22 IAWAIAWA Journal Journal 36 (1), 36 (1),2015: 2015 22–35

Wood anatomy of Tetraclinis articulata from its natural distribution area in southeast Spain

Luis G. Esteban1,*, Paloma de Palacios1, Alberto García-Iruela1, Elena Román- Jordán1, Francisco G. Fernández1, Sandra Díaz Fernández1 and María Conde2 1Universidad Politécnica de Madrid, Escuela Técnica Superior de Ingenieros de Montes, Ciudad Universitaria s/n, 28040 Madrid, Spain 2CIFOR-INIA, Departamento de Productos Forestales, Carretera de la Coruña Km 7.5, 28040 Madrid, Spain *Corresponding author: e-mail: [email protected]

ABSTRACT For the first time, the wood anatomy ofTetraclinis articulata (Vahl) Masters has been studied using representative samples from its natural distribution area in Spain, in Sierra de Cartagena (Region of Murcia). Mature wood was collected from five individuals representative of the forest stand and their anatomy was compared with other genera of the Cupressaceae. Axial tracheids without helical thickenings, low homogeneous rays, cupressoid pits and the absence of normal axial resin canals are characteristic features of this monotypic genus, as they are of most other Cupressaceae genera. An obvious warty layer separates this wood from the genera sharing its territory (Cupressus and Juniperus) and its semi-spherical, slightly anastomosed warts distinguish it from other, geographi- cally distant genera (Actinostrobus and Callitris). The presence of traumatic axial resin canals is reported for the first time and supports the occurrence of this feature outside the Pinaceae. The wood anatomical diversity within the clade comprising Tetraclinis, Microbiota and Platycladus, as reconstructed by molecular analysis, is discussed. Keywords: Cupressaceae,warty layer, traumatic resin canals.

INTRODUCTION

Tetraclinis Mast. is a monotypic genus of the Cupressaceae, T. articulata (Vahl) Masters, comprising trees that can reach a height of 15 metres, although due to human action they do not normally exceed 10–12 metres and are frequently limited to bushy or frutescent shrubs (Ceballos & Ruiz de la Torre 1979) (Fig. 1). The natural distribution of the spe- cies is restricted to north Africa, southeast Spain and the island of Malta. In Africa it covers an area of nearly 800,000 hectares: 600,000 in Morocco, 160,000 in Algeria and 22,000 in Tunisia. Reports of the species in Libya and the Ahaggar Mas- sif, in central Sahara, appear to be confused with cypresses (Charco 1999). In Spain it occurs scattered over four areas (Ibáñez et al. 1989) (Fig. 2): 1) to the northeast of Portman, between Peña del Águila (387 m) and Monte de las Cenizas (337 m), 310

© International Association of Wood Anatomists, 2015 DOI 10.1163/22941932-00000082 Published by Koninklijke Brill NV, Leiden

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1 3

2

Figure 1–3. Tetraclinis articulata. – 1: Small Tetraclinis articulata tree in Monte de las Cenizas, Region of Murcia (Spain). – 2: Geographical distribution in the natural area of the Region of Murcia (Spain). – 3: Sapwood and heartwood markedly different.

