| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
0 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105 USA
Received for publication November 1, 1999. Accepted for publication June 2, 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONDATABASE PAPERSINTERPRETIVE CRITERIACHARACTERISTICS OF FERN...FERN TRACHEARY ELEMENTS: NEW...LITERATURE CITED |
|---|
Key Words: ecological anatomy • ferns • incipient perforation plates • intermittent perforation plates • lateral wall perforation plates • multiple perforation plates • pit dimorphism • pit-membrane porosities • pit membrane remnants • vessel definitions • vessel evolution, xylem
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONDATABASE PAPERSINTERPRETIVE CRITERIACHARACTERISTICS OF FERN...FERN TRACHEARY ELEMENTS: NEW...LITERATURE CITED |
|---|
; vessel presence in Pteridium was confirmed by Bliss (1939)
. Reports of vessels in ferns by Gwynne-Vaughan (1908)
were discounted by Bancroft (1911)
. However, distinctive vessels were reported in Marsilea (White, 1961
), a report confirmed by Loyal and Singh (1978)
. The possibility that vessels might occur in other ferns was hinted by White (1962)
. With light microscopy, White (1962)
found end walls in tracheary elements of Astrolepis, Phlebodium, Polystichum, and Woodsia that were distinct and suggestive of perforation plates, but he could not demonstrate presence of perforations with his methods. In deciding to use SEM to determine presence and nature of perforations, we began with these genera. The usefulness of SEM in determining presence of pit membranes and pit membrane remnants has been demonstrated repeatedly in woody dicotyledons by Meylan and Butterfield (1978)
and by Carlquist (1992, 1997)
. We have investigated vessels of monocotyledons with SEM and illustrated porose pit membranes and pit membrane remnants (see Schneider and Carlquist, 1998a
, and Carlquist and Schneider, 1998a
, and the papers cited therein). When our earlier studies on fern tracheary elements revealed that the distinctive end walls cited by White (1962)
were, in fact, perforation plates (whereas lateral walls of tracheary elements did show well-preserved pit membranes, we extended our studies to other genera and families. We soon concluded that vessels might be much more widespread in ferns than had been suspected, and we also found a series of structural features of interest in fern tracheary elements. The component papers in this series are listed below, so that the numerous citations of species and genera can be made without listing the relevant paper at each mention. The occurrence of vessel elements or incipient vessel elements in so many taxa might arouse skepticism in those who have not had the opportunity to view a large number of preparations such as ours. We have attempted to take into account any possibilities of artifact formation. We have, however, offered a discussion of preparation methods and interpretation below in order to clarify the bases for our reports.
Bierhorst (1960)
presented detailed light microscope studies of tracheary elements of ferns. Not surprisingly, we have been able to see a number of details not figured by Bierhorst. We report, in a later section of this paper, some structures not related to perforation plates that represent new reports in our series.
In the process of surveying xylem in ferns, we searched for correlations between tracheary element strucures and systematics or ecology. Although our sampling represents a small proportion of fern species, the correlations are clear: the variables in structure are few, and therefore relatively easy to interpret. We would like to offer data applicable to understanding of conductive physiology of ferns. However, very little is known about conductive physiology in ferns. We hope that our data on such features as presence of perforation plates on lateral walls of tracheary elements, presence of multiple end wall perforation plates, and highly porose or weblike pit membranes will be taken into account by those who pursue studies on fern physiology.
New data on fern tracheary elements invite comparison with data on xylem of other vascular plants. Such comparisons are complicated by the diversity of opinion concerning the delimitations of ferns and the relationships of ferns (Hasebe et al., 1995
; Pryer, Smith, and Skog, 1995
; Rothwell, 1996
). We have included Psilotaceae in our studies because some authors place Psilotales in ferns (Hasebe et al., 1995
), whereas others do not (Rothwell, 1996
). Comparisons between a group with primary xylem only (living ferns) and groups with secondary growth (cycads, gnetophytes) offer further interpretive concerns. However, the similarities of tracheary elements among the fern families in our studies outweigh the differences among the families. Do these similarities reflect retention of ancient patterns of ferns (and other vascular plants, such as Selaginella: Schneider and Carlquist, in press a, b
)? Is this relative uniformity a reflection of growth forms and conductive physiology, or is it a reflection of phylogenetic unity, or a combination of both factors?
