What the alliance () tells us about the nature of vestured pits in xylem

Sherwin Carlquist

Brittonia

ISSN 0007-196X

Brittonia DOI 10.1007/s12228-017-9477-1

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1 23 Author's personal copy

What the Penaeaceae alliance (Myrtales) tells us about the nature of vestured pits in xylem

SHERWIN CARLQUIST

Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA; e-mail: [email protected]

Abstract. Molecular studies indicate that Penaeaceae, Oliniaceae, and the monospecific families Alzateaceae and Rhynchocalycaceae form a clade of Myrtales. Of these four families, Penaeaceae have tracheids with vestured pits, whereas the others have septate fibers lacking vestures; all have vestured pits in vessels. Tracheid presence in Penaeaceae may be related to the arid South African habitats of the family. Presence of vestures on tracheids in families with vestured vessel pits is one indication that imperforate elements are tracheids and are conduc- tive cells, whereas fiber-tracheids and libriform fibers are non-conductive. Tracheids occur widely in angiosperms and may be plesiomorphies or apomorphies. , the first branch of the Myrtales clade, has a great diversity of vesture features in vessels compared to the Penaeaceae alliance families. has vestures that spread over the inside of the vessels, whereas in most taxa of the alliance, vestures are confined to the pit cavities and pit apertures. Vestures in the alliance tend to be globular in shape, and are bridged together by strands of wall material. Lignotubers and roots in Penaeaceae have vestures much like those in stems. Only a few and genera (notably Alzatea) of the alliance have vesture features the pattern of which correlates with the current taxonomic system. Vestured pits should be viewed from the inside surface of vessels as well as the outer surface, and although sectional views of vestured pits are infrequent, they are very informative. Studies that explore diversity from one order or family to another are needed and offer opportunities for understanding the evolutionary significance of this feature. Keywords: Ecological anatomy, systematic anatomy, tracheids, vessel wall sculpturing, wood physiology.

Vestured pits in wood of angiosperms (and light microscopes can resolve. Scanning electron Gnetum) have been regarded as salient systematic microscopy has greatly enhanced our knowledge features (e.g., Jansen et al., 2001). Although our of vestured pits and similar phenomena (e.g., knowledge of their systematic distribution seems Meylan & Butterfield, 1978;Jansenetal.,2001, relatively well established, we know rather little 2003, 2004), but there are still important contribu- about other aspects, such as correlations with ecol- tions to be made with regard to systematic distri- ogy, wood physiology, and diversity with respect bution (e.g., Carlquist, 2016) and structural diver- to ontogeny. Experimental work is difficult to per- sity. When an earlier study of wood anatomy of form on such minute structures. The most satisfy- Penaeaceae was published (Carlquist & DeBuhr, ing way of observing them is via scanning electron 1977), I did not have access to SEM capabilities. microscopy (SEM), but this requires significant Scanning electron microscopy is now available to amounts of time, and three-dimensional under- me, and I have returned to study vestured pits in standing of vestured pits is still fragmentary. the wood of this family, which I collected in South Most workers cite Bailey (1933) as the first in 1973. The Penaeaceae alliance (Fig. 1), a person to explore vestured pits on both systematic terminal clade of Myrtales (Schönenburger & and structural levels. This required patience and Conti, 2003), consists of Penaeaceae (seven gen- good technique, because the minute size of ves- era, 21 species) from Cape Province, tures places them at the limits of what even the best (Goldblatt & Manning, 2000), Oliniaceae (eight

Brittonia, DOI 10.1007/s12228-017-9477-1 ISSN: 0007-196X (print) ISSN: 1938-436X (electronic) © 2017, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. Author's personal copy

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FIG.1. Phylogenetic of Myrtales. Redrawn from Stevens (2001 onwards). The topology of the Penaeaeae alliance is based on Schönenburger and Conti (2003). species of ), from tropical and southern Af- that current generic assignments of species will rica (Gilg, 1894; Stevens, 2001 onwards), have to be changed, but new combinations have (one species, from southeastern not yet been made, so the nomenclature used by South Africa), and Alzatea (one species, known Goldblatt and Manning (2000) is retained here. from Costa Rica southwards to Peru: Stevens, Although the total number of species is modest, 2001 onwards). The molecular-based phylogenetic their ecological range is considerable: from dry work of Schönenburger and Conti (2003) shows rocky slopes (most Penaeaceae) to humid forest Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE

(Alzatea, Rhynchocalyx). Two species of tracheary elements reported to have vestured pits Penaeaceae, Brachysiphon rupestris Sond. and are tracheids in the sense of Bailey (1936), Sonderothamnus petraeus R. Dahlgren, occur only Carlquist (1984, 1988a, 2001), Lens et al. (2003), in crevices on large boulders. This is probably and Sano et al. (2011). Tracheids are to be primarily related to fire avoidance, but the crevice interpreted as conductive cells (Carlquist, 1984), habitat is certainly an exposed and dry one. This and thus the role that vestures must play in the ecological range invites comparison to diversity in conductive process is underlined and expanded. vestured pits. There has been notable range in diversification with respect to ecology in some genera with vestured pits, such as Acacia, Echium Materials and methods and Eucalyptus. Do vestured pits aid in radiation of genera into a diversity of habitats? The range in The collection data for the specimens studied is habit in the Penaeaceae alliance is also consider- given in Table 1. Unless otherwise stated in cap- able, including small (the rock-crevice spe- tions for figures, all wood samples studied were cies of Penaeaceae) to shrubs with longer branches taken from stems judged to have mature wood and lignotubers (Endonema, Glischrocolla), to patterns. All materials were available in dried small (Alzatea) and medium-sized trees form rather than preserved in liquid. (Olinia, Rhynchocalyx). Wood anatomy terminology follows that of Each group studied is likely to contribute some Carlquist (1984, 1988a, 2001). information relevant to understanding the physio- Except for the specimens of Alzateaceae, logical significance of vestures. Ecology does not , and Rhynchocalycaceae, the necessarily equate to physiological significance, used here had been sectioned on a sliding because vestures are conservative structures, not microtome and made into permanent slides studied easily evolved or modified or even lost, if the by Carlquist and DeBuhr (1977). In order to study comparative data are indicative. Thus a humid the vestured pits on these sections, the slides were forest tree, such as some species of Eucalyptus, soaked in xylene to remove cover slips and dis- may possess vestured pits in vessels even though solve the Canada balsam mounting medium. The ancestrally, Eucalyptus probably occupied arid sections thus retrieved were cleansed in several areas. Vestures have been hypothesized to reduce changes of warm xylene over a period of three the chances of air embolism formation in water days, and dried under pressure between pairs of columns, or possibly aid in water column repair glass slides. The wood samples of Alzateaceae, (Carlquist, 1983, 2016). This hypothesis is bol- Crypteroniaceae, and Rhynchocalycaceae were stered by recent evidence by McCully et al. twig portions removed by curators from herbarium (2014). These workers call attention to the distri- specimens cited above. bution of hydrophilic and hydrophobic areas on The collections of Penaeaceae were made in vessel walls. Pit cavities are hydrophilic. 1973, and authenticating details of these speci- Likewise, Kohonen (2006) and Kohonen and mens were given by Carlquist and DeBuhr Helland (2009) call attention to surface relief in (1977). The studies of that family and of vessels as a source for wettability of vessel walls. Oliniaceae in the present essay were based on There have been other hypotheses for the function sliding microtome sections that were stained and of vestured pits (Jansen, S, et al., 2004). All mor- made into permanent slides mounted with Canada phological variations in vestured pits are potential- balsam. In order to study the vestured pits, the ly significant, because these variations may tell us slides were soaked in xylene, cover slips re- about function. In the present essay, variations with moved, and the sections cleansed in several respect to organography (root, lignotuber, stem) changes of warm xylene over a period of three have been examined. Likewise, variations with days, and dried between pairs of glass slides. respect to the taxonomic system can be examined Twig portions of various diameters of because species from all genera of the Penaeaceae Alzateaceae, Crypteroniaceae, and clade are represented. Rhynchocalycaceae were derived from her- The role of vestures in imperforate tracheary barium specimens. These portions were elements is just beginning to be reported boiled in water, then sectioned by hand with (Carlquist, 2016). These occurrences are informa- single-edged razor blades. The sections were tive and important, because all of the imperforate rinsed in several changes of warm distilled Author's personal copy

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TABLE 1. Source of Myrtales samples examined in this study.

Taxon Collector or Source Provenance

Alzateaceae Alzatea verticillata Ruiz & Pav. H. van der Werff 18,943 (US) Ecuador: Zamora Combretaceae fruticosum (Loefl.) Stuntz Material from San Marcos Growers Cult. Santa Barbara, CA Conocarpus erectus L. O. degener 35,791 (SBBG) Cult. Hawai’i: O’ahu Terminalia catappa L. Joan Evans s.n., Jun, 2015 Hawai’i: Kaua’i Crypteroniaceae paniculata Bl. J. F. Maxwell 87–105 (A) Thailand: Songkla Lythraceae Punica granatum L. S. Carlquist s.n. Cult. Santa Barbara, CA Sonneratia alba Sm. S. Carlquist s.n. Cult. Singapore Bot. Gard. Oliniaceae Olinia cymosa Thunb. S. Carlquist 4598 (RSA) S. Africa: Cape Province Olinia usambarensis Gilg L. J. Brass 16,551 (UC) S. Africa: Natal Penaeaceae Brachysiphon acutus (Thunb.) A. Juss. S. Carlquist 4694 (RSA) S. Africa: Cape Province Brachysiphon fucatus (L.) Gilg S. Carlquist 4753 (RSA) S. Africa: Cape Province Brachysiphon rupestris Sond. S. Carlquist 5000 (RSA) S. Africa: Cape Province Endonema lateriflora Gilg S. Carlquist 4883 (RSA) S. Africa: Cape Province Glischrocolla formosa (Thunb.) R. Dahlgren S. Carlquist 4753 (RSA) S. Africa: Cape Province acutifolia A. Juss. S. Carlquist 4744 (RSA) S. Africa: Cape Province Penaea cneorum Meerb. S. Carlquist 4539 (RSA) S. Africa: Cape Province Saltera sarcocolla (L.) Bullock S. Carlquist 4500 (RSA) S. Africa: Cape Province Sonderothamnus petraeus (W. F. Barker) R. Dahlgren S. Carlquist 4678 (RSA) S. Africa: Cape Province Stylapterus fruticulosus (L.f.) A. Juss. S. Carlquist 4600 (RSA) S. Africa: Cape Province Rhynchocalycaceae Rhynchocalyx lawsoniana Oliv. H. B. Nicholas s.n., 20 April 1952 (US) S. Africa: Natal Vochysia braceliniae Standl. Y. E. J. Mexia 6081 (UC) Peru: Loreto water and dried between clean glass slides bridges of secondary wall material that intercon- under pressure. nect vestures (e.g., Figs. 2Cand3A–D). Vestured All sections, from whichever source, were pits seen from the outer surface of a vessel or mounted on aluminum stubs, coated with gold, tracheid selected for illustration are ones in which and examined with a Hitachi S2600N SEM. the pit membrane has been removed by section- Treatment with bleach (sodium hypochlorite) ing, thus revealing the full extent of vestures. was not undertaken because although this solu- tion may remove artifacts, it can produce other changes in sectioned material. Artifacts can, in Results: Pits in xylem of Myrtales my experience, be readily identified because of their lack of uniformity in size and shape as well A. THE MYRTALEAN MATRIX as other features. That the imperforate tracheary elements of ThedistributionofvesturesinMyrtaleswas Penaeaceae should be termed tracheids rather than presented by van Vliet (1978) and Jansen et al. fiber-tracheids or libriform fibers is shown not (2001). Although I could have restricted the pre- only by their pitting but also by the fact that sentation to one image of each of the species of vessels in Penaeaceae are solitary or nearly so the Penaeaceae alliance for which material was (Carlquist & DeBuhr, 1977;Carlquist,1984), de- available, I have chosen a larger context for the spite the arid habitats of most of the species. following reasons: In some preparations, portions of the pit mem- Our ideas on the composition and phylogenetic brane, a primary wall, cling to some of the ves- relationships of Myrtales have changed because tures (e.g., Fig. 2E). These are not to be confused of the findings in molecular-based studies (e.g., with an entirely different phenomenon, the Schönenburger & Conti, 2003) summarized in Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE

FIG.2. Vestured pits from vessels of Combretaceae (A–E) and Vochysiaceae (F). A–C. Conocarpus erectus. A. Pits seen from the inner surface of a vessel, showing vesture fascicles. B. Pits seen from the outer surface of a vessel; bases of some vesture fascicules seen in sectional view. C. Pit seen from the outer surface of a vessel, vesture tips shown. D. Combretum fruticosum:pit seen from the outer surface of vessel. E. Terminalia catappa: pits seen from the outer surface of a vessel. F. Vochysia braceliniae: pit seen from the inside of a vessel.

Fig. 1. This permits us to see whether vesture pits as derived from optical sections was drawn by morphology and distribution parallels the current Bailey (1933). Those drawings are not only molecular phylogeny. highly informative, they exceed the capabili- Greater attention to seeing vestured pits from ties of most microscopists. Scanning electron both the inner and outer surfaces of vessels im- microscopy can replicate these sectional proves our understanding. A selection of vestured views if that view (e.g., Fig. 6F) is available, Author's personal copy

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FIG.3. Vestured pits in vessels of Sonneratia (Lythraceae) and Crypteronia (Crypteroniaceae). A–C. Sonneratia alba. A. Inner surface of a vessel portion in which vestures extend beyond the pit aperture. B. Pit from an inner vessel surface, vestures confined to pit cavity. C. Outer surface of a vessel, vestures bridged with each other. D–F. Crypteronia paniculata. D. Inner surface of a vessel; vestures randomly interconnected. E. Inner surface of vessel, vestures attached basally into fascicles. F. Outer surface of vestures; vesture tips numerous (some pit membrane remains on pit at right). but views of vestures from both inner and that compilation can always be expanded as re- outer surfaces of vessels gives a good sum- ports are published. mation of three-dimensional structure of ves- Currently available images of vestured pits re- tured pits. fer mostly to vessels, and vestures on pits of Although we have a reasonably accurate un- imperforate tracheary elements are little known. derstanding of which genera have vestured pits, These vestured pits occur on tracheids; the sole Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE exception to that generalization is a report by Combretaceae. Among the species illustrated here, Ohtani (1987)inDamnacanthus indica Gaertn.f. they can be seen in Vochysia (Fig. 2F), Sonneratia of peculiar vestures in septate fibers. As the sole (Fig. 3B, C) and Crypteronia (Fig. 3D, E). Condi- exception reported despite extensive study of tions intermediate between fasciculate fusion of fibriform cells in woods by means of SEM, this vesture bases and random bridges between adja- example proverbially proves the rule that vestured cent vestures are to be expected, and recognition of imperforate tracheary elements are tracheids and particular types becomes less feasible as material is are cells capable of conduction. more thoroughly studied. Punica (Fig. 9F) may The context in which vestured pits have to date represent such an intermediate condition. Vestured been reported is not wide enough yet. For exam- pits in vessels of Punica have been figured by ple, we need to know whether vestured pits occur Bridgwater and Baas (1978). in roots as well as stems, in herbs as well as As seen from the inner surface of vessels, some woody , in mesophytes as well as xero- Myrtales have vestures that spread outward from phytes, and in primary as well as secondary xylem the pit aperture onto the vessel surface. The most (Carlquist, 2016). extreme example of this is Lumnitzera Comparison of a clade with outgroups can give (Combretaceae), in which the inner surface of the us ideas of the evolutionary patterns of vestured vessel is covered with a thick felt of vestures (van pits (e.g., Jansen et al., 2001). Vliet, 1978). Sonneratia (formerly in an indepen- Vessel-to-vessel pits in the early-diverging fam- dent family, Sonneratiaceae, now included in ily Combretaceae (Fig. 2A–E) are characterized by Lythraceae), has a less extreme version of this a large number of vesture tips facing the pit mem- phenomenon (Fig. 3A) on vessel to vessel contacts branes. In the species imaged here, the fewest tips but not on vessel to ray contacts (Fig. 3B). Vestures are evident in the pits of Conocarpus erectus L. extending onto inner surfaces of vessels have been (Fig. 2v); the most are in Combretum fruticosum illustrated by Meylan and Butterfield (1978)for (Loefl.) Stuntz (Fig. 2D) and Terminalia catappa such as Metrosideros. L. (Fig. 2E). There are also differences in the Such vestures may be widespread in Myrtaceae, degree to which vestures are fused into fascicles. but we have comparatively little data on vestured As seen from the lumen side, the vestures are fused pits of Myrtaceae and Melastomataceae. into fascicles or flanges (Fig. 2A). These fascicles Vestures on the bordered pits of imperforate were figured by van Vliet (1978)forTerminalia tracheary elements (= tracheids) of Myrtaceae chiriquensis Pittier. As seen from the outer vessel were reported by Meylan and Butterfield (1974, surfaces, the fused vesture bases can be seen where 1978). They were also reported in tracheids of sectioning has shaved away some of the vessel Crypteroniaceae by van Vliet (1975). They are wall and we have a view deeper into the pit cavity reported to be absent on imperforate tracheary (Fig. 2B). This appearance was figured for elements with vestigial borders on pits (fiber- Quisqualis (Combretaceae) by van Vliet (1979). tracheids) or no borders on pits (libriform fibers) Aview from the inside of the vessel in Crypteronia as a generalization by van Vliet (1978), but he (Fig. 3E) is an example of fusion into fascicles or cites no species in support of this observation. The flanges. Van Vliet (1978) found this kind of ves- figures by van Vliet (1975) of vestured and non- ture in Dissotis of the Melastomataceae. Van Vliet vestured pits side by side on imperforate tracheary (1978) also found this type of vesture in a number elements of (Crypteroniaceae) of species of Terminalia; the appearance of ves- probably represent the result of sectioning remov- tures as seen from the outside of a vessel of ing vestures from some pits. Terminalia catappa (Fig. 2E) does not reveal this, whereas views of pits from the lumen side of the B. THE PENAEACEAE ALLIANCE vessel do show such aggregation. In Combretum fruticosum (Fig. 2D), the ves- (1) Oliniaceae tures are not fused into fascicles, but are linked together. Irregular bridges or linkages that connect In Olinia, imperforate tracheary elements have vestures into a three-dimensional network are per- pits that are narrowly bordered pits. These pits are haps the most common condition in Myrtales, and small, sparse, and non-vestured (Fig. 4A). These were figured by van Vliet (1978)forMedinilla characteristics accord with the demonstration (Melastomataceae) and Strephonema of the (Carlquist, 2014)thatOlinia has septate fibers. Author's personal copy

