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2Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, China; and 3L. H. Bailey Hortorium, 462 Mann Library, Cornell University, Ithaca, New York 14853-4301 USA
Received for publication July 11, 1997. Accepted for publication June 27, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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90 million years before present) of New Jersey are described as a new genus, Microaltingia, in the family Hamamelidaceae. The fossils are remarkably preserved in exceptional detail. Several morphological and anatomical characters suggest affinities with Hamamelidaceae. These include capitate inflorescences, florets with a hypanthium, two-carpellate gynoecia, perigynous flowers, tricolpate reticulate pollen, a three-layered carpel wall, scalariform perforation plates with oblique end walls, and scalariform and opposite/alternate intervascular pitting. The gross morphology of pistillate inflorescences, unisexual flowers, phyllome structure, numerous ovules per carpel, and mode of carpel dehiscence indicate affinities with subfamily Altingioideae, which includes the modern genera Liquidambar and Altingia. Cladistic analysis using a previously published morphological matrix and scoring the fossil for available characters supports the position of the fossil as a sister taxon of modern Altingioideae. Although the fossil exhibits a mosaic of characters found within modern Hamamelidaceae, it is not identical to any modern taxon. Based on cladistic analysis, the fossil appears to be a basal "altingioid" that lacks the derived pollen found in extant Altingioideae and retains the more plesiomorphic tricolpate pollen found in the rest of Hamamelidaceae. The floral characters of the fossils, including phyllomes with stomata, short and straight styles, and small perprolate pollen grains, also indicate the possibility of insect pollination.
Key Words: Altingioideae • Cretaceous • Hamamelidaceae • mosaic • Turonian
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Extant Hamamelidaceae include four subfamilies with 100 species grouped into 30 genera (12 of them monotypic) according to Endress (1993)
or 26 genera (13 of them monotypic) according to Cronquist (1981)
. The family is widespread in both the Old and New Worlds, but is most abundant in subtropical and warm-temperate areas, particularly in eastern Asia (Cronquist, 1981
). The family has been the object of a great deal of attention because of its critical phylogenetic position and extensive fossil record (e.g., Cronquist, 1981
; Friis, 1985a, b
). There have been numerous papers on Hamamelidaceae addressing the taxonomy, biogeography, morphology, palynology, and systematics. These as well as recent analyses of DNA sequence data (Chang, 1958, 1979
; Bogle, 1970, 1986, 1989
; Endress, 1977
; Goldblatt and Endress, 1977
; Bogle and Philbrick, 1980
; Matthew, 1981
; Wisniewski and Bogle, 1982
; Huang, 1986
; Zavada and Dilcher, 1986
; Li and Hickey, 1988
; Ferguson, 1989
; Pan, Lu, and Wen, 1990
; Lu, Li, and Xu, 1991
; Chase et al., 1993
; Lu, Li, and Chen, 1993
; Manos, Nixon, and Doyle, 1993
) provide an excellent framework for the evaluation of new fossil evidence.
