Wood Anatomy and Evolution: a Case Study in the Bignoniaceae

WOOD ANATOMY AND EVOLUTION: A CASE STUDY IN THE BIGNONIACEAE

Marcelo R. Pace1,* and Veronica Angyalossy*

*Departamento de Botaˆnica, Instituto de Biocieˆncias, Universidade de Saõ Paulo, Rua do Mataõ, 277, Cidade Universita´ria, CEP 05508-090, Saõ Paulo, Saõ Paulo, Brazil

Wood (secondary xylem) is responsible for water transport and has been well-studied anatomically, ecologically, physiologically, and phylogenetically. Comparative methods can reveal patterns of evolution for xylem traits using knowledge from the phylogenetic history of the taxa and the branching pattern of phylogenies. Bignoniaceae (Lamiales) is a family of pantropical plants of various growth habits that includes trees, shrubs, and lianas, which display diverse wood anatomies and for which robust phylogenies are available. Here we review important aspects in classical wood anatomy and evolution and test hypotheses regarding patterns of wood evolution using the Bignoniaceae as a model. Altogether, 85% of the genera currently recognized in Bignoniaceae were sampled, and 30 characters were delimited and mapped onto a robust phylogeny of the family. Some patterns of wood evolution within the Bignoniaceae seem to have been shaped by ecophysiological and habit aspects in the family. For example, vessels increase in diameter in the lianoid lineages but decrease in trees and shrubs during evolution. Rays in trees have evolved from a mixture of homo- and heterocellular to exclusively homocellular and storied in some lineages, while in the lianas the opposite pattern was recorded. Other patterns are consistent with more general phylogenetic trends; for example, parenchyma increases in abundance from the most basal to the most derived nodes of the phylogeny. Other characters in the family that are delimited and discussed include growth rings, porosity, perforation plates, ray width, and height. This work provides evidence that wood evolution is rather labile and that the evolution of new habits and the occupation of new habitats greatly inﬂuence wood evolution.

Keywords: Bignonieae, diversiﬁcation, liana, secondary xylem, Tabebuia, tracheary element.

Online enhancement: appendix.

Introduction Secondary xylem is formed by a lateral meristem known as the vascular cambium, a meristem with two types of initials: In this special issue dedicated to the evolution and devel- fusiform initials, which are vertically elongated, and ray ini- opment of wood plants, this article aims to summarize some tials, which are radially elongated (Eames and MacDaniels of the most fundamental information on wood anatomy and 1925; Evert 2006). Together they differentiate into the sec- evolution to date and to explore xylem evolution in the Big- ondary xylem (fig. 1), undergoing secondary wall deposition noniaceae (Lamiales), a diverse family of pantropical plants. and lignification, with fusiform initials giving rise to the con- Wood (secondary xylem) first appeared in the common an- ducting cells (tracheids and/or vessels), fibers, and axial pa- cestor of the progymnosperms and all extant woody plants by renchyma and ray initials giving rise to rays, which are mainly ∼ the middle Devonian, at 390 Ma (Beck 1962; Meyer- parenchymatous in nature (Evert 2006), although radial tra- Berthaud et al. 2000, 2010; Decombeix et al. 2005, 2011), cheids (Thompson 1910; Gordon 1912; Eames and Mac- aside from independent evolution of wood in the extinct ar- Daniels 1925), perforated ray cells (Chalk and Chattaway borescent lycophytes and monilophytes (Kenrick and Crane 1933; Van Vliet 1976; Machado et al. 1997; Sonsin et al. 1997; Simpson 2010). Altogether, the extinct progymnosperms 2008), and radial fibers (Lev-Yadun 1994) can also be present and all extant woody plants form a monophyletic group in rays. The tracheids and vessels are nonliving cells at maturity known as the lignophytes (Meyer-Berthaud et al. 2010; Simp- (Eames and MacDaniels 1925; Bailey 1953; Esau 1960; Pen- son 2010), and all of them likely share a homologous genetic nell and Lamb 1997; Groover and Jones 1999; Fukuda 2000; developmental toolkit (Groover 2005). The evolution from a Bolho¨ ner et al. 2012), while fibers can be living or nonliving simple to a more complex vascular system was likely triggered (Eames and MacDaniels 1925; Fahn and Arnon 1963; Itabashi by the occupation of land and by moving from a more mesic et al. 1999; Bolho¨ ner et al. 2012). Axial and ray parenchyma to a drier climate (Kenrick and Crane 1997; Carlquist 2012). are living at maturity (Esau 1960; Carlquist 1961; Catesson 1990; Nakaba et al. 2006, 2008, 2012a, 2012b), except in 1 Author for correspondence; e-mail: [email protected], heartwood (Stewart 1933; Esau 1960; Nakaba et al. 2012b). [email protected]. All the living cells in the wood play a physiological role in Manuscript received August 2012; revised manuscript received February 2013; food storage and transport (Chaffey and Barlow 2001; Nakaba electronically published August 7, 2013. et al. 2006, 2012a; Yamada et al. 2011), embolism repair

1014 PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1015

1957; Bailey and Howard 1941a, 1941b, 1941c). In their ar- ticles, Bailey, Frost, Cheadle, and coauthors suggested a pattern of evolution for both the vessels and the fibers in which both derived cell types depart from an ancestral tracheid (fig. B1; figs. B1–B3 are available online). On the basis of the evolution of these perforate and imperforate tracheary elements, “lines of evolution” were proposed for axial and ray parenchyma of the secondary xylem (Kribs 1935, 1937; Barghoorn 1940, 1941a, 1941b; figs. B2, B3). The evolution of these cell types was based mainly on statistical correlations, first between the type and morphology of tracheary elements and the taxonomic groups (Bailey and Tupper 1918; Frost 1930a, 1930b, 1931) and later on the type of tracheary elements, the types of axial and ray parenchyma cells, and their arrangements (Kribs 1935, 1937). Altogether these putative evolutionary trends were named “major trends of xylem evolution” by Carlquist (1961) and have strongly influenced numerous theories on xylem cell evolution to date. According to these theories, vessels and fibers evolved from tracheids, and the more similar a vessel is to a tracheid, the more primitive it would be considered (Bailey and Tupper 1918). Regarding ray evolution, Kribs (1935) suggested that the most primitive condition was that of woods with both multiseriate and uniseriate rays cooccurring, with both rays being high and heterocellular in composition. Ac- cording to Kribs (1935), ray evolution involved a gradual decrease in height and number of upright and square cells as Fig. 1 Drawing illustrating the secondary xylem of Handroanthus chrysotrichus, indicating vessels, fibers, and axial and ray parenchyma seen in longitudinal section, eventually evolving into a ho- in the three planes, transverse, radial, and tangential. Drawn by M. mocellular ray (Kribs 1935; fig. B2). For axial parenchyma, Kubo. the primitive type of axial parenchyma was inferred as apotracheal scanty or diffuse, evolving toward progressively larger volumes of parenchyma within the stem and in association (Holbrook and Zwieniecki 1999; Salleo et al. 2004), biological with the vessels (paratracheal parenchyma; Kribs 1937; Carl- defense, or heartwood formation (Stewart 1933; Nakaba et quist 1961; fig. B3). al. 2012b). Since part of the cells are alive in the secondary A caveat of these theories was that the possible mechanisms xylem (sapwood), it is possible, in turn, to perform molecular involved in the evolution of wood were not fully explored. techniques such as DNA and RNA extraction (Oh et al. 2003; Nowadays, it is clear that the environment has an enormous Nieminen et al. 2008), allowing species identification (DNA impact on wood anatomical features (Carlquist 1966, 1975, barcoding of woods; Ho¨ ltken et al. 2012), compilation of gene 1988; Van der Graaff 1974; Van den Oever et al. 1981; Baas expression profiles (Ko and Han 2004; Nieminen et al. 2008), and Schweingruber 1987; Alves and Angyalossy-Alfonso and in situ hybridization (Groover et al. 2006). 2000, 2002), with even closely related taxa having marked Because many cell types constitute the secondary xylem, this differences depending on their growth provenance (e.g., Ilex tissue is considered complex (Evert 2006), and a great deal of spp.; Baas 1973). Some ecological trends are nowadays well diversity in the spatial distribution of its cells can be observed. established for ecological wood anatomy and have been sug- That different taxa can have a totally different distributional gested to be one of the main drivers of wood evolution through pattern of these cells allows us to recognize many plant taxa adaptation (Baas et al. 2003). Vessels, for instance, were shown solely by their wood tissues (Record and Hess 1943; De´tienne to decrease in length and diameter from lower to higher lat- and Jacquet 1983; Schweingruber 1990; reviewed in Wheeler itudes, while the inverse occurs to the abundance of vessels and Baas 1998). Two contrasting examples of such organiza- with scalariform perforation plates and helical thickening tions from tropical woods are seen, for example, in the Sap- (Baas 1973; Van der Graaff and Baas 1974; Baas and Schwein- otaceae and the Leguminosae. Most of the Sapotaceae are dis- gruber 1987; Baas et al. 1983, 2003; Noshiro and Baas 2000). tinctive by having narrow and multiple vessels radially arranged Toward lower latitudes, axial parenchyma is usually more and axial parenchyma in lines, while most of the Papilionoideae abundant, with the rays thinner and the fibers thicker (Baas legumes can be recognized by their wide and solitary vessels in 1973; Wheeler and Baas 1991; Alves and Angyalossy-Alfonso multiples of two or three, with paratracheal, aliform, confluent 2002). These statistically proved correlations evidence that parenchyma forming bands and a storied organization. wood responds actively to environmental conditions, in which The first theories on xylem evolution can be traced back to case convergences (homoplasies) are expected and indeed have the seminal work of Bailey and Tupper (1918), discussed and been recorded in several wood anatomical studies (Baas and further developed by Frost (1930a, 1930b, 1931) for the dicots Wheeler 1996). Despite that, wood anatomy exhibits phylo- and by Cheadle (1943a, 1943b, 1944) for the monocots, in genetic signal in a number of cases, such as the presence of addition to Bailey’s own studies (Bailey 1920, 1944, 1953, broad and tall rays in the fairly dissimilar families that com- 1016 INTERNATIONAL JOURNAL OF PLANT SCIENCES pose the Cucurbitales (e.g., Anisophylleaceae, Begoniaceae, authorship, number of specimens analyzed, and collection in- Cucurbitaceae, Tetramelaceae; Baas et al. 2003); the presence formation). The family has been currently subdivided into nine of vesture pits in entire orders, such as the Gentianales and well-supported clades (Olmstead et al. 2009): Bignonieae, Jac- Myrtales (Jansen et al. 2001; Baas et al. 2003); and the pres- arandae, Tourrettieae, Tecomeae, Oroxyleae, Catalpae, the Ta- ence of crystals delimiting a clade of Spathelioideae (Rutaceae) bebuia alliance (including Crescentieae), the Paleotropical clade from the Old World that reunites rather morphologically dis- (including Coleeae), and the genus Delostoma (see fig. 2 for similar genera (Appelhans et al. 2012). Therefore, our goal their phylogenetic relationships). Genera from all clades were here was to explore the wood anatomical diversity in the Big- sampled except for Tourrettieae, a small group of herbaceous noniaceae and to map this diversity onto a robust phylogeny Andean plants that could not be obtained. No outgroup was of the family to depict the pattern of wood evolution and its used in the ancestral character state reconstructions since the possible drivers in this monophyletic family. inclusion of outgroups for this type of reconstruction would be advisable only when the ancestral state of the entire sister lineage The Bignoniaceae can be inferred; otherwise, it would lead to reconstruction bias. Since the Bignoniaceae are placed in a polytomy with seven other The Bignoniaceae belong to the Lamiales (core eudicots; families of Lamiales (Stevens 2001–; APG III 2009; Scha¨ferhoff APG III 2009) and forms a monophyletic group of plants et al. 2010), it was more conservative to make reconstructions (Spangler and Olmstead 1999; Olmstead et al. 2009) with a exclusively with the ingroup. pantropical distribution and center of diversity in the Neo- Most species analyzed are from the slide collection of Forest tropics (Gentry 1980). Only a few species occur naturally in Products Laboratory (MADw, SJRw), Madison, Wisconsin, temperate or Neotropical montane regions (e.g., Bignonia except for a few samples that either came from other xylaria capreolata, Catalpa section Catalpa spp.; Fischer et al. 2004; (BCTw, Kw) or were collected by the authors (app. A). We Lohmann 2004; Li 2008). The systematic relationships among selected samples exclusively from mature specimens with thick members of the Bignoniaceae have been carefully explored in stems (thicker than 5 cm), except for lianas. Most lianas of the last few years (Zhjra et al. 2004; Lohmann 2006; Grose both tribe Bignonieae and Tecomeae were collected and pro- and Olmstead 2007a, 2007b; Li 2008), and a robust phylogeny cessed by us (app. A). We standardized all liana samples used and classification for the entire family is now available (Olm- in this study to be 2.0 cm in diameter because it has been stead et al. 2009). The Bignoniaceae is well known, since many shown that lianas of this width represent mature plants already of its members have economical (Record and Hess 1943; Mai- in the canopy (Gerwing et al. 2006); it is the most common nieri and Chimelo 1989) and ornamental importance due to diameter found in the field (Schnitzer et al. 2006). In addition, their showy tubular flowers (eight countries have Bignoniaceae the stem diameter has been shown to represent a better proxy as their national trees; Gentry 1992; Lohmann 2004). The for the multiple qualities of the stem than age (Rosell and family is composed mainly of trees and lianas, with a few Olson 2007), therefore ensuring that we had comparable sam- shrubs and herbs (e.g., Argylia in the Andes and Incarvillea in the Himalayas, both herbaceous; Fischer et al. 2004). The family is especially suitable for evolutionary studies since the stem and wood anatomy of many species has already been documented (Gasson and Dobbins 1991; Dos Santos and Mil- ler 1992, 1997; Dos Santos 1995; Pace et al. 2009, 2011; Lima et al. 2010). Interest in the group is motivated in part by the economic importance of wood derived from trees (Record and Hess 1943) as well as by the widespread presence of cambial variants in the lianas (Schenck 1893; Solereder 1908; Dobbins 1971; Pace et al. 2009; Lima et al. 2010). However, previous studies have explored only certain taxonomic groups within the Bignoniaceae, and at present we have a fragmentary view of the wood diversity in the family as a whole. What we do know is that the Bignoniaceae includes diverse wood anatomy, which makes the family a good model in which to study the evolution of wood diversity. We examine here patterns of evolution of all variable xylem characters in the Bignoniaceae and develop hypotheses con- cerning possible triggers of their evolution.