Downloaded from Brill.com10/07/2021 12:26:39AM via free access 24 IAWA Journal 36 (1), 2015 catalogued individuals occupy an area of around 325 hectares; 2) in Cerro de la Cam- pana, in Valle de Escombreras, there are just 50 spontaneous individuals that have regrown from old stumps and 30 more planted trees growing among Aleppo pines (Pinus halepensis); 3) the largest population, in Algameca Grande, west of Cartagena, has more than 345 individuals catalogued in just 100 hectares, some of them more than 11 metres in height; 4) north of Peña del Águila, 58 individuals have been inven- toried, most of them regrown from old stumps, but no trees are more than five metres heigh (Ibáñez et al. 1989). Intense overgrazing and the traditional use of the timber for firewood and char- coal production have brought the species to the brink of extinction. In the first half of the 20th century only a few examples of regrowth from old stumps were visible and regeneration was completely lacking (Jiménez Munuera 1903; Huguet del Villar 1938; Rigual & Esteve 1953; Templado 1974). The decline of livestock grazing, the end of charcoal production, and the protection given to the species have allowed some recovery (Ibáñez et al. 1989), although progress is very slow due to the difficulty of regeneration from seeds and the semi-arid conditions in the region (Costa Tenorio et al. 1990). The rootwood and burrwood of T. articulata, with their characteristic black spots on a reddish brown background, have commonly been used in cabinetmaking. This continues to be an important industry in the ancient city of Mogador (now Essaouira), in Morocco. The wood anatomy of Tetraclinis has been described by various researchers, although their descriptions were based on a limited number of samples, mostly of unknown provenance. Strangely, Castellarnau (1883), in his study of the Spanish conifers, did not describe Tetraclinis and Peraza (1964) was the first to make a complete description of the species in the Spanish stands, using a single sample from Murcia. Saint-Laurent (1926) described Tetraclinis under the name of Callitris articulata (Vahl) Murbeck using a sample from Algeria. The provenance and number of the samples used by Peirce (1937), Phillips (1948), Huber and Rouschal (1954), Greguss (1955) and Jacquiot (1955) are not known. Tetraclinis has since been described by Schweingruber (1990) and Heinz (2004). Like Peraza (1964), Esteban and Guindeo (1988) and Esteban et al. (1996, 2002) described a sample from Murcia. The scarce information about the earlier samples described makes it impossible to determine whether the wood was mature or juvenile or came from branches or trunks and therefore neither the qualitative nor the quantitative features can be compared. A complete description of this wood with samples collected in its natural regions of provenance using mature trunk wood will complement molecular phylogeny studies of this species. Gadek et al. (2000), Little (2006) and Yang et al. (2012) recovered a clade formed by Microbiota Kom., Platycladus Spach and Tetraclinis. The aims of this study were to: 1) describe the wood anatomy of Tetraclinis using trees collected in natural forests of the species in southeast Spain and compare its anatomy with other genera of Cupressaceae; 2) compare the wood anatomy of the species in the clade established by molecular phylogeny.

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MATERIAL AND METHODS

The material used for this study was collected in the natural forests of Tetraclinis in the Regional Park of Calblanque, Monte de las Cenizas y Peña del Águila, in the province of Murcia (Spain). The five trees felled for the study were all adult individuals over 70 years old repre- sentative of the forest. A disc was extracted 50 cm from the ground and samples were obtained from mature wood in each disc for the observations. Microscope slides were prepared following the usual methods of softening, section- ing, staining and mounting. The descriptions were made in accordance with the IAWA Committee (2004). The samples were observed using light microscopy (Leica DM2500 with a DFC 420 camera) with image processing software IM50 v.5 release 220 and scanning electron microscopy (SEM) mod. JEOL JSM-6380. Observation was conducted on samples without staining and stained with safranin for the lignified cell walls and with Sudan 4 for the resin (Jane 1970). SEM samples were prepared following the method described by Heady and Evans (2000). The biometry was conducted on three slides from each tree, on mature wood from a basal disc obtained 50 cm from the ground, on ring 30 counted from the exterior, using the WinCell image analysis programme. From each slide the following measurements were taken: 25 measurements of axial tracheid length and diameter, ray height (mm and number of cells), and number of pits per cross field in the earlywood; 50 measurements of tracheid pit diameter and largest and smallest cross-field pit diameter in the earlywood; and five measurements of the number of rays per square millimetre measured in five different areas of one square millimetre on the tangential section. Tracheid length was measured following Ladell’s indirect method (Ladell 1959). The study of the most frequent ray height values (µm and number of cells) and number of pits per cross field was performed using frequency histograms, and therefore the most frequent value does not equal the mean value. Statistical calculations were made with the Statgraphics Centurion Ver. 15.2 programme, for a 95% significance level.

RESULTS Wood description Transverse section. Sapwood and heartwood markedly different: sapwood with shades of yellow and heartwood reddish brown (Fig. 3). Aromatic with an intense, pleasant odour. Growth rings distinct, with gradual transition from earlywood to latewood (Fig. 4). Tracheids generally rectangular in outline, but also hexagonal in earlywood (Fig. 5). Intercellular spaces absent. On the growth ring boundary tracheid pits are commonly found in the tangential walls (Fig. 6). Axial parenchyma in diffuse arrangement (Fig. 5), marginal in the last row of latewood and tangentially zonate with dark coloured cell content (Fig. 7). Normal resin canals absent, although traumatic axial resin canals were observed in two of the five trees; numerous subsidiary parenchyma cells were associated with traumatic canals (Fig. 8).

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4 5

6 7

8

Figure 4–8. Tetraclinis articulata. – 4: Growth rings distinct, with gradual transition. – 5: Tracheids with rectangular and hexagonal outline and axial parenchyma diffuse. – 6: Tracheid pits in the tangential walls near the growth ring boundary. – 7: Axial parenchyma diffuse and tan- gentially zonate. – 8: Traumatic axial resin canals: a: transverse section, b: radial section. – Scale bars for 4 = 150 μm; for 5 = 100 μm; for 7 = 300 μm; for 8a = 200 μm; for 8b = 175 μm.

