MacedoIAWA et Journalal. – Wood 35 (1),anatomy 2014: of 19–30 Tachigali 19
WOOD ANATOMY OF SEVEN SPECIES OF TACHIGALI (CAESALPINIOIDEAE–LEGUMINOSAE)
Tahysa M. Macedo 1, Claudia F. Barros 2,*, Haroldo C. Lima2 and Cecília G. Costa1, 2 1Programa de Pós-graduação Ciências Biológicas (Botânica), Universidade Federal do Rio de Janeiro, Quinta da Boa Vista s/n, São Cristóvão, 20940-040 Rio de Janeiro-RJ, Brazil 2Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Diretoria de Pesquisa Científica, Rua Pacheco Leão 915, 22460-030 Rio de Janeiro-RJ, Brazil *Corresponding author; e-mail: [email protected]
abstract This article describes the wood anatomy of seven species of Tachigali Aublet with the aim of identifying 1) diagnostic characters at the species level and 2) anatomical features with potential for future combined morphological and molecular phylogenetic analysis. Tachigali species present fibre dimorphism and can be grouped according to the arrangement of the thin-walled fibres: tangential bands of thin-walled fibres alternating with thick-walled fibres, as in T. duckei and T. vulgaris; wavy bands , as in T. paratyensis, T. glauca and T. vulgaris; well-developed bands to describe the abundance of thin-walled fibres in contrast to thick-walled fibres, as inT. denudata and T. pilgeriana; and in islands or groups of thin-walled fibres scattered among ordinary fibres. It is recommended to explore the phylogenetic significance of the different types of fibre dimorphism in future combined molecular and morphological cladistics analyses. Keywords: Wood anatomy, systematics, Sclerolobium, Tachigali, Fabaceae.
INTRODUCTION
Tachigali Aublet includes about 60–70 species and is Neotropical in distribution, extending from Costa Rica to southern Brazil and Paraguay. The greatest number of species occurs in South America (Lewis et al. 2005) with about 70% of the species in Brazil’s Cerrado, Atlantic Rain Forest, and the Amazonian Rain Forest (Silva 2007). These species consist of small to large trees having alternate paripinnate leaves, terminal or lateral racemes or panicules, and fruit strongly laterally compressed and dry (Silva 2007; van der Werff 2008). These hardwood trees are known in Brazil as taxi (Camargos et al. 2001), and they are mainly used in construction (Zenid 1997), but they are also used to build rustic furniture, bridges and fences (Lorenzi 1992, 1998). The wood has also been used in restoration projects, landscaping (Lorenzi 1992, 1998) and as firewood (Oliveiraet al. 2008).
© International Association of Wood Anatomists, 2014 DOI 10.1163/22941932-00000044 Published by Koninklijke Brill NV, Leiden
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Many authors have highlighted the similarity between Tachigali and Sclerolobium, as they differ only in a few flower characteristics, such as the attachment of pistil to stipe, the pubescence of the perianth, and the pattern of the inflorescence (Tulasne 1844; Baillon 1870; Bentham 1865, 1870; Taubert 1892, 1894; Harms 1903, 1928; Dwyer 1954, 1957). As a result, Sclerolobium is considered a synonym of Tachigali based on the similarity of flower morphology (Zarucchi & Herendeen 1993; Barneby & Heald 2002; Pennington et al. 2004; Lewis 2005; Silva & Lima 2007), as well as pollen (Graham & Barker 1981), wood anatomy (Baretta-Kuipers 1981) and molecular characteristics (Haston et al. 2005; Maia 2008). In a review of the tribe Caesalpinieae, Lewis (2005) places Tachigali in the informal “Tachigali group” that also includes Arapatiella Rizzini & A. Mattos and Jacqueshuberia Ducke, which have a cupular hypanthium and stipitate ovary. Haston et al. (2005) found that this group is well sup- ported by molecular data. The wood anatomy of some species of Tachigali has already been examined. Loureiro et al. (1983) presented macroscopic and microscopic descriptions of ten species from the Amazon. Fedalto et al. (1989) macroscopically and microscopically described T. glauca (= T. myrmecophila). Gasson et al. (2003) examined eight species, giving some diagnostic characteristics for the “Tachigali group” (as “Sclerolobium group”), and Pernía & Melandri (2006) analyzed eight species from Venezuela. The present work aims to describe the wood anatomy of seven Tachigali species in order to identify 1) diagnostic characters at the species level and 2) anatomical features with potential for future combined morphological and molecular phylogenetic analysis.