Material and Methods

Taxon Sampling and Anatomical Procedures One hundred three species were sampled (181 specimens), representing 66 of the 77 genera presently recognized in the Bignoniaceae (∼85%; data on the number of genera were re- Fig. 2 Phylogenetic relationships of major Bignoniaceae clades, as trieved from Olmstead et al. 2009; see app. A for species names, proposed by Olmstead et al. (2009). PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1017

Table 1 Characters and Character States Included in This Study Character Character states 1 Habit: self-supporting (0); vine/liana (1); herb (2) 2 Porosity: diffuse (0); semi-ring-porous (1); ring-porous (2) 3 Growth ring marker, parenchyma: absent (0); present (1) 4 Growth ring marker, dilated rays: absent (0); present (1) 5 Growth ring marker, flattened fibers: absent (0); present (1) 6 Vessel arrangement: diffuse (0); tangential bands (1); radial pattern (2) 7 Vessel grouping: solitary (0); solitary to multiples of two or three (1); radial multiples of four or more common (2) 8 Vessel dimorphism: absent (0); present (1) 9 Perforation plate: simple (0); multiple reticulate/foraminate (1) 10 Helical thickening: absent (0); present (1) 11 Axial parenchyma: scanty paratracheal (0); vasicentric (1); aliform (2) 12 Confluence: absent (0); short (1); long, forming bands (2) 13 Diffuse parenchyma: absent (0); present (1) 14 Parenchyma strands: two cells per strand (0); three or four cells per strand (1); five to eight cells per strand (2) 15 Storied structure: absent (0); present (1) 16 Ray width in number of cells: uniseriate (0); 2–4-seriate (1); 5–10-seriate (2) 17 Ray height: short, !1 mm (0); tall, 11mm(1) 18 Ray composition: homocellular (0); homo-heterocellular with one row of upright marginal cells (1); heterocellular with two to four rows of upright or square cells in the margins (2); heterocellular with procumbent, square, and upright cells mixed throughout the ray (3) 19 Vessel-ray pitting: similar to intervessel pits (0); simple to semiareolate (1) 20 Septate fibers: absent (0); present (1) 21 Perforated ray cells: absent (0); present (1) 22 Crystals: absent (0); present in rays (1); present in rays and axial parenchyma (2) 23 Climate of occurrence: tropical (0); subtropical humid (1); subtropical arid (2); subtropical montane (3); temperate (4) ples. Whenever found, however, thicker portions of liana stems First, given that the paratracheal parenchyma is widespread were also collected and processed to guarantee that we were in the family but still includes differences, the first character not missing important data on their wood anatomy. When delimited was the paratracheal parenchyma type, with three differences were encountered, they were explicitly expressed states: scanty, vasicentric, and aliform. The confluence of the in the results. parenchyma, when present, can vary from short to long con- Specimens that we collected in the field were immediately fluences, which represent two character states. In addition, fixed in FAA50-70 (Berlyn and Miksche 1976) and then trans- diffuse parenchyma in combination with paratracheal paren- ferred to 50%–70% ethanol. Since species in the tribe Big- chyma was found in a few species, leading to another character nonieae possess variant secondary growth, to obtain satisfac- with two states, absent and present. It is likely that these char- tory sections we followed the methods described in Barbosa acters are not independent; however, these subdivisions were et al. (2010). Sections were double-stained in astra blue and created to guarantee that no diversity in their distribution would safranin (Bukatsch 1972) and mounted in a synthetic resin to be missed, although we have also considered them together. create permanent slides. Regarding the continuous (quantitative) characters, seven characters were delimited for 68 of the 103 species analyzed Character State Delimitation, Ancestral Character qualitatively. The characters delimited included (i) vessel fre- State Reconstruction, and Phylogenetic quency, (ii) vessel diameter, (iii) parenchyma frequency, (iv) single Independent Contrasts parenchyma cell area measured in transverse section, (v) ray Wood anatomical characters and character states were de- width in micrometers, (vi) ray width in number of cells, and limited according to their variation within the Bignoniaceae. (vii) intervessel pit diameter measured in tangential sections. The 2 Altogether, 23 qualitative characters were delimited (table 1) cell frequencies were calculated within a grid of 0.2 mm , and for all cell types present in wood (vessels, fibers, and axial and both wide and narrow vessels were counted whenever vessel ray parenchyma). In table 1 a list of characters and coded dimorphism was present. Because most axial parenchyma cells character states is provided. The qualitative results for each were generally asymmetrical, their area was calculated instead analyzed species can be found in table 2, while the quantitative of their diameter. All measurements were performed using the characters are depicted in table 3. Although we have mainly free software ImageJ (ver. 1.45s; Rasband 2012), with a mini- used the International Association of Wood Anatomists mum of 30 repetitions. Numbers shown in table 3 correspond (IAWA) list of microscopic features for hardwood identification to means accompanied by standard deviations. For vessels and (IAWA Committee 1989) as the basis for the delimitation of intervessel pit diameters, the data are presented numerically in characters, adjustments were made according to variations spe- table 3 and used for character state reconstructions. cific to the Bignoniaceae (table 1). For instance, three char- A robust molecular phylogeny of the Bignoniaceae (Olm- acters were delimited for the axial parenchyma distribution. stead et al. 2009) was used as the basis for ancestral character Characters Explained in Table 1) currence (Numbers Correspond to Table 2 ical Characters, and Climate of Oc 1234567891011121314151617181920212223 10111011000001011311100 11111011000001011310?10 1111101*1000001121301100 10101011000/1001121301100 00100010000200110000020 00100010000200110000000 10001011000002011301?00 1000?011000001021301100 1210101101000101030?1?4 10111011000001011301100 10111011000001011301100 1010101*1001101010301100 12001011010001010201104 01101010000001010110004 10100010002001010111011 01001010011001010110004 00101010002000/1010100002 01101010010001010111002 001000101011/201100000020 00100010001201100000000 00101010000001000311000 1010001100000101?310100 00100110002201110000000 0010021/20000001010101011 00001010102201010100/1000 00101010002101010100000 1000101*1000001100101100 1010101*1000001100101100 001000101021/201000000000 001010101021/20100/10100000 01101010001101010000000 00100010000000/1110000000 00111010002001010100000 01101010000001010100010 0010?01000000200/11300000 1111101*1001102010311100 1000101*1001101011301100 01100110001101110100010 00001010002100110000000 00101010002100110000000 00101010002200110000000 00011010002101110000000 00111010002100110000000 001000100021010101110?0 00100010000001010111010 0010101000220100/10000010 00001010002202010000010 00100010002201000000000 00111010002101010200000 Categoric Matrix of Habit, Anatom Adenocalymma divaricatum Amphilophium crucigerum Amphilophium pulverulentum Amphitecna latifolia Amphitecna regalis Anemopaegma chamberlaynii Bignonia campanulata Bignonia capreolata Bignonia magnifica Bignonia prieurei Callichlamys latifolia Campsis radicans Catalpa bignonioides Catalpa longissima Catalpa speciosa Catophractes alexandrii Chilopsis linearis Crescentia alata Crescentia cujete Cuspidaria pulchra Cuspidaria convoluta Cybistax antisyphilitica Delostoma integrifolia Deplanchea bancana Digomphia densicoma Dolichandra unguiculata Dolichandra unguis-cati Dolichandrone atrovirens Dolichandrone spathacea Ekmanianthe actinophylla Ekmanianthe longiflora Fernandoa adenophylla Fernandoa magnifica Fridericia platyphylla Fridericia samydoides Fridericia speciosa Godmania aesculifolia Handroanthus albus Handroanthus barbatus Handroanthus chrysotrichus Handroanthus impetiginosus Handroanthus serratifolius Heterophragma quadriloculare Heterophragma sulfureum Jacaranda brasiliana Jacaranda copaia Jacaranda obtusifolia Jacaranda puberula Species Adenocalymma comosum

1018 wide vessels. p 1111001100200101/21301100 01100010101201110100000 00100010001201110100000 00111010002101010200000 00101010002201010010000 1001101*1001101010101100 11101011001101010301100 10011011000001011301100 01101010002101010100011 01101010102101010100011 10101221000001011301100 0010101000220101010(1)000 00101010101101010000000 10001011000001010301110 00100010102201010100000 00001010002111000000010 00111010102101010011000 10001211000002011301110 0000101000210101011(1)000 11101011000002011301?00 00111010001000/10/110000000 001000101021/211010000/1000 11011011000002011301100 00001010002111000000000 10011011000001001301100 10101011000002010301100 11111011000001011301100 0010101000210101010(1)000 0010101010210101010(1)010 0010101000110101010(1)000 0010001000110101010(1)000 00101010011111000000010 00/1101010001101110000000 00111010001101110100000 00100010002200010100000 00100010102101110000000 00100010002101010001000 1011101*1000001010301100 00100010102101110000000 00100010002201110000000 001010100021/201100000010 001010100021/201110000000 001010100021/201(1)10000000 001010100021/200110000000 0010101000210110/10000000 10101011001001011301100 00100010000001010200003 00001010000001010200003 00100010011101010201013 10???0110000010?1301?10 01111110001201010000000 11101011002101010101100 0/10001010000001010301101 present but rare, * p unsampled, () p Note. ? Zeyheria montana Zeyheria tuberculosa Kigelia africana Lundia damazii Manaosella cordifolia Mansoa difficilis Markhamia lutea Markhamia stipulata Martinella obovata Mayodendron igneum Millingtonia hortensis Neojobertia mirabilis Newbouldia laevis Ophiocolea floribunda Oroxylum indicum Pachyptera kerere Pajanelia longifolia Pandorea jasminoides Paratecoma peroba Parmentiera macrophylla Perianthomega vellozoi Phyllarthron bojeranum Pleonotoma melioides Podranea ricasoliana Pyrostegia venusta Radermachera gigantea Radermachera glandulosa Radermachera pinnata Radermachera sinica Rhodocolea telfarii Roseodendron donnell-smithii Sparattosperma leucanthum Spathodea campanulata Spirotecoma spiralis Stereospermum chelonoides Stizophyllum riparium Tabebuia aurea Tabebuia cassinoides Tabebuia fluvialitis Tabebuia heterophylla Tabebuia obtusifolia Tabebuia rigida Tabebuia roseoalba Tanaecium pyramidatum Tecoma cochabambensis Tecoma fulva Tecoma stans Tecomanthe dendrophila Tecomaria capensis Tecomella undulata Tynanthus cognatus Xylophragma pratense Jacaranda ulei