Major questions such as these are opened by our SEM studies. We wish to stress that our results are based on a small sample. Also, our methods represent a limited range of techniques, and thus we emphasize the need for further studies, especially those involving TEM and histochemistry.
|
DATABASE PAPERS |
|---|
|
TOPABSTRACTINTRODUCTIONDATABASE PAPERSINTERPRETIVE CRITERIACHARACTERISTICS OF FERN...FERN TRACHEARY ELEMENTS: NEW...LITERATURE CITED |
|---|
]; Pteridium aquilinum (L.) Kuhn (Pteridaceae) [Carlquist and Schneider, 1997a
]; Phlebodium aureum (L.) Smith (Polypodiaceae) and Polystichum acrostichoides (Mich.) Schott (Aspidiaceae) [Schneider and Carlquist, 1997
]; Astrolepis sinuata (Lag. ex Swartz) D. M. Benham & Windham (Pteridaceae or Cheilanthaceae) [Carlquist and Schneider, 1997b
]; Woodsia scopulina D. C. Eaton (Dryopteridaceae or Woodsiaceae) [Schneider and Carlquist, 1998b
]; Woodsia ilvensis (L.) R. Br. (Dryopteridaceae or Woodsiaceae) [Carlquist and Schneider, 1998b
]; Microgramma nitida A. R. Smith (Polypodiaceae) [Schneider and Carlquist, 1998c
]; Platyzoma microphyllum R. Br. (Pteridaceae or Platyzomataceae) [Carlquist, Schneider, and Kenneally, 1999
]; Dicranopteris linearis (Burm. f.) Underw. (Gleicheniaceae) [Schneider and Carlquist, 1998d
]; Todea barbara (L.) Moore (Osmundaceae), Anemia phyllitidis (L.) Moore and Lygodium flexuosum (L.) Swartz (Schizaeaceae or Lygodiaceae) [Carlquist and Schneider, 1998c
]; Ophioglossum crotalophoroides Walt., O. pendulum L., and O. vulgatum L. (Ophioglossaceae) [Schneider and Carlquist, 1999a
]; Angiopteris evecta Hoffm., Danaea elliptica Sm., D. wendlandii Reichenb. f., Macroglossum smithii (Racib.) D. H. Campbell, and Marattia fraxinea Sm. (Marattiaceae) [Carlquist and Schneider, 1999
]; Nephrolepis exaltata (L.) Schott (Davalliaceae) [Schneider and Carlquist, 1999b
]; Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae or Pteridaceae) [Carlquist and Schneider, 2000a
]; Asplenium nidus L. (Aspleniaceae), Elaphoglossum hirtum (Sw.) C. Christens. (Elaphoglossaceae), and Vittaria lineata L. (Vittariaceae) [Schneider and Carlquist, 1999c
]; Alsophila australis R. Br. (Cyatheaceae), Cibotium splendens (Gaud.) Kraj. ex Skottsb. and Dicksonia antarctica Labill. (Dicksoniaceae), and Sadleria cyatheoides Kaulf. (Blechnaceae) [Carlquist, and Schneider, 2000b
]; Psilotum nudum (L.) Griseb. and Tmesipteris obliqua Chinnock (Psilotaceae) [Schneider and Carlquist, 2000a
]; Bommeria hispida (Mett.) Underw., Cheilanthes californica Hook., C. tomentosa Link, and Pellaea mucronata (D. C. Eaton) D. C. Eaton (Pteridaceae or Cheilanthaceae) [Carlquist and Schneider, 2000c
]; Marsilea drummondii Braun, M. quadrifolia L., and M. vestita Hook. & Grev. (Marsileaceae) [Schneider and Carlquist, 2000b
]; Callistopteris baldwinii (Eaton) Copel., Mecodium recurvum (Gaud.) Copel., and Vandenboschia davallioides (Gaud.) Copel. (Hymenophyllaceae) [Carlquist, Schneider, and Lamoureux, 2000]. In listings of genera below, the above sequence is followed. |
INTERPRETIVE CRITERIA |
|---|
|
TOPABSTRACTINTRODUCTIONDATABASE PAPERSINTERPRETIVE CRITERIACHARACTERISTICS OF FERN...FERN TRACHEARY ELEMENTS: NEW...LITERATURE CITED |
|---|
; Schneider and Carlquist, 1997a). Because pit membranes are sometimes thought to be very delicate with relation to reagents and preparation methods, we have assembled a series of reasons, with citations of earlier papers, that document why we believe our results are reliable.
1) As observed by a wide variety of methods, pores develop as a natural form of cell wall hydrolysis (achieved by pectinase and cellulase) in particular pit membranes of particular species (Butterfield and Meylan, 1982
). The end product of this action can be seen as perforations in vessels of dicotyledons and margos of pit membranes in coniferous tracheids. The result of this lysis is a mesh of threads or, if the action of cellulase is sufficient, removal of the entire pit membrane.
2) Different species of gymnosperms and angiosperms characteristically have pores of particular sizes in pit membranes of tracheary elements; pores of these characteristic sizes are observed despite the use of a variety of different methods of preparation (Shane, McCully, and Canny, in press
, Tables 2 and 3).
