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Anatomy and Morphology |
UA Museum of the North Herbarium, Department of Biology and Wildlife, and Institute of Arctic Biology, University of Alaska Fairbanks, 907 Yukon Drive, Fairbanks, Alaska 99775-6590 USA; School of Life Sciences, Box 874501, Arizona State University, Tempe, Arizona 85287-4501 USA; Department of Botany, MRC-166, Smithsonian Institution, P.O. Box 37012, Washington, D.C. 20013-7012 USA; Laboratory of Systematic and Evolutionary Botany & Herbarium, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
Received for publication July 9, 2006. Accepted for publication May 21, 2007.
ABSTRACT
Altingia (Altingiaceae) is a tropical to subtropical Asian genus of lowland trees for which 5–15 species have been recognized. Morphological diversity, particularly of the mature infructescence, has been poorly known, especially for species with relatively localized and narrow distributions, and our understanding of Altingia has lagged behind that of its close temperate relative Liquidambar (sweet gum). In this contribution, mature infructescence structure, at the levels of anatomy, morphology, and micromorphology, and some distinctive inflorescence features, are described for five recognized species of Altingia, some for the first time. In the phylogenetic framework of both morphology and molecules, characters of Altingia contrast with those of Liquidambar and suggest that character evolution within Altingiaceae is at least partly related to geographic and climatic distribution. Differences in rates of evolution and morphological convergence suggest complex patterns of diversification in Altingiaceae at several different phylogenetic levels: (1) at the deep nodes, characters of the stem lineage fossil Microaltingia persist into crown group Altingiaceae, morphological stasis; (2) at the generic level, convergence within both Liquidambar and Altingia toward their respective habitats; (3) at the infrageneric level, morphological divergence in species diversification within Altingia, in response to diverse habitats of the eastern Asian subtropics; and (4) within the intercontinental disjunct species pair L. orientalis–L. styraciflua, morphological stasis.
Key Words: Altingia • Altingiaceae • biogeography • infructescence • morphological stasis
The genus Altingia Noronha (Altingiaceae) has been reported to consist of about 5–15 species occurring in tropical to subtropical regions of Asia. Two sections have been recognized traditionally: section Oligocarpa, including A. gracilipes Hemsl. and A. siamensis Craib; and section Altingia, including A. chinensis Oliver ex Hance, A. obovata Merrill & Chun, A. yunnanensis Rehder & Wilson, A. poilanei Tardieu-Blot, and A. excelsa Noronha (Chang, 1979
; Ferguson, 1989
). We recognize five of these species in the present study: A. gracilipes, A. siamensis Craib, A. chinensis, A. excelsa, and A. poilanei (Table 1), (Ickert-Bond et al., 2005
). Several additional species that have been included within section Altingia by Chang (1979)
are not treated here because they are poorly known, and their taxonomic status needs to be critically evaluated.
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). Altingia chinensis occurs widely in China and is closely allied with specimens designated as A. yunnanensis from Yunnan, China, and southern Vietnam (Ferguson, 1989
). In this report we consider A. yunnanensis to be synonymous with A. chinensis (Table 1). Altingia gracilipes occurs in Fujian, Hong Kong, Hainan, Guangdong, Jiangxi, and Zhejiang provinces and is highly distinct from the A. chinensis–A. yunnanensis complex in having fewer fruits and a cup-like bract that subtends each infructescence (Zhang et al., 2003
).
Other species described after these initial four taxa include Altingia siamensis Craib, A. obovata, A. angustifolia H.-T. Chang, A. indochinensis H.-T. Chang, A. multinervis Cheng, and A. tenuifolia Chun ex H.-T. Chang. We recognize A. siamensis as a widespread species extending from northern Thailand, Cambodia, Laos and Vietnam, into eastern Guangdong, and southern Yunnan (Craib, 1928
). Altingia obovata was described from the Hainan Island of southern China (Merrill and Chun, 1935
) and was distinguished from populations of A. chinensis on the mainland by its obovate, rather than the typically ovate-to-elliptic, leaves. Because this character is polymorphic throughout populations of A. chinensis (Ferguson, 1989
; S. Ickert-Bond, personal observation), we consider A. obovata as a synonym of A. chinensis.
None of the three species described by Hong-Ta Chang in the 1960s, A. angustifolia from Guangdong province, A. indochinensis from Vietnam, or A. tenuifolia from Guizhou province, is recognized in the present study. Altingia angustifolia is here treated as a synonym of A. siamensis (Zhang et al., 2003
). Altingia indochinensis is a doubtful name and is taxonomically problematic without a confirmed locality, and we consider A. tenuifolia to be a synonym of A. gracilipes (S. Ickert-Bond and J. Wen, unpublished data). We recognize A. poilanei, a species with distinctive, broadly ovate leaves and elongate infructescences, known only from its type locality in northern Vietnam (Tardieu-Blot, 1965
). Altingia multinervis was recognized from a single type specimen (Cheng, 1947
). The first author examined an apparent isotype (Tsoong 256) at the Herbarium of Zhongshan (Sun Yatsen) University (SYS), which consists only of two sterile leaves (S. Ickert-Bond, personal observation). We recently obtained digital images of the holotype from the Herbarium at Nanjing University (N). This specimen includes branches as well as two badly degraded and incomplete infructescences. The lack of information, particularly about fertile remains of A. multinervis, prevents further consideration of this material at present. Variation seen in leaf morphology is consistent with that found in A. chinensis.
