Allertonia 17, 2018, pp. 1–52

Wood Anatomy of and Allies: Strategies of Evolution in Basal Angiosperms Sherwin Carlquist1

Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105

ABSTRACT Atherospermataceae and Gomortegaceae, a clade of , occur in moist, swampy, riverine, and cloud forest habitats. They have apparently departed little in habitat preference from their ancestors, in the cloud forests of Gondwana, whereas Siparunaceae, a clade not far distant from (or sister to) the Atherospermataceae clade have radiated into more diverse habitats in South and Central America. Key features of wood anatomy are related to habitat occupancy shifts rather than to systematics. Narrow thin-walled vessels with scalariform perforation plates denote slow flow rates under low tension. Scalariform perforation plates may sieve out bubbles, as Zimmermann hypothesized, or they may compartmentalize the vessel for increased safety. Longer vessel elements lower flow resistance. All of Atherospermataceae and Gomortegaceae have perforation plate dimorphism; narrower perforations in latewood plates promote conductive safety, whereas non-resistive plates (in most of a growth ring) permit more flow. There is little deviation among Atherospermataceae in perforation plates and other features; the family has shifted very little away from cool moist forests since the breakup of Gondwana. Wider vessels in the of Dryadodaphne differ from the narrow vessels of the relatively small trees of , etc. There is diversification in tracheary elements. Tracheids, the basic type in some species of Atherospermataceae, offer conductive safety, but have been supplanted in other species by septate fiber-tracheids, which combine mechanical strength with photosynthate storage and serve as a cell type substituting for axial parenchyma, which is almost completely absent in the family. Where tracheids and septate fiber-tracheids co-occur, the fiber-tracheids tend to group near vessels, suggesting a mechanism for releasing sugars into vessels. Multiseriate rays consist mostly of procumbent ray cells suggesting radial flow of photosynthates, but lack sheath cells. Upright ray cells in wings of those rays, and throughout uniseriate rays, have scalariform vessel-ray pitting that suggests active transfer of sugar into vessels to maintain water columns. Ray-to-ray cell pits on horizontal and vertical radial walls are sparse by comparison, but tangential walls of ray cells bear numerous pits which are bordered. Oil cells occur idioblastically in upright ray cells of some species, and resin-like deposits were seen idioblastically in rays of all species. Microcrystals of unknown composition occur in several species. Wood of differs from that of Atherospermataceae in abundance of axial parenchyma, potentially better than fiber-tracheids because of denser pitting. Siparunaceae are a model of how an angiosperm group departs from mesic habitats like cloud forests into areas where temperature and humidity fluctuate more markedly. In , perforations plates are scalariform to simple or with a few thin bars (lowered resistance accommodates peak flow in warm but wet habitats), with conversion of wood background to axial parenchyma plus libriform fibers. This division of labor balances better mechanical support against lower conductive resistance. Vessel grouping in Siparunaceae provides redundancy and pathway maintenance to preserve conduction during peak transpiration. KEY WORDS AND PHRASES: Atherospermataceae, Gomortegaceae, Siparunaceae, ecological wood anatomy, flow in rays, septate fiber-tracheids, perforation plate dimorphism, pitting in rays, tracheids, vessel grouping

INTRODUCTION Hemisphere distribution of Gondwanic origin. Recent evidence has shown that Atherosper- One , Juss., is disjunct between mataceae (seven genera, 15 or more species) Chile and New Zealand. Atherospermataceae form a clade with Gomortegaceae (monotypic) occur in moist forest with such long-term as- in Laurales (Renner, 1999). This clade is of spe- sociates as Blume, Podocarpus cial interest because it represents a Southern L’Hérit. ex Pers., and Weinmannia L. Some of

1e-mail: [email protected] 2 ALLERTONIA Volume 17 these localities, although moist, may experience eny of the family. The wood of Atherospermata- frost to various degrees (, southeastern ceae does show a series of variations on a basic , southern Chile). There are fossil re- pattern. Some of those variations are smaller, cords of Atherospermataceae from Antarctica, some greater: atherosperm wood is not uniform, Patagonia, and even South Africa (see Renner but is not diversified in ways that one sees in et al., 2000). Thus, Atherospermataceae can some other families of considerable age (e.g., be said to have become geographically more Dilleniaceae). A rather detailed description of restricted as parts of the Gondwana fragments wood of the family as a whole can be devised, became colder, but expansion into the uplands and is offered below. The main concern of this of some subtropical locations (, essay, however, is the causation of differences New Guinea) has also occurred. Can Atheros- in wood anatomy among the taxa. Are climatic permataceae have reached some of their present differences matched with divergences in wood localities by long distance dispersal? Renner et anatomy in an arboreal group with mesic re- al. (2000) entertained this possibility, although quirements? What anatomical range is to be ex- Schodde (1969) thought otherwise. Atheros- pected within a plesiomorphy-rich (“primitive”) permataceae have bristly achenes that do travel group of ? Do primitive wood features by wind well within continental areas, and may limit the ecological diversification of a clade, have permitted some travel between separating or do radiations of some clades forestall the continental fragments. The habitats of the spe- radiation of others? How do clades with meso- cies, in riverine, marshy or gully habitats, are morphic woods “escape” (in terms of change in disjunct like those of Salix, which also has hairy anatomical features) into apomorphies suited to (comose) seeds. The achenes of Atherosper- climates with greater ranges of temperature, soil mataceae, however, may not be able to survive moisture, and humidity? Can some accommoda- long aerial transport or immersion in seawater tions to seasonality be achieved by ontogenetic (Schodde, 1969). changes (e.g., growth rings)? Origin of Atherospermataceae as a family The summary of Metcalfe (1987) for wood may date from as little as 85 MYA (fossil evi- anatomy of includes Atherosper- dence from Poole and Francis, 1999) to as much mataceae and Siparunaceae. It is based largely as 140 MYA (fossil pollen, which is distinc- on the work of Garratt (1934), Patel (1973), tively disulcate: Erdtman, 1952). Interestingly, Meylan and Butterfield (1978), and Foreman if one hypothesizes no dispersal across oceanic (1984). The work of Stern (1955) and Stern and distances, one must assign a minimal age of Greene (1958) are sources for data on wood of 220–244 MYA (Renner et al., 2000)—an exces- Gomortegaceae. The present account attempts sively ancient period of time, judging by floristic to add new information in the following ways: evidence. Fringing archipelagos and stepping- 1. All of the genera of Atherospermataceae stone islands (e.g., portions of the continent and Gomortegaceae have dimorphic (or Zealandia, now mostly underwater) are omitted sometimes possibly polymorphic) perforation as possibilities in that scenario. The occurrences plates. The adaptive significance of perfora- of such ancient genera as Lactoris Philippi and tion plates with axially wide perforations in Drimys J. R. Forst. & G. Forst. on the Juan Fer- most of a growth ring as compared to axi- nandez Islands shows us that some “primitive” ally narrow perforation plates in latewood is groups have crossed seawater to oceanic islands documented and related to wood ecology and of intermediate distance from continental sites physiology. of origin. The present study does not propose to com- 2. The occurrence of axial elements of the pare wood anatomy to systematics in detail, woods—septate fiber-tracheids, tracheids, because wood is only one element in the phylog- and axial parenchyma strands, is studied here 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 3

because the relative proportions of these el- tomical features are related to entrance by ements in woods of Atherospermataceae, some monimioid genera—as well as by other Gomortegaceae, and Siparunaceae prove to clades of angiosperms—into more stressful differ among the species studied. The evolu- habitats than those occupied by the constantly tionary significance of shifts at genus and spe- cool and moist habitats that characterize most cies levels is examined. Atherospermataceae and Gomortegaceae. 3. In angiosperm woods at large, vessels are mostly solitary in woods of mesic places. If MATERIALS AND METHODS tracheids are the imperforate tracheary ele- The contents of Atherospermataceae at pre- ment type, vessels do not group appreciably, sent appear to be: Lab. (one spe- even if a species occurs in a xeric habitat cies, Tasmania to Queensland); Daphnandra (Carlquist, 1984). Atherospermataceae are a Benth. (six species, ); Dory- group that represents degrees of this phenom- phora Endl. (two species, New South Wales and enon, albeit at the mesic end of the spectrum. Queensland); Dryadodaphne S. Moore (four What does this tell us about vessel grouping species, New Guinea and Queensland); Lau- in woods at large? relia (two species, Chile and New Zealand); Schodde (one species, Chile); and 4. Living cells of wood provide the machinery Nemuaron Baill. (one species, New Caledonia). for photosynthate storage and control of flow Laurelia aromatica Juss. ex Poir. is a synonym in vessels and tracheids. Atherospermataceae of L. sempervirens Tul. Laureliopsis is shown in are an excellent group for showing how the one of Renner (1999) to be nested within density, size, and bordered nature of pits on Laurelia, but with relatively weak support. Ren- ray cell walls and axial parenchyma cell walls ner (1999) does recognize the genus, however. suggest and validate structure-function hy- The following collections were studied, with potheses about living cells in wood. The na- repository in parentheses: ture of pitting can be analyzed independently of cell contents in this regard. Knowledge of Atherospermataceae contents is important, but the nature of the pit- Atherosperma moschata Labill. (MADw ting is a key to how those contents are stored 33829). or flow from cell to cell. Daphnandra micrantha (Tul.) Benth. (KYOw 5. The occurrence of microcrystals in living 3663); D. tenuipes Perkins (Thorne 21503 wood cells of Atherospermataceae is newly RSA). reported and is documented with scanning aromatica F. M. Bailey (USw electron microscopy (SEM). 7226); D. sassafras Endl. (Forestry Commis- sion N.S.W.) 6. In the phylogenetic trees of Laurales of- Dryadodaphne crassa Schodde ex Philipson fered by Renner (1999) and Stevens (2001 on- (MADw 29452); D. novoguineensis (Perkins) wards), Atherospermataceae form a clade to A. C. which Siparunaceae may or may not belong, Smith (MADw 28775); D. trachyphloia although Siparunaceae are certainly close to Schodde (MADw 29452). Atherospermataceae. In Siparunaceae, as well Laurelia novae-zelandiae A. Cunn. (MADw as in Monimiaceae, the ecological range of 5168; MADw 21319); L. sempervirens Ruiz & habitats occupied is greater than in Atheros- Pav.) Tul. (MADw 36623). permataceae and Gomortegaceae. The more Laureliopsis philippiana (Looser) Schodde seasonal (warmer, more humid) habitats of (MADw 52686). some Siparunaceae and Monimiaceae show Nemuaron vieillardii Baill. (McPherson 4726 us how character states in some wood ana- MO). 4 ALLERTONIA Volume 17

Gomortegaceae of Jeffrey’s fluid (Johansen, 1940), stained with Gomortega keule (Molina) I. M. Johnston safranin, and mounted in Canada balsam. (Yw 39370) Lengths of vessel elements, perforation plates, imperforate tracheary elements, and rays as Siparunaceae well as diameters of vessels may vary according Siparuna obovata A. DC. (Krukoff 6876 NY); to age of stem. The dimensions of these struc- S. rimbachii Standl. (UCw 1534). tures tend to increase in diameter. Quantitative The specimens studied were all portions of data on these and other cellular aspects of wood mature trees except for Daphnandra tenuipes, anatomy may be of interest within wide param- which was derived from a three-year-old stem. eters, but precise data and statistical treatments The specimens for Atherospermataceae repre- that include standard deviation are doubtfully sent all of the genera and about as complete a significant. Tracheary element length and ray sampling of the species as can be derived from length change ontogenetically (Bailey and Tup- major xylaria. The single specimen of Gomorte- per, 1918), and the ages and portions repre- ga keule is from a tree specimen. The genus sented by xylarium specimens are almost never Siparuna Aubl. is a relatively large genus of per- recorded. Variation within a cell population is haps 70 species and contains trees and shrubs often pronounced. Some variation in quantita- widely distributed in neotropical areas (Mexico tive data among various authors with respect to to Amazonian Peru and Brazil). The two speci- wood features of Atherospermataceae, as noted mens studied here are from mature trees. Sipa- by Metcalfe (1987) is therefore to be expected. runa is included to show apomorphies in the RESULTS atherosperm clade and thereby the anatomical correlations with occupancy of seasonally more FAMILIAL WOOD DESCRIPTION OF diverse habitats. ATHEROSPERMATACEAE Wood samples were boiled in water, stored in 50% aqueous ethanol, and sectioned on a sliding The fact that a coherent description of wood microtome. Sections for light microscope study anatomy of Atherospermataceae as a whole can were stained by means of Northen’s modification be assembled supports the idea that the family of Foster’s tannic acid-ferric chloride method is a natural one, as defined by Renner (1999) on (Johansen, 1940). Ferric tannate stains primary the basis of molecular studies. However, the co- walls deeply and thus permits identification of hesion of the genera also indicates a similarity septa in septate fiber-tracheids and pit mem- in ecology: all of the genera can be said to have branes in other cell types. Some sections of each mesic preferences (swamps, riverine margins collection were left unstained, washed in three and swamp margins, moist forest), habitats in changes of distilled water, and dried between which no truly dry season prevails. Seasonality clean glass slides under pressure, in to with respect to temperature is experienced by keep them flat. These sections were then sputter- Atherospermataceae, however. Frost certainly coated with gold and examined with an S2600N prevails in winter in some localities of the fam- Hitachi scanning electron microscope. SEM ily (Tasmania, southern Chile, southern New has various advantages in a wood anatomical Zealand, montane New South Wales). Thus, in study. Among these are determining accurately describing wood of Atherospermataceae, we are the nature of pits on ray cells and imperforate describing habitats as well as relationships. tracheary elements, the presence of pit borders, Growth rings are indistinct (Figures 1C, 5, details of perforation plates, and the presence 12). Latewood is brief, with vessels about 2/3 of microcrystals that have hitherto been over- the diameter of earlywood vessels (Figure 1C). looked with light microscopy. Portions of the Latewood vessels are mostly 30 to 60 µm, in di- stored wood samples were macerated by means ameter, and earlywood vessels are mostly 80 to 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 5