3) Although the data cited above are derived from gymnosperms and angiosperms, no worker has suggested that the same kinds of porose pit membranes observed in ferns and Selaginella (Schneider and Carlquist, in press a, b
) are artifacts of reagents or preparation methods in ferns but not in the dicotyledons and monocotyledons where they have been reported (Carlquist, 1992, 1997
; Carlquist and Schneider, 1998a
; Meylan and Butterfield, 1978
; Schneider and Carlquist, 1998a
).
4) Where end wall perforation plates of fern tracheary elements are different from lateral walls (by virtue of different patterns in the underlying secondary wall framework), the end wall perforation plates lack pit membranes while the lateral walls possess them in Woodsia (e.g., Fig. 1–3, 17). If maceration techniques or drying techniques were responsible for removal of pit membranes in the end wall perforation plates of Woodsia spp., the pit membranes should be removed from lateral walls as well, and pit membranes should be removed in a random fashion in tracheary elements in ferns at large. Absence of pit membranes, except in instances we have been able to attribute to handling, is not at all random in pits (or perforations) of the fern tracheary elements we examined. The absence of random removal of pit membranes seems to us very strong evidence for believing that our methods have produced essentially accurate images.
|
|
; Schneider and Carlquist, 1997
) we used both macerated and sectioned materials, and obtained the same results with both techniques. 7) In vessel elements in which the size and morphology of the perforations are like the lateral wall pits, upper and lower ends of perforation plates (as well as incipient perforation plates) often bear porose pit membranes. The porose pit membranes indicate a transition between lateral wall pitting and perforations. In Fig. 16, porose pit membranes of such a transitional area are shown at left, adjacent to a facet with intact pit membranes at right. The distribution of porose pit membranes (in comparison to distribution of non-porose pit membranes) is not random in our preparations.
|
|
10) Striate pit membranes (Figs. 16, 22) represent artifacts, in our opinion. We believe that the action of the SEM electron beam results in this appearance or at the least exaggerates it. We have considered all appearances related to striate nature of pit membranes as potential artifacts. Uneven thickness in pit membranes resulting in weblike appearances, however, is interpreted as natural.
11) We believe that air drying of cells does not produce the porosities or weblike appearances of pit membranes. When a wide range of methods is used to demonstrate presence or absence of pores (including introduction of particles of known diameters into the conductive stream), porosity size is not related to preparation method, but rather characterizes particular species (Shane, McCully, and Canny, in press, Tables 2 and 3). More significantly, students of xylem have repeatedly reported cavitation of xylem cells in the living plant. Ferns have not been studied in this respect, but can be assumed to experience replacement of water by air in tracheary elements under stress conditions but inevitably by age also. Therefore, pit membranes of air-filled tracheary elements have been subjected to air drying in the living plant. To rehydrate such elements in a pickling solution and then apply critical point drying to such cells would be superfluous and illogical. If porose pit membranes were the result of air drying, the extensive areas of intact nonporose membranes on facets adjacent to membranes with porose membranes would be inexplicable.
12) Our results are entirely compatible with results obtained thus far with other methods by other workers. For example, Morrow and Dute (1998, 1999)
did not find pores in pit membranes in Botrychium using transmission electron microscopy, nor did we with SEM (unpublished data).
13) We have avoided use of stem or root portions that could contain meristematic or differentiating cells. Therefore, the presence or absence of pit membranes cannot be attributed, in our preparations, to different degrees of maturation of cells.
14) We did not attempt to control for age of tracheary elements (as indicated by distance from an apical meristem, for example), although we used liquid-preserved portions of living plants. Therefore, in any given preparation, some of the tracheary elements might have been inactive ones while others were actively conducting elements. We did not observe differences among tracheary elements, within a preparation. While conceivably bacterial or fungal action might remove pit membranes from inactive tracheary elements, this is unlikely to account for the patterns we observed, and no evidence for such deterioration of fern tracheary elements has been presented in studies we know. Duerden (1934) claimed vessels with simple perforation plates (but with pit membranes on lateral walls) in homophyllous species of Selaginella. Duerden's (1934) studies have never been questioned, despite the fact that they were based on herbarium species and the preparation method involved only maceration techniques.
|
CHARACTERISTICS OF FERN TRACHEARY ELEMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONDATABASE PAPERSINTERPRETIVE CRITERIACHARACTERISTICS OF FERN...FERN TRACHEARY ELEMENTS: NEW...LITERATURE CITED |
|---|
. A moderate degree of differentiation between perforation plates and lateral wall pitting was also observed in Astrolepis sinuata, Polystichum acrostichoides and Woodsia scopulina. Ferns not mentioned in this and the preceding paragraph were not observed to have secondary wall frameworks for perforation plates that differed from those of the lateral wall pitting.