While Altingia is tropical–subtropical in distribution, its sister taxon, Liquidambar L., the sweet gum, is a mostly temperate taxon (Shi et al., 1998
; Wen, 1998
, 1999
, 2001
). The third genus within Altingiaceae, Semiliquidambar H.-T. Chang (Chang, 1962
) has been hypothesized to have originated via intergeneric hybridization between Altingia and Liquidambar (Bogle, 1986
; Ickert-Bond et al., 2005
). This genus is restricted to subtropical and tropical Asia, especially in southern China, and is currently under study. As with Liquidambar, taxonomic delimitation of Altingia has been based largely on leaf and inflorescence morphology, and until recently, details of mature infructescences of either genus were not clearly known (Ickert-Bond et al., 2005
). This situation has been even more problematic for Altingia because of the difficulty in obtaining material for most taxa, and a revision is in order (Endress, 1993
).
As part of our broader analysis of the family Altingiaceae, we have described the silicified Miocene infructescence Liquidambar changii Pigg, Ickert-Bond and Wen (Pigg et al., 2004
), completed a comparative study of mature infructescences of extant Liquidambar (Ickert-Bond et al., 2005
), and investigated the complexity of the biogeographic history of the family using molecular markers (Ickert-Bond and Wen, 2006
). It is clear that this family has an ancient origin, with earliest evidence of the stem lineage of Altingiaceae in the Late Cretaceous (Microaltingia Zhou, Crepet and Nixon; Zhou et al., 2001
; Hermsen et al., 2006
) and diversification throughout the Tertiary (Ferguson, 1989
; Pigg et al., 2004
). In this contribution we expand the morphological studies of Altingiaceae to include the genus Altingia and to document the diversity therein. The discrepancy between morphological and molecular rates of evolution reported in our earlier studies (Ickert-Bond et al., 2005
; Ickert-Bond and Wen, 2006
) is further considered to examine the patterns of character evolution and diversification within Altingiaceae in the context of geographic and climatic distribution.
MATERIALS AND METHODS
Material for study was obtained from field collections and from herbarium specimens (Table 2, Appendix); material was photographed for general features. Measurements given are the mean of 10 individuals (Table 3). Some specimens were hand-sectioned with a razor blade for general features, and examples from all species were prepared for serial section using standard histological techniques that included embedding in Paraplast Plus Tissue Embedding Medium (Monoject Scientific, Sherwood Medical, St. Louis, Missouri, USA), sectioning on a rotary microtome at 20 µm thick, and staining with standard histological stains (Johansen, 1940
). Mature, woody infructescences were softened with ethylene diamine prior to embedding (Carlquist, 1982
). For anatomical studies, dry seeds were rehydrated for 7 d in equal parts of glycerol, water, and ethanol and then sectioned by hand (Lobova et al., 2003
). Seeds and dissected carpels were mounted on stubs for scanning electron microscopy (SEM), sputter-coated with 200 Å of gold, and scanned with an Amray 1400 and an Amray 1810 SEM (KLA Tencor, Amray Division, Bedford Massachusetts, USA). Terminology follows that of Bogle (1986)
, Endress (1989a)
, and Ickert-Bond et al. (2005)
. Interpretation of infructescence structure in Altingiaceae was discussed in Ickert-Bond et al. (2005)
.
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), and the middle Miocene L. changii Pigg, Ickert-Bond & Wen from western North America (Pigg et al., 2004
). Outgroup selection, (Exbucklandia and Hamamelis) follows that of our previous analysis (Ickert-Bond et al., 2005
). Semiliquidambar was excluded from the analysis because of hypotheses that it originated through intergeneric hybridization (Bogle, 1986
; Ferguson, 1989
; Ickert-Bond et al., 2005
). The Eocene fossil genus Steinhauera Presl (Mai, 1968
; Pigg et al., 2004
) was excluded because it is poorly understood and needs to be reevaluated.