120 µm. One could say that earlywood occupies Imperforate tracheary elements are mostly the majority of a growth ring, because there is tracheids with circular pits (Figures 3F, G, 11C, no gradual diminution of vessel size leading into left, 12C, 13E, 19D, 20G). Pit borders are com- the formation of latewood. monly 5 to 8 µm. The tracheid walls are 4 to Vessel elements are angular (latewood, Figure 7 µm in thickness. Septate fiber-tracheids are 1C) to round in transverse section (earlywood, commonly 15–40% longer than vessel elements Figure 1C). Mean number of vessels per group, as in any given species. Septate fiber-tracheids seen in transverse sections is 1.05 to 1.96 (Figure have pit borders 1 to 5µm in diameter (Figure 17A) or even, in the Daphnandra twig, (Figure 6C). Pit details, especially pit borders, are best 6A) 2.12. The mean number of vessels per group seen in SEM images. is higher (above 1.50) in species with a higher Axial parenchyma is very scarce in the family. proportion of septate fiber-tracheids. Mean num- It was observed in only two species (Doryphora ber of vessels per mm2 is higher in twig material; aromatica, Nemuaron vieillardii), and it is very the density of vessels is roughly inversely propor- sparse in those species (Figure 21E, F). tional to vessel diameter. Vessel element length Multiseriate rays are more common than is mostly 1600–1800 µm, less in Laurelia and uniseriate rays. Multiseriate rays lack sheath Laureliopsis and in twig material. End walls are cells on the multiseriate portion and are 2 to highly oblique. Perforation plates are scalariform 5 cells wide (Figures 1B, 5B, 6B, 8B, 12B, exclusively, some with as many as 100 or more 13B, 17B, 20B, 21B), and may either have or bars (Figures 12A, 15A) but mostly with around lack uniseriate wings. The multiseriate portions 30–40 bars (Figures 3A, C–E, 13C), fewest of the multiseriate rays are composed wholly (15) in Laurelia sempervirens (Figure 19E–H) of procumbent cells (Figure 11D). Uniseriate and in twig material. The perforation plates are wings consist of 1 to 5 files of upright cells dimorphic, with thick bars and narrower perfora- as seen in tangential sections (Figures 14D, tions in latewood (Figures 1A–E, 8C, right, 12C, 18A). Uniseriate rays are composed wholly 15A, 19G, H). These plates are presumptively of upright cells, sometimes with a few square more resistant to flow. The majority of a growth cells. Upright cells predominate in wood of ring has perforation plates of a non-resistive type, rays of stems one to three years old (Figure with much more widely-spaced, thin bars (Fig- 6B). ures 3A, C–E, 8C, left, 12F, 13C, 16A, 19E, 20E). Tangential walls of procumbent ray cells Pit membrane remnants are extensive in a propor- may be vertically oriented (Figure 14E, F) or tion of perforation plates of Atherosperma mos- diagonally oriented (Figure 14A, G). Pitting on chata (Figure 2B–E), but are evident in a number tangential walls of procumbent ray cells fea- of the species as small portions of pit membranes tures large areas of pit membranes separated by in the lateral ends of perforations (Figures 3B, comparatively smaller areas of secondary wall 9C, 15D, 20F) and in perforations transitional (Figures 4F, 5F, 14E, F, 20H). Radial vertical to lateral wall pitting (Figures 3B, 15C). Upper walls of procumbent cell bear relatively few and lower termini of perforation plates are either pits (Figure 14A, B). Pits are relatively denser well-defined and distinct from the lateral-wall pit- on radial horizontal surfaces of procumbent ray ting (usually at overlapping vessel tips and where cells (Figures 4E, F, 8C, 14A, B). Upright ray vessels are grouped) or else transitional to the lat- cells bear scalariform pitting on radial facets eral wall pitting; both types were observed in all that contact vessels (Figures 4D, 11F, G, 14C, species. Vessel to ray pitting is scalariform (Fig- D). Pits are denser on tangential walls of upright ures 1F, 4D, 14C, D). Vessel to axial parenchyma cells than on horizontal radial walls (Figures pitting is scalariform to transitional (Figure 23E). 4C, 11A). Upright ray cell surfaces that contact Vessel to tracheid or to septate fiber-tracheid pit- imperforate tracheary elements bear pits that are ting is circular. circular and sparse. 6 ALLERTONIA Volume 17

Ray cell pits that have borders may be seen WOOD DESCRIPTIONS OF SPECIES on a number of the ray cell photographs. They STUDIED are perhaps clearest on light microscope photo- graphs (Figure 4C–F) but can be seen in SEM Atherosperma moschata (Figures 1–4) images also (Figures 20I). Those accustomed to Growth ring is indistinct (Figure 1A, near bot- identifying pit border in face view will need to tom). Vessels solitary or in small groupings, av- reorient themselves to visualizing pit borders in eraging 1.15 vessels per group. Vessel diameter sectional view. SEM study of the outer surfaces mostly between 70–80 µm in earlywood, mostly of tangential walls of procumbent ray cells is between 50–60 µm in latewood (Figure 1C, ar- also a way to reveal dense bordered pitting (Fig- row). Mean number of vessels per group, 1.22. ures 4B, 5F). Mean number of vessels per mm2, 270. Vessel Oil cells were observed to be present as idi- element length mostly between 900 and 1300 oblasts among upright ray cells in three species µm. Number of bars per perforation plate mostly (Dryadodaphne novoguineensis, D. trachy- 40–60, but occasionally more (Figures 2B–E, phloia, and Nemuaron vieillardii (Figure 22G). 3C–E). Perforation plates commonly with pit Such oil cells were reported by Metcalfe (1987) membrane remnants in the form of strands (Fig- for two additional species, Daphnandra micran- ure 2B) or laminar with pores (Figure 2D, E). tha and . Idioblasts con- Bars are mostly thin, but some latewood plates taining resin-like compounds were observed in have wide bars and axially narrow perforations rays. (about 3 µm axial width: Figure 2A, top); These Microcrystals, the size, morphology, and ar- are not to be confused with lateral wall pitting, rangement of which suggest they that they might which is scalariform-transitional and located in be different from ordinary calcium oxalate crys- overlapping vessel tips and on tangential ves- tals, were observed in ray cells of Daphnandra sel walls where a pair of vessels is in contact micrantha (Figure 5G), Doryphora aromatica, (Figure 2F). Vessel to upright ray cell pitting is and Nemuaron vieillardii (Figure 22E–G). These scalariform as seen from inside a vessel (Figure crystals resolve well only with SEM imaging, 2F). Perforation plates grade into lateral wall and are likely to be found in other species of the pits on some perforation plates (Figure 3B, 3D, family. They also occur (as do oil idioblasts) in top), but other perforation plates are clearly de- the bark of Nemuaron vieillardii (Figure 22D). limited at their tops or bottoms (Figure 3A, C, Tyloses, formed from the invasion of vessels E). Forking bars are one (Figure 3A, C) to sev- by protoplasts of septate fiber-tracheids, oc- eral (Figure 3D, E) per plate. cur in the vessels of several species, and were Imperforate tracheary elements are mostly notably abundant in one collection of Laurelia tracheids. These have pits about 8 µm in diame- novae-zelandiae (Figure 19B–F). ter (Figure 3G). Septate fiber-tracheids comprise Starch grain remnants were observed in sep- 20% of the imperforate tracheary elements tate fiber-tracheids in the twigs of Daphnandra and are chiefly adjacent to vessels (Figure 1E). tenuipes, which probably dried more rapidly Pits of the septate fiber-tracheids are about 5 µm following collection than did the samples from in diameter (Figure 3F). large stems of the other species. Starch grains Multiseriate rays are 2–3 cells wide at their tend to vanish relatively rapidly as a result of widest point and either have or lack uniseriate bacterial action if wood samples are dried slow- wings (Figure 1B). The multiseriate portions of ly. The slowness of drying is evident in the pres- multiseriate rays are composed of procumbent ence of fungal hyphae in a number of the SEM cells. Uniseriate rays are mostly 2–6 cells tall images presented here. and are composed of upright cells (Figure 1B). 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 7

Tangential walls of upright ray cells are relative- riate wings, multiseriate rays are composed of ly densely pitted (Figure 4A, C), although the procumbent cells. Uniseriate rays and uniseriate tangential walls of procumbent cells are larger wings of multiseriate rays are composed of up- and denser (Figure 4B). The wall shown in right cells. Tangential walls of procumbent cells Figure 4B would probably have revealed more bear densely-placed bordered pits (Figure 5F). numerous pits had the plane of section been Bordered pits are often present on other ray cell slightly different. Radial walls of the upright facets. Upright cells facing vessels have scalari- cells have scalariform pits on ray cell to vessel form pitting. Microcrystals were observed in ray element interfaces, but a small number of circu- cells (Figure 5G). lar pits on ray cell to tracheid interfaces (Figure 4D). The majority of these pits are bordered, Daphnandra tenuipes (Figure 6, 7) although some of the borders are conspicuous Although only a twig of this species was (Figure 4C, E, F, vertical walls), whereas others available, the wood of it provided interesting are inconspicuously bordered or non-bordered hints about how wood anatomy of a smaller (Figure 4C, E, F, horizontal walls). A few cells stem is related to ontogeny and hydraulics. Pres- of the rays contain resin-like deposits (Figure ence of growth rings is evidenced by a decrease 4E, F), distributed idioblastically. in vessel diameter for a few cell layers (Figure The apparent pit membranes in Figure 2C 6A, top). Vessels are commonly grouped (Fig- are probably an instance of tylosis walls, which ure 6A), often in radial rows. Only a few ves- are non-porose, overlying a scalariform per- sels are solitary, and the mean number of vessels foration plate. Examples of this are illustrated per group is 2.12 (the greatest degree of vessel more extensively in Figure 18 for Laurelia grouping in the Atherospermataceae studied). novae-zelandiae. Vessel diameter is mostly between 30 and 50 µm (Figure 6A). Mean number of vessels per mm2 Daphnandra micrantha (Figure 5) of transverse section is 496. The mean number Growth rings are inconspicuous. Vessels are of bars per perforation plate is about 50 (Figure mostly solitary, mean  1.29 vessels per group 7A–C). Bars are narrowly bordered (Figures 6F, (Figure 5A). Radial vessel diameter of vessels as 7D). Perforations in most of the plates are about seen in transverse sections is commonly 40–80 7 µm in axial width, and the lateral ends of the µm, mean  65 µm. The mean number of ves- perforations are rounded rather than acute (Fig- sels per mm2 is 159. The mean vessel element ure 6D). Some dimorphism in perforation plates length is 1320 µn. Perforation plates are dimor- is evident (Figure 7B: plate with wider perfo- phic (Figure 5C); the thick-barred perforation rations above, plate with narrower perforations plates are found in latewood. Vessel to vessel below). Pit membrane remnants in perforations pitting is scalariform and occurs on tangential are mostly absent (some probable remnants in walls where a pair of vessels is in contact (Fig- a plate, Figure 7B, below). Some perforations ure 5D) and is distinguishable from the latewood grade into lateral wall pitting (Figure 7A, C) scalariform perforation plates, which occur on but some plates are well defined at axial ends radial walls of vessels. The mean number of bars (Figure 7B). Lateral wall pitting is commonly per perforation plate is 37. evident on the tangential walls of vessels (Fig- Imperforate tracheary elements are all (or ure 6B) because the high degree of radial vessel nearly all) septate fiber-tracheids (Figure 5E). grouping results in many intervascular contacts. Pit borders are 2 µm in diameter. Septate fiber- Imperforate tracheary elements are almost all tracheids are mostly 1400 to 1700 µm in length. septate fiber-tracheids (Figure 6C; 6D, arrows). Multiseriate rays are 2–5 cells wide at the Pit borders on septate fiber-tracheids are 1–5 µm widest point (Figure 5B). Except for the unise- in diameter (Figures 6C, 7D, bottom). A very 8 ALLERTONIA Volume 17 small number of tracheids are present. Tracheid lous bar pattern is shown in Figure 9B. Perfora- wall thickness is mostly 3 µm. Length of septate tion plates grade into lateral wall pitting in some fiber-tracheids is mostly 550–960 µm. plates (Figure 10C, D), but are more commonly Ray cells are all upright to square (Figure 6B, clearly defined at upper and lower ends (Figures E). Rays are uniseriate and biseriate; no wider 9A, 10A). Lateral wall pitting is scalariform, and multiseriate rays are present because of the ju- is best seen in face view in tangential sections venile nature of the material. Axial parenchyma (Figure 10E, F). Pit membrane holes (Figure is apparently lacking. Idioblastic cells contain- 10A) may be a result of aging or handling rather ing resin-like deposits are present in rays (Figure than a characteristic feature. 7F). Imperforate tracheary elements (Figure 11A– In radial sections that include pith (Figure C) are mostly tracheids and are about 2000 µm 6E, F), no imperforate tracheary elements were long. Their pits have borders about 8–9 µm in di- observed, but some may be present and would ameter. The diameter of the tracheids is about 30 be helical elements that have no pits within µm (Figure 8A). The walls are about 5.5 µm in the primary walls, which are poorly shown in thickness. About 10% of the imperforate trache- the preparation. The helical thickenings in late ary elements are septate fiber-tracheids (Figure protoxylem/early metaxylem elements are nu- 11B) with pits about 5 µm in diameter (Figure merous and occur in many elements (Figure 11A). One axial parenchyma strand (Figure 6E), but no “transitional” pitting was observed 11C) was observed. in tracheary elements distal to the helical ones. Vascular rays are multiseriate and up to 5 cells Instead, helical elements are followed by scalar- wide at their widest point (Figure 8B), or unise- iformly pitted ones. Some slight widenings be- riate rays. The multiseriate portion of multiseri- tween the helices may indicate conductive zones ate rays is composed of markedly elongate cells. in the primary wall (Figure 6F). Tips of multiseriate rays are composed of radially shorter procumbent cells (Figure 11D, top). Uni- Doryphora aromatica (Figures 8–11) seriate rays are composed of upright cells only. Growth rings are almost imperceptible, but are Tangential walls of ray cells are more densely indicated by a few markedly narrow vessels (Fig- pitted than the horizontal walls (Figure 11F). Up- ure 8A). The mean number of vessels per group right ray cell pitting facing vessels can be subdi- is 1.08. Vessels are commonly 50 to 123 µm in vided, sometimes intricately (Figure 11G). diameter; the mean is 91 µm. The vessel wall Microcrystals, like those illustrated for thickness is 2–3 µm (Figure 8A). Most vessel el- Nemuaron (Figure 22) occur in ray cells of D. ements are between 1200 and 1700 µm in length. aromatica. Perforation plates commonly have 30–35 bars. The plates are dimorphic (Figure 8C, compare Doryphora sassafras (Figure 12) wide perforation plate at left with the two narrow Growth rings are almost imperceptible (Fig- perforation plates at right). Wider perforations ure 12A, latewood at top). Vessels are mostly are about 8 µm in axial width, and the narrower solitary (Figure 12A). The mean number of perforations are about 3 µm in axial width. Bars vessels per group is 1.05. The mean number of are narrowly bordered in the plates with wider vessels per mm2 is 913. Vessel elements average perforations. Perforation plates are typically on about 1700 µm length. The number of bars per radial facets of vessel elements (Figures 9A–G; perforation plate is mostly between 30 and 45 10A–D). Latewood perforation plates have thick (Figures 12C–E). Perforation plates are dimor- bars (Figures 9A, C–E; 10D). Earlywood plates phic. The more resistant latewood plates have (which occur in the vast majority of a growth perforations that are about 3 µm wide axially ring) have thinner bars (Figures 9F, G; 10A–C). (Figure 12D). A plate with even narrower per- An aberrant perforation plate with an anoma- forations, which could be confused with lateral 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 9 wall pitting, is shown in Figure 12C. Less re- seriate rays, and are 2–5 cells wide at their wid- sistant plates, present in most of a growth ring est point (Figure 13B). Procumbent ray cells are (Figure 12E) have perforation plates about 8 µm markedly elongate (Figure 14A). Pits are sparser in axial width. on horizontal radial ray cell walls than on tan- Imperforate tracheary elements are chiefly gential walls (Figure 14E). Pit membrane areas tracheids about 1900 µm in length and with on tangential walls are large, with intervening bordered pits about 7–8 µm in diameter. Fewer wall areas proportionately restricted (Figure than 10% of the imperforate tracheary elements 14E–G). Minute borders are often present on ray are septate fiber-tracheids; they have circular cell walls (Figure 14E–G). Tangential walls of bordered pits about 5 µm in diameter (Figure procumbent ray cells are often diagonal (Figure 12F). As seen in transverse section, tracheids are 14E, G). Sheath cells are absent on the multise- about 32 µm in diameter and have walls about 5 riate portions of multiseriate rays. Deep-staining µm in thickness. These occur near vessels. No resin-like deposits present idioblastically in ray axial parenchyma was observed. cells (Figure 14G). Multiseriate rays may lack wings or have wings of 1–3 cell files (Figure 12B). The mul- Dryadodaphne novoguineensis (Figures 15, tiseriate portions of multiseriate rays are com- 16) posed of procumbent cells; no sheath cells are Growth rings are minimally defined. Vessels present (Figure 12B, E). Multiseriate rays av- are solitary or in pairs or small grouping. The erage about 1300 µm in height. Microcrystals mean number of vessels per group is 1.62. Ves- were observed in ray cells. sel diameter lies mostly between 80–160 µm, the mean  132 µm. The mean number of ves- Dryadodaphne crassa (Figures 13, 14) sels per mm2 is 1708 µm. The number of bars per Growth rings are present, but latewood is perforation plates is 47 (Figure 15B), but may minimal. Vessels are mostly solitary; the mean range to more than 100 (Figure 15A). Perfora- number of vessels per group is 1.17 (Figure 13A, tion plates are dimorphic. The latewood plates D). The mean vessel diameter is 94 µm (Figure have wider bars and pits about 3 µm in axial 13A, D). The mean number of vessels per mm2 width (Figure 15B). The remaining perforation is 75. The mean vessel element length is 1805 plates have perforations about 9 µm in axial µm. The average number of bars per perforation width (Figure 15B). Pit membrane remnants are plate is 56. Perforation plates are dimorphic, present at lateral ends of the perforations in the latewood plates with wider bordered bars, some plates (Figure 15C, center to left; Figure the remaining plates with thin bars and narrow 15D, left). Lateral wall pitting is scalariform, border (Figure 13C). Perforations of latewood with only a few transitional pits (Figure 16B). plates are 4–5 µm wide axially, perforations in Imperforate tracheary elements are all septate the rest of the wood are 7–8 µm wide axially fiber-tracheids (borders on septate fiber-tracheid (Figure 13C). Vessel walls are very thin (Figure pits are about 5 µm in diameter (Figure 16C). No 13D), 1–2 µm in thickness. axial parenchyma was observed. Imperforate tracheary elements are mostly Ray histology is like that in D. crassa. Oil idi- tracheids (Figure 13D), with pit border about 8 oblasts occur among the upright ray cells (Fig- µm in diameter. About 10% of the imperforate ure 16D). tracheary elements are septate fiber-tracheids. These are located adjacent to vessels (Figure Dryadodaphne trachyphloia 13C, arrows). Borders of septate fiber-tracheids Growth rings are almost imperceptible. Ves- are circular, about 5 µm in diameter. No axial sels are solitary or in small groups; the mean parenchyma stands were seen. number of vessels per group is 1.60. Vessel di- Multiseriate rays are more common than uni- ameter ranges from about 60 µm (latewood) to 10 ALLERTONIA Volume 17

