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Anatomy and Morphology |
2Laboratory of Plant Systematics, Institute of Botany and Microbiology, Kasteelpark Arenberg 31, K.U.Leuven, BE-3001 Leuven, Belgium; 3National Herbarium of the Netherlands–Leiden University Branch, P.O. Box 9514, NL-2300 RA Leiden, The Netherlands; 4Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond, Surrey TW9 3DS, UK
Received for publication June 15, 2006. Accepted for publication February 1, 2007.
ABSTRACT
The wood structure of 71 species representing 24 genera of the pantropical Lecythidaceae s.l., including the edible Brazil nuts (Bertholletia excelsa) and the spectacular cannon-ball tree (Couroupita guianensis), was investigated using light and scanning electron microscopy. This study focused on finding phylogenetically informative characters to help elucidate any obscure evolutionary patterns within the family. The earliest diverging subfamily Napoleonaeoideae has mixed simple/scalariform vessel perforations, scalariform vessel-ray pitting, and high multiseriate rays, all features that are also present in Scytopetaloideae. The wood structure of Napoleonaea is distinct, but its supposed close relative Crateranthus strongly resembles Scytopetaloideae. The isolated position of Foetidia (Foetidioideae) can be supported by a unique type of vessel-ray pitting that is similar in shape and size to intervessel pitting (distinctly bordered, <5 µm). The more derived Planchonioideae and Lecythidoideae share exclusively simple perforations and two types of vessel-ray pitting, but they can easily be distinguished from each other by the size of intervessel pitting, shape of body ray cells in multiseriate rays, and the type of crystalliferous axial parenchyma cells. The anatomical diversity observed is clearly correlated with differences in plant size (shrubs vs. tall trees): the percentage of scalariform perforations, as well as vessel density, and the length of vessel elements, fibers, and multiseriate rays are negatively correlated with increasing plant size, while the reverse is true for vessel diameter.
Key Words: Ericales • Lecythidaceae s.l. • Lecythidaceae s.s. • Napoleonaeaceae • Scytopetalaceae • systematic wood anatomy
Lecythidaceae s.l., including Napoleonaeaceae and Scytopetalaceae, comprise about 25 genera and 315 species. The family is represented by tall to small trees and shrubs largely distributed in the moist lowland neotropics, while other genera are restricted to tropical West and East Africa, Madagascar, Mauritius, and tropical Asia to North Australia (Appel, 2004
; Prance, 2004
; Prance and Mori, 2004
). A main center of diversity is lowland Amazonia, in which the two most famous Lecythidaceae species grow: the Brazil nut (Bertholletia excelsa Humb. & Bonpl.), known for its edible seeds, and the spectacular cannon-ball tree (Couroupita guianensis Aubl.), which is commonly used as an ornamental plant in (sub)tropical gardens.
Although the family includes some well-known representatives, much more work is needed to clarify the controversial inter- and intrafamily relationships. With respect to its higher level classification, Lecythidaceae were previously placed close to Myrtaceae based on the shared occurrence of separate petals, numerous stamens, and a syncarpous inferior ovary with axile placentation (e.g., Miers, 1874
). However, Lecythidaceae can be clearly distinguished from typical Myrtales taxa based on their alternate leaves, bitegmic and tenuinucellar ovules, lack of intraxylary phloem and vestured pits in wood, and a series of embryological features (see Prance and Mori, 1979
for a detailed taxonomic history; Jansen et al., 1998
). These marked differences led Cronquist (1981)
to the conclusion that Lecythidaceae must be removed from Myrtales (Rosidae) and included in an order of its own close to Theales and Malvales (both Dilleniidae). More recent morphological results (Tsou, 1994
) and molecular sequence data (Morton et al., 1997
; Anderberg et al., 2002
; Schönenberger et al., 2005
) support the Theales link and place the family in the enlarged Ericales sensu APG (APG II, 2003
). Nevertheless, the search for the most closely related families of Lecythidaceae remains ongoing. Some recent molecular analyses hypothesize a sister relationship with Sapotaceae (Morton et al., 1997
; Anderberg et al., 2002
) or Ebenaceae (Bremer et al., 2002
), but the most elaborate parsimony analysis based on 11 molecular markers places Lecythidaceae in a large polytomy together with the rest of the Ericales except for balsaminoids (Schönenberger et al., 2005
). A Bayesian analysis of the same comprehensive data set results in a large tritomy including Lecythidaceae, Fouquieriaceae-Polemoniaceae, and the rest of the Ericales without balsaminoids (Schönenberger et al., 2005
).