We emphasized reproductive structures and expanded the data matrix used by Ickert-Bond et al. (2005)
. Forty-nine characters were selected on the basis of interspecific variations among the sampled taxa (Table 4). They consisted of 41 binary and seven multistate characters. All multistate characters were treated as unordered. Quantitative characters were coded following simple gap coding (Archie, 1985
). Data were mainly derived from our own observations and partly from the literature, as cited under Materials and Methods in Ickert-Bond et al. (2005)
. We added seven characters to the annotated list of all characters from our earlier analysis (Table 2 in Ickert-Bond et al., 2005
). These additional characters were character 15: pollen, (0) tricolpate, (1) polyporate; character 26: outer fruit wall, (0) little differentiation, (1) well differentiated; character 27: distribution of resin canals and fiber bundle formation in outer fruit wall, (0) dispersed throughout, (1) predominantly in outer infructescence fruit wall with arclike fiber bundles; character 33: dehiscence pattern, (0) septicidal and loculicidal, (1) septicidal and ventricidal, (2) septicidal, ventricidal, and loculicidal; character 35: infructescence shape, (0) globose, (1) compressed globose; character 40: peduncle L : W ratio, (0) less than 15 : 1, (1) 16–25 : 1, (2) >26 : 1, and character 46: seed coat anatomy, (0) mesotestal, (1) exotegmic. The current morphological matrix is presented in Table 4. Parsimony analysis was performed using a branch-and-bound search with MULPARS and furthest addition sequence options in PAUP* (version 4.0b10; Swofford, 2002
). Character states were coded as unordered, and all characters were weighted equally. The amount of support for monophyletic groups revealed in the most parsimonious tree(s) (MPTs) was examined with 100 bootstrap replicates (Felsenstein, 1985
) with the random addition and the heuristic search options.
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). We have excluded sampling of Semiliquidambar because of its putative hybrid origin, as suggested by several authors (Bogle, 1986
; Ferguson, 1989
; Ickert-Bond et al., 2005
). Our molecular sampling in the current study is comparable to that used in the morphological data set (Table 2). Maximum parsimony was used to reconstruct phylogenetic relationships using heuristic search methods and addition sequence options as outlined in Ickert-Bond and Wen (2006)
. A strict consensus tree was generated, and the support of individual clades was estimated with the bootstrap method (Felsenstein, 1985
). Bootstrap proportions (BP) were obtained from 2000 replicates of heuristic searches (1000 random addition sequences, tree-bisection-reconnection [TBR] branch swapping, and MulTrees selected). RESULTS
Morphological description—general features of Altingia in comparison with Liquidambar (Figs. 1–25)
In contrast to Liquidambar's typically spherical inflorescences, those of Altingia are spherical to occasionally elongate. Both develop into persistent, woody infructescences (Figs. 1, 3). They are composed of closely spaced, multiple (
6–35) bicarpellate fruits helically arranged around a central axis that extends into an elongate peduncle. Although infructescences are generally considered to be unisexual, it is not unusual to find a few, often presumably functional stamens, clustered within the infructescence heads in both genera (Fig. 6). While extrafloral structures of Liquidambar can be spine-like, those of Altingia are typically mammilate or knoblike (Fig. 11). Two species, A. gracilipes and A. siamensis, have a cuplike bract at the base of the infructescence (Figs. 3, 45, 65). Styles on inflorescences are short and recurved with broad stigmatic surfaces (Fig. 6). Stigmas are typically persistent in Liquidambar (Figs. 2, 7, 12) but are lacking in Altingia. However, style bases typically become sclerified, and these short, knob-like bases can occasionally be found on mature infructescences (Fig. 11). Altingia infructescences are similar to those of L. acalycina but differ from those of other species of Liquidambar in having a thicker and more differentiated fruit wall (Fig. 10) and more loosely attached fruits, with the infructescence disaggregating when sectioned (Figs. 8–9).
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Fruits of Altingia and Liquidambar are anatomically similar, although there are several differences. The outer zone of the entire infructescence (of all the fruit walls collectively) is typically thicker and more highly differentiated in Altingia than in Liquidambar. While both genera have a region of tangentially elongate fibers in the outer fruit walls, this zone is more prominent in Altingia (Figs. 21, 22). To the periphery of this zone, the fruit walls in Altingia have several layers not typically present in Liquidambar. The first zone has numerous veins, which are each associated with resin canals and fiber bundles (Fig. 21). Next is a zone of cuboidal parenchyma cells about 8–10 cells thick, which are sparsely interspersed with resin canals. Within this region are shorter cells that appear to be tangentially divided and may have limited cambial activity (Fig. 21). To the outside is a region 3–4 cells thick of more elongate cells, typically filled with dark, tanniferous contents. The epidermis is uniseriate and is made up of palisade cells (Figs. 10, 21).
In contrast, the entire infructescence of Liquidambar is parenchymatous. Rather than producing a thick, compact infructescence with thickened peripheral fruit walls and only small remnants of style bases left behind as in Altingia, a larger proportion of tissue is committed to the extrafloral structures between adjacent fruits, which appear as elongate processes (Fig. 22). Only in the outermost boundary of the ground tissue are there regions with dark, tanniferous cells (Fig. 22). Differences are also evident within individual fruits; those of Altingia have more elaborate structure to the ventral margins where the carpels of each bicarpellate fruit are fused (Figs. 21, 23–25).
