Wood anatomy of Cupressus and its relation to geographical distribution
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48 IAWA Journal
IAWA 37 (1),
Journal 2016:
37 (1), 48–68
2016
Wood anatomy of Cupressus and its relation to
geographical distribution
Elena Román-Jordán*, Luis G. Esteban, Paloma de Palacios, and
Francisco G. Fernández
Universidad Politécnica de Madrid, Escuela Técnica Superior de Ingenieros de Montes,
Departamento de Sistemas y Recursos Naturales, Ciudad Universitaria s/n, 28040 Madrid, Spain
*Corresponding author; e-mail: elena.roman@upm.es
ABSTRACT
The wood anatomy of 14 species of Cupressus was studied to determine whether
there is a pattern of wood anatomical diversity between the species from the
North and Central American (western) region and the Eurasian (eastern) region.
Xanthocyparis vietnamensis and Chamaecyparis nootkatensis (syn. Xantho-
cyparis nootkatensis) were also studied to compare their wood anatomy, given
their recent inclusion by some authors in Cupressus. The arrangement of the axial
parenchyma, morphology of the transverse end walls of the axial parenchyma,
presence of ray tracheids, typology of the end walls of the ray parenchyma cells
and ray height support to some extent the division of Cupressus into two large
groups: the American group (western region) and the Eurasian group (eastern
region), as proposed in molecular phylogenetic studies. The wood anatomy of
Chamaecyparis nootkatensis shares the presence of ray tracheids and the same
ray typology with American Cupressus, and has the same ray height as Eurasian
Cupressus. In contrast, Xanthocyparis vietnamensis shares the absence of ray
tracheids and the same ray typology with Eurasian Cupressus, and has the same
ray height as American Cupressus.
Keywords: Callitropsis, Chamaecyparis, Cupressaceae, Hesperocyparis, phylo
geny, wood anatomy, Xanthocyparis.
INTRODUCTION
Since ancient times, cypress wood has not only been used in construction, but has
also been widely planted for its high ornamental and religious value. Cupressus L. is
distributed throughout the warm temperate zone of the northern hemisphere, in the
circum-Mediterranean region, Asia (eastern, or Eurasian, region) and North and Central
America (western, or American region). Because of its wide distribution, Koch (1873)
considered that, geographically, Cupressus presented two morphologically well defined
groups distributed in Eurasia and America. Although this hypothesis was shared by
Malejeff (1928), it had no further impact. Wood anatomy studies of Cupressus have
been solely descriptive and have not addressed the wood anatomical similarities among
species.
© International Association of Wood Anatomists, 2016 DOI 10.1163/22941932-20160120
Published by Koninklijke Brill NV, Leiden
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Govaerts and Farjon (2014) reported that Cupressus has 19 species and 16 varie-
ties, including Chamaecyparis nootkatensis and Xanthocyparis vietnamensis, a higher
number than the 15 species and 17 varieties recorded by Farjon (2005). The taxonomic
treatment by Farjon (2005) was followed in this study.
Despite the importance of Cupressus, wood anatomical studies are limited and gen-
erally refer to species with high commercial value or wide distribution. In particular,
C. cashmeriana, C. chengiana and C. sargentii have been little studied. Earlier studies
indicated some differentiation between species from the eastern and western regions
based on ray height. In most North American species ray height ranges from 1–10
cells. In C. arizonica, C. lusitanica and C. macrocarpa rays are 1–15 cells high and
maximums of 25 cells were recorded in C. lusitanica (Carvalho 1996; De Magistris
1997) and up to 30 cells in C. arizonica (De Magistris 1997) and C. macrocarpa
(Carvalho 1996; De Magistris 1997). The most frequent ranges for Eurasian species
are 1–15 cells or 1–20 in C. sempervirens and C. torulosa, with maximums of up to
26 recorded for C. funebris (Jiang et al. 2010), 25– 40 for C. sempervirens (Huber &
Rouschal 1954; Greguss 1955; Peraza 1964; Parsa Pajouh & Schweingruber 1985;
Fahn et al. 1986; Schweingruber 1990; Akkemik & Yaman 2012) and even up to 45
in C. torulosa (Esteban et al. 2002). In the study by Heinz (2004), a possible division
between species was observed based on the presence of ray tracheids, which are more
frequent in species from the American region. The most complete study on Cupressus
was by Esteban et al. (2004), which described 12 species and reported small differences
such as the higher occurrence of axial parenchyma with nodular transverse end walls
in the western group. The division between Cupressus in the American and Eurasian
regions has recently been supported through studies of pollen morphology and cytology
(Danti et al. 2010).