Multiple end-wall perforation plates
Reduction in number of bars in perforation plates, described in the preceding section, has been considered an indicator of phylogenetic specialization in angiosperms. Most ferns, however, do not exemplify this trend and have vessel elements with end walls that resemble lateral walls (Fig. 13). However, multiple end-wall perforation plates, a feature rarely reported in other vascular plants, were observable in a number of fern tracheary elements.
Multiple perforation plates per vessel element tip are illustrated here by Microgramma (Figs. 8, 9). In the element tip of Fig. 8, the three facets shown lack pit membranes. The vessel element portion shown in Fig. 9 illustrates absence of pit membranes in all facets, both those of the facing facets and those on the back facets. We have figured the occurrence of several perforation plate facets per tracheary element tip in Polystichum acrostichoides, Woodsia scopulina, Platyzoma microphyllum, Dicranopteris linearis, Todea barbara, Ophioglossum pendulum, O. vulgatum, Danaea wendlandii, Macroglossum smithii, Marattia fraxinea, Nephrolepis exaltata, Elaphoglossum hirtum, Sadleria splendens, Alsophila australis, Dicksonia antarctica, Cheilanthes californica, Marsilea spp., Callistopteris baldwinii, and Vandenboschia davallioides. However, multiple perforation plates are probably more widespread in ferns than our reports presently indicate. The occurrence of multiple end-wall perforation plates on tracheary elements can be correlated with the arrangement (packing) of tracheary elements in ferns, as discussed later.
Pit dimorphism
Pit dimorphism that results in the formation of wide perforations alternating with one or more narrow intervening pits is illustrated here for Microgramma nitida (Fig. 9), Vandenboschia davallioides (Fig. 10), and Bommeria hispida (Figs. 11, 12). Similar pit dimorphism resulting in formation of perforations interspersed with pits on a wall was figured by us in Phlebodium aureum, Polystichum acrostichoides, Platyzoma microphyllum, Dicranopteris linearis, Anemia phyllitidis, Ophioglossum pendulum, Danaea elliptica, D. wendlandii, Psilotum nudum, and Cheilanthes californica. Wide pits (possibly perforations) alternating with narrow pits were figured by Bierhorst (1960)
for Angiopteris evecta Hoffm., Asplenium viride Huds., and Osmunda cinnamomea L. Bierhorst's work was based on light microscopy, so he could not have readily observed absence of pit membranes in the wide pits, and thus his lack of comment on this phenomenon is understandable.
Lateral-wall perforation plates
In macerations of some ferns, lateral walls are not readily distinguished from end walls. This is not true in Pteridium, in which lateral walls are easily distinguished from the end wall perforation plates. In our Pteridium study (Carlquist and Schneider, 1997
, Figs. 11–13), we showed areas of lateral wall pits in which pores are so large that one should likely say that the pits have become converted into perforations, and therefore, lateral-wall perforation plates are present. These lateral wall perforation plates are readily distinguished from the end-wall perforation plates of Pteridium, which have fewer, narrower bars intervening between wide perforations, and no pit membrane remnants in the perforations. In the present paper, lateral-wall perforation plates are illustrated for Woodsia obtusa (Fig. 7), in which porose pit membranes are present, and Ceratopteris thalictroides (Fig. 18), in which relatively large holes are present.
Intermittent perforation plates
The lateral-wall perforation plate figured for Ceratopteris thalictroides (Fig. 18) is subdivided by intact pits, and is thus an intermittent perforation plate. We observed such intermittent perforation plates in other ferns as well. By definition, pit dimorphism in which the wide pits are perforations results in intermittent perforation plates.
At left in Fig. 16 is a lateral-wall facet with porose pit membranes; this facet therefore constitutes an incipient lateral wall perforation plate.
We could identify perforations as present on lateral walls in some tracheary elements. However, in our preparations, wall facets are very long and few elements are isolated well enough and intact enough to designate all facets either as end walls or as lateral walls. Thus, certain identification of lateral wall perforation plates in all cases was not possible.