1019 m) m 5 5 6 9 5 3 4 6 3 6 5 4 5 6 6 4 8 6 11 5 5 7 6 7 3 7 5 4 4 7 5 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ) Ray width ( 2 m m 66 19 16149140 35 15 19 44 20 311 25 65136448 42 17 16 65231 26 32 21109114 20 15 32 22 30 87 26 10662113 21 33 27 53 41 2311011596 34 25 141 21 28 40 35 ? 37 18 15213377 20 30 24 9572 41 18 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע mean area ( Axial parenchyma cell frequency (%) Axial parenchyma 3 2 200 1 14 354 2 11 187 2 3 111 2 7 557 23 6 6 185 811 34 2 7 246 388 2 4 128 13 7 4 310 277 11 62 1 2 192 .813 19 1 4 321 268 351 3 4 171 4?2? ? ?2? ? ? ? ? 232 183 34 5 13 504 492 257 494 17 89 1 1 155 2? ? ? 1 1 113 242 10 9 5 313 685 278 13 23 1 300 171 m) m ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע size ( Intervessel pit 8 5.6 7 4.1 8 5.2 7 7.3 9 5.2 8 11.1 9 5.3 4 6.4 6 8.2 6?? ? ? 10 11.2 11 9.0 8 7.2 m) m ע ע ע ע ע ע ע ע ע ע ע ע ע Table 3 119 NA NA 5.4 ? 45 539 15 28 16 31 25 NA ? 29 501 816 19 NA 4.3 10 NA 6.3 36 26 29 NA 6.5 22 NA 6.1 60 33 17 32 64223 NA NA 16 3.1 9.4 12 NA 4.0 15 12 1126 NA NA 19.1 8.3 82 NA NA 5.3 12.2 36 26 22 19 7408 NA NA NA 7.2 8.4 10.3 10 NA 4.2 28 26 2037 NA 20 6.1 19 NA 5.2 29 27 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע Mean vessel diameter ( Anatomical Continuous Characters of Bignoniaceae ) Wide vessels Narrow vessels 2 755 459 22 137 10 142 769 663 61 106 4 131 11 200 6 107 972 36 293 3 204 445 547 125 111 20 70 32 70 997 6 112 165 42 125 91 158 868 510 300 75 17 45 10 137 572 36 133 21 92 25 156 ?? ?????? ? ? ????? ? ?A?? ? ??NA?? ?? ?????? ? ?A?? ? ??NA?? ?A?? ? ??NA?? ?????? ? ??? ? ? ? NA NA NA 11.2 12.4 11.3 ?? ?????? ? ?74 ? ? ??NA?? ? ? NA 10.9 ?A?? ? ??NA?? ?????? ? ?A?? ? ??NA?? ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע 9 6 6 3 48 31 16 34 11 14 13 10 98 10 43 46 25 14 26 12 21 10 28 45 14 73 (per mm 131 122 140 236 320 118 Vessel frequency Bignonia prieurei Crescentia alata Crescentia cujete Bignonia capreolata Bignonia magnifica Bignonia campanulata Chilopsis linearis Catophractes alexandrii Amphitecna latifolia Amphilophium pulverulentum Amphitecna regalis Anemopaegma chamberlaynii Catalpa longissima Catalpa speciosa Ekmanianthe actinophylla Dolichandrone atrovirens Dolichandrone spathacea Ekmanianthe longiflora Amphilophium crucigerum Catalpa bignonioides Cybistax antisyphilitica Dolichandra unguiculata Dolichandra unguis-cati Delostoma integrifolia Deplanchea bancana Digomphia densicoma Adenocalymma divaricatum Handroanthus barbatus Handroanthus chrysotrichus Heterophragma quadriloculare Godmania aesculifolia Handroanthus albus Handroanthus impetiginosus Handroanthus serratifolius Campsis radicans Callichlamys latifolia Jacaranda puberula Jacaranda brasiliana Cuspidaria pulchra Cuspidaria convoluta Heterophragma sulfureum Jacaranda copaia Jacaranda obtusifolia Species Adenocalymma comosum Fridericia platyphylla Fridericia speciosa Fernandoa magnifica Fridericia samydoides Fernandoa adenophylla

1020 8 6 5 5 2 4 18 5 9 4 20 8 4 5 10 4 8 3 7 3 5 8 5 6 18 7 3 7 8 2 9 7 12 3 8 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע 78105 50 34 52 30 328012428 52 35 14 35 4591 57 18 3245 32 20 53121 63 40 38 19 60 15 50 ? 55 31 55 13 140 33 28268118 25 24 12 455299744 29 41 21 30 4413240114 53 21 21 33 65 12 144 31 6412642236 30 39 32 39 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע 4 2 244 3 8 221 1 4 116 2211 1 10 14 3 165 278 259 206 13 1 9 154 213 2 12 165 1? ? ? 12 9 14 276 291 3 4 103 2 1 167 3 1 113 3 7 123 2 1 100 1 14 212 2? ? ? 312 2 26 27 103 505 366 212 38 16 10 1198 356 359 2 3 127 2 5 185 142 7 .5 7 338 106 374 2 5 126 3? ? ? 2 27 499 12141 86 13 18 22 279 371 577 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע 11 7.0 8 8.4 9 9.6 9 6.0 5?380 5 1.6 7 6.2 6 12.4 7 8.8 6 8.3 5 8.3 9 9.4 3 6.9 5 7.6 7 10.3 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע 26 NA 3.1 914 NA NA 4.3 2.2 25 NA 5.1 32 35 34 NA 5.2 6 NA 4.3 15 23 13 NA 6.7 26 29 25 22 14 14 65 15 18 19 43 23 15 NA54 21 4.3 12 NA 8.3 18 NA 5.3 191428 NA NA 24 4.7 2.2 134 NA NA 4.3 5.6 2337 NA 17 9.0 1325 NA 15 7.5 26 NA 7.2 57 20 3456 NA NA 7.8 10.7 181130 NA NA 14 2.5 6.3 25 16 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע 880 974 877 597 19 192 29 96 10 44 17 112 16 59 18 138 14 139 17 83 15 265 20 66 20 216 10 66 40 290 754 4 179 51212 133 68 118 1138 73 30 1125 70 208 1427 51 167 4 137 30 232 510 136 158 181919 83 50 190 7 109 ?A?? ? ??NA?? ?A?? ? ? ? ? ? ??NA?? ??NA?? ??NA?? ?A?? ? ??NA?? ?A?? ? ??NA?? ? ? NA 6.3 ?A?? ? ??NA?? ?A?? ? ? ? ? ? ? ? ???NA?? ??NA?? ??NA?? ??NA?? ? NA 5.2 ?A?? ? ? ? ? ? ??NA?? ??NA?? ??NA?? ? ? NA 10.2 ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע ע 4 6 8 9 27 24 34 12 51 97 49 47 30 75 20 33 14 60 27 11 21 35 28 28 47 39 88 60 52 100 109 165 126 142 101 100 not applicable. p unsampled, NA p Note. ? Millingtonia hortensis Mayodendron igneum Neojobertia mirabilis Radermachera glandulosa Radermachera sinica Rhodocolea telfarii Radermachera gigantea Radermachera pinnata Roseodendron donnell-smithii Sparattosperma leucanthum Martinella obovata Markhamia lutea Markhamia stipulata Parmentiera macrophylla Paratecoma peroba Perianthomega vellozoi Zeyheria montana Zeyheria tuberculosa Pyrostegia venusta Mansoa difficilis Pandorea jasminoides Pajanelia longifolia Xylophragma pratense Podranea ricasoliana Manaosella cordifolia Tabebuia cassinoides Tabebuia obtusifolia Tabebuia rigida Tabebuia roseoalba Tanaecium pyramidatum Tabebuia aurea Tabebuia fluvialitis Tabebuia heterophylla Newbouldia laevis Ophiocolea floribunda Oroxylum indicum Pachyptera kerere Tecoma fulva Tecoma stans Tecomaria capensis Tecoma cochabambensis Tecomanthe dendrophila Tecomella undulata Tynanthus cognatus Phyllarthron bojeranum Pleonotoma melioides Kigelia africana Lundia damazii Jacaranda ulei Spathodea campanulata Spirotecoma spiralis Stereospermum chelonoides Stizophyllum riparium

1021 1022 INTERNATIONAL JOURNAL OF PLANT SCIENCES state reconstruction of both qualitative and quantitative char- species, such as those in the genus Catalpa, grow at the geo- acters. The tree topology was based mainly on Olmstead et graphical limits of the distribution of the family, having occupied al. (2009), with more information and resolution on the subtropical and temperate regions (tables 1, 2; fig. 4B,4E). branches manually corrected on the basis of more specific stud- There are even a few lianas, such as Bignonia capreolata and ies with single clades of the family (e.g., for tribe Coleeae, Campsis radicans (fig. 4C,4D), growing in temperate regions Zhjra et al. 2004; for tribe Bignonieae, Lohmann 2006; for that have semi-ring-porous to ring-porous woods. Even in the the Tabebuia alliance, Grose and Olmstead 2007a, 2007b;for tropics, a number of species, both self-supporting and lianas tribe Catalpae, Li 2008). All analyses of ancestral character (especially in Bignonieae), live in marked seasonal environments reconstructions were performed in Mesquite (ver. 2.75; Mad- with a conspicuous dry season (e.g., Catophractes alexandrii, dison and Maddison 2009) with both parsimony and maxi- an extreme example from subtropical Africa), and these species mum likelihood algorithms. Whenever differences were ob- usually develop semi-ring-porous woods (tables 1–3). tained from these two different reconstruction inferences, the results for both were presented. In addition, to estimate Vessels whether the continuous characters had a pattern of evolution independent from their phylogenetic history, phylogenetic in- Vessel diameter. The Bignoniaceae have a wide diversity dependent contrasts were performed using the Phenotypic Di- of vessel diameters, even among only self-supporting plants. versity Analysis Program (PDAP; ver. 1.15; Midford et al. These range from very narrow vessels of 30 mm in shrubs of 2003) implemented in Mesquite 2.75. Tecomaria capensis to wide vessels of 300 mminJacaranda copaia (table 3; fig. 5A–5C). The lianas have vessel dimorphism Results (fig. 3E)—a combination of very wide and narrow vessels— and in general the difference between these two categories is Wood Anatomy of the Bignoniaceae remarkable: the wide vessels are up to 250–350 mm in some specimens, and the narrow vessels can be as narrow as 12 mm The more general wood anatomical features of the Bigno- in width (e.g., Xylophragma pratense; table 3). When the vessel niaceae are presented here and summarized in tables 1–3. In diameter is reconstructed, the highest values are concentrated the Bignoniaceae, the vessels are arranged mostly in a diffuse- in the tribe Bignonieae (fig. 5D)—a tribe formed mainly of porous fashion (fig. 3A,3B), with distinct growth rings usually lianas—with an increase in the vessel diameter toward the most marked by the presence of a band or line of marginal paren- terminal nodes (fig. 5D). The opposite scenario is seen in the chyma (fig. 3A,3B) and sometimes also with locally dilated clade Crescentiina (Tabebuia alliance ϩ Paleotropical clade), rays (fig. 3C) and radially flattened fibers. Vessels are oval to with an ancestral diameter reconstructed as 104 mm, while the circular in outline, solitary to multiples of two or three (fig. following nodes present increasingly lower values (fig. 5D), 3A–3C), with perforation plates of horizontal end walls bear- indicating a decrease in diameter along evolution in the most ing simple perforation plates; intervessel pits are round in out- species-rich clade of trees in the Bignoniaceae. line and alternate (fig. 3D), and vessel-ray pitting is similar to Vessel arrangement. Most species in the Bignoniaceae intervessel pits in size and shape. All lianas studied developed have a diffuse arrangement of vessels (fig. 6A), except for a very wide vessels (maximum diameter ∼200–350 mm; see table few exceptions that have vessels arranged in a radial pattern 3), and these were always associated with very narrow vessels (fig. 6B) or in tangential bands (fig. 6C). The radial arrange- (15–35 mm; see tables 1–3; fig. 3E), a feature called vessel ment has evolved independently three times in the Bignoni- dimorphism that is absent in trees and shrubs (fig. 3A,3B, aceae (fig. 6D), once in Delostoma and twice in the tribe 3F). The wood of the Bignoniaceae usually has a straight grain Bignonieae (Pachyptera and Martinella). The tangential ar- (fig. 3G; axial elements parallel to the longitudinal axis), but rangement is also homoplastic, having evolved once in a clade a wavy grain can be present in some specimens (fig. 3H). Ty- that reunites Godmania and Cybistax and in the genus loses are present in the heartwood of several species (fig. 3F) Tecomella (fig. 6D). The ancestral character state for the tribe and occur more rarely and sparsely in the lianas (fig. 3C). The is inferred as diffuse (fig. 6D). axial parenchyma is paratracheal in all species (fig. 3A–3C, Helical thickening in the lateral walls. Helical thickening 3E,3F). Fibers are always libriform, generally with minute, is rare in the Bignoniaceae but is present in species growing inconspicuous pits and thin to thick walls. Crystals are un- in temperate (e.g., Bignonia capreolata, Catalpa, Chilopsis; fig. common and randomly distributed in the family; when present, 7A), montane (e.g., Tecoma stans), and arid (e.g., Rhodocolea they are usually in the ray cells (fig. 3I) and occur more rarely telfarii; fig. 7B) regions. When present in lianas, it occurs in in the axial parenchyma. The crystals can be prismatic, elon- both wide and narrow vessels (e.g., Campsis radicans, Big- gate, or acicular (fig. 3I). All other wood features are more nonia capreolata; fig. 7A) in early- and latewood. When variable and will be treated separately below. mapped onto the phylogeny of the Bignoniaceae (fig. 7C), helical thickening has at least five independent origins, once in Wood Anatomy Diversity and Evolution Bignonieae (e.g., Bignonia capreolata), twice in Catalpeae, in the Bignoniaceae once in Coleeae, and twice in Tecomeae (fig. 7C). All these species occur in strongly seasonal environments, either tem- Porosity perate or xeric. As a mainly tropical family, most species of Bignoniaceae have Intervessel pit diameters. Intervessel pit diameters were diffuse-porous woods (fig. 4A; table 3), and this state is recon- rather homogenous in all tribes, ranging from 7 to 10 mmin structed as ancestral for the family (fig. 4E). However, some most species (table 3; fig. 8C). Outliers were found in the tribe Fig. 3 Common features in Bignoniaceae wood anatomy. A, Godmania aesculifolia (tree), transverse section (TS). B, Handroanthus barbatus (tree), TS. A, B, Diffuse-porous wood, growth rings delimited by marginal parenchyma (arrows), vessels solitary to multiples of two or three, oval to circular in outline. Axial parenchyma aliform confluent. C, Xylophragma pratense (liana), TS, wide vessel with tyloses. Dilated rays delimiting the growth rings (arrows). D, Handroanthus chrysotrichus (tree), longitudinal tangential section (LT), vessel with round alternate pits, axial parenchyma, and rays. E, Amphilophium crucigerum (liana), TS. Vessel dimorphism, wide vessels (asterisks) associated with narrow vessels (arrows). Parenchyma scanty paratracheal. F, Spathodea campanulata (tree), TS, heartwood vessels with tyloses (arrows). G, Handroanthus chrysotrichus (tree), LT, straight-grained wood with storied structure, with vessel elements, rays, and axial parenchyma in horizontal tiers. Note biseriate rays (arrows) and axial parenchyma with two cells per strand. H, Dolichandrone atrovirens (tree), LT, wavy grained wood without storied structure. I, Radermachera glandulosa (tree), longitudinal radial section LR, elongate crystals (arrows) and acicular crystals (arrowhead) in ray cells. Scale bars: A–C, F–H p 200 mm; E p 250 mm; D, I p 50 mm. 1024 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 4 Wood porosity, transverse section. A, Radermachera glandulosa (tree), diffuse-porous wood. B, Catalpa speciosa (tree), semi-ring- porous wood. C, Campsis radicans (liana), ring-porous wood. D, Bignonia capreolata (liana), ring-porous wood. E, Ancestral character state reconstruction for wood porosity in the Bignoniaceae. Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma, Tec. p Tecomeae, Jacar. p Jacarandeae. Scale bars: A, C p 600 mm; B p 1 mm; D p 250 mm.