Cupressus taxonomy has changed little in more than a century (Adams et al. 2009).
Most species were discovered and described in the 19th century. However, the descrip-
tion of Xanthocyparis vietnamensis Farjon & Hiep (Farjon et al. 2002) as a new spe-
cies of Cupressaceae after its discovery in 1999 in northern Vietnam, on the border
with China, and the use of new molecular phylogeny tools provide new arguments in
the classification of this genus.
Some molecular, morphological and anatomical studies have reported differen-
tiation within the genus Chamaecyparis Spach, noting a clear separation between
Ch. nootkatensis (D. Don) Spach and the other species (Young & Watson 1969; Alden
1997; Gadek et al. 2000; Wang et al. 2003; Little et al. 2004; Debreczy et al. 2009).
Using morphological and anatomical studies, Farjon et al. (2002) included Ch. noot-
katensis in the new genus Xanthocyparis as X. nootkatensis (D. Don) Farjon & Harder.
Little et al. (2004) indicated that, because this species does not belong to Cupressus
L., it should be called Callitropsis nootkatensis (D. Don) Örest, as it was described
in 1865. Eckenwalder (2009) considered both X. nootkatensis and X. vietnamensis as
species of Cupressus.
Molecular studies have indicated that Cupressus is not monophyletic, but comes
from two well supported groups geographically divided between North and Central
America (western region) and Eurasia (eastern region) (Fig. 1). As Xiang and Li (2005)
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indicated, the phylogenetic relations that keep this genus united depend on whether
or not Xanthocyparis (Callitropsis) is accepted as a separate genus. If it is accepted,
a clear division is seen between the clade formed by the American Cupressus and
Xanthocyparis and Callitropsis, and the clade comprising the Eurasian Cupressus
Thujopsis dolabrata (Thunb. ex L. f.) Siebold & Zucc.
Thuja occidentalis L.
Thuja plicata Donn ex D. Don
Fokienia hodginsii (Dunn) A. Henry & H.H.Thomas
Chamaecyparis thyoides (L.) Britton, Stearns & Poggenb.
Chamaecyparis formosensis Matsum.
Chamaecyparis pisifera (Siebold & Zucc.) Endl.
Chamaecyparis lawsoniana (A. Murray bis) Parl.
Chamaecyparis obtusa (Siebold & Zucc.) Endl.
Tetraclinis articulata (Vahl) Mast.
Microbiota decussata Kom.
Platycladus orientalis (L.) Franco
Calocedrus decurrens (Torr.) Florin
Calocedrus macrolepis Kurz
Cupressus duclouxiana Hickel
Cupresses sempervirens L.
Juniperus procera Hochst. ex Endl.
Juniperus conferta Parl.
Juniperus drupacea Labill.
Chamaecyparis nootkatensis (D. Don) Spach
Xanthocyparis vietnamensis Farjon & Hiep
Cupressus lusitanica Mill.
Cupressus arizonica Greene
Cupressus macnabiana A. Murray
Cupressus macrocarpa Hartw. ex Gordon
Cupressus pigmaea (Lemmon) Sarg.
Cupressus goveniana Gordon
Figure 1. Phylogenetic relationships of the cupressoid clade recovered by Little et al. (2004),
Juniperus conferta = Juniperus rigida var. conferta (Parl.) Patschke; Cupressus pigmaea =
Cupressus goveniana var. pigmaea Lemmon.
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(Little et al. 2004; Little 2006; Adams et al. 2009; Terry et al. 2012; Yang et al. 2012).
In the angiosperms, phylogenetic analyses have also demonstrated evolutionary dif-
ferentiation between species of genera distributed in the Old World (eastern) and New
World (western) regions (Donoghue et al. 2001; Xiang et al. 2004; Lo et al. 2009).
The objective of this study was to describe the wood anatomy of the species of the
genus Cupressus, as well as Xanthocyparis vietnamensis and Chamaecyparis noot-
katensis, to determine whether there is a pattern of wood anatomical diversity among
the species of Cupressus and define the affinities of Ch. nootkatensis and X. vietnam-
ensis with the genus, and to compare the results with the clades obtained by molecular
phylogeny.