Altingia chinensis (Figs. 26–34)
Infructescences are subglobose (Figs. 26, 28) and 18.04–24.94 (
= 21.79) mm high x 22.41–27.15 ( = 25.30) mm wide, with a length : width (L : W) ratio ranging from 0.75–1.00 : 1 ( = 0.86 : 1). Peduncles are 32.14–58.05 ( = 43.29) mm long x 1.32–2.30 ( = 1.69) mm wide (Fig. 26). Each inflorescence or infructescence is made up of 16–18 ( = 17.50) individual bicarpellate fruits (Figs. 26–29). Within mature inflorescences, styles are relatively short (up to 3 mm long), fairly thick, and strongly recurved (Fig. 27). Styles are deciduous and represented on mature infructescences only by slightly bumpy style bases where they were attached (Fig. 29). Individual fruits are 6.73–9.23 ( = 7.88) mm long x 2.73–4.61 ( = 3.44) mm wide (Fig. 29).
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25–30 cells thick (Figs. 31, 33) and an inner, uniseriate palisade layer of macrosclereids (Figs. 30, 32). Individual rectangular cells of the palisade layer are vertically elongate and have somewhat unevenly thickened cell walls (Fig. 30). The outer fruit wall is parenchymatous with cells that are isodiametric to slightly elongated tangentially and appearing stretched, vascular bundles with prominent fibers and separate fiber bundles, and numerous, well-defined resin canals up to 8 µm in diameter (Fig. 34). Fiber bundles, as seen in transverse section, are rectangular and tangentially elongate, 10 cells thick x 30 cells wide. Seeds are 4.43–5.67 ( = 5.16) mm long x 2.27–3.27 ( = 2.92) mm wide (L : W ratio = 1.77 : 1) with a circular flange surrounding the central body.
Distinctive features of this species include medium-sized infructescences containing numerous fruits ( = 15) borne on very long and thick peduncles, a sclerenchymatous, uniseriate, palisade inner fruit wall with relatively elongate cells, and relatively short, thick, and strongly recurved styles in pistillate flowers.
Altingia excelsa (Figs. 35–44)
Infructescences are compressed-globose and 13.94–16.55 ( = 15.73) mm high x 15.65–22.22 ( = 19.03) mm wide with a length : width (L : W) ratio ranging from 0.65–1.02 : 1 ( = 0.84 : 1) (Fig. 35, 37–38). Peduncles are 22.05–38.47 ( = 29.35) mm long x 0.75–1.70 ( = 1.36) mm wide. Each inflorescence or infructescence is made up of 9–25 ( = 15) individual bicarpellate fruits. Pistillate flowers have straight, thick styles, and the entire infructescence is subtended by hyaline bracts (Fig. 36). Remnants of the style bases are still present on many fruits (Fig. 37).
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= 5.53) mm long x 2.86–3.31 ( = 3.19) mm wide (L : W ratio = 1.73 : 1).
Distinctive features of this species include compressed globose infructescences borne on relatively long and thin peduncles; a uniseriate, palisade inner fruit wall with almost cuboidal cell shape and highly unevenly, thickened walls; as well as a medium number of fruits ( = 15) per infructescence. Pistillate flowers have almost straight styles, and the inflorescences are subtended by hyaline bracts.
Altingia gracilipes (Figs. 45–54)
Infructescences are obconical and 9.56–13.44 ( = 11.96) mm high x 11.86–16.90 ( = 14.67) mm wide with a length : width (L : W) ratio ranging from 0.74–0.91 : 1 ( = 0.82 : 1) (Figs. 45, 46). Peduncles are 14.93–28.18 ( = 22.26) mm long x 0.85–1.24 ( = 1.04) mm wide (Fig. 45). Each inflorescence or infructescence is made up of 5–6 ( = 5.78) individual bicarpellate fruits (Figs. 48, 49). A distinctive, cuplike bract subtends each infructescence (Fig. 45). Style bases appear as small, beaklike structures on slightly raised circular platforms (Fig. 46).
Fruits are 7.15 mm long x 3.48 mm wide and elongate (Fig. 47). The fruit wall is composed of an inner sclerenchymatous palisade layer 1–2 cells thick (Figs. 50, 53, 54) and a three-zoned outer region (Figs. 48, 52). Cells of the palisade layer are vertically elongate and 5–6 sided. Where the ventral margins of the adjacent carpels of the fruit meet, the region of the fruit wall immediately to the outside of the palisade layer is composed of a dark, fibrous tissue. This darker tissue extends around and encircles the palisade layer as extensions of the septum (Figs. 50, 53). The outer fruit wall contains an inner zone with small vascular bundles that are associated with small fiber bundles and abundant resin canals (Figs. 50, 53). This zone is surrounded by tangentially elongate, fibrous cells that encircle the inner area of the fruit (Fig. 48, 52). The outer fruit wall is composed of numerous, larger vascular bundles, fiber bundles, resin canals, and 4–5 rows of slightly radially elongate cells with dark contents. (Figs. 51, 52). The epidermis is uniseriate. Seeds are 3.00–6.05 ( = 4.26) mm long x 1.67–3.08 ( = 2.28) mm wide (L : W ratio = 1.90 : 1) and have a light brown halo at the edge of the circular flange that surrounds the central seed body.