Coleeae (Paleotropical clade), which had some of the narrow- Perforation plates. Simple perforation plates (fig. 9A) are est pit diameters (≤3 mm; table 3; fig. 8A), and in species of present in all species of the family. However, a few species have Handroanthus, which had pits that were always wider than a combination of simple perforation plates (predominant) and 10 mm and were as wide as 20 mm (table 3; fig. 8B). When foraminate plates (fig. 9B), reticulate plates, or a combination the pit diameters were mapped onto the phylogeny of Big- of foraminate and reticulate plates (fig. 9C,9D). Both forami- nonieae, the likely ancestral state for the entire family was nate and reticulate plates occur in horizontal end walls. Ances- reconstructed as 7 mm, with approximately the same value in tral character state reconstruction shows that this character has all major nodes of most inclusive clades (fig. 8C). probably evolved at least seven times independently in the family PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1025

Fig. 5 Vessel diameters, transverse section. A, Tecomaria capensis, narrow vessels (mean p 30 mm), radial pattern. B, Heterophragma quadriloculare, median vessels (mean p 112 mm), diffuse arrangement. C, Jacaranda copaia, wide vessels, diffuse arrangement (mean p 300 mm), axial parenchyma winged-aliform (arrows). D, Ancestral character state reconstruction of vessel diameters (continuous character,parsimony). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma,Tec.p Tecomeae, Jacar. p Jacarandeae. Scale bars: A–C p 200 mm. (fig. 9E). Reticulate and foraminate perforation plates can be Rays found in the Asian tribe Oroxyleae, the clade that reunites the tribe Crescentieae (except Amphitecna) ϩ Spirotecoma (Tabe- Ray composition. Four different ray compositions are buia alliance), the species Tabebuia aurea, the Paleotropical present in the Bignoniaceae: (i) all rays homocellular (homo- clade Dolichandrone ϩ Markhamia, the species Newbouldia, geneous; fig. 10A,10B), (ii) rays homocellular and heterocel- and the genus Deplanchea (Tecomeae; fig. 9E). lular (heterogeneous) with body ray cells procumbent and one 1026 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 6 Vessel arrangements, transverse section. A, Dolichandrone spathacea, vessels in diffuse pattern. B, Pachyptera kerere, vessels in radial pattern. C, Cybistax antisyphilitica, vessels in tangential bands. D, Ancestral character state reconstruction of vessel arrangements (parsimony). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma,Tec.p Tecomeae, Jacar. p Jacarandeae. Scale bars: A–C p 500 mm. row of square marginal cells cooccurring (fig. 10C,10D), (iii) in ray composition during ontogeny. These woods have ho- rays heterocellular with body ray cells procumbent and two mocellular rays in their adult wood but heterocellular rays with to four upright to square marginal cells (fig. 10E,10F), and body cells procumbent and one row of square marginal cells (iv) rays heterocellular with procumbent, square, and upright in their juvenile wood. Because of this variation, we used ex- cells mixed throughout the ray (fig. 10G,10H). For two species clusively mature wood for all the comparisons and mapping (Oroxylum indicum and Tabebuia aurea) for which we had of the analyzed species. the entire stem, we could check whether there were differences The character mapping shows multiple evolutions of all types Fig. 7 Helical thickening in vessels. A, Bignonia capreolata, longitudinal radial section; all vessels have lateral walls with helical thickening. B, Rhodocolea telfarii, longitudinal tangential section, vessel with helical thickening. C, Ancestral character state reconstruction of the presence of helical thickening in the vessels of the Bignoniaceae (parsimony reconstruction). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma, Tec. p Tecomeae, Jacar. p Jacarandeae. Scale bars: A p 250 mm, B p 50 mm. 1028 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 8 Intervessel pit diameters, as seen in longitudinal tangential section. A, Rhodocolea telfarii, vessel with very minute pits (∼3 mm) in the lateral wall. B, Handroanthus chrysotrichus, vessel with very wide pits (∼18 mm). C, Ancestral character state reconstruction of intervessel pit diameters (continuous character, parsimony). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma, Tec. p Tecomeae, Jacar. p Jacarandeae. Scale bars: A, B p 60 mm. Note that A and B are on the same scale. of ray compositions in the family (fig. 10I). However, some gives rise to tribes Oroxyleae ϩ Catalpeae ϩ Tabebuia alliance consistency is generally found in the ray distributions of the clade ϩ Paleotropical clade is reconstructed as having homo- major clades, with the Tabebuia alliance clade (Neotropics) ex- cellular and heterocellular rays with one row of square marginal hibiting most of the species with homocellular rays, along with cells cooccurring (fig. 10I). On the other hand, most lianas have tribes Coleeae (Paleotropical clade) and Oroxyleae and a clade heterocellular mixed rays, and since most of the tribe Bignonieae formed by Stereospermum ϩ Kigelia (fig. 10I). The node that is composed of lianas or shrubs of lianoid ancestry, heterocel- PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1029

Fig. 9 Perforation plates, as seen in SEM. A, Tabebuia aurea, vessel element with simple perforation plate. B, Oroxylum indicum, foraminate perforation plate. C, Millingtonia hortensis, foraminate-reticulate perforation plate as seen from one side. D, Millingtonia hortensis, foraminate- reticulate perforation plate as seen from the other side. E, Ancestral character state reconstruction of foraminate/reticulate perforation plates in the Bignoniaceae (parsimony). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma, Jacar. p Jacarandeae. Scale bars: A, C, D p 20 mm; B p 50 mm. lular mixed rays are reconstructed as ancestral in this tribe (fig. case since it assigns a 50% probability that the ancestral state 10I). A similar scenario is seen for the tribe Tecomeae (fig. 10I), in the family was either homocellular or heterocellular. On the where most genera are lianas, with the majority having hetero- subsequent node (core Bignoniaceae), however, the maximum cellular mixed rays, while Campsis (liana) and the trees and likelihood reconstruction assigns an 80% chance that the rays shrubs of the tribe exhibit heterocellular rays with two to four were ancestrally heterogeneous there. In other clades within the upright to square marginal cells (fig. 10I). family, in Tecomeae the rays are reconstructed as heterocellular The parsimony analysis was unable to estimate the ancestral with two to four upright to square marginal cells, with the character state for the entire family and the subsequent node evolution of both heterocellular mixed (lianas) and heterocel- (fig. 10I). The maximum likelihood does not shed light on this lular with one row of upright to square marginal cells within Fig. 10 Ray composition, transverse section, longitudinal radial section. A, B, Jacaranda copaia, homocellular ray. C, D, Spathodea campanulata, heterocellular ray with body of procumbent cells and one row of square marginal cells. E, F, Jacaranda puberula, heterocellular ray with two to four rows of square and upright ray cells. G, H, Xylophragma seemaniana, heterocellular ray with procumbent, square, and upright cells mixed. I, Ancestral character state reconstruction with a parsimony inference. Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma, Tec. p Tecomeae, Jac. p Jacarandeae. Scale bars: A–H p 200 mm. PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1031 the tribe (fig. 10I). Similarly, in Bignonieae it is inferred that Multiple transitions from multiseriate to uniseriate rays were heterocellular mixed rays evolved from homo- and heterocellular also encountered (fig. 11F)—at least one in the Tabebuia al- rays with one square marginal cell (fig. 10I). On the other hand, liance, one in the Paleotropical clade, and one in tribe Jaca- in the clade that reunites Catalpeae, Oroxyleae, the Tabebuia randeae (fig. 11F). alliance, and the Paleotropical clade, there are multiple transi- Perforated ray cells. In the Bignoniaceae, perforated ray tions from homo- and heterocellular rays evolving into exclu- cells bear simple perforate plates (fig. 12A,12C) and seem to sively homocellular rays (fig. 10I). connect wide vessels to their adjacent narrow vessels on either Ray height and width. The majority of species in the Big- sides of the rays (fig. 12B). Perforate ray cells are extremely noniaceae have short rays, smaller than 1 mm (fig. 11A,11B). frequent in some species (e.g., Stizophyllum riparium, Doli- However, a correlation between ray height and the lianoid chandra unguis-cati) while rather infrequent in others (e.g., habit was encountered (fig. 11E), with most lianas having very Podranea ricasoliana). They are widespread in the lianas but large rays taller than 1 mm (fig. 11C,11D), especially in the absent in the shrubs and tree species (fig. 12D,12E). tribe Bignonieae (fig. 11E). A similar correlation is seen for ray width (fig. 11F). While most species of the Bignoniaceae Axial Parenchyma have 2–4-seriate rays (fig. 11B), several lianoid species have 5–10-seriate rays (fig. 11C) and commonly even more than Axial parenchyma type and abundance. All species of the 10-seriate rays in thicker stems. Bignoniaceae have paratracheal axial parenchyma (fig. 13).