120 µm (remainder of growth ring); most vessels sent in lateral ends of perforations (Figure 17F). are about 100 µm in diameter. The mean number Axial tips of peroration plates are well defined vessels per mm2 is 115. The mean vessel ele- (Figure 17C, top) or with transitions into lateral ment length is 1864 µm. The number of bars per wall pitting (Figure 17C, bottom). Intervascular perforation is mostly near 40, but ranges from wall pitting of vessels occurs on tangential fac- 30 to 60 or more. Perforation plates are dimor- ets and is scalariform (Figure 17E). phic. Latewood plates have perforations about 3 Imperforate tracheary elements are nearly µm wide axially, whereas perforations in the re- all septate fiber-tracheids (Figures 17D, right; mainder of the wood are about 6 µm wide axial- 17G). The mean length of septate fiber-tracheids ly. Vessel wall thickness is 2–3 µm. Lateral wall was estimated to be about 2050 µm. The mean pitting of vessels is scalariform, and is mostly on diameter of septate fiber-tracheids at their wid- tangential walls of vessels. est point is about 32–50 µm; mean wall thick- Imperforate tracheary elements are apparent- ness is about 4µm. Pit borders are about 5 µm ly all septate fiber-tracheids. The mean septate in diameter. No axial parenchyma was observed. fiber-tracheid length is 2390 µm. Septate fiber- Multiseriate rays are at least twice as common tracheid diameter is about 25–32 µm at their as uniseriate rays (Figure 17B). Multiseriate widest point; their walls are about 5 µm in thick- rays often have uniseriate wings. The uniseri- ness. The diameter of pit borders is about 5 µm. ate wings as well as the cells of uniseriate rays The length of the pit apertures exceeds the di- are composed of square to upright cells. No ax- ameter of the pit borders. No axial parenchyma ial parenchyma is present. Multiseriate rays are strands were observed. mostly two cells wide, but some rays are three Rays are like those of the other two species of cells wide at their widest point (Figure 17B). Dryadodaphne with respect to histology, pitting, and dimensions. Resin-like deposits occur idio- Laurelia novae-zelandiae (MADw 21319; blastically throughout the rays. Oil cells occur Figure 18) idioblastically in upright ray cells. Some tyloses This collection has abundant tyloses formed were observed in vessels. by invasion of vessels by the protoplasts of sep- tate fiber-tracheids or possibly ray cells adjacent Laurelia novae-zelandiae (MADw 5168; to the vessels. Tyloses may appear as transverse Figure 17) walls crossing vessels (Figure 18A, E). Tyloses Growth rings are present, not pronounced, are most evident where two tyloses touch, leav- but with latewood vessels appreciably narrower ing a triangular intercellular space between them (Figure 17A). Vessels are mostly solitary, but (Figure 18B). Tyloses may penetrate into vessel also in groups (Figure 17A); the mean number tips, where they form rounded outlines (Figure of vessels per group is 2.10. Mean vessel diam- 18C, bottom). eter at widest point is about 50 µm in latewood, At first glance, tyloses appressed to perfora- but 100–120 µm otherwise. The mean number of tion plates may appear to be pit membranes of vessels per mm2 is 92. The mean vessel element lateral wall pitting or pit membrane remnants in length is 1630 µm. The number of bars per per- perforations (Figure 18D). However, separation foration plate is commonly around 40 (Figure between adjacent walls of vessels reveals that 17C, D). Perforation plates are dimorphic (com- these are not pit membranes of vessels sand- pare Figure 17C to 17D). The latewood perfora- wiched between two adjacent vessels, but are tion plates have axially narrower (about 5 µm) appressed to the inner surfaces of vessels. The perforations (Figure 17D, left). The perforation walls of tyloses lack pores (Figure 18B, F) that plates in other parts of each growth ring (Figure characterize pit membrane remnants (compare 17C, left) have perforations that are about 8 µm with true pit membrane remnants in Atheros- in axial width. Pit membrane remnants are ab- perma moschata, Figure 2). 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 11

Tyloses were so abundant and pervasive in this multiseriate rays are composed of procumbent collection of L. novae-zelandiae) that the sam- cells. ple studied did not sink after extended boiling. No tracheids were observed in MADw 21319. Laureliopsis philippiana (Figure 20) Axial parenchyma was not detected. Growth rings are inconspicuous, with late- wood brief. Vessels are appreciably narrower Laurelia sempervirens (Figure 19) in latewood (Figure 20A, bottom). Vessels are Growth rings are not pronounced, but are the mostly solitary (Figure 20A); the mean number most distinct observed in the Atherospermatace- of vessels per group is 1.21. The mean vessel ae studied. Latewood is composed of narrower diameter in latewood is about 30 µm; the diam- vessels interspersed among tracheids. Vessels eter elsewhere in growth rings is mostly 60–80 are mostly solitary; the mean number of vessels µm. The mean number of vessels per mm2 of per group is 1.10 (Figure 19A), the lowest ob- transverse section is 193. Vessel elements aver- served in Atherospermataceae. Vessel diameter age 952 µm in length. Perforation plates mostly ranges from about 40 µm in latewood (Figure have 30–50 bars (Figure 20C–E). Perforation 19H) to 60 µm (earlywood, Figure 19E). Mean plates in latewood have perforations about 3 number of vessels per mm2 is 94. Most vessel µm wide axially (Figure 20C center; 20D, left). elements are between 600 and 720 µm long, Wide (earlywood) perforations are about 5-6 which is rather short for Atherospermataceae. µm wide axially (Figure 20E). The bars in ear- The number of bars per perforation plate most- lywood plates are very narrowly bordered. Pit ly ranges between 12 and 35 (Figure 19E–H). membrane remnants occur in lateral ends of Perforations in latewood perforation plates are perforations (Figure 20F). Perforation plates ei- about 3 µm wide axially (Figure 19C, center; ther grade into lateral wall pitting at their upper 19E). Perforation plates are well defined at their or lower ends (Figure 20C, center; 20D) or are upper and lower ends; only a few have plates clearly delimited from lateral wall pitting (Fig- that grade into lateral wall pitting. Perforation ure 20E, top). plates are dimorphic or polymorphic (the range Imperforate tracheary elements are mostly is shown in Figure 19E–H). Wide (earlywood) tracheids (Figure 20C, lower right), with pits perforations are about 7 µm in axial width; late- 5–10 µm in diameter. Pit apertures are clearly in- wood perforations measure about 3 µm. Lateral cluded within the pit borders (Figure 20G). Less wall pitting on vessels is scalariform. Intervas- than 10% of the imperforate tracheary elements cular pitting is scarce because vessel grouping are septate (action of fungi may have reduced is so minimal. the number of septa in the specimen studied). Imperforate tracheary elements are almost all The mean length of imperforate tracheary ele- tracheids with large circular borders and aper- ments is 1285 µm. No axial parenchyma was tures included within the borders (Figure 19D). observed. A very small number of septate fiber-tracheids Multiseriate rays are more common than uni- is present (the grouping of three together in Fig- seriate rays (Figure 20B). Multiseriate rays at ure 19C is quite unusual). Imperforate tracheary their widest point are 2–3 (rarely 4) cells wide elements are mostly 34–37 µm in diameter, and (Figure 20B). The multiseriate portions of mul- their wall thickness is about 3 µm. Mean imper- tiseriate rays are composed of procumbent cells. forate tracheary element length is 976 µm. No Upright cells comprise the wings, or more com- axial parenchyma was observed. monly, the solitary file of tip cells at the upper Rays are mostly biseriate, rarely three cells and lower ends of the multiseriate rays. Multi- wide (Figure 19B). Multiseriate rays have a sin- seriate rays mostly measure between 190 and gle tip cell, or less commonly, uniseriate wings 400 µm tall. Tangential walls of procumbent (Figure 19B). Multiseriate (biseriate) portions of cells have prominent pits (Figure 20H, arrow). 12 ALLERTONIA Volume 17

Uniseriate rays are composed of upright cells. small size and limited depth of focus. This may Tangential walls of the upright cells have clearly account for omission of this feature in previous bordered pits as seen in sectional view (Figure descriptions of wood in the family. By means 20I). of SEM, these crystals resolve well (Figure 22 E–G) and prove to be much smaller than raphi- Nemuaron vieillardii (Figures 21, 22) des. They are not organized into packets the way Growth rings are very weakly demarcated that raphides are, and appear to be randomly (Figure 21A). Vessels are mostly solitary; the scattered within the cells in which they occur. mean number of vessels per group is 1.26. Vessel Although somewhat varied in size, all of the mi- diameter as seen in transverse sections is mostly crocrystals have tapered ends. Observation with close to 50 µm, and ranges from 35 to 100 µm. polarized light showed that the microcrystals The mean number of vessels per mm2 is 140. are birefringent. In rays, the microcrystals oc- Vessel element length ranges from 1050 to 1420 cur both in upright (Figure 22E) and in procum- µm, and is mostly about 1200 µm. The number bent (Figure 22F, C) cells. They vary in size, as of bars per perforation plate is commonly 60 to shown in Figure 22F. 100 (Figure 21C). Perforation plates are dimor- phic (compare Figure 21D, left, with 21D, right. GOMORTEGACEAE The latewood perforation plates have perfora- Wood of Gomortegaceae was carefully stud- tions about 3 µm, whereas perforations in the re- ied by Stern (1955) and Stern and Greene (1958), mainder of the vessels in growth rings are about and their observations have been summarized by 5 µm in axial width. Perforation plates mostly Metcalfe (1987). Conclusions in these sources transition into scalariform lateral wall pitting at were offered prior to the development of global the upper and lower ends of the plate. Vessel to molecular phylogenies of angiosperms. Today, upright cell pitting is scalariform (Figure 22A). Gomortegaceae are regarded as a sister family Axial parenchyma strands (Figure 22E, F) are to Atherospermataceae by many workers (e.g., few and sparse, comprising 5% or less of the Soltis et. al., 2005). The number of wood char- wood volume. Axial parenchyma to vessel ele- acteristics shared by the two families is consid- ment pitting is scalariform (Figure 21E, F). Pits erable, and includes presence of tracheids and a on lateral and cross walls of the strand bordered low number of vessels per group, a feature asso- (Figure 22E). ciated with tracheid presence (Carlquist, 1984). Rays are mostly multiseriate and wide, four to Perforation plates are scalariform (Figure five cells in thickness at the widest point (Figure 23C), typically with 13 to 15 bars. Because 22B). Uniseriate wings are composed of files of Atherospermataceae have dimorphic plates, I upright cells or only a single file of cells at the searched for radial sections of G. keule to see upper and lower tips of the rays. Sheath cells are whether “resistant” latewood plates occur in absent. Tangential walls of the procumbent cells this species. Stern (1955) and Stern and Greene of the multiseriate rays bear numerous bordered (1958) did not mention any dimorphism or poly- pits (Figure 22A, center). Tangential walls of the morphism in the perforation plates of Gomorte- upright cells of rays of uniseriate rays are dense- ga. I did observe small numbers of perforation ly pitted and have bordered pits (Figure 22B). plates with wide bars and narrow perforation Oil cells occur idioblastically among the up- plates. These plates occur in latewood, although right ray cells, as well as in the axial parenchy- latewood is minimal. Lateral wall pitting of ves- ma of bark phloem (Figure 22C, 22D, right oc). sels in Gomortega is scalariform, as in Atheros- Microcrystals are visible in large numbers in permataceae, and vessel to upright cell pits thus axial parenchyma of bark phloem (Figure 22D), characterize both families. but do not resolve well at high magnification The rays of Gomortega (Figure 23B, F, G) by means of light microscopy because of their are like those of Atherospermataceae in having 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 13 procumbent cells in the multiseriate portions of 1. Mostly few bars per perforation plate (or multiseriate rays (Figure 23B, G) and upright simple perforation plates) (Figure 24A, E). cells in the tips of multiseriate rays. Multiseri- More numerous bars have been reported in ate rays are shorter than those of Atherosper- S. bifidaA. DC. (Metcalfe, 1987) and S. the- mataceae. The multiseriate rays rarely exceed caphora A. DC. (Mark Olson, unpublished two cells in width and some of the procumbent data). cells contain dark-staining resin-like materials 2. Lateral wall pitting of vessel composed of in an idioblastic fashion (Figure 23B). Uniseri- alternate circular pits (Figure 24E). ate rays are present (Figure 23B, upper right), but less frequent than in Atherospermataceae. 3. Imperforate tracheary elements with sim- Tangential walls of both upright and procum- ple pits (some vestigial borders reported by bent ray cells (Figure 23F) bear numerous bor- Money et. al., 1950). dered pits. Oil cells were not observed in rays 4. Axial parenchyma common and grouped of Gomortega, but oil cells were observed in the into diffuse-in-aggregates or narrow bands bark (Figure 23H), although they differ from (Figure 24C). those of Atherospermataceae in their spherical shape. 5. Rays with numerous upright cells (Fig- Axial parenchyma is relatively common in ure 24B, D, F), indicative of protracted wood of Gomortega (Figure 23B, D, E). It is juvenilism. diffuse, and the cross-walls (the axial paren- The vessels of Siparuna are grouped (more so chyma strand is oriented horizontally in Figure in S. rimbachii, Figure 24A, than in S. obovata, 23H) are densely pitted. Figure 24C). The degree of grouping of ves- The characters by which wood of Gomortega sels is higher with increased conductive stress differs from that of Atherospermataceae may (Carlquist, 1984). In angiosperms with tracheids be regarded as autapomorphies in Gomortega. rather than fiber-tracheids or libriform fibers, de- Some of these features (smaller size of rays, gree of vessel grouping is minimal (below 1.5 more common nature of axial parenchyma, few- vessels per group), as indicated by Atherosper- er bars per perforation plate) can be considered ma moschata, Doryphora spp., Dryadodaphne differences of degree rather than presence-or-ab- crassa, Gomortega keule, Laurelia sempervi- sence differences. The wood of Atherospermata- rens, and Laureliopsis philippiana. ceae has tracheids, although they are uncommon In sum, these represent the successful shift of in those species in which septate fiber-tracheids the atherosperm clade from habitation of cool substitute for tracheids. Atherospermataceae is a mesic localities to radiation into zones with family in transition in this regard, although one warmer periods (and higher peak transpiration may conclude that change in relative frequency rates) and more mechanisms to prevent embo- of these types of imperforate tracheary elements lisms or reverse them. The simple perforation is easily achieved, since the species of Dryado- plates of most Siparunaceae permit greater con- daphne differ in this regard. Tracheids in Go- ductivity. Greater transpiration (in Siparuna mortegaceae are probably a plesiomorphy. caused by warmer temperatures) creates higher SIPARUNACEAE tensions, which makes the alternate pitting valu- able (in contrast with the mechanically weaker Molecular-based trees of Laurales (e.g., Solt- scalariform pitting on vessel walls in Atheros- is et al., 2005) show that Atherospermataceae, permataceae and Gomortegaceae). Grouping of Gomortegaceae, and Siparunaceae form a clade vessels provides redundancy that probably helps from which Siparunaceae branch early. Wood retain a functioning conductive pathway. Axial synapomorphies that help to define Siparunace- parenchyma functions in carbohydrate storage ae include: that osmotically maintains water columns. Pre- 14 ALLERTONIA Volume 17