Following the family concept of Prance and Mori (1979)
, Lecythidaceae include 20 genera and four subfamilies, i.e., Lecythidoideae (neotropics), Foetidioideae (East Africa, Madagascar and Mauritius), Napoleonaeoideae (Napoleonaea and Crateranthus in tropical West Africa, Asteranthos in the neotropics) and Planchonioideae (Old World tropics). According to the embryological study of Tsou (1994)
, Lecythidoideae and Planchonioideae form the core group of Lecythidaceae, while Foetidioideae and Napoleonaeoideae should be segregated from it and recognized as separate families. Cladistic analyses based on morphological and molecular data further reveal that Scytopetalaceae (including Asteranthos) must be treated as a fifth subfamily in order to maintain the monophyly of the Lecythidaceae (Morton et al., 1997
, 1998
; APG II, 2003
). The earliest diverging lineage is formed by Napoleonaeoideae followed by Scytopetaloideae (including Asteranthos), which is sister to a clade including Planchonioideae-Foetidioideae and Lecythidoideae (Morton et al., 1998
). The inclusion of Scytopetalaceae into the enlarged Lecythidaceae agrees with general morphological resemblances, but both families can be easily distinguished from each other based on the presence/absence of stipules and endosperm, type of stomata, hypogynous vs. epigynous flowers, and the type of aestivation (Letouzey, 1961
; Appel, 1996
, 2004
). According to Appel (1996
, 2004
), these distinctive characters provide sufficient arguments to split the diverse Lecythidaceae s.l. into three morphologically well-established families, i.e., Napoleonaeaceae (Napoleonaea and Crateranthus), Lecythidaceae s.s. (including subfamilies Foetidioideae, Planchonioideae, and Lecythidoideae), and the former Scytopetalaceae. The close relationships of these three evolutionary lines, however, have never been doubted (Prance, 2004
; Prance and Mori, 2004
).
The wood structure of Lecythidaceae has been the subject of several studies, although none of them intended to give an overview of all major lineages in the family. Most wood anatomical papers deal with neotropical representatives, i.e., Lecythidoideae plus Asteranthos (Diehl, 1935
; Richter, 1982
; Détienne and Jacquet, 1983
; de Zeeuw and Mori, 1987
; de Zeeuw, 1990
). Carl de Zeeuw also started a detailed study of the Old World Foetidioideae, Napoleonaeoideae, and Planchonioideae, but unfortunately he passed away before completion of his work (de Zeeuw, [no date]a
–f
). In order to present a thorough overview of the entire family, we have chosen to evaluate de Zeeuw's Old World descriptions and additional literature data (Moll and Janssonius, 1914
; Pearson and Brown, 1932
; Metcalfe and Chalk, 1950
; Normand, 1960
; Normand and Pacquis, 1976
; Carlquist, 1988
) in combination with original observations from all major lineages (Table 1, Appendix 1). In addition to the general descriptive wood studies, there are some papers on Lecythidaceae that focus on crystalliferous cells in the secondary xylem (Chattaway, 1956
; ter Welle, 1976
; Parameswaran and Richter, 1984
).
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in order to evaluate the evolutionary wood patterns and its taxonomic usefulness. We have chosen to focus our phylogenetic results on the subfamily level, because at this moment the current molecular framework has only strong support values at this taxonomic rank. Additional molecular data from trnL-trnF and ndhF regions support the basic Morton topology (Mori et al., 2007
). A final objective is to correlate differences in wood structure with the huge variation in life forms (small shrubs vs. giant trees). MATERIALS AND METHODS
In total, 88 wood specimens of Lecythidaceae s.l. representing 71 species and 24 genera were investigated using LM and SEM (Appendix 1). Most samples were represented by mature sapwood, except for the juvenile twigs of Barringtonia macrostachya Kurz (USw 1205) and Grias peruviana Miers (MADw 43463). The present paper presents the first detailed wood anatomical descriptions for the genera Brazzeia, Oubanguia, and Pierrina (Scytopetaloideae). No wood material could be obtained from Abdulmajidia, a small palaeotropical genus for which we have found no information in the literature.
The methodology of wood sectioning and the subsequent steps are described in Lens et al. (2005)
. The wood anatomical terminology follows the "IAWA list of microscopic features for hardwood identification" (IAWA Committee, 1989
). This also applies for the terminology of crystalliferous axial parenchyma strands, except for the unusual wall thickenings that are not included in the IAWA list; these strands can be unilaterally thickened (only at one side that touches a neighboring fiber) or uniformly thickened (at all sides). Readers who are interested in a more specialized terminology of these strands may refer to Parameswaran and Richter (1984)
. When distinctly bordered vessel-ray pits are mentioned, we mean that the pit pairs are half-bordered, because the pit on the vessel side is bordered, but predominantly simple on the parenchyma cell side. Additional illustrations of microscopic wood pictures of Lecythidaceae can be found on the InsideWood website (http://insidewood.lib.ncsu.edu/search, micrographs taken by F. Lens).
To compare the observed wood diversity with habit, species are subdivided into three groups, i.e., shrubs to small trees growing in the understory (<25 m tall), canopy trees (25–35 m high), and giant emergent trees (up to 60 m) (cf. Mitchell and Mori, 1987
; Mori and Lepsch-Cunha, 1995
). Various floras and revisions were consulted to assign the species to one of the three groups (Perrier de la Bâthie, 1954
; Letouzey, 1961
; Payens, 1968
; Liben, 1971
; Mori and collaborators, 1987
; Bosser, 1988
; Mori and Prance, 1990
), and all wood samples were taken into account, except for the two species with juvenile twigs. The statistical significance of differences in mean values of a given continuous wood character between the three habit categories was calculated using the software package Statistics Calculator version 8.0 (StatPac Inc., Bloomington, Indiana, USA).
