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Anatomy and Morphology |
2Laboratory of Plant Systematics, Institute of Botany and Microbiology, K.U.Leuven, Kasteelpark Arenberg 31, B-3001 Leuven, Belgium; 3Forschungsinstitut Senckenberg, Senckenberganlage 25, D-60235 Frankfurt/M., Germany; 4Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS UK
Received for publication July 23, 2004. Accepted for publication February 8, 2005.
ABSTRACT
Wood samples of 49 specimens representing 31 species and 11 genera of woody balsaminoids, i.e., Balsaminaceae, Marcgraviaceae, Pellicieraceae, and Tetrameristaceae, were investigated using light microscopy and scanning electron microscopy. The wood structure of Marcgraviaceae, Pellicieraceae, and Tetrameristaceae is characterized by radial vessel multiples with simple perforation plates, alternate vessel pitting, apotracheal and paratracheal parenchyma, septate libriform fibers, and the presence of raphides in ray cells. Tetrameristaceae and Pellicieraceae are found to be closely related based on the occurrence of unilaterally compound vessel-ray pitting and multiseriate rays with long uniseriate ends. The narrow rays in Pelliciera are characteristic of this genus, but a broader concept of Tetrameristaceae including Pelliciera is favored. Within Marcgraviaceae, wide rays (more than five-seriate) are typical of the genus Marcgravia. Furthermore, there is evidence that the impact of altitude and habit plays an important role in the wood structure of this family. The wood structure of Balsaminaceae cannot be compared systematically with other balsaminoids because of their secondary woodiness. Balsaminaceae wood strongly differs due to the presence of exclusively upright ray cells in Impatiens niamniamensis, the absence of rays in Impatiens arguta, and the occurrence of several additional paedomorphic features in both species.
Key Words: Balsaminaceae • balsaminoid clade • Ericales • Marcgraviaceae • paedomorphism • Pellicieraceae • Tetrameristaceae • wood anatomy
The balsaminoid clade of Ericales comprises Balsaminaceae, Marcgraviaceae, Pellicieraceae, and Tetrameristaceae (Anderberg et al., 2002
; Bremer et al., 2002
). These families include a total number of 12 genera and about 1130 species, depending on the number of species accepted within Impatiens L. (more than 900 and still increasing according to Yuan et al., 2004
; about 1000 according to Fischer, 2004
). Balsaminaceae, which include the monotypic Hydrocera Blume and the huge genus Impatiens, are predominantly herbaceous and often grow in montane areas of the tropics and subtropics of the Old World. Only a few Impatiens species have a stem with a woody base, while the three other families are all woody. The neotropical Marcgraviaceae, comprising seven genera and about 130 species, include many lianas but also climbing shrubs and some trees (Dressler, 2004
). The mangrove tree Pelliciera rhizophorae Planch. & Triana, the only representative of Pellicieraceae, grows in tidal swamps along the Pacific coast from Costa Rica to Ecuador (Kobuski, 1951
) and more sparsely on the Atlantic coast of Nicaragua, Panama, and Colombia (Roth and Grijalva, 1991
). The two genera of Tetrameristaceae have a peculiar distribution pattern: Tetramerista Miq. is represented by large trees growing in tropical Southeast Asia, while the monotypic Pentamerista Maguire is a shrub or small tree occurring in the Guayana Highlands of Venezuela (Maguire et al., 1972
).
