A Geographical Analysis of Morphological Characters for Taxus contorta (Taxaceae)

R. W. Spjut

World Botanical Associates

Bakersfield, CA 93380-1145

May 2006
Nomenclature updated Jan 2008
 

Taxus contorta Griffith has been clearly established as a distinct species for the yew in Northwest Himalayas based on morphological data (Spjut 2007a, 2007b) and molecular data

Data in this table are summarized for eight characters scored from 45 herbarium specimens studied of Taxus contorta; the herbarium collection data, the SR and MC data were extracted from another ms on the phytogeography of Taxus prepared in 2001, which was submitted to Sida for peer review.  Characters include the number of stomata rows (SR), the number of epapillose cells along the abaxial leaf margin (MC), and other less taxonomically useful characters—abbreviated as PAP, CSL, CSX, LA, LS, and PAR; an explanation for each is given below.  The specimens are arranged geographically from west to east, and also by increasing number of stomata rows within each geographic area.

SR: Stomata Rows, number of stomata rows in a stomata band. Stomata count can vary on a plant; for example, Stewart 8414 was represented by three specimens from three different herbaria in which stomata were found to be either in 5, 6 or in 7 rows per band.  A difference of 2 rows on a plant is not uncommon, and even a difference of 1 row can be found in stomata bands on a leaf, the result of which is expressed as an intermediate value; for example, a leaf with 7 to 8 rows of stomata is indicated as 7.5.

Number of stomata rows increase from west to east in the Himalayas for T. contorta, while a reverse trend occurs for T. wallichiana. This is better visualized for stomata data plotted on a geographic map of Asia. http://www.worldbotanical.com/taxus_wallichiana_group.htm#wallichiana%20grp

The higher counts in plants of T. contorta from Nepal and Bhutan are believed to be the result of hybridization between T. contorta and Taxus wallichiana.  Thus, it is suggested that where T. contorta may have come into contact with T. wallichiana, the T. contorta plants are hybrids that have gained more stomata rows in their bands, whereas other alleged hybrid plants assigned to T. wallichiana have lost stomata.  The general evolutionary trend for leaf stomata in Taxus is a gradual loss of stomata as the plants adapt to climatic changes over time.  Examples are evident in North America and in the NW Himalayas.

MC: Marginal Cells, number of marginal epidermal cells on abaxial surface without papillae.  The leaf margin in T. contorta—where the adaxial and abaxial surfaces come together—is difficult to identify due to the nature of the broadly round margins that characterizes the species.  The leaf margin is determined by where the epidermal cells are smallest in width and in height, and is usually marked by a single mammilla. From an evolutionary view, the marginal border of cells lacking in papillae appear to be a modification of the adaxial epidermal cells as the species adapts to changes in climate. 

The abaxial marginal cells of T. contorta, along with the number of stomata rows, are remarkably consistent in having 4–5 rows of epapillose cells for many specimens from the NW Himalayas.  This is in contrast to specimens of T. contorta from the Central Himalayas that generally have a wider marginal border of cells, as seen in specimens from Nepal and Bhutan where Taxus contorta var. mucronata is recognized.  Leaves in this variety resemble T. umbraculifera in phyllotaxy and marginal cells, while it is also believed that T. umbraculifera evolved from T. chinensis by loss of loss of papillae on marginal cells and by reduction in papillae stature.  However, specimens of T. contorta var. contorta that have long-wide-spreading leaves resemble T. wallichiana.  One explanation is that the wider leaf margin seen in var. mucronata may have been acquired from a late Tertiary contact with a T. umbraculifera-chinensis ancestor type, whereas the increase in stomata may be the result of more recent contact with T. wallichiana (since the Pleistocene).

PAP: Papillae, position of papillae on epidermal cells, classified as either medial or marginal.  Medial papillae are oriented towards the center of the cell, and if multiple papillae develop, papillae often lie opposite each other in two or more rows.  Marginal papillae, on the other hand, are nearer the cell wall, and in specimens with multiple rows of marginal papillae on a cell, the papillae appear alternate instead of opposite.

The difference in orientation of papillae is believed to be a genetically determined trait, which can vary on a leaf.  Some specimens are noted to have marginal papillae in one region of the leaf and medial papillae in another area of the leaf.  The ancestral condition is believed to be marginal in which there is little differentiation between the midrib and stomata band as exemplified by Taxus wallichiana; however, Taxus wallichiana var. yunnanensis is distinguished from the typical variety by its medial orientation of papillae on epidermal cells.  The differences in medial vs. marginal papillae in T. contorta are believed to be related to ecological factors.  Collection data suggest a partial correlation with altitude. 