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FIG.4. Pits on tracheary elements of Oliniaceae. A–D. Olinia cymosa. A. Outer surface of a fiber-tracheid, vestures absent. B. Vestures extend a little beyond pit apertures on inner surface of a vessel. C. Vestures occur in a groove between two pits on inner surface of a vessel. D. Pits seen from outer surface of a vessel. E, F. Olinia usambarensis. E. Pits seen on the inner surface of a vessel; vestures sparser than in O. cymosa. F. Pits seen on the outer surface of a vessel.

The vessels and vessel pits of two species of Olinia (Fig. 4B, C). Occasional bridges of wall material (Fig. 4B–F) are, however, prominently vestured, interconnect the vestures (Fig. 4B–F). with some vestures extending a little beyond the pit (2) Penaeaceae aperture onto the inner surface of the vessel wall (Fig. 4B, C, E). Such Bextra-limital^ vestures may All Penaeaceae have tracheids with well- extend laterally between adjacent pit apertures developed bordered pits that are vestured Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE

FIG.5. Vestured pits in wood of Penaeaceae. A–C. Brachysiphon acutus. A. Outer surface of a tracheid to show sparseness of pits. B. Outer tracheid surface; pits are vestured (some cut away by sectioning). C. Outer surface of a vessel. D. Brachysiphon fucatus: inner surface of a vessel. E, F. Glischrocolla formosa: vessels from lignotuber. E. Vestured pits seen on the inner surface of vessel. F. Vestured pits seen from the outer surface of vessel.

(Figs. 5A, B; 6E; 7A, B; 8A; 9A, B). Vestures are acutus (Thunb.) A. Juss. Fig. 5C) and absent in parts of the two pits in Fig. 5A, B B. fucatus (L.) Gilg (Fig. 5D), pits are about because of the Bscrape away^ effect of sectioning. as dense on vessels as they are on tracheids, Pits on vessels are all vestured, with the pits and vestures are randomly bridged by wall predominantly vessel-to-tracheid because ves- material. Brachysiphon rupestris (Fig. 7E) is sels are minimally grouped. In Brachysiphon a small restricted to crevices in large Author's personal copy

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FIG.6. Vestured pits in wood of Endonema (Penaeaceae). A, B. E. lateriflora. A. Two vestured pits seen on the inner surface of vessel. B. Vestured pit seen from the outer surface of a vessel. C–F. E. retzioides. C. Three pits seen on the inner surface of a vessel. D. A pit seen on the outer surface of a vessel. E. Three vestured pits in face view on the inner surface of a tracheid. F. Vestured pit on inner surface of tracheid wall in sectional view, corresponding to the bottom center of 6E; vestures in the central part of a pit cavity. boulders (as is Sonderothamnus petraeus, F) appear to have a vesture-free zone at the pe- Fig. 7F). The vessel pits of B. rupestris are riphery of pit cavities. This is interpreted as due to like those of the other, more robust shrubby the sectioning away of some of the proximal species of Brachysiphon. portion of the pit cavity, judging by the results in Lignotuber vessels of Glischrocolla formosa Punica (Fig. 9F) in which some vestures are (Thunb.) R. Dahlgren illustrated here (Fig. 5E, present at the periphery of some pits (bottom) Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE

FIG.7. Vestured pits in wood of Penaeaceae. A–D. Saltera sarcocolla. A. Pits seen from the inner surface of a tracheid. B. Vestures seen in a pit canal on a tracheid, part of the wall sectioned away. C. Smaller pits on the inside of a vessel, close to a perforation plate; note bridges between vestures. D. Larger pit on the inside of a vessel, midway along the length of the vessel. E. Brachysiphon rupestris: pits as seen on the inner surface of a vessel. F. Sonderothamnus petraeus: a vestured pit seen on the inner surface of a vessel. but absent in others (top). There is no appreciable Sond. (Fig. 6C, D). There is a slight tendency for difference between stem and lignotuber vessel vestures to extend beyond the pit apertures. Ves- pits in Glischrocolla. tures are connected with each other by random Vessel pits in Endonema lateriflora Gilg bridges rather than by coalescence into fascicles. (Fig. 6A, B) are very similar to those of E. retzioides The sizes of pits and also their vestures are about Author's personal copy

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FIG.8. Vestured pits in the wood of Penaea. A–D. Penaea cneorum Meerb. A. Row of pits on a tracheid, seen from the outer surface. B. Pits on a tracheid with some wall layers sectioned away, showing clustered globular vestures in pit canals. C. Pit on a tracheid, seen from the inner tracheid surface. D. Pits on a vessel, seen from the outer vessel surface. E, F. Penaea acutifolia. E. Pit seen on the inner surface of vessel in a root. F. Pit seen from the outer surface of a vessel in a root. thesameinthetwospeciesofEndonema.The shape and bordered. By contrast, pits in the ves- imperforate tracheary elements of E. retzioides have sels of S. sarcocolla (L.) Bullock are circular in more widely spaced vestured bordered pits than shape (Fig. 7C, D). Pit size and number of ves- those of E. lateriflora (Fig. 6E, F). tures differ in size from one place on a vessel to Saltera tracheids (Fig. 7A, B) have prominent- another (Fig. 7C, D). The vestures are bridged ly vestured pits which are slit-like in aperture with each other by very slender strands of wall Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE

FIG.9. Vestured pits of Stylapterus ofthePenaeaceae(A–E), and Punica of the Lythraceae (F). A–E. Stylapterus fruticulosus. A. Pits spaced along the outer surface of a tracheid wall. B. Pits on the outer surface of a tracheid at higher magnification to show vesturing. C. Vestures extend onto the inner vessel wall surface. D. Small vestures on inner surface of a vessel occur in groove between pits adjacent in a helix. E. A pit seen from the outer surface of a vessel. F. Punica granatum: pits on a vessel, seen from the outer surface. material. On the inner surfaces of vessels, vestures Penaea cneorum Meerb. has tracheids with extend onto the vessel wall surface to a moderate round pits in axial rows along the tracheid degree (Fig. 7D). surfaces (Fig. 8A).Theyaredenselyvestured. Sonderothamnus petraeus has narrow pit aper- Sections below the wall surface (Fig. 8B) re- tures in vessels. The pits are densely vestured as vealed that vestures are globular and incon- seen on the inner surfaces of vessels (Fig. 7F). spicuously bridged. In tracheids of P. cneorum Author's personal copy

