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Wood Anatomy of Onagraceae, with Notes on Alternative Modes of Photosynthate Movement in Dicotyledon Woods

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Wood Anatomy of Onagraceae, with Notes on Alternative Modes of Photosynthate Movement in Dicotyledon Woods WOOD ANATOMY OF ONAGRACEAE, WITH NOTES ON ALTERNATIVE MODES OF PHOTOSYNTHATE MOVEMENT IN DICOTYLEDON WOODS SHERWIN CARLQUIST Reprinted from ANNALS OF THE MISSOURI BOTANICAL GARDEN Vol. 62, No. 2, 1975 pp. 386-424 Made in United States of America WOOD ANATOMY OF ONAGRACEAE, WITH NOTES ON ALTERNATIVE MODES OF PHOTOSYNTHATE MOVEMENT IN DICOTYLEDON WOODS SHERWIN CARLQUIST Reprinted from ANNALS OF THE MISSOURI BOTANICAL GARDEN Vol. 62, No. 2, 1975 pp. 386-424 Made in United States of America WOOD ANATOMY OF ONAGRACEAE, WITH NOTES ON ALTERNATIVE MODES OF PHOTOSYNTHATE MOVEMENT IN DICOTYLEDON WOODS' SHEHWTN CARLQUIST2 ABSTRACT Vessel elements in Onagraceae correlate perfectly with groups of species; elements are long and wide in mesomorphic species, shortest and narrowest in the most xeromorphic species. Libriforra fibers in the family are thin-walled, hut many have gelatinous inner walls. The possibility that these represent not tension wood hut a water-storage mechanism is examined. Libriform fibers are mostly septate or nucleate or hoth in the family; this indicates longevity and simulation ol parenchyma in starch-stora.ue hmction. These fibers may compensate for the paucity of axial parenchyma. Interxylary phloem ("included phloem") does not occur in Fuchsia. Hauya, and Ludwigia, the genera in the family most generalized in other respects, and is absent in most annuals studied. Selective pressure for formation of interxylary phloem in the three genera may be minimal because of slow rates of photosynthate translocation within wood and selective pressure for formation of interxylary phloem in annuals may be minimal for spatial reasons. Interxylary phloem may be related to massive flowering that draws rapidly on stored starch, chiefly in the shrubby perennials. The relationships of Onagraceae seem closest to Lythraceac, Sonneratiaccae, Punicaceae, Crvpteroniaceae, and Combretaceae; also close are other myrtalean families: Melastomaceae, Myrtaceae, Penaeaceae, Oliniaceae. These affinities are clearly evident from wood features alone: vestured pits on vessels; ray cells upright to square; intraxylary phloem present adjacent to pith; libriform fibers septate or nucleate; prismatic crystals in fibers and rays. Onagraceae tend to show herbaceous characteristics in wood of herbaceous genera; woody genera such as Hauya show no indicators of herbaceous structure. The ancestral habit of Onagraceae was probably shrubby, and without interxylary phloem; interxylary phloem may have evolved more than once in the family. A practical but compelling reason for presenting this study at this time is the availability to me of an exceptional collection of wood samples. Numerous Onagraceae have woods with technically important features: interxylary phloem and associated thin-walled cells; nucleate fibers: and starch in various cell types. These features are present in or can be studied adequately only in liquid-preserved material. Dr. Peter II. Raven appreciated these facts and assembled a very fine basic collection of liquid-preserved wood samples of Onagraceae over a period of years. lie has kindly placed this collection at my disposal. Although additional wood samples have been incorporated in this investigation, the Raven collection, which represents the work of Dr. Raven and Dr. Dennis E. Breedlove (see Table 1) provided an unusual opportunity and a pleasant challenge for understanding of wood structure. Probably no other study on wood anatomy of dicotyledons has been based on such a high proportion of liquid-preserved samples. The usual assumption by wood anatomists is that little of value is lost when wood samples are prepared by drying. Even if this is true in many families, it clearly is not in certain others. 1 This study has been supported by grants from the National Science Foundation, GB 14092 and GB 38901, and the collection of materials by other National Science Foundation grants to Dr. Filer II. Raven. Mr. David Wheat prepared some of the sections and data used in this investigation. 'Claremont Graduate School and Rancho Santa Ana botanic Garden, Claremont. California 91711. \N\. MISSOURI BOT. GARD. 62: 386-424. 1975. 