The balsaminoid clade, which is sister to all other ericalean families, is one of the few groups in Ericales that is well supported based on molecular sequence data (Savolainen et al., 2000
; Soltis et al., 2000
; Anderberg et al., 2002
; Bremer et al., 2002
; Geuten et al., 2004
). Marcgraviaceae, Pellicieraceae, and Tetrameristaceae were considered to be closely related by most earlier botanists, and Hallier (1916
, 1921
) even placed them in one family. On the other hand, the inclusion of Balsaminaceae is surprising because of the aberrant systematic position of this family in previous morphological classifications (Cronquist, 1988
; Dahlgren, 1989
; Takhtajan, 1997
; Thorne, 2000
). Furthermore, interfamily relationships within the balsaminoid clade remain obscure. It is clear that Pelliciera is closely related to Tetrameristaceae, and should possibly be merged in Tetrameristaceae sensu lato (s.l.) (Bremer et al., 2002
; APG II, 2003
), but the question of whether this family is more related to Marcgraviaceae than to Balsaminaceae is still a matter of dispute. Anderberg et al. (2002)
suggest that Balsaminaceae take the most basal position with Marcgraviaceae sister to Pellicieraceae and Tetrameristaceae, while in the analyses of Bremer et al. (2002)
Marcgraviaceae turn out to be the most basal family with Balsaminaceae sister to Tetrameristaceae s.l. In addition, the balsaminoid clade according to Geuten et al. (2004)
is divided into two sister clades, a Balsaminaceae-Marcgraviaceae clade and a Pellicieraceae-Tetrameristaceae clade.
Intrafamily relationships of Balsaminaceae and Marcgraviaceae are far from being resolved. Within Impatiens, the delimitation of species groups is very difficult due to hybridization processes (Grey-Wilson, 1980
). Molecular analyses of ITS sequence data revealed some interesting new relationships within Impatiens, although the basal groups remain poorly understood (Yuan et al., 2004
). Within Marcgraviaceae, variation in inflorescences and differences in the shape and position of nectary bracts resulted in three new genera that were recently elevated from the Norantea Aubl. s.l. complex, i.e., Marcgraviastrum (Wittm. ex Szyszyl.) de Roon & S. Dressler, Sarcopera Bedell, and Schwartzia Vell. (de Roon and Dressler, 1997
). Phylogenetic analyses based on chloroplast sequences supported two subfamilies, Marcgravioideae (including Marcgravia L.) and Noranteoideae (including all other genera), but relationships within Noranteoideae were poorly resolved (Ward and Price, 2002
).
The wood structure of the balsaminoid clade has received only little attention. Wood samples of Pelliciera were studied by Record (1942)
and Baretta-Kuipers (1976)
, and Tetrameristaceae were investigated by Maguire et al. (1972)
. A wood anatomical comparison of Tetrameristaceae, Pellicieraceae, and Marcgraviaceae was made by Bedell (1980)
in her unpublished master's thesis. Consequently, the secondary xylem of Marcgraviaceae is poorly known, and only a few studies deal with some representatives of this family, such as Juel (1887)
, Beauvisage (1920)
, Williams (1936)
, Vestal (1937)
, Record and Hess (1943)
, Metcalfe and Chalk (1950)
, de Roon (1975)
, and Dressler (1994)
. Furthermore, as far as we know, only one paper described very briefly the wood structure of an Impatiens species (Gerard, 1917
).
This study provides detailed wood anatomical descriptions of the poorly known families Balsaminaceae and Marcgraviaceae, which are compared with additional observations of Pellicieraceae and Tetrameristaceae. Wood anatomical variation in Marcgraviaceae will be used to test intrafamily relationships and to determine to what extent differences in habit and altitude may influence the secondary xylem. Within the predominantly herbaceous Balsaminaceae, the possibility of secondary woodiness of two Impatiens species is investigated. The wood anatomical variation observed will be used to comment on the difficult interfamily relationships within the balsaminoid clade.
MATERIALS AND METHODS
Wood samples of 49 specimens representing 31 species and 11 genera were investigated using LM and SEM. Transverse and longitudinal sections of approximately 25 µm were cut using a sledge microtome (Reichert, Vienna, Austria). After bleaching, the sections were stained with a mixture of safranin and alcian blue (35 : 65), dehydrated in an ethanol series (50, 75, 96%) and mounted in Euparal (Agar Scientific, Stansted, UK). Macerations were prepared according to Franklin (1945)
. Sections were observed using a Dialux 20 light microscope (Leitz, Wetzlar, Germany) and photographed with a DP50-CU digital camera (Olympus, Hamburg, Germany). Wood sections for SEM observations were gold-coated with a sputter coater (SPI Supplies, West Chester, Pennsylvania, USA), and observed using a JEOL JSM-5800 LV scanning electron microscope (JEOL, Tokyo, Japan).