Fig. 11 Ray height and width, as seen in longitudinal tangential section. A, Ophiocolea ﬂoribunda, short uniseriate rays. B, Roseodendron donnell-smith, short multiseriate rays of two to four cells in width. C, Xylophragma pratense, short and tall rays, tall rays deriving from fusion, multiseriate rays of four to eight cells in width. D, Perianthomega vellozoi, very tall rays, taller than 1 mm. Multiseriate rays of two to four cells in width. E, Ancestral character state reconstruction of habit versus ray height (parsimony). F, Ancestral character state reconstruction of habit versus ray width (parsimony). Scale bars: A–D p 500 mm. 1032 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 12 Perforated ray cells. A, Callichlamys latifolia, transverse section, perforated ray cell (arrow). B, Stizophyllum riparium, longitudinal tangential section, perforated ray cell (arrow) connecting two adjacent vessels. C, Campsis radicans, longitudinal radial section, perforated ray cell. D, Ancestral character state reconstruction of the habits in the Bignoniaceae. E, Ancestral character state reconstruction of perforated ray cells in the wood of the Bignoniaceae. Scale bars: A, C p 100 mm; B p 80 mm.

However, the type and abundance can vary greatly, with three three states were delimited: (i) scanty paratracheal (fig. 13A, major characters delimited (table 1): paratracheal parenchyma 13B), typical of the liana species; (ii) vasicentric (fig. 13C); type, parenchyma confluence type, and apotracheal diffuse pa- and (iii) aliform (fig. 13D–13H). Both the vasicentric and the renchyma present or absent. aliform parenchyma can be confluent, having either short (fig. Within the first character, paratracheal parenchyma type, 13C–13F) or long (fig. 13G,13H) confluences, in the latter Fig. 13 Axial parenchyma types, transverse section. A, Pleonotoma melioides, parenchyma scanty paratracheal. B, Catalpa bignonioides, parenchyma scanty paratracheal. C, Millingtonia hortensis, parenchyma vasicentric, forming short confluences. D, Jacaranda copaia, parenchyma winged-aliform. E, Tabebuia aurea, parenchyma aliform with short and long confluences. F, Crescentia alata, parenchyma aliform with short and long confluences. G, Jacaranda brasiliana, parenchyma winged-aliform with long confluences. H, Amphitecna regalis, parenchyma aliform with long confluences, forming bands. I, Ophiocolea floribunda, parenchyma scanty paratracheal combined with diffuse. Scale bars: A p 200 mm, B–I p 500 mm. 1034 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 14 Ancestral character reconstruction of axial parenchyma diversity (parsimony). A, Axial parenchyma type. B, Axial parenchyma confluence. C, Diffuse axial parenchyma. case forming bands. Sometimes a combination of short and cestral character state was assigned to this node in the parsi- long confluences can be found (fig. 13F). mony analysis, while the maximum likelihood suggests a 48% Character state reconstruction under a parsimony inference probability that the ancestral state was scanty paratracheal, shows uncertainty in the ancestral state of axial parenchyma compared with 30% for aliform and 22% for vasicentric. in the family (fig. 14A), likely because Jacarandeae has para- Confluent axial parenchyma was present in most tree spe- tracheal aliform parenchyma while its sister group, the core cies. In the character state reconstruction, the transition was Bignoniaceae, is reconstructed as having a scanty paratracheal exclusively from axial parenchyma with short confluences to parenchyma. Maximum likelihood reconstruction does not long confluences, suggesting an overall increase in parenchyma shed light on this question since it assigns a 50% probability abundance (fig. 14B). To test this hypothesis, we calculated to either scanty or aliform parenchyma to be present as the the frequency of parenchyma and mapped it onto the phylog- ancestral state for the family. Overall, multiple evolutions of eny of the Bignoniaceae as a continuous character (fig. 15). In all traits were found, with at least three transitions from scanty this reconstruction, there is a slight decrease in the abundance to vasicentric to aliform, one in Bignonieae, one in Crescentiina of parenchyma in the two nodes that lead to lianoid lineages, (Tabebuia alliance ϩ Paleotropical clade; fig. 14A), and one both Tecomeae and Bignonieae. However, within each major in Tecomeae. However, there are also two transitions from lineage there is an increase in the amount of parenchyma from vasicentric parenchyma to scanty paratracheal in Bignonieae the most basal to the most terminal nodes (fig. 15), especially and one in Ekmanianthe (Tabebuia alliance). In the lianoid in the Oroxyleae, the Tabebuia alliance, and the Paleotropical tribe Bignonieae, the reduction in paratracheal parenchyma clade (fig. 15). The same pattern is seen within the Bignonieae coincided with the shrubby habit transition within the Arra- tribe, which has very little parenchyma in the basalmost node bidaea and allies clade (Fridericia platyphylla and Cuspidaria of the tribe but shows an increase toward the terminal nodes, pulchra). There are also two transitions from aliform paren- especially in the species-rich Arrabidaea and allies clade (fig. chyma to scanty paratracheal in the Paleotropical clade (fig. 15). The overall increase in parenchyma was corroborated by 14A). The clade with most diversity in terms of type of pa- the analysis of phylogenetic independent contrasts (PDAP with renchyma is that of Catalpeae ϩ Oroxyleae. An uncertain an- one-tailedP p 0.01 , two-tailedP p 0.007 ,R2 p 0.11 ). PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1035

Fig. 15 Ancestral character reconstruction of the axial parenchyma frequency on the wood of the Bignoniaceae. Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma,Tec.p Tecomeae, Jac. p Jacarandeae.

Diffuse parenchyma was extremely rare but was encoun- Septate Fibers tered in all species of the Coleeae tribe (Paleotropical clade; Septate fibers are living cells with one (fig. 18A)ormore fig. 13I) and, to a lesser extent, in Parmentiera macrophylla (fig. 18B) septa subdividing the cell, which in the Bignoniaceae (tribe Crescentieae, Tabebuia alliance; fig. 14C). are present in more than half of all species (tables 1–3; fig. Axial parenchyma strand length. In the Bignoniaceae, there 18C), being widespread in Bignonieae, Catalpeae, Oroxyleae, are three types of parenchyma strands: (i) strands with two cells Tecomeae, and some small clades within the Paleotropical (fig. 16A), (ii) strands with three or four cells (fig. 16B), and clade (fig. 18C). Correlation was found between scanty para- (iii) strands with five to eight cells (fig. 16C). Most species of tracheal parenchyma and the presence of septate fibers (fig. the Bignoniaceae have three or four cells per parenchyma strand, 18C), although some taxa with more abundant parenchyma with multiple transitions of the other two characters (fig. 16D). sometimes also present septate fibers (tables 1–3; e.g., Hetero- Except for Jacaranda copaia, all other species with five to eight phragma, Parmentiera, Radermachera, and Delostoma). cells per parenchyma strand are lianas, even though most lianas Septate fibers are ambiguously reconstructed in the ancestral also have three or four cells per parenchyma strand. All Han- node of the family in the parsimony reconstruction (fig. 18C), droanthus species have two cells per parenchyma strand (except while the maximum likelihood analysis suggests a 54% chance for a reversion in Handroanthus impetiginosus, which has three that the ancestor of the Bignoniaceae would not possess septate to four cells per parenchyma strand), as do the analyzed spec- fibers. The presence of septate fibers is reconstructed as an- imens of Amphitecna, Tabebuia rigida (fig. 16A), and Spathodea cestral for several of the most inclusive clades of the tribe campanulata. Two species, Ekmanianthe longiflora and Cato- except for Crescentiina, in which septate fibers are derived, phractes alexandrii, were polymorphic, presenting strands with indicating multiple reversions to this character. In Tecomeae, both two and three or four cells (fig. 16D). Catalpeae, and Bignonieae, nonseptate fibers are derived from Axial parenchyma cell area. Although the majority of the ancestors with septate fibers (fig. 18C). parenchyma cells have diameters of ∼15–18 mm, some species have diameters as small as 7–9 mm (fig. 17A,17B), while others Storied Structure have quite wide cells, reaching a diameter of 25 mminNew- bouldia (fig. 17C). When the area data are mapped onto the In the Bignoniaceae, three different character states can be phylogeny of the Bignoniaceae, the higher area values belong delimited for the storied structure: (i) absent, (ii) present for to the trees (fig. 17D), while the narrowest values are found all cells (fig. 19A,19B), and (iii) present only for axial paren- among the lianas (fig. 17D). However, multiple origins of wide chyma and fibers (fig. 19C). Most genera in the Bignoniaceae and narrow parenchyma cells are found in both groups and lack a storied structure completely, and this state is recon- along the entire phylogeny (fig. 17D). structed as ancestral for the family (fig. 19D). However, there 1036 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 16 Axial parenchyma strand length (arrows), longitudinal tangential section. A, Tabebuia rigida, two cells per parenchyma strand. B, Markhamia stipulata, four cells per parenchyma strand. C, Jacaranda copaia, five to eight cells per parenchyma strand. D, Ancestral character state reconstruction of number of cells per parenchyma strand (parsimony). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma, Tec. p Tecomeae, Jac. p Jacarandeae. Scale bars: A, B p 200 mm; C p 250 mm. is one large, species-rich lineage, the Tabebuia alliance (Neo- macrophylla and the other in Ekmanianthe actinophylla (fig. tropics), which in general has a storied structure for both axial 19D). Another clade, the Bignonieae (also Neotropical), in- and radial parenchyma cells (sometimes irregularly storied); cludes some taxa with a storied structure (fig. 19C). The genus the presence of this character state is likely a synapomorphy Dolichandra possesses short rays (lower than 1 mm), and both of this clade with only two reversions, one in Parmentiera axial and radial parenchyma are storied (fig. 19B). On the PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1037

Fig. 17 Axial parenchyma cell transverse area, transverse sections. A, Podranea ricasoliana, very narrow parenchyma cells (mean area p 103 mm2, mean diameter p 6mm). B, Parmentiera macrophylla, narrow parenchyma cells ( mean area p 165mm2, mean diameter p 9 mm). C, New- bouldia laevis, very wide parenchyma cells (mean area p 1198mm2, mean diameter p 22 mm). D, Continuous character mapping for axial parenchyma area (parsimony). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma, Tec. p Tecomeae, Jac. p Jacarandeae. Scale bars: A–C p 100 mm. other hand, Amphilophium, Mansoa, and Perianthomega have Cambial Variants or Irregularities tall rays (higher than 1 mm), and in these genera only axial in the Stems of Lianas parenchyma and fibers are storied (fig. 19C). In the widespread species Amphilophium crucigerum the narrow vessels are also Cambial variants in the Bignoniaceae have been thoroughly storied, along with the axial parenchyma and fibers. A storied studied elsewhere (Schenck 1893; Dobbins 1971; Pace et al. structure was not found in the other genera of the tribe (tables 2009, 2011) and therefore will not be deeply explored here. 1–3; fig. 19D). It is worth mentioning, however, that the variant secondary Fig. 18 Septate fibers. A, Perianthomega vellozoi, longitudinal radial section, one septum per fiber. B, Catalpa longissima, longitudinal tangential section, more than one septum per fiber. C, Character state reconstruction of the axial parenchyma versus the presence or absence of septate fibers. Scale bars: A p 100 mm, B p 200 mm. PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1039

Fig. 19 Storied structure, longitudinal tangential section. A, Crescentia alata, axial and radial parenchyma storied. B, Dolichandra unguis-cati, axial and radial parenchyma storied (arrows indicate the horizontal tiers). C, Perianthomega vellozoi, fibers (arrows) and axial parenchyma storied. D, Ancestral character reconstruction of the storied structure (parsimony). Cat. p Catalpeae, Orox. p Oroxyleae, Del. p Delostoma,Tec.p Tecomeae, Jac. p Jacarandeae. Scale bars: A–C p 200 mm. growth with the formation of phloem wedges (fig. 20A)is scription of development and the pattern of evolution of this present in all genera of tribe Bignonieae and represents a syn- feature; fig. 20A). apomorphy of this clade (Lohmann 2006). In these genera, Within Tecomeae, lianas can develop three different orga- four to multiples of four regions of an initially regular growing nizations: (i) regular secondary growth, (ii) formation of shal- cambium start producing less xylem and more phloem, cre- low arcs with the production of more phloem and less xylem ating shallow arcs equally spaced and in alternation with the than the adjacent regions (fig. 20B), and (iii) formation of a decussate leaves. While development progresses, the four initial wavy cambium. Campsis and Tecomaria have regular second- regions with altered activity stop dividing anticlinally, leading ary growth, while Pandorea jasminoides has irregular phloem to the inclusion of the variant cambia and the formation of arcs (fig. 20B), and Podranea ricasoliana has a wavy cambium deep phloem wedges (see Pace et al. 2009 for a detailed de- (fig. 20C). 1040 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 20 Cambial variants and other cambial oddities of lianas, transverse section. A, Pleonotoma tetraqueta, cambial variant of the furrowed xylem type, with the formation of four phloem wedges. B, Pandorea jasminoides, four to ﬁve shallow phloem arcs. C, Podranea ricasoliana, cambium with a distinctly wavy conﬁguration. Scale bars: A p 4 mm, B p 7 mm, C p 1 mm.

