INTRODUCTION

Delimitation of species in Taxus has been a taxonomic problem due to neglect in applying standards (types) and rules (ICBN, Greuter et al. 2000) to the chosen names and to difficulties in determining species morphological characteristics. Taxus wallichiana Zuccarini is one example of three that I will discuss. It was described by Zuccarini (in Siebold & Zuccarini 1843) to clarify its relationship to the genus Torreya, which had been described only five years earlier based on the discovery of T. taxifolia Arnott (1838) in Florida. Siebold & Zuccarini (1843) realized that Taxus nucifera L. in Japan belonged to Torreya (T. nucifera (L.) Siebold & Zuccarini 1843, 1846), whereas collections by Wallich and others in the Himalayas identified as “Taxus nucifera?” (e.g., Wallich 6054A) were not that species. Siebold & Zuccarini (1843) also saw a similar problem with another species in Japan “T. cuspidata Sieb.& Zuccar.” validly published in footnote by specific reference to [a description (ICBN, Art. 32.4)] T. baccata in Thunberg (1784, Fl. Jap. 275, “foliis solitariis, linearibus, cuspidatis, approximatis”), which they also felt was distinct from T. baccata Linnaeus (1753, Sp. Pl. 1040,“foliis approximatis”) in Europe, T. globosa Schlechtendal (1838) in Mexico, and T. canadensis Marshall (1785) in northeastern temperate North America; undoubtedly, this disjunct geographic distribution justified each of them as distinct. Zuccarini did not cite specimens, but did provide a Latin description, an illustration, and a reference to another illustration and name (“Taxus nucifera?”) in Wallich (1826).

As Taxus was discovered in other regions, species differentiation became more of a problem. This included new species—T. brevifolia Nuttall (1849) from western North America, T. floridana Nutt. ex Chapman (1860) from Florida, and others from Asia erroneously placed in the genus Cephalotaxus—C. sumatrana Miquel (1859) from Sumatra and C. celebica Warburg (1900) from Celebes (Pilger 1903). Pilger (1903), in a monograph of Taxus, decided there was only one species, T. baccata.

Pilger (1903), however, recognized six former species as subspecies. In addition to ssp. baccata, these included: 1—wallichiana, 2— cuspidata, 3—brevifolia, 4—canadensis, 5— floridana, and 6—globosa; the latter two subspecies were later considered to hardly differ from ssp. canadensis (Pilger 1916, 1926). He also described two new varieties (Pilger 1903; under ssp. cuspidata), var. latifolia and var. chinensis, and recognized 21 forms of baccata (Pilger 1903, 1916). He applied morphological characters that seem to best fit a phytogeographic separation of the taxa; for example, ssp. wallichiana was characterized by lax branching and persistent bud-scales, and by leaves more or less falcate, rigid, narrowly linear, 2.5–3.0 cm long, notably arcuate at base, and acuminate or acute; 12 representative specimens were then cited from eastern India to Sumatra. He also cited synonyms with reference to the source publications where further citations of specimens may be found, including presumed types in cases where only one specimen is cited, but types were not indicated as this generally was not the practice then.

Although it might be argued that the lack of any significant variation in cone structures of Taxus hardly justifies recognition of more than one species (Pilger 1903), other taxonomists still maintained geographically distinct populations as species (Cheng & Fu 1978; Florin 1948a; Hu 1964; Rehder 1919, 1936, 1940; Wilson 1916), sometimes describing new species without a clear understanding of types or nomenclatural rules.

This has led to much confusion to interpreting species of Taxus, particularly T. chinensis (Pilg.) Rehder (1919) and T. wallichiana. For example, Rehder (1936), upon discovering that Tsuga mairei Lemée & H. Léveillé (Léveillé 1914) belonged to Taxus, treated it as a synonym of T. chinensis; the ICBN (Art. 11.4) requires that the earlier epithet, mairei, be adopted. S. Y. Hu (in Liu 1960) made the combination, but excluded Cephalotaxus celebica and C. sumatrana because their types were not available or known to her. Then Cheng & Fu (1978) established T. chinensis var. mairei, an illegitimate combination that had been earlier introduced invalidly (Cheng et al. 1975; ICBN Art. 33.2). This was transferred—T. wallichiana var. mairei (Lemée & H. Lév.) L. K. Fu & Nan Li (in Li & Fu 1997)—but this too is illegitimate; the authors failed to account for types of T. baccata var. sinensis A. Henry, C. celebica Warburg, and that of Cephalotaxus sumatrana Miq—earlier valid names that must be considered (ICBN Art. 11.5), especially since the epithet mairei does not have legitimacy below the rank of species (see also Art. 45.3). However, the circumscription of this taxon was emended by arbitrarily excluding names of Taxus outside of the Flora of China (Fu et al. 1999).

Florin (1948a), who on one hand recognized Henry 7155 as the type for his new combination, T. wallichiana var. chinensis, did not clearly identify the type for T. wallichiana when he made that combination.  Additionally, he distinguished a new species, T. speciosa, for which he cited an earlier legitimate name whose epithet should have been adopted (Cephalotaxus celebica Warb.) as later done by Li (1963), whereas de Laubenfels (1978, 1988) applied an earlier name, Cephalotaxus sumatrana Miq. (Pilger 1903, 1916), but also excluded T. wallichiana for reasons that are not clear. W-c. Cheng & Fu (1978), along with C-y. Cheng (1975), described T. yunnanensis because they assumed from literary accounts that T. wallichiana occurred mostly in the western Himalayas (Li & Fu 1997), whereas Hu (1964) had correctly recognized it. Li & Fu (1997), attempting to rectify the error, decided that T. yunnanensis should be placed in synonymy, and in so doing published another superfluous name—T. fuana Nan Li & R. R. Mill for T. contorta Griffith—the name for the common yew in the western Himalayas.

Besides nomenclatural confusion, herbarium specimens themselves are often confusing, and no doubt this has contributed more confusion. Labels are sometimes attached to the wrong specimens (e.g., Wallich 6054A), or label data are not always consistent for the same collection found in different herbaria (e.g., Griffith 5002), or the same number has been applied to many specimens from a wide geographic area (e.g., George Forrest in Yunnan; Cox 1945), or different letters may be appended to differentiate collectors or geographical variants (e.g., Wallich 6054/A, B, C, D, & E), or mixed specimens are often mounted on the same sheet.