Vessel elements and tracheids
In Ceratopteris thalictroides, the shortness of tracheary elements and the success of macerations permitted us to see isolated tracheary elements well. Some of these elements were wider and shorter and had perforation plates on end walls and thus were clearly vessel elements (Fig. 14). Other tracheary elements in this species were narrower, and end walls were revealed with sufficient clarity, so that we could reasonably identify them as tracheids (Fig. 15). In other ferns, we were rarely able to make this distinction. Because the SEM method can only reveal the surfaces facing away from the mount, there is always some degree of doubt about whether a facet hidden from view contains perforations or not. Nevertheless, we can generalize, based on the abundance of perforation plates observed in our preparations, that in the xylem of ferns we studied, tracheids were few or none. Prior to our studies, vessel elements were assumed to be absent in most ferns. In the ferns in which vessels had been reported (e.g., Pteridium), earlier authors did not present analyses of whether tracheids were also present (e.g., Bliss, 1939)
. Thus, no study prior to our work on Ceratopteris presented the likelihood that vessel elements could coexist with tracheids in fern xylem. Further work, perhaps with particles of various sizes introduced into actively conducting xylem, needs to be done to confirm the idea that fern xylem can consist mostly or wholly of vessel elements.
Porose pit membranes and incipient perforation plates
Porose pit membranes (Figs. 19, 20) were observed in all of our studies, cited above. The modes of occurrence of these pores are as follows: (1) throughout incipient perforation plates (usually lateral wall perforation plates, Fig. 16, left); (2) at upper and lower ends of perforation plates, where the porose pits form a transition between perforations and intact pits; (3) in narrow pits, where accompanied by wide pits in instances of pit dimorphism (Fig. 12, upper left).
Modifications of porose pit membranes in the direction of enlargement of pores are common. These modifications include: (1) occurrence of one to several large holes as well as porose membranes, forming an incipient perforation (Figs. 17, 20, 22) or else presence of large holes without porose pit membranes (Fig. 18); (2) threadlike or weblike pit membrane remnants (Fig. 21), which may or may not include porose segments.
Most of the facets we examined, however, possess intact pit membranes (Fig. 23) in which pores, if present, were so minute that they were beyond the resolving ability of our equipment and which probably would be referable to the category of plasmodesmata rather than pores.
Other newly reported structural details
During the course of our studies to determine presence of vessel elements in the ferns we studied, we encountered a number of noteworthy structures.
1) Tracheary elements that are short and have numerous short facets (Fig. 23). These were observed only in Cyatheaceae.
2) Grooves interconnecting pit apertures (Fig. 24). These were observed only on the inner surfaces of vessels of Pteridium aquilinum. Such grooves may be more widespread in ferns, but we viewed the inner surfaces of vessels only in our first two fern studies in which sections of tracheary elements were prepared and observed. Such grooves (also termed "coalescent pit apertures") are widespread in dicotyledons, but our report is apparently the first in ferns.
|
4) In Vandenboschia davallioides (Fig. 28), Dicranopteris linearis, and Anemia phyllitidis we observed that at facet edges, the horizontal secondary wall framework segments terminate. Thus, the secondary wall framework consists of transverse bars with widened ends, and the facet angle therefore consists of primary wall separating the ends of these barlike structures. Ordinarily, a secondary wall framework that forms a continuous skeleton for the tracheary element is illustrated for fern metaxylem, and a vertical (axial) ridge of secondary wall material, rather than an absence of secondary wall material, is characteristic of tracheary elements of most ferns.
5) We examined roots and stems (rhizomes) of all ferns we studied (the axis of Psilotaceae is not differentiated into roots and stems, however). In all species for which we had both root and stem material that yielded good results, vessel elements were observed in both roots and stems.
|
FERN TRACHEARY ELEMENTS: NEW INTERPRETATIONS |
|---|
|
TOPABSTRACTINTRODUCTIONDATABASE PAPERSINTERPRETIVE CRITERIACHARACTERISTICS OF FERN...FERN TRACHEARY ELEMENTS: NEW...LITERATURE CITED |
|---|
|
3) Most ferns have multiple end-wall facets that are converted into perforation plates by lysis of pit membranes (Fig. 8), rather than single perforation plates per end wall. These multiple perforation-plate facets are likely related to packing of metaxylem elements (Fig. 28). The end of a given tracheary element is not in contact with the end wall of a single superposed element at either end, but with side walls of a multiplicity of elements. The multiple contacts among tracheary elements in most ferns may predispose the tracheary elements to develop both lateral-wall and end-wall perforation plates, as suggested under (1) above. Tracheary elements in ferns are often very long, and the differentiation into end-wall and lateral-wall facets is minimal.
4) The occurrence in ferns of both end-wall and lateral-wall perforation plates has the effect of converting a fascicle of tracheary elements into a kind of aggregate vessel. No part of such a fascicle of elements is isolated from any other part in terms of conduction. Fascicles of vessel elements interconnected with each other by lateral perforation plates as well as end-wall perforation plates have not been reported in other groups of vascular plants except Selaginella, depending on definition of lateral-wall perforation plate (Schneider and Carlquist, in press a, b).