The wood anatomical terminology follows the "IAWA list of microscopic features for hardwood identification" (IAWA Committee, 1989
). In order to investigate the impact of altitude and habit on the wood of Marcgraviaceae, four groups were made. These four groups include 16 climbing lowland specimens (growing under 1000 m), four climbing montane species (occurring above 1000 m), two erect species from the lowlands, and three erect species from the montane regions. Only species with mature wood were taken into account. In general, a stem diameter of 15 mm or more was considered to include mature wood, except for the mature wood specimen Marcgravia pedunculosa Triana & Planch. (Uw 4837, 12 mm). In addition, the wood specimen of Marcgravia brownei (Triana & Planch.) Krug & Urb. (FR, 15 mm) was considered to be juvenile because of the large amount of pith parenchyma tissue. The species used in the four categories are indicated in Table 2. Statistical differences were calculated at the 0.5% level using the software program Statistics Calculator version 8.0. (StatPac Inc., Bloomington, Indiana, USA).
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and Carlquist (2001)
. Therefore, we prefer to give a detailed description of these fibers. For all quantitative data on fibers, 25 measurements based on clearly identifiable cells in maceration slides were taken into account. The wood samples studied are listed in Table 1 with reference to the origin, collector, and the diameter of the wood sample in millimeters.
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The material studied is described according to family. For each genus examined, the numerator gives the number of species studied and the denominator includes the total number of species. Numbers between brackets are extreme values. Values for vessel multiples, pits, bar number, axial parenchyma cells per strand, ray width, and ray density are maximum ranges. A summary of the results is presented in Table 2.
Balsaminaceae (Impatiens 2/ca. 1000; Figs. 1–7)
Growth ring boundaries absent. Wood diffuse-porous. Vessels (10)– 30–50–(64)/mm2, usually solitary (Figs. 1–2), occasionally in radial multiples of 2–3, vessel outline angular. Vessel perforation plates generally simple (Fig. 5), but very few scalariform perforations with 1–3 bars in I. arguta Hook. f. & Thoms. Lateral wall pitting mostly scalariform or sometimes reticulate (Figs. 6–7), minutely bordered, pit cavities 10–75 µm in horizontal size, non-vestured. Tangential diameter of vessels (25)–40–80–(100) µm, vessel elements (130)–210– 300–(450) µm long; vessels storied in I. niamniamensis Gilg; thin-walled tyloses abundant in vessels of I. niamniamensis (Figs. 2, 4). Tracheids absent. Fibers non-septate, thin-walled, and relatively wide, (360)–570–640–(900) µm long, with mostly simple to occasionally minutely bordered pits equally distributed in radial and tangential walls, pits 1–3 µm in diameter, fibers occasionally storied in both species. Axial parenchyma scanty paratracheal in I. arguta (Fig. 1), 3–7 cells per strand; abundant in I. niamniamensis (Fig. 2), vasicentric or in bands of 2–3 cells wide, sometimes up to 5 cells, 1–2 cells per strand. Rays absent in tiny stem of I. arguta (Fig. 3), but exclusively multiseriate in I. niamniamensis, ray cells storied (Fig. 4), 11–21 cells wide (Figs. 2, 4), more than 7000 µm high, 1–2 rays/mm, consisting of upright cells only; sheath cells absent; very small simple pits between ray cells, usually 2 µm in horizontal size. Rare occurrence of raphides in tyloses of I. niamniamensis.