Figure 1. Atherosperma moschata. Wood sections seen by light microscopy (A– E) and SEM (F). A. Transverse section; latewood about ¼ of the distance from the bottom. B. Tangential section. Uniseriate rays are somewhat less frequent than bi- seriate and triseriate rays. C. Transverse section; arrow points to a narrow latewood vessel. D. Radial section of multiseriate ray. Resin-like deposits in both upright and procumbent ray cells. E. Radial section. Arrows point to septa in septate fiber- tracheids; vessel at center. F. Inner surface of vessel from radial section, oriented horizontally; vessel-to-upright–ray-cell pitting shown. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 15

Figure 2. Atherosperma moschata. SEM micrographs of radial sections of vessel portions (A–E) and of lateral-wall pitting from a vessel, tangential section. A. Bars in two latewood perforation plates. B. Porose pit membrane remnants. C. Probable tylosis wall covering perforations. Some artifact formation and tearing are evident. D. Porose pit membrane remnants in earlywood; some artifact formation is evi- dent. E. Perforations from latewood; pit membranes are probably naturally porose. F. Intervascular lateral wall pitting: scalariform-transitional pattern. 16 ALLERTONIA Volume 17

Figure 3. Atheroperma moschata, SEM micrographs of radial sections, showing earlywood perforation plates (A–E) and tracheids (F–G). A. Shorter perforation plate with well-defined ends. B. End of perforation plate that transitions into later- al-wall pitting (right); some pit membrane remnants present. C–D. Medium-length perforation plates. C. Perforation plate well-defined at upper and tower ends. D. Perforation plat that transitions into lateral wall pitting at upper and lower ends. E. Variously forking bars. F. Linear arrangement of pits. G. Pit apertures included within pit borders. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 17

Figure 4. Atherosperma moschata, Pitting details of ray cells from tangential (A, B) and radial (C–F) sections; SEM (A, B, D) and light microscope (C, E, F) sections. A. Upright ray cell, pitting seen from upper surface. B. Pits on tangential wall of procumbent cell. C. Tangential wall of radial section (vertical wall); pits are bordered. D. Scalariform ray cell to vessel pitting; portions of two perforation plates below. E, F. Procumbent cells from a multiseriate ray. E. Idioblasts with resin-like contents; gray in other cells = starch remnants. F. Procumbent ray cell with dark-staining contents outlining bordered pits on tangential walls. 18 ALLERTONIA Volume 17

Figure 5. Daphnandra micrantha. Wood sections imaged with light microscopy (A, B, E) and SEM (C, D, F, G). A. Transverse section. Latewood is above mid- dle. B, Tangential section; rays are notably tall, wide. C. Radial section. Latewood perforation plate at left, earlywood plate at right. D. Tangential section. Intervas- cular lateral wall pitting on vessel. E. Radial section. Septate fiber-tracheids (two septa are indicated by arrows. F, G. Ray cells from tangential section. F. Pitting on procumbent ray cell, seen from outer surface. G. Microcrystals lining the interior of a ray cell. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 19

Figure 6. Daphnandra tenuipes. Light microscope photographs (A, B, D) and SEM images (C, E, F) of wood sections. A. Transverse section; radial groupings and chains of vessels are evident. B. Tangential section; rays are uniseriate or bi- seriate. Arrows indicate lateral wall pitting on vessels. C. Outside surfaces of sep- tate fiber-tracheids, from radial section. D. Radial section, perforation plate at left, septate fiber-tracheids at right (arrows point to septa). E, F. Radial sections of pri- mary xylem. E. Sequence from loose helices to scalariform. F. Tight helices and a helical-to-scalariform transitional element. 20 ALLERTONIA Volume 17

Figure 7. Daphnandra tenuipes, SEM (A–E) and light microscope images (F) of radial sections. A. Radial chain of vessels. B. Perforation plate with wide perfora- tions (above) and plate with narrow openings (below) with some pit membrane remnants. C. Two perforation plates, showing transitions to lateral wall pitting at ends of plates. D. Portion of a perforation plate, showing bordered bars and round- ed lateral ends of perforations. E. Ray composed of upright and square cells (up- right ray cells are oriented horizontally in this SEM image). F. Idioblasts contain resin-like compounds, Orientation as in E. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 21

Figure 8. Doryphora aromatica. Light microscope (A, B) and SEM images of wood. A. Transverse section; latewood above, arrow points to a narrow vessel). B. Tangential section; rays mostly do not have uniseriate wings. C. Radial section. Procumbent cells of a multiseriate ray, below; above, an earlywood perforation plate (at left), and, at right, two latewood perforation plates. 22 ALLERTONIA Volume 17

Figure 9. Doryphora aromatica. Radial sections imaged with light microscopy (A, B), and SEM (C–G). A. Latewood perforation plate. B, Anomalous perforation plate with intermixed wide and narrow bars. C. Portion of latewood perforation plate, showing pit membrane remnant at lateral ends of perforations. D, Bordered bars of an earlywood plates. E. Perforation plate with transition into lateral wall pitting (below). F. Earlywood plate with well-defined end (bottom). G. Earlywood plate containing some pit membrane remnants. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 23

Figure 10. Doryphora aromatica. SEM images of radial (A—D) and tangential (E, F) sections of wood. A. Unusually wide perforations; vessel to axial paren- chyma pitting at right. B. Pit membrane remnants at lateral ends of perforations. C. Perforation plate with (right) some transitional lateral wall pitting, D. Perfora- tion plate transitioning into lateral wall pitting, at right. E, F. Lateral wall pitting between vessels. E. Scalariform nature of lateral wall pitting. F. Pit membrane presence (holes are probably artifacts). 24 ALLERTONIA Volume 17

Figure 11. Doryphora aromatica. Details of Imperforate tracheary elements, axial parenchyma, and ray cells from radial sections as seen with light microscopy (B—E) and SEM (A, F. G). A. Outer surface of tracheid. B. Septate fiber-tracheids (septum at upper right). C. A strand of axial parenchyma to show a cross-wall. D. Section of a multiseriate ray; two files of upright cells at top; the remainder is composed of procumbent cells. E. A vertically-oriented tangential wall of an up- right cell; pits bordered. F, G. Scalariform vessel to ray pitting. F. Scalariform pits crossed by strands of secondary wall. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 25

Figure 12. Doryphora sassafras. Wood details as seen with light microscopy (A, B, F) and SEM (C, D, E). A. Transverse section. Latewood at top. B. Tangential section; multiseriate rays are four to five cells wide. C–F. Radial sections. C. Late- wood perforation plate, with very narrow perforations. D. Tip of perforation plate (bottom) and lateral wall pitting (center). E. Earlywood perforation. F. Septum in a septate fiber-tracheid. 26 ALLERTONIA Volume 17

Figure 13. Dryadodaphne crassa. Light microscope (A, B, D) and SEM (C, E) images of wood details. A. Transverse section. Most vessels are solitary. B. Tan- gential section; Rays are two to five cells wide. C. Earlywood perforation plate from radial section. Fungal hyphae evident. D. Portion of transverse section. Ar- rows indicate probable septate fiber-tracheids (wide lumina, thin walls). E. Pitting on a tracheid, radial section. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 27

Figure 14. Dryadodaphne crassa. Light microscope (A, E–G) and SEM (B–D) images of radial sections of wood. A. Multiseriate portion of multiseriate ray; cells are strongly procumbent, and about half of the tangential walls are diagonally- oriented. B. Pitting on procumbent cells; Pit membranes are intact. Scalariform vessel to procumbent ray cell pitting. D. Scalariform vessel to upright ra ycell pitting; other upright cells more sparsely pitted. E–G. Tangential walls of procum- bent ray cells. E. Pitting much denser on tangential wall than on horizontal wall. F. Vertically-oriented tangential wall with wide pit membranes. G, Diagonal wall with bordered pits. 28 ALLERTONIA Volume 17

Figure 15. Dryadodaphne novoguineensis. SEM images of radial sections. A. Portions of three perforation plates; center plate is a latewood high-resistance plate. B. Earlywood perforation plate with slender bars. C. Transition into lateral wall pitting; various quantities of pit membrane remnants are present in lateral ends of perforations. D. Bordered bars and pit membrane remnants. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 29

Figure 16. Dryadodaphne novoguineensis. Radial sections (A, C, D) and a tan- gential section (B) as seen by light microscopy (A) and SEM (B–D). A. Numerous septate fiber-tracheids and a perforation plate. B. Scalariform lateral wall pitting. C. Bordered pits seen from outer surface of a septate fiber-tracheid. D. Idioblastic oil cell from a radial file of upright ray cell. 30 ALLERTONIA Volume 17

Figure 17. Laurelia novae-zelandiae, MADw 5169, Wood sections seen by light microscopy (A, B) and SEM (C–H). A. Transverse section. Grouped vessels are common. B. Tangential section; rays are tall, two to three cells wide. C. Earlywood (left) and latewood (right) perforation plates from radial section. D. Latewood per- foration plate and some septate fibers, from radial section. E. Tangential section, scalariform lateral wall pitting. F–H. Radial section details. F. Narrowly bordered bars from a perforation plate. G. Septum in a septate fiber-tracheid. H. Outer walls of septate fiber-tracheids, showing small bordered pits. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 31

Figure 18. Laurelia novae-zelandiae, MADw 21319. Light microscope (A) and SEM images (B–F) of radial sections, showing presence of tyloses. A. Transverse wall in vessel, center, is a tylosis wall; most of the imperforate tracheary elements are septate fiber-tracheids. B. Juncture between two tyloses; a triangular intercel- lular space, above. C. Rounded tylosis tips pointing downwards in three vessel elements. D. Tylosis superimposed onto perforations of perforation plate. E. Ves- sels and septate fiber-tracheids, oriented horizontally; transverse tyloses subdivide several vessels. F. Tylosis wall superimposed onto a perforation plate. 32 ALLERTONIA Volume 17

Figure 19. Laurelia sempervirens. Light microscope (A–C) and SEM (D–H) im- ages A. Transverse section; vessels are relatively sparse and mostly solitary. B. Tan- gential section; rays are mostly short, biseriate. C—H Radial sections. Although septate fiber-tracheids are scarce in this species, septa in three are illustrated here. D. Bordered pits on the outer surface of a tracheid. E. Earlywood perforation plates with wide perforations. F. Perforation plate with vessel tip at top, rounded outline of perforation plate below. G. Latewood scalariform perforation plate. H. Narrow latewood scalariform-transitional perforation plate. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 33

Figure 20. Laureliopsis philippiana. Wood sections as seen by light microscope (A, B, H) and SEM (C–G, I) imaging. A. Transverse section. Vessels are relatively narrow, sparse, and solitary. B. Tangential section; rays are short, mostly biseri- ate. C–F. Radial sections of perforation plates. C. Latewood perforation plate with thick bars (center) and an earlywood plate (left). D. Perforation plate with transi- tion, at top, into lateral wall pitting. E. Earlywood perforation plate with thin bars and axially wide perforations. F. Lateral edges of perforation plate. Two bordered pits on the outside of a tracheid, from radial section. H. Ray in tangential section, showing large pits in face view on tangential wall of a procumbent cell. I. Tangen- tial wall of upright ray cell in sectional view; pits are markedly bordered. 34 ALLERTONIA Volume 17

Figure 21. Nemuaron vieillardii. Light microscope photographs of wood sec- tions. A. Transverse section. Vessels are narrow, sparse, and mostly solitary. B. Tangential section. Rays are wide multiseriate plus (center) uniseriate. C—F. Ra- dial sections. C. Bars are numerous in perforation plate portions. D. Portions of an earlywood plate (left) and a latewood plate (right). E—F. Portions of axial pa- renchyma strands, showing cross-wall. E. Ray cell to vessel pitting is scalariform; Cross wall has bordered pits. F. Axial parenchyma to upright ray cell pitting; tra- cheid at right. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 35

Figure 22. Nemuaron vieillardii. Light microscope photographs of radial sec- tions (A–D) and SEM images of tangential sections (E–G). A. Upright ray cell to vessel pitting (above); bordered pits in tangential wall of procumbent cell, center. B. Upright ray cells; Bordered pits in tangential walls. C. Oil cell in bark. D. Phlo- em parenchyma cell portions containing microcrystals plus (far right, an oil cell (oc). E–F Microcrystals in ray cells. E. Upright ray cell. F. Procumbent ray cell; larger microcrystal at left, others at right grade downward in size. G. Dense accu- mulation of microcrystals in procumbent cell. 36 ALLERTONIA Volume 17

Figure 23. Gomortega keule. Light microscope photographs (A, B, D–H) and an SEM image (C). A. Transverse section. A narrow latewood band from left to right, center. B. Tangential section; several axial parenchyma strands are present. C. Radial section of an earlywood perforation plate. D. Portion of transverse sec- tion. At center is a vessel (large cell) plus the cross wall of an axial parenchyma strand (dark gray). E—H. Radial sections. E. Portion of axial parenchyma strand (oriented horizontally); pits are outlined by dark-staining deposits. F. Upright (be- low) and procumbent (above ray cells; numerous bordered pits, especially on tan- gential walls. F. Subdivided upright ray cells (above); procumbent ray cells with variously-oriented tangential walls (below). H. Oil cells in the bark (left); brachy- sclereids at left. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 37