MATERIALS AND METHODS This study was based on 32 samples of seven species of Tachigali (Table 1). Some samples were collected in the State of Rio de Janeiro, and others were provided from the wood collections of the Instituto de Pesquisas Tecnológicas de São Paulo (BCTw)
Table 1. Collection sites and RBw of Trachigali species sampled.
Species Collection sites Wood collection (RBw) T. denudata Floresta da Tijuca (Rio de Janeiro) 3274, 8763, 8764, 8765 Parque Nacional das Fontes do Ipiranga (São Paulo) 9115 T. duckei Parque Nacional de Itatiaia (Rio de Janeiro) 9056, 9057, 9058, 9059, 9060, 9061 T. glauca Floresta Nacional do Tapajós (Pará) 6658, 9116, 9117 T. paratyensis Arboreto do Jardim Botânico do Rio de Janeiro (Rio de Janeiro) 36, 3003, 5205, 9051 T. pilgeriana Arboretum of Jardim Botânico do Rio de Janeiro (Rio de Janeiro) 9052, 9123 Serra de Paranapiacaba (São Paulo) 9118 T. rugosa Parque Nacional de Itatiaia (Rio de Janeiro) 9053, 9054, 9055 T. vulgaris Paracatu (Minas Gerais) 4996 Santarém (Pará) 374, 2374, 9120, 9121, 9122 Caxias (Maranhão) 6107 Tocantins 9119
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Table 2. Summary of the qualitative, differential anatomical features of the species studied. These features were used in PCA (data not shown) and cluster analysis. T. = Trachigali, A. = Arapatiella. — 0 = absent; 1 = present; min /mean /max. T. denudata T. duckei T. glauca T. paratyensis T. pilgeriana T. rugosa T. vulgaris T. A. trepocarpa Growth rings distinct, marked by a distinct fibre zone 1 0 1 0 1 0 0 0 Growth rings indistinct 1 1 0 0 0 1 0 0 Shape of alternate pits polygonal 1 1 1 1 1 1 1 0 Thin-walled fibres in wavy bands 0 0 1 1 0 0 1 0 Thin-walled fibres in tangential bands 0 1 0 0 0 1 0 0 Thin-walled fibres in islands 0 1 1 1 0 0 0 0 Well-developed thin-walled fibre bands 1 0 0 0 1 0 0 0 Thin- to thick-walled fibres 1 1 1 1 1 0 1 0 Thick-walled fibres 0 0 0 0 0 1 0 1 Scanty paratracheal parenchyma 0 1 0 0 0 1 1 0 Vasicentric parenchyma 1 1 1 1 1 1 1 0 Aliform parenchyma 1 0 1 1 1 0 1 0 Banded parenchyma 0 0 0 0 0 0 0 1 Two cells per parenchyma strand 1 0 0 1 1 0 0 0 3–4 cells per parenchyma strand 1 1 1 1 0 1 1 1 5–8 cells per parenchyma strand 0 1 1 0 1 0 1 0 Biseriate rays 1 1 0 1 0 1 0 1 Heterocellular rays 1 1 1 1 1 1 1 0 Silica bodies 0 0 0 0 0 0 1 0 and Instituto de Pesquisas Jardim Botânico do Rio de Janeiro (RBw) (Table 1). The scientific nomenclature followed the “Lista de Espécies da Flora do Brasil 2012” (Lima 2012) and “W³ Tropicos” (http://www.tropicos.org/). Wood sections were prepared in three planes, and their thickness ranged from 15 to 20 µm. All samples were bleached, stained with safranin and astra blue (Bukatsch 1972), dehydrated (Johansen 1940; Sass 1958) and mounted in synthetic resin. The hardest samples were softened by boiling in water or glycerin 50%. When this method failed, polyethylene glycol (PEG) 1500 was used instead (Rupp 1964). Macerations were prepared with Franklin’s solution (Jane 1956), stained with aqueous safranin 1% and mounted on semi-permanent slides with glycerin 50% (Strasburger 1924). The descriptions, measurements and images were obtained with an Olympus BX50 light microscope with a digital image processing system (Image Pro Plus, version 3.0 for Windows) fitted with a video camera (Media Cybernetics CoolSNAP-Pro). The termi- nology followed the “IAWA List of Microscopic Features for Hardwood Identification” (IAWA Committee 1989).