Distinctive features of this species include the leafy cuplike bract subtending each infructescence (Fig. 45), obconical infructescence shape, small number of bicarpellate fruits, and well-differentiated outer fruit wall (Figs. 48, 52).
Altingia poilanei (Figs. 55–64)
Infructescences are turbinate (Figs. 55, 56) and 21.91–30.98 ( = 26.94) mm high x 21.47–26.80 ( = 23.87) mm wide, with a length : width (L : W) ratio ranging from 0.59–0.79:1 ( = 1.124 : 1). Peduncles are 20.26–31.49 ( = 24.23) mm long x 0.93–1.20 : 1 ( = 1.08) mm wide. Each infructescence is generally made up of 25 individual bicarpellate fruits (Figs. 56, 59, 60), although triloculate carpels were also observed (Fig. 57).
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= 6.50) mm long x 2.84–4.05 ( = 3.53) mm wide (L : W ratio = 1.86 : 1).
Distinctive features of this species include turbinate infructescence shape, large size, numerous fruits per infructescence ( = 25), fibers with large lumina in the fruit tissue, and a lobed outer fruit wall with lenticel-like structures in the epidermis.
Altingia siamensis (Figs. 65–75)
Infructescences are compressed globose and 8.70–13.48 ( = 11.27) mm high x 11.70–21.65 ( = 15.81) mm wide, with a length : width (L : W) ratio ranging from 0.59–0.79 : 1 ( = 0.71 : 1) (Figs. 65, 66). Peduncles are 20.26–31.49 ( = 24.23) mm long x 0.93–1.20 ( = 1.08) mm wide (Fig. 65). Each inflorescence or infructescence is made up of 6–7 individual bicarpellate fruits (Figs. 66–68, 71). A cuplike bract, similar to that of A. gracilipes but less well developed, subtends each infructescence (Fig. 65). Carpels bear short, stout, recurved styles with broad, elongate stigmatic areas (Fig. 69, 70).
The carpel wall is composed of an inner sclerenchymatous palisade layer one-to-several cells thick and an outer fruit wall that appears relatively thin compared to that of other Altingia species (Fig. 72). Resin canals, somewhat flattened tangentially, are associated with distinctive arclike fiber bundles (Figs. 72, 73, 75). Both resin canals and arclike fiber bundles are more pronounced in the outer fruit wall. The palisade layer is composed of very thin, vertically elongate sclerenchymatous cells with uniformly thin walls (Fig. 74). Seeds are 4.04–6.75 ( = 5.37) mm long x 2.0.7–3.53 ( = 2.68) mm wide (L : W ratio = 2.00 : 1).
Distinctive features of this species include small, compressed, globose infructescences subtended by a cuplike bract (Fig. 65), few fruits per infructescence ( = 6), and numerous resin canals throughout the outer fruit tissues, each associated with an arclike fiber bundle cap (Figs. 72, 73).
Seed morphology and anatomy (Figs. 76–85)
While a large number of anatropous ovules are borne on the ventral margin of each carpel in Altingia, only a few typically mature into seeds. As in Liquidambar, viable seeds tend to be produced near the infructescence axis. Mature seeds in Altingia are broadly ovate with a circular flange (Figs. 76, 78) and 5–9 mm long x 2.5–4 mm wide (Table 3). They are typically speckled or striped, but none of this variation is species specific (Fig. 4). Seed surface micromorphology is fairly homogenous. Cells are arranged parallel to the long axis of the seed and are more or less polygonal (Figs. 79–81). The seed coat has five tissue layers based on differing cell types (Figs. 82–85), with the outermost layer a uniseriate epidermis (Fig. 83, 85). Beneath the epidermis is a hypodermal zone 1–2 cells thick of parenchyma containing calcium oxalate crystals (Figs. 83, 85), followed by a third layer 2–3 cells thick of thin, tangentially elongate, crushed parenchyma (Fig. 84). To the inside is a fourth zone 2–3 cells thick, which is the mechanical layer and is composed of macrosclereids (Figs. 84, 85). To the inside of this layer is a fifth zone of often crushed, tangentially elongate cells 1–2 cells thick that may represent the nucellus (Fig. 84).
