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Vessels in Ferns: Structural, Ecological, and Evolutionary Significance1

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Vessels in Ferns: Structural, Ecological, and Evolutionary Significance1 American Journal of Botany 88(1): 1±13. 2001. INVITED SPECIAL PAPER VESSELS IN FERNS: STRUCTURAL, ECOLOGICAL, AND EVOLUTIONARY SIGNIFICANCE1 SHERWIN CARLQUIST2 AND EDWARD L. SCHNEIDER Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105 USA We have studied macerated xylem of ferns, supplemented by sections, by means of scanning electron microscopy (SEM) in a series of 20 papers, the results of which are summarized and interpreted here. Studies were based mostly on macerations, but also on some sections; these methods should be supplemented by other methods to con®rm or modify the ®ndings presented. Guidelines are cited for our interpretations of features of pit membranes. Fern xylem offers many distinctive features: (1) presence of numerous vessels and various numbers of tracheids in most species; (2) presence of vessels in both roots and rhizomes in virtually all species; (3) presence of specialized end walls in vessels of only a few species; (4) multiple end-wall perforation plates in numerous species; (5) lateral-wall perforation plates in numerous species; (6) porose pit membranes associated with perforation plates in all species; and (7) pit dimorphism, yielding wide membrane-free perforations alternating with extremely narrow pits. Multiple end wall perforation plates and lateral wall perforation plates are associated with the packing of tracheary elements in fascicles in ferns: facets of tips of elements contact numerous facets of adjacent elements; all such contacts are potential sites for conduction by means of perforations. This packing differs from that in primary xylem of dicotyledons and monocotyledons. Porosities in pit membranes represent a way of interconnecting vessel elements within a rhizome or root. In addition, these porosities can interconnect rhizome vessel elements with those of roots, a feature of importance because roots are adventitious in ferns as opposed to those of vascular plants with taproots. Fully-formed or incipient (small-to-medium sized porosities in pit membranes) perforation plates are widespread in ferns. These are believed to represent (1) ease of lysis of pit membranes via pectinase and cellulase; (2) numerous potential sites for perforation plate formation because of fasciculate packing of tracheary elements; (3) evolution of ferns over a long period of time, so that lysis pathways have had time to form; (4) lack of disadvantage in perforation plate presence, regardless of whether habitat moisture ¯uctuates markedly or little, because ferns likely have maintaining integrity of water columns that override the embolism-con®ning advantage of tracheids. Although all ferns share some common features, the diversity in xylem anatomy discovered thus far in ferns suggests that much remains to be learned. 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 de®nitions; vessel evolution, xylem. Vessels were ®rst reported for the ferns Nephrodium ®lix- White (1962) were, in fact, perforation plates (whereas lateral mas (L.) Schott and Pteridium aquilinum (L.) Kuhn by Rus- walls of tracheary elements did show well-preserved pit mem- sow (1873); vessel presence in Pteridium was con®rmed by branes, we extended our studies to other genera and families. Bliss (1939). Reports of vessels in ferns by Gwynne-Vaughan We soon concluded that vessels might be much more wide- (1908) were discounted by Bancroft (1911). However, distinc- spread in ferns than had been suspected, and we also found a tive vessels were reported in Marsilea (White, 1961), a report series of structural features of interest in fern tracheary ele- con®rmed by Loyal and Singh (1978). The possibility that ments. The component papers in this series are listed below, vessels might occur in other ferns was hinted by White (1962). so that the numerous citations of species and genera can be With light microscopy, White (1962) found end walls in tra- made without listing the relevant paper at each mention. The cheary elements of Astrolepis, Phlebodium, Polystichum, and occurrence of vessel elements or incipient vessel elements in Woodsia that were distinct and suggestive of perforation so many taxa might arouse skepticism in those who have not plates, but he could not demonstrate presence of perforations had the opportunity to view a large number of preparations with his methods. In deciding to use SEM to determine pres- such as ours. We have attempted to take into account any ence and nature of perforations, we began with these genera. possibilities of artifact formation. We have, however, offered The usefulness of SEM in