Figure 24. Light microscope photographs of wood sections of Siparuna (Sipa- runaceae). A–B. S. rimbachii. A. Radial section; bars on perforation plates are few and slender. B. Radial section; ray cells are upright. C–F. S. obovata. C. Transverse sections; diffuse-in-aggregates axial parenchyma is conspicuous. D. Tangential section; multiseriate rays are tall; some have uniseriate wings. E. Radial section; one perforation plate with a single bar, center; several strands of axial parenchyma are evident. F. Radial section; most ray cells are square to upright; a few procum- bent files are at top. 38 ALLERTONIA Volume 17 dominance of upright cells in rays, along with plates in that species provided imped- axial parenchyma, serves to shunt carbohydrates ance that would have been valuable (in upward into flowering and fruiting structures. confining embolisms to individual ves- The various shifts in structure permit accom- sel elements) on most days. Possibly the modation of greater fluctuation in flow rates and Maxwell Hill locality had canopy loss that aiding in supply of carbohydrate sinks while permitted the excessive transpiration, but maintaining conductive safety. Numerous clades in any case, the limits inherent in the sca- of angiosperms have acquired and/or modified lariform perforation plate mechanism as a all of these variations. The changes between means of water management are evident. Atherospermataceae  Gomortegaceae and c. Longer vessel elements moderate the Siparunaceae offer examples with broad evolu- impedance within vessels somewhat, while tionary significance where water management is retaining the capability to sieve out bubbles concerned. These wood anatomical changes can formed after ice thaws or confine embo- be seen in numerous clades. The value of scalar- lisms to individual vessel elements rather iform perforation plates in confining embolisms than allow embolism of an entire vessel. characterizes woody species in cool, wet, cloudy Bailey and Tupper (1918) show that vessel areas, but is superseded by other mechanisms elements and imperforate tracheary ele- for maintaining water columns in areas that ments become longer with increase in stem are subject to greater extremes in moisture and diameter, but do not offer explanations as in temperatures than occur in the areas where to why this should be true. Longer vessel Atherospermataceae and Gomortegaceae occur. elements provide less impedance (fewer CONCLUSIONS AND HYPOTHESES perforation plates per unit length); longer imperforate tracheary elements offer great- General Principles er potential mechanical strength (greater bonding surface if longer: see Carlquist, 1. Atherospermataceae exemplify “primitive” 1975, for a discussion). angiosperms by long-term occupancy of more mesic, cool habitats to which they are suited d. If transpiration rates are moderate, the by virtue of: number of embolized vessels is small enough so that formation of new wood a. Small to intermediate vessel diameter is (rather than extensive latewood) could pro- linked to slower, steadier conductive rates. vide conductive safety. b. Perforation plates provide consider- e. Lower tensions in vessels permit the able impedance (tolerable by virtue of greater area of scalariform lateral wall pit- slow transpiration) but also offer safety ting to be effective despite the lower me- in confining embolisms to individual ves- chanical strength of scalariform pitting. sel elements, which may be considered “megatracheids” in a sense. These features f. Tracheids can function in the majority of are especially pronounced in latewood Atherospermataceae as a conductive system perforation plates. An interesting exam- subsidiary to vessels in water conduction, ple of this is furnished by the wilting of but, more importantly, are embolism-free new foliage of all individuals of Illicium under most circumstances. Voigt (2011) L. on a very hot day on Maxwell Hill in shows that Sorbus, which has tracheids, re- the Malaya Highlands (Carlquist, 1975). sists breakage of water columns, whereas Although the soil is wet, the transpira- Sambucus, which has libriform fibers, has tion rate evidently exceeded the conduc- the ability to refill water columns under the tive rates because scalariform perforation same situations. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 39

g. Septate fiber-tracheids substitute for hydrological system quite different from axial parenchyma in Atherospermataceae. those of . Although septate fiber-tracheids are less ef- The above features of Atherospermataceae ficient at photosynthate input and retrieval are mostly shared by Gomortegaceae (which has (small slit-like pits) than axial parenchyma, more axial parenchyma). Atherospermataceous the mechanical strength of the walls of sep- wood characteristics favor safety over conduc- tate fiber-tracheids can be hypothesized to tive efficiency. rise to the level of fibers. 2. Siparunaceae (and the majority of angio- h. Ray cells can also substitute for some ax- sperm families) represent a departure from ial parenchyma functions (transfer of pho- the above patterns, and are adaptive where tosynthates into vessels): this is evident in peak flow is more extreme than in Atherosper- the lack of sheath cells on multiseriate rays mataceae. Alternative mechanisms for repair/ and in the large area of scalariform vessel prevention of embolisms under conditions to ray pits on upright ray cells. of more extreme temperature, humidity, and i. Speciation increases as clades enter soil moisture regimens accompany shift into ecological conditions with greater water a different syndrome of wood anatomical fea- stress due to drought and cold. This can tures. These “departures into seasonality” are be shown by the various clades of Cam- shown in geographic terms by the radiation panulidae (Tank and Donoghue, 2010), of Siparunaceae into Mesoamerican regions if one draws a line separating the clades with warm to hot climates. The mechanisms with scalariform perforation plates from shown by Siparunaceae include: those with simple perforation plates, as a. Vessels are wider in diameter, accommo- done in Carlquist, 2012, p. 920, Figure dating high flow volumes per unit of time. 14). Evidently the impedance provided by scalariform perforation plates inhibits the b. Vessels are grouped to provide redun- required handling of fluctuating tensions dancy and maintain pathways should em- in water columns to such an extent that bolisms occur. other methods for maintaining unbroken c. The length of vessel elements is much water columns (e.g., sugar transfer into less relevant than in Atherospermataceae, vessel elements from adjacent parenchyma and provides less safety (embolism preven- cells) become valuable. For example, the tion) due to simple or near-simple perfora- basal clades of are species poor, tion plates. Conductive safety functions are whereas Asteraceae are extremely species- transferred largely to axial parenchyma. rich. Moist, perpetually cool habitats such as cloud forest are stable and probably d. Lateral wall pitting of vessels consists saturated, offering fewer opportunities of circular bordered pits, a pattern that for speciation. As Asteraceae show, habi- features a compromise (more favorable tats that have greater extremes in mois- to contact area than in Atherospermata- ture and temperature are not only greater ceae) between strength (the “geodesic” or in geographical extent than cloud forests, “graphene” pattern) of thick wall material they are subject to more lethal extremes around the contact (pit membrane) area. that require mechanisms for maintaining This is related to presumptive greater ten- water columns (or, in the case of annuals, sions in the water columns of Siparuna. total cessation of growth), and are also less e. Axial parenchyma is well developed, saturated where speciation is concerned. providing a system for countering embo- Atherospermataceae represent a kind of lisms by osmotic means. Axial parenchyma 40 ALLERTONIA Volume 17

cells form a network in contact with rays, so much with systematics as with various so that direct and indirect contact with ves- means of water management related to ecol- sels is possible and the benefits of transfer ogy and physiology. Our understanding of of sugar into the apoplastic system is easily this has been delayed by the complexities of achieved. The evolution of vessels requires wood anatomy and by the difficulties of ex- associated living cells, as Gnetales show. perimental methods (isolating single factors successfully when wood is such a complex f. Imperforate tracheary elements attain a matrix). Bridging comparative anatomy and mechanical function rather than a conduc- comparative physiology is rendered diffi- tive one in some clades, and their design cult by the enormous anatomical diversity of and distribution changes accordingly. Tra- woods on the one hand, and the tendency for cheids represent a conductively “safe” cell wood physiologists or wood anatomists not type (embolisms do not travel from one tra- to cross disciplinary boundaries on the other cheid to another). Mechanically superior hand. The Atherospermataceae clade shows imperforate tracheary elements (libriform that combinations of details of anatomy as fibers) prevail in, for example, the Amazon seen by means of SEM and light microscopy rain forest, where the value of conduction can yield vistas into ecology, physiology, and of greater water volumes (accomplished growth form. by wider vessels) and mechanical strength of imperforate tracheary elements (= libri- 5. The persistence of Atherospermataceae form fibers) exceeds the value for conduc- for a long time (Renner et al., 2000) shows tive safety. that even in a moist forest habitat, Atheros- permataceae are adapted to their environ- 3. A wood in which tracheids are the imper- ments just as other plant groups are adapted forate tracheary elements has minimal vessel to theirs. One must be cognizant of what grouping (below about 1.5 vessels per group), characters vary and what they mean, however. because tracheids, as conducting cells, can Metcalfe (1987) quotes Foreman (1984), who conduct even though associated vessels em- studied wood of Monimiaceae and allies, as bolize. Loss of conductive ability (fiber- being skeptical about ecological interpreta- tracheids, libriform fibers) in imperforate tion of woods because “many of the genera tracheary elements is accompanied by vessel in which these differences occur can be found grouping. This shift in the mechanism for con- growing within a few meters of each other in ductive safety in wood (Carlquist 1984) has the same patch of rain forest.” This misses the interesting implications: tracheids are virtu- point that any particular species and its xylem ally embolism free, and can possibly maintain are adapted to a particular habitat in a way the conductive pathways until new wood is different from those of another species. There formed, as in Quercus. With vessel grouping, are multiple ways of utilizing the resources of the redundancy of vessels in a group means a particular area. Should one expect only one that pathways are protected to the extent that type of wood in a particular ecological loca- some water columns in a vessel group can tion (i.e., a monoculture)? No, and that does survive. Atherospermataceae include exam- not invalidate ecological interpretation of ples of both mechanisms, even within a genus, wood anatomy at all. whereas Siparunaceae do not have conductive imperforate tracheary elements. 6. In woods of groups that are relatively slow- evolving, like Atherospermataceae, we tend 4. Although comparative wood anatomy be- to notice plesiomorphies more. This may gan as a study of differences among angio- account, in part, for the tendency of phylo- sperms arranged on a systematic basis, the genists in pre-molecular days to cite plesio- features of particular woods are linked not 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 41

morphies as evidence of relationships (failure ciency. Typical scalariform perforation plates to recognize the numerous homoplasies in are not re-evolved as a clade with simple per- wood evolution is another reason). We can foration plates enters a cool cloud forest (e.g., now identify apomorphies within “primitive” most of the wet forest genera in Hawaii). groups, however. The various degrees of pres- Genera with simple perforation plates have ence of septate fiber-tracheids within the gen- other mechanisms adapted to maintenance era of Atherospermataceae exemplify such of water columns that are more effective than apomorphies. scalariform perforation plates. 7. Atherospermataceae is a “truly woody” 9. “Primitive” features such as scalariform group in which adult conditions are attained perforation plates are adaptive in mesic situa- relatively rapidly in early secondary xylem. tions and should not be regarded as relicts that The twig of Daphnandra tenuipes shows limit the evolutionary capabilities of woods. some stages in this ontogenetic series. In The family Illiciaceae includes the notori- Siparunaceae, on the contrary, there are some ously “primitive” wood of Illicium (a small indications of protracted juvenilism in wood: tree or shrub), with scalariform perforation ray cells are predominantly upright, even in plates that contain pit membrane remnants, stems larger than twigs. A wood can have one suggesting vessel elements minimally dif- or more juvenilistic features without having ferent from tracheids, although much wider. the full roster of characters cited as indicative However, Illiciaceae also now contains Kad- of paedomorphosis (Carlquist, 1962). sura Kaempf. ex Juss., which can have simple perforation plates in wider vessels (adaptive 8. Is the hydraulic and mechanical architec- because it is a liana). This example, if applica- ture of any given wood designed in terms of ble to angiosperms at large (and I believe that surviving extremes, or is it designed primar- it is) shows that “primitive” features such as ily to perform under “ordinary” (lower stress) scalariform perforation plates and other ple- conditions? Atherospermataceae can be cited siomorphic features of Atherospermataceae, as an example of how in a mesic environ- are optimal adaptations because ecology and ment, the mechanisms for promoting conduc- growth forms favor that stasis, and that an- tive safety are fewer. If extreme conditions are giosperms, rather than being limited in evolu- never present, there is no pressure to adapt to tionary adaptations by ancient wood features them. Annuals mostly grow in sites that are that are not changeable, are better regarded as ephemerally mesic, and a species in these adaptive and opportunistic. Escape in perfora- conditions may be successful primarily in tion plate architecture from long scalariform terms of seed production (annuals show vari- to simple may also be found in Dilleniaceae ous degrees of wood xeromorphism, probably and Actinidiaceae as well as some other fami- depending on how far into drier seasons they lies. Some families may, by earlier radiation, persist). Prominent axial parenchyma and pre-empt the opportunities open to others wide rays, lacking in Atherospermataceae, competing later for the same habitat, and this may relate to prevention/repair of embolisms. tendency is difficult to discern or analyze with The relatively high (compared to Monimi- certainty. aceae) number of vessels per mm2 suggests a safety mechanism, although other wood fea- 10. Particular wood cell types or conforma- tures of Atherospermataceae connote moder- tions in a wood may sometimes be found in ate tensions in vessels. We are left with the very small numbers. An example of this in proposition that each wood has its own bal- Atherospermataceae is found in those gen- ance between particular kinds of conductive era with very small numbers of septate fiber- safety and particular kinds of conductive effi- tracheids (Atherosperma, Doryphora, and 42 ALLERTONIA Volume 17

Nemuaron). Completeness in wood descrip- Atherospermataceae. This suggests an ability tions requires that these are reported, although of Atherosperma (the range of which includes a very sparsely represented condition may be Tasmania) to restrict embolisms to single ves- without function. What such features do show sel elements. The dissolution of the pit mem- is the evolutionary plasticity of wood in a par- branes in perforation plates occurs relatively ticular species: proportions of cells may shift late in the ontogeny of vessels at large, so rather easily if genetic information for a char- that one can hypothesize that the retention of acter is present. a pit membrane (or pit membrane remnants) is achieved relatively easily. In terms of con- Growth Rings duction versus safety, a vessel with occluded 11. The growth rings in Atherospermataceae perforation plates may be considered a “meg- and Gomortegaceae have only a brief incre- atracheid” functionally. “Megatracheids” ment of latewood and are not conspicuous, of this sort do not occur in clades of angio- suggesting that the species may experience sperms because the high impedance of end a few degrees of frost, but not winter-long walls of such vessel is favorable only in a few freezing of vessels. The presence of evergreen circumstances. The scalariform perforation foliage can be cited to support this hypoth- plate is not of negative value where conduc- esis. The portion of a growth ring devoted to tion rates and transpiration are consistently latewood in these families is small compared low, and where embolisms are occasional at to the broad expanse of the remainder of the most and not pervasive. growth ring, so that use of the term “early- 15. Smaller diameter of vessels, combined wood” for such a large proportion of a growth with more numerous vessels per mm2, found ring may strike some as inaccurate. in the twig of Daphnandra tenuipes, provides 12. Pittermann and Sperry (2003) find that in more conductive safety, but with a tradeoff conifers, resistance to embolism formation in terms of lowered conductivity. The high- by tracheids has a threshold at 43 µm, so that er embolism resistance of narrower vessels, tracheids with diameters narrower than 43 µm demonstrated by Hargrave et al. (1994) has cannot recover from embolisms. This may ap- not been confirmed by all wood physiolo- ply to narrower angiosperm vessels; the su- gists, but the pattern of small diameter vessels perparamo composite Loricaria Wedd. has in latewood is so pervasive in angiosperms vessels below this diameter (Carlquist, 2001, and Gnetales that I believe that this correla- p. 146). In Atherospermataceae, latewood tion will be validated. vessels are narrower than 43 µm, suggesting 16. Perforation plate dimorphism proves to be that recovery from freezing could be achieved a conspicuous, albeit hitherto overlooked fea- by this feature alone. ture of Atherospermataceae and Gomortega- 13. The narrow diameter of vessels, the low ceae. The narrow (measured in an axial conductive area (per unit of transverse wood direction) perforations (3–5 µm) of latewood section), and the probable high impedance of perforation, with correspondingly wide bars latewood perforation plates in Atherosper- between them, contrast with the wide (around mataceae and Gomortegaceae are features 7–8 µm) perforations in earlywood plates. that suggest resistance to moderately elevated The uniformity within Atherospermataceae in tension at the end of the growth season. width of these perforations within these cate- gories is striking. It suggests that bubbles that Vessels and Vessel Elements form within vessels are a little larger than 8 14. Pit membrane remnants are conspicuous µm in earlywood, but that in cooler tempera- in Atherosperma, but much less so in other tures when latewood is formed, bubbles are 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 43