Examples for all of these have been seen on Wallich specimens of T. wallichiana regarded as original material, which might be equivalent to syntypes and isosyntypes except for the fact that no specimens were cited by Zuccarini in Siebold & Zuccarini (1843). These specimens may be labeled 6054A, or 6054B, or without number; one from München has a label indicating it was collected in Japan, but it could have been collected only in the Himalayas based on its morphology. Parlatore (1868), Pilger (1903), and Nasir & Ali (1987) interpreted both Wallich 6054A and 6054B to belong to T. wallichiana, while others recognized only 6054A (Hara et al. 1978) as that species. Wallich 6054 also included further designations of C, D, and E for which I have not seen specimens; these probably belong to other genera. Additionally, Wallich 6055 has reportedly been collected in northwestern Himalaya by [Dr. George] Govan & Webb, and identified Taxus baccata L.? (Anonymous 1913); I have not seen this either. Most specimens of Wallich 6054A (from Nepal) belong to T. wallichiana, while most Wallich 6054B (from Kumaon) are T. contorta.

This paper clarifies the taxonomy of three confusing species of Taxus—T. wallichiana Zucc., T. contorta Griff., and T. chinensis (Pilg.) Rehder—that occur from the Himalayas to southwestern China.  Their (lecto)types are designated, morphological features are described, and taxonomic relationships are discussed.  Clarification is needed because of interest in the anticancer compound taxol (Kingston et al. 1990; Kingston 1996; Wani et al, 1971) and related taxoids in Taxus (Appendino 1995; Croom 1995) that are being reported under species names without any indication as to how they are distinguished.

METHODS

Stafleu & Cowan (1976–1988) were consulted for location of types, other specimens of historical relevance to this study, and references. I studied more than 1000 herbarium specimens (A, BH, BM, BOLO, E, GH, K, M, NA, NY, P, PE, PH, S, U, US; Holmgren et al. 1990) of Taxus from throughout the natural range of the genus to assess morphological variation in characters that involve branches, bud-scales, leaves, and cones. Each specimen was photographed using 35 mm color film in a Nikon camera with 35 mm and 60 mm lenses. From each specimen one mature leaf was soaked in water (8-16 hrs) and then transversely and longitudinally sectioned in the mid regions, using a single-edge razor blade and dissecting needle as a guide; the longitudinal sections consisted of the ventral (abaxial) epidermal layer (with parenchyma scraped-off), usually from 0.5–2.0 mm, occasionally the entire abaxial surface of the leaf. These sections were examined under magnifications of 100×, 250×, and 400× (using a Nikon binocular microscope) for cell shape, number of stomata rows, number of cells marginal to stomata bands, and presence, position, and distribution of papillae. The results were sketched and described on 3 × 5 inch packets. A temporary slide of the sections and photographs of the herbarium specimen were retained for each packet. Additionally, many leaves from a single plant of selected species were also studied. This included, top, middle, and lower branches of T. brevifolia from trees in California and Oregon, young and old shoots of Taxus spp. from Taiwan and cultivation, and of cultivars related to T. cuspidata.

This study initially attempted to identify morphological features that would satisfy the geographical taxa concept mentioned earlier in the introduction (Spjut 1992, 1993; Spjut in Hils 1993); however, this concept could not be justified for specimens from Eurasia.  Herbarium specimens were then classified according to pattern recognition of shared morphological features.  These involved characters of branching pattern, persistence of bud-scales, texture of bud-scales, length of bud-scales, color of branchlets, leaf arrangement, leaf shape, leaf thickness, leaf color, leaf curvature lengthwise, leaf curvature across adaxial surface, midrib on adaxial surface, leaf margins, shape of cones in bud, at maturity, and others.  In May 1994 a list of characters and their character states were created in DELTA (DEscriptive Language TAxonomy) format as done in other studies (see Spjut 1996).  This list included 85 morphological characters, 44 of which involved leaf anatomy. Specimens were reviewed for scoring character states in each of 15 species items.  Variations in certain character features that appeared significant were treated as item variants; 23 were identified.  Species descriptions were then generated using DELTA software and were subsequently modified by word processing software.  The DELTA format was maintained until May1996 when it was decided that changes in keys and descriptions, which had been done frequently, were much easier for this author  to make looking at real language descriptions rather than in numerical codes.

Author names of plants for species of Taxus are spelled out in full when first mentioned, in references to publications, and in literature cited; elsewhere, they—along with authors for species names in other genera—are abbreviated according to Brummitt & Powell (1992).  Literature for nomenclatural citations is abbreviated according to Stafleu & Cowan (1976–1988), except journals.  Reference to color is based on comparison of specimens or leaves with a commercially available color chart  (Berol Prismacolcor), which shows 120 different colors on a single page, each with a descriptive name.

A major loan from Harvard (A, GH), and smaller loans from Kew (K), Bailey Hortorium (BH), München (M), and Utrecht (U) had to be returned though the curator at the U. S. National Arboretum (July 1996) before this study was completed because the USDA Agricultural Research Service could no longer support this research. Consequently, these specimens were annotated (in adnot.); this included designation of types and notations for names not yet published (“Spjut ined.”). However, this study continued in World Botanical Associates with further reviews of specimens at the British Museum of Natural History (BM), Kew (K), U.S. National Arboretum (NA), Paris Museum of Natural History (P), Academy of Natural Sciences of Philadelphia (PH), and U.S. National Herbarium (US), while other loans were obtained from the Royal Botanic Garden at Edinburgh (E) and Swedish Museum of Natural History in Stockholm (S). Additionally, I have studied more than 400 fresh specimens from England, France, Sweden, China (Sichuan, Hubei, Gansu, “northeast”), Korea, Japan, Philippines, Taiwan (Hualien, 11 locations; “Tong-shi,” “Dong-shi”) Mexico, Canada (BC), and United States (CA, OR, WA, ID, MT, OH, WI, NH, ME, FL), and also photographed and reviewed living yew collections at Kew Gardens in England, National Arboretum in Washington, D.C., and Secrest Arboretum in Wooster, Ohio.