determining presence of pit mem- a discussion of preparation methods and interpretation below branes and pit membrane remnants has been demonstrated re- in order to clarify the bases for our reports. peatedly in woody dicotyledons by Meylan and Butter®eld Bierhorst (1960) presented detailed light microscope studies (1978) and by Carlquist (1992, 1997). We have investigated of tracheary elements of ferns. Not surprisingly, we have been vessels of monocotyledons with SEM and illustrated porose able to see a number of details not ®gured by Bierhorst. We pit membranes and pit membrane remnants (see Schneider and report, in a later section of this paper, some structures not Carlquist, 1998a, and Carlquist and Schneider, 1998a, and the related to perforation plates that represent new reports in our papers cited therein). When our earlier studies on fern trache- series. ary elements revealed that the distinctive end walls cited by In the process of surveying xylem in ferns, we searched for correlations between tracheary element strucures and system- 1 Manuscript received 1 November 1999; revision accepted 2 June 2000. atics or ecology. Although our sampling represents a small 2 Author for reprint requests. proportion of fern species, the correlations are clear: the var- 1 2 AMERICAN JOURNAL OF BOTANY [Vol. 88 iables in structure are few, and therefore relatively easy to 1998c]; Ophioglossum crotalophoroides Walt., O. pendulum interpret. We would like to offer data applicable to understand- L., and O. vulgatum L. (Ophioglossaceae) [Schneider and Ca- ing of conductive physiology of ferns. However, very little is rlquist, 1999a]; Angiopteris evecta Hoffm., Danaea elliptica known about conductive physiology in ferns. We hope that Sm., D. wendlandii Reichenb. f., Macroglossum smithii (Ra- our data on such features as presence of perforation plates on cib.) D. H. Campbell, and Marattia fraxinea Sm. (Maratti- lateral walls of tracheary elements, presence of multiple end aceae) [Carlquist and Schneider, 1999]; Nephrolepis exaltata wall perforation plates, and highly porose or weblike pit mem- (L.) Schott (Davalliaceae) [Schneider and Carlquist, 1999b]; branes will be taken into account by those who pursue studies Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae or Pter- on fern physiology. idaceae) [Carlquist and Schneider, 2000a]; Asplenium nidus L. New data on fern tracheary elements invite comparison with (Aspleniaceae), Elaphoglossum hirtum (Sw.) C. Christens. data on xylem of other vascular plants. Such comparisons are (Elaphoglossaceae), and Vittaria lineata L. (Vittariaceae) complicated by the diversity of opinion concerning the delim- [Schneider and Carlquist, 1999c]; Alsophila australis R. Br. itations of ferns and the relationships of ferns (Hasebe et al., (Cyatheaceae), Cibotium splendens (Gaud.) Kraj. ex Skottsb. 1995; Pryer, Smith, and Skog, 1995; Rothwell, 1996). We have and Dicksonia antarctica Labill. (Dicksoniaceae), and Sadler- included Psilotaceae in our studies because some authors place ia cyatheoides Kaulf. (Blechnaceae) [Carlquist, and Schneider, Psilotales in ferns (Hasebe et al., 1995), whereas others do not 2000b]; Psilotum nudum (L.) Griseb. and Tmesipteris obliqua (Rothwell, 1996). Comparisons between a group with primary Chinnock (Psilotaceae) [Schneider and Carlquist, 2000a]; xylem only (living ferns) and groups with secondary growth Bommeria hispida (Mett.) Underw., Cheilanthes californica (cycads, gnetophytes) offer further interpretive concerns. Hook., C. tomentosa Link, and Pellaea mucronata (D. C. Ea- However, the similarities of tracheary elements among the fern ton) D. C. Eaton (Pteridaceae or Cheilanthaceae) [Carlquist families in our studies outweigh the differences among the and Schneider, 2000c]; Marsilea drummondii Braun, M. quad- families. Do these similarities re¯ect retention of ancient pat- rifolia L., and M. vestita Hook. & Grev. (Marsileaceae) terns of ferns (and other vascular plants, such as Selaginella: [Schneider and Carlquist, 2000b]; Callistopteris baldwinii (Ea- Schneider and Carlquist, in press a, b)? Is this relative unifor- ton) Copel., Mecodium recurvum (Gaud.) Copel., and Van- mity a re¯ection of growth forms and conductive physiology, denboschia davallioides (Gaud.) Copel. (Hymenophyllaceae) or is it a re¯ection of phylogenetic unity, or a combination of [Carlquist, Schneider, and Lamoureux, 2000]. In listings of both factors? genera below, the above sequence is followed. Major questions such as these are opened by our SEM stud- ies. We wish to stress that our results are based on a small INTERPRETIVE CRITERIA sample. Also, our methods represent a limited range of tech- niques, and thus we emphasize the need for further studies, Our studies are based mostly
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