smaller. Zimmermann (1983) proposed that of the Daphnandra tenuipes twig do not cor- bubbles formed as ice thaws in vessels are relate with lack of water but with a wood plan sieved out by scalariform perforation plates, featuring greater conductive safety earlier in thereby preventing spread of embolisms the ontogeny. length of the vessel. Styrax and Sassafras have 19. Vessels do not group as a safety mecha- wider bars (and narrower perforations) in late- nism if tracheids are present in appreciable wood vessels, but simple perforation plates in numbers to serve as a subsidiary conductive earlywood vessels (Carlquist, 2001, p. 27), system (Carlquist, 1984). Vessels do group if which suggests that simple perforation plates the imperforate tracheary element type asso- enhance conduction in earlywood and sca- ciated with vessels is non-conductive—fiber- lariform plates enhance conductive safety in tracheids or libriform fibers or septate fibers of those genera. The impedance of scalariform some kind. Atherospermataceae demonstrate perforation plates is not disadvantageous in a these phenomena within the family. Athero- habitat where transpiration is relatively low, sperma moschata, Doryphora aromatica, D. such as in a cloud forest. sassafras, Dryadodaphne crassa, Laurelia 17. Atherospermataceae have relatively nar- sempervirens, Laureliopsis philippiana, and row vessels compared to those of Moni- Nemuaron vieillardii all have woods in which miaceae (Money et al., 1950), in which septate fiber-tracheids comprise less than Atherospermataceae were formerly included. 10% of the fibrous secondary xylem (which Narrower vessels resist deformation better thereby is composed mostly of tracheids). than wider vessels of the same vessel wall The vessels per group figures for the named width. They also provide better potential safe- species are, respectively, 1.15, 1.07, 1.05, ty because the number per mm2 is higher than 1.17, 1.10. 1.21, and 1.26. The remaining spe- in Monimiaceae. In Monimiaceae, the pres- cies studied were Daphnandra micrantha, D. ence, albeit never abundant, of axial paren- tenuipes, Dryadodaphne novoguineensis, D. chyma (claimed to be scanty paratracheal by trachyphloia, and Laurelia novae-zelandiae. Metcalfe, 1987) suggests the participation of The vessels per group figures for this latter axial parenchyma in osmotic regulation of the group of species are 1.97, 2.12, 1.62, 1.60, conductive process. This would help counter and 2.10, respectively. Thus, in the first group, the vulnerability of vessels in Monimiaceae, the abundance of tracheids serves as a very which are in general wider than those of Ath- effective back-up conductive system and de- erospermataceae (Metcalfe, 1987). ters vessel grouping. In the latter group, the predominance of septate fiber-tracheids (evi- 18. In general, vessels increase in diameter as dently valuable as sources of photosynthate a stem becomes wider in diameter. There are storage) is not a source of conductive safety, some notable exceptions. In shrubs, decrease and so vessel grouping becomes a viable in vessel diameter as shrubs senesce is com- strategy. monly observable. In the case of these shrubs, one can correlate senescence with competi- 20. Vessel grouping tends to be higher in tion with other shrubs for water resources earlywood of Atherospermataeae because near the surface of the soil. Trees do not ex- vessels are more numerous and wider in di- perience the same competition, because they ameter. In latewood, vessels are sparser and are better positioned to tap deeper soil levels narrower. The twig material of Daphnandra that tend to be wetter and less contested (Tor- tenuipes shows that wood samples from twigs rey and Clarkson, 1975). Atherospermataceae may be reliable with respect to qualitative have wider vessels in larger trees, suggesting characters, but not for quantitative characters. this correlation. However, the narrow vessels The difference is definitely not sharp. For ex- 44 ALLERTONIA Volume 17

ample, the rays in D. tenuipes have square to 22. Perforation plates in Siparunaceae have upright cells, whereas in the wood samples very few bars, widely spaced, or no bars at taken from larger tree stems, the multiseriate all. This may be indicative of a family in tran- portions of multiseriate rays are prominently sition; the last vestiges of a structure some- procumbent. One could say that this could be times disappear slowly in evolutionary terms. reduced to a length/width ratio for ray cells, In some groups such as Dilleniaceae, one can and that there is increasing procumbency of find an ecological correlation. Long perfora- ray cells as a tree grows. In any case, the role tion plates with numerous bars can be found of protracted juvenilism (Carlquist, 1962) in in woods of the cloud forest species of Dil- its various manifestations has still not been lenia L., but the perforation plates of Hib- incorporated into our understanding of wood bertia J. Kenn. ex Andrews (Dilleniaceae) in anatomy to the degree that it should be. The Western Australia are few-barred or simple wood of annuals and woody herbs of various (Dickison et al., 1978), appropriate to the sorts is still considered peripheral to the sci- Mediterranean-type climate there. ence, whereas these growth forms comprise 23. High peak tensions generated by greater an appreciable portion of the world’s flora. mid-day transpiration are probably correlated 21. Within Atherospermataceae, there is no with the alternate circular lateral wall pitting progressive loss of bars on perforation plates on vessels in Siparuna (as well as in most or widening of perforations. Some species angiosperm woods). A gain in wall strength may have more bars than others (the lowest with little loss in contact area has been hy- number for the family is probably in Laurelia pothesized by evolution of alternate circular sempervirens). However, the width of perfora- bordered pits (Carlquist, 1975). This is the tions is sufficiently uniform within the family theory behind such diverse structures as geo- that one can hypothesize that perforation width desic domes, Volvox coenobia, and graphene (measured axially) suffices to deter spread of sheets. The efficacy of the polygonal dispo- air bubbles from one vessel element into the sition of wall material between circular pits one above or below. If wider perforations were can be seen in the fact that while 15 species present the safety conferred by the perforation in the sampling of Frost (1930) were found plate would be lost, even though impedance to have scalariform lateral wall pitting, 183 would be lowered and conductivity would be species were found to have alternate circular increased. Certainly there are some angio- (or polygonal) pits. We can even think of the sperm woods with few bars on perforation fibrous wood background in an angiosperm plates and with wide spaces between the bars. wood, when seen in a tangential section, as One can cite Empetraceae (empetroid Ericace- being like a vertically stretched polygon, with ae), Magnoliaceae, and Rhizophoraceae as ex- rays (especially when they are wide), being emplars of this condition, although many other the discontinuous phase. examples exist (see those families denoted “F” 24. Vessel-to-ray pitting in Atherospermata- and “R” in Carlquist, 2001, p. 63). Families ceae and Gomortegaceae is typically scalari- such as these three may benefit from greater form. The most logical hypothesis is that an perforation plate strength related to counter- extensive surface (scalariform offers more ing tensions in vessel elements combined with than alternate pits do) of pit membranes is lowered impedance by having few bars. The advantageous except when there is a selec- perforation plate bars of Atherospermataceae tive value for strength considerations, such are mostly slender, evincing low mechanical as tension in water columns. The Athero- strength. Wider bars occur in latewood perfora- spermataceae can be hypothesized to have tion plates in the family; appropriately, higher moderate peak tensions in vessels, although tensions probably prevail in latewood). 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 45

no measurements have been made. The wood tion—alternate pit sequence in tracheary ele- characteristics of Atherospermataceae and ments should be hypothesized to be optimally Gomortegaceae are congruent with low to functional at all points in this sequence. Sca- moderate water tensions. lariform pitting is appropriate for maximal intercellular contact when conductive safety 25. Scalariform perforation plates such as (high water column tensions) is not an issue, those found in Atherospermataceae are most and in young stems, strong negative pressures common in cloud forest areas. Cloud forests have not been found (Zimmermann, 1983). have not been demonstrated to be consis- tently cool and humid throughout the year, Imperforate Tracheary Elements with no prolonged warm periods. Mark Ol- son (personal communication, 2018) has 28. Starch storage in living cells serves at least demonstrated this with the aid of constantly- in part for events that are seasonal: flowering, recording weather stations in Mexican cloud fruiting, vegetative growth. Photosynthate forests. Frost can occur at higher elevations storage in Atherospermataceae is performed or at higher latitudes in a cloud forest, but ex- by ray cells and septate fiber-tracheids. Ax- tended periods of heat (which is moderate at ial parenchyma is very scarce in the family. most) do not. Kribs (1937) classified a number of families as having “Absent” axial parenchyma with- 26. More numerous vessels per mm2 are re- out comment other than referring to them as corded here for the Daphnandra tenuipes twig belonging more to lower levels of “special- (but not for the wood sample of D. micrantha ization” than to higher levels. The Frost and from a larger stem) and for Atherosperma Kribs correlation tables should be disregard- moschata. Twigs show greater conductive ed, or at least re-interpreted, since they are safety than do main stems (narrower vessels, not based on phylogenetically provable ideas. shorter vessels and shorter vessel elements) in Some families, such as Atherospermataceae, angiosperms woods at large (Carlquist, 1975; substitute septate fibers for axial parenchyma Zimmermann, 1983). The elevated density in (Carlquist, 2015). Atherosperma may be related to occupancy by this species of winter-cool localities such 29. Atherospermataceae may employ septate as Tasmania. fiber-tracheids instead of axial parenchyma for photosynthate storage because septate 27. The primary xylem of Daphnandra tenui- fiber-tracheids offer better mechanical char- pes progresses from annular and helical el- acteristics than axial parenchyma strands. ements directly to scalariform perforation Septate fiber-tracheids also can thus occupy plates and lateral wall pitting. This sequence the entirety of the fibrous tissue in a wood, does not culminate in transitional, opposite, whereas a wood the fibrous or background or alternate pitting as in most angiosperm tissue of which consists wholly of axial pa- woods. Some might be tempted to interpret renchyma has not been exploited except in such an example as demonstrating “ontog- some succulents (e. g., Crassulaceae, Cari- eny recapitulates phylogeny.” I think that we caceae). Septate fiber-tracheids, however, should be very skeptical that , which by being mechanically strong, are provided seem remarkably efficient in structure and with narrow slit-like pits that are not adapted show so much homoplasy in evolution of opti- to rapidity in photosynthate input/retrieval. mal-functioning anatomical conditions, leave Such fiber-tracheids could be adaptive in Ath- behind historical markers of their phylogenet- erospermataceae because input and retrieval ic history encoded in earlier-formed portions. of photosynthates correlates with the slower Rather, the scalariform wall structure with growth patterns (as opposed to flushing) and an annular—helical—scalariform—transi- 46 ALLERTONIA Volume 17

less massive sugar inputs for flowering and cheids in Atherospermataceae. The lack of fruiting. In addition, I am hypothesizing that fibriform cells intermediate in morphology Atherospermataceae do not use axial paren- between tracheids and septate fiber-tracheids chyma or septate fiber-tracheids for water- is noteworthy. As a hypothesis, one may of- column maintenance to the degree that woody fer the idea that an “either/or” morphology plants in habitats with greater temperature functions better than a “both/and” morphol- and humidity fluctuations do. ogy. Degrees of expression that are intermedi- ate are more easily modified genetically than 30. The shift from tracheids to septate fiber- degrees of expression that are more markedly tracheids is not a gradual shift, such as may different (vestigial, for example). be hinted in the much-reproduced drawings of Bailey and Tupper (1918) or the tables of 33. Where present along with tracheids, as Kribs (1937). The ability to form all of these in Dryadodaphne crassa, the septate fiber- cell types probably already resides in the ge- tracheids occur in close proximity to the ves- netic codes of Atherospermataceae and other sels. This suggests a functional equivalency “axial parenchyma absent” families. Mere in- between axial parenchyma and septate fiber- crease in the longevity of a fiber can convert tracheids. Paratracheal parenchyma is the it from being a libriform fiber to a living fiber most common form of axial parenchyma in (Carlquist, 2015). Commonly, living fibers angiosperm woods (Kribs, 1937), a condition are septate. A species that has libriform fibers very likely linked to osmotic control of con- in secondary xylem actually has the genetic duction in vessels. information to form bordered pits—they are 34. Although a few instances of axial paren- produced in vessels. Thus, Rosmarinus Tourn. chyma strands one cell long have been report- ex L. (Lamiaceae) has evolved tracheids as an ed in angiosperm woods, the vast majority autapomorphy (tracheids are resistant to em- of axial parenchyma stands are composed of bolism formation) rather than retaining them two or more cells. The majority of living fib- as a plesiomorphy from some ancestor. In ers, as far as we know, are septate, whereas Atherospermataceae, the occurrence of a few non-septate fibers presumably die as soon as axial parenchyma strands (Nemuaron) shows they have completed a secondary wall. Atten- how an alternate cell type can be formed oc- tion has not been focused on why cells with a casionally without becoming common in a longer lifespan should be subdivided. One ap- species. pealing hypothesis is that cyclosis within cells 31. Shift away from tracheids to septate fibers is less effective in very long non-subdivided has occurred in Daphnandra, Dryadodaphne, cells that in subdivided cells. and Laurelia novae-zelandiae. These instanc- 35. One might expect that in latewood of es deserve further study, with comparisons to Atherospermataceae, the component axial the species of Atherospermataceae that have cells would be the same in relative frequency tracheids predominantly, in order to ascertain as in earlywood. This does not appear to be possible physiological significance of this true: vessels are not only narrower, they are change. This phenomenon is not referable to less frequent. Scarcity of vessels in latewood fiber dimorphism (Carlquist, 2014), which in- does, in fact, characterize a scattering of an- volves relative parity of living and non-living giosperms, especially those with tracheids, fibers within a wood, as in Acer Tourn. ex L. such as Myrica L., as well as Ephedra Tourn. 32. Vestigial borders (some quite minimal) ex L. (Carlquist, 2001). A latewood that con- are present on the septate fiber-tracheids of sists wholly of tracheids presumably has the Atherospermataceae. These contrast clearly ultimate degree of conductive safety. with the “pits fully bordered” nature of tra- 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 47

36. The length of cells in an axial parenchy- other angiosperm families such as Fabaceae, ma strand in Atherospermataceae is longer in which large sheaths of axial parenchyma than the cellular units within a septate fiber surround vessels and vessel groups. Compar- (axial parenchyma is scarce within the family, ing the septate fiber-tracheids of Atherosper- however). This can be shown in Nemuaron. mataceae, the moderate axial parenchyma of The ratio between length and width in a pa- Gomortegaceae, and the massive vessel-cen- renchyma cell may be indicative of flow of tered axial parenchyma strands of Fabaceae, solutes within that cell. In this connection, one sees a probability that increase in amount the radially very long procumbent cells of and change in positioning of axial parenchy- the multiseriate portions of multiseriate rays ma can be paired with ecological and physi- in Atherospermataceae are noteworthy. The ological shifts. We need physiological studies multiseriate ray cells of paedomorphic woods of woods with these anatomical differences, are upright, an indication of directionality of because how angiosperms have “escaped” flow, at least in part. from steadily mesic habitats into habitats with greater fluctuation in all climatic parameters 37. We commonly think in terms of three kinds is incomplete at present. of imperforate tracheary elements: tracheids, fiber-tracheids, and libriform fibers (Bailey, 39. In angiosperm woods, one can generalize 1936; IAWA Committee on Nomenclature, that a link exists between axial parenchyma 1964). Families such as Atherospermataceae and sheath cells on multiseriate rays, be- suggest that two additional categories, sep- cause they form a network (Carlquist, 2018). tate fibers and septate fiber-tracheids, should Atherospermataceae have neither sheath cells be added. There are, to be sure, living non- on multiseriate rays nor any but very rare septate fibers, but only a relatively few in- axial parenchyma, so the pathways for photo- stances of these have been reported, because synthates contained in these living cells must so few anatomical studies have been done obviously be somewhat different. This may on liquid-preserved wood samples. Acer has account for the prominent scalariform pit- fiber dimorphism (Carlquist, 2014). The wide ting between vessels and upright ray cells in fibers in Acer exemplify living non-septate the family, but more is undoubtedly involved. fibers, and are physiologically important be- This situation underlines that the results of cause they store photosynthates during winter experimental work on one plant species is not months. Non-septate living fibers exist, but necessarily applicable to others. This is espe- are under-reported because of the widespread cially true in woods, where so many variables use of xylarium samples, in which nuclei can- are in play. Ideally experimental work isolates not be detected. two differing conditions without interplay with other factors, but the problems of experi- Axial Parenchyma ment design on wood are clearly complicated. 38. In Gomortegaceae, axial parenchyma is clearly present and is abundant relative to Rays the few strands seen in Atherospermataceae. 40. The rays of Atherospermataceae, Go- This suggests a shift in the functions of liv- mortegaceae, and Siparunaceae are multi- ing cells in Gomortegaceae as compared to seriate and uniseriate, with uniseriates less Atherospermataceae. The axial parenchyma common and composed wholly of square to in Gomortegaceae is mostly paratracheal, upright cells. The number of rays per mm suggesting some relationship to water col- (measured across a tangential section) is high- umn maintenance. The amount and pattern- er in Atherospermataceae and Gomortegace- ing of axial parenchyma in Gomortegaceae is, ae than in Siparunaceae. A larger number of however, much less prominent than in some rays per mm can be correlated with tracheid 48 ALLERTONIA Volume 17