5) A series of wide perforations alternating with narrow pits, a condition that we are terming "pit dimorphism," has a potential effect on the conductive stream of a scalariform perforation plate. Evidently ferns have been able to develop these vicarious perforation plates by means of pit dimorphism more successfully than have other vascular plants, because we know of no reports of pit dimorphism resulting in perforation-plate equivalents in groups other than ferns except for Selaginella (Schneider and Carlquist, in press a, b).
6) Porose pit membranes that range from incipient perforation plates (where pores are small) to perforation plates in which the pores in pit membranes open large portions of a pit membrane to the conductive stream, are common in ferns. The existence of this range of perforation plates has not, hitherto, been reported in other groups of vascular plants, except for recent instances such as our studies of vessels of monocotyledons (e.g., Carlquist and Schneider, 1998a
; Schneider and Carlquist, 1998a
) and Selaginella (Schneider and Carlquist, in press a, b).
7) The occurrence in ferns of numerous incipient perforation plates or of perforation plates with appreciable areas of pit membrane remnants in perforations raises the question of terminology with respect to vessel elements. When are pit membranes provided with pores of such size and abundance that one must say perforations (and therefore vessel elements) are present? By using the term incipient perforation plate, we recognize a transition, even if we do not define a distinction between tracheids and vessel elements in such transitional instances. One might use quantitative criteria, such as the ability to transmit microspheres of known diameters from one tracheary element to another. Even this definition would likely be arbitrary. One notes the capability of margo pores in conifer tracheids to allow passage of relatively large particles in comparison to porosities in pit membranes of tracheary elements of other vascular plants (Shane, McCully, and Canny, in press
), yet undoubtedly this information would not lead anatomists to question the presence of tracheids in conifers. As a working definition, we have tended to regard presence of porosities totalling 
50% of the area of a pit membrane or more as constituting a perforation. However, such criteria as passage of air bubbles of minimal size or other physiological criteria are needed: terminology of tracheary elements should reflect functional distinctions, if possible.
8) Porosities in pit membranes offer a potential method of interconnection between tracheary elements that are in contact but which have no intercontinuous ontogenetic relationship with each other. A prime example of this is the interconnection of vessels in adventitious roots with the vessels of the stem on which the adventitious roots form. The possible function of porosities in pit membranes to form a pathway for the conductive stream is important, because if vessels occur in both stems and roots of ferns (see above) and monocotyledons (Carlquist and Schneider, 1998a
, and earlier papers in that series), such a mechanism for facilitating conduction between root and stem vessels is of selective value. Such a possible function has been mentioned in maize by Shane, McCully, and Canny (in press), and is equally applicable to ferns.
9) In those ferns with end-wall perforation plates that differ in framework from lateral-wall pitting (or lateral-wall perforation plates), the simplification of the perforation plate is related to ecology. Marsilea, Pteridium, and Woodsia, which exemplify this, live in situations with marked fluctuation in water availability and show trends to fewer bars associated with wider perforations. However, other ferns occur in ecological regimes in which drying or freezing of soil offers extremes as severe as those experienced by those three genera, yet these other ferns (e. g., Cheilanthes, Pellaea, Platyzoma) do not have such modifications of the secondary-wall framework of perforation plates. These latter genera do, however, have other means other than simplified perforation plates by which the conductive stream potentially can be facilitated during brief periods of water availability. Such means include multiple end wall perforation plates, lateral-wall perforation plates, and perforations that result from pit dimorphism. In angiosperms, degree of simplification of perforation plate is closely keyed to degree of fluctuation in water availability (Carlquist, 1975
). Enhancement of the conductive capabilities of a vessel of an angiosperm must be accomplished by modification of the end wall, because the variety of perforation plates and perforation-plate substitutes present in ferns are not available in angiosperms.
10) Vessels are much more common in ferns than hitherto supposed. Because many ferns that have perforation plates occur in habitats with relatively uniformly moist environments (e.g., Marattiaceae), strong fluctuation in moisture availability cannot be hypothesized as a requirement to explain vessel origin in ferns. Lysis of pit membranes by pectinase and cellulase is apparently not a complicated process (Butterfield and Meylan, 1982
). If this is true, vessels could be expected to develop independently in a number of clades of vascular plants. Once large porosities are formed, removal of most or all of the pit membrane remnants is all but inevitable. Special mechanisms (e.g., fibrils separating large pores in margos of pits of conifer tracheids) that do not follow this pattern but represent alternative mechanisms for enhancement of conduction exist. Perforation plates (or equivalent structural enhancements of conductive capability) are not known to be of any detriment in mesic situations. For example, dicotyledons of bogs show no fewer simple perforation plates than do plants of noninundated areas (Carlquist, unpublished data). The potential role of imperforate tracheary elements in deterring spread of air embolisms has often been cited, and undoubtedly does occur. However, mechanisms for control of transpiration may override the potential advantages of tracheids in increasing safety and integrity of the water columns of a plant from spread of air bubbles. For example, Gates (1968)
measured a diffusive resistance in Pteridium higher than that of any other vascular plant he studied.