Discussion section Macrocatalpa). Catalpa section Catalpa and Chilopsis (Catalpa’s sister group, which also grows in temperate cli- In this article, we explore the diversity and evolution of the mates) develop semi-ring-porous to ring-porous woods, with wood anatomy of the Bignoniaceae and show that habitat and many samples showing helical thickening, while the tropical habit transitions strongly influenced the patterns of evolution species from section Macrocatalpa have diffuse-porous woods of wood in the family. The Bignoniaceae have a wood with and no helical thickening. Li (2008) hypothesized that the Ca- many shared features that support it as a natural group, such ribbean island genera are derived from a dispersion event from as the widespread paratracheal parenchyma, distinct growth an ancestral population native to the continent, implying that rings generally delimited by a line or band of marginal paren- the ancestor of tribe Catalpeae likely possessed semi-ring- chyma and radially flattened fibers, alternate intervessel pits, porous to ring-porous woods, losing it when occupying a more simple perforation plates, and a straight grain. At the same mesic, humid climate. More signals of this lability are sug- time, its wood anatomy includes a great deal of diversity, and gested by the fact that different samples of the same species most of it is homoplastic, being convergent (sensu Arendt and can have either diffuse or semi-ring-porous woods (e.g., Reznick 2008) in different lineages of the family. Since these Roseodendron donnell-smithii). convergences are potentially linked with other aspects, such Plants growing in xeric regions also develop semi-ring- as climate, habit, or even other anatomical features, we are porous to ring-porous wood, such as Catophractes, from the led to a hypothesis of adaptation. As Futuyma (1979) states, African savannas of Botswana and Namibia. Among the li- “That parallel evolution [here treated as a synonym of convergence] should be common is not surprising. If related species anas, those growing in temperate regions show strikingly ring- have similar patterns of development, they are likely to be porous wood with helical thickening, while those occurring in modified in similar ways if subject to similar selection pres- the tropical regions usually have semi-ring-porous woods sures” (p. 145). Two main aspects apparently played a critical (without helical thickening), something that has been related role in the evolution of wood anatomy of the Bignoniaceae: to the seasonal periods of drought typical of the tropics (Lima ecophysiological factors and the lianoid habit. et al. 2010). All other species of the Bignoniaceae are diffuse- porous but develop growth rings delimited by other growth Ecophysiological Factors Affecting the Evolution markers, such as marginal parenchyma, radially flattened fi- of Wood in the Bignoniaceae bers, and locally dilated rays (see tables 1, 2; Lima et al. 2010), suggesting switches in cambial activity. Another plant family, Porosity and helical thickening. In the Bignoniaceae, semi- ring-porous and ring-porous wood evolved from ancestors the Sapindaceae, with a center of diversity in the tropics also with diffuse-porous woods (see fig. 4E) and no helical thick- had multiple evolutions of ring-porous woods in three distant ening. After a consideration of semi-ring-porous to ring-porous branches of the phylogeny (Koelreuteria, Sapindus, and Xan- wood and the place of occurrence of plants (tables 1, 2), this thoceras), which correspond to genera that have occupied evidences that porosity is directly correspondent to the occu- higher latitudes (Klassen 1999; Baas et al. 2003). pation of more seasonal climatic areas derived from putative Ecologically, semi-ring-porous and ring-porous woods allow ancestors growing in more mesic habitats. The most patent for higher conduction of water during favorable seasons (sum- case is seen in Catalpa, which possesses two lineages (Li 2008), mer or rainy season) with the presence of wide vessels, while one growing in temperate climates (Catalpa section Catalpa) they become safer against embolism during the unfavorable and the other growing in a tropical mesic climate (Catalpa seasons (winter or dry season), when vessels get much nar- PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1041 rower and therefore less prone to embolisms caused by either a tribe that also possesses big trees (e.g., Oroxylum, Milling- freezing or drought (Hargrave et al. 1994; Carlquist 2001). tonia); once in Tecomeae; once in Bignonieae; and once in Helical thickening has also been correlated with ecological Tourrettieae. The last three tribes are composed mainly of li- factors, with a higher occurrence both at high latitudes (Baas anas, even though Tecomeae, as circumscribed by Olmstead 1973; Carlquist 2001; Lens et al. 2004; Wheeler et al. 2007) et al. (2009), also possesses small trees. In this work, only and in arid regions (Carlquist 2001; Wheeler et al. 2007), lianas of Tecomeae and Bignonieae were available, and even suggesting that helical thickening likely plays a role in pro- though they represent distantly related lineages within the fam- tection against embolism and acts in embolism repair (Carl- ily, they shared a number of anatomical features that can be quist 2001; Jansen et al. 2003, 2004). Our results corroborate connected to the lianoid habit. For instance, all lianas studied the suggestions that the presence of helical thickening is cor- had vessel dimorphism (associated narrow and wide vessels), related with the environment since all plants that develop heli- a term coined by Carlquist (1981) in his work on Nepenthes cal thickening in the Bignoniaceae were growing either at wood and used largely afterward. Vessel dimorphism is a per- higher latitudes (e.g., Campsis) or in arid regions (e.g., vasive feature in lianas (Carlquist 1985, 1991, 2001; Klassen Rhodocolea). 1999) and has been related to an efficient hydraulic conduction Foraminate and reticulate perforation plates. Simple per- through the long and typically narrow stems of lianas, which foration plates are present in all species of the Bignoniaceae. are known to usually support canopies as large as those of However, some of them also develop foraminate and reticulate very tall trees (Ewers et al. 1990; Ewers and Fisher 1991; Zhu perforation plates or even a combination of the two (e.g., Mil- and Cao 2009). Wide vessels are highly efficient in conduction lingtonia). It has been suggested that foraminate perforation but at the expense of safety, as they are also more susceptible plates are derived from either simple or scalariform perforation to embolisms (Carlquist 1977; Zimmermann 1983; Cochard plates (Carlquist 1961), and they are commonly found co- et al. 1994; Hargrave et al. 1994), and it has been proposed occurring with scalariform perforation plates (Rao et al. 1987; that embolism risk is one of the major factors limiting liana Ohtani et al. 1992). Here, the foraminate perforations are occupation in higher latitudes and arid climates (Isnard and reconstructed as derived from simple perforation plates and Silk 2009). In the event of a vessel embolism (“vessel” referring are constantly present in the taxa in which they occur, being to a series of interconnected vessel elements), the vessel be- characteristic of the Asian tribe Oroxyleae, the Central Amer- comes blocked by an air bubble, interrupting the water col- ican tribe Crescentieae (except, apparently, for Amphitecna, umn. Lianas, however, seem to have mitigated this disadvan- but surveys of more samples are necessary for confirmation), tage by combining wide and narrow vessels. When a wide some members of the Neotropical Tabebuia alliance (this vessel becomes embolized, the neighboring narrow vessels can work; Metcalfe and Chalk 1950; Dos Santos and Miller 1992; function as a bypass, redirecting water while maintaining wa- Sonsin et al., forthcoming), the Paleotropical clade, and some ter column integrity (Raven et al. 2005)—a mechanism espe- Tecomeae (e.g., Deplanchea), indicating that this is a highly cially useful when root pressure is not sufficient for embolism homoplastic character. The selective pressure favoring its evo- repair, as has been shown experimentally for many angiosperm lution, if present at all, is, however, not clear, as we found no vines (Ewers et al. 1997). correlations between this state and the other variables ana- Perforated ray cell was another feature strongly correlated lyzed. Christman and Sperry (2010) showed that both scalar- with the lianoid habit (fig. 12). Nearly all lianas analyzed pre- iform and foraminate perforation plates added additional re- sented perforated ray cells, in both Bignonieae and Tecomeae. sistance above that of the vessel lumen. There are many On the other hand, this feature was absent in trees and shrubs theories why multiple perforation plates may be more adap- of the same tribes and elsewhere in the family. Perforated ray tive—for instance, for trapping air bubbles, avoiding them to cells were observed to link narrow and wide vessels at each become larger, or reducing their size when crossing the bars side of the rays and are likely another source of hydraulic (in scalariform perforations; Zimmermann 1983); to facilitate conduction safety and efficiency (Angyalossy et al. 2012). embolism repair; and even to avoid vessel implosion when Other families in which trees lack perforated ray cells include submitted to strong negative pressures (Carlquist 2001)—but lianas that present this character, such as the Leguminosae none of these theories have found experimental support so far (Angyalossy et al. 2009), thus supporting the hypothesis that (Christman and Sperry 2010). this may be a character correlated with the lianoid habit. Septate fibers. A strong correlation between septate fibers Yet another feature that was correlated with the lianoid habit and scanty axial parenchyma was found. A correlation be- was ray height and width. Tall and wide rays are not present tween scanty parenchyma and septate fibers had already been in all lianas of the Bignoniaceae, but whenever present in the reported for many other angiosperms (Harrar 1946; Carlquist family they were in lianas. This might be a feature related to 1988, 2001; Wheeler et al. 2007), and it has been hypothesized the architectural safety of the wood, avoiding breakage of the that septate fibers, which are known to store starch (Harrar axial system when twining (Schenck 1893; Carlquist 1985, 1946), assumed the role of parenchyma in those woods. Most 1991), providing the stems of lianas with high flexibility to species with scanty parenchyma are lianas, and this is a feature reach the canopy (Gallenmu¨ ller et al. 2001; Rowe et al. 2004; that is widespread among them. Isnard and Silk 2009). The combination of tall and wide rays has also been reported in many other liana families, such as Multiple Origins of the Lianoid Habit and Its Impact Aristolochiaceae, Celastraceae, Dilleniaceae, Leguminosae, on Wood Anatomy in the Bignoniaceae Menispermaceae, and Piperaceae, among others (Carlquist The lianoid habit has evolved at least four times indepen- 1991; Tamaio 2006; Rajput et al. 2012). Two of these studies dently in the Bignoniaceae (see fig. 11E), once in Oroxyleae, showed that the rays were not only tall and wide but also 1042 INTERNATIONAL JOURNAL OF PLANT SCIENCES heterocellular, with mixed procumbent, square, and upright Cambial variants are present in all lianas of Bignonieae, and cells (Tamaio 2006; Rajput et al. 2012). In the Bignoniaceae, their diversity has been known for many years (Schenck 1893; the same combination was encountered. Thus, highly hetero- Solereder 1908). The evolution of the cambial variant in Big- geneous rays may be another common feature of lianas as a nonieae involved the alteration of four to multiples of four whole, a feature not unveiled until now. According to our regions of the cambium that reduced the production of xylem character state reconstructions, these heterocellular mixed rays and increased the production of phloem, leading to the for- are derived from ancestors with homocellular ray structure or mation of deep phloem wedges interrupting the xylem (Dob- heterocellular with just one row of square marginal cells. The bins 1971; Pace et al. 2009). The phloem produced by the common evolution of heterocellular rays in distantly related regular and the variant portions of the cambium were shown lianoid clades within the Bignoniaceae and other angiosperm to be different and likely evolving independently (nonmodu- families is intriguing. There might be a link between hetero- larly; Pace et al. 2011). The formation of shallow arcs in the cellular ray cells that are vertically oriented and a more efficient stem of Pandorea jasminoides was noted previously by both vertical conduction of water in plants with usually narrow Schenck (1893) and Gasson and Dobbins (1991) and is some- stems, something also reported for herbs and secondarily how similar to what is seen in Podranea ricasoliana’s wavy woody plants (Carlquist 1966). On the other hand, various cambium. This organization would probably not constitute a arboreal taxa of families that possess tall and wide rays— cambial variant per se but rather an irregular formation of namely, the Acanthaceae, Annonaceae, Dilleniaceae, Theaceae, secondary vascular systems in these plants. A similar wavy Violaceae, and Winteraceae—also possess heterogeneous rays, cambium was encountered in a mutant of Populus overex- despite their thick stems; therefore, biomechanical or physi- pressing ARBORKNOX1 (35S:ARK1), an orthologue of ological studies of conduction are needed to test and clarify Arabidopsis SHOOT MERISTEMLESS (STM; Groover et al. the correlations between tall and wide rays, their heterocellular 2006). In this mutant there is a marked reduction in the pro- composition, and a possible function, if present. duction of xylem in comparison to the wild type (Groover et In most liana species outside the Bignoniaceae, axial paren- al. 2006). Lianas also possess a quite reduced cambial activity, chyma is very abundant and has also been suggested to provide as shown in studies of wood formation in these plants (Davis flexibility to the climbing stems and act as a storage tissue and Evert 1970; Lima et al. 2010). These molecular studies (Carlquist 1985). However, the axial parenchyma, which in suggest that only slight modifications in the level of expression the Bignoniaceae as a whole is generally quite abundant, is of certain genes can have pivotal results in the amount of wood a rather common feature of tropical plants (Alves and formed and may have been involved in the evolution of lianas Angyalossy-Alfonso 2002), being, however, rather scarce in from tree ancestors. the lianas. The evolution of lianas seems to have been accompanied by a reduction in the volume of parenchyma, except The Evolution of Vessels, Rays, and Axial for a reversion in the Arrabidaea and allies clade on a terminal Parenchyma in the Bignoniaceae node of the Bignonieae. How during evolution scanty parenchyma could be selectively advantageous will remain unan- Vessels. In the Bignoniaceae, two opposite patterns are swered, but in turn many of the functions attributed to the seen in vessel element width evolution. In all lianoid lineages axial parenchyma in Bignoniaceae lianas seem to have been the vessels increase in size, while in the clades of trees, such compensated for by other features. For instance, the storage as Crescentiina (Tabebuia alliance ϩ Paleotropical), we see the function in the species with scanty parenchyma seems to have opposite pattern. From an ancestor reconstructed as likely hav- been taken by the septate fibers. The function of flexibility, at ing vessels of 110 mm in diameter, descendents exhibit nar- least in Bignonieae, might have been compensated for by the rower vessels toward more apical nodes, with most species ubiquitous presence of variant secondary growth, with the for- having vessels ∼65–70 mm. Whether there are selective pres- mation of masses of phloem interrupting the xylem (Schenck sures driving the reduction in width of this vessels is hard to 1893; Dobbins 1971). In the Bignonieae, stems with cambial say, since these plants occupied myriad environments, includ- variant can vary from having four to multiples of four phloem ing Amazonian terra firma forest, the Cerrado, African savan- wedges (Schenck 1893; Dos Santos 1995; Pace et al. 2009), nas, mangroves, and monsoon forests, so it would be too spec- and as noted by Gentry (1980), the more phloem wedges there ulative to try to find direct answers at this time. are, the more flexible the stems. Rays. Rays in the Bignoniaceae are quite varied, but with- In the large and species-rich lianoid lineage of Bignonieae, out branching resolution in the phylogeny of tribe Jacarandeae there have been multiple evolutions from lianas to shrubs, (sister group to all other Bignoniaceae), which possesses species especially in the occupation of savannahs (Lohmann 2003). In with homocellular rays in section Monolobos and species with the Arrabidaea and allies clade, the sole clade of Bignonieae heterogenous rays in section Dilobos (Dos Santos and Miller with more abundant parenchyma, there were two transitions 1997), it is impracticable to reconstruct the ancestral state for from lianas ancestors to shrubs, one in Fridericia and one in the entire Bignoniaceae. In some clades within the family, how- Cuspidaria. Surprisingly, in these cases there has been a re- ever, there are some transitions from heterocellular rays with duction in the amount of associated parenchyma. More studies procumbent body cells and one row of square marginal cells with more taxa of shrubs in Bignonieae—and perhaps also in to heterocellular mixed rays, contrary to what Kribs (1935) Tecomeae—are needed, comparing self-supporting and lianoid has suggested as the trend for dicotyledons as a whole. On the genera to test whether this reduction in parenchyma is a com- other hand, there have been also evolutions from heterocellular mon aspect in these habit transitions from lianas to shrubs, a rays with procumbent body cells and one row of square mar- still largely unexplored aspect (Baas et al. 2003). ginal cells to homocellular rays in Crescentiina and Oroxyleae. PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1043