CSL: Cell Shape in Longitudinal section, as actually seen on the abaxial leaf surface in the marginal region.  The abaxial marginal cells may appear short and somewhat pentagonal, or somewhat hexagonal, referred to as diamond shaped in the table, or they may appear longer and narrowed towards one end, referred to as rectangular (rect) in outline, but if notably rounded at both ends and also relatively narrow, the cells are then described as fusiform (this character attribute was not present on marginal cells for specimens of T. contorta, although the midrib cells are fusiform). Taxus canadensis and T. sumatrana are examples of species with leaves that have relatively long rectangular epidermal cells along the abaxial margins.  Specimens of Taxus contorta from Nepal and Bhutan more frequently had shorter (diamond) cells, similar to that seen in Taxus chinensis.

CSX: Cell Shape in Cross section.  The epidermal cells may appear globose (very rare, British Isles, T. baccata), elliptical (common in T. baccata and allies), rectangular to isodiametrically square (common in T. wallichiana and allies), and isodiametric rounded-angular (occasional in T. contorta).  Shape of epidermal cells in x-section is difficult to evaluate as it depends on making good x-sections of leaves, and because the differences are often relatively minor.  Taxus contorta is similar to T. baccata in having short elliptical cells, in contrast to smaller and wider elliptical cells of T. cuspidata and its allies.   However, when color of epidermal cells is taken into consideration, as seen on older herbarium specimens, the differences between T. contorta and T. wallichiana are more easily discernible.

LA: Leaf Arrangement (phyllotaxy). Leaves in Taxus are spirally arranged. Differences in Taxus phyllotaxy are related to leaf density along the branch, a feature that is more easily observed than defined by mathematical ratios.  Each species generally has a distinctive arrangement of leaves.  In other words, phyllotaxy is constant for a species.  An example is shown for two specimens of Taxus biternata placed one on top of another so that the branch of one from Japan appears to be the same as that for the other from South Korea; see http://www.worldbotanical.com/images/wpe-biternata-mixed.gif. 

However, phyllotaxy may be distorted by leaf spread (LS), which is affected by direct exposure to light (leaf orientation) as explained below, or it can vary in more complex species such as T. baccata for which many varieties have been recognized.

In the Euro-Mediterranean, T. recurvata is distinguished from T. baccata by radial leaves appearing notably arcuate (recurved) in which the leaves curve downwards, and by their difference in color between the abaxial and adaxial surfaces (discolorous).  Leaves in T. baccata are more distichous, concolorous, glaucous, and upturned (towards the light source).  Thus, for these Euro-Mediterranean species, leaf arrangement, leaf spread, and leaf color are correlated.

In Taxus contorta, leaf arrangement varies from somewhat radial to somewhat distichous. The differences between radial and the distichous types of T. contorta are difficult to evaluate taxonomically.  Leaves on young branchlets appear more distichous than on older branchlets, while older branches may also lose some of their leaves. Nevertheless, data in the table suggests that leaf orientation in Taxus contorta is variable throughout its range.

LS: Leaf Spread (leaf orientation), the angle at which leaves spread outwards from branches.  This is influenced by amount of exposure to light and to what extent plants are adapted to growing in shade vs. sunlight.  Taxus contorta is an understory tree in spruce, pine and oak forests of the western and central Himalayas.  Its branches might vary form horizontal to weeping and the spread of leaves would also expect to vary accordingly.  Nevertheless, leaves were classified as spreading at 45 degrees, 60 degrees, 80 degrees and 90 degrees from branches.

From the data in the table, it can be seen that leaves from specimens collected in Nepal and Bhutan spread more widely, commonly at 80-90 degrees from branchlets.   This is seen as further evidence of hybridization between T. wallichiana and T. contorta, where the two species are sympatric. Specimens with relatively short leaves and radial phyllotaxy are considered a distinct variety, T. contorta var. mucronata. Intermediates have similarly short leaves but a distichous leaf arrangement, or long leaves that spread at nearly right angles from branchlets.

PAR: Parenchyma Cells, the shape of cells in spongy parenchyma layer of leaves, varies from elliptical, globose, to angular in T. contorta.  This is in contrast to bone-like cells of T. wallichiana and related species.  Old herbarium specimens of T. contorta appear to have heavy deposits of resinous-like (terpenoid) substances on parenchyma cell walls, but this is not evident in young specimens such as those that were approximately one-year old in which the cells all appear clear.  Nevertheless, the spongy parenchyma cells still appeared loose without any adhesiveness as seen in older dried specimens.  Thus, in relatively recently collected specimens of T. contorta, the loose arrangement of the globular cells is still evident, a features that characterizes this species.  Taxus baccata is recognized to have similar parenchyma cells, and the differences between these species would seem to be leaf curvature (straight vs. falcate leaf blades).