In summarizing our data, we wish to emphasize that our survey, although it covers all major families of ferns, is based on limited material when one considers the large number of fern species in existence. The opportunities for research in structure of fern tracheary elements by means of electron microscopy are extensive. Moreover, we hope that plant physiologists will become interested in studying vascular plants such as ferns that offer a range of conductive pathways not present in angiosperms or gymnosperms.
|
FOOTNOTES |
|---|
2 Author for reprint requests.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONDATABASE PAPERSINTERPRETIVE CRITERIACHARACTERISTICS OF FERN...FERN TRACHEARY ELEMENTS: NEW...LITERATURE CITED |
|---|
Bierhorst, D. W., 1960 Observations on tracheary elements. Phytomorphology 10: 249–305
Bliss, M. C., 1939 The tracheal elements in the ferns. American Journal of Botany 26: 620–624[CrossRef][ISI]
Butterfield, B. G., and B. A. Meylan. 1982 Cell wall hydrolysis in the tracheary elements of the secondary xylem. In P. Baas [ed.], New perspectives in wood anatomy, 71–84. Dr. Martinus Nijhoff/Dr. W. Junk, The Hague, The Netherlands
Carlquist, S., 1975 Ecological strategies of xylem evolution. University of California Press, Berkeley, California, USA
———. 1992 Pit membrane remnants in perforation plates of primitive dicotyledons and their significance. American Journal of Botany 79: 666–672
———. 1997 Pentaphragma: a unique wood and its significance. IAWA Journal 18: 3–12
———, and E. L. Schneider. 1997a SEM studies on vessels in ferns. 2. Pteridium. American Journal of Botany 84: 581–587[Abstract]
———, and ———. 1997b SEM studies on vessels in ferns. 4. Astrolepis. American Fern Journal 87: 43–50[CrossRef]
———, and ———. 1998a Origin and nature of vessels in monocotyledons. 5. Araceae subfamily Colocasioideae. Botanical Journal of the Linnean Society 128: 71–86[CrossRef]
———, and ———. 1998b SEM studies on vessels in ferns. 6. Woodsia ilvensis, with comments on vessel origin in ferns. Flora 193: 179–185[ISI]
———, and ———. 1998c SEM studies on vessels in ferns. 10. Selected Osmundaceae and Schizaeaceae. International Journal of Plant Sciences 159: 788–797[CrossRef]
———, and ———. 1999 12. Marattiaceae, with comments on vessel patterns in eusporangiate ferns. American Journal of Botany 86: 457–464
———, and ———. 2000a SEM studies of vessels in ferns. 14. Ceratopteris. Aquatic Botany 66: 1–8[CrossRef]
———, and ———. 2000b SEM studies of vessels in ferns. 16. Pacific tree ferns (Blechnaceae, Cyatheaceae, Dicksoniaceae). Pacific Science 54: 75–86
———, and ———. 2000c SEM studies of vessels in ferns. 18. Montane cheilanthoid ferns (Pteridaceae) of North America. Aliso 19: 31–39
———, ———, and K. F. Kenneally. 1999 SEM studies on vessels in ferns. 8. Platyzoma. Australian Journal of Botany 47: 277–282[CrossRef]
———, ———, and C. Lamoureux. 2000 SEM studies on vessels in ferns. 20. Hawaiian Hymenophyllaceae. Pacific Science 54: 365–375
———, ———, and G. Yatskievych. 1997 SEM studies on vessels in ferns. 1. Woodsia obtusa. American Fern Journal 87: 1–8[CrossRef][ISI]
Gates, D. M., 1968 Transpiration and leaf temperature. Annual Review of Plant Physiology 19: 211–238
Gwynne-Vaughan, D. T., 1908 On the real nature of the tracheae in the ferns. Annals of Botany 22: 517–523
Hasebe, M., P. G. Wolf, K. M., Pryer, K. Ueda, M. Ito, R. Sano, G. J. Gastony, J. R. Manhart, N. Murakami, E. H. Crane, C. H. Haufler, and W. D. Hauk. 1995 Fern phylogeny based on rbcL sequences. American Fern Journal 85: 134–181[CrossRef]
Loyal, D. S., and L. Singh. 1978 A further investigation of the morphology of vessels in Marsilea. Proceedings of the Indian Academy of Sciences (Plant Sciences—4) 87B: 335–346
Meylan, B. A., and B. G. Butterfield. 1978 The structure of New Zealand woods. DSIR Bulletin 222. New Zealand Department of Scientific and Industrial Research, Wellington, New Zealand