Needles from a number of herbarium specimens were subjected to DNA extraction, but there was little extractable DNA (Krupkin, pers. comm.). Employing RFLP; Vance & Krupkin (1993) have distinguished chloroplast DNA among T. baccata, T. brevifolia, T. canadensis, T. cuspidata, and T. floridana.

Species of Taxus are differentiated by vegetative features, usually two or more character attributes that appear to be correlated; however, taxonomic weighting is given to single character attributes where it was necessary to maintain taxonomic clarity in related species.  Analysis is largely subjective, but see phytogeographical data for number of leaf stomata rows and number of marginal cells that border stomata bands (defined by the absence of papillae), and for leaf divergence.

TAXONOMIC PHILOSOPHY

Taxus cones show only minor differences; thus, evidence for reproductive isolating mechanisms is difficult to evaluate.  This is further complicated by the dioecious habit for most species except T. canadensis. 

One of the yew’s reproductive strategies is to survive by vegetative reproduction.  Yew trunks have been reported be several thousand years old (Loudon 1844; Silber and deWolf 1970; Voliotis 1986), and when they fall they do not necessarily die; they can live on by regenerating from branches that root (layering), or by stump sprouts (Loudon 1844)—until, perhaps, a climate change forces them out, or to adapt.

Despite the lack of morphological or chemical reproductive isolating mechanisms in Taxus, species status appears warranted for populations exhibiting morphological differences in vegetative features that appear to have evolved over millions of years (Spjut 2007a).

Substantial polymorphism exists within species populations of Taxus as reported for T. brevifolia (Doede et al. 1993), and three genetically different groups have been recognized in British Columbia (El-Kassaby and Yanchuk 1994); however, morphological data for genetically distinct populations or individuals was not studied.  Nevertheless, morphological differences among related North American species of Taxus are relatively minor compared to their relatives in Asia (Spjut 1993, 1998a; Spjut in Hils 1993). This is not surprising in view of one of the world’s richest gymnosperm areas lies in Sichuan, China, where 88 species in 27 genera occur, among which there are 14 endemic species represented by “living fossils” in Cathaya, Gingko, and Metasequoia, and there are other notable relict species in Abies, Amentotaxus, Cephalotaxus, Cryptomeria, Cunninghamia, Cycas, Keteleeria, Pinus, Picea, Podocarpus, Torreya, and Tsuga (Anonymous 1994); California, by comparison, has 60 species in 14 genera of which 7 species are endemic (Hickman 1993). Many relicts occur in southwestern China because the climate remained relatively mild during the Pleistocene, whereas in Europe and North America the glacial climate caused greater devastation to their floras (Anonymous 1994).

The disjunct distribution of extant Taxus in North America (Ferguson 1978) might be correlated with paleobotanical evidence since the Oligocene (27–38 mya)—as summarized in numerous historical accounts (e.g., Axelrod 1975, 1976, 1986; Frederiksen 1994, 1995; Graham 1972, 1973, 1993, 1999; Srivastava 1994; Wolfe 1975), but evolution of Taxus may date back to the Triassic (Florin 1958, 1963; Harris 1976; Meyen 1984; Miller 1976, 1977). A summary of the fossil record by Gaussen (1979) listed 11 extinct species of Taxus from Eurasian Tertiary deposits, three from Mesozoic Eurasian deposits, and various indeterminate species, including three records from North American mid Tertiary deposits.  However, identifications of Taxus fossils are not always reliable (Harris 1976). Taxus jurassica Florin, for example is clearly not Taxus; it has opposite leaves, not spirally arranged leaves (Harris 1976). Several other related species from Jurassic and Cretaceous deposits have narrow stomata bands similar to T. jurassica (Florin 1958; Kvaček 1986), and in my opinion are not Taxus. Kvaček (1986) mentioned several other species, T. inopinata Givulsec, and T. grandis Krausel and described two others (Taxus sp. 1, Taxus sp. 2) from Lower Miocene and Upper Plicoene deposits that I cannot differentiate from modern T. canadensis, which I also recognize to occur naturally in Europe and W. Asia (Spjut 2000).  The genus Taxus is defined by its phyllotaxy of spirally inserted leaves with hypostomatic papillose bands (Dilcher 1969; Florin 1931; Kvaček 1986).

From my extensive study of leaf characters, I have seen many examples of continuous variation that would be best explained by gradual evolution, while I have also seen many examples of different character combinations involving habit, phyllotaxy, seed shape, and leaf anatomical features that indicate frequent hybridization (Spjut submitted).  In flowering plants, the evolution of vicarious species is often attributed to cyclic climatic changes as glaciers advanced and retreated during the past 2.5 million years (e.g., Prance 1982); in Taxus such changes may have done more to promote hybridization between formerly distinct species. Evidence for such hybrids has been reported in other conifers, e.g., Picea rubens Sarg. and P. mariana (Mill.) Britton, Sterns & Poggenb. (Bobola et al. 1996), Picea glauca (Moench) Voss, and P. engelmannii Parry ex Engelm. (Wilkinson et al. 1971), and species of Pinus (Axelrod 1986).

Recently, Manchester (1994) described T. masonii from seed in Middle Eocene deposits of Oregon. It was distinguished from seed of extant species by the lenticular shape, which might be compared to that of T. chinensis and English yew. Another extinct species, T. engelhardtii Kvaček (1986), from a late Oligocene deposit in Bohemia (Czech Republic), is similar to extant T. mairei in phyllotaxy and to T. chinensis in leaf anatomy; however, rare extant specimens of Taxus from China also show these combined features. The taxonomic differences in species of Taxus described below are believed to have evolved before the Miocene (5+ mya) based upon comparative morphological data for extant plants on North America, Europe, and Asia (Spjut 1993, 1998a, 2000a, b, c), and the occurrence of T. canadensis in North America, Europe, and W Asia (Spjut 2000a, b, c).

