlier, are all mechanisms
Author's personal copy
Monocot Xylem Revisited
143
that are in play in the monocots with all-tracheid systems in stems and leaves. We
need to study xylem anatomy in relation to transpirational and flow characteristics.
In this regard, one notes that monocots with vessels in stems and leaves may have
some characteristics different from those of monocots that have only tracheids in
stems and leaves. Palms are an interesting example of a growth form with ecological
and habital capabilities that are different from those of the monocots with vesselless
stems and leaves. They, like grasses, may have conductive systems that operate to an
appreciable extent on root pressure, and thereby are able to occupy habitats different
from those of the monocots without vessels in stems and leaves.
Arborescence: Xylary Strategies and Limitations in Monocots
There are two major kinds of arborescence within monocots: the palm habit (with
absence of secondary bundles); and other arborescent forms with secondary bundles.
Palms have wide late metaxylem vessel elements in roots and stems. Such vessels can
be correlated with high transpirational demands, which in turn are related to the
massive size of leaves (which in turn are correlated with infrequency of branching in
palms). Lack of secondary bundles in palms requires compensation in the form of
great longevity in palm xylem and phloem, which can have durations that exceed
100 years. Palms are capable of unusually high root pressures, which may be
achieved by with the aid of parenchyma sheaths that can mediate ion and photosynthate content of vessels. The bundles in palm stems contain a xylary dimorphism:
imperforate early metaxylem tracheary elements (0 tracheids) combined with wide
late metaxylem vessels. This dimorphism provides both conductive safety and maximal flow rates. The syndrome of palm stems and roots and their xylem features does
not occur in other monocots, although Kingia (Dasypogonaceae) and Pandanus
(Pandanaceae) have some of the same features.
Other arborescent monocots have vesselless stems and leaves, mostly narrow
leaves (some species of Cordyline excepted), that are usually slender and have
various mechanisms for restricting transpiration (Napp-Zinn, 1984). In addition to
various degrees of succulence (notably in Aloë), one sees thick cuticles (Yucca), and
stomata sunken in grooves (Beaucarnea, Hesperoyucca) in the non-palm tree monocots. The transpiration limitations of such leaves correlate with the all-tracheid
constitution of the stem and leaf vascular bundles. Branching is much more frequent
in non-palm monocots than in palms.
The presence of a lateral meristem, here called the monocot cambium, which
produces secondary bundles in the non-palm monocots, adds to the conductive
capabilities of stems, and in most of these monocots, by far the majority of bundles
are secondary ones. The xylem in such bundles, however, consists wholly of tracheids. This is a consequence of the adventitious habit of roots, because there is no way
for vessels in adventitious roots to connect with those of stems. Secondary bundles
are also formed on roots in Dracaena draco and other species of Dracaena.
The non-palm arborescent monocots thus have limitations in plant size, flow
fluctuation capabilities, transpiration, restriction in number of leaves, and leaf surface
area. These limitations are balanced against the capabilities of an all-tracheid stem
and leaf xylem to resist spread of air embolisms from one xylem cell to another, and
the all-tracheid formula is in turn necessitated by the fact that vessels in roots must
Author's personal copy
144
S. Carlquist
end blindly where they contact stem bundles because of the adventitious nature of
roots. One should also take into account other features that factor into this formula,
such as crassulacean acid metabolism, which has been shown to exist in Agave, Aloë.
and Yucca (Nelson et al., 2005).
The Scalariform System in Angiosperm Tracheary Elements and Its Significance
While celebrating the remarkable success of the conifer torus-margo system in
coniferous tracheid pits, Pitterman et al. (2005) overlook the underlying significance
of associated pit shape. The torus-margo system works in conifers (including Gnetales) because the pits are circular. Thus, the slender threads of the margo (which offer
maximal conductive space between them for the margo holes) can carry the central
torus easily, because stress is distributed evenly throughout the margo. Displacement
of the torus to the pit aperture is thus easily accomplished. The great length of the end
wall of a conifer tracheid expands the conductive capabilities of the coniferous pit
very considerably. Radial widening of a conifer tracheid is not accompanied by
widening of pits. Instead, it is accompanied by replication of circular pits, so that
two or three series of circular bordered pits may be observed on some conifer walls
(Bailey, 1925), such as those of Sequoia. Pit redundancy rather than pit widening is
the strategy seen in the pits of coniferous tracheids (and in the vessels of Ephedra).
Even in primary xylem of conifers and Gnetales, one sees circular bordered pits
intercalated into the helical bands
Vesselless woody angiosperms all have scalariform widening of pits on end walls
of wider tracheids: Amborella (Carlquist & Schneider, 2001), Trochodendraceae
(including Tetracentron: Carlquist, 1988), and some Winteraceae (notably Tasmannia
and Zygogynum, but not Exospermum or Pseudowintera: Carlquist, 1989). All of the
early-diverging vessel-bearing woody angiosperms have scalariform perforation
plates on end walls of vessels, and this is certainly true of vessels in earlydiverging monocots as well.
Angiosperms seem, from their point of origin onwards, not to have had the genetic
information or developmental pathways to replicate the conifer pattern. From the
outset, the conifer-margo pattern seen in conifers was absent.