Morrow, A. C., and R. R. Dute. 1998 Development of the torus-bearing pit membrane in Botrychium dissectum. IAWA Journal 19: 429–441[ISI]
———, and ———. 1999 Electron microscopic investigation of the coating found on torus-bearing pit membranes of Botrychium dissectum, the common grape fern. IAWA Journal 20: 359–373[ISI]
Pryer, K., A. R. Smith, and J. E. Skog. 1995 Phylogenetic relationships of extant ferns based on evidence from morphology and rbcL serquences. American Fern Journal 85: 205–262[CrossRef][ISI]
Rothwell, G. W., 1996 Phylogenetic relationships of ferns: a palaeobotanical perspective. In J. M. Camus, M. Gibby, and R. J. Johns [eds.], Pteridology in perspective, 395–404. Royal Botanic Gardens, Kew, Richmond, Surrey, UK
Russow, E. 1873 Vergleichende Untersuchungen betreffend die Histologie (Histographie und Histogenie) der vegetativen und sporenbildenen Organe und die Entwicklung der Sporen der Leitbundel-Kryptogamen, mit Berücksichtigung der Histologie der Phanerogamen, ausgehend von der Betrachtung der Marsiliaceen. St. Petersburg Academy of Sciences Memoirs, Series 7, 19(1): 1–207
Schneider, E. L., and S. Carlquist. 1997 SEM studies on vessels in ferns. 3. Phlebodium and Polystichum. International Journal of Plant Sciences 1158: 343–349
———, and ———. 1998a Origin and nature of vessels in monocotyledons. 4. Araceae subfamily Philodendroideae. Journal of the Torrey Botanical Society 125: 253–260[CrossRef][ISI]
———, and ———. 1998b SEM studies on vessels in ferns. 5. Woodsia scopulina. American Fern Journal 88: 17–23[CrossRef]
———, and ———. 1998c SEM studies on vessels in ferns. 7. Microgramma nitida. Anales del Instituto Biologico de la Unversidad Autonomica de México 69: 1–7
———, and ———. 1998d SEM studies on vessels in ferns. 9. Dicranopteris (Gleicheniaceae) and vessel patterns in leptosporangiate ferns. American Journal of Botany 85: 1028–1032[Abstract]
———, and ———. 1999a SEM studies on vessels in ferns. 11. Ophioglossum. Botanical Journal of the Linnean Society 129: 105–114[CrossRef]
———, and ———. 1999b SEM studies on vessels in ferns. 13. Nephrolepis. American Fern Journal 89: 171–177[CrossRef]
———, and ———. 1999c SEM studies on vessels in ferns. 15. Selected rosette epiphytes (Aspleniaceae, Elaphoglossaceae, Vittariaceae). International Journal of Plant Sciences 160: 1013–1020[CrossRef][ISI][Medline]
———, and ———. 2000a SEM studies on vessels in ferns. 17. Psilotaceae. American Journal of Botany 87: 176–181
———, and ———. 2000b SEM studies on vessels in ferns. 19. Marsilea. American Fern Journal 90: 32–41[CrossRef]
———, and ———. In press a SEM studies on vessels of the homophyllous species of Selaginella. International Journal of Plant Sciences
———, and ———. In press b SEM studies on vessels of the heterophyllous species of Selaginella. Journal of the Torrey Botanical Society
Shane, M. W., M. E. McCully, and M. J. Canny. In press Architecture of branch-root junctions in maize: structure of the connecting xylem and the porosity of pit membranes. Annals of Botany
White, R. A., 1961 Vessels in roots of Marsilea. Science 133: 1073–1074
———. 1962 A comparative study of the tracheary elements of the ferns. Ph.D. dissertation, University of Michigan, Ann Arbor, Michigan, USA
This article has been cited by other articles:
|
|
 |
|
  M.E. Collinson, D.C. Steart, A.C. Scott, I.J. Glasspool, and J.J. Hooker Episodic fire, runoff and deposition at the Palaeocene-Eocene boundary Journal of the Geological Society, January 1, 2007; 164(1): 87 - 97. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. E. SCHECKLER and J. GALTIER Tyloses and Ecophysiology of the Early Carboniferous Progymnosperm Tree Protopitys buchiana Ann. Bot., May 1, 2003; 91(6): 739 - 747. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Carlquist and E. L. Schneider The tracheid-vessel element transition in angiosperms involves multiple independent features: cladistic consequences Am. J. Botany, February 1, 2002; 89(2): 185 - 195. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