KEY

The results are species descriptions as defined by a key based on data from dried specimens; the distinction in color may not be the same for live material (Spjut 2000c, submitted).  The key presented here pertains only to the three species in this paper. All key features should be considered equally except where weighted (bold type).  Other related species are excluded from the key, but their relationships are discussed. Phyllotaxy is spiral but leaves often twist along their petioles and blades to spread ± in two ranks.  Distribution data are from herbarium specimens and the locations are correlated with references to vegetation types that cited Taxus. The vegetation types mentioned are not standardized. Nomenclature and references for the three species and their varieties are discussed according to priority of publication: (1) T. wallichiana, (2) T. contorta, and (3) T. chinensis.

1. Dried leaves with loose, dark reddish parenchyma cells, resembling
broken egg shells, usually falling out when leaves are sectioned;
stomata in (5-) 7–8 (-11) rows/band; leaf epidermal cells often elliptical
in transverse sections, especially in NW Himalayan plants; seed
subcylindrical to subglobose (Fig. 2)…………..……................................…… T. contorta—2

Fig. 4: Taxus chinensis, with pointed angled seeds,
Sino-Amercan Exped. 1854, from Guizhou, China (GH).  

1. Dried leaves with adhesive reddish to greenish
parenchyma cells; stomata 11–21 rows/band; leaf
epidermal cells angular or elliptical in x-section;
seed conical, gradually tapering to apex from
mid region (Fig. 4)………………………………..…………. 3

4. Leaves linear (Fig. 7, 9–10); not long tapering to the margin in x-section;
abaxial surface with epidermal cells in x-section not enlarged, generally
shorter than those on adaxial surface, 15–25 µm wide,
decreasing in length near margins; papillae mostly alternate on midrib and
marginal cells, or along cell walls (Fig. 6); NE India, Nepal, Bhutan,
Myanmar, Sichuan, Yunnan………………..…...…T. wallichiana var. wallichiana

NOMENCLATURE, DESCRIPTION, AND DISCUSSION

1. Taxus wallichiana Zuccarini, in Siebold & Zuccarini, Abh. math.-phys Cl. k. Bayer. Akad. Wiss. (München) 1 (3): 803, Tab. 5 (Fig. 9). 1843. Taxus baccata subsp. wallichiana (Zucc.) Pilger in Engler, Pflanzenreich IV (5): 112. 1903. Taxus baccata var. wallichiana C. K. Schneider ex Silva Tarouca, Freiland-Nadelgehölz. 276. 1913. No specimens cited by Zuccarini, original material at M: specimens from NEPAL, INDIA. Lectotype (designated by Spjut in adnot. 23 Mar 1995, in J. Bot. Res. Inst. Texas 1: 230. 2007): specimen with male cones, “Herb. Zuccarini”—India: eastern, communicavit Wallich, year 1835—Wallich s.n. (Fig. 10, M!). Other related material: Wallich 6054A, p.p.,“Kumaon,” with Schultes label, in adnot. Torreya nucifera, Taxus nucifera, and Taxus wallichiana, one large branch with mature male cones (M!). Duplicates of Wallich 6054 (see below): GH! K! NY! P! PH! S! 

1a. Var. wallichiana. Shrub or tree to 20 m or more; branchlets yellowish green, or reddish orange, becoming gradually darker in age, or abruptly dark purplish (maroon) in 2^nd yr; bud-scales persistent at base of 1–2 yr branchlets, these pale yellowish to brownish red (maroon), usually numbering 5–10, overlapping in 3–4 ranks, the lower scales loosely adnate, ovate, ca. 0.5 mm long, upper scales spreading, concave and incurved towards apex (cuspidate), to 1 mm long. Leaves ± evenly spreading but not evenly distributed, linear, acuminate, straight to commonly falcate, 1.5–3.5 cm long, 1.5–2.5 mm wide, usually ca. 350 µm thick, thinner in plants of NE India bordering Myanmar and Tibet, glossy (resinous) dark green above, paler below, convex on upper surface to a rounded midrib, less concave below to a flush to slightly rounded midrib, becoming revolute near margins (80–90º), especially in upper third of dried leaves; upper (adaxial) epidermal cells angular in x-sect., rectangular, quadrangular, or taller than wide, commonly ca. 25 µm diam., or 20–30 µm tall and 20–40 µm wide; abaxial epidermis papillose except for  (2-) 4 (-6) cells across from margins, or 4–6 (-8) cells wide in plants from Mt. Emei (Sichuan), the epidermal cells usually not inflated, short rectangular, 1.5–3 times (×) longer than wide (l/w),  gradually becoming quadrate or short trapezoidal but not particularly narrower towards margin, occasionally long rectangular near margins in plants from Nepal (4–8× l/w) but then not tall, usually 8–12 µm tall, (10-) 15–25 µm wide, similar in shape and length on midrib, or often narrower and longer on midrib, 3–10× l/w; papillae usually distinct, often aggregate, positioned more marginally than medially in 2–3 alternate rows, or medial in some specimens but then cells not inflated; stomata usually 11–18 (-21) rows in yellowish green to reddish orange bands (dried leaves), the stomata rows generally decreasing in number from east to west, palisade parenchyma 1 row, generally 50–70 µm long; spongy parenchyma cells ellipsoidal to bone-like, forming a periclinal net, not falling apart when sectioned. Male cones maturing on 1^st and 2^nd yr branchlets, ca. 1.5 wide and 4 mm long in bud, to 2 mm wide and 6 mm long at maturity. Female cones maturing on 1^st or 2^nd yr or older branchlets; seed conical in upper third, 6 mm long, 4 mm diam., slightly thickened at base, recessed at attachment point, with red or yellow aril.

Wallich yew. Distribution: E Himalayas to SW China; montane coniferous forests with Picea, Abies, Tsuga, or broadleaved evergreen forests of Lithocarpus, or Quercus, (1500-) 2300–3200 m; C & E Nepal, Bhutan, NE India (Assam, Manipur, Khasia Hills, West Bengal), Myanmar, China (SE Tibet, Sichuan, Yunnan). In Nepal evidently occurring abundantly with Abies spectabilis (D. Don) Spach on limestone (Stainton 1972), and in Bhutan apparently scattered from Ha to Mongar districts (Grierson and Long 1983).

