Vestured Pits in Wood of Onagraceae: Correlations with Ecology, Habit, and Phylogeny1

VESTURED PITS IN WOOD OF Sherwin Carlquist2 and Peter H. Raven3 ONAGRACEAE: CORRELATIONS WITH ECOLOGY, HABIT, AND PHYLOGENY1 ABSTRACT All Onagraceae for which data are available have vestured pits on vessel-to-vessel pit pairs. Vestures may also be present in some species on the vessel side of vessel-to-ray pit pairs. Herbaceous Onagraceae do not have fewer vestures, although woods with lower density (Circaea L. and Oenothera L.) have fewer vestures. Some Onagraceae from drier areas tend to have smaller vessel pits, and on that account may have fewer vestures (Epilobium L. and Megacorax S. González & W. L. Wagner). Pit apertures as seen on the lumen side of vessel walls are elliptical, occasionally oval, throughout the family. Vestures are predominantly attached to pit aperture margins. As seen from the outer surfaces of vessels, vestures may extend across the pit cavities. Vestures are usually absent or smaller on the distal portions of pit borders (except for Ludwigia L., which grows consistently in wet areas). Distinctive vesture patterns were observed in the several species of Lopezia Cav. and in Xylonagra Donn. Sm. & Rose. Vestures spread onto the lumen-facing vessel walls of Ludwigia octovalvis (Jacq.) P. H. Raven. Although the genera are presented here in the sequence of a recent molecular phylogeny of Onagraceae, ecology and growth forms are more important than evolutionary relationships with respect to abundance, degree of grouping, and morphology of vestured pits. Designation of vesture types is not warranted based on the distribution of named types in Onagraceae and descriptive adjectives seem more useful, although more data on vesturing in the family are needed before patterns of diversity and their extent can be fully ascertained. Vestures are less common and may have a more complicated genetic basis than helical thickenings in vessels, but may be a more effective form of water column maintenance. Key words: Ecological wood anatomy, growth form, Onagraceae, pit shape, wood xeromorphy. Our knowledge of vestured pits is still quite incom- Myrtales progresses, patterns in the evolution of these plete. Bailey (1933) offered a major advance by not only structures will become more evident. documenting their systematic distribution, but also by The diversity of vestured pits within families of describing and figuring three-dimensional morphology Myrtales and the relationship of these structures to of vestures, using light microscopy with amazing skill. ecology and habit have been largely unexplored because With the availability of SEM, our knowledge of vestured SEM work is time-intensive. Efforts to date have largely pits has advanced much further. Vestures in vessels featured recording which families and genera have and tracheids are in a magnification range (35000 vestured pits and which do not (Jansen et al., 2001). to 315,000) at which SEM excels; the depth of focus These broad surveys have not permitted the examination of SEM facilitates three-dimensional imaging that is of diversity within genera and they are incomplete with needed for understanding these structures. Vestured respect to the three-dimensional imaging of how ves- pits have been surveyed in two groups of Myrtales, tures are grouped and how they traverse the pit cavities Combretaceae (van Vliet, 1978; Carlquist, 2017a) and pit apertures. More detailed studies of this sort have and the Penaeaceae alliance (Carlquist, 2017a). These been attempted in the Penaeaceae alliance (Carlquist, two groups lie at opposite poles of the Myrtales clade: 2017a) and in the genus Echium L. of the Boraginaceae Combretaceae is sister to all remaining Myrtales; (Carlquist, 2017b). Studies of this kind will permit Onagraceae–Lythraceae are sister to all remaining correlations between vesture abundance and morphol- Myrtales except Combretaceae (Berger et al., 2016). ogy to be correlated with diversity in ecology and growth Penaeaceae and allied families (Alzateaceae, Olinia- form. ceae, Rhynchocalycaceae) represent a crown group of When further studies are carried out, we will un- Myrtales (Stevens, 2001 onward; Berger et al., 2016). derstand more fully how these minute structures relate As our knowledge of vestured pits in the families of to the evolutionary and ecological radiation of particular 1 Those who collected or furnished wood samples deserve special thanks and are listed in Table 1. Warren L. Wagner kindly provided material of Megacorax gracielanus S. González & W. L. Wagner. The use of the SEM at Santa Barbara Botanic Garden was essential to this project, and Dr. Steve Windhager, the Director, deserves special thanks. Peter Hoch revised the last version of this paper in light of the new phylogenetic classification. We are pleased to acknowledge the role that Dr. Pieter Baas played earlier in originating a survey of myrtalean wood; a number of the resultant monographs represent the work of Dr. Ger van Vliet. 