Wood Anatomy of the Altingiaceae and Hamamelidaceae

Home , Altingiaceae, Cercidiphyllum, Corylopsis, Corylopsis spicata, Disanthus cercidifolius, Distylium

IAWA Journal, Vol. 31 (4), 2010: 399–423

WOOD ANATOMY OF THE ALTINGIACEAE AND HAMAMELIDACEAE

Elisabeth A. Wheeler1, Sung Jae Lee2 and Pieter Baas3

SUMMARY Wood anatomical data for all three extant genera of the Altingiaceae and 23 of the 27 extant genera of the Hamamelidaceae were compiled in an effort to find features distinctive to genera, tribes, or subfamilies within these families. All genera studied have diffuse porous wood (except Corylopsis which tends to be semi-ring porous), vessels are predominantly solitary and narrow (<100 µm, usually < 50 µm) and angular in outline, vessel elements are long (>800 µm) with scalariform perforation plates with average bar numbers of 9–44, intervessel pits are mainly scalariform to opposite, vessel-ray parenchyma pits are scalariform with slightly reduced borders and usually are in the square to upright marginal ray parenchyma cells, rays are heterocellular and narrow, usually 1–3-seriate. Although the wood anatomy of both families is relatively homogeneous, it is possible to key out many genera using a combination of qualitative (presence/absence and location of helical thickenings in vessel elements and fibers, crystal occurrence, axial parenchyma abundance, degree of ray heterogeneity) and quantitative features (number of bars per perforation plate and ray width). Helical thickenings are present throughout the vessel elements in three genera (Loropetalum, Altingia, Semiliquidambar) and are restricted to the vessel element tails in two genera (Corylopsis, Liquidambar). Loropetalum has helical thickenings in ground tissue fibers as well. Axial parenchyma abundance varies from scarce to relatively abundant diffuse to diffuse-in-aggregates. One clade of the tribe Fothergilleae (Distylium, Dis- tyliopsis, Sycopsis, Shaniodendron, Parrotia, Parrotiopsis) has more abundant axial parenchyma and is characterized by narrow, usually interrupted bands of apotracheal parenchyma. Nearly exclusively uniseriate rays occur in some species of Hamamelis and in Exbucklandia, Chunia, Dicoryphe, and Fothergilla. These data on extant Altingiaceae and Hamamelidaceae not only provide information relevant for systematic, phylogenetic and ecological wood anatomy and wood identification, but also give context for reviewing the fossil woods assigned to them. A new combination is proposed for the Miocene Liquidambar hisauchii (Watari) Suzuki & Watari from Japan: Altingia hisauchii (Watari) Wheeler, Baas & Lee. Key words: Altingiaceae, Hamamelidaceae, systematic wood anatomy, Eocene, fossil wood, Hamamelidoxylon.

1) Department of Forest Biomaterials, North Carolina State University, Raleigh, NC 27695-8005, U. S. A. [E-mail: [email protected]]. 2) Gangwon Forest Development Research Institute, 200-140 Chunchon, South Korea. 3) National Centre for Biodiversity Naturalis, National Herbarium of the Netherlands, P.O. Box 9514, 2300 RA Leiden, The Netherlands. Associate Editor: Frederic Lens

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INTRODUCTION

The Hamamelidaceae constitute a family of trees and shrubs, with a tropical to temperate distribution, being especially diverse in Eastern Asia. The family is placed in the Saxi- fragales, with the Altingiaceae, Cercidiphyllaceae, and Daphniphyllaceae recognized as the most closely related families within the order (APG III 2009; see also Stevens 2001-onward). Genera of the Altingiaceae (Altingia, Semiliquidambar, Liquidambar) formerly were considered members of the Hamamelidaceae. The Angiosperm Phylog- eny Website lists three subfamilies for the Hamamelidaceae: 1) Exbucklandoideae with the genera Chunia, Exbucklandia, Mytilaria, and Rhodoleia (composition according to Endress 1989), occurring in East Asia, including Assam, East Malesia to Sumatra, 2) Disanthoideae comprised of the monotypic Disanthus cercidifolius of Japan, and the largest subfamily 3) Hamamelidoideae. Li and Bogle (2001) considered Hamamelidoideae monophyletic, and their analysis of morphological and molecular features recovered three monophyletic groups within the Hamamelidoideae. They proposed recognition of two tribes within each group (see Fig. 1). There are different estimates of the number of species per genus, but only three genera (Corylopsis, Dicoryphe and Distylium) are estimated to have more than 10 species. A remarkably high proportion of the genera, 11 of 27, are monotypic.

Corylopsis (Asia) Loropetalum (Asia) Tetrathyrium (Asia) Matudaea (S. America, Mexico) Embolanthera (Asia) Maingaya (Asia) Dicoryphe (Madagascar) Trichocladus (Africa) Neostrearia (Australia) Noahdendron (Australia) Ostrearia (Australia) Eustigma (Asia) Fortunearia (Asia) Sinowilsonia (Asia) Molinadendron (Central America) Distylium (Asia) ⎫ ⎪ Distyliopsis (Asia) ⎪ ⎪ Sycopsis (Asia) ⎬Banded parenchyma ⎪ Shaniodendron (Asia) ⎪ Parrotia (Asia) ⎪ ⎪ Parrotiopsis (Asia) ⎭

Fothergilla (N. America, 1s rays only) Hamamelis (Asia: 1–3s rays; N. America: 1s rays only)

Figure 1. Phylogenetic relationships within the Hamamelidoideae. Redrawn from Li & Bogle (2001) and Radtke et al. (2005).

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The Hamamelidaceae and Altingiaceae have a fossil record dating back to the Late Cretaceous, including an inflorescence interpreted as a basal “altingioid” with pollen characters found in the Hamamelidaceae (Zhou et al. 2001) and a Late Cretaceous (Campanian) flower attributed to the tribe Hamamelideae (Magallon-Pueblaet al. 1996). Some genera now endemic to Asia (Corylopsis, Disanthus, Fortunearia) occurred in North America and Europe during the Tertiary (Manchester et al. 2009). Hamamelis and Liquidambar (Altingiaceae) are classic examples of genera with a present-day disjunct distribution (e.g., Manchester 1999). Tracing the history of the family from fossil seeds is made difficult because “seeds [of Hamameloideae] have converged on very similar morphology … some of the genera might be difficult or impossible to distinguish based on seed morphology alone …” (Manchester et al. 2009). Consequently, it is of interest to determine if any genera, tribes, or subfamilies of Hamamelidaceae can be distinguished by their wood anatomy so that fossil wood might be used to better understand the history and diversification of the Hamamelidaceae. The Kew Micromorphology database and Gregory (1994) list publications describing wood anatomy of the Hamamelidaceae and Altingiaceae. An especially useful reference, although it lacks figures, is Tang’s paper (1943), which tabulates data and includes a key to 19 genera (Altingiaceae and Hamamelidaceae). This paper apparently was a major source for the family description by Metcalfe and Chalk (1950). Subsequent relatively comprehensive treatments, with figures, are by Skvortsova (1975, 14 genera, 20 species studied) and Huang (1986, 9 Chinese genera studied).

Materials and Methods

Wood samples were obtained from various institutional wood collections. Unfortunately, some of the wood samples lack information on simultaneously collected herbarium material (see Barker 2008 for risks entailed in erroneous identifications). Following, in alphabetical order by genus within family, is a list of specimens examined and the information available on their provenance. The numbers of species per genus are from the Flora of China (FOC) (Zhang et al. 2003) and Mabberley (2008). Slides are deposited in the National Centre for Biodiversity Naturalis - National Herbarium of the Netherlands. Additional images are available on the InsideWood web site (InsideWood 2004-onwards). Images of additional samples and species on InsideWood, provided by FFPRI, Tsukuba, Japan (TWTw and courtesy of S. Noshiro), CSIRO (FPAw and courtesy of J. Ilic), National Herbarium of the Netherlands (Uw, UN) and Imogen Poole (slides at Kew, Kw) are listed below in brackets.

Altingiaceae (3 of 3 genera examined) Altingia Noronha (Evergreen trees, Indomalesia, 8–10 species, 4 examined): A. chi- nensis (Champ. ex Benth.) Oliv. ex Hance, SJRw 21920, Coll. C.L.Tso, Kwangtung, China, Fan Memorial Institute Biology — A. excelsa Noronha, TWTw 3123 (= BZFw N4472), Forest Research Institute, Bogor, Indonesia; [FPAw 10616] — A. gracilipes Hemsl., CAFw 11260, mature tree, China — A. obovata Merr. & Chun, SJRw 29562, Ngai Yuen, Hainan, China.

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Liquidambar L. (Deciduous trees, east Asia, east Mediterranean, southeast North America to northern Central America, 3–5 species, 3 examined): L. formosana Hance, CAFw 18047, mature tree, China; [TWTw 17405] — L. orientalis Miller, MADw 14115, cultivated, Riverside Co., CA, USA — L. styracifluaL., TWTw 6459, cultivated Osaka City, Japan; TWTw 15982, cultivated Forest Tree Breeding Institute, Kasahara-cho, Mito City, Ibaraki Pref., Japan; BWCw 8148; [FPAw u.45, Kw Liqstyr, Tw 52940, Uw 6759, RBHw 1447, Hw 17232]. Semiliquidambar H.T. Chang (Evergreen-deciduous trees, eastern China, 3 species, 1 examined): S. cathayensis H.T. Chang, Liu Peng s.n., Kwangtung, China, 23° N, 113° E.