The formation of scalariform pits in end walls of vessels and tracheids in angiosperms does not permit a torus-margo system like that of conifers. The stresses on
margo threads would not be equally distributed on the margo, and thus the torus
would not be a reliable closure device. Instead, angiosperms have invented pit
membranes of various thicknesses. While some of these have what have been called
tori or pseudotori (Dute & Rushing, 1987; Rabaey et al. 2006), they lack the
important feature of a coniferous torus-margo system: the wide margo spaces that
enhance conduction. One compensation for this lack, in vesselless species, is thinness
of pit membranes. The pit membranes of Amborella are very thin and break easily
during handling, so some have even considered them to be absent at maturity (Feild et
al., 2000), but in fact, they are present if handled correctly and are highly porous
(Carlquist & Schneider, 2001). This is true in Bubbia also (Carlquist, 1983). Thin,
easily broken but porous pit membranes may be tolerable because in the habitats
where these vesselless angiosperms grow, deflection of the pit membranes (due to
pressure changes among tracheids) is likely to be minimal. Thin porous membranes in
Author's personal copy
Monocot Xylem Revisited
145
end walls of tracheids—and then vessels—may be the angiospermous compensation
for lack of the margo spaces that conifers have. There is no differentiation between
end walls and lateral walls in coniferous tracheids. Jansen et al. (2009) have shown
that thinner pit membranes (as on vessel element end walls) have larger pores. In
angiosperms, however, lateral walls of vessels have relatively non-porous (and
variously thick) pit membranes, which resist deflection and aspiration at the cost of
lowered conduction of water. Conduction is achieved by the porous end walls. This is
shown well by orchids (Carlquist & Schneider, 2006; see above also). The selective
pressure to develop wider tracheids (and thereby scalariform end walls, and subsequent to that, scalariform perforation plates in vessel elements) in angiosperms comes
from the value of wider capillaries (conductivity equal to the fourth power of the
diameter, the Hagen-Poiseuille equation), so that widened capillaries of vessels, even
if only a little wider than tracheids, have enhanced conductivity by virtue of the total
area of the perforations on the end walls, and the permeability to water flow of the
thin porous pit membranes in the end walls. Ellerby and Ennos (1998) find that
resistance of the end walls is not substantial conpared to the resistivity to conduction
of the lateral walls in angiosperm vessels. Hacke et al. (2007) offer a dimmer view of
the advantage of the vessel, at least in its early evolutionary states. However, more
primitive woods tend to occur in such places as cloud forests with wet soil and humid
air, where demands on the conductive system for conductive efficiency are modest.
Thus angiosperms have exploited a scalariform system with advantages and
disadvantages quite unlike those of the circular bordered pit system of gymnosperms.
Similarities in the tori or pseudotori of some angiosperm pits (Dute & Rushing, 1987;
Rabaey et al., 2006) to the coniferous pit, with its highly conductive margo portion,
are misleading. Angioperm tori and pseudotori may aid in pit aspiration (closure), but
the accompanying margos are not at all like those of conifers in conductive ability,
and the great area of pits on conifer end walls has no counterpart in angiosperms.with
tori or pseudotori. Angiosperms have followed paths of end wall dimorphism (perforation plates different from lateral wall pitting) and varied thicknesses of pit
membranes, a series of adaptations entirely different from those of conifers.
Conductive Problems in Monocots: What is Involved?
The conductive system of vascular plants consists of dead cells—tracheids and/or
vessels. Or does it? Experimental work on how xylem functions has been done
mostly on woody species, because they are more convenient experimental material.
In woody angiosperms, an emerging picture trends to show that early angiosperms
have high resistivity and low vulnerability in xylem: they conduct less efficiently but
cavitate infrequently (Carlquist, 2012). This trend is not without exceptions—and
ecological shifts that may be accompanied by new structural modes. In clades that
have moved into drier habitats, the balance frequently shifts toward low resistivity but
with higher vulnerability—daily cavitations occur and must be refilled (Vogt, 2001).
This seeming paradox is explained by the fact that in order to capture one molecule of
CO2, a plant may have to lose several hundred water molecules (Jones, 1992), a
process colorfully described by Holbrook et al. (2002) as "foraging" with an attendant
cost. Risk reduction can occur in the form of CAM photosynthesis (Agave) or C4
photosynthesis (grasses), in which nocturnal opening of stomata involves lowered
Author's personal copy
146
S. Carlquist
loss of water while achieving CO2 absorption.. Cavitation can be repaired even while
a plant experiences negative pressures in xylem, as demonstrated in Oryza (Stiller et
al., 2005).
Risk reduction is not risk elimination. How do plants reverse embolisms if they
occur frequently, even daily? In the case of woody plants, the answer appears to
reside in the activity of axial parenchyma cells that accompany vessels (Holbrook et
al., 2002). Indeed, there is no other obvious explanation for the common occurrence
of axial parenchyma in woody angiosperms (Carlquist, 2012)—axial parenchyma can
serve in water or photosynthate storage, but that is not prominent in most woods, nor
would it explain the vessel-centered distribution of most axial parenchyma in woods
that do not have a tracheid background.. In the case of monocots, axial parenchyma is
not present, but metaxylem vessels are often sheathed with parenchyma (Metcalfe,
1960; Tomlinson, 1961, 1969, 1990) that may have an equivalent function.