2 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105, U.S.A. 3 Missouri Botanical Garden, 4344 Shaw Blvd., St. Louis, Missouri 63110, U.S.A. VERSION OF RECORD PUBLISHED ON 16 OCTOBER 2018. doi: 10.3417/D1700001 ANN.MISSOURI BOT.GARD. 103: 443–461. 444 Annals of the Missouri Botanical Garden families and genera. For example, the two arboreal MATERIALS AND METHODS (sometimes shrubby) genera that are most species- Although presence of vestured pits in Onagraceae was rich in Australia, Acacia Mill. (Fabaceae) and Euca- noted and illustrated by means of light microscopy earlier lyptus L’Hér. (Myrtaceae), both have vestured pits, (Carlquist, 1975, 1977, 1982), those illustrations were leading one to suspect that vestured pits might have limited compared to what can be achieved using SEM. played a role in the dominance of these genera on this driest of all continents. Onagraceae offer a variety of As in the study of the Penaeaceae alliance of Myrtales growth forms, from annuals to trees to aquatic herbs, and (Carlquist, 2017a), permanent slides of wood sections range from moist forests to deserts; thus, they are an mounted in Canada balsam made decades ago proved ideal group in which to investigate the extent to which entirely satisfactory for the present study. For most species vestured pits may be related to ecology and habit. studied here, these slides were soaked in xylene until the Jansen et al. (2004) concluded that groups with vestured cover slips loosened and could be removed. The sections pits have radiated most in warm subtropical climates, were then retrieved. Because vessels in Onagraceae are but also pointed out that to test this relationship further, grouped in radial rows and vessel-to-vessel pits are optimal one should examine the range of variation in this for study of vesturing, tangential sections were preferred. character in individual families and genera. For exam- After retrieval, sections were cleansed of Canada balsam ple, in Brassicaceae (3710 species), a large family not with three changes of xylene at 60°C. The sections were considered by Jansen et al. (2004), all species appar- then dried under pressure between pairs of glass slides ently have vestured pits (Carlquist, 2016). The distri- to assure flatness. Sections were mounted on aluminum bution of Brassicaceae may be characterized as mostly stubs, sputter-coated with gold, and examined with a boreal to cool temperate, and the family is relatively rare Hitachi S2600N SEM (Tokyo, Japan). in the tropics. Some wood samples for key taxa not examined in If we posit that vestured pits aid in the water earlier studies (Epilobium canum (Greene) P. H. Raven, economy of dry land Myrtaceae such as Eucalyptus, Megacorax gracielanus S. González & W. L. Wagner, can vestured pits be held to function similarly in dry and Oenothera elata Kunth subsp. hookeri (Torr. & A. land Onagraceae such as the members of the annual Gray) W. Dietr. & W. L. Wagner) were taken from dried genus Clarkia Pursh? Clarkia flowers late in the spring stem portions and boiled in water. They were then stored and completes its life span after the places it grows in 50% aqueous ethanol and sectioned with single- have dried up. The secondary xylem of an annual can edged razor blades. The sections were next subjected to be regarded as a single growth ring, with vestured pits three changes of warm 50% aqueous ethanol and dried clearly functional structures; this relationship is dis- under pressure between clean glass slides. Tangential cussed further in the terminal section of this paper. sections were studied unless otherwise indicated. The extremely small size of these vestured pits ac- Various methods have been used by particular workers counts for the historical lack of study of vestured pits examining woods for vestured pits. There has been concern by wood physiologists. that minute droplets of substances that are artifacts might Here our observations are presented according to be interpreted as vesturing. Sodium hypochlorite (bleach) the evolutionary relationships proposed for Onagra- has been applied to sections in an attempt to minimize or ceae (Levin et al., 2004; Wagner et al., 2007), a reduce such artifacts (Jansen et al., 2001). We have tried predominantly herbaceous family that is not well this technique (comparative preparation of the three spe- represented in wood collections. Our study includes cies listed in the preceding paragraph) and found that some 23 species (Table 1), a small but representative swelling can occur—a minor artifact, perhaps, but one that sample of the 657 species in the family (Wagner deserves attention. Artifacts usually are easily detectable et al., 2007); each of the seven tribes is represented, because of their patterns: varied and irregular in shape, and we have made an attempt to cover the ecological present in one part of a section but not consistently present range of the family (Table 1, column 3). As we shall in or related to pits. White flecks on the sections of Fig- discuss later, the distribution of different kinds of ure 6 are considered artifacts, but they are easily distin- vestured pits in Onagraceae seems clearly to be more guishable from the vestures.

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