presence and with more mesic habits in some kind of flow, and they do not participate, as far families of angiosperms (Carlquist, 2018), as known, in apoplastic sap flow, but there is although a generalization at this time would evidence that procumbent ray cells are active be unwise because reports on this feature are in radial flow of solutes, especially photosyn- relatively few. Conifers (excluding Gnetales) thates (Sauter et al., 1973). have uniseriate rays almost exclusively, and a 44. Upright ray cells occur in uniseriate rays large number of rays: the significance of this and in uniseriate wings of multiseriate rays in pattern has not been elucidated. Atherospermataceae and Gomortegaceae. The 41. No sheath cells were observed on the tangential walls of upright cells in these fami- multiseriate portions of multiseriate rays in lies bear numerous, densely placed, bordered either Atherospermataceae, Gomortegaceae, pits, which suggest radial flow despite the cell or Siparunaceae. Thus, procumbent cells shape. Upright ray cells are not densely pitted are in contact with axial parenchyma in Go- on other surfaces, but the pitting is sufficient mortegaceae and Siparunaceae. There is to account for transfer of photosynthates into contact between procumbent cells and either vessels as well as into septate fiber-tracheids. tracheids or septate fiber-tracheids in Athero- The possibility that upright ray cells with rel- spermataceae. The pitting between vessels atively abundant pitting may play some role and the septate fiber-tracheids is not promi- in radial flow of photosynthates should be nent in Atherospermataceae, but prominent entertained. scalariform pitting interconnects vessels with 45. The upright ray cells, as well as procum- upright ray cells in the family. Thus, some bent ray cells, in Atherospermataceae bear kind of physiological interaction between the prominent scalariform pits on walls facing rays and vessel elements may be present in vessels. The most obvious interpretation is Atherospermataceae. that these pits convey photosynthates into 42. Shape of ray cells is a key to direction of vessels as a mode of osmotic control of con- flow (Carlquist, 2018). Horizontally elongate duction. In the larger context, we should look (procumbent) ray cells, so prominent in rays with much greater care at the nature of pitting of older stems of Atherospermataceae, could of ray cells with regard to potential function. account for active input and retrieval of pho- The fact that bordered pits occur widely in ray tosynthates in the wood. Not surprisingly, cells, whereas bordered pits have traditionally most of the ray cells in the twig of Daphnan- been viewed in face view in tracheids and dra are upright to square, a juvenile pattern vessel elements, is one reason for this salient that would promote vertical (as well as some omission. Thus, an enormous source of poten- horizontal) flow of photosynthates. tial information about wood function has been overlooked. 43. Tangential walls of procumbent ray cells have large, densely laced, and often bordered 46. Upright cells, particularly those in uni- pits in Atherospermataceae and Gomortegace- seriate rays, could account for input of pho- ae. These attributes would confer greater radi- tosynthates into septate fiber-tracheids. One al flow efficiency to the procumbent cells. The can observe that having no upright ray cells cells are long, and thus have fewer tangential in any rays appears to be the most efficient walls per unit of radial length of ray, provid- method of achieving radial flow of photosyn- ing less impedance. Another feature that ef- thates, as in the rays of Acer. Acer wood has fectively increases the area of pit membranes been chemically tested for this active flow by on the tangential walls is the diagonal orien- phosphatase methods (Sauter et al., 1973). tation of many of these walls. Ray cells are However, Acer has large bundles of wide not commonly considered as promoting any starch-bearing fibers that intersect the mul- 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 49

tiseriate rays, presumably offering vertical by virtue of their sieve plates (and lateral-wall pathways. Atherospermataceae have either sieve areas). We need better documentation of septate fiber-tracheids or tracheids as a back- how photosynthates travel from the phloem ground cell type in woods. Upright ray cells into secondary xylem. Presumably, the route probably account, in part, for vertical function is from phloem parenchyma to phloem ray pa- of photosynthates. We must be careful about renchyma into xylem ray parenchyma. There applying physiological findings in one spe- are no sieve areas or other specialized struc- cies to the many unstudied species that exist. tures that would mediate this pathway. How- ever, in view of the above discussion of how 47. In Siparunaceae, the majority of ray cells tangential walls of xylem ray cells have maxi- are vertically elongate (upright). This sug- mized pit membrane surface areas, we might gests that vertical photosynthate flow may be stress that the walls of phloem parenchyma more active than horizontal flow in such ray and phloem ray parenchyma usually consist cells. Verticalized flow in ray cells is a prob- of primary walls without any secondary walls able aspect of the Siparunaceae with predomi- overlying them, thereby providing surfaces nance of upright cells in rays. Siparunaceae, optimal for cell-to-cell transfer. Because only which includes shrubs as well as trees, may phloem fibers and sclerenchyma in secondary possess wood with upright ray cells for longer phloem are specialized for mechanical sup- periods than Atherospermataceae. In stem on- port, the remaining cells of secondary phloem togeny, Atherospermataceae proceed rather are potentially ideal for symplastic transport. rapidly toward a “truly woody” pattern (rapid Phloem cells most often collapse after a sin- shift to procumbent ray cells ontogenetically) gle season. Xylem ray cells, in contrast, often in which radial flow in and out of a stem of have secondary walls, because they are an in- appreciable diameter is achieved by procum- tegral part of a tissue designed for mechanical bent ray cells. The value of vertical (axial) strength. conduction by means of upright cells can be seen when flowering or fruiting terminates 50. Microcrystals in secondary xylem ray stems, as in annuals and many perennials cells and in phloem parenchyma of bark are (Carlquist, 2018). newly reported here for Atherospermataceae. They were noted in Daphnandra micran- 48. Ethereal oil cells occur in upright ray tha, Doryphora aromatica, D. sassafras, cells in Atherospermataceae in idioblastic and Nemuaron vieillardii. These crystals are fashion. Idioblastic distribution of oil cells in smaller than the calcium oxalate crystals seen the rays, like distribution of all types of idi- in other Laurales by an order of magnitude, oblasts, assures maximal division of labor of which may explain why they have been pre- cells within a cell population. This certainly viously overlooked. They are strongly elon- applies to deposition of resin-like substances gate in shape, but with tapered ends, and are in ray cells of Atherospermataceae and Go- scattered at random within cells rather than mortegaceae. Although idioblasts containing grouped in packets as raphides are. The mi- these substances are more abundant than the crocrystals, moreover, show no tendency to oil cell idioblasts, careful examination shows occur idioblastically in rays: a ray that has that most ray cells are, in fact, free from the them in one ray cell apparently has them in dark-staining resin-like deposits, the distribu- all cells of that ray. I was unable to find the tion of which is thus idioblastic. microcrystals in the woods I examined of 49. The upward pathway of photosynthates Gomortegaceae and Siparunaceae. The pos- through sieve-tube elements in the phloem has sibility that they might be related to mineral been well documented because sieve-tube ele- accumulation should be investigated. ments are clearly specialized for this function 50 ALLERTONIA Volume 17

51. Crown groups of clades in angiosperms a much more frequent basis than in the cloud are sometimes speciose and may contain more forest species. Species adapted to dryland numerous families or genera with simple habitats and to highly seasonal (e.g., boreal) or few-barred perforation plates. These forests are hypothesized to require embolism crown groups are accompanied by basal resistance/reversal mechanisms more difficult clade branches with rather few species that to achieve than the conductive safety mecha- sometimes have scalariform perforation nisms of the cloud forest species. Thus, the plates, a few with a large number of bars. forests areas with greater daily or seasonal ex- Atherospermataceae and Gomortegaceae tremes are less saturated with species, and any are examples of small basal branches of the groups successful in these habitats are likely Laurales clade with long scalariform per- to speciate more extensively. foration plates. , a crown group with numerous species, have simple perfo- ACKNOWLEDGEMENTS ration plates in wood. Now that we have a This investigations would have been impos- more complete phylogeny of Asterales, we sible without the wood samples kindly fur- can see an even more dramatic example: As- nished by curators. Thanks go especially to Alex teraceae are highly speciose and have simple C. Wiedenhoeft for specimens from the Forest perforation plates, whereas a number of small Products Laboratory (MADw) in Madison, Wis- families with scalariform perforation plates consin. Others who provided samples include lie at the base of the Asterales clade (e.g., Mare Nazaire, RSA Herbarium, Claremont Alseuosmiaceae, Argophyllaceae, Penta- (Daphnandra tenuipes); Peter H. Raven, Mis- phragmataceae. Rousseaceae). Mark Olson souri Botanical Garden (McPherson collection (personal communication, 2018) has called of Nemuaron vieillardii from MO); and Junji my attention to this phenomenon and asked Sugiyama, RISH Xylarium, Kyoto (Daphnan- for my interpretation. dra micrantha). David Lorence was very helpful My explanation is that scalariform n editorial matters. Mark Olson provided help perforation plates form a device for embolism on conceptual matter and Edward L. Schneider resistance where embolisms are not frequent, offered useful suggestions. but when they occur, can be confined to single vessel elements. More often, such vessels are LITERATURE CITED less likely to develop embolisms because of Bailey, I. W. 1936. The problem of differentiation and classifi- cation of tracheids, fiber-tracheids, and libriform fibers. the steady and slow transpiration, with low Trop. Woods 45: 18–23. xylem tensions, in species that occupy cool Bailey, I. W. and W. W. Tupper. 1918. Size variation in tra- moist and cloud-forest habitats. These habi- cheary cells. I. A comparison between the secondary xylems of vascular cryptogams, gymnosperms, and tats are characteristic of species with scalari- angiosperms. Proc. Amer. Acad. Arts Sci. 54: 149–204. form perforation plates in wood (Carlquist, Carlquist, S. 1962. A theory of paedomorphosis in dicotyle- 2001). Tropical rain forests and boreal forests donous woods. Phytomorphology 12: 30–45. Carlquist, S. 1975. Ecological strategies of xylem evolution. have high transpiration rates and do not con- University of California Press, Berkeley. form to this construct. Cloud forest and other Carlquist, S. 1984. Vessel grouping in dicotyledons woods: habitats where transpiration is moderate tend significance and relationship to imperforate tracheary elements. Aliso 10: 505–525. to be saturated with species, whereas dry- Carlquist, S. 2001. Comparative wood anatomy. Ed. 2. land and hot areas have higher rates of tran- Springer Verlag, Berlin & Heidelberg. spiration, associated with simple perforation Carlquist, S. 2012. How wood evolves: a new synthesis. Bot- any 90: 901–940. plates. Embolisms in vessels of the dryland/ Carlquist, S. 2014. Fibre dimorphism: cell type diversification highly seasonal woody species are more fre- as an evolutionary strategy in angiosperm woods. Bot. J. quent and may require other devices for main- Linnean Soc. 174: 44–67. Carlquist, S. 2015. Living cells in wood. 1. Absence, scarcity tenance of water columns (e.g., transfer of and histology of axial parenchyma as keys to function. sugars into vessels) or refilling of vessels on Bot. J. Linnean Soc. 177: 291–321. 2018 CARLQUIST: WOOD ANATOMY OF ATHEROSPERMATACEAE 51

Carlquist, S. 2018. Living cells in wood. 3. Overview; Func- Pittermann, J., and J. S. Sperry. 2003. Tracheid diameter is tional anatomy of the parenchyma network. Bot. Rev. the key trait determining the extent of freezing-induced 84: 242–294. embolism in conifers. Tree Physiol. 23: 907–914. Dickison, W. C., P. M. Rury, and G. L. Stebbins. 1978. Xylem Poole, I., and J. E. Francis. 1999. The first record of atheros- anatomy of Hibbertia in relation to ecology and system- permataceous wood from the upper Cretaceous of Ant- atics. J. Arnold Arb. 59: 32–49. arctica. Rev. Palaeobot. Palyn. 107: 97–107. Erdtman. G. 1952. Pollen morphology and plant . Renner, S. S. 1999. Circumscription and phylogeny of the Angiosperms. Almqvist & Wiksell, Stockholm. Laurales: evidence from molecular and morphological Foreman, D. B. 1984. The morphology and phylogeny of the data. Amer. J. Bot. 86: 1301–1315. Monimiaceae ( lato) in Australia. Thesis, Univer- Renner, S. S., D. B. Foreman, and D. Murray. 2000. Timing sity of New England, Armidale, Australia. transantarctic disjunctions in the Atherospermataceae Frost, F. H. 1930. Specialization in secondary xylem in di- (Laurales): evidence from coding and noncoding chlo- cotyledons. II. Evolution of end wall of vessel segment. roplast sequences. Syst. Biol. 49: 579–591. Bot. Gaz. 90: 198–212. Sauter, J. J., Iten, W. I., and M. H. Zimmermann. 1973. Stud- Garratt, G. A. 1934. Systematic anatomy of the woods of the ies on the release of sugar into the vessels of sugar ma- Monimiaceae. Trop. Woods 39: 18–44. ple (Acer saccharum). Can. J. Bot. 51: 1–8. Hargrave, K. R., K. J. Kolb, F. W. Ewers and S. Davis. 1994. Schodde, R. 1969. A monograph of the family Atherosper- Conduit diameter and drought-induced embolism for- mataceae R. Br. Thesis, Adelaide. mation in Salvia mellifera Greene (Labiatae). New Phy- Soltis, D. E., P. S. Soltis, P. K. Endress, and M. W. Chase. tol. 126: 695–705. 2005. Phylogeny and evolution of angiosperms. Sinauer IAWA Committee on Nomenclature. 1964. Multilingual glos- Associates, Sunderland, Massachusetts. sary of terms used in wood anatomy. Verlagsbuchanstalt Stern. W. L. 1955. Xylem anatomy and relationships of Go- Konkordia, Winterthur, Switzerland. mortegaceae. Amer. J. Bot. 42: 874–885. Johansen, D. A. 1940. Plant microtechnique. McGraw Hill, Stern. W. L., and S. Greene. 1958. Some aspects of variation New York. in wood. Trop. Woods 108: 65–71. Kribs, D. A. 1937. Salient lines of specialization in the wood Stevens, P. 2001 onwards. Angiosperm phylogeny website. parenchyma of dicotyledons. Bull. Torrey Bot. Club 64: http://www.mobot.org/MOBOT/Research/APweb/wel- 177–186. come.html Metcalfe, C. R. 1987. Anatomy of the dicotyledons. Ed. 2. Tank, D. C. and M. J. Donoghue. 2010. Phylogeny and phy- Vol. III. Magnoliales, Illiciales, and Laurales. Clarendon logenetic nomenclature of the Campanulidae based on Press, Oxford. an expanded sample of genes and taxa. Syst. Bot. 356: Meylan, B. A., and B. G. Butterfield. 1978. The structure 425–441. of New Zealand Woods. DSIR Publication 122. N. Z. Torrey, J. G., and D. T. Clarkson (eds.). 1975. Development DSIR, Wellington. and function of roots. Academic Press, New York. Money, L. L., Bailey, I.W., and B.G. L. Swamy. 1950. The Voigt, U. K. 2001. Hydraulic vulnerability, vessel refilling, morphology and relationships of the Monimiaceae. J. and seasonal courses of stem water potential of Sorbus Arnold Arb. 31: 372–404 aucuparia L. and Sambucus nigra L. J. Exp. Bot. 52 Patel, R. N. 1973. Wood anatomy of the dicotyledons indig- (360): 1527–1536. enous to New Zealand. 3. Monimiaceae and Atherosper- Zimmermann, M. H. 1983. Xylem structure and the ascent of mataceae. N. Z. J. Bot. 11: 587–598. sap. Springer Verlag, Berlin & Heidelberg. 52 ALLERTONIA Volume 17

INDEX TO BOTANICAL NAMES Names occurring in the title, abstract, references cited, tables, and appendices are not indexed. An asterisk (*) indicates a figure.