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Phylogenetic analysis based on molecular data
Analysis of the combined cpDNA data revealed three MPTs of 719 steps with a CI = 0.98 and a RI = 0.92. The strict consensus tree when rooted with Hamamelis virginiana shows a strongly supported monophyletic Altingiaceae (Fig. 87; BP = 100%). Furthermore, three distinct clades are highly supported: (1) a L. styraciflua and L. orientalis clade (BP = 100 %); (2) a clade of two species from China and North Vietnam, A. chinensis and A. poilanei (BP = 97 %); and (3) a clade containing the remaining taxa. Within this larger well-supported clade (BP = 91%), a clade of A. excelsa from Indonesia to southern China and A. siamensis from Indochina diverges at the base, sister to a highly supported clade (BP = 96%) composed of A. gracilipes, L. formosana, and L. acalycina.
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Infrageneric variation in Altingia
Species of Altingia are all of similar morphologic construction. The major distinguishing characters are infructescence size, shape and fruit number. Another distinctive feature is the presence or absence of a cuplike bract subtending the infructescence and its size. Hyaline bracts also occur at least in some species but are only rarely found, probably because of their ephemeral nature and early deciduousness. Other characters that are variable and of potential taxonomic value include: structure of ventral carpel walls in fruits, details of outer fruit wall, distribution and shape of fiber bundles, and number and distribution of resin canals.
Infructescence size and shape, fruit number, and details of axis in Altingia
The number of fruits per infructescence is correlated with the size of the infructescence and equates to roughly one fruit per millimeter of axis length. The largest infructescence (A. poilanei, = 27 mm long) also has the largest number of fruits ( = 25), those of intermediate size have fewer fruits (A. chinensis, = 18 mm, = 18 fruits; A. excelsa, = 16 mm, = 15 fruits), and the smallest infructescences A. gracilipes ( = 11 mm) and A. siamensis (12 mm) have very few fruits (six each) (Table 3) (Ferguson, 2002
). The shape of infructescences in Altingia ranges from globose (A. chinensis), to obconical (A. gracilipes and A. siamensis), to slightly elongate to turbinate (A. poilanei). The infructescences of both A. gracilipes, and to a lesser extent A. siamensis, are subtended by a cuplike bract (Figs. 3, 45, 65).
Peduncle length varies from very long in A. chinensis (43 mm) to long in A. excelsa (29 mm), while the shortest are in A. poilanei, A. siamensis (both 24 mm), and A. gracilipes (22 mm). Peduncle width is not consistently correlated with length, as previously noted by Ferguson (1989)
. While A. chinensis, which has the longest peduncles (43 mm), also has one of the thickest (1.7 mm wide); the relatively short peduncles of A. poilanei (24 mm) are also thick (1.8 mm). The shortest peduncles, on A. siamensis (24 mm long) and A. gracilipes (22 mm long), are also the thinnest (1.1 mm and 1.0 mm wide, respectively).
Infructescence anatomy in Altingia
Additional differences between species of Altingia are based on variation in the anatomy of the infructescence ground tissue, including details of inner carpel wall and outer fruit tissues. Inner palisade carpel walls of most species of Altingia are uniseriate, but in A. siamensis this region may be up to four cells thick (Fig. 74). The palisade cells of the inner carpel wall vary among the taxa in shape and wall thickness from cuboidal and thick walled (A. excelsa), to somewhat radially elongate and thick walled (A. chinensis, A. gracilipes, A. poilanei), to elongate with quite thin walls (A. siamensis). Wall thickness can also vary within a cell.
In the outer fruit wall, the distribution and shape of fiber bundles and resin canals can vary. All species contain these elements, but resin canals are considerably larger and more numerous in the outer fruit walls in A. siamensis than in other species (Figs. 72, 73). In addition, the resin canals of A. siamensis are associated with arclike fiber bundles (Fig. 73), whereas other species have less well-defined bundles with fewer fibers. Fruits all have outer fruit walls with tangential fiber zones, but this feature is particularly well developed in A. gracilipes (Figs. 10, 52). All fruits have a uniseriate epidermis; however, in A. poilanei the outermost fruit wall has lenticel-like structures that presumably develop from periclinal divisions of the outer ground tissue (Fig. 63).
Infrafamiliar variation: fruit dehiscence in Altingiaceae
An important taxonomic character that has been used to separate genera within Altingiaceae is variation in dehiscence type (Ferguson, 1989
; Zhang et al., 2003
). However, two problems have been inherent in using dehiscence as a taxonomic character: (1) differences in terminology used (Table 5), and (2) problems in understanding the process.
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), while Liquidambar and Semiliquidambar are described as septicidal (Table 5) (Ferguson, 1989
). These authors are identifying the septum of septicidal dehiscence as the area created by the fused ventral margins of the two carpels that make up the bicarpellate fruit. Loculicidal in this case refers to the splitting of each carpel at right angles to the septum (in the center). In contrast, Endress (1989a)
described dehiscence in Liquidambar as septicidal and ventricidal. Endress thus uses the term septicidal in the same sense as the previous authors but refers to the separation of the ventral margins of each individual fruit as ventricidal rather than loculicidal. However, Endress follows Mai (1968)
in suggesting that Altingia and the fossil Steinhauera dehisce septicidally and loculicidally. Zhang et al. (2003)
use loculidicidal for Altingia and Liquidambar and also describe the resulting structure (Table 5).