Representative Specimens—Nepal: Arun Valley, N of Kutiar, 9000 ft., Stainton et al. 1398 (BM); Eastern Nepal, Duon Kosi, Chaunrikarua, 27º40'N, 86º40'E, 9500 ft, Stainton et al. 6601 (BM); Stainton et al. 4496 (BM); Solukhumbu Dist., Dudh Kosi River, Lamujo to Chumava, 2450 m, Hideo Tabata et al. 10585 (A, BM); Thulo Kobar to Ran Thanti, 83º45’ E, 28º24’N, 2600 m, Ohba et al. 8310264 (BM). Bhutan: Tunle La, near Kinga Rapden, 27º27’N, 90º37’E, 11,000 ft, Ludlow et al. 18672 (BM, GH); Thimphu Dist., summit of Dochong La, 27º29’ 89º45, Tsuga/Rhododendron forest, 3110 m, Grierson & Long 4417 (A); 7500 ft, Cooper & Bulley 2600 (BM); above Motithang directly W of Thimphu, Bartholomew & Boufford 3917 (A); illegible, 9000-10,000 ft, Griffith 2006 (BM, K, p.p., with T. sumatrana). India—West Bengal: Singalila Range, along trail from Rimbick to Sandakphu, 8400 ft, very large tree with circumference near base of 11’6", Voss et al. 148 (NA). Assam: without additional locality data, Griffith 2706 (BM). Khasia [Meghalaya]: 4500 ft, Vale of rocks, C. B. Clarke 436743 (BM); Khasia, 5000–6000 ft, J. D. Hooker 77, 87 (GH, p.p., lower left of 3 specimens on one sheet; P; PH).  East Himalaya, without locality, Griffith 5002 (P: 2 sheets, one distributed by K, the other ex Herb. Bunge). Manipur: Seriphari, 10,000 ft, Jan. 1882, G. Watt 5955 (GH, P), 6208 (P), 6493 (P). Sirhoi: 8000 ft, small tree, scattered in forest, not common, only conifer above 7000 ft, Kingdon Ward 17271 (A, BM). India (without specific locality data), K. Biswas 439 (A, US). Myanmar (Burma): Northern: Adung Valley, 27–28º30'N, 97–98º30'E, 7000-8000 ft, shrub, of dry forest, Kingdon Ward 9375 (A); Adung Valley, 6000 ft, shrub, scattered through the thickets along river, Kingdon Ward 9214 (A, BM). China—SE Tibet: Cha Yu, 2370 m, tree ca. 15 yrs in age, occurring with Pinus sp., ChaYu Forestry Bureau Staff Expert CYW007 (ChaYu Forestry Bureau). Sichuan: Mt. Emei [Shan], 2300 m, Yu-shih Lin 1196 (A, US); 2400 m, T.T. Yu 482 (A), 492 (A); W. P. Fang 3945 (A); W.K. Hu 8166 (A); T.C. Lee 4465 (A); Pan-lan-shan W of Kuan Hsien, 5000–6000 ft, Wilson 4053 (A, BM, US). Yunnan: Salween, Kiukiang Divide, Shawlongwang, 2600 m, among mixed forest in valley, tree 40–60 ft, bark purplish brown, thinly scaly, leaves dark green above, yellowish beneath, seed brownish green, half covered by the coral red fleshy aril, rare, Nov 1938, T.T. Yu 21036. Cultivated—India: Dehra Dun, Bot. Gard. Darjeeling, Raijada 18919 (A). Specimen data questionable: Uttar Pradesh (Kumaon): Blinkworth s.n., in adnot. T. virgata (BM), probably not collected by Blinkworth and probably not collected in Kumaon.

Duplicates of Original Material (Isosyntypes) by institution: GH: label with handwriting similar to Wallich, “Taxus nucifera Wall.” “Napalia.” s.n. K: Four sheets. (1) with two specimens, the larger specimen has a pasted label below it with handwriting “6054a” and no indication of locality data, the smaller one is a single branch with mature seed, correctly annotated T. wallichiana by S. G. Harrison, but it is not 6054A, or not a type since it is not from a male plant; (2) two specimens, one large specimen with an imprinted stamp nearby—Herb. Hookerianum, with handwriting similar to Wallich, 6054/A, Nepal, accompanied by a smaller specimen in left corner, with a large label below, Watt 6493 from Munipur, det. T. wallichiana by Spjut; (3) has four specimens, but only the lower left specimen is a type (T. wallichiana), below it are several labels, one printed—ex Herb. George Gordon, presented by J. D. Hooker, 1878, the other bears handwritten annotation—"Taxus wallichiana," two largest specimens with letters a and b written nearby on left and right, respectively, and with Herb. Benthamum imprinted in center, belong to T. contorta; uppermost annotated T. virgata, det. by Spjut to be a young shoot of T. baccata. NY: 2 sheets, 6054A, NY accession numbers 30328 and 30329 (det. via photocopy). P: “Napalia,” 6054 with “A” inserted, annotated Taxus nucifera Kaempf.? on label ex. Herb. Richard, and additional label ex. Herb. E. Drake. PH: “6054A Wallich.”

The lectotype was selected from several Wallich specimens among Zuccarini collections at München that best matched the illustration (Siebold & Zuccarini 1843, Tab. 5); however, Zuccarini (Siebold & Zuccarini 1843) did not cite specimens. Thus, the Wallich specimens of T. wallichiana studied by Zuccarini might appear to be syntypes, while those in other herbaria not seen by Zuccarini could be considered isosyntypes.  This would be the case according to the International Code of Zoological Nomenclature; however, the ICBN is not clear on this issue.  Thus, uncited specimens have to be referred to as original material or duplicates of original material. 

Zuccarini was one of many recipients of specimens distributed by Wallich who generally assigned collection numbers to species rather than to specimens in which a particular specimen number may come from different localities.  For example, Wallich 6054A has been reported from Central Midlands near Kathmandu Valley in Nepal fide Hara et al. (1978) and Anonymous (1913), or “Cachemiro” fide Parlatore (1868), whereas the lectotype—without number—was reportedly from eastern India.  The lectotype was indicated by Zuccarini to have been collected or sent to him in the year 1835, after distribution of Wallich 6054, sometime  between 1831 and 1832 (Anonymous 1913).   It was probably collected in Assam where Wallich was know to have collected during 1835 (Burkhill 1965).  Because the ICBN (Art. 8.2) links the type to a single gathering, isolectotypes cannot be recognized in this case. It should be noted that types have male cones, reddish orange branchlets, non-inflated epidermal cells on abaxial surface of leaves, and 12-15 rows of stomata/band.