Storied structure is derived in the Bignoniaceae and has evolved adaptive pressures. Phylogenetic mappings strongly suggest at least three times from ancestors without a storied structure. that the evolution of wood acts in response to selective pres- Virtually all tree species of the Tabebuia alliance (Neotropics) sures; therefore, a single line of evolution is not present, but have a storied or irregularly storied wood structure, and this it is the lability of traits that likely allowed the occupation of is likely a synapomorphy of this clade. new niches, habits, and habitats in the family. New studies Axial parenchyma. Axial parenchyma in the Bignoniaceae combining phylogenetic and anatomical data are encouraged as a whole is uncertainly reconstructed, since Jacarandeae is to increase our knowledge of the patterns of evolution for the reconstructed as having aliform confluent parenchyma and its wood of angiosperms as a whole and to better understand sister group, the core Bignoniaceae, as having scanty paratra- what the responses of woody plants are to the realm of hab- cheal parenchyma. Focusing on the core Bignoniaceae, scanty itats, habits, and niches they have conquered throughout their axial parenchyma is ancestral in clades that later evolved vasi- evolution. centric and aliform parenchyma. The confluence, in turn, also evolved from short to long confluences (see fig. 13E–13H). Overall, an increase in the abundance of parenchyma was re- Acknowledgments corded toward the most apical nodes in the whole family, a pattern supported by the analysis of phylogenetic independent We express our gratitude to Andrew Groover for the invi- contrasts. This result agrees with the more general evolution- tation to write this article on wood evolution; Alex C. Wie- ary trends proposed for the evolution of axial parenchyma in denhoeft, Michael Wiemann, and Regis Miller for their warm the dicotyledons (Kribs 1937). reception, availability, clarifications, and good company dur- In contrast, the evolution in the Coleeae tribe of diffuse ing our laborious work at Forest Products Laboratory (Mad- parenchyma combined with paratracheal parenchyma from ison, WI); Antonio C. F. Barbosa for last-minute sections of ancestors of exclusively paratracheal parenchyma is rather un- Stereospermum; the Institute for Technological Research (IPT; usual in wood evolution as a whole and runs contrary to the Saõ Paulo, Brazil; Maria Jose´ Miranda and Rafael Pigozzo) general trend proposed for the dicotyledons (Kribs 1937). De- for allowing us to analyze and photograph part of its slide termination of whether the evolution of this rather unusual collection; Gabriella Pace and Lisana Rezende for all the sup- trait was a response to a selective pressure (adaptation) or port in the completion of this article; all the personnel of the simply a result of a founder effect connected to island speci- University of Saõ Paulo and Museo Noel Kempff Mercado for ation in Madagascar (genetic drift; Mayr 1942) would merit help in collections in Brazil and Bolivia, respectively; Andrew further investigation. Groover, Dewey Litwiller, Giuliano Locosselli, Guillermo An- geles, Pieter Baas, and three anonymous reviewers for inval- Conclusion uable suggestions on the manuscript; and CAPES, CNPq The evolution of diversity in the Bignoniaceae has been (481034/2007-2), and FAPESP (2012/01099-8) for financial shown to be likely driven by both ecophysiological and habit support.