To clear up this confusion, we look to the original definition of the terms. Winkler (1936)
defined dehiscence as septicidal if it occurs longitudinally along the juncture of adjacent carpels or loculicidal if it occurs along the plane of the median (central or dorsal) bundle of each carpel (Stopp, 1950
; Esau, 1965
). Ventricidal dehiscence occurs along the inner or ventral surfaces of a carpel, where its adjacent lateral arms meet (Stopp, 1950
). In this sense, we concur with Endress's use of ventricidal.
To better understand the actual process of dehiscence, we studied fruits and flowers of both Liquidambar and Altingia at several stages of development (Figs. 13–20). Dehiscence in Altingiaceae takes place via hygroscopic tension, which arises as each fruit wall dries out. Fruit walls tend also to break down tangentially, along planes of weakness, resulting in the common fractured appearance of fruits within the infructescence (Figs. 2, 26, 45, 56).
The fruit consists of two involute carpels (Bogle, 1986
) (Figs. 13–20). The inner edges of the involute portion of the ventral margins of each carpel are fused together, and the outer ventral margins of the two carpels composing the fruit are then fused to each other. (This entire structure produces the ventral septum sensu Bogle, 1986
.) Centrally within the fruit the involute margins are fused to themselves ventrally and to each other, separating the two locules from one another (Figs. 19, 20). Distally, the lateral margins of each of the carpels split ventricidally, resulting in a large, common locule (Fig. 18). More distally, the two carpels are also separated from one another (Figs. 15–18).
In fruits of Liquidambar and Semiliquidambar, the long, persistent styles not only obscure the view of the fruit openings but also help to maintain its structural integrity. Fruits of Altingia have only small remnants of style bases. Because Altingia fruits lack prominent styles, dehiscence is more pronounced, allowing the splitting of the bilocular fruits into four valves upon maturity as an additional loculicidal split does occur along the dorsal side of the carpel (Fig. 16). In Liquidambar and Semiliquidambar, the outer fruit wall is relatively thin, while in Altingia the wall is considerably thicker and more highly differentiated. In all altingioids, however, the drying that causes dehiscence also causes splitting of the fruit walls, allowing additional "room" for the fruits to open. As fruits mature and become desiccated, numerous fractures form throughout the ground tissues of the outer fruit walls.
A uniform terminology for dehiscence and a clearer understanding of the process are both essential to the value of this feature as a taxonomic character. Consistent terminology is also important when evaluating homologies and tracking character evolution within the group as a whole (Hermsen et al., 2006
). Nowhere is it more important than in the study of the fossil record. In particular, the Eocene genus Steinhauera has been compared both to Liquidambar and Altingia (Kirchheimer, 1943
, 1957
; Mai, 1968
). Mai (1968)
contended that Steinhauera's lack of persistent styles and possession of a fibrous axis demonstrated its closer relationship to Altingia, a genus that he suggested as basal within the family. This hypothesis has not been tested, and a reassessment of the numerous specimens of Steinhauera is needed. We do know, however, from our study of Miocene fossils that fruit weathering in extant Liquidambar can result in infructescences that look superficially like those of Altingia (Pigg et al., 2004
). We are currently evaluating fossil Altingiaceae in this context.
Seed surface micromorphology in Altingiaceae
Seed surface micromorphology in Altingia is relatively homogenous with cells arranged parallel to the long axis of the seed (Figs. 76–81). In all species of Altingia and in L. acalycina, the surface of the seed coat is composed of polygonal cells (Figs. 79–81), while the other three species of Liquidambar have tangentially elongate and rectangular cells (Ickert-Bond et al., 2005
). It is interesting to note that seeds of Altingia and L. acalycina have ovate seeds with a circular flange, while seeds of the other three species of Liquidambar have elongate seeds with a distal wing. Thus, epidermal cell pattern on seeds tend to correlate with seed shape in Altingiaceae.
Significance of seed anatomy in Altingiaceae
As with dehiscence, there have been difficulties in understanding the seed anatomy of Altingiaceae. Much of the difficulties arise because classification of seed anatomy is based on the developmental origin of the most mechanically prominent, usually sclerified, layer of the seed coat, and these relationships are not always obvious in mature seeds (Corner, 1976
; Boesewinkel and Bouman, 1984
; Schmid, 1986). Because most angiosperms are bitegmic, either the inner or outer integument provides the major mechanical layers of the seed coat. Seed coats developed primarily from the outer integument (testa) are termed testal, while those mostly from the inner integument (tegmen) are termed tegmic. The given region of the integument involved is included (e.g., mesotestal, endotegmic) in this classification (Corner, 1976
).