Wallich specimens of T. wallichiana with notations of “Kumaon” may be an error in numbering or labeling since collections from “Kumaon” generally belong to T. contorta, whereas Wallich collections without number may indicate uncertainty of taxonomic assignment. 

Taxus wallichiana has been the name applied to all yews in southeastern Asia (Hu 1964; Pilger 1903 as ssp. (wallichiana); however, de Laubenfels (1988) adopted T. sumatrana for his treatment of gymnosperm taxa in Flora Malesiana. He indicated that several species may overlap in the eastern Himalayas, suggesting that T. wallichiana was outside the Flora Malesiana region, but considering the numerous synonyms and references he provided, one might have also expected more on distinction between T. wallichiana and T. sumatrana (Miq.) de Laub. Taxus wallichiana has largely been ignored by Rehder (e.g., Rehder 1940, 1949) and Hortus Third (Liberty Hyde Bailey Hortorium Staff 1976), while others have mentioned it as a species confined to the Himalayas (Krüssman 1985), or more limited to the northwestern Himalayas (Wilson 1926), or as one of two partially sympatric species predominantly Himalayan in distribution (Silba 1984). Since Pilger (1903, 1916) did not cite any specimens for Taxus in western Himalayas, but indicated T. wallichiana to occur in eastern Himalayas, this omission may reflect uncertainty on his part as he noted there were intermediates to T. baccata.

I do not accept all morphological variation of Taxus in southeastern Asia to belong to a single species (Appendix 1). My interpretation agrees in part with that of Handel-Manzzetti (1929), Florin (1948a), and Hu (1964). They recognized another sympatric species by the lack of papillae on the abaxial leaf midrib, which I consider applicable to a species group typified by T. sumatrana (Spjut 1998b, 2000a, Spjut 2007b). This includes the types of T. mairei, T. speciosa, and T sumatrana and other undescribed species.  However, Kwei & Hu (1974) and Cheng & Fu (1978) recognized intermediates between T. wallichiana (papillose midrib) and T. sumatrana (smooth midrib), and treated the latter as a variety under two illegitimate combinations (T. chinensis var. mairei, T. wallichiana var. mairei), whereas Spjut (1993, 1998b, 2000a) reported other correlative features such as epidermal cells in transverse sections appearing angular in a Wallichiana Subgroup of species (C & E Himalayas to SW China; North America) and elliptical in a Sumatrana Group of species (E Himalayas to Indonesia, Philippines).

The Sumatrana Group is generally found at lower elevations—on mainland Asia, below 1700 m (Hu 1964), or below 1200 m (Li & Fu 1997)—whereas T. wallichiana usually occurs above 2300 m.  Within the Sumatrana Group, I distinguish T. mairei by the acute to obtuse leaves with relatively short trapezoidal, somewhat inflated (mammillose) epidermal cells on an elevated, truncate to channeled midrib as seen on the abaxial surface—indicated in my annotations accompanied by crude illustrations (A, GH, June 1996).  Leaves of T. sumatrana differ by tapering to an acuminate apex and by nearly rectangular shape of abaxial epidermal cells.  Leaves of T. sumatrana var. sumatrana are mostly puckered on drying with revolute margins and a raised abaxial midrib in contrast to those of T. celebica that are relatively flat with a flush midrib.  Taxus speciosa differs from T. mairei only in features of branching and color (in dried specimens), treated as a variety of T. mairei in my annotations. Also, I recognized another species by conspicuous persistent bud-scales at base of branchlets, and by leaves that are rigid, evenly tapered to base and apex (e.g., Fig. 2 in Li 1963), and with a rusty orange color in the herbarium (T. kingstonii Spjut ined.).  Differences in seed shape and color are also evident among these taxa, but taxonomic emphasis on seed characteristics could lead to recognizing more taxa.

The taxonomic and ecological significance of midrib papillae on the abaxial (ventral) epidermal surface of leaves in Taxus was studied by Bertrand (1874), Cheng & Fu (1978), Deryugina & Nesterovich (1981), Florin (1931, 1948a, 1948b), von Frimmel (1911), Kwei & Hu (1974), Orr (1937), and Spjut (1992, 1993, 1998a, 2000a; Spjut in Hils 1993); however, intermediates have been recognized by partially papillose midribs.  These intermediate usually have elliptical shaped epidermal cells in leaf transverse sections and are thus considered to belong to the. Sumatrana Group, in contrast to entirely papillose midribs of the Wallichiana Group or the entirely smooth midrib cells that is characteristic of the Sumatrana Group.  Whether these intermediate represent evolutionary, environmental, or hybrid variants, has yet to be determined.  I suspect all three contribute to variation in leaf anatomy.

Nonetheless, I consider the ancestral type of Taxus leaf to have stomata distributed completely across the undersurface without differentiation of an epidermal midrib. The evidence for this is seen by comparing stomatal features of other taxads with those of Taxus, and by phytogeographical patterns on numbers of stomata rows within the genus Taxus (Spjut 2007a).  The stomata in extant Taxus are always encircled by papillose accessory cells (only partially in T. canadensis), in contrast to other taxad genera. Austrotaxus, for example, has hypostomatic leaves that lack papillae and distinct bands, and stomata are more randomly distributed; Pseudotaxus (Nothotaxus Florin 1931, 1948b) has 23–28 rows of stomata in bands well defined by glaucous cells instead of papillose cells, although subsidiary cells are papillose, and is also ancestral in regard to additional sterile scales in male cones (Florin 1948b; Miller 1988). Within Taxus, particularly T. wallichiana and T. chinensis, stomata are occasionally seen on the epidermal midrib that divides the stomatal region into two bands, extending almost continuously across the midrib in Kingdon Ward 8594 (K) from Assam, and in Hooker & Thomson s.n. (GH) from Sikkim (var. yunnanensis), and stomata may also extend to near the leaf margins in up to 21 rows, whereas in North American plants not more than 11 stomata rows/band have been found (Spjut 1992, 1993, 1998a, 2000a).