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The fibre dimorphism was defined according to Ter Welle and Koek-Noorman (1978, 1981) and Van Vliet (1981). It should be noted that the two articles used different ter- minology: pseudoparenchyma and fibre dimorphism, respectively. The different arrange- ments of thinner and thick-walled fibres was classified based mainly on Ter Welle & Koek-Noorman (1981), although other important papers were examined to understand these features (Ter Welle & Koek-Noorman 1978; Baas & Zweypfenning 1979; Ter Welle & Koek-Noorman 1981; Van Vliet 1981; Van Vliet & Baas 1984; Baas 1986; Archer & Van Wyk 1993; Graham et al. 1993; Mennega 1997; Olson & Carlquist 2001; Graham et al. 2005; Marcon-Ferreira 2008). As a result, in this study, fibre dimorphism is described as: i) tangential bands of thin-walled fibres alternating with bands of thick- walled fibres (Ter Welle & Koek-Noorman 1981; Van Vliet 1981; Archer & Van Wyk 1993; Olson & Carlquist 2001); ii) well-developed bands with thin-walled fibres more abundant than the thicker-walled fibres (Van Vliet 1981); iii) wavy bands of thin-walled fibres (Ter Welle & Koek-Noorman 1981); and iv) islands or groups of thin-walled fibres scattered among ordinary fibres (Ter Welle & Koek-Noorman 1981). To test the validity of the wood anatomical features in separating the species ana- lyzed, unweighted cluster analysis and principal components analysis (Manly 1994) were performed, and Table 2 summarizes the anatomical features used. All the analyses were carried out in vegan package (Oksanen et al. 2012) from R software (R Devel- opment Core Team 2012). The species Arapatiella psilophylla (Harms) R.S. Cowan (= Arapatiella trepocarpa Rizz. & A.Mattos) was used as an outgroup based on its af- finity withTachigali , according to molecular studies (Maia 2008). The anatomical data for this species were abstracted from Rizzini & Mattos-Filho (1972).
RESULTS
The studied Tachigali species share the following features: small/medium-sized poly- gonal intervessel pits, fibre dimorphism, and both homocellular and heterocellular rays with one row of square and/or upright cells in the margins, all characteristics which separate them from Arapatiella psilophylla (Fig. 1). Furthermore, the observed species can be separated into two different groups based on the expression of fibre dimorphism.
Group I (Table 2 & 3) – T. rugosa (Mart. ex Benth.) Zarucchi & Pipoly (Fig. 1C & 2F) and T. duckei (Dwyer) Oliveira-Filho. Growth rings: indistinct or distinct, if present, marked by thick-walled and flattened latewood fibres; also marked by distinct fibre zones inT. duckei. Vessels: diffuse-porous, solitary and in radial multiples of 2–4; simple perforation plates. Intervessel pits medium-sized (T. rugosa 5–7–9 μm; T. duckei 5–7–10 μm), alternate, vestured, polygonal. Vessel-ray and vessel-parenchyma pits similar to the intervessel pits in size and shape. Libriform fibres: thin-walled fibres in islands and in tangential bands, alternating with thin- to thick-walled bands in T. duckei and thick-walled bands in T. rugosa; forked fibres observed.