RESULTS
The material studied is described according to the subfamily classification of Morton et al. (1998)
. For each genus examined, the numerator represents the number of species studied and the denominator includes the total number of species. Numbers without parentheses are ranges of means, while numbers between parentheses represent minimum or maximum values. A summary of the results is shown in Table 1.
Lecythidaceae-Napoleonaeoideae (Crateranthus 2/3, Napoleonaea 3/8; Figs. 1–10)
Growth ring boundaries indistinct to absent (Figs. 1, 2). Diffuse-porous. Vessels (7–) 10–35 (–40)/mm2, mostly solitary and in radial multiples of 2–4 (–6) (Fig. 2), in Napoleonaea additional vessel clusters of 3–7 present (ranging from 5–40% of the total number of vessels) plus a few tangential multiples of 2–3 (Fig. 1); vessel outline rounded to elliptical; perforation plates in Napoleonaea usually simple but sometimes scalariform with 5–20 bars, exceptionally reticulate, in Crateranthus perforations plates equally mixed simple/scalariform with 1–12 (–21) bars (Fig. 5; Table 1). Intervessel pits alternate to opposite, pits 5–8 µm (Napoleonaea) or 4–6 µm (Crateranthus) in horizontal diameter, nonvestured. Vessel-ray pits in Napoleonaea typically scalariform (to opposite) with indistinct borders to even simple, pit borders 5–35 µm in horizontal diameter, in co-occurrence with few smaller distinctly bordered pits often occurring in different ray cells (Fig. 6), pit borders 5–10 µm in horizontal diameter; in Crateranthus scalariform vessel-ray pitting with strongly reduced borders (Fig. 7), pit cavities 15–55 µm in horizontal diameter (up to 110 µm in Crateranthus talbotii). Wall sculpturing absent. Tyloses occasionally present in both genera. Tangential diameter of vessels (30–) 50–100 (–130) µm, vessel elements (300–) 550 (–900) µm long in Napoleonaea, and (300–) 1000 (–1600) in Crateranthus. Some vasicentric tracheids present near vessel clusters in Napoleonaea (Fig. 8), (450–) 550–850 (–1200) µm long, occasionally co-occurring with tracheid-like elements with one small perforation. Nonseptate fibers (very few septa found in C. talbotii), with simple to minutely bordered pits concentrated in radial walls, thick- to very thick-walled in Napoleonaea but thin- to thick- walled in Crateranthus, (1700–) 2150 (–3000) µm long in Napoleonaea and (2000–) 2700 (–3200) µm in Crateranthus, pit borders 2–4 µm in diameter. Axial parenchyma in Napoleonaea uniseriately banded (Fig. 1), diffuse-in-aggregates to uniseriately banded in Crateranthus (Fig. 2), in 3–10 celled strands. Uniseriate rays in Napoleonaea scarce to absent, 0–1 rays/mm, length (75–) 250 (–600) µm, consisting of square to upright cells; in Crateranthus uniseriate rays common, 4–6 rays/mm, length (200–) 750 (–2300) µm, consisting of square to upright cells. Multiseriate rays in Napoleonaea generally 5–10-seriate (Fig. 3), sometimes up to 17-seriate, (650–) 2100 (–5000) µm high, 1–5 rays/mm, consisting of procumbent and square body ray cells and 1–2 rows of upright to square marginal ray cells; in Crateranthus multiseriate rays 3–7-seriate (Fig. 4), (1200–) 2500 (>5000) µm high, consisting of generally procumbent body ray cells and more than four (up to 20) rows of upright to square marginal ray cells; sheath cells sometimes present in Crateranthus. Dark amorphous contents absent. Few solitary prismatic crystals in (sometimes chambered) marginal ray cells of Crateranthus and in body ray cells of Napoleonaea (Fig. 10), together with few small styloids in body ray cells of both genera; in Crateranthus integumented crystals abundantly present in chambered axial parenchyma cells with uniform wall thickenings (Fig. 9), in Napoleonaea prismatic crystals sometimes in nonchambered axial parenchyma cells without wall thickenings; silica bodies absent in both genera.
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Wood anatomical diversity within Lecythidaceae s.l.
As defined by recent phylogenetic analyses, the broadly circumscribed Lecythidaceae show a high wood anatomical diversity (Figs. 1–63). Despite this conspicuous variation, some common wood features can be listed: solitary vessels that co-occur with distinct radial vessel multiples, simple vessel perforations, alternate intervessel pits, fibers with simple to minutely bordered pits, diffuse-in-aggregates to banded axial parenchyma of 1–3 cells wide, multiseriate heterocellular rays, and prismatic crystals in rays and/or axial parenchyma. More variation is observed in the average vessel diameter (30–260 µm) and vessel element length (350–1130 µm), size of intervessel pitting (3–20 µm in horizontal diameter), arrangement of vessel-ray pits (scalariform, opposite to scalariform, or alternate), fiber wall thickness (very thin- to very thick-walled), width of axial parenchyma bands (one to more than 10 cells wide), abundance of uniseriate rays, width and height of multiseriate rays (2–17-seriate and 260–2765 µm high, respectively), and the number of rows of marginal ray cells in multiseriate rays (1–20). Compared to other ericalean families, a similarly large wood anatomical diversity within one family is only encountered in Ericaceae (Lens et al., 2003
, 2004a
, c
).