MATERIAL AND METHODS
The material used in this study came from the wood collections of several research
centres. Samples of the 15 species of Cupressus considered by Farjon (2005) were ob-
tained except for C. chengiana S.Y. Hu. Many wood samples had localities far beyond
the natural distribution of the species concerned, testifying to the wide cultivation of
Cupressus species in parks and arboretums.
Species studied and contributing wood collections (abbreviated according to Stern
1988; Lynch & Gasson 2010) are: Cupressus arizonica Greene (USw36178, C.B.Wolf,
11299, Arizona, USA; UPMAw-X0932, collector unknown, s.n., Spain (cult.);
UPMAw-X1808, collector unknown, s.n.; UPMAw-X2521, collector unknown, s.n.,
Huesca, Spain; MADRw683, collector unknown, s.n., Spain); Cupressus bakeri Jeps.
(USw32134, O.V. Matthews 38, California, USA; MADRw684, collector unknown,
s.n., USA); Cupressus cashmeriana Royle ex Carrière (K-Jw19142, collector un-
known, s.n., United Kingdom); Cupressus duclouxiana Hickel (USw22613, collector
unknown, s.n., South Africa (cult.); K-Jw19143, collector unknown, s.n., northern
China); Cupressus dupreziana A. Camus (K-Jw19145, D. Murc, s.n.); Cupressus
funebris Endl. (USw26630, collector unknown, s.n., India; K-Jw19146, collector un-
known, s.n., Calcutta, India); Cupressus goveniana Gordon (USw36143, C.B.Wolf
6264, California, USA; UPMAw-X0933, collector unknown, s.n., California, USA;
UPMAw-X1220, collector unknown, s.n.; UPMAw-X1585, collector unknown, s.n.;
MADRw686, collector unknown, s.n., USA; MADRw686-2, collector unknown,
s.n., USA); Cupressus guadalupensis S. Watson (USw19540, G.McCarthy 705, Red-
lands, California, USA; K-Jw19149 W2, collector unknown, s.n., United Kingdom
(cult.); MADRw686-1, collector unknown, s.n., USA); Cupressus lusitanica Mill.
(USw20127, M. Acosta Solis 11601, Quito, Pichincha, Ecuador; UPMAw-X1219,
collector unknown, s.n.; MADRw687, collector unknown, s.n., USA; K-Jw19152,
collector unknown, s.n., West tropical, South America); Cupressus macnabiana
A. Murray (USw36099, C.B.Wolf 6145, California, USA; MADRw687-1, collec-
tor unknown, s.n., USA); Cupressus macrocarpa Hartw. ex Gordon (USw23162,
H.H. Smith s.n., California, USA; UPMAw-X0028, collector unknown, s.n., Cercedilla,
Madrid, Spain); Cupressus sargentii Jeps. (USw36122, C.B.Wolf 6191, California,
USA; USw36117, C.B.Wolf 6185, California, USA); Cupressus sempervirens L.
(USw37617, collector unknown, s.n., Italy; UPMAw-X0037, collector unknown, s.n.,
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Spain; X0214, collector unknown, s.n.; X1747, collector unknown, s.n.; X1953, col-
lector unknown, s.n.); Cupressus torulosa D. Don (USw4432, collector unknown,
Y.3806, India; K-Jw70768, collector unknown, s. n., India); Chamaecyparis nootka-
tensis (D. Don) Spach (UPMAw-X0930, collector unknown, s.n., Canada); Xantho-
cyparis vietnamensis Farjon & Hiep (MADw 33537, D.K. Harder 6091, Vietnam).
The microscope slides were prepared following the usual methods of softening, sec-
tioning, staining and mounting. Samples were observed without staining and stained
with safranin for lignified cell walls and Sudan 4 to observe any resin (Jane 1970). The
samples for scanning electron microscopy were prepared using the method described
by Heady and Evans (2000). The anatomical description was made following the ter-
minology of the IAWA Committee (2004).
The samples were observed by light microscopy (Leica DM2500 with a DFC 420
camera) and image processing software IM50 v. 5 release 220, and scanning electron
microscopy (SEM mod. JEOL JSM-6380, Phillips XL-30 ESEM with LaB6 and
Leica StereoScan 440 with LaB6).
The ray height ranges included in the study were taken from the literature. Where in-
sufficient data were found for species, an approximate height range based on the sam-
ples studied was included.