Additionally, species that have more conspicuous papillae along cells walls (e.g., T. brevifolia, T. globosa, T. wallichiana) appear less variable in the distribution of papillae on the undersurface of leaves (including juvenile leaves), compared to those species that have papillae more erect on upper surface of cells (e.g., T. sumatrana). This may relate to a gradual evolutionary loss of leaf stomata followed by a reduction in the width of the stomatal region in T. wallichiana, compared to a possible widening of the leaf by addition of cells within the marginal region in T. sumatrana.

The presence of papillae on the undersurface of leaves in the T. sumatrana Group may be of secondary origin—after papillae and stomata became lost. This is evident by a sharp demarcation between the stomata bands and adjacent epidermal cells that are variable in distribution of papillae.  For example, leaves of Wilson 1265 (A, BM, K, S, US) collected from 600–650 m in western Sichuan were found with15–21 stomata rows/band bordered by a partially papillose marginal region with papillae on 6 of the 16–25 cells across. Leaves of three specimens from a related plant grown from seed of Wilson 1265 at the Royal Botanic Gardens in Kew all lacked papillae entirely along an abaxial margin zone of 18–28 cells across, but consistently had 8–10 stomata rows/band. Other related specimens cultivated in the United States for which I received 20 leaves (Phyton s.n.)—from apical buds to 3^rd yr branchlets—were found to be relatively constant in the number of marginal cells without papillae—9 cells across—and also in having 16–18 rows of stomata rows/band, but were variable in shape and length of epidermal cells, and in the development of midrib papillae, especially the young leaves. This introduction of Wilson 1265, apparently from Sichuan near Mt. Emei at 600 m and/or Yachou Fu at 600 m, is not T. chinensis as indicated in the literature (Rehder & Wilson in Sargent 1914); however, Wilson 1265 was reportedly collected from three localities (Rehder & Wilson in Sargent 1914), one of which I have identified a specimen as T. chinensis—from western Hubei south of “Ichang,” 600–1300 m.

Taxus wallichiana is also interpreted to occur on Mt. Emei in Sichuan (China) where it integrades with T. chinensis.  Subtle differences in size of bud-scales and color of branchlets make it difficult to consistently separate the two species. These problematical plants may be hybrids between T. wallichiana var. yunnanensis and T. chinensis, and/or possibly another species I recognized by slightly larger and more persistent scales at base of branchlets (T. scutata Spjut ined, inadnot., A).

Species appearing most related to T. wallichiana include T. globosa and T. brevifolia in North America (Spjut 1998b) and two undescribed in Asia. They share character features of conspicuous bud-scales at base of 1^st year branchlets, angular epidermal cells in leaf transverse sections, leaves densely papillose on the abaxial midrib with papillae most conspicuous along cell walls, and seeds maturing on 2^nd yr or older branches (Wallichiana Species Group Spjut 1992, 1993, 1998b; Wallichiana Subgroup, Spjut 2000a, c).  One in Myanmar (T. suffnessii Spjut ined., type Kingdon Ward 20902 [A, BM]) is distinct for its relatively large persistent bud-scales (2–3 mm long) with a conspicuous midnerve. Another in Yunnan and Sichuan (T. florinii Spjut ined., type from Yunnan,  R.C. Ching 21980, A) is much like T. globosa and T. brevifolia in North America by the large angular epidermal cells in leaf x-sections, and by stomata developing in less than 12 rows/band; it seems to differ from the North American species by the thicker walled epidermal cells.

1b. Taxus wallichiana var. yunnanensis (W. C. Cheng & L. K. Fu) C. T. Kuan, Fl. Sichuan. 2: 215. 1983. Taxus yunnanensis W. C. Cheng & L. K. Fu, Acta Phyto. Tax. Sin. 13 (4): 86, fig. 52, 4–7. 1975. Taxus chinensis (Pilg.) Rehder var. yunnanensis (W. C. Cheng & L. K. Fu) L. K. Fu, Vasc. Pl. Hengduan Mount. 1: 214. 1993. Type: CHINA. Tibet: Zayul, 2100 m, Zhang 916 (holotype: CAF; isotype: PE-leaf fragment! photocopy! http://www.cvh.org.cn/pic/pe/0/00000090.jpg). Topotypes: PE (no other data, leaf fragments!], BM (Kingdon Ward 10398!).

Shrub or tree to 20 m high; branchlets subpinnate, simple to isodichotomously or isotrichotomously divided, yellowish green, reddish orange or abruptly reddish purple in 2^nd yr, leafy to base; bud scales persistent, brownish, overlapping in 3–4 ranks, the lower scales adnate, ovate, ca. 0.5 mm long, upper scales thick, incurved, spreading, concave, ca. 1.5 mm long. Leaves ± in two ranks, slightly overlapping in pairs, more evenly spaced along branchlets than in typical variety, lanceolate, acuminate, mostly straight, rarely falcate, 1.5–3.5 (-4.7) cm long, 2.0–4.0 mm wide, 150–250 µm thick, dark glossy green above, pale green to yellowish green below (in dried specimens), slightly convex above to a rounded midrib that forms a channel along the base on the lower half of leaf, nearly flat below to a flush to slightly rounded midrib, plane to abruptly revolute 80-90º near margins; upper (adaxial) epidermal cells mostly rectangular in x-sect., some cells appearing quadrate, occasionally taller than wide, 25 (-50) µm tall, 25–37 (-50) µm wide; lower (abaxial) epidermal cells often similar in size to upper in x-sect. as seen near margin, usually taller than those of var. wallichiana, numbering 7–28 between margin and stomata band, irregularly rectangular, often 3–5× l/w, becoming  longer and more uniformly rectangular near margins, entirely papillose across the abaxial surface, or papillae lacking on up to 6  rows across, midrib cells narrow rectangular, 3–7× l/w; papillae mostly erect, medial in 2–4 opposite rows on midrib cells, medial on marginal cells; stomata bands broader than marginal region, with 13–19 stomata rows/band. Male cones maturing on 1^st and 2^nd yr branchlets, scales in 4–5 ranks; microsporangia 6–8 (5 fide Cheng), pinkish or brownish. Female cones, 1–2 mm long in bud, scales in 5–9 ranks, basal scale not conduplicate, maturing on 1^st or 2^nd yr branchlets; seed conical, 4 mm long, 3 mm diam.; sharply pointed at apex, purplish.