Carl de Zeeuw's published and unpublished results can generally be confirmed, although the presence of septate fibers needs some comments: according to de Zeeuw (de Zeeuw, [no date]c
, e
, f
), septate fibers occur in all seven species of Planchonia and sometimes in other Planchonioideae (few species of Careya, Chydenanthus, and Barringtonia). After a careful re-examination, we only found a very small proportion of septate fibers in few species of Crateranthus, Oubanguia, and Planchonia. The presence of dark amorphous material and wall fragments in fibers of these genera can easily be mistaken for septa. Therefore, we conclude that septate fibers are of very little significance in the family. Within Foetidia, variation in vessel diameter and vessel density is greater than described here: F. asymetrica and F. retusa both have a mean vessel diameter of 50 µm or less and a vessel density of more than 200/mm2 (de Zeeuw [no date]a;
P. Détienne, unpublished results, InsideWood website http://insidewood.lib.ncsu.edu/search). Additional minor differences that could not be corroborated in our study include few scalariform or reticulate perforations in Barringtonia racemosa and B. scortechinii, and silica bodies in Planchonia andamanica and P. grandis (de Zeeuw, [no date]e
, f
). Furthermore, we found two new wood features that were previously unknown in the family: (1) small styloids in Brazzeia, Crateranthus, Napoleonaea, and in a few Barringtonia species and (2) a small number of vasicentric tracheids near vessel clusters in Napoleonaea and in Grias peruviana (USw 40764).
Intrafamily relationships
The genera Napoleonaea and Crateranthus of Napoleonaeoideae (NAP) can be identified by a combination of several characters, such as the occurrence of mixed simple and scalariform vessel perforations, predominantly scalariform vessel-ray pitting with distinct to strongly reduced borders, and broad (3–10-seriate) and high (2000–2500 µm) multiseriate rays (Figs. 3–7). Furthermore, silica bodies and parenchyma bands of over one cell wide are absent. The secondary xylem of NAP mostly resembles that of Scytopetaloideae (SCY), which is indicated by the mixed simple/scalariform perforations (also in Barringtonia and Grias), scalariform vessel-ray pitting, diffuse-in-aggregates to uniseriately banded axial parenchyma, and the abundance of uniseriate rays. Moreover, both subfamilies possess high multiseriate rays (on average more than 1 mm high; also present in Barringtonia, Grias, and Gustavia) with long uniseriate tails (except in Napoleonaea and Scytopetalum), while silica bodies are always absent. No clear differences could be found to distinguish NAP from SCY because of the striking similarities of the SCY with Crateranthus. However, because molecular sequence data of Crateranthus are still lacking at this moment, it is possible that this genus has more affinities to SCY than to Napoleonaea. If this should be the case, Napoleonaeoideae comprises only the type genus, which can be supported by its distinctive wood structure (a limited number of vasicentric tracheids surrounding the vessel clusters, wide rays up to 17-seriate; Figs. 3, 8), but also by other distinguishing morphological features such as a chromosome number of x = 16 and extrorse anther dehiscence (Morton et al., 1997
).
Within SCY, two distinct groups can be made based on the vessel perforation plate morphology: (1) Brazzeia, Pierrina, and Rhaptopetalum have a high percentage of scalariform perforations (more than 80%), and (2) Asteranthos, Oubanguia, and Scytopetalum have predominantly simple perforations (Table 1; Figs. 18–20). This supports the recognition of subfamilies Rhaptopetaloideae and Scytopetaloideae sensu Appel (1996)
, a division that is based on differences in leaves, flowers, pollen, and seeds. Despite the systematic value of the vessel perforation type, this feature is clearly correlated with different life forms (shrubs and small trees vs. large trees; discussed later).
There are several morphological synapomorphies that indicate the isolated position of Foetidioideae (FOE), including amongst others the lack of petals (also observed in Asteranthos, Crateranthus, and Napoleonaea; Morton et al., 1997
). The wood structure provides two additional characters that can be used to identify this monogeneric subfamily: small intervessel pits (3–4 µm, also observed in Gustavia) that are similar in shape and size to the vessel-ray pits (Fig. 31) and weakly developed vessel wall thickenings that accompany pit apertures at the inside of vessel elements (Fig. 33). Furthermore, Foetidia has silica bodies in rays (Fig. 34) and in axial parenchyma, a combination that is only found elsewhere in Cariniana, Eschweilera, and Petersianthus (de Zeeuw, 1990
).