Hamamelidaceae (23 of 27 genera examined) Chunia H.T. Chang (Evergreen tree, China, 1 species): C. bucklandioides H.T. Chang, Tw 41881, coll. Forest Research Institute, Guangdong, China; Liu Peng s.n., Kwangtung, China, 23° N, 113° E. Corylopsis Siebold & Zucc. (Shrub to small tree, evergreen to semi-evergreen, China, Japan, India, 7–29 species, 3 examined): C. gotoana Makino, TWTw 13872, w. ridge of 810.7 m peak, Horado Mura, Mugi Gun, Gifu Pref., Japan — C. spicata Siebold & Zucc., TWTw 6309; TWTw 6310, Asakawa Experimental Forest Hachioji City, Tokyo, Japan — C. multiflora Hance var. multiflora (syn. C. wilsonii Hemsl.), SJRw 21958, from Y. Tang, Fan Memorial Institute Biology, China. Dicoryphe Thouars (Evergreen shrub to tree, Madagascar, Comoros, 12 species, 1 examined): D. stipulacea J. St.-Hil., L.J. Dorr & L.C. Barnett 3341 (Lw), Tamatave Province, west of Foulpointe, Madagascar, branch. Disanthus Maxim. (Deciduous shrub, Japan, 1 species): D. cercidifolius Maxim., TWTw 19323, Kawachi Valley, Japan, 36° N, 136° E; [TWTw 13963]. Distyliopsis P.K. Endress (Evergreen tree, China, Laos, Malaysia, c. 6 species, 1 species examined): D. dunnii (Hemsl.) P.K. Endress, Coode 5561 (Lw), tree, north coast of Mindoro, Philippines; FFPRI 667 (IFw 22639); [FPAw ngf.6061]. Distylium Siebold & Zucc. (Evergreen shrub to small tree, east Asia, Malesia, India, c. 18 species, 5 species examined): D. lepidotum Nakai, SJRw 32151, Bonin Island, from R. Kanehira, Fukuoka, Japan — D. myricoides Hemsl., CAFw 12602, China — D. racemosum Siebold & Zucc., TWTw 16191, Yaku cho, Kumage Gun, Kagoshima Pref., Japan, 30° 20' N, 130° 36' E, DBH = 8 cm; [TWTw 12910, TWTw 15159, UN 403, USw 14122 (S. Carlquist photo) — D. stellare Kuntze, SJRw 30801, from Janssonius, Central Java — D. tsiangii Chun ex Walker, SJRw 21886, coll. Y. Tsiang, Kweichow, China, Fan Memorial Inst. Biology. Eustigma Gardner & Champion (Evergreen shrub to small tree, China, 3 species, 1 examined): E. oblongifolium Gardner & Champion, Tw 41883, from Forest Research Institute, Guangdong, China. Exbucklandia R.W. Brown (2–4 species, 2 examined): E. populnea (R.Br. ex Griff.) R.W. Brown, S.J. Lee 2975 (slide); [FPAw 12130] — E. tonkinensis (Lecomte) Hung T. Chang, CAFw 13463, mature tree, China.

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Fortunearia Rehder & E.H. Wilson (Deciduous shrub to small tree, China, 1 species): F. sinensis Rehder & E.H. Wilson, SJRw 29817, Y. Tang, Fan Memorial Institute Biology, China. Fothergilla Murray (Deciduous shrub, southeast USA, 2 species, 1 examined): F. major (Sims) Lodd., MADw 46794 (M. Nee 40413), NY Botanic Garden, NY, USA. Hamamelis L. (Deciduous shrub to small tree, east USA, east Asia, 4–6 species, 4 examined): H. japonica Siebold & Zucc., TWTw 2884, Coll. S. Noshiro, T. Fujii, T. Sugawa, Shizuoka Pref., 35° 10–13' N, 138° 06' E, diam. 7 cm; TWTw 14949, Coll. N. Seto, T. Takahashi, M. Suzuki, near Kunimiyama, Ishikawa Pref. Japan, 36° 25' N, 136° 40' E; [TWTw 14783, 18118, 18428, 18500, 18601, Kw Hamajap] — H. mollis Oliver, SJRw 32366 — H. vernalis Sargent, MADw 18320 (J.W. Thieret 1087), Washington Co., Missouri, USA — H. virginiana L., PACw 7133; PACw 7215; [Page slide 6475]. Loropetalum R.Brown (Shrub to small tree, evergreen to semi-evergreen, China, Japan, India, 2–3 species, 1 examined): L. chinense (R.Brown) Oliver, SJRw 29789, from Y. Tang, China, W-8479 from Fan Memorial Institute of Biology, coll. Chungking, Szechwan, China. Maingaya Oliver (Shrub to small tree, evergreen to semi-evergreen, Malaysia, 1 species): Maingaya malayana Oliv., KEPw 10610. Molinadendron P.K. Endress (Evergreen tree, Mexico-Central America, 3 species, 1 examined): M. hondurense (Standl.) P.K. Endress, MADw 29869 (L.L.Willliams 72839), tree, east of Tatcumbla, alt. 1500 m, Honduras, SJRw 29869. Mytilaria Lecomte (Evergreen tree, China, Laos, Vietnam, 1 species, 1 examined): M. laosensis Lecomte, Tw 41886, coll. Forest Research Institute, Guangdong, China; Liu Peng s.n., Kwangtung, China, 23° N, 113° E. Ostrearia Baill. (Evergreen tree, Australia/Queensland, 1 species): O. australiana Baill., FPAw 10073 (CSIRO), north Queensland. Parrotia C. A. Meyer (Deciduous tree, Iran, China, 2 species, 1 examined): P. persica (DC.) C.A. Meyer, FPAw 24935 (CSIRO), cultivated old Botanic Garden, Smithsonian Inst., USA; Uw 474; [UN 278]. Parrotiopsis (Nied.) C.K.Schneid. (Deciduous shrub to small tree, Himalayas, Afghanistan, 1 species): P. jacquemontiana (Decne.) Rehder, SJRw 32053, Punjab, India, 31° N, 76° E. Rhodoleia Champ. ex Hook. (Evergreen tree to shrub, China, southeast Asia, 1–10 species, 2 examined). Note: 10 species according to FOC, but PROSEA suggests genus monotypic with R. championii the only species (Soerinegara & Lemmens 1993), 1–7 species according to Mabberley (2008) — R. championii Hook f., FPAw 5145 (CSIRO); [C. Davidson 1405, S. Carlquist photos] — R. teysmannii Miq., MADw 17728 (= FHOw 3564), Malaysia. Sinowilsonia Hemsley (Deciduous shrub to small tree, China, 1 species): S. henryi Hemsley, SJRw 31988, cultivated Brooklyn Botanic Garden; Boufford 1483, small stem with pith.

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Sycopsis Oliver (Evergreen shrub to small tree, China, northeast India, 2 or 3 species, 1 examined): S. sinensis Oliver [synonym: Sycopsis formosana (Kanehira) Kanehira & Hatusima], W-3075, Taiwan, 23° N, 121° E; Cult. Botanic Garden 287, Basel, Switzerland (Lw). Tetrathyrium Benth. (1 species): T. subcordatum Benth. [syn. Loropetalum subcordatum (Benth.) Oliv.], SJRw 29816, “very small”, Y. Tang, Fan Memorial Institute Biology, China. Trichocladus Pers. (5–6 species, 2 examined): T. crinitus (Thunb.) Pers., FHOw 1552 — T. ellipticus Eckl. & Zeyh., SJRw 29441, Kilimanjaro, Tanzania, 3° S, 37° E; T. ellipticus subsp. malosanus (Baker) Verdc. [syn. T. malosanus], Tw 47283, coll. Kisimba & Muzinga, Katanga, Dem. Rep. Congo. Genera not examined: Embolanthera Merr. (2 species, SE Asia); Matudaea Lundell (2 species, central Mexico to Honduras), Neostrearia L.S. Sm. (1 species, NE Australia), Noahdendron Endress (1 species, N. Queensland). Tables 1 and 2 summarize the characteristics of the genera, based on samples we had slides of, and give for each genus its habit (tree, small tree, shrub), leaf phenology (deciduous, semi-evergreen, evergreen). Data are arranged by family, subfamily, and tribe.