Species vs. varietal designation.  Species status in Taxus depends on specimens either having a combination of unique features, or a large number of shared features among many specimens over a wide geographic area.  In the NW Himalayas, the majority of specimens have relatively long, narrow, straight leaves with rounded margins, 5-8 (-10) stomata rows per band and an abaxial margin of (0-) 3–6 marginal cells.  All the specimens had hardened resinous parenchyma cells in the leaf mesophyll and a papillose midrib on the abaxial surface.  The presence of hardened parenchyma cells in the leaf mesophyll is unique to Taxus contorta.  Most of the other features mentioned above also help separate T. contorta from the E Himalayan species, e.g., T. wallichiana, T. sumatrana.  Therefore, the numerous correlated features seen among the NW Himalayan Taxus lends support to its species status.  The major problem has been in the application of the correct name due in part to a failure by many botanists to examine all relevant types from the geographic region.  This has led to superfluous names such as T. fuana (nomen illegit.) for T. contorta, and T. yunnanensis for T. wallichiana.  Another more easily forgivable error has been not recognizing the earliest available name; for example, Bertonini’s T. orientalis has been thought to be the earliest valid name because the separate publications by Griffith for the earliest name (T. contorta) do not constitute valid publication by themselves; it is only when they are taken together in which Griffith did refer back to his earlier description.

An example of a taxon with a much narrower range in occurrence was first recognized as a species based on a specimen by Ludlow and Sheriff 16035 (GH) from Bhutan.  It had the leaf parenchyma cells of T. contorta, but it was still considered a distinct species for the relatively short abruptly apiculate leaves that spread from branchlets at nearly 90º in a mostly radial arrangement, and the leaf epidermal features also were found to differ substantially from other NW Himalayan specimens in having 11 stomata rows and 9 rows of epapillose cells along the abaxial margin. In July 1996 this specimen was annotated Taxus mucronata Spjut ined and designated holotype. The ineditus (unpublished) status was indicated because all specimens of Taxus being studied had to be returned prematurely due to a request made by the USDA Agricultural Research Service that the study of Taxus be terminated; however, the study was continued outside the USDA in the World Botanical Associates. Upon a further review of Taxus in other herbaria in October 1997, similar specimens were discovered at the Museum of Natural History in London (BM), and at the Kew herbarium (K).  These were also annotated T. mucronata, including one isotype (BM).  Also, discovered at Kew were specimens to have been annotated T. fuana that were all regarded by Spjut as T. contorta; these were annotated by Spjut in October 1997 as T. contorta.

One exception, however, soon appeared in the November 1997 issue of Novon where T. fuana was described as a new species (http://www.fna.org/china/novon/lifu7-3.htm); in a commentary the authors (Nan Li and R. R. Mill in Li & Fu 1997) indicated there was an illustration for the species in the Flora of China (Cheng & Fu 1978). Whereas all the specimens cited by the authors clearly belonged to T. contorta, the  illustration they mentioned in Cheng & Fu (1978) was clearly Spjut's T. mucronata.  In China T. contorta appears to occur only within a narrow region of SW Tibet (Jilong)—where also considered endangered. The holotype from Jilong and leaf fragments received from Da Cheng Hao from several sites in Jilong (Sep 2007) compare favorably with the lectotype for T. contorta.  While the illustration was clearly not drawn from the type (as Spjut had thought, unpublished), it also seems likely that it was prepared from a specimen collected in Nepal or Bhutan instead of China.  W. C. Cheng (Cheng & et al. 1975; Cheng & Fu 1978) seemed to have selected extreme variants to show clear separation of Taxus species; for example, when T. yunnanensis was described as a new species, the type specimen was not from Yunnan but rather from Tibet, near the border with India.  The reason for this may be that Cheng may have recognized other variation in Yunnan Taxus worthy of taxonomic status. Spjut (1996 via annotation labels and 2007), for example, recognized T. florinii, an endemic species to China found in Yunnan, Sichuan, and Xinjiang Uygur.

Taxus contorta Griffith has been clearly established as a distinct species for the yew in Northwest Himalayas based on morphological data (Spjut 2007a, 2007b) and molecular data (Amin Shah et al. 2008).  In addition to the morphological separation between the Central and East Himalayan T. wallichiana from the Northwest Himalayan T contorta, molecular data that includes specimens from the Baccata Alliance reported three distinct lineages; thus, T. contorta is clearly separated from yews of the Euro-Mediterranean Region.  Unfortunately, Amin et al. (2008) chose to uphold an illegitimate name (T. fuana), while the nomenclature at the NPGS/GRIN has been based on an unsubstantiated and outdated taxonomic concept of a single Himalayan species of yew (T. wallichiana).

Upon further study of the leaf fragments from additional specimens at BM, and at K, the anatomical distinction between T. contorta and T. mucronata could not be upheld due to intermediates; therefore, the new taxon (T. mucronata Spjut ined.) was recognized only as a variety, T. contorta var. mucronata (Spjut 2007b).

Additional Reference noted here: Shah, A., D.-Z. Li, M. Möller, L.-M. Gao, M. L. Hollingsworth and M. Gibby 2008.  Delimitation of Taxus fuana Nan Li & R.R. Mill (Taxaceae) based on morphological and molecular data  Taxon (http://www.ingentaconnect.com/content/iapt/tax/pre-prints/571shah).