Besides its unique syntricolpate pollen grains (Muller, 1972
), Planchonioideae (PLA) have a distinctive wood structure due to the large intervessel pitting (more than 10 µm in horizontal diameter, Fig. 41; also observed in Couroupita), multiseriate rays with mixed procumbent/square body ray cells (Fig. 44), and crystalliferous axial parenchyma cells without wall thickenings (also in Napoleonaea). Other common wood features within PLA include exclusively simple perforations and the presence of vessel-ray pitting consisting of small distinctly bordered pits that co-occur with larger simple pits in mostly different cells. This type of vessel-ray pitting is also sporadically found in Napoleonaea and in members of SCY, thereby forming a link with PLA (Figs. 6, 23, 42, 43). Also the occurrence of long uniseriate tails of multiseriate rays in Crateranthus, SCY, and PLA support this association (Figs. 4, 15, 16, 38, 39).
Most members of Lecythidoideae (LEC) can be identified by vessel-ray pitting consisting of many small distinctly bordered pits that co-occur with large simple pits in the same cells (Figs. 57, 58), scarce uniseriate rays, narrow (2–4-seriate) and low (<1000 µm) multiseriate rays (Figs. 51, 52), lack of prismatic crystals in rays, and chambered crystalliferous axial parenchyma strands showing many septa and unilaterally thickened walls (Fig. 61). Another common feature is the presence of silica bodies in ray cells (Fig. 63). From a wood anatomical point of view, LEC resembles the sister clade including Foetidia (exclusively simple perforations, narrow and low multiseriate rays, and silica bodies) and PLA (predominantly simple perforations, two types of vessel-ray pits, and silica bodies) (de Zeeuw and Mori, 1987
; de Zeeuw, 1990
). In addition to the distinguishing wood anatomical characters, Lecythidoideae can be characterized by a specific basic chromosome number of x = 17 (Morton et al., 1997
).
Within LEC, some wood characters agree with relationships hypothesized previously. For example, Mori et al. (2005)
find that Grias and Gustavia are basal to the remaining LEC. This placement can be supported by their characteristically wide (more than 4-seriate) and high (on average more than 1 mm) multiseriate rays that have heterocellular body ray cells (Figs. 53, 54; also present in PLA), prismatic crystals in rays (also present in NAP, SCY, and PLA), and their nonseptate crystalliferous axial parenchyma cells with uniformly thickened walls (Fig. 62; also present in Crateranthus and SCY). Furthermore, the clade recognized by Morton et al. (1998)
, including Allantoma, Cariniana, Corythophora, Couratari, Eschweilera, and Lecythis, is the only LEC group in which silica bodies occur (Fig. 63). The sister genus of this group, Bertholletia, has several characters in common, such as the unique crystalliferous strands, and narrow and low multiseriate rays that lack prismatic crystals (Figs. 51, 52, 61). The wood structure of the latter clade is very homogeneous and does not permit commenting on the disputed generic boundaries of several genera (cf. Mori et al., 2005
).
Evolution of the wood structure within Lecythidaceae s.l.
As demonstrated in combined molecular/morphological analyses, NAP are the earliest diverging lineage followed by SCY, while FOE, LEC, and PLA have a more derived position (Morton et al., 1997
, 1998
). The wood structure provides arguments that seem to corroborate these relationships. Long vessel elements with scalariform perforations, common in NAP but also in SCY (mean length 770 µm), correspond to the primitive vessel type according to the Baileyan trends (Bailey and Tupper, 1918
), while derived vessels in the Baileyan sense are much shorter (on average 530 µm in LEC; 400 µm in FOE) and have exclusively simple perforations. PLA have intermediate vessel element lengths. Despite the general phylogenetic value of vessel element length in woody angiosperms, the suggested character polarity must be treated with caution in Lecythidaceae s.l. because of its correlation with plant size (discussed later), but this does not always mean that taxonomically informative and habit-related characters are mutually exclusive (cf. ray width differences between lianous Marcgravia and other Marcgraviaceae; Lens et al., 2005
). Another possible phylogenetically important character is the vessel-ray pitting that evolves from the so-called primitive scalariform type (NAP, SCY) to the more derived alternate type on the one hand (FOE) and to the development of two distinct pit types on the other (LEC, PLA), although Frost (1931)
also mentions a specialization from half-bordered to entirely simple vessel-parenchyma pits. There is also a general reduction in multiseriate ray height from more than 1500 µm in NAP and most SCY toward less than 700 µm in FOE and most LEC, while PLA have intermediate values. In addition, the proportion of uniseriate rays dramatically decreases from NAP and SCY toward the other subfamilies (on average 4–6 vs. 0–2 rays/mm, respectively). A final character that has taxonomic value is the morphology of the crystalliferous axial parenchyma cells: uniformly thickened cells in Crateranthus, FOE, and SCY evolve to nonthickened cells in PLA and to unilaterally thickened cells with many septa in most LEC. In other wood characters, more homoplasious variation is found, for instance in the distribution of axial parenchyma and the width of multiseriate rays.