Descriptions Al t i n g i a c e a e Altingia, Liquidambar, Semiliquidambar Family description (Fig. 2): Growth rings and porosity — Growth rings present and marked by a few rows of radially flattened fibers (e.g., Altingia gracilipes, Liquidambar and Semiliquidambar) or indistinct to absent (Altingia excelsa). Woods diffuse porous. Most vessels solitary; 95% solitary in Altingia obovata, but less than 85% in the other species, least (57%) in Liquidambar formosana. Solitary vessels slightly angular in outline. Vessels — Vessels narrow and typically numerous. Average tangential diameters range from 39 to 89 µm; vessel densities (vessels per mm2) range from 48 (Altingia excelsa) to 183 (Liquidambar orientalis) (see Table 2). Average vessel element lengths more than 800 µm, with lengths >1.5 mm in Altingia. Perforation plates exclusively scalariform, average number of bars most commonly between 15 and 20 (Fig. 2E). Because most vessels are solitary, intervessel pitting is infrequent, the non-vestured intervessel pits scalariform to opposite. The size and shape of vessel-ray parenchyma pits similar to intervessel pits, but usually the pits with reduced borders (Fig. 2F). Vessel-ray parenchyma pits usually confined to the square and upright marginal ray cells. Helical thickenings restricted to the tips of vessel elements in Liquidambar, and throughout the vessel elements of Semiliquidambar (Fig. 2G) and Altingia, usually faint; no helical thickenings observed in A. excelsa. Widely spaced tyloses observed in some samples of all species. Fibers — Fibers non-septate with distinctly bordered pits on both radial and tangential walls. Average fiber lengths range from 1.34 to 2.43 mm. Fiber walls medium thick (Liquidambar) to very thick (Altingia, Semiliquidambar). Helical thickenings absent. (text continued on page 409)

Downloaded from Brill.com09/29/2021 12:32:35AM via free access Wheeler, Lee & Baas — Altingiaceae and Hamamelidaceae 405 – – – – – – + CryEn – – – – – (+) (+) CryAc (continued on next page) – – – – – + + CryRc – – + + (+) (+) (+) CryR III, II Rcc II, III III (II) II, III III (II) II, I II, I

1(–2) RW 1–2(–3) 1(–2) 1–3(–4) 1(–2) 1–2(–3) 1–2(–3)

D* AP R, D* R, D* D R, D* R R, D, DA*

T FW T T T T T, vT T, T – – – – – – – HTF

– – – – – – T HTV

19–20, ir 25–27, ir 44, ir 25–26, ir 31 B/PP 20, ir 33–38, ir

I I I I P P P GR e a e e a e e a e l o i d e

i s a n t h o i d a m a m xbucklanoid D H E E. tonkinensis E. populnea Corylopsis (Shrub-smTree, decid, s–evg) (Tree, evg) Chunia (Tree, (Tree, evg) (Tree, Mytilaria Rhodoleia (Tree/Shrub, evg) evg) (Tree, Exbucklandia Disanthus (Shrub, decid)

procumbent with mostly 2–4 rows of upright and/or square marginal cells, I = Body ray cells procumbent with mostly over 4 rows of upright and/ cells. or square marginal cells. axial parenchyma cells — CryEn = Crystals in enlarged Subfamily

Subfamily CryR = Crystals in upright/square ray cells — CryRc = Crystals in chambered upright/square or procumbent ray cells — CryAc = Crystals in chambered in Crystals = CryAc — cells ray procumbent or upright/square chambered in Crystals = CryRc — cells ray upright/square in Crystals = CryR Table 1. Features of potential systematic value in Hamamelidaceae and Altingiaceae woods. 1. Features of potential systematic value in Hamamelidaceae and Table For all features: * = rare; – absent; + present; (+) variable or rare. = present, I indistinct to absent. GR = Growth rings: P B/PP number of bars per perforation plate, ir = irregular reticulate. Average = = in vessel element tails only. T = Helical thickenings in vessel elements: B throughout the body of element, HTV HTF = helical thickenings in fibers. = very thick-walled. = thin- to thick-walled, vT T = Fiber wall thickness: FW B = narrow bands, M marginal. = diffuse-in-aggregates, DA Apotracheal parenchyma: R = rare, D diffuse, = AP = Ray width (cells): mean(–max). RW Rcc = Ray cellular composition: III = Body ray cells procumbent with mostly one row of upright and/or square marginal cells, II = Body ray cells ––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––– ––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––– Family HAMAMELIDACEAE Subfamily I. Corylopsideae Tribe

Downloaded from Brill.com09/29/2021 12:32:35AM via free access 406 IAWA Journal, Vol. 31 (4), 2010 – – – – – – – – – – – + + + + + + + + + CryEn – – – – – – – – – + + + + + + (+) (+) (+) (+) (+) CryAc – – – – + + + + + + + + + + + + + + + (+) CryRc – – – – – + + + + + + + (+) (+) (+) (+) (+) (+) (+) (+) CryR III (II) III (II) II (III, I) II (III) II (I, III) II (I, III) II (I, III) II, I (III) II (I, III) II (III, I) II (I, III) II (I) II (I, III) II (I) Rcc I (II) I (II, III) I (II) I (II) I (II) I (II)

1–3(–5) 1–2(–3) 1–3(–4) 1(–2) 1–2(–3) 1–2(–3) 1, 1–2(–3) 1–2(–3–4) 1–3(–4) 1–2(–3–5) 1–2(–3) 1–2(–3) 1–3(–3) 1–2(–3) 1–2(–3) 1–2(–3) 1–2(–2) 1–3(–5) 1(–2) 1–2(–3) RW

R, D* D, DA* D, DA, (M) R, D* B*, DA, D B*, DA, D R, D* B, DA, D B*, DA, D B*, DA, D D, DA* D*, DA, B D D, DA* D D, DA* R D D, DA, B* D AP

T T, vT T, T vT T, T vT T, T vT vT T, vT T, T T T, vT T, T vT T vT vT vT T, vT FW – – – – – – – – – – – – – – – – – – – + HTF

– – – – – – – – – – – – – – – – T B B T, B T, HTV

13–17 14 16 15–17 11 11 12–14 9–15 12 12–15 15 11 13 20 11 19–47, ir 19 38 8–14, ir 38 B/PP

P P, I P, P P, I P, P I I P, I P, P P P P P P, I P, I I I I P P GR

(Shrub-smTree, dec) (Shrub-smTree, (Shrub, decid) (Tree, evg) (Tree, (Tree, decid) Liquidambar (Tree, Altingia evg–dec) Semiliquidambar (Tree, (Shrub-smTree, dec) (Shrub-smTree, Parrotiopsis Fothergilla (Shrub-smTree, evg) Distylium (Shrub-smTree, (Tree, evg) Distyliopsis (Tree, (Shrub-smTree, evg) Sycopsis (Shrub-smTree, decid) (Tree, Parrotia (Shrub-smTree, dec) Hamamelis (Shrub-smTree, (Tree, evg) (Tree, Molinadendron Sinowilsonia (Shrub-smTree, dec) Fortunearia (Shrub-smTree, (Shrub-smTree, Tetrathyrium evg) Maingaya (Shrub-smTree, evg) Dicoryphe (Tree/Shrub, evg) (Tree/Shrub, Trichocladus evg) (Tree, Ostrearia (Shrub-smTree, evg) Eustigma (Shrub-smTree, (Shrub-smTree, (Shrub-smTree, Loropetalum

Family ALTINGIACEAE Family

Tribe VI. Fothergillieae Tribe

Tribe V. Hamamelideae V. Tribe

evg–s.evg) III. Dicorypheae Tribe Tribe IV. Eustigmateae IV. Tribe ––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––– 1 continued) (Table ––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––– II. Loropetaleae Tribe evg–s.evg) –––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––

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Table 2. Selected quantitative features of Hamamelidaceae and Altingiaceae woods. For all features: – = no information; % sol = Percentage of solitary vessels (%); VF = Vessel frequency, vessels per sq. mm, mean or range of means; TD = Mean or range of means of tangential vessel lumen diameter (µm); VEL = Mean or range of means of vessel element length (µm); FL = Mean or range of means of fiber length (µm); RH = Mean or range of means of ray height in mm: mean (max).