BRITTONIA [VOL stems, pit apertures facing the vessel lumen vestured (Fig. 10E). Vestures do not extend are narrow and oval (Fig. 8C); vestures are onto the vessel surface, but are confined to the densely grouped. As seen from the outside pit apertures (Fig. 10F). As seen from the outer surfaces of vessels, the pit cavities are circular vessel surface, pit cavities are circular and densely vestured (Fig. 8D). Relatively (Fig. 10G). Vestures are variously bridged to- small pits occur in roots of P. acutifolia A. gether into groupings. Van Vliet (1975)report- Juss. (Fig. 8E). As seen from the outer sur- ed that R. lawsoniana has septate fibers. The faces of vessels, the vestures are globular pits of the septate fibers are vestigially bordered (Fig. 8F). Vestures are bridged by easily (Fig. 10H). Gelatinous fibers are present in ad- discerned strands of wall material (Fig. 8E, F). ditiontotheseptatefibers(vanVliet,1975). Stylapterus fruticulosus (L.f.) A. Juss.has tra- cheids with clearly circular pit apertures as seen from outer surfaces (Fig. 9A). Where Discussion and conclusions sectioning scrapes away some of the tracheid VESTURED PITS IN TRACHEIDS: AN UNAPPRECIATED wall, parts of the tracheid pit canals may CORRELATION appear to lack vestures in places (Fig. 9B), but that apparent absence is only a sectioning Vestured pits are clearly related to the conduc- artifact. As seen from vessel inner surfaces, tive process in vessels (see Introduction). The S. fruticulosus pits are elliptical, with a mod- likelihood that vestures are hydrophilic and play erate tendency for vestures to extend beyond a role in the prevention of embolisms and/or the the pit apertures onto the vessel surface reversal of embolisms has been presented (Fig. 9C). Where pits are closely adjacent (Carlquist, 1983). Other forms of vessel wall on the vessel wall, the depression between sculpture, such as helical thickenings, a frequently the pit apertures often bears vestures encountered feature in angiosperms (especially (Fig. 9D). As seen from the outer surfaces those of xeric areas) may have a similar effect of vessels, pits of S. fruticulosus have rela- (Kohonen, 2006; Kohonen & Helland, 2009; tively large (for the family) circular pit cav- McCully et al., 2014). ities with numerous vestures that are clearly Tracheids in wood can resist passage of air bridged into groups (Fig. 9E). bubbles from cell to cell because of the restric- (3) Alzateaceae tion that pit membranes offer. A tracheid popu- lation can retain functioning water columns The sole species, Alzatea verticillata Ruiz & while water columns in adjacent vessels have Pav., has prominently vestured vessel-to-vessel been broken by air embolisms. This leads to the pits (Fig. 10A). The vestures extend for various phenomenon of solitary vessels in wood that distances onto the inner surface of the vessels; contains tracheids or vasicentric tracheids Fig. 10A shows a moderate amount of this, while (Carlquist, 1984). In wood with fiber-tracheids Fig. 10B illustrates extensive vesture presence on or libriform fibers, grouping of vessels serves as wall surfaces. Both conditions may be present in a a mechanism for achieving conductive safety. single vessel. Vessel to ray pits in A. verticillata Tracheid presence is thus shown to be superior are large, sometimes scalariform, and window- to vessel grouping as a means to maintain water like, much larger than vessel-to-ray pits in other column integrity (Carlquist, 2016). If vestures are effective in preventing families of the Penaeaceae alliance (Fig. 10C, D). embolismsinvessels,theyshouldalsobeex- Higher magnification of the vestures in these pits pected in tracheids of vessel-bearing angio- (Fig. 10D) reveals conspicuous bridging between sperms that have vestures in vessels. Vestures the vestures. Alzatea has septate fibers with sim- are indeed present in the tracheids of vessel- ple, vestigially bordered non-vestured pits bearing Brassicales (Carlquist, 2016)and (Fig. 10E) as reported by van Vliet (1978). Some Myrtales. Helical thickenings and similar gelatinous fibers are also present. sculpturing in vessels tends to be present, of- (4) Rhynchocalycaceae ten in more pronounced form, in narrow ves- sels and tracheids of those species (Carlquist, The sole species, Rhynchocalyx lawsoniana 1988a, 2001). In Myrtales, tracheids occur in Oliv., has vessel-to-vessel pits that are densely Penaeaceae, Crypteroniaceae, and in some Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE

FIG.10. Pits on tracheary elements of Alzatea of the Alzateaceae (A–E) and Rhynchocalyx of the Rhynchocalycaceae (F–H). A–E. Alzatea verticillata. A. Inner surface of a vessel, vestures mostly restricted to pit aperture vicinity. B. Inner surface of a vessel; pits extend onto the vessel surface. C. Large vessel-ray pits, seen from the outer surface of a vessel. D. Smaller vessel-ray pit (some vestures sectioned away), seen from the outer surface of a vessel. E. Simple pits seen on the outer surface of a septate fiber. F–H. Rhynchocalyx lawsoniana. F. Pits seen on inner surface of vessel. G. Pits seen from the outer surface of a vessel. H. Outer surface of a septate fiber-tracheid, pit border vestigial.

Melastomataceae and Myrtaceae. In Myrtaceae 1978). There is only a single record of ves- with septate fibers (and grouped vessels), no tures in septate fibers (Ohtani, 1987). The vesturing is present in the septate fibers, but presence of vestures on pits of an imperforate vesturing is present in the tracheids of tracheary element offers a reliable indicator Metrosideros (Meylan & Butterfield, 1974, that element is a tracheid. Author's personal copy