Interfamily relationships
Considering the huge wood diversity of Lecythidaceae s.l. and its ambiguous taxonomic position within Ericales, it is difficult to assign its closest relatives. Based on the wood structure, several candidates can be suggested, such as Ebenaceae, Fouquieriaceae, Polemoniaceae, and Sapotaceae (Table 2). These families share the presence of radial vessel multiples with 2–4 cells that co-occur with solitary vessels, predominantly simple perforations, alternate intervessel pitting, diffuse-in-aggregates to banded axial parenchyma (more variation in Polemoniaceae), fibers with minutely bordered to simple pits (more variation in Polemoniaceae), and prismatic crystals in axial parenchyma cells (absent in Polemoniaceae) (Carlquist et al., 1984
; Carlquist, 2001b
; Lens, 2005
; Table 2). A combined wood/molecular bootstrap analysis at the Ericales level shows that Lecythidaceae are sister to Fouquieriaceae-Polemoniaceae, although support value for this surprising relationship is low (Lens et al., in press
).
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and Anderberg et al. (2002)
. Indeed, the presence of two types of vessel-ray pits is restricted to a few woody angiosperm families, such as Erythroxylaceae (Malpighiales), Lecythidaceae and Sapotaceae (both Ericales), and Olacaceae and Santalaceae (both Santalales) (IAWA Committee, 1989
), and might therefore be considered as a phylogenetically informative character. However, a potential close relationship between Lecythidaceae and Sapotaceae is contradicted by striking differences in flowers and fruits (Appel, 2004
; Pennington, 2004
; Prance, 2004
; Prance and Mori, 2004
). It is more likely that Ebenaceae and Sapotaceae are more closely related to primuloids than to Lecythidaceae (Schönenberger et al., 2005
; Lens et al., in press
).
Impact of environmental conditions and life form
Lecythidaceae generally grow in moist tropical lowland forests, which may be periodically inundated, with only few species occurring at elevations above 1000 m a.s.l., while others are restricted to savannas (Lecomte, 1920
; Letouzey, 1961
; Payens, 1968
; Liben, 1971
; Prance and Mori, 1979
; Mitchell and Mori, 1987
; Bosser, 1988
). We found no differences in wood structure between species that are typically growing in periodically flooded forests (e.g., species of Allantoma, Brazzeia, Couroupita, Pierrina, and Rhaptopetalum) or noninundated forests (the majority of the species studied). A minor exception is the presence of distinct growth rings, which is more pronounced in the inundated species (Figs. 11, 12) compared to the nonflooded ones (cf. Worbes, 1989
), although indistinct growth rings are widespread among the nonflooded group. de Zeeuw's (1990)
extensive sampling of Eschweilera, the only genus that occurs above 1000 m a.s.l., shows no altitudinal trends in the secondary xylem compared to the lowland genera.
de Zeeuw ([no date]a
) and Détienne (P. Détienne, unpublished results, InsideWood website, http://insidewood.lib.ncsu.edu/search) found significant differences in the wood structure of Foetidia: F. asymetrica and F. retusa growing in the dry and hot regions of western Madagascar have significantly higher vessel densities and lower vessel diameters compared to the (sub)humid species in the central and eastern part of the country (on average 250 vs. 40 vessels/mm2 and 45 vs. 70 µm in tangential width, respectively) (Perrier de la Bâthie, 1954
; Bosser, 1988
). The single species in the present study, F. mauritiana, corresponds to the wet Malagassy group of species. It is the only sample with a slight development of wall sculpture accompanying the pit apertures (coalescent or not) on the inside of vessel elements (Fig. 33). In a more extensive shape, this character can develop into helical thickenings, a character that is most common in temperate and mediterranean zones (Baas and Schweingruber, 1987
) or in areas that are drier or subject to freezing (Carlquist, 2001a
). It is possible that other Foetidia species also show wall sculpture patterns in their vessels, although de Zeeuw's and Détienne's descriptions did not mention this character.
The great diversity of life forms in Lecythidaceae, ranging from small shrubs to giant emergent trees, provides the opportunity to relate the wood structure with different habits. Table 3 gives a summary of the most important results: the wood structure of canopy and emergent trees is almost identical (except for a slightly larger vessel diameter in the emergent trees), but the two groups clearly differ from the understory woody plants in the presence of exclusively simple perforations, wider vessel diameters, lower vessel densities, and a shorter length of vessel elements, fibers, and multiseriate rays. These habit trends generally agree with correlations found in previous studies, except for the length of vessel elements (and fibres) that are normally larger in tall trees compared to shrubs (Baas, 1976
; Carlquist and Hoekman, 1985
; Baas and Schweingruber, 1987
; Carlquist, 2001a
; Lens et al., 2004b
). Furthermore, there is a tendency for wider rays in the understory species, although there is too much variation to generalize this. According to Carlquist (1988)
, the presence of fibers with conspicuously bordered pits in the genera Rhaptopetalum and to a lesser extent in Pierrina may be related to the understory habit, although this can be questioned because this fiber type is not encountered in other understory species. Within the understory group, we find similar correlations between the 15 larger trees (15–25 m high; UC in Table 1) and the 38 shrubs or low trees (below 15 m) for the percentage of species with scalariform perforations (8 vs. 19%), vessel diameter (110 vs. 85 µm), vessel density (11 vs. 19/mm2), and multiseriate ray height (1200 vs. 1520 µm).