RESULTS
Wood anatomical observations
Table 1 shows the anatomical wood features observed in the species of Cupressus,
separated into the two geographical regions of North and Central America and Eurasia,
as well as the features observed for Chamaecyparis nootkatensis and Xanthocyparis
vietnamensis.
The wood anatomy of Xanthocyparis vietnamensis has not previously been described.
It has distinct growth rings with an abrupt transition from earlywood to latewood
(Fig. 2A), where the latewood is composed of a few rows of tracheids with pits in the
tangential walls. Axial parenchyma is scarce, in diffuse arrangement. In the samples
studied it was not possible to observe the typology of the transverse end walls. Tracheid
pitting in radial walls is exclusively uniseriate. Tracheid pits with well defined torus
(Fig. 2B). Uniseriate rays, 1–10 cells high (Fig. 2C). Rays are composed solely of ray
parenchyma cells, with smooth horizontal walls and end walls (Fig. 2D). Cross-field
pits are cupressoid (Fig. 2E). The number of pits per cross field is 3–5, although some
marginal ray cells have as many as 6. Helical and callitroid thickenings absent. Warty
layer present on the inner layer of the tracheids (Fig. 2F). Resin canals were not ob-
served.
Macroscopic features
Macroscopically, the wood of Cupressus does not show a clear differentiation be-
tween the two geographical regions. The colour of the eastern Cupressus woods varies,
but occasionally the sapwood and the heartwood cannot be distinguished by colour in
species such as C. arizonica and C. macrocarpa. The sapwood is described as whitish
or yellowish for all species and is generally accompanied by heartwood ranging from
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pale brown in C. goveniana, yellowish or pinkish brown in C. lusitanica to pinkish
or reddish brown in C. macrocarpa. Streaks have been described only in C. arizonica
(Wolf & Wagener 1948) and C. lusitanica (Chudnoff 1984; Lincoln 1986; Bergman
et al. 2010). The Cupressus woods in the eastern group also show some variation. The
sapwood and heartwood cannot be distinguished in C. cashmeriana and C. sempervi-
rens, as they are both light-coloured. Like the western group, the species in the eastern
Figure 2. Xanthocyparis vietnamensis. – A: Growth rings distinct. – B: Pits with well defined torus
(arrow). – C: Ray height low. – D: Horizontal and end walls of ray parenchyma cells smooth. –
E: Cross-field pits cupressoid. – F: Warty layer. — Scale bars: A = 100 µm; B, D = 25 µm;
C = 200 µm; E, F = 20 µm.
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Table 1. Anatomical features observed in the species of Cupressus, and features observed for Chamaecyparis nootkatensis and Xanthocyparis vietnamensis.
Numbers in brackets correspond to the number of the feature according to the IAWA Committee (2004). (–) absent; (+) present; (+/–) weak/variable.
North American region Eurasian region
Anatomical features
vietnamensis
nootkatensis
C. arizonica
C. bakeri
C. goveniana
C. guadalupensis
C. lusitanica
C. macnabiana
C. macrocarpa
C. sargentii
C. cashmeriana
C. duclouxiana
C. dupreziana
C. funebris
C. sempervirens
C. torulosa
Xanthocyparis
Chamaecyparis
Growth rings
Distinct (40) + + + + – + + + + + + + + + + +
Indistinct or absent (41) – – – – + – – – – – – – – – – –
Abrupt transition (42) – – – – – – – – – – – – – – + –
Gradual transition (43) + + + + – + + + + + + + + + – +
Tracheids
Tracheid pits in tangential walls + + + + + + + + + + + + + + + +
Tracheid pitting in radial walls uniseriate (44) + + + + + + + + + + + + + + + +
Tracheid pitting in radial walls biseriate (45) – – – – – – – – – – – – – – – +/–
Biseriate tracheid pitting in radial walls
opposite (46) – – – – – – – – – – – – – – – +/–
Intercellular spaces (53) +/– +/– – +/– +/– + – +/– – – +/– +/– – +/– – –
Tracheid pits in radial walls with well defined
IAWA Journal 37 (1), 2016
torus (56) + + + + + + + + + + + + + + + +