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ECOLOGICAL AND ORGANOGRAPHIC DISTRIBUTION Do vestured pits in Penaeaceae exhibit OF VESTURED PITS organographic correlations? Although extensive comparisons were not made, the few that were show As noted above, tracheid presence is more effec- no major differences, except for somewhat smaller tive at promoting conductive safety than vessel size of pits in Penaea roots. The morphology and grouping. Genera with tracheids or abundant extensiveness of vestures is much the same through- vasicentric tracheids (Quercus) are capable of living out the body, including the lignotubers. in localities with pronounced seasonal drought. Genera with vestured pits (Acacia, Echium,and Eucalyptus) have radiated well in such localities. FUNCTION OF VESTURED PITS: EVIDENCE FROM OUTSIDE Eucalyptus has both vasicentric tracheids and ves- THE PENAEACEAE ALLIANCE tured pits—and the radiation of Eucalyptus in Aus- tralia into habitats that are dry, hot, or wet and cold Although vestured pits occur in a limited num- is astonishing. The radiation of Brassicaceae and berofangiosperms(Jansenetal.,2001), warty wall Capparaceae may also be attributed to presence of layers on the inner surfaces of tracheids and vessels vestured pits (Carlquist, 2016). Metrosideros occur more widely (Wardrop et al., 1959;Parham (Myrtaceae), with vestured pits in vessels and in &Baird,1974), notably in conifers. These struc- tracheids, is present in wet rain forest, bogs, dry tures may be functionally equivalent to vestures. forest, on new lava, and in many intermediate hab- Tracheids of Winteraceae that are native to cooler itats in the Hawaiian Islands (Wagner et al., 1990). areas have warty inner tracheid surfaces, whereas Penaeaceae are most often small, sparsely species from warmer areas lack these structures branched shrubs in relatively barren areas of (Carlquist, 1988b, 1989). Meylan and Butterfield Table Mountain Sandstone in Cape Province, (1978) illustrate inner tracheid surfaces in South Africa. These regions qualify as xeric. Pseudowintera (Winteraceae), a New Zealand en- Two species, Brachysiphon rupestris and demic. Pseudowintera axillaris (J.R.Forst.&G. Sonderothamnus petraeus,growincreviceson Forst.) Dandy, from more northern (warmer) and boulders (but rarely on the adjacent flats). This coastal localities (35–42°S) has smooth tracheid habitat preference may be based on fire avoid- surfaces, whereas P. colorata (Raoul) Dandy from ance, but the boulder habitat is certainly xeric. colder localities (36–47°S) has warty inner tracheid Only a few Penaeaceae occur near streams or in surfaces. Warty inner tracheid surfaces occur in a forests (Goldblatt & Manning, 2000), and all are number of conifers (Wardrop et al., 1959)aswell in sunny areas. In a study of of the as angiosperms. Meylan and Butterfield (1978) Penaeaceae alliance, Dickie and Gasson (1999) state that Bwhen present, the warty layer commonly emphasize low nutrient content of the soils where lines the pit chambers^ in the New Zealand coni- Penaeaceae grow rather than dryness, but low fers they studied. This is significant because nutrient content promotes scantiness of vegetation McCully et al. (2014) found that pit cavities in cover, with attendant high evaporation rates. Un- the material they studied are hydrophilic. der these circumstances, xeromorphic xylem and By extension, one would expect vestures in leaves are to be expected, a correlation evident wood of species to be hydrophilic, and thus by when one does field work in these regions. Sim- meniscus effects not to allow passage of air bub- ilar correlations are clearly evident in southwest- bles in or out of a cell with vestured pits (whereas ern Australia (Carlquist, 1974). Most habitats of air bubbles travel relatively more readily from one Penaeaceae are fire-adapted, and areas that burn vessel element to another). A concept presented frequently show xeromorphic woods in Califor- earlier (Carlquist, 1983). The work of Kohonen nia, Australia, and South Africa (unpubl. Data). (2006) and Kohonen and Helland (2009)onthe Oliniaceae, Alzateaceae, and Rhychocalycaceae hydrophilic nature of helical sculpturing in vessels are the other members of the Penaeaceae alliance can be cited as supporting this possibility. Those (Fig. 1). These three families have septate fibers authors were working primarily with angiosperm rather than tracheids (van Vliet, 1978; Baas, 1979), vessels. Jeje and Zimmermann (1979) found that and all are trees of humid forests. Septate fibers such sculpturing accelerates travel of water into a may serve as storage cells for starch, as in vessel, but that might not be the most important Oliniaceae (Carlquist, 2014), facilitating rapid effect of this form of relief. In a large sample of flushing of leaves. Asteraceae (Carlquist, 1966), helical sculpturing Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE proved to be associated with drier climates, and the Type B of van Vliet (1978); it occurs not Asteraceae in these climates have narrower ves- merely in a number of Myrtales, but in Brassica- sels. In various angiosperms, helical thickenings ceae, such as Armoracia (Carlquist, 2016)aswell. are more prominent, where present, in latewood Extension of vestures onto the inside surface than in earlywood (Carlquist, 1975, 1988a, 1988b, of a vessel wall can be seen in Combretaceae. 2001). Water flow in latewood is presumably Lumnitzera has probably the most extreme ex- slower than in earlywood because of increased pression of this feature in angiosperms (van friction (Zimmermann, 1983). Admittedly, helical Vliet, 1978). This feature may be related to thickenings are quite different in appearance from the mangrove habitat of Lumnitzera;strong vestures, but if both serve similar purposes by negative pressures have been recorded in man- virtue of their wettability and surface area, they grove xylem (Scholander et al., 1962). In the should be taken into consideration where interpre- Penaeaceae alliance, the presence of vestures tation of vestures and warts is concerned. Compar- on the inner vessel surface is thus far known ative anatomy shows that helical sculpturing in only in Alzatea (Fig. 10B). It occurs in a variety vessels is much more widespread that vestures. of Myrtales other than Combretaceae, such as The simplest explanation seems to be that while Sonneratia (Fig. 3A) and Metrosideros both serve similar functions, vestures have evolved (Meylan & Butterfield, 1974, 1978). in relatively fewer species because vestures are Globular vestures, such as are typical of the developmentally more difficult to achieve (and Penaeaceae clade, occur in Strephonema of the vestures are by no means uniform throughout an- Combretaceae. Globular vestures that are intercon- giosperms and Gnetales). Helical sculpture follows nected by a network of seemingly random bridges the cyclosis pattern of cytoplasm in elongate cells, of varying thickness characterize the Penaeaceae and thus represents a simple deviation from a clade (Fig. 7C, D). Caution is required in stating smooth wall pattern. the occurrence of vestures and their diversity in The concept that vestures are a mechanism for any systematic group. Only a small fraction of the minimizing deflection of pit membranes during pits in any given wood section can be imaged with pressure change events in tracheary elements (see SEM, and studies that examine more than one Jansen, S, et al., 2003) does not appear to be collection of a species are still unusual. supported. The occurrences of vestures on vessel walls facing a vessel lumen (e.g., Alzatea, Metrosideros) is one of several phenomena that HOW VESTURED PITS AND ALLIED PHENOMENA SHOULD are discordant with that idea. Safeguarding water BE INVESTIGATED columns may involve various mechanisms that are not yet understood in detail (Holbrook & Themostcommonmethodemployedfor Zwieniecki, 1999). reporting of vestured pits is to image pits on the outer surface of a vessel, pits from which the pit membrane has been removed by sectioning, thus RANGES OF EXPRESSION WITHIN THE PENAEACEAE exposing the pit cavity. Because outer surfaces of ALLIANCE a vessel are convex, the image formed by the electron beam is very good. Imaging the vestures The four families of the Penaeaceae clade do as seen from the inside of a vessel, which is not contain the entirety of vesture expressions that concave, is potentially more difficult but is often can be found within the order Myrtales. The di- well within the capabilities of a SEM technician. versity of vestures in Myrtales is greatest in Pits as seen on the inner surface of a vessel Combretaceae, which departs earliest from the offer information that complements the view from Myrtales clade (Fig. 1). The Penaeaceae alliance outer vessel surfaces, and is essential to a three- possesses no features not found in other families dimensional understanding of vestures. Conse- of Myrtales. For example, grouping of vestures quently, both views have been employed here. into fascicles, somewhat like the branches of a Ideally, one wishes for a three-dimensional view coral, is found in a number of genera of of vestured pits. Such views were offered in the Combretaceae such as Conocarpus (Fig. 2A–C). drawings by Bailey (1933), made by very careful This feature also occurs in Crypteroniaceae observation at the upper limits of resolution of a (Fig. 3), sister to the Penaeaceae clade. This is light microscope. By means of fortunate sections Author's personal copy