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T. vulgaris Figure 1. A: Dendrogram of Cluster Analysis showing the different spe- cies groups formed. T. glauca Light grey – Arapatiella psilophylla separated from Tachigali species by banded parenchyma, rays exclu- T. paratyensis sively homogeneous and presence of oval and minute intervessel pits. T. pilgeriana White line – T. duckei and T. rugosa characterized by thin-walled fibres in tangential bands. T. denudata Dark grey – T. denudata and T. pil- geriana with well-developed thin- T. rugosa walled fibre bands. Black – T. paratyensis, T. glauca and T. vulgaris with thin-walled T. duckei fibres in wavy bands.
A. psilophylla B: A. psilophylla. C: T. rugosa. TS. D: T. paratyensis. E: T. pilgeriana. TS.
TS = transverse section. Scale bar = 100 μm.
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Table 3. Summary of the quantitative anatomical features (average/SD) of the species studied. — T. = Trachigali, A. = Arapatiella. * T. denudata T. duckei T. glauca T. paratyensis T. pilgeriana T. rugosa T. vulgaris T. A. trepocarpa
Vessels (mm²) 5/2.3 4/2 7/2 6/2.2 7/3.2 5/1.6 6/2.2 14 Vessel element length 419/98 447/98 465/109 461/109 404/124 397/86 399/119 625 Vessel diameter 141/67 177/54 144/27 169/60 151/74 192/50 190/60 100 Intervessel pits (µm) 6/1.3 7/1 6/1 9/1 7/1 7/1 7/1 3 Fiber length 1009/177 1126/144 1003/135 1029/182 993/200 1081/148 970/156 1400 Rays (mm) 8/2.5 9/1.6 9/3 9/2 8/3.3 10/3 10/2.6 8 Rays (µm) 284/184 208/64 177/46 220/113 202/54 230/55 182/81 182
*The anatomical data for A. trepocarpa were abstracted from Rizzini & Mattos-Filho (1972) where only the averages were given.
Axial parenchyma: scanty paratracheal, vasicentric, and confluent surrounding two or three vessels; strands of 3–8 cells in T. duckei and 3–4 cells in T. rugosa; chambered crystals present in series up to 28 elements in T. duckei, rare in T. rugosa (series up to 10, when present). Rays: mostly homocellular, composed of procumbent cells, and occasionally hetero- cellular with one row of square marginal cells; uni- and biseriate; disjunctive ray cells frequently observed.
Group II (Table 2 & 3) – T. denudata (Vogel) Oliveira-Filho (Fig. 2A–E), T. glauca Tul., T. paratyensis (Vell.) H.C. Lima (Fig. 1D & 2G), T. vulgaris L.G. Silva & H.C. Lima, and T. pilgeriana (Harms) Oliveira-Filho. Growth rings: distinct and marked by thick-walled and flattened latewood fibres in all species. Tachigali denudata also has growth ring boundaries marked by distinct fibre zones or growth ring boundaries indistinct. Vessels: diffuse-porous; solitary and in radial multiples of 2–5 (T. denudata, T. paratyensis and T. pilgeriana), and 2–4 (T. glauca and T. vulgaris); simple perforation
← Figure 2. A–E. Tachigali denudata. – A: Growth ring boundaries (asterisks), well-developed thin-walled fibre bands (WD), thick-walled fibres (arrowhead). TS. – B: Growth ring boundary (asterisk), well-developed thin-walled fibre bands (WD). TS. – C: Growth ring boundary (aster- isk), well-developed thin-walled fibre bands (WD), thick-walled fibres (arrowhead) traversing areas of thinner walled fibres. TS. – D: Thin-walled fibres (arrows), thick-walled fibres (white arrowheads), axial parenchyma (star). TLS. – E: Thin-walled fibres (arrows), thick-walled fibres (arrowheads), homocellular rays (star). TLS. — F:T. rugosa, thin-walled fibres in tangen-tial bands (TB), and in islands (circles), thick-walled fibres (arrowheads). TS. — G:T. paratyensis, thin-walled fibres in wavy bands (WB). — TS = transverse section; TLS = tangential longitudinal section. — Scale bars = 100 μm.