As stated by van Ieperen (2007), "there is increasing support for the idea that ions
in xylem sap can influence the hydraulic conductance of the xylem in plants." Porous
pit membranes may permit water flow from one tracheary element to another, but at a
cost: more than 80 % of the resistance to flow in xylem is provided by the pit
membranes (Tyree & Zimmermann, 2002; Choat et al., 2006). Is there any way of
changing this in a living plant? One recent idea (Holbrook et al., 2002) cites "hydrogels.": "With increasing concentrations of ions, these hydrogels are hypothesized to
shrink, increasing the porosity of the pit membrane and thus decreasing its resistance
to water flow" (Holbrook et al., 2002). The implications of this for the pores in end
walls of monocot tracheids are especially interesting, because of the abundance of
vesselless tissues in aerial portions in so many monocots. Transfer of water from one
tracheid to the next in a vertical series is mediated by pores in end walls—which both
confer safety (confining air bubbles to individual tracheids) and decrease flow. The
implications also apply to vessels, in that perforations plates permit maximal conductive flow but lateral wall pits are often in contact with other vessels in monocots.
The porous pit membranes in end walls of vessel elements in some monocots, such as
those of orchids and others cited in this paper, may relate to hydrogel presence, and
explain why pit membranes have been retained in end walls of otherwise vessel-like
tracheary elements of some monocots.
Monocot Origins
Molecular phylogenies as well as anatomical evidence favor the origin of monocots
from vessel-bearing basal angiosperms. The contention by Cheadle (1953) that
vessels evolved independently in monocots and dicots can no longer be supported
—at least in the way Cheadle envisioned it. All recent global molecular phylogenies
of angiosperms (e.g., APG III, 2009) show monocots nested within basal angiosperms, all of which except for Amborellales and Nymphaeales are considered to
have vessels (or to have lost them secondarily, as in Winteraceae). The angiosperms
closest to the origin of monocots include Chloranthaceae and the Piperales (Aristolochiaceae, Lactoridaceae, Piperaceae, and Saururaceae), all of which do have vessels. By reduction of cambial activity in stems like those of Chloranthaceae or
Saururaceae, one can achieve monocot-like stem structure (Carlquist, 1992a, b,
2009) with respect to bundles and ground tissue. The three-dimensional patterns of
Author's personal copy
Monocot Xylem Revisited
147
bundles in these families differ from those of monocots. Certainly pertinent is the fact
that Chloranthales and Piperales are sympodial and have adventitious roots (Carlquist, 2009), circumstances probably basic to monocots, in which those interrelated
features are symplesiomorphic. One could also imagine very long scalariform vessel
elements in monocots, such as those of Astelia, to have been derived from similar
vessels in Chloranthaceae.
Is it conceivable that the earliest monocots may have been vesselless? That
possibility cannot be ruled out entirely, and Chloranthaceae show why. Primary
xylem and, in the stems, even secondary xylem of Sarcandra is vesselless, as claimed
by Bailey and Swamy (1950). The report of Takahashi (1988) that shows some
alteration in a few pit membranes of secondary xylem stem tracheids of Sarcandra,
based on TEM, does not give convincing evidence. There is no differentiation among
the stem tracheids of Sarcandra, all of which are monomorphic in diameter and
pitting. There is dimorphism in tracheary elements in the secondary xylem of roots of
Sarcandra, and vessels are demonstrably present there (Carlquist, 1987, 2009).
However, if the secondary xylem of chloranthoids like Sarcandra were reduced
phylogenetically, one would obtain a vesselless condition.
Imagining why a chloranthoid such as Sarcandra would lose vessels is another
matter. Saururaceae, the marsh-inhabiting close relatives of Chloranthaceae, have
nearly lost cambial activity in stems, but they have not lost metaxylem vessels.
Progression to the habit of a submersed aquatic would probably be a necessary step
in such a phylesis. Genera of Alismatales with emergent leaves, such as Sagittaria,
have vessels in roots (Wagner, 1977; Tomlinson, 1983).
Acorus, which has generally been considered sister to the remaining monocots
(Davis et al., 2004; APG III, 2009) may prove, depending on one's terminology, to be
entirely vesselless or with tracheidlike vessels, because pit membranes on tracheary
element end walls in roots are reticulate to somewhat porous on end walls of roots,
and vessels are lacking in stems (Carlquist & Schneider, 1997); see also above.
Cheadle (1942) regarded Acorus as having vessels in roots, but he did not have the
benefit of SEM, which proves crucial in these matters.
The next most basal branch of the monocot tree (Fig. 14), Arales, does have
vessels in roots (Cheadle, 1942, Carlquist & Schneider, 1998; Schneider & Carlquist,
1998), although the tribe Orontieae, sister to the remaining Araceae (French et al.,
1995) has not been monographed with respect to xylem.
If one imagines a scenario in which monocots originated in an aquatic environment and had little metaxylem, and subsequently acquired late metaxylem with
tracheary elements wide enough to develop into vessels, monocots could have
originated in an aquatic environment—probably with stems mostly submersed. The
problem with this "mostly submersed" scenario is that basal pre-monocot angiosperms would have had to have entered the aquatic environment, perhaps as submersed aquatics to account for vessel absence. Niches for submersed aquatics are
relatively few and require a series of concurrent adaptations for dealing with low
oxygenation and other features. In any case, the vast radiation of monocots would
have occurred after vessels were acquired according to this scenario. Origin of vessels
is conceivable in an aquatic monocot that has active transpiration in leaves but grows
in moist soil. Acoraceae and Typhaceae exemplify functionally vesselless monocots
that have what I would consider tracheids representing a "pre-vessel" condition. One
Author's personal copy
148
S. Carlquist
should note that various degrees of intermediacy in expression must be reflected in
terminology now that we have SEM information. We can no longer pretend that light
microscopy can be the sole method on which concepts of tracheary elements is based.