Tracheid pits with torus extensions (58) – – – – – – – – – – + + – – – –
Pits with notched borders (59) – – – – – – – – – – – – – – – +/–
Warty layer (60) + + + + +/– + + + + + + + + + +/– +/–
Axial parenchyma
Present (72) + +/– +/– +/– +/– + + + + +/– + + + + +/– –
Arrangement diffuse (73) +/– + +/– + – – + +/– + + + + + + + –
Arrangement tangentially zonate (74) + – + – + + – + +/– – +/– +/– +/– +/– – –
Arrangement marginal (75) – – – + – + + +/– – – – – +/– – – –
Transverse end walls smooth (76) + – + + + – + – + + + + + + (*) –
Transverse end walls irregularly thickened (77) + + +/– – +/– + +/– + – – – – – – (*) –
Transverse end walls nodular (78) – + +/– – – + + – – – – – – – (*) –
(continued on the next page)
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North American region Eurasian region
Anatomical features
vietnamensis
nootkatensis
C. arizonica
C. bakeri
C. goveniana
C. guadalupensis
C. lusitanica
C. macnabiana
C. macrocarpa
C. sargentii
C. cashmeriana
C. duclouxiana
C. dupreziana
C. funebris
C. sempervirens
C. torulosa
Xanthocyparis
Chamaecyparis
Ray composition
Ray tracheids present (79) +/– + – – + – + – – +/– – – – – – +
Homogeneous rays (80) + + + + + + + + + + + + + + + +
End walls smooth (85) + – +/– + + + + +/– + + + + + + + +
End walls nodular (86) +/– + + +/– +/– + +/– + – +/– – – – – – +/–
Horizontal walls smooth (87) + + + + + + + + + + + + + + + +
Horizontal walls pitted (88) – – – +/– – – – – – – – – – – – +/–
Indentures (89) + + + + +/– + + + – + – – – – – +
Cross-field pits
Cupressoid (93) + + + + + + + + + + + + + + + +
1–2 pits per cross field (97) + + + + + + + + + + + + + + – +
1–3 pits per cross field (98) – – – – – – – – – – – – – – – –
3–5 pits per cross field (99) – – – – – – – – – – – – – – + –
Ray size
Range in ray height in a number of cells
(102–105) 1–15 1–10 1–10 1–10 1–15 1–10 1–15 1–10 1–20 1–15 1–15 1–15 1–20 1–20 1–10 1–15
Uniseriate (107) + + + + + + + + + + + + + + + +
2–seriate in part (108) – – – – +/– – – – – – – – – – – +/–
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(*) could not be assessed.
55
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Figure 3. Cupressus I. – A: Growth rings distinct. C. arizonica. – B: Growth rings indistinct.
C. lusitanica. – C & D: Tracheid pitting in tangential walls. C. cashmeriana and C. torulosa. –
E: Tracheid pitting in radial walls uniseriate. C. lusitanica. — Scale bars: A = 100 µm; B = 150 µm;
C, D = 20 µm; E = 60 µm.
group have yellowish white sapwood, but the shades of brown in the heartwood vary
geographically. Species in the zone of Europe and India have a lighter shade than spe-
cies from China, which have reddish tones.
Review and discussion of microscopic features
A general feature of Cupressus (Table 1) is the presence of distinct growth rings
(Fig. 3A), characteristic of conifers in the temperate and boreal regions, although growth
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rings are indistinct or absent in C. lusitanica from tropical Central America (Fig. 3B)
(Huerta Crespo 1978; Barefoot & Hankins 1982; Lincoln 1986; Esteban et al. 2004;
Heinz 2004). In all the samples studied the transition from earlywood to latewood
is gradual. This feature is considered to be of limited diagnostic value (Peirce 1936,
1937; Bannan 1954; Carlquist 1980; IAWA Committee 2004) as it can be influenced
by many factors (Esteban et al. 2003). In all species, tracheid pits were observed in the
Figure 4. Cupressus II. – A & C: Pits with well defined torus (arrow in A). C. dupreziana. –
B: Pits with well defined torus (arrow). C. cashmeriana. – D: Warty layer. C. sempervirens. –
E & F: Cross-field pits cupressoid. C. cashmeriana and C. bakeri. — Scale bars: A = 20 µm;
B = 5 µm; C, D, F = 10 µm; E = 25 µm.
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tangential walls (Fig. 3C, D), generally confined to the latewood (Peirce 1937; Esteban
et al. 1996; De Magistris 1997). Tracheid pitting in radial walls is uniseriate (Fig. 3E).