Downloaded from Brill.com10/01/2021 05:26:14AM via free access 26 IAWA Journal 35 (1), 2014 plates. Intervessel pits small in T. denudata (4–6–10 μm) and T. glauca (5–6–9 μm), but medium-sized in T. paratyensis (7–9–11 μm), T. pilgeriana (6–7–10 μm), T. duckei (5–7–10 μm), and T. vulgaris (5–7–10 μm), alternate, vestured, polygonal. Vessel-ray and vessel-parenchyma pits similar to the intervessel pits in size and shape. Libriform fibres: thin-walled fibres in islands and in wavy bands, alternating with medium-thick to thick-walled fibres inT. glauca, T. paratyensis and T. vulgaris; well- developed thin-walled fibre bands in T. denudata and T. pilgeriana, and forked fibres presented in all species. Axial parenchyma: vasicentric, aliform, and confluent surrounding two or three vessels in all species, scanty paratracheal also observed in T. vulgaris; strands of 2–4 cells in T. denudata and T. paratyensis, 3–8 cells in T. glauca and T. vulgaris, and 5–8 cells in T. pilgeriana; abundant chambered crystals in series of up to 16 elements in T. denudata, 23 elements in T. paratyensis, 25 elements in T. glauca and 26 elements in T. pilgeriana. Rays: mostly homocellular, composed of procumbent cells, and occasionally hetero- cellular with one row of square marginal cells; biseriate and uniseriate in T. denudata and T. paratyensis, but uniseriate only in T. glauca, T. pilgeriana and T. vulgaris; disjunctive ray cells frequently observed; silica bodies observed only in T. vulgaris.
DISCUSSION
The wood anatomical analyses of the studied species demonstrate the similarity of the species previously included in Sclerolobium (Tachigali duckei, T. denudata, T. pilgeri- ana, T. rugosa and T. vulgaris) and in Tachigali (T. glauca and T. paratyensis), as they did not form separate groups. This similarity was previously reported in the literature (e.g., Loureiro et al. 1983; Gasson et al. 2003; Pernía & Melandri 2006) and supports the proposal to merge the two genera (Zarucchi & Herendeen 1993; Barneby & Heald 2002; Pennington et al. 2004; Lewis 2005; Silva & Lima 2007). According to Gasson et al. (2003), the “Tachigali group”, previously known as the “Sclerolobium group”, is characterized by uniseriate, non-storied rays, the cells of which often contain silica bodies, and tangential bands of thick-walled fibres traversing areas of thinner-walled fibres. All these features were found in the studied species, except the silica bodies, which were only found in T. vulgaris and the biseriate rays observed in T. denudata and T. duckei. The prevalence of homocellular rays composed of procumbent cells and the oc- casional presence of heterocellular rays with one row of square marginal cells, as observed by Loureiro et al. (1983), were found in all species analyzed. Disjunctive ray cells were registered in the species analyzed, characteristics already described for other families, such as Myrtaceae (Ragonese 1977) and Sapotaceae (Cozzo 1951 apud Carlquist 2001), but not yet mentioned in Leguminosae, according to the references consulted. The type of axial parenchyma is an important feature for separating tribes of the Caesalpinioideae (Baretta-Kuipers 1981). Gasson et al. (2003) refers to the paratracheal patterns in Caesalpinioideae that form a continuum, which is difficult to record for the