% Sol VF TD VEL FL RH

Family Hamamelidaceae

Subfamily Exbucklandoideae Exbucklandia E. populnea 92 65 62 – – 0.6 (1.4) E. tonkinensis 59 204 43 1579 1784 0.6 (0.9) Mytilaria 71-75 112-115 45-55 1386-1945 2243-2299 0.6 (1.4) Rhodoleia 90-93 34-71 58-79 1513-2012 190-1190 0.4-0.5 (0.9-1.2) Chunia 80-84 123-125 48-49 1498-1795 2255-2302 0.5 (1.1)

Subfamily Disanthoideae Disanthus 84 257 28 1096 1407 0.6 (1.3)

Subfamily Hamameloideae Tribe I. Corylopsideae Corylopsis 80-87 212-266 31-39 1256-1313 1702-1936 0.6-0.9 (1.4-2.3)

Tribe II. Loropetaleae Loropetalum 98 101-109 36-40 1211-1369 1676-1876 0.7 (1.3-1.9) Tetrathyrium 92 98-210 28-37 1309 1662 0.6 (1.2) Maingaya 96 57 76 1590 2056 0.5 (1.0)

Tribe III. Dicorypheae Dicoryphe 96 89 43 1678 1969 1.0 (2.4) Trichocladus 91-97 113-244 27-40 1125-1179 1505-1515 0.5-0.6 (1.0-1.8) Ostrearia 88 109 49 2053 2446 1.8 (4.1)

Tribe IV. Eustigmateae Eustigma 89 227 31 1300 1595 0.5 (1.3) Fortunearia 93 160 34 – – 0.4 (0.8) Sinowilsonia 89 164 31 – – 0.4 (0.9) Molinadendron 90 114 44 1085 1843 0.7 (1.3)

Tribe V. Hamamelideae Hamamelis 66-94 296-402 27-36 911-1103 1193-1461 0.5-0.7 (1.3-1.8)

Tribe VI. Fothergillieae Distylium 91-95 78-137 31-51 1059-1082 1523-1590 0.5-1.2 (1.2-2.8) Distyliopsis 92 105 51 1323 – 0.8 (2.0) Sycopsis 91-95 62-166 39-54 859-1316 1338-2068 0.4-0.5 (0.9-1.3) Parrotia 90 244 30 877 1273 0.3 (0.7) Parrotiopsis 94 118 39 959 1307 0.4 (0.7) Fothergilla 83 398 29 1021 1353 0.3 (0.7)

Family Altingiaceae Altingia 74-95 (48) 90-145 43-56 (89) 1362-1874 1754-2437 0.5 (1.4) Semiliquidambar 84 113 55 1325 2025 0.5 (1.0) Liquidambar 57-73 139-183 39-57 923-1501 1341-2128 0.6 (1.1)

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A B C

D F G

Figure 2. Altingiaceae – A: Diffuse porous wood, traumatic gum canals, Liquidambar styraciflua, Hw 17232. – B: Diffuse porous wood, very thick-walled fibers, traumatic gum canals,Altingia excelsa, TWTw 3123. – C: Diffuse and diffuse-in-aggregates axial parenchyma, very thick-walled fibers, Semiliquidambar cathayensis, Liu Peng s.n.. – D: Rays commonly 3-seriate, occasional portions 4-seriate; scalariform and opposite intervessel pits, Liquidambar orientalis, MADw 14115. – E & F: Altingia gracilipes, CAFw 11268. – E: Scalariform perforation plates. – F: Vessel-ray parenchyma pits. – G: Prismatic crystal in inflated ray cell, helical thickenings in vessel element, Semiliquidambar cathayensis, Lw s.n. — Scale bars = 200 µm in A; 100 µm in B, C, D, E; 50 µm in F, G.

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Axial parenchyma — Parenchyma rare (Liquidambar) to diffuse (Semiliquidambar (Fig. 2C), Altingia p.p.) to diffuse-in-aggregates (Altingia p.p.). The number of cells per strand generally 5–8. Rays — Rays narrow, mostly 1–3(–4)-seriate. Heterocellular, with procumbent body cells and usually 2–4 marginal rows of square to upright cells. Ray parenchyma cell walls with abundant pits; walls usually nodular, and appear almost disjunctive in marginal upright cells that are markedly narrower (as viewed in radial section) than the procumbent cells in the ray. Traumatic axial canals sometimes present, in long tangential lines, seen in some samples of Altingia and Liquidambar (Fig. 2A, B). Examination of more specimens of Semiliquidambar may show their occurrence in this genus as well. Crystals — Solitary crystals in square /upright ray parenchyma cells relatively common in Semiliquidambar with crystalliferous cells sometimes enlarged (Fig. 2G), occasional crystals in square/upright ray cells of Altingia; crystals not observed in any sample of Liquidambar or reported in the literature.

Ha m a m e l i d a c e a e Family description (Fig. 3–6): Growth rings and porosity (Fig. 3) — Growth rings distinct or indistinct to faint; most deciduous shrubs of the temperate zone with distinct growth rings (e.g., Corylopsis, Fortunearia, Sinowilsonia, Hamamelis, Fothergilla); most of the evergreen trees with indistinct growth rings (e.g., Exbucklandia, Chunia, Maingaya, Ostrearia). Growth rings marked by radially flattened latewood fibers. Diffuse porous, except forCorylop- sis (Fig. 3A) and Fothergilla whose vessel diameters decrease from earlywood to latewood and appear semi-ring porous. Vessels predominantly solitary; more than 90% solitary in Rhodoleia, Loropetalum, Maingaya, Dicoryphe, Trichocladus, Fortunearia, Molinadendron, Distylium, Distyliopsis, Parrotia, Parrotiopsis, Sycopsis; more than 80% solitary in Chunia, Disanthus, Corylopsis, Ostrearia, Eustigma, Sinowilsonia, Fothergilla; more than 70% solitary in Mytilaria. Solitary vessels usually somewhat angular in outline, but more rounded to oval in Molinadendron and Rhodoleia. Vessels — Vessels narrow and typically numerous; average tangential diameters range from 27 to 79 µm, with the narrowest (less than 50 µm) vessels in the shrubs and the widest in the trees (e.g., Maingaya, Rhodoleia). Vessel frequencies (vessels per mm2) range from 34 (Rhodoleia) to 402 (Hamamelis), with more than 100 in most species (see Table 2). Average vessel element lengths almost always more than 800 µm, frequently more than 1.5 mm, and reaching more than 2 mm in Ostrearia. Perforation plates scalariform (Fig. 4A–D), The average number of bars most commonly between 10 and 15, but averages of more than 20 occur in Corylopsis (31–38), Dicoryphe (38), Exbucklandia (31–54), Mytilaria (25–26), Ostrearia (38) and Rhodoleia (25–27), per- forations occasionally irregular (Fig. 4B). Because most vessels are solitary, intervessel pitting is infrequent, pits non-vestured and scalariform (Fig. 4E) to opposite (Fig. 4B). Vessel-ray parenchyma pits horizontally elongated, and often with reduced borders (Fig. 6F). Vessel-ray parenchyma pits usually confined to the square and upright ray cells (text continued on page 414)

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A B C

D E F

Figure 3. Cross sections of Hamamelidaceae. – A: Vessel diameter decreasing throughout the growth ring, Corylopsis gotoana, TWTw 13872. – B: Diffuse porous wood with indistinct growth ring bound- ary, Exbucklandia tonkinensis, CAFw 13463. – C: Diffuse porous wood, vessel multiples present, Ostrearia australiana, FPAw 10073. – D: Distinct growth ring, vessels angular in outline, axial parenchyma diffuse and as occasional cells touching vessels, Molinadendron hondurense, MADw 29869. – E: Diffuse porous wood, solitary angular vessels, diffuse and diffuse-in-aggregates axial parenchyma common, Dicoryphe stipulacea, Dorr & Barnett 3341. – F: Axial parenchyma commonly in bands, growth rings distinct, Distylium racemosum, TWTw 16191. — Scale bars = 200 µm in A, C, E, F; 100 µm in B, D.

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A B C

D E F G

Figure 4. Perforation plates and pitting in Hamamelidaceae. – A: Multiple perforation plate, fibers with distinctly bordered pits,Corylopsis spicata, TWTw 6310. – B: Multiple perforation plates, opposite intervessel pits, Corylopsis gotoana, TWTw 13872. – C: Scalariform perforation plate, fiber pits distinctly bordered, Exbucklandia tonkinensis, CAFw 13463. – D: Scalariform perforation plate, <15 bars, Loropetalum chinense, SJRw 29789. – E: Scalariform intervessel pits, Distyliopsis dunnii, Coode 5561 (Lw). – F: Scalariform perforation plates, elongate vessel ray parenchyma pits, Sycopsis sinensis, W-3075, Taiwan. – G: Helical thickening in vessel element tip, Corylopsis gotoana, TWTw 13872. — Scale bars = 50 µm in A, B, C, D, F; 25 µm in E; 15 µm in G.

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A B C

D E F

Figure 5. Ray features in Hamamelidaceae. – A: Rays exclusively uniseriate, except for rare biseriate portions, Chunia bucklandioides, Tw 41881. – B: Rays with alternating uniseriate and biseriate portions and tendency for uniseriate and biseriate portions to be of same width, Molinadendron hondurense, MADw 29869. – C: Rays 1–2-seriate, Sycopsis sinensis, W-3075, Taiwan. – D: 1–2(–3)-seriate heterocellular rays, body ray cells circular in outline, axial parenchyma strands, Fortunearia sinensis, SJRw 29817. – E: Markedly heterocellular rays, with alternating sections of procumbent and upright ray cells, crystals in chambered axial parenchyma and chambered ray parenchyma cells, Fortunearia sinensis, SJRw 29817. – F: Rays 1–2-seriate heterocellular rays, with long uniseriate portions, uniseriate and biseriate portions frequently alternate, Ostrearia australiana, FPAw 10073. — Scale bars = 100 µm in A–F.