BRITTONIA [VOL through pits, one can image the disposition of all subsequent examples are then referred to vestures within the pit cavity, including vesture the proposed terms. However, extensive stud- branchings and interconnections (e.g., Fig. 6F). ies may demonstrate that existing terminology Perfect sections through the pit cavities of pits are is inadequate and misleading. Should the old rarely common even with good technique. Ideally, terminology be retained in the interest of con- one would like these Blongitudinal^ or Bsagittal^ sistency, or should terminology reflect the ad- sections through pits in addition to views from the vances in a science? Retention of obsolete outside and inside of a vessel. In an analogous terms tends to hinder understanding and to way, in studies of wood anatomy one wants trans- freeze a branch of science into a past era. On verse, tangential, and radial sections to reach a full the other hand, new terms should be proposed understanding of any wood three-dimensionally. on the basis of compelling new evidence. Our High magnification SEM imaging and trans- knowledge of vestured pits is probably not mission electron microscopy (TEM) are needed sufficiently advanced so that we can for further understanding of vestures. Vestures are confidently propose terminology. Ohtani usually figured as smooth structures, but do some et al. (1984) suggest using Bvestures^ and of them have rough surfaces, as suggested by the Bvestured layer^ as blanket terminologies to vestures in Vochysia (Fig. 2F)? Outside of cover what have been variously called ves- Myrtales, rough-surfaced vestures occur in tures, warts, warty layer, etc. (Wardrop et al., Echium of the Boraginaceae (unpubl. Data). 1959;Parham&Baird,1974). Ohtani’spro- Tracheids in Penaeaceae as well as in some posal seems entirely acceptable. If studies other Myrtales (e.g., Metrosideros)havevestures show distinctions in vestures, we can always and lead one to the conclusion that one must look use adjectives to describe these variations. beyond vessels in the study of vestures. This has In this regard, we should note that we lack been shown in such brassicalean families as ontogenetic knowledge of vestures. No study Pentadiplandraceae (Carlquist, 2016)and known to me has as yet followed the stages in Stixaceae (Carlquist et al., 2013). vesture development as vessel walls are laid Techniques for the study of vestures have been down. Our knowledge of vestures at the spe- described by Jansen et al. (2001). One standard cies level is only incipient. Unfortunately, method involves treatment of sections with bleach SEM is not available to most workers, and (sodium hypochlorite solution) in order to remove thus our exploration of vestured pits is still secondary compounds. We do not know the en- in its initial stages. This fact, however, indi- tirety of what this or other reagents do. Unfortu- cates that much new information remains, and nately, microtechnique is rarely subject to experi- vestures and vestured wall layers in vessels mentation. We would like to know the effect of and in tracheids comprise a promising field various reagents on sections of a given wood. for further investigation. However, vestures seem to be composed of the same materials as the secondary walls of vessels and tracheids, and thus can probably be treated Acknowledgements with the same reagents as used on wood sections Special mention should go to the work of Ger J. for light microscope observation without C. M van Vliet and others in the wood anatomy of appreciable damage. So far, there is no evidence Myrtales project, which was the idea of Pieter Baas, that reagents damage vestured pits, although as and which has produced a number of excellent noted by Jansen et al. (2001)wedohaveevidence studies. Individuals who provided me with material of the presence of secondary products naturally include David Boufford, Vicki Funk, and Chris deposited in the wood. These create artifacts and Niezgoda. My fieldwork in South Africa was aided have led to incorrect reports of vestured pits in by grants from the National Science Foundation some taxa. and the Simon Guggenheim Foundation. That fieldwork would have not been successful without the help of Elsie Esterhuysen (University of TERMINOLOGY AND ITS CONNOTATIONS Cape Town) and the staff of the Compton Herbar- ium (especially John Rourke). Thanks go to Steve Terminology is sometimes imposed on Windhager, for availability of a scanning electron wood structures as a result of a few studies; microscope at Santa Barbara Botanic Garden. Author's personal copy

2017] CARLQUIST: VESTURED PITS IN PENAEACEAE ALLIANCE

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