The fossil record, especially that of the Cretaceous, plays a very important role in understanding the origin, diversity, and phylogeny of angiosperms. However, the early diversity and evolution of the family Hamamelidaceae are still unclear due to the relatively poor Cretaceous fossil record. In contrast, fossil leaves, wood, seeds, pollen grains, staminate inflorescences, fruit, and fruiting heads dating from the Tertiary have been found from widespread sites in both the New and Old Worlds (Hu and Chaney, 1940
; Brown, 1946
; Chandler, 1961
; Mai, 1968
; Ferguson, 1971, 1989
; Wolfe, 1973
; Christensen, 1976
; Knobloch and Kvacek, 1976
; Tanai, 1976
; Mai and Walther, 1978
; WGCPC, 1978
; Tiffney, 1986
; Wang, 1992
). Several hamamelidaceous floral fossils have been described from Cretaceous sediments (Friis, 1985a, b
; Friis and Crane, 1989
; Friis and Endress, 1990
; Magallon-Puebla, Herendeen, and Endress, 1996
). Previous to the fossils described here, the oldest fossil flowers of broadly hamamelidaceous affinity were from the same site in the Turonian Raritan Formation of the Upper Cretaceous in New Jersey (Crepet et al., 1992
). These fossil remains include staminate heads, pollen grains, and pistillate inflorescences. The latter were not well preserved due to abrasion, but retained critical structural details, particularly of the carpel and floral envelope (Crepet et al., 1992
). The position and transitional morphology of the latter fossil's stamens also support a staminal origin of petals in the hamamelid–rosid lineage (Crepet et al., 1992
). Because characters of these fossils include features found in modern Hamamelidaceae as well as possibly more plesiomorphic features of other basal tricolpates (e.g., Platanaceae) they do not represent Hamamelidaceae sensu stricto and they support a relatively close phylogenetic relationship between Hamamelidaceae and Platanaceae (Crepet et al., 1992
). Another younger fossil flower, Allonia decandra, with affinities to subtribe Loropetalinae, has been described from Campanian deposits in Georgia (Magallon-Puebla, Herendeen, and Endress, 1996
). Finally, a well-described hamamelidaceous fossil flower, Archamamelis bivalvis, is from Late Santonian or Early Campanian (Upper Cretaceous) deposits of the Kristianstad Basin, Sweden (Endress and Friis, 1991
). This fossil flower is apparently bisexual, 6(7)-merous, with a bicyclic perianth, one whorl of stamens, and 2–3 carpels. It most closely resembles the genus Hamamelis, but with the three-carpellate gynoecium indicating a possible affinity with Fagaceae (Endress and Friis, 1991
).
In the present paper, we describe a fossil taxon based on nine separate fossil pistillate inflorescences including pollen grains (on stigmas), fruits, and seeds from the Turonian of New Jersey. The fossils are quite well preserved, allowing comparison of several morphological details of the flowers and inflorescences with those of extant plants. Superficially, the fossil taxon presents a striking character mosaic, with its characters now distributed among the modern subfamilies Hamamelidoideae, Exbucklandioideae, and Altingioideae. However, a preliminary cladistic analysis using the published matrix of Hufford (1992)
strongly and unequivocally supports placement of the fossil as a sister taxon of subfamily Altingioideae (including Liquidambar) within the Hamamelidaceae. The fossil has some strong synapomorphies with modern altingioids (e.g., floral phyllomes), and the characters of the fossil not found in modern Altingioideae are plesiomorphic features within the family Hamamelidaceae, indicating that the fossil represents an early offshoot of the lineage that led to modern altingioids. The morphology of the fossils' styles, stigmas, and pollen size suggest that they were insect pollinated, in contrast to the anemophilous modern species of Altingioideae.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Doyle and Robbins, 1977
; Grimaldi, Beck, and Boon, 1989
; Crepet et al., 1992
; Nixon and Crepet, 1993
). The fossils are charcoalified (fusainized). The three-dimensional preservation with extraordinary cellular detail has been interpreted as the result of rapid charcoalification during ancient flash forest fires (Friis, Crane, and Pedersen, 1988
; Crepet et al., 1992
; Herendeen, Crepet, and Nixon, 1993, 1994
; Nixon and Crepet, 1993
; Crepet and Nixon, 1994
; Lupia, 1995
). Fossils described here are a series of inflorescences, infructescences, flowers, and seeds. These structures are extremely small in comparison to related modern taxa, a feature seen in a number of other floral remains from the same deposits (Crepet et al., 1992
; Herendeen, Crepet and Nixon, 1993, 1994
; Nixon and Crepet, 1993
; Crepet and Nixon, 1994
).