Acer, 46, 47, 48 Illicium, 38, 41 Actinidiaceae, 41 Kadsura, 41 Alseuosmiaceae, 50 Lactoris, 2 Argophyllaceae, 50 Lauraceae, 50 Asteraceae, 39, 50 Laurales, 1, 3, 13, 49, 50 Asterales, 39, 50 Laurelia, 1, 3, 5 Atherosperma, 3, 41, 42, 45 —aromatica, 3 —moschata, 3, 5, 6, 10, 13, 14*, 15*, 16*, 17*, 43, 45 —novae-zelandiae, 3, 6, 7, 10, 11, 30*, 31*, 43, 46 Atherospermataceae, 1, 2, 3, 4, 7, 11, 12, 13, 38, 39, 40, 41, —sempervirens, 3, 5, 11, 13, 32*, 43, 44 42, 43, 44, 45, 46, 47, 48, 49, 50 Laureliopsis, 3, 5 Campanulidae, 39 —philippiana, 3, 11, 13, 33*, 43 Caricaceae, 45 Loricaria, 42 Crassulaceae, 45 Magnoliaceae, 44 Daphnandra, 3, 5, 46, 48 Monimiaceae, 2, 3, 40, 41, 43 —micrantha, 3, 6, 7, 18*, 43, 45, 49, 50 Myrica, 46 —tenuipes, 3, 4, 6, 7, 19*, 20*, 41, 42, 43, 44, 45, 50 Nemuaron, 4, 8, 42, 46, 47 Dillenia, 44 —vieillardii, 3, 5, 6, 12, 34*, 35*, 43, 49, 50 Dilleniaceae, 2, 41, 44 Nothofagus, 1 Doryphora, 3, 13, 41 Pentaphragmataceae, 50 —aromatica, 3, 5, 6, 8, 21*, 22*, 23*, 24*, 43, 49 Podocarpus, 1 —sassafras, 3, 6, 8, 25*, 43, 49 Quercus, 40 Drimys, 2 Rhizophoraceae, 44 Dryadodaphne, 3, 10, 13, 46 Rosmarinus, 46 —crassa, 3, 9, 26*, 27*, 43, 46 Rousseaceae, 50 —novoguineensis, 3, 6, 9, 28*, 29*, 43 Salix, 1 —trachyphloia, 3, 6, 9, 43 Sambucus, 38 Empetraceae, 44 Sassafras, 43 Ephedra, 46 Siparuna, 4, 13, 37*, 39, 44 Ericaceae, 44 —bifida, 13 Fabaceae, 47 —obovata, 4, 13, 37* Gnetales, 40, 42, 48 —rimbachii, 4, 13, 37* Gomortega, 12, 13 —thecaphora, 13 —keule, 4, 12, 13, 36* Siparunaceae, 2, 3, 4, 13, 38, 39, 40, 41, 44, 47, 48, 49 Gomortegaceae, 1, 2, 3, 4, 12, 13, 38, 39, 42, 44, 45, 47, Sorbus, 38 48, 49, 50 Styrax, 43 Hibbertia, 44 Volvox, 44 Illiciaceae, 41 Weinmannia, 1 Publications of the National Tropical Botanical Garden Occasional Papers and Books Available for Purchase Prices reflected in U.S. Dollars •• Multiple copies (10 or more) for resale: Depending on inventory availability, may be purchased with a 30% discount by retail stores and subscription services…plus $10.00 Handling Fee and US Postal Service price for shipping •• Single copies may be purchased with 40% discount by public libraries, universities or colleges … plus $10.00 Handling Fee and US Postal Service price for shipping. These orders must come directly to the attention of [email protected] •• Single copies of JEWELS OF HAWAI’I may be purchased in person at the Southshore Gift Shop at 4425 Lawai Road, Poipu, HI 96756, or by phone at: 808-742-2433

OCCASIONAL PAPERS

Allertonia

Volume 1 (complete Volume; includes Table of Contents and Index $40.00): No. 1 Rare and Endangered Species of Hawaiian Vascular Plants by F.R. Fosberg and Derral Herbst. April 1975. ($7.00) No. 2 The Pacific Species of Pittosporum Banks ex Gaertn. (Pittosporaceae)by Judith E. Haas. May 1977. ($9.00) No. 3 The Family Thelypteridaceae in the Pacific and Australasiaby R.E. Holttum. August 1977. ($6.50) No. 4 Revision of Perymenium (Asteraceae-) in Mexico and Central America by John J. Fay. January 1978. ($6.00) No. 5 Wood Anatomy and Relationships of Bataceae, Gyrostemonaceae, and Stylobasiaceae by Sherwin Carlquist. February 1978. ($4.00) No. 6 A Precursor to a New Flora of Fiji by Albert C. Smith. March 1978. ($8.00) No. 7 A Revision of the Genus Ptychosperma Labill. (Arecaceae) by Frederick B. Essig. August 1978. ($6.50) Volume 2 (complete Volume; includes Table of Contents and Index -$45.00): No. 1 A Synopsis of the Indigenous Genera of Pacific Rubiaceaeby Steven P. Darwin. January 1979. ($4.00) No. 2 The Vegetation of Eastern Samoa by W. Arthur Whistler. April 1980. ($16.00) No. 3 Anatomy and Systematics of Balanopaceae by Sherwin Cariquist. May 1980. ($6.00) No. 4 The Genus Galium Section Lophogalium (Rubiaceae) in South America by Lauramay T. Dempster. May 1980. ($4.00) No. 5 Comparative Wood Anatomy and Evolution of Cunoniaceae by William C. Dickison. October 1980. ($5.50) No. 6 The Vegetation of Late, Tonga by W.R. Sykes. January 1981. ($4.00) No. 7 Wood Anatomy of Pittosporaceae by Sherwin Carlquist. March 1981. ($5.00) No. 8 The Genus Galium (Rubiaceae) in South America. II by Lauramay T. Dempster. July 1981. ($4.50) Volume 3 (complete Volume; including Table of Contents and Index $50.00): No. 1 Erythrina Symposium IV. Erythrina (Fabaceae: Faboideae) by Rupert C. Barneby, B.A. Krukoff, and Peter H. Raven. February 1982. ($20.00) No. 2 Leaf Anatomy and Classification of the Olacaceae, Octoknema, and Erythropalumby P. Baas, E. van Oosterhoud, and C.J.L. Scholtes. September 1982. ($7.00) No. 3 The Genus Galium (Rubiaceae) in South America. III by Lauramay T. Dempster. December 1982. ($6.50) No. 4 A Revision of Flueggea (Euphorbiaceae) by Grady L. Webster. March 1984. ($7.00) No. 5 The Indigenous Palms of New Caledonia by Harold E. Moore, Jr. and Natalie W. Uhl. September 1984. ($12.00) No. 6 A Revision of Jasminum in Australia by P.S. Green. October 1984. ($5.50) Volume 4 - beginning with Volume 4, each number is individually indexed. (Incomplete Volume, due to Out of Stock of one number; includes Table of Contents; reduced volume price $50.00): No. 1 Monograph of the Hawaiian Madiinae (Asteraceae): Argyroxiphium, Dubautia. and Wilkesia by Gerald D. Carr. August 1985. ($18.00) No. 2 Essays on Ficus by E.J.H. Corner. September 1985. ($6.00) ***OUT OF STOCK*** No. 3 A Systematic Study of Delarbrea Vieill. (Araliaceae) by Porter P. Lowry II. August 1986. ($5.00) No. 4 A Biosystematic Revision of Hawaiian Tetramolopium (Compositae: Astereae) by Timothy K. Lowrey. November 1986. ($10.00) No. 5 Rheophyles of the World: Supplement by C.G.G.J. van Steenis. June 1987. ($10.00) No. 6 A Taxonomic Revision of the Hawaiian Species of the Genus Chamaesyce (Euphorbiaceae) by Daryl L. Koutnik. September 1987. ($9.50) No. 7 A Revision of Deppea (Rubiaceae) by David H. Lorence and John D. Dwyer. July 1988. ($8.00) Volume 5 (complete Volume, includes Table of Contents -$50.00): No. 1 A Precursory Study of Fijian Orchids by Paul J. Kores. April 1989. ($25.00) No. 2 The Origin and Distribution of Kava (Piper methysticum Forst. f., Piperaceae): a Phytochemical Approach by V. Lebot and J. Lévesque. September 1989. ($10.00) No.3 The Genus Galium (Rubiaceae) in South America. IV by Lauramay T. Dempster. January 1990. ($10.00) No. 4 Ethnobotany of the Cook Islands: the plants, their Maori names, and their uses by W. Arthur Whistler. April 1990. ($10.00) Volume 6 (complete Volume, includes Table of Contents -$60.00): No. 1 The Taxonomy of Old World Heliconia (Heliconiaceae) by W.J. Kress. May 1990. ($20.00) No. 2 The Revegetation and Rehabilitation of Strip Mined Bauxitic Soils by Richard A. Howard, R. L. Fox, et al. January 1991. ($20.00) No. 3 Studies in Indo-Pacific Rubiaceae by F. R. Fosberg and Marie-Hélène Sachet. November 1991. ($10.00) No. 4 Wood Anatomy of Solanaceae: A Survey by Sherwin Carlquist. April 1992. ($8.00) No. 5 The Genus Columnea (Gesneriaceae) in Ecuador by Lars P. Kvist and Laurence E. Skog. January 1993. ($10.00) Volume 7 (complete Volume, includes Table of Contents. $60.00): No. 1 A Revision of Timonius Subgenus Timonius (Rubiaceae: Guettardeae) by Steven P. Darwin. June 1993. ($8.00) No. 2 The Forster Pacific Islands Collections from Captain Cook’s Resolution Voyageby F. R. Fosberg. December 1993. ($9.00) No. 3 A Systematic Study of the Genus Acianthus (: ) by Paul J. Kores. November 1995. ($25.00) No. 4 Botanical Results of the 1988 Fatu Hiva Expedition to the Marquesas Islands edited by David H. Lorence. February 1997. ($14.00) No. 5 A Catalogue of the Herbarium Specimens From Captain Cook’s First and Second Expeditions Housed in the Copenhagen Herbarium (C) by Bertel Hansen and Peter Wagner. February 1998. ($9.00) Volume 8 (complete Volume, includes Table of Contents. $35.00): No. 1 On the Taxonomy and Biogeography of Euodia and Melicope (Rutaceae) by T. G. Hartley. February 2001. ($35.00) Volume 9 No. 1 A Revision of Psychotria (Rubiaceae) in the Marquesas Islands (French Polynesia) by David H. Lorence and Warren L. Wagner. November 2005. ($22.50) No. 2 Herbal Medicine in Samoa by W. Arthur Whistler. December 2006. ($22.50) Volume 10 Checklist of the Vascular Plants of Pohnpei, Federated States of Micronesia with Local Names and Uses by Katherine Herrera, David H. Lorence, Timothy Flynn, and Michael J. Balick. October 2010. ($35.00) NOTE: Effective beginning with Volume 10, Allertonia will no longer be published in separate issue numbers, but each issue will constitute a separate, stand-alone volume. Volume 11 Botanical Survey of the Ringgold Islands, Fiji by W. Arthur Whistler. April 2012. ($20.00) Volume 12 A Revision of Barringtonia (Lecythidaceae) by Ghillean T. Prance. December 2012. ($35.00) Volume 13: Honoring Beekman and Rumphius: Proceedings of the Symposium for the 2011 David Fairchild Medal for Plant Exploration, edited by M. Patrick Griffith and David H. Lorence. January 2014. ($35.00) Volume 14: Annotated List of Tahitian Plant Names by W. Arthur Whistler. September 2015. ($35.00) Volume 15 Tales of the Solomons by E. J. H. Corner. December 2016. ($25.00) Volume 16 Studies on the Gender and Breeding System of Kadua haupuensis (Rubiaceae), an endemic species from Kaua’i, Hawaiian Islands by William G. Laidlaw and David H. Lorence. December 2017. ($12.00) Volume 17 Wood Anatomy of Atherospermataceae and Allies: Strategies of Wood Evolution in Basal Angiosperms by Sherwin Carlquist. December 2018. ($25.00)

BOOKS

Polynesian Herbal Medicine. Dr. W. Arthur Whistler. 248 pp., 117 figures, including 115 color photographs. 1992. Discusses ailments and plants commonly used in treatments, both past and present. $32.95. A Chronicle and Flora of Niihau. Juliet Rice Wichman and Harold St. John. 168 pp., 29 figures, including 8 pp. of color. 1990. A historical account of the Hawaiian island of Niihau, with a catalog of the island’s flora, including both non-vascular and vascular plants. $9.95. Wilson Popenoe: Agricultural Explorer, Educator, and Friend of Latin America. Dr. Frederic Rosengarten, Jr. 182 pp., 92 figures. 1991. An illustrated biography of this well-known horticulturist. $22.95. Annotated Bibliography of Mascarene Plant Ljfe. David H. Lorence and Reginald E. Vaughan. 274 pp., 14 figures. 1992. A comprehensive work, bringing together 1,600 references dealing with Mascarene plant life. $15.00. Flora Vitiensis Nova: A New Flora of Fiji. Albert C. Smith. Volume 1. 501 pp., 101 figures, including 16 pp. of color. 1979. Includes introduction and treatments of gymnosperms and (Families 1-43, except Orchidaceae). $55.00. Volume 2. 818 pp., 208 figures, including 8 pp. of color. 1981. Includes treatments of 73 families of dicotyledons (Families 44-116). $95.00. Volume 3. 764 pp., 192 figures, including 8 pp. of color. 1985. Includes treatments of 47 families of dicotyledons (Families 117-163). $90.00. Volume 4. 383 pp., 132 figures, including 8 pp. of color. 1988. Includes treatments of 6 families of dicotyledons (Families 164-169). $55.00. Volume 5. 632 pp., 92 figures, including 8 pp. of color. 1991. Includes treatments of 17 families of dicotyledons (Families 170-186) and 1 family of monocotyledons (Family 32- Orchidaceae); Addenda et Corrigenda; and Index of families, genera, species, and infraspecific taxa. $85.00. Comprehensive Indices. 125 pp. 1996. Covers Volumes 1-5. Index of scientific names, including synonyms, and index of vernacular names, including English, Fijian, and Hindi. $24.00 Price Savings for Complete Set: Volumes 1-5 plus Comprehensive Indices: $380.00 Limu: An Ethnobotanical Study of Some Hawaiian Seaweeds. Isabella Aiona Abbott. Fourth edition. 39 pp., color photographs. 1996. An illustrated guide to the commonly used seaweeds, discussing their identification, distribution,scientific and common names, methods of preparation, and uses by various ethnic groups living in Hawai‘i. $5.95.

Jewels of Hawaii. ONLY SOLD at our Southshore, Kauai VISITOR CENTER GIFT SHOP at 4425 Lawai Road, Poipu, HI 96756. Soft cover, 48 pages. More than 90 stunning photographs by noted nature photographer Louise Tanguay capturing the scenic beauty and fascinating plants of NTBG’s Southshore Gardens. $9.95

Flora of The Cook Islands by W.R. Sykes. Hardcover only, 973 pp. 2016. Flora of the Cook Islands is a complete account of plants found wild in the Cook Islands and plants common in cultivation written by W. R. (Bill) Sykes. Descriptions and keys are provided for 108 fern and 567 species. Of these, 104 ferns and 187 flowering plant species are indigenous. Available for $95.00 + $3.99 shipping – from www.amazon.com, or International Association for Plant Taxonomy (IAPT): http://www.iapt-taxon.org Order Instructions for Retail Stores, Subscription Services, Libraries, Universities, or Colleges

All orders should be placed via email, phone, or fax to our Publications Order Desk in the Botanical Research Center at NTBG Headquarters in Kalāheo, HI

Email (preferred method): [email protected] Fax: (808) 332-9765, attn: David Lorence Phone: (808) 332-7324, ext. 2273

•• Include a list of title(s) and quantity(ies) needed by title •• Include billing and shipping addresses •• Include purchase order number •• Include contact name with email (preferred method) and/or phone number •• New customers - please indicate whether your business is:: Retail store Subscription Service Library - Public, University, College Other (Describe)

The Publications Order Desk will check inventory and respond with information as to: •• Qualifying Discount •• Estimated Date for Shipping •• Whether pre-payment is required (payable to National Tropical Botanical Garden)

Please note that orders on a consignment basis are not accepted.

The mission of the National Tropical Botanical Garden is to enrich life through discovery, scientific research, conservation, and education by perpetuating the survival of plants, ecosystems, and cultural knowledge of tropical regions.