Intertracheid pits have a well defined torus (Fig. 4A, B, C). The warty layer on the in-
ner layer of the tracheids (Fig. 4D) is common to all the species (Liese 1965; Xiaomei
& Ying 1989; De Magistris 1997; IAWA Committee 2004), although the quantity of
warts varies. Neither helical nor callitroid thickenings were observed in any of the
species. Axial parenchyma was present in all the species but was particularly sparse in
C. bakeri, C. duclouxiana and C. lusitanica. Rays are homogeneous, composed solely
of ray parenchyma cells, with ray tracheids present in some species. Uniseriate rays
were observed in all the samples, with cupressoid cross-field pits (Fig. 4E, F), which
are common in the Cupressaceae except in Thuja (IAWA Committee 2004); 1–2 pits
per cross field.
The presence of intercellular spaces has occasionally been recorded in many of these
species and is considered a characteristic feature of C. arizonica (Harrar 1957; Esteban
& Guindeo 1988; Esteban et al. 2000), C. lusitanica (Huerta Crespo 1978; Carvalho
1996; Esteban et al. 2004), C. macrocarpa (Butterfield & Meylan 1980; Esteban &
Guindeo 1988; Carvalho 1996) and C. torulosa (Pearson & Brown 1932; Mahmood
& Athar 1997). Their presence is associated with tracheids with a circular outline and
they must not be confused with the spaces associated with compression wood. In the
samples observed this is an occasional feature and is most common in C. macnabiana
(Fig. 5A).
Other features sporadically cited were not observed, such as pits with notched bor-
ders in C. dupreziana (IAWA Committee 2004), crassulae in C. funebris (De Magistris
1997), C. goveniana (Gerry 1910) and C. sempervirens (Fahn et al. 1986; De Magistris
1997), and organic deposits in the tracheids of C. lusitanica (Blanco et al. 2005). Torus
extensions were observed (Fig. 5B) in the woods of C. dupreziana and C. funebris.
This feature has not previously been described for these species.
Traumatic resin canals have occasionally been described in C. funebris (Gamble
1902) and C. macrocarpa (De Bratati & Datta 1987). They are absent in the other
species, which have a group of resin cells as a traumatic response (Shimakura 1937)
that is prominent in very old trees (Gamble 1902; Barefoot & Hankins 1982), e.g., in
C. torulosa (Gamble 1902). In the samples studied, no resin canals were observed.
Based on the samples studied and the literature consulted, it is considered that the
arrangement of the axial parenchyma, the transverse end walls of the axial parenchyma,
the presence or absence of ray tracheids, the typology of the end walls of the ray pa-
renchyma cells and ray height can be used to differentiate between Cupressus in the
western and the eastern groups.
The arrangement of the axial parenchyma in the Eurasian species is diffuse (Fig. 5C)
and occasionally tangentially zonate in some growth rings, whereas in the American
species the arrangement is frequently tangentially zonate (Fig. 5D) or even marginal
(Fig. 5E), as in C. guadalupensis, C. macnabiana and C. macrocarpa. The typology
of the transverse end walls also differentiates the western and eastern species, as the
walls are exclusively smooth (Fig. 5F) in the Eurasian species and smooth, irregularly
thickened (Fig. 6A) or nodular (Fig. 6B, C) in the American species. This differentiation
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was reported in the study by Esteban et al. (2004). IAWA Committee (2004) considered
the possibility of finding both smooth and irregularly thickened end walls in some
species at the same time, but contemplated the presence of both smooth and nodular
walls only as an exception, in very limited areas such as juvenile wood. Smooth and
nodular end walls were found to occur simultaneously by Visscher and Jagels (2003) in
Figure 5. Cupressus III. – A: Intercellular spaces. C. macnabiana. – B: Pits with torus extensions
(arrow). C. funebris. – C: Axial parenchyma diffuse. C. dupreziana. – D: Axial parenchyma
tangentially zonate. C. macnabiana. – E: Axial parenchyma marginal. C. guadalupensis. –
F: Transverse end walls of axial parenchyma cells smooth (arrow). C. sempervirens. — Scale
bars: A = 50 µm; B = 10 µm; C = 100 µm; D = 120 µm; E = 60 µm; F = 25 µm.
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Glyptostrobus, Gasson et al. (2011) in Fitzroya, and Esteban et al. (1996, 2002, 2004)
in Cryptomeria, Diselma, Fokienia and Sequoiadendron. All these authors confirm-
ed the possibility of joint occurrences of smooth and nodular walls in a single species,
as observed in this study in the American Cupressus samples.