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A B C

D E F

Figure 6. Miscellaneous ray and crystal features. – A: Ray parenchyma cell walls thick-walled, sometimes nodular, Disanthus cercidifolius, TWTw 13923. – B: Ray with inflated crystalliferous cell, Eustigma oblongifolia, Tw 41883. – C: Crystals in chambered ray cells, Loropetalum chinense, SJRw 29789. – D: Crystals in chambered axial parenchyma, Distyliopsis dunnii, IF 22739. – E: Ray with single marginal row of upright cells, vessel-ray parenchyma pits in marginal row. Height of upright cells approx. twice that of the procumbent cells, Exbucklandia tonkinensis, CAFw 13464. – F: Vessel-ray parenchyma pits with reduced borders, height of marginal upright cells more than twice that of procumbent cells, Mytilaria laosensis, Tw 41886. — Scale bars = 100 µm in B, D, E; 50 µm in A, C, F.

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(Fig. 4F, 6A, E). Helical thickenings occur in the tips of vessel elements in Corylopsis (Fig. 4G), and throughout the vessel elements of Loropetalum. Tang (1943) reported helical thickenings in Hamamelis, but we did not observe them. Fibers — Fibers non-septate with distinctly bordered pits on both radial and tangential walls. Average fiber lengths range from 1.19 to 2.48 mm. Within the small sample we examined, fiber length variation was as expected with the longest fibers (>2 mm) in trees, Mytilaria, Rhodoleia, Chunia, Ostrearia, Distyliopsis. Most Hamamelidaceae have medium thick-walled fibers (Fig. 3B, D), very thick-walled fibers (Fig. 3E, F) char- acterize genera of tribe Dicorypheae (Dicoryphe, Ostrearia, Trichocladus) and also occur in Distylium, Distyliopsis, and Loropetalum. Fibers with helical thickenings occur in Loropetalum. Axial parenchyma — Parenchyma abundance varies from rare to diffuse to diffuse- in-aggregates to narrow bands (Fig. 3). Most abundant, with diffuse-in-aggregates to narrow bands, in Distylium, Distyliopsis, Parrotia, Parrotiopsis, and Sycopsis, all members of tribe Fothergilleae. The number of cells per strands generally 5–8 (Fig. 5D), but often over 8. Rays (Fig. 5) — Rays narrow and heterocellular throughout the family, mostly 1–2-seriate, occasionally 3-seriate, with rare partially 4-seriate rays in Mytilaria, Dis- tylium p.p., Distyliopsis, and Sycopsis. Nearly exclusively uniseriate rays occur in Exbucklandia, Chunia, Dicoryphe, Hamamelis p.p., and Fothergilla. Ray parenchyma cell walls have abundant pits; walls are usually nodular, and appear almost disjunctive in the marginal upright cells that are markedly narrower (as viewed in radial section) than the procumbent cells in the ray. Upright cells 2× to >4× as high as the procumbent ray cells. Total average ray heights generally less than 1 mm, but >1 mm in Ostrearia, and also in Dicoryphe and Distylium stellare, both of which commonly have alternating uniseriate and 2–3-seriate portions. Rays with procumbent body cells and marginal rows of upright and/or square cells, frequently 2–4 marginal rows, but rays with 1 marginal row and >4 rows also occur. Vertical ray fusion occurs at varying frequency. Although ray composition varies within single radial sections, and even individual rays may have a single marginal row of square to upright cells on one side and 2–4 rows on the other side, the predominance of rays with either one, two to four, or over four marginal rows is diagnostic, often at the genus or even higher clade level (ray types I–III, Table 1). Rays are numerous, usually more than 12 per mm. Crystals (Fig. 6B, C, D) — Crystals not observed in Exbucklandia, Fothergilla, or Corylopsis gotoana, but present in all other genera as well as in other species of Corylopsis. Crystals in non-chambered ray parenchyma cells, chambered ray parenchyma, and less commonly in chambered axial parenchyma, enlarged crystalliferous cells observed in Chunia, Eustigma, Fortunearia, Distylium, and Parrotiopsis. Crystal occurrence variable, from common to rare in species with crystals observed.

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DISCUSSION Related Saxifragalean Families The Altingiaceae (ALT) and Hamamelidaceae (HAM) have many wood anatomical features in common with the closely related Cercidiphyllaceae (CDP) and Daphniphyl- laceae (DPH). The difficulties in distinguishing woods of these families have been noted by Brazier and Franklin (1961) and in the paleobotanical literature (e.g., Mathiesen 1932; Sakala & Privé-Gill 2004). All four families have wood with mostly solitary vessels which are narrow, numerous, and often angular in outline, exclusively scalariform perforation plates, scalariform-opposite intervessel pitting, scalariform vessel- ray parenchyma pits with slightly reduced borders, non-septate fibers with distinctly bordered pits, narrow heterocellular rays and apotracheal axial parenchyma. Table 3 compares selected features of these four Saxifragalean families. The Altingiaceae can be distinguished from the Cercidiphyllaceae and Daphniphyllaceae because the latter two families consistently have more bars per perforation plate. However, perforation plates with more than 40 bars occur in Exbucklandia and Corylopsis of the Hamamelidaceae, thus the distinctions between the Hamamelidaceae and the Cercidi- phyllaceae and Daphniphyllaceae are not clear-cut. Traumatic axial canals have only been observed in the Altingiaceae.

Table 3. Comparison of selected features of the Cercidiphyllaceae (CDP), Daphniphyllaceae (DPH), Hamamelidaceae (HAM), and Altingiaceae (ALT). Bars = number of bars per perforation plate, for CDP – total range, for DPH, HAM, ALT – range of averages; Exc. 1s rays = rays nearly exclusively uniseriate; Crystals, AP = chambered axial parenchyma, RP = ray parenchyma, RPc = chambered ray parenchyma; Tr. Canals = traumatic canals. — *Metcalfe & Chalk (1950), **Carlquist (1982).

Family Bars Exc. 1s rays Crystals Tr. Canals

CDP* 20–50 No Rare, RP No DPH** 37–96 No Rare, AP No HAM 8–44 Yes / No Yes/ No, AP, RP, RPc No ALT 14–17 No Yes / No Yes / No

Altingiaceae Phylogenetic analyses using molecular data found Altingia nested within Liquidam- bar and so it has been suggested that it might be appropriate to merge all Altingiaceae species into a single genus (Shi et al. 2001). It has been hypothesized that Semi- liquidambar is a hybrid of Altingia and Liquidambar (Bogle 1986; Ickert-Bond et al. 2005). However, Liquidambar and Altingia are distinct morphologically (Ickert- Bond et al. 2005); there are some wood anatomical differences as well (Table 1). Liquidambar wood does not have crystals, axial parenchyma is rare, while Altingia and Semiliquidambar woods have crystals in ray cells, and axial parenchyma is diffuse to diffuse-in-aggregates. Morphological differences between Liquidambar and Altingia have been hypothesized to be related to their evolution in temperate vs. subtropical

Downloaded from Brill.com09/29/2021 12:32:35AM via free access 416 IAWA Journal, Vol. 31 (4), 2010 to tropical environments (Ickert-Bond et al. 2007). The wood anatomical differences between these two genera also are consistent with different environmental histories: tropical woody plants in general having more parenchyma, longer vessel elements, and crystals being more frequent (Wheeler et al. 2007). The Indonesian Altingia excelsa is the only species of Altingiaceae whose vessel elements lack helical thickenings.

Fossil woods of Altingiaceae Fossil woods assigned to Liquidambar and Liquidambaroxylon are reported from Asia (Suzuki & Hiraya 1989; Suzuki & Terada 1996), Europe (Burgh 1964; Gottwald 1992; Greguss 1969; Iamandei & Iamandei 1998; Sakala et al. 1999; Sakala & Privé-Gill 2004), and North America (Prakash & Barghoorn 1961; Roy & Stewart 1971; Wheeler & Dillhoff 2009). Some are referred to as Liquidambar sp. or Liquidambaroxylon sp. Differences between the named fossil wood species of Liquidambar and Liquidambar- oxylon seem slight and are based on variations in vessel diameter, density, ray size, all features known to vary within a species and within a single tree. The differently named species seem more a reflection of different geographic sources and investiga- tors, rather than of significant differences in anatomy. It is difficult to compare them, as some descriptions are incomplete. One species of Altingioxylon is reported from south central Asia (Kramer 1974) (see Gregory et al. 2009 for a full list with synonyms). Liquidambar hisauchii (Watari) Suzuki and Watari (1994) originally was assigned to the Theaceae (Ternstroemiacinium hisauchii Watari 1943), but the sample has traumatic gum canals, a feature unknown for the Theaceae (Deng Liang & Baas 1990). Thus, the wood subsequently was assigned to Liquidambar. However, this Japanese fossil wood has large crystalliferous cells, and this feature is not known to occur in extant Liquidambar. Given that traumatic canals and enlarged crystalliferous cells occur in Altingia, the Japanese wood’s characteristics are more consistent with that genus than with Liquidambar. Suzuki and Watari also noted that the fossil’s rays were wider (to 4-seriate) than typical of extant Liquidambar, which also would be consistent with a relationship with Altingia. Consequently, we propose a new combination Altingia hisauchii (Watari) Wheeler, Baas & Lee. Yamamoto and Chadwick (1982) reported multiple samples of Liquidambar wood from the early middle Eocene of Yellowstone National Park. Superficially the Yellow- stone woods resemble Liquidambar as they have narrow, numerous, mostly solitary vessels and have exclusively scalariform perforation plates, but because the vessel-ray pits are small and not horizontally elongate they are more likely related to Myricaceae or Symplocaceae (Wheeler, Yamamoto & Chadwick, work in progress). Melchior (1998) reported Liquidambar from the Paleocene of South Carolina, which would be the oldest record of wood of the genus. This wood has traumatic canals and likely belongs to the Altingiaceae; however, the description lacks details that confirm its identify as Liquidambar; unfortunately, the thin sections of this wood cannot be located.