The other available hypothesis would place monocot origin in moist terrestrial
environments, such as at the margins of streams and lakes, or in marshes subject to
water fluctuation. In this "moist terrestrial" scenario, monocots would have originated
from basal angiosperms that had limited vascular cambial activity. This would
explain why early monocots would have vessels in roots (an adaptive feature that
permits rapid uptake of water rapidly from soil as it dries or begins to dry). Campynemataceae, Taccaceae, and Lapageria of the Philesiaceae might exemplify cases of
vesselless monocots living in moist but not aquatic environments.
Vessellessness in shoots and leaves characterizes many species of monocots
(chiefly Arales, Liliales, and Asparagales), and is often coupled with devices to limit
transpiration. The disjunction between vessel-bearing roots and vesselless stems has
certainly not deterred radiation of monocots, which have taken advantage of this
feature in habitats with frequently-changing moisture availability. Vessels in adventitious roots cannot connect to vessels in stems, so adventitious roots and the
associated sympodial (often rhizomatous or prostrate) branching systems associated
with adventitious roots in monocots have a water conduction system in which
vessellessness in stems and leaves is not disadvantageous, provided that high peak
volumes of water are not required to be transferred from roots into stems. The earliest
angiosperms appear to have been sympodial (Carlquist, 2009). There are many
favorable habitats for sympodial growth forms, as shown by both monocots and
ferns. Taproots are not adaptive in environments which become so moist that
oxygenation is problematic. Prostrate sympodial growth forms are advantageous in
this case. Prostrate sympodial stem systems are also excellent for colonizing wider
areas, in contrast to the territorial restriction imposed by having a taproot system
coupled with upright stems.
The differences between sympodial systems with adventitious roots and monopodial systems with taproots are profound. Monocots certainly exemplify the former,
and show some unappreciated correlations. In a prostrate sympodial system, available
moisture is limited to relatively superficial soil layers—or to aquatic and semi-aquatic
systems (palms and a few other monocots are exceptions). Related to this, very likely,
is the vesselless condition of many monocot stems and leaves, because a tracheidonly system offers conductive safety that can counter the fluctuations in moisture
ability of upper soil levels (taproots are advantageous where a water table can be
reached by roots). Restricted leaf surface (and other foliar modifications) are related
to the sympodial habit by virtue of greater fluctuation in moisture availability also:
the linear to lanceolate shape of leaves of many monocots exemplifies this, but such
leaves, as with conifer needles, are adaptive where light levels are high. Broader, netveined leaves in monocots (most commonly found in species of shady habitats) have
been shown to have originated at least 26 times and lost eight times in monocots
(Givnish et al., 2005).
The lack of cambium in monocots can be understood in terms of the progressive
death and decay of older portions of the sympodial system. Investment in secondary
tissue would not be economical if any given rhizome portion is relatively short-lived,
and newer portions are served by adventitious roots. To be sure, monocots that
Author's personal copy
Monocot Xylem Revisited
149
produce additional bundles from a monocot cambium are exceptions to this, but such
monocots can be seen as having superimposed a new vascular formula onto a basic
monocot vascular system as seen in, say, Arales or Zingiberales. Monocots with
additional bundles are also upright, and therefore tend to escape from the limitations
of the prostrate system with respect to light-gathering capabilities and also, indirectly,
water acquisition (roots can have longer duration if attached to stems of indefinite
longevity). These considerations, as well as the molecular evidence, show that
arborescence does not represent the ancestral life form in monocots. The idea that a
monocot cambium ("secondary thickening meristem") was a symplesiomorphic feature in monocots was proposed by Rudall (1991), but is not supported by recent
phylogenetic work.
The differences between the "aquatic" and "moist terrestrial" hypotheses are not
great. The differences between tracheids with porous membranes in end walls and
vessel elements in which pit membranes are swept away by the conductive stream
likewise are not great. The numerous shifts and radiations in early basal angiosperms
have probably masked forever the precise nature of the earliest angiosperms in
general, and the earliest monocots in particular. We may wish for plants to show us
ancient structural modes, but in fact, survival to the present demands constant
modifications that meet contemporary requirements. Comparative anatomy of living
plants should be interpreted primarily in terms of present-day functions and ecology.
Plant structure does not evolve independently of function, ecology, and habit. The
case of Acorus shows us that vesselless and vessel-bearing conditions are not sharply
defined (a fact made abundantly clear by SEM studies), but both offer a range of
possible structures. Trying to define vesselless and vessel-bearing so as to be mutually exclusive not only runs counter to observed fact, it makes the evolutionary shifts
in xylem evolution more difficult to understand.
Acknowledgements The encouragement and help of Edward L. Schneider, with whom I collaborated
earlier in SEM studies of monocot xylem, are much appreciated. Materials for original SEM data reported
here came from various sources, notably including the National Tropical Botanical Garden, the Fairchild
Tropical Garden, and the Lotusland Foundation. David Lorence, Ken Wood, Kevin Kenneally, and Virginia
Hayes deserve special thanks for collecting and sending liquid-preserved materials. Thomas J. Givnish
kindly gave permission for use of the phylogenetic tree reproduced in Fig. 15. Dr. Larry H. Klotz, of
Shippensburg University, gave me a copy of his 1977 Cornell thesis on palm xylem, and this unpublished
document, rich in data, has been of substantial importance. John Garvey deserves special acknowledgement
for his aid in preparation of illustrations. Dennis W. Stevenson provided valuable editorial support.