Downloaded from Brill.com10/01/2021 05:26:14AM via free access Macedo et al. – Wood anatomy of Tachigali 27 purpose of cladistics, but may be diagnostic. In our study, the axial parenchyma was important to separate the Tachigali species, and the analysis of more species would be helpful to confirm this feature as a phylogenetic character. Gasson et al. (2003) refer to the potential of the intervessel pitting as a diagnostic and taxonomic feature in the Caesalpinioideae. In the present study, the shape and size of the intervessel pits were important to separate Arapatiella psilophylla, with oval and minute pits, from Tachigali, with polygonal, small or medium-sized pits. The 16 species described by Loureiro et al. (1983) and Pernía & Melandri (2006) have the same features. The intervessel pitting and the detailed description of the vestured pits could be relevant in future combined anatomical and molecular analyses to separate the “Tachigali group” as it was in the Boraginaceae (Rabaey et al. 2010). The occurrence of fibre dimorphism was mentioned in the literature for some families, such as Celastraceae (Janssonius 1908 apud Ter Welle & Koek-Noorman 1978; Archer & Van Wyk 1993; Mennega 1997), Lythraceae (Baas & Zweypfenning 1979; Van Vliet & Baas 1984; Baas 1986), Melastomataceae (Ter Welle & Koek-Noorman 1978, 1981; Van Vliet 1981; Marcon-Ferreira 2008), Moringaceae (Olson & Carlquist 2001), and Sapindaceae (Janssonius 1908 apud Ter Welle & Koek-Noorman 1978). All of these families are in the Rosid clade, to which also the Leguminosae belong. However, the extreme form of fibre-dimorphism resulting in parenchyma-like fibre bands in families like Celastraceae, Lythraceae and Melastomataceae (cf. IAWA Committee 1989) does not occur in the “Tachigali group” or – to our knowledge – other Leguminosae. Carlquist (2012) referred to fibre dimorphism as another type of origin of axial paren- chyma and related it to a division of labor. Similar hypotheses were proposed earlier by Van Vliet & Baas (1984). Although a small number of Tachigali species is described in this study, the fibre dimorphism seems to be promising for combining morphological and molecular analy- sis in the future. The previous literature for the genus did not mention this feature, although Loureiro (1983) described “regions of thick-walled fibres” inTachigali alba Ducke, and Gasson et al. (2003) reported “tangential bands of thick-walled fibres tra- versing areas of thinner-walled fibres” as a characteristic of the “Sclerolobium Group” (now “Tachigali Group”). Maia (2008) demonstrated the monophyly of the “Tachigali group” and the monophyly of Tachigali (including Sclerolobium) by using three DNA regions (trnL-F, rps16 and ITS), but no clades could be defined by any morphological or anatomical character used in Tachigali taxonomy; hence, the homoplastic nature of the morphological characters make it difficult to use them for phylogenetic infra- generic classification. We recommend the use of fibre dimorphism in future combined morphological and molecular data analyses of the “Tachigali group”.
ACKNOWLEDGEMENTS
We thank the Laboratório de Botânica Estrutural and the Instituto de Pesquisas Jardim Botânico do Rio de Janeiro for technical support, the Museu Nacional do Rio de Janeiro-UFRJ where the Master’s thesis was carried out, the Instituto de Pesquisas Tecnológicas that contributed samples, Dr. Arno Brandes, Msc. Luciana Silva, Dr. Vitor Hugo Maia, and Msc. Michel Barros and Robson Daumas (in memoriam) for help during the field work and taxonomic identification, David Martin for the English
Downloaded from Brill.com10/01/2021 05:26:14AM via free access 28 IAWA Journal 35 (1), 2014 language review, and Pieter Baas, Frederic Lens and Elisabeth Wheeler for the careful revision of the manuscript. We also thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), PPBIO (Programa de Pesquisa em Biodiversidade), and FAPERJ (Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro) for the research fellowship grant.
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Accepted: 1 September 2013
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