Subfamily Exbucklandoideae, Hamamelidaceae Helical thickenings in vessel elements were not observed in samples of this subfamily we examined, although Tang (1943) and Skvortsova (1975) reported they rarely

Downloaded from Brill.com09/29/2021 12:32:35AM via free access Wheeler, Lee & Baas — Altingiaceae and Hamamelidaceae 417 occurred in vessel element tips in Rhodoleia. Axial parenchyma consistently is rare. Within the subfamily, based on the material we examined and on information from the literature, it seems that the four genera in this subfamily can be distinguished on the basis of ray width and crystal occurrence. The samples of Exbucklandia we examined have almost exclusively uniseriate rays and lacked crystals as did the 13 specimens of Exbucklandia that Tang (1943) examined. The number of bars per perforation plate averages over 30; up to 54 according to Tang (1943). Chunia also has nearly exclusively uniseriate rays, but has crystals in normal, chambered, and enlarged ray cells. In Rhodoleia crystals occur in axial parenchyma cells as well as in ray cells. Mytilaria has crystals only in regular ray cells, and rays, although mostly 1–3-seriate, do reach 4-seriate. More samples of Mytilaria and Rhodoleia should be examined to confirm that these are consistent differences, especially as Skvortsova’s (1975) figures that show only small areas of tangential sections of Rhodoleia parvipetala and R. teysmannii show only uniseriate rays.

Subfamily Disanthoideae The monotypic Disanthus, a deciduous shrub, is the only genus in this subfamily. Its vessel elements are narrower, more numerous, and shorter than vessel elements of the Exbucklandoideae, whose members are evergreen and reach tree size. Rays often have more than 4 upright/square marginal rows. These quantitative differences between the two subfamilies as well as differences in ray structure most probably are related to differences in habit. Tang (1943) examined two samples, vessel element lengths were somewhat shorter (700–900 µm), but otherwise our observations are similar to his.

Subfamily Hamameloideae, Tribe Corylopsoideae Li and Bogle (2001) found this monotypic tribe to be basal in the subfamily. Accord- ing to the Flora of China, there are 29 species of Corylopsis, 19 of which are endemic to China. All species apparently are deciduous shrubs to small trees. As Figure 3A shows, growth rings are distinct, and the wood is semi-ring porous, this is a feature not seen in the other genera of Hamamelidaceae, except for some Fothergilla samples. Quantitative characteristics are similar for the samples of the four Corylopsis species we examined, the six species that Tang (1943) examined, and the two (C. spicata, C. gotana) described in the FFPRI database. Vessel frequencies average more than 200 per sq.mm, mean vessel tangential diameter is less than 40 µm. This genus has a relatively high number of bars per perforation, averaging more than 30 in the samples we examined. Tang (1943) reported 25–57 bars; Skvortsova (1975) observed 25–54 bars in C. wilsonii, 23–36 bars in C. spicata, and 15–45 bars in C. pauciflora. Helical thickenings were observed in vessel element tips of all species.

Subfamily Hamameloideae, Tribe Loropetaleae Loropetalum and the monotypic Tetrathyrium are closely related according to Li and Bogle (2001). Feng et al. (1999) and Zhang et al. (2003) submerged Tetrathyrium into Loropetalum. There are wood anatomical differences between the samples of these

Downloaded from Brill.com09/29/2021 12:32:35AM via free access 418 IAWA Journal, Vol. 31 (4), 2010 genera that Tang (1943) and we examined. The number of bars per perforation plate of Tetrathyrium (synonym: Loropetalum subcordatum) is double that of Loropetalum chinense. Helical thickenings do not occur in vessel elements or fibers ofTetrathyrium, but they do in Loropetalum chinense. Crystalliferous ray parenchyma cells are often enlarged in Loropetalum, also illustrated by Skvortsova (1975). The wider vessels and lower vessel density of Maingaya, a tree native to Malaysia, compared to Loropetalum and Tetrathyrium are consistent with the differences in habit and habitat of the genera. Most rays of the three genera in this tribe that we examined had more than 4 marginal rows of square/upright cells. We did not have access to samples of the two other genera in this tribe, Matudaea (native to Mexico and northern South America) and Embolanthera (Vietnam and the Philippines).

Subfamily Hamameloideae, Tribe Dicorypheae There are two groups in this tribe endemic to the Southern Hemisphere (Endress 1989; Li & Bogle 2001). One group comprised of Dicoryphe (Madagascar) and Trichocladus (Africa), the other group comprised of the Australian genera Neostrearia, Noahdendron, and Ostrearia. No wood samples of Neostrearia and Noahdendron were available to us. Trichocladus has fewer bars per perforation plate (8–14) and shorter rays (average < 0.6 mm) than either Dicoryphe or Ostrearia (38 bars; rays >1 mm). Skvortsova (1975) reported for Ostrearia a remarkably high number of bars per perforation plate (50–100). It is likely that this count included scalariform intervessel pits in vessel element tails. We counted 34 and 44 bars in the two perforation plates visible in her Plate X, fig. 4. Thick-walled fibers and rays with mostly 4 or more marginal rows char- acterize this tribe.

Subfamily Hamameloideae, Tribe Eustigmateae According to Endress (1989), there are three genera in this tribe: the East Asian Eustigma, Fortunearia, and Sinowilsonia. The molecular analysis of Li and Bogle (2001) supported the inclusion of the Central American Molinadendron into this tribe and they found it closely allied to Sinowilsonia. Our observations of the Asian species are similar to those made by Tang (1943). Crystals are relatively common in Eustigma and Fortunearia and crystalliferous cells are sometimes enlarged differentiating their woods from the other two genera. Axial parenchyma is somewhat more abundant in Fortunearia. Fu and Gao (1992) compared the wood anatomy of Sinowilsonia to that of Corylopsis, Distylium, Fortunearia, and Hamamelis and concluded that its wood anatomical characteristics supported placing Sinowilsonia and Fortunearia in the same clade. There are no wood anatomical characteristics of the Central American Molinadendron that would argue against its inclusion in this otherwise East Asian tribe, but its suite of characteristics is also found in other tribes (see Table 1).

Subfamily Hamameloideae, Tribe Fothergilleae Except for the North American Fothergilla, genera in this tribe are Asian. Li and Bogle (2001) recovered Fothergilla as sister to the other genera. The woods of Fother- gilla are distinct from other genera in this tribe, they have nearly exclusively uniseriate

Downloaded from Brill.com09/29/2021 12:32:35AM via free access Wheeler, Lee & Baas — Altingiaceae and Hamamelidaceae 419 rays, crystals were not observed, and axial parenchyma is rare. This contrasts with the other genera, which have rays 1–2–3 (4) cells wide, commonly have crystals, and axial parenchyma is relatively abundant, sometimes in narrow interrupted bands. Tang’s (1943) observations of Distylium, Fothergilla, Parrotia, and Sycopsis found these same differences. Fang and Deng (1996) examined wood of Parrotia subaequalis, described under its synonym Shaniodendron subaequale, and found its anatomy (especially the abundance of axial parenchyma) consistent with placement in the tribe Fothergilleae. These differences in wood anatomy between Fothergilla and other members of its tribe are as great or greater than the wood anatomical differences between any two tribes in the Hamamelidaceae. Within the Hamamelidaceae, axial parenchyma bands are unique to the Fothergilleae (all genera, but Fothergilla).

Subfamily Hamamelidoideae, Tribe Hamamelideae Hamamelis is the sole genus in this tribe, which is sister to the tribe Fothergilleae. The present-day geographic distribution of Hamamelis is an example of the classic eastern Asia and eastern North America disjunct distribution. Li et al. (2000) investigated the relationships of the species and concluded that the Japanese species (H. japonica) was more closely related to the North American species (H. virginiana, H. vernalis, H. mexi- cana) than to the Chinese species (H. mollis). Ray width differences lend some support to this proposal. The H. mollis samples we examined had the widest rays in the genus, reaching 3-seriate and the crystalliferous ray cells were non-chambered. Seven of eight H. japonica FFPRI samples have predominantly uniseriate rays and Skvortsova’s (1975) key used exclusively uniseriate rays as a distinguishing feature of H. japonica. Some samples of H. vernalis (MADw 18320) and H. virginiana (Page s.n., slide 6475) have (nearly) exclusively uniseriate rays.