The methods employed to isolate fossils from the unconsolidated silt clay matrix follow Crepet et al. (1992)
, Herendeen, Crepet, and Nixon (1993, 1994), Nixon and Crepet (1993)
, Gandolfo et al. (1997)
, Gandolfo, Nixon, and Crepet (1998)
, and Nixon, Weeks, and Crepet (in press)
. The definition and circumscription of the subfamilies of the Hamamelidaceae follow Endress (1993)
. The fossil specimens are stored in the L. H. Bailey Hortorium Paleobotanical Collection of Cornell University (CUPC).
Cladistic analyses
The published morphological matrix of Hufford (1992)
was reanalyzed using the program NONA (Goloboff, 1998
). The data set was analyzed as originally published first and then with Microaltingia included. The matrix without Microaltingia has 80 taxa and 60 morphological and chemical characters. We were able to score Microaltingia for 21 characters used in the Hufford (1992)
matrix (Table 1); the remainder were scored as missing. Standard parsimony analyses with thousands of randomly generated Wagner trees as starting points were performed followed by tree bisection recognition (TBR) swapping holding various numbers of trees. In general, this data set can be considered very difficult for the number of taxa. This difficulty can be attributed to very high levels of ambiguity and the low number of characters relative to taxa, in addition to the presence of several complex multistate nonadditive (unordered) characters with many possible states. Initial analyses with NONA discovered trees shorter than those reported by Hufford (1992)
using PAUP 3.0. Additional analyses were therefore performed using the parsimony ratchet (Nixon, 1999
) as implemented in Winclada (Nixon, 2000)
using NONA as a tree search engine. Ratchet analyses used 10% character sampling and 500 iterations per run. Approximately 25 ratchet analyses were performed, and trees were collected in Winclada and filtered to retain only the shortest trees. These trees were then resubmitted to NONA and TBR swapping was performed holding an excess of trees (10 000) to obtain as many trees as possible from the islands of shortest trees found with the ratchet analyses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Family—Hamamelidaceae
Subfamily—Altingioideae Reinsh (1890)
Microaltingia gen. nov.
Type species—Microaltingia apocarpela sp. nov.
Diagnosis
Pistillate inflorescences globose to subglobose, with about ten tightly packed florets. Capitula pedunculate. Vessel members in the peduncle have oblique end walls with scalariform perforation plates and intervascular pitting that is scalariform to opposite/alternate. Individual florets unisexual (pistillate only), actinomorphic, small (1.2 mm). Two to three whorls of glabrous phyllomes inserted on the rim of the hypanthium. Phyllomes bearing stomata. In immature flowers, there are apparently at least 13 lobes in the first cycle of phyllomes. The lobes are fleshy, sterile, and usually concentrically fused. Two to three cycles of phyllomes can be observed in fruits. No evidence of stamens or staminodia is found in the pistillate florets. The gynoecium consists of two carpels composing a semi-inferior ovary that is distally free from the hypanthium and forms a perigynous flower. There are no trichomes on the surface of the gynoecium. The carpels are distally apocarpous. The ovary is bilocular with each locule having its own carpellary wall in the region of contiguity. The styles and stigmas are completely free and are lost in the mature fruits. The stigmas are apical, capitate, and have multicellular shallow papillae. Each carpel contains about ten marginal seeds arranged in two rows. All seeds look to be of the same size and shape (elliptic to polygonal, slightly impressed, saddle-shaped) with an apical hilum. There are ridges on the seed surface and seeds lack wings. At maturity, the carpels undergo apical dehiscence both septicidally and loculicidally. The pollen grains, found on the stigmas and the surface of the peduncle, are relatively small, 9–10 µm in polar (P) diameter, only 3.1–3.5 µm in equatorial (E) diameter, perprolate (P/E 
2.86), and consistently tricolpate. Colpi extend almost the entire polar length of the grains. There is no indication of an endoaperture in any of the grains examined with scanning electron microscopy (SEM). Exine sculpturing is reticulate with relatively large lumina that show some variation in size.
Microaltingia apocarpela sp. nov.
Specific diagnosis—as for the genus Microaltingia
Holotype—CUPC 1062.
Paratype—CUPC 1063; 1064; 1065; 1066; 1067; 1068; 1070; 1071; 1072.