Appendix A

Taxa, Voucher Information, and Geographic Origins

Taxa, vouchers with the acronyms for wood collections and herbaria where the samples are deposited, and geographic origin are shown for all Bignoniaceae sampled. In 2002, the MAD herbarium was incorporated into the WIS herbarium but was kept as a separate collection (data from Index Herbariorum). Species, voucher (wood collection and/or herbarium), geographic origin. Adenocalymma comosum (Cham.) DC., Pace 53 (SPFw, SPF), Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil. Adenocalymma divaricatum Miers, Udulutsch 2808 (SPFw, HRCB), Lenço´ is, Bahia, Brazil. Amphilophium crucigerum (L.) L.G. Lohmann, Pace 1, Pace 2, Pace 3, Pace 34 (SPFw, SPF), Saõ Paulo, Saõ Paulo, Brazil. Amphilophium pulverulentum (Sandwith) L.G. Lohmann, Dos Santos 279 (MADw, MAD, MO, MG), Senador Jose Porfirio (Sozel), Para´, Brazil. Amphitecna latifolia (Mill.) A.H. Gentry, Fairchild Tropical Garden x-3-369, Florida, USA. Amphitecna regalis (Linden) A.H. Gentry, Nee & Taylor 29900, Las Choapas, 5 km NW of El Doce, Uxpanapa region, Veracruz, Mexico. Anemopaegma chamberlaynii (Sims) Bureau & K. Schum., Zuntini 15 (SPF), Vale do Rio Doce Forest Reserve, Espı´rito Santo, Brazil. Bignonia campanulata Cham., Pace 39 (SPFw, SPF), Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil. Bignonia capreolata L., Nogle s.n. (MADw), Norfolk County, Dismal Swamp, Virginia, USA; Wilson 19 (MADw, F), Cow Creek, Texas, USA. Bignonia magnifica W. Bull, Pace 51 (SPFw, SPF), Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil. Bignonia prieurei DC., Zuntini 13 (SPFw, SPF), Linhares, Espı´rito Santo, Brazil; Dos Santos 87 (MADw, MAD, MO, MG), Maraba´, Para´, Brazil. Callichlamys latifolia (Rich.) K. Schum, Zuntini 175 (SPF), Vale do Rio Doce Forest Reserve, Espı´rito Santo, Brazil; Pace 42 (SPFw), Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil; Pace 63 (SPFw, SPF), Ducke Forest Reserve, Manaus, Amazonas, Brazil. Campsis radicans (L.) Seem., Hicock 841 (SJRw, Y), Connecticut, USA; Pond 448 (MADw, MAD), Camden County, Dismal Swamp, North Carolina, USA. Catalpa bignonioides Walter, Erdman & DeVall s.n. (MADw, MAD, NY), Gainesville, Florida, USA. Catalpa longissima (Jacq.) Dum.Cours., Pimentel & Garcia 965 (SJRw, NCI), San Cristo´ bal, El Tablaso, Nigua riverside, Cordillera Central, Dominican Republic; collector unknown s.n. (USw2942, US), Hispaniola Island. Catalpa speciosa (Warder ex Barney) Warder ex Engelm., collector unknown s.n. (SJRw, RBHw3217), location unknown; 1044 INTERNATIONAL JOURNAL OF PLANT SCIENCES collector unknown s.n. (SJRw, Uw17977), location unknown. Catophractes alexandri D.Don, Dechamps 1219 (MADw, Tw, MAD), Mocamedes, Angola. Chilopsis linearis (Cav.) Sweet, Pidgeon s.n. (SJRw, WIS), Otero County, New Mexico, USA; Johnson s.n. (MADw, BWCw), Campaign Wash, Arizona, USA; collector unknown s.n. (Kw), location unknown. Crescentia alata Kunth, Wiemann & Lemckert 23 (MADw, CR, LSU), Can˜ as, Guanacate, Costa Rica; collector unknown s.n. (SJRw), Cuastecomate, Mexico; Ortega 12 (USw), Sinaloa, Mexico. Crescentia cujete L., Pace 80,Saõ Paulo, Saõ Paulo, Brazil; Dugand 149 (MADw, SJRw, MAD), Totuma, Colombia. Cuspidaria convoluta (Vell.) A.H. Gentry, Pace 48 (SPFw, SPF), Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil. Cybistax antisyphilitica (Mart.) Mart., Reitz & Klein 7354 (MADw, HBRw, HBR), Salto do Pilaõ, Lontras, Santa Catarina, Brazil; collector unknown s.n. (BWCw, SJRw42602), Saõ Paulo, Brazil. Delostoma integrifolium D.Don, Acosta-Solis 6694 (MADw, SJRw, MAD, F), Limo´ n, Bolivar, Ecuador; Acosta-Solis 11648-A (MADw, F), Ecuador. Deplanchea bancana (Scheff.) Steenis, Lai et al. 68559 (Kw, K), Sarawak, Malaysia; Forest Department of Java 2751 (SJRw, L), Menjabing, Dutch East Indies. Digomphia densicoma (Mart. ex DC.) Pilg., Nee 31168 (MADw,VEN, NY), Cerro de la neblina, Amazonas, Venezuela; Maguire 28311 (BWCw, USw), Me´rida, Venezuela. Dolichandra unguiculata (Vell.) L.G. Lohmann, Zuntini 176 (SPFw, SPF), Vale do Rio Doce Forest Reserve, Espı´rito Santo, Brazil. Dolichandra unguis- cati (L.) L.G. Lohmann, Ceccantini 2687 (SPFw, SPF), Matozinhos, Minas Gerais, Brazil; Groppo 322 (SPF), Saõ Paulo, Saõ Paulo, Brazil. Dolichandrone atrovirens (Roth) K.Schum., Brown s.n. (DDw, DD), Dehradun, India; collector unknown s.n. (SJRw), Myanmar; Kanehira 132 (SJRw), Palau, Micronesia. Ekmanianthe actinophylla (Griseb.) Urb., Fors 11 (MADw, SJRw, MAD), Havana, Cuba; Leon 14358 (SJRw, NY), Cuba. Fernandoa adenophylla (Wall. ex G.Don) Steenis, collector unknown s.n. (Kw 108, 427, 433, 435), location unknown. Fernandoa magnifica Seem, Schlieben 459 (SJRw, MAD), Tanganyika, Tanzania. Fridericia platyphylla (Cham.) L.G. Lohmann, Pace 22, Pace 23 (SPFw, SPF), Uberlaˆndia, Minas Gerais, Brazil. Fridericia samydoides (Cham.) L.G. Lohmann, Pace 49 (SPFw, SPF), Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil. Fridericia speciosa Mart., Pace 40 (SPFw, SPF), Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil. Godmania aesculifolia (Kunth) Standl., Breedlove 9563 (MADw, DS), Chiapas, Mexico; Williams 10233 (MADw, F), Aragua, Venezuela; Smith 3368 (SJRw, MAD), British Guiana. Handroanthus barbatus (E.Mey.) Mattos, Loureiro s.n. (BCTw11727, INPA); Maguire 41572 (SJRw, NY), Rio Pacimoni-Yatua, Venezuela. Handroanthus chrysotrichus (Mart. ex DC.) Mattos, Pinho 6 (BCTw, SP), Saõ Simaõ,Saõ Paulo, Brazil; Pace 188, 190 (SPFw, SPF), Saõ Paulo, Saõ Paulo, Brazil. Handroantus impetiginosus (Mart. ex DC.) Mattos, Ducke 363 (SJRw, MAD), Brazil. Handroanthus serratifolius (Vahl) S.O.Grose, Lima s.n. (BCTw), Para´, Brazil; Silva 3281 (BCTw, INPA), Jari, Para´, Brazil. Heterophragma quadriloculare (Roxb.) K.Schum., Brown s.n. (SJRw, DDw1106), India; Dehra Dun s.n. (SJRw, DDw 241), India; Pearson s.n. (MADw), India. Heterophragma sulfureum Kurz, Conservator of Forests 1238 (SJRw), Burma. Jacaranda brasiliana Lam., collector unknown s.n. (FPBw1755), Brazil; collector unknown s.n. (SJRw, MAD), Brazil. Jacaranda copaia (Aubl.) D.Don, Cabrera 41, 42 (MADw, MAD), Puerto Carare, Santander, Colombia. Jacaranda obtusifolia Bonpl., Conservator of Forests 2049 (SJRw), British Guiana; Smith 3125 (SJRw, MAD), British Guiana. Jacaranda puberula Cham., Hoehne 28168 (SJRw, MAD), Brazil; Reitz 14198 (BWCw, MAD), Santa Catarina, Brazil. Jacaranda ulei Bureau & K.Schum., Dos Santos 167, 168 (MADw, MAD, MO, MG), Parauapebas, Para´, Brazil. Kigelia africana (Lam.) Benth., Schlieben 368 (SJRw, MAD), Tanganyika, Democratic Republic of Congo. Lundia damazii C. DC., Pace 55, Pace 56 (SPFw, SPF), Saõ Paulo, Saõ Paulo, Brazil. Manaosella cordifolia (DC.) A.H. Gentry, Pace 41 (SPFw, SPF), Brazil, Living Collection Plantarum Institute, Nova Odessa, Saõ Paulo, Brazil; Dos Santos 88 (MADw, MAD, MO, MG), Maraba, Rio Doce S. A. Forest Reserve, 48 km from Maraba´, Para´, Brazil; Dos Santos 308 (MADw, MAD, MO, MG), Senador Jose´ Porfirio, Xingu riverside. Mansoa difficilis (Cham.) Bureau & K. Schum., Pace 35 (SPFw), Saõ Paulo, Saõ Paulo, Brazil; Zuntini 4 (SPF), Vale do Rio Doce Forest Reserve, Espı´rito Santo, Brazil. Markhamia lutea (Benth.) K.Schum., collector unknown s.n. (Kw525), Equatorial Guinea. Markhamia stipulata (Wall.) Seem., collector unknown s.n. (Kw440), Thailand. Martinella obovata (Kunth) Bureau & K. Schum., Zuntini 7 (SPF), Vale do Rio Doce Forest Reserve, Espı´rito Santo, Brazil; Dos Santos 237 (MADw, MAD, MO, MG), Porto de Moz, Xingu riverside, Para´, Brazil; Dos Santos 317 (MADw, MAD, MO, MG), Gurupa, Moju riverside, tributary of the Amazon River, Para´, Brazil. Mayodendron igneum (Kurz) Kurz, Conservation of Forests 2444 (SJRw), Burma. Millingtonia hortensis L.f., van Beusekom 3426 (TWTw, L), Saeat Kanchanaburi, Thailand; Brown 3160 (SJRw, DDw), India; collector unknown s.n. (Kw), Thailand. Neojobertia mirabilis (Sandwith) L.G. Lohmann, Dos Santos 48 (MADw, MAD, MO, MG), Buriticupu Forest Reserve, Maranhaõ, Brazil. Newbouldia laevis (P.Beauv.) Seem., Vigne 1722 (SJRw, MAD), Gold Coast, Nsuta, Ghana. Ophiocolea floribunda (Bojer ex Lindl.) H.Perrier Zhjra s.n. (MADw, MAD), Masoala Peninsula, Madagascar. Oroxylum indicum (L.) Kurtz, China Academy of Foresty s.n. (TWTw7424, CAFw13841), China; Jacobs 8493 (TWTw, L), Lampung, Sumatra; Kanehira s.n. (TWTw, FUw B.401), Java, Indonesia; Brown 1179 (SJRw, DDw), India. Pachyptera kerere (Aubl.) Sandwith, Castanho 143, Lohmann 834 (SPF), Negro riverside, Amazonas, Brazil; Santos 226 (MADw, MAD, MO, MG), Melgaco, Marajo´ Island; Mapari riverside, Para´, Brazil; Dos Santos 274 (MADw, MAD, MO, MG), Porto de Moz; Xingu riverside near the Açai River, Para´, Brazil; Dos Santos 291 (MADw, MAD, MO, MG), Senador Jose´ Porfirio, Xingu River near foz do Igarape´ Guara´; Dos Santos 292 (MADw, MAD, MO, MG), Maraba´, Rio Doce S. A. Forest Reserve, Sororo´ riverside. Pajanelia longifolia (Willd.) K.Schum., Conservator of Forests 8188 (SJRw), Rangoon, Burma; collector unknown s.n. (Kw528), Malaya, Malaysia. Pandorea jasminoides (Lindl.) K.Schum., Pace 18, 19 (SPFw, SPF), cultivated in Campinas, Saõ Paulo, Brazil. Paratecoma peroba (Record) Kuhlm., Castro 284, 578 (BCTw), Rio Doce, Espı´rito Santo, Brazil. Parmentiera cereifera Seem., Curtis s.n. Fairchild Bot. Gard. X4-183 (MADw), Florida, USA. Parmentiera macrophylla Standl., Cooper 402 (MADw, SJRw, MAD), Panama; Stork 1894 (SJRw, MAD), Costa Rica. Perianthomega vellozoi Bureau, Pace 10, Pace 15 (SPFw, SPF), Mata do Paraı´so, Viçosa, Minas Gerais, Brazil; Pace 28, Pace 29 (SPFw, SPF), Santa Cruz de la Sierra, Santa Cruz, Bolivia. Phyllarthron bojeranum DC., G31(SJRw, CTFw), Region Cotier Est, Madagascar. Pleonotoma melioides (S. Moore) A.H. Gentry, Dos PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1045

Santos 174 (MADw, MAD, MO, MG), Parauapebas, Serra dos Carajas Biological Reserve; Dos Santos 298 (MADw, MAD, MO, MG), Senador Jose´ Pontifı´rio, Para´, Brazil. Pleonotoma tetraquetra (Cham.) Bureau, Ozo´ rio-Filho 11, Saõ Paulo, Saõ Paulo, Brazil. Podranea ricasoliana (Tanfani) Sprague, Pace 11 (SPF), Saõ Paulo, Saõ Paulo, Brazil. Pyrostegia venusta (Ker Gawl.) Miers, Pace 17 (SPFw, SPF), Campinas, Saõ Paulo, Brazil; Pace 36 (SPFw, SPF), Saõ Paulo, Saõ Paulo, Brazil. Radermachera gigantea (Blume) Miq., Van de Koppel 4780 (SJRw, L), Java, Indonesia. Radermachera glandulosa (Blume) Miq., Janssonius 1214g (SJRw), Java, Indonesia; collector unknown s.n. (Kw), Burma. Radermachera pinnata (Blanco) Seem., Philippine Bureau of Forestry 342 (SJRw), Phillipines. Radermachera sinica (Hance) Hemsl., NTU 408, Taiwan. Rhodocolea telfairii (Bojer ex Hook.) H.Perrier, collector unknown s.n. (SJRw10766), Madagascar. Roseodendron donnell-smithii (Rose) Miranda, Williams 8734 (MADw, F), Fortuno, Coatzacoalcos River, Veracruz, Mexico; Williams 9382 (MADw, F), Ubero, Oaxaca, Mexico; William 9458 (MADw, F), Mexico; collector unknown s.n. (Kw920), Venezuela. Sparattosperma leucanthum (Vell.) K.Schum., collector unknown s.n. (BCTw 2486), Brası´lia, Distrito Federal, Brazil. Spathodea campanulata P.Beauv., Chevalier 140 (SJRw, K), Gabon; collector unknown s.n. (Kw529), Uganda. Spirotecoma spiralis (C.Wright ex Griseb.) Pichon, Bucher 90 (SJRw, MAD), Cuba. Stereospermum chelonoides (L.f.) DC., Istituto Botanico dell’Universita` di Firenze 706 (BCTw), India. Stizophyllum riparium (Kunth) Sandwith, Pace 16, Pace 33 (SPFw, SPF), Saõ Paulo, Saõ Paulo, Brazil; Zuntini 9 (SPF), Vale do Rio Doce Forest Reserve, Espı´rito Santo, Brazil. Tabebuia aurea (Silva Manso) Benth. & Hook.f. ex S.Moore, Gerolamo 3 (SPFw), Saõ Paulo, Saõ Paulo, Brazil. Tabebuia cassinoides (Lam.) DC., Williams 13809 (MADw, F), Puerto Ayacucho, Amazonas, Venezuela. Tabebuia fluviatilis (Aubl.) DC., Lobato 447 (MADw, MGw, MG), Barcarena, Para´, Brazil; Conservation of Forests 4071 (SJRw), British Guiana; collector unknown (SJRw12019), location unknown. Tabebuia heterophylla (DC.) Britton, Dungand 33754 (BCTw), Colombia. Tabebuia obtusifolia (Cham.) Bureau, Kuhlmann (BCTw, RB), Espı´rito Santo, Brazil. Tabebuia rigida Urb., Instituto de Tecnologia do Rio Grande do Sul s.n. (BCTw), Rio Grande do Sul, Brazil. Tabebuia roseoalba (Ridl.) Sandwith, CVRD Morais Jesus s.n. (BCTw), Linhares, Espı´rito Santo, Brazil. Tanaecium pyramidatum (Rich.) L.G. Lohmann, Pace 14, Pace 35 (SPFw, SPF), Saõ Paulo, Saõ Paulo, Brazil; Dos Santos 101 (MADw, MAD, MO, MG), Maraba´, Rio Doce S. A. Forest Reserve, Sororo´ riverside, Para´, Brazil. Tecoma cochabambensis (Herzog) Sandwith, Salomon 6684 (MADw, MO) Murillo, La Paz, Bolivia. Tecoma fulva (Cav.) G.Don, collector unknown s.n. (SJRw32082), location unknown. Tecoma stans (L.) Juss. ex Kunth, Jack 5693 (SJRw, MAD), Santa Clara, Belmonte, Cuba; Dugant 216 (SJRw, MAD), Colombia; Williams 12254 (MADw, F), Federal District, Venezuela. Tecomaria capensis (Thunb.) Spach, Rimbach 832 (SJRw, MAD), Ecuador. Tecomella undulata (Sm.) Seem., colletor unknown s.n. (Kw550), location unknown. Tynanthus cognatus (Cham.) Miers, Pace 9a, Pace 9b (SPFw, SPF), Saõ Paulo, Saõ Paulo, Brazil. Xylophragma pratense (Bureau & K.Schum.) Sprague, Dos Santos 140 (MADw, MAD, MO, MG), Maraba´, Rio Doce S. A. Forest Reserve, Para´, Brazil. Zeyheria montana Mart., Pacheco 2762 (SJRw), Minas Gerais, Brazil; Heringen 4130 (BCTw, MADw), Rio de Janeiro, Brazil. Zeyheria tuberculosa (Vell.) Bureau ex Verl., Schmidt 143 (SJRw, M), Bolivia.

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