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9 10

11 12

13 14

Figure 9–14. Tetraclinis articulata. – 9 &10: Transverse end walls of axial parenchyma smooth. – 11: Transverse end walls of axial parenchyma irregularly thickened. – 12. Tracheid pits in tangential wall. – 13: Low ray height. – 14: Rays partly biseriate, less than 10%. – Scale bars for 10 & 11 = 25 μm; for 12 = 100 μm; for 13 = 150 μm; for 14 = 125 μm.

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15 16

17 18

19

Figure 15–19. Tetraclinis articulata. – 15: Tracheid pitting uniseriate in radial wall and warty layer present. – 16: Tracheid pits biseriate in opposite arrangement in earlywood with crassu- lae. – 17: Horizontal and end walls of rays smooth. – 18: Crassulae abundant. – 19: Trabeculae with warty layer. – Scale bars for 15 = 20 μm; for 16, 17 & 19 = 25 μm.

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Tangential section. Transverse end walls of axial parenchyma generally smooth (Fig. 9, 10), although some are irregularly thickened (Fig. 11). Abundant tracheid pits in uniseriate arrangement in both earlywood and latewood (Fig. 12), normally on the growth ring boundary. Uniseriate rays up to 23 cells high, but the most frequent height is 3 cells (Fig. 13). Biseriate rays not more than 10% (Fig. 14). Radial section. Organic deposits and helical thickenings absent in axial tracheids. Tracheid pits normally in uniseriate arrangement, although in some earlywood tra- cheids they are biseriate in opposite arrangement (Fig. 16). Without torus extensions (Fig. 15). Warty layer present (Fig. 15, 19). Rays homogeneous, with smooth horizontal and end walls (Fig. 17). Indentures absent. Cross-field pits cupressoid, 1–4 pits per field, normally 1 or 2. Abundant presence of crassulae (Fig. 18). Trabeculae present in four of the five trees, with warty layer (Fig. 19).

Biometry The biometry data are shown in Table 1.

Table 1. Biometry of Tetraclinis articulata from southeast Spain (means with SD and full range, or most frequent value) and data from the literature. (2002) (1996) et al. et al. Esteban Features Mean value ± SD and range (min–max) Saint-Laurent (1926) Greguss (1955) Jacquiot (1955) Peraza (1964) Esteban

Tracheids Diameter (µm) 23.6±4.8 (10–40) – – – 26–29–33 25–30 31–32 Length (mm) 4.2 ± 0.9 (2–6) – – – – 2.3 – Diameter tracheid pits 15.1±2.3 (8–23) – – – – 10–15 13–18 (µm) Rays Height (µm) 86.4±48.3 (13–386) 50–650 – – 24–360 – – Most frequent height 58.7±10.8 (31–103) – – – – – – in µm (*) Height (no. cells) (1–23) – 1–17 1–15 1–20 1–28 1–17 Most frequent height in 3 (1–7) – (1–2) (2–3) (2–4) – (1–6) number of cells (*) No. rays/mm2 50.5±9.4 (27–66) – – – – – – Cross fields Largest diameter cross- 4.9±1.2 (2–9) – – – – – – field pits (µm) Smallest diameter cross- 2.1±1.0 (1–7) – – – – – – field pits (µm) No. pits per cross field 1.8±0.9 (1–4) – 1–5 2– 4 1– 4 1– 4 1– 4 Most frequent number of 2 – (1–2) – (1–2) (2) (2–3) pits per cross field (*)

(*) Most frequent values calculated from the frequency histogram.