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There are several disagreements between the descriptions given in this work and earlier studies, and this is especially the case for Marcgraviaceae. For example, Vestal (1937)
and Metcalfe and Chalk (1950)
mentioned that the wood structure of Norantea s.l. differs in many aspects from the wood of Marcgravia and Souroubea, but this is refuted in this study and in some previous studies (de Roon, 1975
; Bedell, 1980
). Furthermore, Bedell (1980)
mentioned several features that could not be supported by us, i.e., vestured, opposite to transitional intervessel pits in Ruyschia, fibers with helical thickenings in Marcgravia, Norantea s.l., and Souroubea, predominantly homocellular rays consisting of mainly upright cells, and the presence of secretory canals in Schwartzia. This author also reported a lack of axial parenchyma in Ruyschia and Schwartzia and the absence of uniseriate rays in species of Marcgravia, Ruyschia, and Souroubea, two features that are present in all wood samples that we examined. According to our observations, at least some of these differences may be due to the juvenile nature of the wood. Indeed, some of our juvenile Marcgravia samples had very little axial parenchyma, almost no uniseriate rays, and multiseriate rays with exclusively upright ray cells. Previous wood anatomical descriptions of Tetrameristaceae and Pellicieraceae are similar to our results, although Bedell (1980)
did not observe uniseriate rays in Tetramerista, a feature that was clearly observed by us.
Wood anatomical comparison of Marcgraviaceae, Pellicieraceae, and Tetrameristaceae
The close relationship of Marcgraviaceae, Pellicieraceae, and Tetrameristaceae is supported by several wood anatomical features, such as a high frequency of radial vessel multiples, predominantly simple vessel perforation plates, alternate intervascular pitting, a mixed occurrence of apotracheal and paratracheal parenchyma, predominantly septate libriform fibers, co-occurrence of uniseriate and multiseriate rays, and raphides in ray cells (see also Beauvisage, 1920
; Baretta-Kuipers, 1976
; Bedell, 1980
). Most of these characters are also observed in the unrelated woody primuloids, but the presence of raphides in rays is typical of balsaminoids. In addition, two other features that clearly distinguishes woody balsaminoids from primuloids is the general absence of uniseriate rays in Myrsinaceae and Theophrastaceae, and the lack of apotracheal parenchyma in primuloids (Lens et al., 2005
).
Despite the anatomical resemblances mentioned, the wood structure allows us to distinguish the three balsaminoid families from each other (Table 3). Tetrameristaceae are defined by exclusively, very thick-walled fibers and diffuse-in-aggregates axial parenchyma, two features that are normally absent in Pellicieraceae and Marcgraviaceae. The low percentage of septate fibers within Tetrameristaceae could be underestimated because of the very thick fiber walls that complicate the observation of septa. Furthermore, the genus Tetramerista is characterized by the presence of raphides in procumbent ray cells and by the occurrence of very long fibers, often between 2500 and 3000 µm. Long fibers are not unusual in Ericales; they are also found in Lecythidaceae s.l. (Carlquist, 1988
), Symplocaceae (van den Oever, 1981
), and Theaceae (Liang and Baas, 1990
). Pellicieraceae are defined by long radial vessel multiples of up to nine cells, sparse axial parenchyma (diffuse apotracheal and scanty paratracheal), and narrow multiseriate rays. Typical features of Marcgraviaceae include vasicentric parenchyma, multiseriate rays including upright, square, and procumbent body ray cells, and multiseriate rays with few rows of marginal ray cells. In addition, the presence of very wide vessels (more than 250 µm), which are always rounded in outline, and wide (more than five-seriate) and high multiseriate rays (more than 10 mm) are diagnostic of Marcgraviaceae wood.