Yunnan yew. Distribution: mixed forests types, generally at higher elevations than var. wallichiana, 2100–3500 m; India (Sikkim, Nagaland), Myanmar, China (Tibet, Yunnan), occurring with Larix griffithiana Carrière. and Picea spinulosa (Griff.) A. Henry in the Sikkim region (Rau 1974).  Reported from Sichuan in Spjut (2007b) based on two specimens cited on this web page that were erroneously placed here; however, this variety might be expected to occur in Sichuan.

Representative Specimens—India—Sikkim: Terup, 7000–10,000 ft, Hooker s.n., Herb. Hook. fil., right specimen (GH); ex Hooker fil & Thomson (BM, GH); Tongloo [“immense tall tree with long sparse branches and slender drooping twigs,” “9500-10,000 feet” fide J. Hooker, Elwes & Henry 1906], Kurz s.n. (A). Nagaland: Barail Range, Naga Hills, 28º35’N, 93º55’E, 9-10,000 ft, tree, scattered along summit ridge, Kingdon Ward 7755 (K); “Japuo Range,” 7300 ft, Kingdon Ward 18990 (BM);  “Jakpho,” “Naja Hill,” 8500 ft, Clarke 41238B (K). Myanmar (Burma): Mt. Viatoria, 9000-10,000 ft, tree with weeping habit, smooth almost purplish bark, Kingdon Ward 22819 (BM); Myitkyina Dist., Laikam Fenshuling Rd, 8000 ft, tree 40-50 ft, Kernode 17205 (K). China—Tibet: Zayul, Rong Tö Valley, 8000 ft, spreading tree with brilliant green foliage, amongst deciduous trees on slopes and in gullies, Kingdom Ward 10398 (BM); Delei Valley, 9000 ft, Kingdon Ward 8594 (K); Delei Valley, Chiban, 28º10'N, 96º30'E, Kingdon Ward 8090 (K). Yunnan: [Nur ein Baum ober den Tempeln auf dem] Dji-shan ad boreo-orientem urbis Dali (Talifu), 3200 m, Handel-Mazzetti 6408 (GH); Xangbi Xian, W side of Diancang Shan mountain range, Malultang, vicinity of Chang Shan, mixed broad-leaved evergreen forest, 2700 m, 25º46' 100º01, 1984 Sino-Amer. Bot. Exped. 388 (GH, US); W, Shangschang, above Yangbi, 2700 m, tree to 8 m, 1981 Sino-Brit. Exped. To Cangshan 0419 (A, K); Lung-pan la Champu fung, small tree, 10 ft, forest, fruit gray, C.W. Wang 67412 (A), 67414 (A); Chen-Kang Hsien, ravine, 20 m high, male, C.W. Wang 72417 (A); Kiemiu-ingdi above Yangbi, 3000 m, Sino-Brit. Exped., Cangshan 0227 (K).  [Note: Prior to July 2007, two specimens from Sichuan were mentioned here.  These have always been regarded as T. florinii. It appears that they had been inadvertently placed here].

Taxus yunnanensis has been confused with T. wallichiana in the Flora of China (Cheng & Fu 1978). The authors had evidently considered the type for T. wallichiana to represent the species mainly in NW Himalayas; consequently, they described T. yunnanensis—indicating it was found in eastern Himalayas (Bhutan, Tibet, Myanmar) to Yunnan and Sichuan (Cheng et al. 1975; Cheng & Fu 1978). Later, it was reduced to a variety of T. wallichiana as cited above, and more recently placed in synonymy (Li & Fu 1997), although it had been included in synonymy by de Laubenfels (1988) under his broadly circumscribed T. sumatrana.

Most specimens I annotated T. yunnanensis (A, GH, July 1996; BM, Oct. 1997; Spjut 1998b) were from Yunnan and Sichuan. They were distinguished from typical T. wallichiana by the leaves appearing slightly wider (nearly lanceolate), more evenly distributed, less markedly curved above and paler green below than above, and having medial papillae on the abaxial epidermal cells.  At the time I had seen only leaf fragments of a type—from Tibet near the border with Myanmar and India; it differed from the type of T. wallichiana by the abaxial surface having a broad region of large epidermal cells with medial papillae between the margins and stomata bands. These features were seen more often in yew specimens from Yunnan and Sichuan than in those from northeastern India. Later, I received a B/W photocopy of a PE isotype from Dr. Z-y. Cao who had earlier sent me leaf fragments of topotypes, and found that the leaf arrangement and shape compare closer to the type of T. wallichiana than to specimens from Yunnan and Sichuan. Thus, plants most typical of this variety as seen in northeastern India and nearby Tibet are intermediate forms, distinguishable only by leaf anatomical characters. For this reason T. yunnanensis is reduced to a variety.  Nevertheless, it is important to differentiate these and one other related species under study (T. florinii Spjut ined) in order to distinguish the North American species (T. brevifolia, T. globosa) from their Asian relatives; otherwise, they would have to be included under T. wallichiana.

Photocopy of relevant pages from Griffith, Notulae Plantas Asiaticus, 1854.

Taxus fuana Nan Li & R. R. Mill in Li & Fu, Notes on gymnosperms I. Taxonomic treatments of some Chinese conifers. Novon 7: 263. 1997 (Nov.).—TYPE: CHINA. Tibet (Xizang): Jilong, 3000 m, Qingzhang Expedition 7032; holotype PE! http://www.cvh.org.cn/typus/details.asp?RecordNo=00002643&mode=1&guan=PE

Taxus orientalis Bertoloni, Mem. Acad. Sci. Bologna ser. 2, I, 229, pl. 2 (1862); Misc. bot. 23: 17, Tab. 2. no specimens cited. TYPE: northeastern India, western Sikkim, 8,000 ft (Holotype: BOLO [leaf fragments!]).

West Himalayan yew. Distribution: Mixed coniferous-hardwood forests of W Himalayas, 2300–3500 m; Afghanistan, Pakistan, India, W Nepal, China (SW Tibet). Noted to be common in t