Literature Cited
APG III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of
flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105–121.
Bailey, I. W. 1925. Some salient lines of specialization in tracheary pitting. I. Gymnospermae. Annals of
Botany 39: 587–598.
——— 1944. The development of vessels in angiosperms in morphological research. American Journal of
Botany 31: 421–428.
——— & B. G. L. Swamy. 1950. Sarcandra, a vesselless genus of the Chloranthaceae. Journal of the
Arnold Arboretum 31: 117–129.
——— & W. W. Tupper. 1918. Size variation in tracheary cells. I. A comparison between the secondary
xylems of vascular cryptogams, gymnosperms, and angiosperms. Proceedings of the American
Academy of Arts and Sciences 54: 149–204.
Author's personal copy
150
S. Carlquist
Baker, W. J., V. Savolainen, C. B. Asmussen-Lange, M. W. Chase, J. Dransfield, F. Forest, M. M.
Harley, N. W. Uhl & M. Wilkinson. 2009. Complete generic level phylogenetic analyses of palms
(Arecaceae) with comparisons of ssupertree and supermatrix approaches. Systematic Botany 58: 240–
256.
Bessey, C. E. 1915. The phylogenetic taxonomy of flowering plants. Annals of the Missouri Botanical
Garden 2: 109–164.
Bierhorst, D. W. & P. M. Zamora. 1965. Primary xylem elements and element associations of angiosperms. American Journal of Botany 52: 657–710.
Butterfield, B. G. & B. A. Meylan. 1982. Cell wall hydrolysis in the tracheary elements of the secondary
xylem. In: P. Baas (ed). New perspectives in wood anatomy (pp 71-84). Martinus Nijhoff, Publishers,
The Hague.
Carlquist, S. 1975. Ecological strategies of xylem evolution. University of California Press, Berkeley.
——— 1980. Further concepts in ecological wood anatomy, with comments on recent work in wood
anatomy and evolution. Aliso 9: 499–553.
——— 1983. Wood anatomy of Bubbia, with comments on the origin of vessels in dicotyledons. American
Journal of Botany 70: 578–590.
——— 1984a. Vessel grouping in dicotyledons: significance and relationship to imperforate tracheary
elements. Aliso 10: 505–525.
——— 1984b. Wood anatomy of Lardizabalaceae, with comments on the vining habit, ecology, and
systematics. Botanical Journal of the Linnean Society 88: 257–277.
——— 1985. 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.
——— 1987. Presence of vessels in Sarcandra (Chloranthaceae); comments on vessel origins in angiosperms. American Journal of Botany 74: 1765–1771.
——— 1988. Comparative wood anatomy. Springer Verlag, Heidelberg.
——— 1989. Wood anatomy of Tasmannia; summary of wood anatomy of Winteraceae. Aliso 12: 257–
275.
——— 1992a. Pit membrane remnants in perforation plates of primitive dicotyledons and their significance. American Journal of Botany 79: 660–672.
——— 1992b. Wood anatomy of Chloranthus; summary of wood anatomy of Chloranthaceae, with
comments on vessellessness, and the origin of monocotyledons. IAWA Bulletin, new series 13: 3–16.
——— 2007. Successive cambia revisited: ontogeny, histology, diversity, and functional significance.
Journal of the Torrey Botanical Society 134: 301–332.
——— 2009. Xylem heterochrony: an unappreciated key to angiosperm origins and diversification.
Botanical Journal of the Linnean Society 161: 26–65.
——— 2010. Caryophyllales: a key group for understanding wood anatomy characters and their evolution.
Botanical Journal of the Linnean Society 164: 342–393.
——— 2012. How wood evolves: a new synthesis. Botany (in press).
Carlquist, S. & E. L. Schneider. 1997. Origins and nature of vessels in monocotyledons. 1. Acorus.
International Journal of Plant Sciences 158: 51–56.
——— & ———. 1998. Origins and nature of vessels in monocotyledons. 5. Araceae subfamily
Colocasioideae. Botanical Journal of the Linnean Society 128: 71–86.
——— & ———. 2001. Vegetative anatomy of the New Caledonian endemic Amborella trichopoda. New
data, relationships with Illiciaceae, and implications for vessel origin and definition. Pacific Science
55: 305–312.
——— & ———. 2006. Origins and nature of vessels in monocotyledons. 8. Orchidaceae. American
Journal of Botany 93: 963–971.
——— & ———. 2010a. Origins and nature of vessels in monocotyledons. 1. Primary xylem microstructure, with examples from Zingiberales. International Journal of Plant Sciences 171: 258–266.
——— & ———. 2010b. Origins and nature of vessels in monocotyledons. 12. Pit membrane microstructure diversity in tracheary elements of Astelia. Pacific Science 64: 607–618.
——— & ———. 2011. Origins and nature of vessels in monocotyledons. 13. Scanning electron
microscopy studies of xylem in large grasses. International Journal of Plant Sciences 172:
Carlquist, S., E. L. Schneider & K. Kenneally. 2008. Origins and nature of vessels in monocotyledons.
10. Boryaceae: xeromorphic xylem structure in a resurrection plant. Journal of the Royal Society of
Western Australia 91: 13–20.
——— & S. Zona. 1988. Wood anatomy of Papveraceae, with comments on vessel restriction paterns.
IAWA Bulletin new series 9: 253–267.
Chase, M. 2004. Monocot relationships: an overview. American Journal of Botany 91: 1645–1655.