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APPENDIX
List of taxa investigated in this study with reference to their locality and vouchers. Institutional wood collections used in this study are abbreviated according to Index Xylariorum (Stern, 1988
).
Subfamily
Species—Locality; Voucher data.
Napoleonaeoideae
Crateranthus letestui H.Lec.—Gabon; Normand 196 (CTFw 5187). C. letestui H.Lec.—Gabon; Forest Research Institute 1315 (CTFw 8603). C. talbotii Bak.f.—Cameroon; Letouzey 10833 (CTFw 20321). Napoleonaea leonensis Hutch. & Dalziel—Liberia; Cooper 86A (MADw 30899). N. septentrionalis Liben—Democratic Republic of Congo; Ntahobavuka s.n. (Tw 57631). N. sp.—Ivory Coast; Bamps 2377 (MADw 32810). N. sp.—Ivory Coast; Bamps 2553 (MADw 32803). N. vogelii Hook. & Planch.—Ivory Coast; Détienne 90 (MADw 36819). N. vogelii Hook. & Planch.—Democratic Republic of Congo; Dechamps s.n. (MADw 41143). N. vogelii Hook. & Planch.—Democratic Republic of Congo; Dechamps s.n. (MADw 41120).
Scytopetaloideae
Asteranthos brasiliensis Desf.—Venezuela (Amazonas); Maguire et al. 41834 (Tw 36193). A. brasiliensis Desf.—Brazil; Ducke 57 (USw 8661). Brazzeia congoensis Baill.—Democratic Republic of Congo; Bertault 100 (CTFw 18363). B. soyauxii Tiegh.—Gabon; Forest Research Institute 1088 (CTFw 8488). Oubanguia africana Baill.—Democratic Republic of Congo; Louis 104 (Tw 32808). O. sp.—Democratic Republic of Congo; Louis 1972 (Tw 33343). Pierrina zenkeri Engl.—Cameroon (near Kribi); Bos 3856 (WAG). Rhaptopetalum beguei Mangenot—The Netherlands (Wageningen Botanic Gardens); van Setten 478 (WAG). R. sp.—Cameroon; Breteler 2754 (MADw 36223). Scytopetalum brevipes Tiegh.—Gabon; Normand 194 (MADw 36939). S. klaineanum Pierre—Gabon; Gavage s.n. (Tw 25725). S. tieghemii Hutch. & Dalziel—Democratic Republic of Congo (Kasai); Dechamps 292 (Tw 22970). S. tieghemii Hutch. & Dalziel—SE Ivory Coast; Détienne 163 (Tw 29979).
Foetidioideae
Foetidia mauritiana Lam.—Mauritius; Dentzman A1791 (MADw 10231). F. mauritiana Lam.—Mauritius; Collector unknown (MADw 30811).
Planchonioideae
Barringtonia acutangula Gaertn.—Burma; Forest Botanist 1654 (MADw 30777). B. asiatica (L.) Kurz—Philippines; Philippine Bureau of Forestry 28145 (MADw 6763). B. edulis Seem.—Fiji Islands; Smith s.n. (SJRw 27719). B. lanceolata (Ridl.) Payens—Brunei; Ogata et al. s.n. (MADw 48144). B. pauciflora Lauterb.—New Guinea (West Irian); Collector unknown (USw 34332). B. longisepala Payens—Malaysia; Meijer 122304 (MADw 48591). B. macrostachya Kurz—Malaysia; Forest Research Institute s.n. (SJRw 28940). B. macrostachya Kurz—Malaysia (Sumatra); Boeeca 1205 (USw 1205). B. procera (Miers) Knuth—Papua New Guinea (Gazelle Peninsula); Waterhouse s.n. (SJRw 29763). B. samoensis A.Gray—Samoa (Tutuila); Bryan Jr. s.n. (SJRw 24496). B. scortechinii King—Malaysia; Forest Research Institute s.n. (SJRw 28939). B. speciosa J.R.Forst. & G.Forst.—Philippines; Philippine Bureau of Forestry s.n. (MADw 30779). B. spicata Blume—Java; Janssonius 1655m (SJRw 30916). Careya arborea Roxb.—India; Stewart & Brandis 1479 (MADw 1439). Chydenanthus excelsus (Blume) Miers—origin unknown; Collector unknown (WIBw 5182, WAG). Petersianthus macrocarpus (Beauv.) Liben—Democratic Republic of Congo; Martincic & Lju 85772 (MADw 39312). P. quadrialatus Merr.—Philippines; Philippine Bureau of Forestry 12814 (MADw 36628). Planchonia andamanica King—India (Andaman Islands); Lee s.n. (USw 5075). P. papuana Knuth—New Guinea; Collector unknown 20212 (USw 24046). P. spectabilis Merr.—Philippines; Philippine Bureau of Forestry 1666 (MADw 30900). P. timorensis Blume—Papua New Guinea; Department of Forests 39 (MADw 21794). P. valida Blume—Democratic Republic of Congo; Collector unknown (MADw 17791).