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DISCUSSION

As in all the Cupressaceae, the axial tracheids do not have helical thickenings, the rays are homogeneous (i.e., ray tracheids are absent), the cross-field pits are cupressoid (except in Thuja L.) and there are no normal resin canals, making it difficult to separate Tetraclinis from other Cupressaceae. The difference in colour between the sapwood and the heartwood is characteristic in Tetraclinis. The reddish brown heartwood is similar in colour to Sequoia sempervirens (D. Don) Endl. and Fitzroya cupressoides (Molina) I. M. Johnst. and to the naked eye its grain is similar to these species due to its curious and numerous pin knots. This reddish brown colour is similar to the colour described for other species of Cupressaceae, which Ahuja (2009) termed redwoods. Under this name he included Sequoia sempervirens, Fitzroya cupressoides, Metasequoia glyptostroboides Hu & W.C. Cheng, Sequoiaden- dron giganteum (Lindl.) J.Buchholz, Cunninghamia lanceolata (Lamb.) Hook. and Cryptomeria japonica (Thunb. ex L. f.) D. Don. Although its odour is characteristic, this must be interpreted with caution, as it is similar to the odour of other genera such as Juniperus L. and Cupressus L. The axial tracheids have pits with tori, although they lack extensions such as those described in Cryptomeria D. Don (Fujii et al. 1997; Kitin et al. 2009), Fitzroya Lindl. (Willebrand 1995; Gasson et al. 2011), Juniperus spp. (Willebrand 1995), Metasequoia Hu & W.C. Cheng (Dute et al. 2008), Pilgerodendron Florin (Roig 1992; Esteban et al. 1996; Gasson et al. 2011), Thujopsis Siebold & Zucc. ex Endl. and Widdringtonia Endl. (Willebrand 1995). No notches were observed on the pit borders, unlike those described by Willebrand (1995) in some Cupressaceae (Athrotaxis cupressoides D. Don, A. selaginoides D. Don, Chamaecyparis pisifera (Siebold & Zucc.) Endl., Crypto- meria, Cupressus dupreziana A. Camus, Juniperus thurifera L., Papuacedrus papuana (F. Muell.) H.L. Li, Sequoia Endl., Taiwania Hayata and Thuja occidentalis L.) and by de Palacios et al. (2014) in Juniperus brevifolia (Seub.) Antoine. Tetraclinis has an obvious warty layer, as do other taxa in Cupressaceae, such as Actinostrobus Miq., Athrotaxis D. Don, Callitris Vent., Chamaecyparis Spach, Cryp- tomeria, Cupressus, Fitzroya, Juniperus, Sequoia, Sequoiadendron J. Buchholz, Thuja, Thujopsis and Widdringtonia. The presence of warts on the inner layer of the tracheids has often been a notable feature in descriptions of this species (Cronshaw et al. 1961; Peraza 1964; Liese 1965; Esteban & Guindeo 1988; Schweingruber 1990; IAWA Com- mittee 2004) and is very common in Cupressaceae (Huber & Rouschal 1954; IAWA Committee 2004). Studies on the morphology, size and frequency of warts, such as the works of Heady et al. (1994) on Callitris and Heady and Evans (2005) on Actinostrobus, and their comparison with studies of other genera, could allow this feature to be used to separate Cupressaceae genera. The warts in Tetraclinis are normally semi-spherical and slightly anastomosed, unlike those in Actinostrobus and Callitris, which are more prominent and longer and are sometimes anastomosed in pairs. Clearly a comparison of the warty layer in the genera of Cupressaceae would be very interesting to determine its relevance for wood identification in this group of conifers.

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Intercellular spaces such as those described by Greguss (1955) were not found, probably because his description included compression wood, which is common in individuals obtained from coppicing. Tangential tracheid pitting was observed, particularly in the last rows of latewood tracheids, although it was not as abundant as in Abietoideae (Esteban & de Palacios 2009). Like other Cupressaceae, Tetraclinis often has trabeculae, with a marked warty layer. Axial parenchyma, as in the other Cupressaceae genera (except Neocallitropsis Florin), is present in Tetraclinis, although authors differ about its arrangement. In this study axial parenchyma was found to be diffuse, tangentially zonate and terminal, but other authors have described it as tangentially zonate (Schweingruber 1990; Heinz 2004). The transverse end walls are smooth or irregularly thickened. Although the mor- phology of the transverse end wall is often considered a diagnostic feature in softwood anatomy, in Cupressaceae it must be interpreted with caution, because co-occurrence of smooth and irregular walls have sometimes been observed , e.g., by Visscher and Jagels (2003) in Glyptostrobus Endl., Gasson et al. (2011) in Fitzroya, and Esteban et al. (2002) in Sequoiadendron, Cryptomeria, Diselma Hook. f. and Fokienia A. Henry & H. H. Thomas. Rays are homogeneous, although Holden (1913), Peirce (1937) and Jacquiot (1955) reported the presence of ray tracheids in branch wood samples. The horizontal walls are smooth, although Peirce (1937) considered them to be pitted. The end walls are also smooth, but they have been reported as nodular (Jacquiot 1955; Greguss 1955). As in the other Cupressaceae (except Thuja), cross-field pitting is cupressoid and the most frequent number of pits is 2 per cross field. The most abundant rays are three cells high, although they can be up to 23 cells high. This range in height in a number of cells is the most common in the Cupressaceae, although in some genera, such as Sequoia, more than 30 cells have been reported in several studies (Brown & Panshin 1940) and even as many as 60 (Carvalho 1996). Further reports of cell height include Metasequoia at 40 cells high (Hejnowicz 1973; Visscher & Jagels 2003), Glyptostrobus with 30 cells in some cases (Peirce 1936; Greguss 1955; Gromyko 1982; Esteban et al. 1996, 2002, 2004; Visscher & Jagels 2003) and Taiwania having up to 36 (Kanehira 1921; Shimakura 1937; Yang & Yang 1987; Esteban et al. 1996) or even 50 cells (Kanehira 1921). Tetraclinis has no normal resin canals and no reports of traumatic resin canals are known. The presence of traumatic axial resin canals in the samples collected is a further report of these types of canals in Cupressaceae, and with the descriptions by Bailey and Faull (1934) in Sequoia sempervirens, Jeffrey (1903) in Sequoiadendron and Benkova and Schweingruber (2004) in Microbiota, it supports the statement that traumatic resin canals can be found in non-Pinaceae families that normally lack resin canals. Therefore, despite the anatomical similarities of Tetraclinis wood to other genera of Cupressaceae that make their separation difficult,Tetraclinis wood is easy to differenti- ate anatomically from the Cupressaceae genera whose territory it shares – Cupressus and Juniperus – because of the distinctness of the warty layer, which is clearly visible even with light microscopy.