Author's personal copy
Monocot Xylem Revisited
151
———, et al. 1993. Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene
rbcL. Annals of the Missouri Botanical Garden 80: 528–580.
———, M. F. Fay, D. S. Devey, O. Maurin, N. Ronsted, J. Davies, Y. Pillon, G. Peterson, O. Seberg,
M. N. Tamura, C. B. Asmussen, K. Hilu, T. Borsch, J. I. Davis, D. W. Stevenson, J. C. Pires, T. J.
Givnish, K. J. Sytsma, M. M. McPherson, S. W. Graham & H. S. Rai. 2006. Multi-gene analyses of
monocot relationships: a summary. Pp 63–75. In: J. T. Columbus, E. A. Friar, J. M. Porter, L. M.
Prince, & M. G. Simpson (eds). Monocots: Comparative Biology and Evolution (including Poales).
Rancho Santa Ana Botanic Garden, Claremont, CA.
Cheadle, V. I. 1937. Secondary growth by means of a thickening ring in certain monocotyledons. Botanical
Gazette 98: 535–555.
——— 1942. The occurrence and types of vessels in the various organs of the plant in the Monocotyledoneae. American Journal of Botany 29: 441–450.
——— 1943a. The origin and certain trends of specialization of the vessel in the Monocotyledoneae.
American Journal of Botany 30: 11–17.
——— 1943b. Vessel specialization in the late metaxylem of the various organs in the Monocotyledoneae.
American Journal of Botany 30: 484–490.
——— 1953. Independent origin of vessels in the monocotyledons and dicotyledons. Phytomorphology 3:
23–44.
——— 1963. Vessels in Iridaceae. Phytomorphology 13: 245–248.
——— 1968. Vessels in Haemodorales. Phytomorphology 18: 412–420.
——— & H. Kosakai. 1971. Vessels in Liliaceae. Phytomorphology 21: 320–333.
——— & J. M. Tucker. 1961. Vessels and phylogeny of Monocotyledoneae. In Recent Advances in
Botany (pp. 161-165). University of Toronto Press, Toronto.
Choat, B., T. W. Brodie, A. R. Cobb, M. A. Zieniecki & N. M. Holbrook. 2006. Direct measurement of
intervessel pit membrane hydraulic resistance in two angiosperm tree species. American Journal of
Botany 93: 993–1000.
Clearwater, M. J. & G. Goldstein. 2005. Embolism repair and long distance water transport. Pp 375–400.
In: N. M. Holbrook & M. A. Zwieniecki (eds). Vascular transport in plants. Elsevier Academic Press,
Oxford.
Davis, T. A. 1961. High root pressures in palms. Nature 192: 277–278.
Davis, J. I., D. W. Stevenson, G. Petersen, O. Seberg, L. M. Campbell, J. V. Freudenstein, D. H.
Goldman, C. H. Hardy, F. A. Michelangeli, M. P. Simmons, C. D. Specht, F. Vergara-Silva & M.
Gandolfo. 2004. A phylogeny of the monocots, as inferred from rbcL and atpA sequence variation, and a
comparison of methods for calculating jacknife and bootstrap values. Systematic Botany 29: 467–510.
Dransfield, J., N. Uhl, C. Asmussen, W. J. Baker, M. Harley & C. Lewis. 2008. Genera palmarum. The
evolution and clasification of palms. Royal Botanic Garden, Kew, Kew Publishing.
Dute, R. R. & A. E. Rushing. 1987. Pit pairs with tori in the wood of smanthus americanus. IAWA
Bulletin, new series 8: 237–244.
Ellerby, D. J. & A. R. Ennos. 1998. Resistance to fluid flow of model xylem vessels with simple and
scalariform perforation plates. Journal of Experimental Botany 49: 979–985.
Ewers, F. W. 1985. Xylem structure and water conduction in conifer trees, dicot trees, and lianas. IAWA
Bulletin, new series 6: 309–317.
———, G. B. North & P. S. Nobel. 1992. Root-stem junctions of a desert monocotyledon and a
dicotyledon: hydraulic consequences under wet conditions and during drought. New Phytologist
121: 377–385.
———, H. Cochard & M. T. Tyree. 1997. A survey of root pressures in vines of a tropical lowland forest.
Oecologia 110: 191–196.
Fahn, A. 1954. Metaxylem elements in some families of the Monocotyledoneae. New Phytologist 53: 530–
540.
Feild, T. S., H. A. Zwieniecki, T. Brodribb, T. Jeffrey, M. J. Donoghue & N. M. Holbrook. 2000.
Structure and function of tracheary elements in Amborella trichopoda. International Journal of Plant
Sciences 161: 705–712.
Fisher, J., G. Angeles, F. W. Ewers & J. Lopez-Portillo. 1997a. Survey of root pressure in tropical vines
and woody species. International Journal of Plant Sciences. 158: 44–50.
Fisher, J. B., H. Cochard & M. T. Tyree. 1997b. A survey of root pressures in vines of a tropical lowland
forest. Oecologia 110: 191–196.
French, J. C., M. G. Chung & Y. K. Hur. 1995. Chloroplast DNA phylogeny of the Ariflorae. Pp 255–
175. In: P. J. Rudall, P. J. Cribb, D. F. Cutler, & C. J. Humphries (eds). Monocotyledons: systematics
and evolution. Royal Botanic Gardens, Kew.
Author's personal copy
152
S. Carlquist
Frost, F. H. 1930a. Specialization in secondary xylem in dicotyledons. I. Origin of vessel. Botanical
Gazette 89: 67–94.