Sporadic presence of ray tracheids has been cited in all species of the genus (Holden
1913; De Magistris 1997; Heinz 2004). However, they were observed (Fig. 6D, E)
Figure 6. Cupressus IV. – A: Transverse end walls of axial parenchyma cells irregularly thick-ened
(arrow). C. sargenti. – B & C: Transverse end walls of axial parenchyma cells nodular (arrow
in B). C. macnabiana. – D & E: Ray tracheids. C. macrocarpa and C. lusitanica. — Scale bars:
A, B, D = 20 µm; C, E = 10 µm.
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only in the samples of C. bakeri, C. lusitanica and C. macrocarpa and occasionally in
C. arizonica and C. duclouxiana in the marginal rows of the rays or forming rays one
cell high. Except for C. duclouxiana, these are all American species.
The end walls of ray parenchyma cells are exclusively smooth (Fig. 7A) in the
Eurasian species, with the exception of C. duclouxiana, in which nodular end walls
were also occasionally observed. In the American species, smooth and nodular end
Figure 7. Cupressus V. – A: Horizontal and end walls of ray parenchyma cells smooth. C. fu-
nebris. – B: End walls of ray parenchyma cells nodular (arrow). C. macrocarpa. – C: Inden-
tures (arrow). C. goveniana. – D: Ray height low. C. macnabiana. – E, F: Ray height medium.
C. cashmeriana. — Scale bars: A, B = 20 µm; C = 10 µm; D, E, F = 200 µm.
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walls were observed (Fig. 7B) in most species, with indentures (Fig. 7C). In the east-
ern group, indentures were observed only in C. duclouxiana, as described by Esteban
et al. (2002, 2004). The horizontal ray cell walls are smooth in all the Cupressus spe-
cies and also occasionally pitted in C. guadalupensis.
The differentiation in ray height in number of cells is seen in the lower height range
in the American species (Fig. 7D). Concurring with the literature studied, a height
range less than 10 or 15 cells high was observed in the rays in the western Cupressus.
Figure 8. Chamaecyparis nootkatensis I. – A: Growth rings distinct. – B: Pits with well defined
torus. – C: Pits with notched borders (arrow). – D: Trabecula. – E: Ray tracheids. — Scale bars:
A = 100 µm; C, E = 10 µm.
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The highest values found in the study samples were 16 in C. macnabiana, 18 in C.
arizonica and 20 in C. lusitanica. In the eastern Cupressus, cell height ranged from
1–15 and 1–20 cells (Fig. 7E, F) and the highest values were in C. cashmeriana, C.
sempervirens and C. torulosa. The maximum values observed were higher than 20
cells in all species and were particularly high in C. sempervirens, where rays were up
to 50 cells high. However, the origin of the samples and the age of the tree or branch
influence ray height, as observed in the study of C. sempervirens by Fahn et al. (1986).
Partially biseriate rays were observed in C. lusitanica, but they were less than 10% of
the total.
Genetic diversity studies (RAPDs) in Cupressus, on both American (Bartel et al.
2003) and Eurasian species (Rushforth et al. 2003; Xu et al. 2010), raised some of the
varieties considered by Farjon (2005) to species level. Anatomical data on Cupressus
and most other woody genera does not provide evidence for or against the delimitation
of species or varieties.
Cupressus lusitanica is distributed in Mexico, Guatemala, Belize, Honduras, El Sal-
vador and Nicaragua (Farjon 2005). Anatomically, a few warts were observed on the
inner layer of the tracheids and sparse axial parenchyma was observed. The characteristic
indentures of the North American Cupressus are less conspicuous and less abundant,
and some authors reported their absence (Phillips 1948; Kukachka 1960). Ray height
is greater or similar to the Eurasian species.
Chamaecyparis nootkatensis has been extensively described. It is distributed on the
Pacific coast of the United States, from Alaska to California. The wood is yellowish,
with a sharp odour and a bitter taste. The anatomical features observed (Table 1) include
the presence of distinct growth rings (Fig. 8A) with a gradual early-to-latewood transi-
tion, and tracheid pits in tangential walls in the latewood, as reported by other authors
(Penhallow 1907; Brown et al. 1949; Harrar 1957; Panshin & De Zeeuw 1964; Esteban
et al. 2000, 2002, 2004). Tracheid pitting in the radial walls is uniseriate and also oc-
casionally biseriate in opposite arrangement in the earlywood tracheids, with a well
defined torus (Fig. 8B). Pits with notched borders were observed sporadically (Fig. 8C).