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Other characteristic features are the presence of the three types of parenchyma ar- rangement, as in Taiwania, the low number of pits per cross field and the low value for the most frequent height in number of cells in the rays. The latter feature was considered by Schweingruber (1990), although it also occurs in Diselma, Microbiota, Neocallitropsis, Papuacedrus H.L. Li and Thujopsis. In terms of biometry, two values are noteworthy because they are characteristic of Cupressaceae: the low ray height in number of cells and the low number of cross-field pits (Table 1). A comparison of the biometry with earlier studies (Table 1) shows that, apart from the work by Esteban et al. (1996, 2002), none of the studies are complete. The tracheid diameter range is within the ranges obtained by other authors (Peraza 1964; Esteban et al. 1996, 2002). The highest values for maximum ray height in number of cells are seen in the studies by Peraza (1964), with 20 cells, Esteban et al. (1996), with 28, and this study, with 23. The cause of this difference from the values observed by other authors may be that some samples were from branches and others from stems. Fahn et al. (1986) recorded the presence of lower rays in branch wood than that in mature stem wood in Cupressus and Juniperus. The number of pits per cross field is similar in all cases except the value given by Greguss (1955), who recorded the occasional presence of up to five pits per cross field in the earlywood. Clearly the wood anatomical homogeneity of the Cupressaceae does not facilitate separation of genera and makes separating species even more difficult. However, ob- taining samples of mature wood representative of the genus or the species from their natural distribution areas could make it possible to clarify the differences in some of the existing descriptions, many of which were made using samples of doubtful origin or from branches or juvenile wood. As for phylogenetic classification, the first studies did not resolve the position of Tetraclinis within the Cupressaceae. Analyses of rbcL (Brunsfeld et al. 1994; Gadek et al. 2000) associated Tetraclinis with Thujopsis and Thuja, and NLY analyses as- sociated it with Calocedrus Kurz (Yang et al. 2012), although neither case presented a well-supported clade. However, the study by Gadek et al. (2000) using matK recon- structed a clade consisting of Tetraclinis, Microbiota and Platycladus. By combining molecular data, Little (2006) and Yang et al. (2012) strongly supported the existence of this clade. It shows an interesting wood anatomical diversity. Microbiota has both cupressoid and taxodioid cross-field pits and Platycladus has axial parenchyma with nodular transverse end walls, and its rays have indentures and both smooth and pitted horizontal walls. Greguss (1955) noted the high similarity between Microbiota and Platycladus in the smooth transverse end walls of their longitudinal parenchyma, with perhaps one or two nodules, and differentiated the two genera by the higher number of cupressoid pits in the cross-field pitting ofMicrobiota.

ACKNOWLEDGEMENTS

The authors are grateful to the Directorate General of Natural Heritage and Biodiversity of the Murcia Regional Ministry of Agriculture and Water for collaboration in obtaining the samples required for this study.

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Accepted: 30 September 2014

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