388 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VOL. 62 1972, before histological deterioration occurred. Accession numbers of these Fuchsia plants at the Botanical Garden are indicated in Table 1; no voucher specimens exist. A liquid-preserved wood sample of Zauschneria cana (voucher in RSA) was prepared from a shrub approximately eight years old at the Rancho Santa Ana Botanic Garden. A few collections could not be studied with respect to wood anatomy because grain of wood proved excessively twisted, because stems were too small, or because pickled material had dried. Most woods of Onagraceae are relatively soft. Because of this or small size, a few had to be embedded in paraffin and sectioned on a rotary microtome. The vast majority, however, were sectioned on a sliding microtome; these sections range between 18 and 26/x in thickness. In each collection, I selected the largest stems in order to present the most mature wood pattern. However, wood of relatively small stems in annuals and biennials can be expected to be different from that of a tree, such as Hauija. Changes during ontogeny were noted, as in the rays of Hauya (Figs. 8-10). Some sections were stained with safranin only. However, counterstaining with haematoxylin or Fast Green proved valuable for improved visibility of phloem strands and associated thin-walled parenchyma. Sections counterstained with Fast Green tend to show differential staining of gelatinous fibers: the outer portions of secondary walls stain red because of lignification, whereas the inner non- lignified portions stain green. This can be seen clearly in Fig. 33. Polarizing apparatus was used during examination of wood sections to detect presence of crystals and starch. Some photographs were made under polarized light employing various degrees of crossing of the nicol elements. Non-polarized light was used for photographs unless otherwise stated. In the photographic figures, wood transections are oriented with outer (toward cambium) portion of wood upward unless otherwise indicated. If only one collection of a species or infraspecific entity was studied, the collection is not mentioned in the figure legend, but is cited in Table 1. Where more than one collection of an entity was studied, the photographed section is identified by- collection number in the figure legend. Authors of binomials are cited in Table 1, and not used elsewhere in this paper. Tabular Data.—Table 1 lists species according to tribes. These tribes and their generic content agree basically with the scheme of Raven (1964). However, because of its distinctive wood features, I have listed Hauya within the tribe Hauyeae. as did Munz (1965) and Kurabayashi, Lewis & Raven (1962). Raven ( 1969) may well be correct in his reasons for including Hauya within Onagreae. I have isolated Hauyeae and placed it at the end of Table 1 for convenience in comparing wood features; this placement does not represent a taxonomic or phylogenetic judgment. Ludwigia is used in the sense of Raven (1962, 1963). Calylophus and Camissonia are employed in agreement with Raven's (1964, 1969) concepts. Gongylocarpus includes Burragea, as in Carlquist & Raven (1966). Because the Carlquist and Raven paper incorporated photographs, only tabular data on Gongylocarpus is included in the present paper. Treatment of the tribe Lopezieae 197.5] CARLQUIST—WOOD ANATOMY OF ONAGRACEAE 387 The nature of cells related to photosynthate conduction in wood has been poorly appreciated, yet Onagraceae proves a key group in comprehending this phenomenon. Only recently have beginnings been made, as the works by Braun (1970) and Wolkinger (1969. 1970. 1971) demonstrate. I have attempted to integrate concepts of photosynthate translocation and storage into a hypothesis of xylem evolution (Carlquist, 1975) that stresses the preliminary and tentative nature of our knowledge. However, Onagraceae are a group of exceptional interest with respect to wood anatomy for other reasons as well. Growth forms in this family range from small annual herbs to large annual and biennial herbs; from subshrubs to large shrubs: and even to medium-sized trees (Hauya, Fuchsia). A family with this range of growth forms and with a high proportion of herbs or woody herbs deserves special attention because our knowledge of characteristics of wood of herbs and herb-like plants is still quite inadequate. We do not know whether wood anatomy can be decisive in discerning direction of phylesis from woody to herbaceous or the reverse. Onagraceae is obviously a strategic family in this regard. The question of whether Onagraceae as a whole are primitively woody or herbaceous has not been answered, nor do we have any well-supported concepts of which tribes of the family represent phylesis to or from woodiness or herbaceousness. In addition, only a small proportion of woods in the family have been studied by wood anatomists, as the account of Metcalfe & Chalk (1950) shows. This lack derives from the fact that, most frequently, wood of tree species has formed the basis for wood collections and these collections in turn, formed the basis for studies by wood anatomists. Obviously we cannot fully understand the nature of wood anatomy in tree species without broadly-based comparisons with wood of non-arboreal families, genera and species. MATERIALS AND METHODS The liquid-preserved collection of wood samples prepared by
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