Fossil woods of Hamamelidaceae Species of Hamamelidoxylon are reported from the Cretaceous of Japan (Takahashi & Suzuki 2003, 2005), Tertiary of Europe (occurrences reviewed by Crawley 2001), and Miocene and Eocene of the Pacific Northwest, USA (Wheeler & Manchester 2002; Wheeler & Dillhoff 2009). Features of Hamamelidoxylon, as diagnosed by Lignier (1907), include solitary vessels, scalariform perforation plates, apotracheal diffuse parenchyma, scalariform vessel-ray parenchyma pits, and exclusively uniseriate (very rarely biseriate) rays. Subsequently, fossil woods with 2–3-seriate rays have been assigned to the genus and it has come to be used for woods with the general features of the family, e.g. the Japanese Cretaceous Hamamelidoxylon obiraense (Takahashi & Suzuki 2003) and the German Eocene H. daphniphylloides (Gottwald 1992). These two species and the Eocene H. uniseriatum (Wheeler & Manchester 2002, Oregon, USA) have a relatively high number of bars per perforation plate (average >30 bars). As reflected in its name, Gottwald noted that H. daphniphylloides shares many features with the Daphni- phyllaceae. The type specimen of H. daphniphylloides is a small diameter stem (<1 cm in diameter) with attached secondary phloem with characteristics said to be consistent with both the Daphniphyllaceae and Hamamelidaceae. The anatomical features reported for Hamamelidoxylon daphniphylloides, as well as the details visible in the plates, are

Downloaded from Brill.com09/29/2021 12:32:35AM via free access 420 IAWA Journal, Vol. 31 (4), 2010 not sufficient for establishing that this wood has features unique to the Hamamelidaceae. It is possibly an extinct genus of woody Saxifragales. Distylium chiharu-hirayae Suzuki & Terada (1996; Jeong et al. 2004) and Distylium sp. (Suzuki & Hiraya 1989) are reported from the Miocene of Japan. The co-occurrence of uniseriate bands, crystals in chambered axial parenchyma and chambered ray cells which are often swollen, and markedly thickened fiber walls indicate that this fossil belongs to tribe Fothergilleae, and, as established by Suzuki and Terada, is most similar to Distylium because parenchyma bands are relatively common. The Eocene Corylopsites groenlandicus Mathiesen (1932) resembles Cercidiphyllum as well as Corylopsis. This Eocene wood has crystals in both ray and axial parenchyma. Mathiesen did not observe crystals in extant Cercidiphyllum wood, so he used the absence of crystals in the fossil to infer a relationship with Corylopsis. Subsequently Swamy and Bailey (1949) observed the sporadic occurrence of crystals in upright ray parenchyma cells of Cercidiphyllum leading to the suggestion that the Greenland wood might be Cercidiphyllum. This suggestion was prompted because leaves resembling Cercidiphyllum are common in early Tertiary beds of the Northern Hemisphere. How- ever, the occurrence of crystals in axial parenchyma indicates that the affinities are more likely with Corylopsis. Moreover, recent work shows that Corylopis also had an extensive fossil record in the Northern Hemisphere (reviewed by Manchester 1999; Manchester et al. 2009), including seeds from the lower Eocene of southern England and western North America and leaves from the lower Eocene of Washington State, USA (Radtke et al. 2005).

Conclusions

The wood anatomy of the closely related Altingiaceae and Hamamelidaceae is similar, with no consistently occurring feature that distinguishes them, although traumatic canals only occur in two genera of Altingiaceae, and uniseriate rays and perforation plates with an average number of bars more than 25 only occur in some genera of Hamamel- idaceae. Within the Hamamelidaceae, there is overlap in the wood anatomical features of the three subfamilies (Exbucklandoideae, Disanthoideae, Hamameloideae), but unique combinations of features distinguish some tribes and genera of Hamameloideae. Tribe Corylopsideae (Corylopsis) has semi-ring porous wood, scalariform perforation plates with an average bar number of more than 30, helical thickenings at the tips of vessel elements. Loropetalum has helical thickenings the whole length of the vessel element and in fibers. It and other members of the tribe Loropetaleae have rays that frequently have more than 4 marginal rows of square to upright cells and usually have thick-walled fibers. Tribe Fothergilleae, except for Fothergilla, has relatively abundant axial parenchyma that is diffuse-in-aggregates to banded. It is noteworthy that Fothergilla (North America), tribe Fothergilleae, is more similar wood anatomically to Hamamelis (Asia and North America), tribe Hamamelideae, than to the Asian genera of tribe Fothergilleae. Differences between Loropetalum and Tetrathyrium in number of bars per perforation plate and occurrence of helical thickenings and crystals support keeping these two genera of tribe Loropetaleae separate.

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The genera described in the literature as being deciduous have distinct growth rings. Some evergreen species have indistinct growth rings; some have distinct growth rings. The Southern Hemisphere tribe Dicorypheae, all evergreen species, has indistinct growth rings, while the evergreen genera of tribe Eustigmateae have distinct growth rings. We did not have data on the height and diameter of the source plants for the wood samples we examined, so relied on literature descriptions. Most genera in the Hamamelidaceae are described as shrubs to small trees. Chunia, Mytilaria, Exbuck- landia (Exbucklandoideae), Ostrearia (Dicorypheae), Molinadendron (Eustigmateae), Distyliopsis, Parrotia (Fothergilleae) are described as trees only and Disanthus (Dis- anthoideae) and Fothergilla (Fothergilleae) described as shrubs only. For the trees, the average tangential diameter is 47 µm and the average number of vessels per square mm is 135; for the shrubs, the respective values are 28.5 µm and 327. These types of differences between vessel diameter and density of trees (wider and fewer) and shrubs (narrower and more numerous) are of general occurrence.

REFERENCES

APG III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot. J. Linnean Soc. 161: 128–131. Barker, J. 2008. Disconnection and reconnection: misconceptions and recommendations pertain- ing to vouchers in wood science. IAWA J. 29: 425–437. Bogle, A.L. 1986. The floral morphology and vascular anatomy of the Hamamelidaceae: subfamily Liquidambaroideae. Ann. Missouri Bot. Gard. 73: 325–347. Brazier, J.D. & G.L. Franklin. 1961. Identification of hardwoods. A microscope key. Forest Products Research Bulletin No. 46: 96 pp. Burgh, J. van der. 1964. Hölzer der Niederrheinischen Braunkohlenformation. 1. Hölzer der Braunkohlengrube ‘Anna’ zu Haanrade (Niederländisch-Limburg). Acta Bot. Neerl. 13: 250–301. Carlquist, S. 1982. Wood anatomy of Daphniphyllaceae. Brittonia 34: 252–266. Crawley, M. 2001. Angiosperm woods from British Lower Cretaceous and Palaeogene deposits. Special Papers in Palaeontology 66: 100 pp. Deng Liang & P. Baas. 1990. Wood anatomy of trees and shrubs from China. II. Theaceae. IAWA Bull. n.s. 11: 337–378. Endress, P.K. 1989. A suprageneric taxonomic classification of the Hamamelidaceae. Taxon 38: 371–376. Fang, Yan-Ming & Mao-Bin Deng. 1996. Wood anatomy of Shaniodendron subaequale (Hama- melidaceae) and its systematic implication. J. Plant Resources and Environment 5: 50–54. Feng, Y-x., Z-d. Chen, X-q. Wang, K-y. Pan & D-y. Hong. 1999. A taxonomic revision of the Loropetalum-Tetrathyrium complex and its systematic position in the Hamamelidacae, based on morphology and ITS sequence data. Taxon 48: 680–700. Fu, Z. & S. Gao. 1992. A systematic study of the genus Sinowilsonia wood anatomy. Acta Bot. Boreal. Occident. Sin. 12: 188–192. Gottwald, H. 1992. Hölzer aus Marinen Sanden des Oberen Eozän von Helmstedt (Niedersach- sen). Palaeontographica B 225: 27–103. Gregory, M. 1994. Bibliography of systematic wood anatomy of dicotyledons. IAWA Journal, Suppl. 1: 265 pp. Gregory, M., I. Poole & E.A. Wheeler. 2009. Fossil dicot woods - an annotated list of all species names with a full bibliography. IAWA Journal, Suppl. 7: 220 pp.