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; Bedell, 1980
). However, the wood of Pelliciera rhizophorae can be clearly distinguished from Tetrameristaceae by the presence of narrow multiseriate rays. Besides this, Pelliciera shows a significantly lower vessel diameter and vessel element length and a higher vessel density. The difference in vessel diameter and vessel density in Pelliciera can be explained by the high xylem tensions in mangrove trees due to the physiological dry (saline) environment. Indeed, the mangrove environment often results in a high number of narrow vessels, which increase the safety of the sap stream (Tomlinson, 1986
). The shorter vessel elements in Pelliciera might have the same effect (Carlquist, 1977
), although Panshin (1932)
and van Vliet (1976)
noticed that the vessel element length of mangrove species does not differ significantly from inland representatives in various families. In conclusion, we think that it is justified to accept the enlarged family concept of Tetrameristaceae with inclusion of Pelliciera, as has already been proposed by Bremer et al. (2002)
and APG II (2003)
.
Phylogenetic and ecological wood anatomy of Marcgraviaceae
The wood structure of Marcgraviaceae shows various features that are typical of lianas, such as wide vessel elements in co-occurrence with narrow vessels (vessel dimorphism), simple vessel perforations, paratracheal parenchyma and interspersed apotracheal parenchyma, and wide rays (Carlquist, 1989
). However, true tracheids or vasicentric tracheids, which are also common in lianas, were not observed. Although Marcgraviaceae are wood anatomically homogeneous, there is considerable variation in the width of the multiseriate rays. Mature wood of Marcgravia is often characterized by wide multiseriate rays (usually 5–15-seriate, sometimes up to 42-seriate), while most species of Noranteoideae have narrower (2–5-seriate) multiseriate rays. This difference remains when Marcgravia species, which grow exclusively as lianas, are compared with the other scandent species that characteristically show a more self-supporting, scrambling habit (on average nine-seriate vs. three-seriate, respectively). Therefore, the difference in multiseriate ray width caused by dissimilar growth strategies is phylogenetically important within the family, and it may represent an additional feature to distinguish Marcgravioideae from Noranteoideae, besides other features such as the specific umbellate inflorescence, the tetramery in the perianth, and the occurrence of leaf dimorphism in Marcgravia (Dressler, 2004
). Other ericalean taxa with very wide rays (more than 20-seriate) include the unrelated epacrids (Ericaceae) and primuloids (Theophrastaceae and Myrsinaceae), although lianas are mostly absent in these groups (Lens et al., 2003
, 2005
).
As mentioned in previous studies, altitudinal ranges may influence the wood structure, although altitudinal trends are less pronounced than latitudinal trends (Van der Graaff and Baas, 1974
; van den Oever et al., 1981
; Baas, 1986b
; Carlquist, 2001
; Lens et al., 2004
). Within Marcgraviaceae, the most manifest differences between the 16 species representing lowland climbers and the four montane climbing species are the multiseriate ray width (seven-seriate vs. three-seriate, respectively) and height (6330 vs. 3990 µm, respectively) (Table 4). The two erect species from the lowlands differ from the three montane erect species in having a lower percentage of scalariform perforations (5% vs. 35%, respectively), larger vessel diameters (160 vs. 100 m, respectively), a lower vessel density (7 vs. 14, respectively), longer vessel elements (1005 vs. 705 µm, respectively) and fibers (1345 vs. 1010 µm, respectively), and higher multiseriate rays (2630 vs. 2090 µm, respectively). These trends are in agreement with general altitudinal trends reported by the above authors, although none of these trends are significant at the 0.5% level.
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; Carlquist, 2001
; Lens et al., 2004
). The mean vessel diameter between climbers and erect species from the montane regions demonstrates the clearest habit trend in our analysis because the values are statistically significant at the 0.5% level (205 vs. 100 µm, respectively; Table 4). Several other trends can be mentioned, such as the higher percentage of scalariform perforations and a higher vessel density in montane erect species compared to montane climbers. Furthermore, climbing species from both lowland and montane regions have higher multiseriate rays than their erect counterparts (Table 4). The data on perforation types explain why scalariform perforations are more common in the Norantea s.l. complex because of the abundant occurrence of montane shrubs and treelets among this group (Vestal, 1937
; Metcalfe and Chalk, 1950
). The impact of habit on the vessel element and fiber lengths is somewhat contradicting (see also Carlquist, 1989
). Indeed, montane climbers have longer vessel elements and fibers than montane erect species, but lowland climbers show shorter mean vessel elements and fibers than lowland erect species.