Seed anatomy of Altingiaceae has been described by several authors (Netolitzky, 1926
; Melikian, 1971
, 1973
; Rao, 1974
; Takhtajan, 1996
; Zhang and Wen, 1996
). This feature has been interpreted variously as mesotestal (Corner, 1976
), endotestal (Doweld, 1998
), or exotegmic (Rao, 1974
). As the ovule of Altingiaceae develops, the outer integument has 2–3 cell layers and the inner integument has 3–4 layers (Endress and Igersheim, 1999
). In the mature seed, the outer integument of the ovule is represented by a layer only 2–5 cells thick. It is composed of the epidermis and a hypodermis with oxalate crystals (Figs. 9G–J in Ickert-Bond et al., 2005
) (Figs. 76–85). From our observations, we interpret the thin, crushed, tangentially elongate layer (immediately outside the embryo cavity) and the mechanically prominent macrosclereids to the inside of this thinner layer as being derived from the inner integument (Fig. 85). In this case, the seeds of Altingiaceae would thus be considered exotegmic, because the mechanical layer comes from the tegmen. The innermost layer of crushed, tangentially elongate cells immediately outside the embryo cavity are thought to represent the nucellus.
In contrast, seed coats of Hamamelidaceae s.s. have been described as mesotestal, with the mechanical tissue derived from the middle layer of outer integument (Corner, 1976
; Boesewinkel and Bouman, 1984
), or exo-mesotestal, with this layer derived from both the outer and middle layers of the outer integument (Doweld, 1998
). Developmentally, a mature hamamelid ovule has an outer integument 6–8 cells thick and an inner one of 2–3 cells (Endress and Igersheim, 1999
). In the mature seed, the outer seed coat is massive and up to 30 cells thick, with centrally positioned sclerotic tissue, and the inner layers are considerably thinner (Rao, 1974
; Zhang and Wen, 1996
). This type of seed is thus classified as mesotestal. (Boesewinkel and Bouman, 1984
; Schmidt, 1986
).
In summary, Altingiaceae seed coats differ from those of Hamamelidaceae because they are exotegmic with relatively little cell division occuring during development. In contrast, Hamamelidaceae seeds have a massive sclerotic testa derived from an initially thick outer integument with considerable cell division having occurred to produce this mesotestal seed coat (Zhang and Wen, 1996
). Thus seed coat, along with differences in pollen structure (Bogle and Philbrick, 1980
; Zavada and Dilcher, 1986
), wood anatomy (Sakala and Privé-Gill, 2004
), and several other features mentioned herein, reinforce the recognition of Altingiaceae as an independent family distinct from the closely related Hamamelidaceae (Endress, 1989b
; Ferguson, 1989
; Ickert-Bond and Wen, 2006
; Stevens, 2000 onward
).
Comparison between morphological and molecular phylogenies within Altingiaceae
Analyses based on several molecular markers suggest that Altingia is nested within Liquidambar (Fig. 87) (Shi et al., 1998
; Ickert-Bond et al., 2005
; Ickert-Bond and Wen, 2006
). Yet our morphological analysis strongly supports Altingia and Liquidambar as mutually exclusive sister clades (Fig. 86) (Ickert-Bond et al., 2005
). The Cretaceous fossil Microaltingia is supported as sister to the Altingiaceae within the stem lineage of Altingiaceae (Fig. 86) (Ickert-Bond and Wen, 2006
). Results in Hermsen et al. (2006)
place Microaltingia below a clade of Altingiaceae and place Cercidiphyllum L. slightly further from Altingiaceae, as originally proposed in Zhou et al. (2001)
. Liquidambar and Altingia are each defined by several morphological synapomorphies and have been maintained as separate genera in modern taxonomic treatments (Vink, 1957
; Tardieu-Blot, 1965
; Zhang et al., 2003
). The apparent incongruence of these phylogenies appears to be due to discordant rates of evolution in molecules and morphology as well as morphological convergence.
The five species of Altingia are morphologically distinct. For example, A. gracilipes and A. siamensis are easily distinguished from the other three species (A. chinensis, A. excelsa, and A. poilanei) by having only few fruits per small infructescence and a distinct cuplike bract subtending the fruits (Table 3). While both A. chinensis and A. poilanei have relatively thick peduncles and thick coriaceous leaves, A. excelsa has thinner peduncles and chartaceous leaves. Long, thick peduncles bearing medium-sized fruits set A. chinensis apart from A. poilanei, which has larger fruits borne on much shorter peduncles.
Molecular divergence is lower in Altingia than in Liquidambar: the average chloroplast DNA (trnL-trnF intergenic spacer [IGS], the psaA-ycf3 IGS, the rps16 intron, the trnS-trnG IGS, and