Downloaded from Brill.com09/29/2021 12:32:35AM via free access 422 IAWA Journal, Vol. 31 (4), 2010

Greguss, P. 1969. Tertiary angiosperm woods in Hungary. Akademiai Kiado, Budapest. Huang, G. 1986. Comparative anatomical studies on the woods of Hamamelidaceae in China. Acta Sci. Nat. Univ. Sunyatseni 1: 22–28. Iamandei, S. & E. Iamandei. 1998 [1999]. Liquidambaroxylon pravalense n.sp., in the pyrrho- clastics of Pravaleni, Metalliferous Mts. Acta Hort. Bot. Bucurest. 27: 223–232. Ickert-Bond, S.M., K.B. Pigg & J. Wen. 2005. Comparative infructescence morphology in Liquidambar (Altingiaceae) and its evolutionary significance. Amer. J. Bot. 92: 1234 –1255. Ickert-Bond, S.M., K.B. Pigg & J. Wen. 2007. Comparative infructescence morphology in Altingia (Altingiaceae) and discordance between morphological and molecular phylogenies. Amer. J. Bot. 94: 1094–1115. InsideWood. 2004-onwards. Published on the internet: http://insidewood.lib.ncsu.edu/search Jeong, E.K., K. Kim, J.H. Kim & M. Suzuki. 2004. Fossil woods from Janggi Group (Early Mio- cene) in Pohang Basin, Korea. J. Plant Research 117: 183–189. Kramer, K. 1974. Die Tertiären Hölzer südost-Asiens (unter Ausschluss der Dipterocarpaceae). Palaeontographica 144B: 45–181. Li, J.-H. & A.L. Bogle. 2001. A new suprageneric classification system of Hamamelidoideae based on morphology and sequences of nuclear and chloroplast DNA. Harvard Papers Bot. 5: 499–515. Li, J.-H., A.L. Bogle, A.S. Klein & M.J. Donoghue. 2000. Phylogeny and biogeography of Hamamelis. Harvard Papers Bot. 5: 171–178. Lignier, O. 1907. Végétaux fossiles de Normandie. IV. Bois divers (1). Mém. Soc. Linn. Norman- die 22: 237–333 + pl. x v i i –x x i i i . Mabberley, D.J. 2008. Mabberley’s Plant-book: A portable dictionary of plants, their classification and uses. Ed. 3. Cambridge University Press, New York, Cambridge. Magallon-Puebla, S., P.S. Herendeen & P.K. Endress. 1996. Allonia decandra: floral remains of the tribe Hamamelideae (Hamamelidaceae) from Campanian strata of southeastern USA. Plant Syst. Evol. 202: 177–198. Manchester, S.R. 1999. Biogeographical relationships of North American Tertiary floras. Ann. Missouri Bot. Gard. 86: 472–522. Manchester, S.R., Z-D. Chen, A-M. Lu & K. Uemura. 2009. Eastern Asian endemic seed plant genera and their paleogeographic history throughout the Northern Hemisphere. J. Systemat- ics and Evolution 47: 1–42. Mathiesen, F.J. 1932. Notes on some fossil plants from East Greenland (Cape Dalton, Turner Sound, Cape Brewster, and Sabine Island). Meddel. Grønland 85 (4): 1–62. Melchior, R.C. 1998. Paleobotany of the Williamsburg Formation (Paleocene) at the Santee Rediversion site Berkeley County, South Carolina. In: A.E. Sanders (ed.), Paleobiology of the Williamsburg Formation (Black Mingo Group; Paleocene) of South Carolina, U.S.A. Trans. Amer. Philosoph. Soc. 4 (4): 49–121. Metcalfe, C.R. & L. Chalk. 1950. Anatomy of the Dicotyledons. 2 vols. Clarendon Press, Ox- ford. Prakash, U. & E.S. Barghoorn. 1961. Miocene fossil woods from the Columbia basalts of Central Washington. J. Arnold Arbor. 42: 165–203. Radtke, M.G., K.B. Pigg & W.C. Wehr. 2005. Fossil Corylopsis and Fothergilla leaves (Hama- melidaceae) from the lower Eocene flora of Republic, Washington, USA, and their evolutionary and biogeographic significance. Int. J. Plant Sciences 166: 347–356. Roy, S.K. & W.N. Stewart. 1971. Oligocene woods from the Cypress Hills Formation in Sas- katchewan, Canada. Can. J. Bot. 49: 1867–1877. Sakala, J. & C. Privé-Gill. 2004. Oligocene angiosperm woods from northwestern Bohemia. IAWA J. 25: 369–380.

Downloaded from Brill.com09/29/2021 12:32:35AM via free access Wheeler, Lee & Baas — Altingiaceae and Hamamelidaceae 423

Sakala, J., C. Privé-Gill & J.-C. Koeniguer. 1999. Silicified angiosperm wood from the Dangu locality (Ypresian of the Gisors region, Eure, France): the problem of root wood. C.r. Acad. Sci., Paris, Sci. Terre et Planètes 328: 553–557. Shi, S., Y. Huang, Y. Zhong, Y. Du, Q. Zhang, H. Chang & D.E. Boufford. 2001. Plant Syst. Evol. 230: 13–24. Skvortsova, N.T. 1975. Comparative morphological study of representatives of the family Hamamelidaceae R.Br. and their phylogenetic relationships. In: L.Yu Budantsev (ed.), Voprosy sravnitel’noi morfologii semennykh rastenii: 7–24. Soerianegara, I. & R.H.M.J. Lemmens (eds.). 1993. Plant Resources of South-East Asia. 5 (1). Timber trees: major commercial timbers. Pudoc Scientific Publishers, Wageningen. 610 pp. Stevens, P.F. 2001-onwards. Angiosperm Phylogeny Website. Version 9, June 2008. Suzuki, M. & C. Hiraya. 1989. Fossil wood flora from the pumice tuff of Yanagida Formation (Lower Miocene) at Mawaki, Noto Peninsula. Ann. Sci. Kanazawa Univ. 26: 47–75. Suzuki, M. & K. Terada. 1996. Fossil wood flora from the Lower Miocene Yanagida Formation, Noto Peninsula. IAWA J. 17: 365–392. Suzuki, M. & S. Watari. 1994. Fossil wood flora of the Early Miocene Nawamata Formation of Monzen, Noto Peninsula, Central Japan. J. Plant Research 107: 63–96. Swamy, B.G.L. & I.W. Bailey. 1949. The morphology and relationships of Cercidiphyllum. J. Arnold Arbor. 30: 187–210. Takahashi, K. & M. Suzuki. 2003. Dicotyledonous fossil wood flora and early evolution of wood characters in the Cretaceous of Hokkaido, Japan. IAWA J. 24: 269–309. Takahashi, K. & M. Suzuki. 2005. Cretaceous dicotyledonous fossil woods from Hokkaido, Japan, and early evolution of wood characters. Jap. J. Histor. Bot. 13: 55–77. Tang, Y. 1943. Systematic anatomy of the woods of the Hamamelidaceae. Bull. Fan Mem. Inst. Biol. Peking (NS) 1: 8–62. Watari, S. 1943. Studies on the fossil woods from the Tertiary of Japan. IV. A new silicified wood of the Ternstroemiaceae from the Pliocene of Yokohama City. Jap. J. Bot. 13: 261–267. Wheeler, E.A., P. Baas & S. Rodgers. 2007. Variations in wood anatomy. A global analysis based on the InsideWood database. IAWA J. 28: 229–258. Wheeler, E.A. & T.A. Dillhoff. 2009. The Middle Miocene wood flora of Vantage, Washington, USA. IAWA Journal, Suppl. 7: 101 pp. Wheeler, E.A. & S.R. Manchester. 2002. Woods of the Middle Eocene Nut Beds flora, Clarno Formation, Oregon, USA. IAWA Journal, Suppl. 3: 188 pp. Yamamoto, T. & A. Chadwick. 1982. Identification of fossil wood from the Specimen Creek area of the Gallatin Petrified Forest, Yellowstone National Park, Montana, U.S.A. Part II. Angiosperms. J. San-iku Gakuin Junior College 11: 49–66. Zhang, Z., H. Zhang & P.K. Endress. 2003. Hamamelidaceae. Flora of China 9: 18–42. Zhou, Z-K., W.L. Crepet & K.C. Nixon. 2001. The earliest fossil evidence of the Hamamelida- ceae: Late Cretaceous (Turonian) inflorescences and fruits of Altingioideae. Amer. J. Bot. 88: 753–766.

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Wood anatomy news

Beauty in Wood. Macroscopic to Microscopic. Available from http://www.lulu.com USD 29.95 + postage and handling.

This 30-page photo book was created in response to a question that David Mabberley (author of The Plant-Book) asked Peter Gasson (Kew, U.K.) late in 2009 – Are the wood anatomists going to do anything for Pieter Baas’s birthday? What to do? Answer: assemble a collection of attractive photographs of wood as a surprise late birthday present for Pieter and give it to him at the IAWA-IAWS meeting in Madison in June 2010.

“Beauty in Wood” is that present. It features photographic contributions from over 30 wood anatomists worldwide. Images range from the macroscopic (attractive grain patterns in modern and fossil wood) through light microscopic (features of systematic and functional importance) through electron microscopic (including SEMs and TEMs of pit structure and development as well as details of 70 million year old charcoals). This book illustrates not only some of the diversity and beauty of wood structure, but also some of the diversity of techniques used to study it. Each group of photos is accompanied by a few references that provide additional information on the subject matter illustrated and an entry into the relevant literature.

Given the positive response to the book at the IAWA-IAWS meeting, it seemed a good idea to make the book public, with profits to go to IAWA. The book was assembled on the Lulu Press website, which publishes books and calendars on demand, so that this project did not cost the coordinators (Steven Jansen, Peter Gasson, and Elisabeth Wheeler) anything other than time.

Beauty in Wood is now available from Lulu Press, http://www.lulu.com (Search for books and “Beauty in Wood”). The secure Lulu site accepts credit card payments, with discounts for orders of five or more copies. “Beauty in Wood” would make a perfect holiday present for colleagues and friends interested in natural history or plant anatomy, and would be useful for university departments to have on hand as an inspiring reference for wood science and plant anatomy courses. And remember all of this is to support IAWA! Elisabeth Wheeler

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