Secondary woodiness in Balsaminaceae
From a wood anatomical point of view, the systematic position of Balsaminaceae is difficult to compare with other balsaminoid members because of the secondary woodiness of this family. Indeed, the few Impatiens species with a limited production of secondary xylem are scattered throughout the molecular tree of Yuan et al. (2004)
, indicating that this phenomenon has evolved multiple times from herbaceous ancestors. Two features that provide wood anatomical evidence for the occurrence of secondary woodiness are the raylessness in I. arguta and the presence of exclusively upright ray cells in I. niamniamensis (Carlquist, 1992
). Furthermore, the wood anatomical search for close relatives of Balsaminaceae is complicated more because of additional paedomorphic features, a term indicating that primitive features from the primary xylem are transferred into the secondary xylem (Carlquist, 1962
). The most important evidence for paedomorphism within the two species studied is the gradual decrease of vessel element length from the center of the stem towards the cambium. Indeed, vessel elements in the primary xylem are clearly longer (280–330 µm in I. arguta, 380–450 µm in I. niamniamensis) than vessel elements that are situated near the cambium (130–170 µm in I. arguta, 170– 220 µm in I. niamniamensis). Other paedomorphic features include wide scalariform to reticulate vessel pits, and thin-walled libriform fibers that are relatively wide. Furthermore, I. niamniamensis shows abundant axial parenchyma and wide and high rays, two features that are common in paedomorphic woods (Carlquist, 1962
).
As seen in tangential sections of I. niamniamensis, the shape and size of the ray cells corresponds fairly well with the libriform fibers (Fig. 4). In I. arguta, the difference between ray cells and libriform fibers is vague, resulting in raylessness. This is in agreement with the hypothesis of Carlquist (1970)
stating that the increase of xylem production in woody herbs with very short fusiform cambium initials may lead to libriform fibers that are histologically equivalent to ray cells.
Our observations of I. niamniamensis resemble the wood of I. lyallii, which also shows a high percentage of parenchyma tissue (Gerard, 1917
). Nevertheless, major differences in I. lyallii are the presence of narrow (1–2-seriate) and low (200– 300 µm) rays, and extremely short fibers (150–250 µm). Because raphides are occasionally observed in the wood of I. niamniamensis, this character remains the only anatomical– morphological link between Balsaminaceae and the other three balsaminoid families. Besides this observation, Balsaminaceae characteristically show raphides within special cells of the leaves, cortex, and in the anther walls (Cronquist, 1988
; Fischer, 2004
).
FOOTNOTES
1 The authors thank the directors of the Botanic Garden and Botanic Museum Berlin-Dahlem (B), National Botanic Garden of Belgium (BR), Forschungsinstitut Senckenberg (FR), Missouri Botanical Garden (MO), New York Botanical Garden (NY), Swedish Museum of National History (S), the directors of the xylaria of Madison (MADw), Tervuren (Tw), Utrecht (Uw), and Washington (USw), and Dr. Yuan (University of Neufchâtel, Switzerland) for their supply of wood samples. We also thank Anja Vandeperre (K.U.Leuven) for technical assistance and Marcel Verhaegen (National Botanic Garden of Belgium) for preparing SEM images. This work has financially been supported by research grants from the K.U.Leuven (OT/01/25) and the Fund for Scientific Research–Flanders (Belgium) (G.0104.01, 1.5.069.02, 1.5.061.03, G.0268.04). Steven Jansen was 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.ac.be
)
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