This feature has not previously been described in this species. Trabecula are occasionally
present (Fig. 8D). Sparse warts occur on the inner layer of the tracheids. The samples
studied lacked axial parenchyma. The literature describes axial parenchyma as absent
to very abundant, depending on the author and the sample (the discrepancy may be due
to descriptions using misidentified samples), in diffuse arrangement (Penhallow 1907;
Brown et al. 1949; Harrar 1957; Panshin & De Zeeuw 1964) or tangential (Penhallow
1907; Brown et al. 1949; Harrar 1957; Panshin & De Zeeuw 1964; Heinz 2004). The
transverse end walls have been described as smooth (Heinz 2004; IAWA Committee
2004), irregularly thickened (Heinz 2004) and nodular (Panshin & De Zeeuw 1964;
Hoadley 1990). Rays are generally homogeneous, but rays 1–2 cells high frequently
have ray tracheids (Fig. 8E), as reported by other authors (Holden 1913; Peirce 1937;
Brown et al. 1949; Harrar 1957; Panshin & De Zeeuw 1964). Some authors concur that
the presence of ray tracheids is a diagnostic feature of the species (Belyea 1919;
Bannan 1952; IAWA Committee 2004). The ray parenchyma has smooth and occa-
sionally nodular end walls (Fig. 9A), smooth horizontal walls with sporadic pitting
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(Fig. 9B) and conspicuous indentures (Fig. 9C), which were described only by Panshin
and De Zeeuw (1964). Cross-field pits are cupressoid (Fig. 9D), generally 1–2 pits per
cross field, although taxodioid pits have also been reported (Heinz 2004). Rays are
uniseriate (Fig. 9E) and occasionally biseriate in less than 10% of the rays (Penhallow
1907; Brown et al. 1949; Harrar 1957; Panshin & De Zeeuw 1964). Rays are 1–15
cells high (Harrar 1957; Panshin & De Zeeuw 1964; Esteban et al. 2000, 2004), with
maximum heights of up to 25 cells in the samples studied.
Figure 9. Chamaecyparis nootkatensis II. – A: End walls of ray parenchyma cells nodular. –
B: Horizontal walls of ray parenchyma cells pitted. – C: Indentures (arrow). – D: Cross-field
pits cupressoid. – E: Tall rays, partially biseriate in less than 10% of the rays. — Scale bars:
A, B, C, D = 10 µm; E = 100 µm.
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via free accessRomán-Jordán et al. – Cupressus: wood anatomy and distribution 65
The relation between Chamaecyparis nootkatensis and Xanthocyparis vietnamensis
is supported phylogenetically in some studies (Little et al. 2004; Xiang & Li 2005;
Little 2006; Rushforth 2007) in which a well resolved clade has been reconstructed.
The anatomical features described for Chamaecyparis nootkatensis and Xanthocyparis
vietnamensis (Table 1) show major differences between these species, such as the
typology of the ray walls, the ray height, the higher number of pits per cross field in
X. vietnamensis, and, in particular, the presence of ray tracheids in Ch. nootkatensis.
Considering its geographical distribution, it can be seen that anatomically, Ch. noot-
katensis has the presence of ray tracheids in common with various American Cupressus
species. Other common features are the typology of the ray walls and the presence of
indentures. However, its ray height is similar to the Eurasian species of Cupressus,
with maximums of up to 20 cells observed. Similarly, X. vietnamensis has features in
common with the Eurasian Cupressus (absence of ray tracheids and typology of the
ray walls) and with the American Cupressus (ray height, with maximums of 10 cells).
The wood anatomical study of Ch. nootkatensis and X. vietnamensis is not conclusive
for placing these species in either Cupressus or Xanthocyparis or maintaining them as
separate genera. Future studies on these species may determine their affinities.
ACKNOWLEDGEMENTS
The authors thank the research centres that provided samples for the study, in particular the Smithsonian
Institution for making its facilities available to prepare some of the samples and for allowing the use
of the SEM. The authors are also grateful to the Jodrell Laboratory and Kew Gardens libraries for the
documentation provided for the study of the literature.
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