——— 1930b. Specialization in secondary xylem in dicotyledons. II. Evolution of end wall of vessel
segment. Botanical Gazette 90: 198–212.
——— 1931. Specialization in secondary xylem in dicotyledons. III. Specialization of lateral wall of vessel
segment. Botanical Gazette 91: 88–96.
Givnish, T. J., J. C. Pires, S. W. Graham, M. A. McPherson, L. M. Prince, T. B. Patterson, H. S. Rai,
E. H. Roalson, T. M. Evans, W. J. Hahn, K. C. Millam, A. W. Meerow, M. Molivray, P. J. Kores,
H. E. O'Brien, J. C. Hall, W. J. Kress & K. J. Sytsma. 2005. Repeated evolution of net venation and
fleshy fruits among monocots in shaded habitats confirms a priori predictions: evidence from an ndhF
phylogeny. Procedings of the Royal Society B 272: 1481–1490.
———, J. H. Leebens-Mack, M. Ames Sevillano, J. R. McNeal, P. R. Steele, J. I. Davis & C. Ané.
2010. Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of
Poales. Annals of the Missouri Botanical Garden 87: 584–616.
Hacke, U., J. S. Sperry, T. S. Feild, Y. Sano, E. H. Sikkema & J. Pitterman. 2007. Water transport in
vesselless angiosperms: conductive efficiency and cavitation safety. International Journal of Plant
Sciences 1168: 1113–1126.
Hargrave, K. R., K. L. Kolb, F. W. Ewers & S. D. Davis. 1994. Conduit diameter and drought-induced
embolism in Salvia mellifera Greene (Labiatae). New Phytologist 126: 695–705.
Holbrook, N. M. & M. A. Zwieniecki. 1999. Embolism repair and xylem tension: do we need a miracle?
Plant Physiology 120: 7–10.
———, ——— & P. J. Melcher. 2002. The dynamics of "dead wood": maintenance of water transport
through plant stems. Integrative and Comparative Biology 42: 493–496.
Jansen, S., B. Choat & A. Pletsers. 2009. Morphological variation of intervessel pit membranes and
implications to xylem function in angiosperms. American Journal of Botany 96: 409–419.
Jones, H. G. 1992. Plants and microclimate: a quantitative approach to environmental plant physiology.
Cambridge University Press, Cambridge.
Judd, W. S., W. L. Stern & V. I. Cheadle. 1993. Phylogentic position of Apostasia and Neuwiedia
(Orchidaceae). Botanical Journal of the Linnean Society 13: 87–94.
Keating, R. C. 2003. The anatomy of monocotyledons. IX. Acoraceae and Araceae. Clarendon, Oxford.
Klotz, L. H. 1977. A systematic survey of the morphology of tracheary elements in palms. Ph. D. Thesis,
Cornell University, Ithaca.
Kocyan, A., Y.-L. Qiu, P. K. Endress & E. Conti. 2004. A phylogenetic analysis of Apostasioideae based
on ITS, trnL-F and matK sequences. Plant Sytematics and Evolution 247: 203–213.
Kohonen, M. M. & A. Helland. 2009. On the function of wall sculpturing in xylem conduits. Journal of
Bionic Engineering 6: 324–329.
Kribs, D. A. 1935. Salient lines of structural specialization in the wood rays of dicotyledons. Botanical
Gazette 96: 547–557.
——— 1937. Salient lines of structural specialization in the wood parenchyma of dicotyledons. Bulletin of
the Torrey Botanical Club 64: 177–186.
Lamont, B. B. 1980. Tissue longevity of the arborescent monocotyledon, Kingia australis (Xanthorrhoeaceae). American Journal of Botany 67: 1262–1264.
McCully, M. E., C. X. Huang & L. E. C. Ling. 1998. Daily embolism and refilling of xylem vessels in the
roots of field-grown maize. New Phytologist 138: 327–342.
Metcalfe, C. R. 1960. Anatomy of the monocotyledons. I. Gramineae. Clarendon, Oxford.
Napp-Zinn, K. 1984. Anatomie des Blattes. II. Angiospermen Band 2. Experimentelle und ökologische
Anatomie des Angiospermblattes. Handbuch der Pflanzenanatomie. Gebrüder Borntraeger, Berlin.
Nelson, E. A., T. L. Sage & R. F. Sage. 2005. Functional leaf anatomy of plants with crassulacean acid
metabolism. Functional Plant Biology 32: 409–419.
Nobel, P. S. 1988. Environmental biology of agaves and cacti. University of California Press,
Berkeley.
——— & T. L. Hartsock. 1978. Resistance analysis of nocturnal carbon dioxide uptake by a crassulacean
acid metabolism succulent, Agave deserti. Plant Physiology 61: 510–514.
Parthasarathy, M. V. 1980. Mature phloem of perennial monocotyledons. Berichte der deutschen botanischen Gesellschaft 93: 57–70.
——— & P. B. Tomlinson. 1967. Anatomical features of metaphloem in stems of Sabal, Cocos and two
other palms. American Journal of Botany 54: 1143–1151.
Patel, R. N. 1965. A comparison of the secondary xylem in roots and stems. Holzforschung 19: 72–
79.
Author's personal copy
Monocot Xylem Revisited
153
Pickard, W. F. & W. F. Melcher. 2005. Perspectives on the biophysics of xylem transport. Pp 3–18. In: N. M.
