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What the Penaeaceae Alliance (Myrtales) Tells Us About the Nature of Vestured Pits in Xylem

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What the Penaeaceae Alliance (Myrtales) Tells Us About the Nature of Vestured Pits in Xylem What the Penaeaceae alliance (Myrtales) tells us about the nature of vestured pits in xylem Sherwin Carlquist Brittonia ISSN 0007-196X Brittonia DOI 10.1007/s12228-017-9477-1 1 23 Your article is protected by copyright and all rights are held exclusively by The New York Botanical Garden. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 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. Combretaceae, the first branch of the Myrtales clade, has a great diversity of vesture features in vessels compared to the Penaeaceae alliance families. Alzatea 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 species 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 wood 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 Africa 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, South Africa 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 BRITTONIA [VOL FIG.1. Phylogenetic tree of Myrtales. Redrawn from Stevens (2001 onwards). The topology of the Penaeaeae alliance is based on Schönenburger and Conti (2003). species of Olinia), 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 Rhynchocalyx (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 shrubs (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 trees (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 Crypteroniaceae, and Rhynchocalycaceae, the necessarily equate to physiological significance, woods 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
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