Lecythidoideae
Allantoma lineata Miers—Brazil (Amapa); Collector unknown (Tw 37426). A. lineata Miers—Brazil; Maguire et al. 51738 (MADw 21433). Bertholletia excelsa Humb. & Bonpl.—Guiana; Smith 2868 (Tw 27251). Cariniana decandra Ducke—Brazil; Krukoff 7193 (MADw 12861). C. micrantha Ducke—Brazil (Matto-Grosso); Krukoff 1439 (Tw 34677). C. multiflora Ducke—Brazil; Krukoff 8624 (MADw 30790). C. pyriformis Miers—Colombia; Curran 353 (MADw 30792). Corythophora alta Knuth—Brazil; Pires & Cavalcante 52664 (MADw 22720). C. amapaensis S.A.Mori & Prance—Brazil (Amapa); Collector unknown (Tw 37160). C. rimosa W.A.Rodrigues—Brazil; Ducke s.n. (SJRw 21345). Couratari guianensis Aubl.—French Guyana; Fouquet 1353 (Tw 47829). C. guianensis Aubl.—Brazil; Maguire 51854 (MADw 21542). C. macrosperma A.C.Sm.—Brazil; Krukoff 1653 (MADw 30796). C. multiflora Eyma—Brazil; Krukoff 1901 (MADw 30794). C. scottmorii Prance—Costa Rica; Wiemann 67 (MADw 42705). Couroupita guianensis Aubl.—Brazil (Para); Krukoff 1236 (Tw 34585). C. guianensis Aubl.—Brazil; Krukoff 1705 (MADw 30804). C. nicaraguensis DC.—Panama; Cooper & Slater 302 (MADw 30808). C. subsessilis Pilg.—Brazil; Krukoff 4741 (MADw 18541). C. subsessilis Knuth—Brazil; Krukoff 8066 (MADw 30803). Eschweilera amazonica Knuth—Brazil; Zarucchi et al. 3190 (MADw 48836). E. calyculata Pittier—Panama; Cooper 475 (MADw 30853). E. gigantea Knuth—Brazil; Krukoff 8664 (MADw 30843). E. sclerophylla Cuatrec.—Colombia; Cuatrecasas 16517 (MADw 30882). Grias cauliflora L.—Costa Rica; Nee & Mori 3567 (MADw 25993). G. cauliflora L.—Costa Rica (Puntarenas); Nee & Mori 3574 (Tw 31515). G. colombiana Cuatrec.—Colombia; Fuchs 21914 (USw 38210). G. neuberthii J.F.Macbr.—Peru; Williams 2337 (MADw 15313). G. peruviana Miers—Ecuador; Dorr et al. 5822 (MADw 43463). G. peruviana Miers—Peru; Schunke 4463 (USw 40764). Gustavia augusta L.—Brazil (Matto-Grosso); Krukoff 1525 (Tw 33922). G. gigantophylla Sandwith—Venezuela; Nee & Mori 4058 (MADw 25995). G. poeppigiana O.Berg—Brazil; Krukoff 8440 (MADw 30819). G. cf. pulchra Miers—Colombia; Nee & Mori 3801 (MADw 26001). Lecythis ampla Miers—Colombia; Curran 305 (MADw 7170). L. confertiflora (A.C.Sm.) S.A.Mori—Guyana; British Guyana Forestry Department 4806 (MADw 3783). L. corrugata Poit.—Guiana; Smith 2695 (Tw 27253). L. lurida (Miers) S.A.Mori—Brazil (Para); Krukoff 1213 (Tw 34583). L. mesophylla S.A.Mori—Colombia; Nee & Mori 3728 (MADw 26005). L. turyana Pittier—Panama; Holdridge 6286 (MADw 24829). L. zabucajo Aubl.—NW Guiana; Maguire et al. 40551 (Tw 37173).
FOOTNOTES
1 This manuscript is dedicated to the late Carl de Zeeuw (professor at the State University of New York, Syracuse) who made significant contributions in the elucidation of the microscopic structure of Lecythidaceae wood. The curators of the xylaria of Madison, Montpellier, Tervuren, and Washington are greatly acknowledged for their supply of wood samples, and valuable comments of R. Miller, S. Mori, E. Wheeler, and one anonymous reviewer are appreciated. The authors thank Ms. A. Vandeperre (K.U.Leuven) and Ms. B.-J. Van Heuven (NHN Leiden) for technical assistance. This work has been financially supported by research grants of the K.U.Leuven (OT/05/35) and the Fund for Scientific Research-Flanders (Belgium) (G.0268.04). F.L. is a postdoctoral fellow of the Fund for Scientific Research–Flanders (Belgium) (F.W.O.–Vlaanderen). 
5 Author for correspondence (e-mail: frederic.lens{at}bio.kuleuven.be
)
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