Holbrook & Ma A. Zwieniecki (eds). Vascular transport in plants. Elsevier Academic Press, Oxford.
Pitterman, J., J. S. Sperry, U. G. Hacke, J. K. Wheeler & E. H. Sikkema. 2005. Torus-margo pits help
conifers compete with angiosperms. Science 310: 1924.
Rabaey, D., F. Lens, E. Smets & S. Jansen. 2006. The micromorphology of pit membranes in tracheary
elements of Ericales: new records of tori or pseudotori? Annals of Botany 98: 943–951.
Rudall, P. 1991. Lateral meristems and stem thickening growth in monocotyledons. The Botanical Review
57: 150–163.
——— 1995. New records of secondary thickening in monocotyledons. IAWA Journal 16: 261–268.
Sauter, J. J., W. I. Iten & M. H. Zimmermann. 1973. Studies on the release of sugar into the vessels of
sugar maples (Acer saccharum). Canadian Journal of Botany 51: 1–8.
Schneider, E. L. & S. Carlquist. 1998. Origins and nature of vessels in monocotyledons. 4. Araceae
subfamily Philodendroideae. Bulletin of the Torrey Botanical Club 125: 253–260.
Silvera, K., L. S. Santiago, J. C. Cushman & K. Winter. 2010. The incidence of crassulacean acid
metabolism in Orchidaceae derived from carbon isotope ratios: a checklist of the flora of Panama and
Costa Rica. Botanical Journal of the Linnean Society 163: 194–222.
Slatyer, R. O. 1976. Plant-water relationships. Academic, London.
Smith, S. D., T. L. Hartsock & P. S. Nobel. 1983. Ecophysiology of Yucca brevifolia, an arborescent
monocot of the Mojave Desert. Oecologia 60: 10–17.
Solereder, H. & F. J. Meyer. 1930. Systematische Anatomie der Monokotyledonen. Heft VI. Scitamineae.
Verlag Fischer, Berlin.
Soltis, D. E., P. S. Soltis, M. W. Chase, M. E. Mort, D. C. Albach, M. Zanis, V. Savolainen, W. H.
Hahn, S. B. Hoot, M. F. fay, M. Axtell, S. M. Swensen, L. M. Prince, W. J. Kress, K. C. Nixon & J.
S. Farris. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133: 381–461.
Sperry, J. S. 1985. Xylem embolism in the palm Rhapis excelsa. IAWA Bulletin, new series 6: 283–292.
——— 1986. Relationship of xylem embolism to xylem pressure potential, stomata closure, and shoot
morphology in the palm Rhapis excelsa. Plant Physiology 80: 110–116.
———, U. G. Hacke, T. S. Feild, Y. Sano & E. H. Sikkema. 2007. Hydraulic consequences of vessel
evolution in angiosperms. International Journal of Plant Sciences 168: 1127–1139.
Stevenson, D. W. 1980. Radial growth in Beaucarnea recurvata. American Journal of Botany 67: 476–
489.
Stiller, V., J. S. Sperry & R. Lafitte. 2005. Embolism conduits of rice (Oryza sativa, Poaceae) refill
despite negative pressure. American Journal of Botany 92: 1970–1974.
Takahashi, A. 1988. Morphology and ontogeny of stem xylem elements of Sarcandra glabra (Thunb.)
Nakai (Chloranthaceae): additional evidence for the occurrence of vessels. The Botanical Magazine
(Tokyo) 101: 387–395.
Thorsch, J. 2000. Vessels in Zingiberaceae: a light, scanning, and transmission microscope study. IAWA
Journal 21: 61–76.
Tippo, O. 1946. The role of wood anatomy in phylogeny. American Midland Naturalist 36: 362–372.
Tomlinson, P. B. 1961. Anatomy of the monocotyledons. II. Palmae. Clarendon, Oxford.
——— 1969. Anatomy of the monocotyledons. III. Commelinales–Zingiberales. Clarendon, Oxford.
——— 1983. Anatomy of the monocotyledons. VII. Helobieae (Alismatidae). Clarendon, Oxford.
——— 1990. The structural biology of palms. Clarendon, Oxford.
——— & M. H. Zimmermann. 1969. Vascular anatomy of monocotyledons with secondary growth—an
introduction. Journal of the Arnold Arboretum 50: 159–179.
Turrill, W. B. 1942. Taxonomy and phylogeny. Part II. Botanical review 8: 473–532.
Tyree, M. T. & M. H. Zimmermann. 2002. Xylem structure and the ascent of sap, ed. 2. Springer Verlag,
Berlin.
Van Ieperen, W. 2007. Ion-mediated changes of xylem hydraulic reistance in planta: fact or fiction?
Trends in Plant Science 12: 137–142.
Vogt, K. 2001. Hydraulic vulnerability, vessel refilling, and seasonal courses of stem water potential of
Sorbus aucuparia L. and Sambucus nigra L. Journal of Experimental Botany 52: 1527–1536.
Wagner, P. 1977. Vessel types of the monocotyledons. A survey. Botaniska Notiser 130: 119–147.
Woodhouse, R. M., J. G. Williams & P. S. Nobel. 1980. Leaf orientation, radiation interception, and
nocturnal acidity increases by the CAM plant Agave deserti. American Journal of Botany 67: 1179–
185.
Young, D. A. 1981. Are the angiosperms primitively vesselless? Systematic Botany 6: 313–320.
Zimmermann, M. H. 1983. Xylem structure and the ascent of sap. Springer Verlag, Berlin.