Type locality—Old Crossman Clay Pit, Sayreville, New Jersey
Age and stratigraphic position—Late Turonian, Lower Magothy Formation, South Amboy Fire Clay.
Description and commentary
The species is represented by nine fossil pistillate inflorescences and fruits. Staminate inflorescences have not been identified. Fossil pistillate inflorescences are globose to subglobose or truncated-spheroidal in shape (Figs. 1–3), 7 mm in diameter. There are 8–12 florets, usually >10, in each head. The florets are sessile and tightly packed in the head. Nearly half of the fossil capitulas are preserved with peduncles (Figs. 3, 25, 26). The preserved parts of the peduncles are 0.2 to 0.4 mm long. Peduncles are elliptical-circular in cross-section (e.g., CUPC 1062; Fig. 27) and have well-preserved anatomical details (Figs. 27–30). There is a narrow cortex, a vascular cylinder composed mostly of secondary xylem and a small pith with large often elongate parenchyma cells with secondary walls containing opposite-alternate, elliptical-circular intercellular pitting (Figs. 27, 33–35). Vascular tissue can be observed in a more or less longitudinal section in one area of the broken peduncle of CUPC 1062 (Figs. 35, 36). While the vessel elements are not exposed for their entire lengths on the broken surface, it is possible to observe some scalariform and oblique perforation plates, and intervessel pitting is scalariform. Individual pits are bordered and elliptical in shape (Fig. 35). Pitting between the conductive cells and associated parenchyma is opposite to alternate, with circular to elliptical bordered pits (Fig. 29).
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1.2 mm in diameter; Figs. 4–6). The gynoecium is surrounded by 2–3 whorls of fleshy, sterile phyllomes (Figs. 5, 12). In the young flowers (CUPC 1064, 1063), there are 13 phyllomes in the inner cycle (Figs. 5, 12). No hairs are found on phyllome surfaces. Because of frequent fusion between the second and third cycles of phyllomes in mature fruits, the numbers in each cycle are difficult to distinguish (Fig. 15). Stomata can be observed on the phyllomes (Figs. 16, 21, 22), but the subsidiary cell pattern is unclear due to preservation or perhaps because these are stomata modified for a secretory function. Each stomate is 12.9 µm long and 8.6 µm wide, broadly elliptical in shape with a wide rim and narrow aperture (Figs. 21, 22). In one specimen (CUPC 1068), several vessel members can be seen in transverse section in the third cycle of phyllomes (Figs. 17, 23, 24). These vessel members have scalariform intervascular pitting and oblique scalariform perforation plates (Figs. 23, 24). In mature flowers, the phyllomes appear more massive and they are often fused to each other (Figs. 4, 6). In contrast to the fossil, there is only one whorl of phyllomes in extant Altingioideae, and stamens are inserted outside of the phyllomes on the periphery of the floret (Bogle, 1986
). Thus, the outside whorl of phyllomes in the fossils is in the same position as the stamens of "pistillate" flowers of extant Altingioideae. However, no anther or clearly transitional structure has yet to be identified among the phyllomes, and the fossil flowers recovered thus far are only pistillate (Figs. 12, 13).
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The anatomical structure of the carpel walls can be observed in some specimens (CUPC 1064; Figs. 18, 19). The carpel walls consist of 3–4 cell layers. The inner (adaxial) layer is composed of epidermis-like cells that are small with relatively thick cell walls. The middle layer consists of one layer of radially elongate cells that are narrow in the tangential plane. And there are 1–2 layers of outer (abaxial) cells that are also epidermis-like but a little larger and less regular than those on the adaxial side. Cells of the outer layer are sometimes irregular in section as though they were partially crushed (Fig. 18).
Each carpel bears several ovules or seeds (Figs. 3, 6, 8, 9, 10, 13). The exact number of ovules/seeds in each open carpel is not certain. However, in most cases there are more than eight, and ten or more have been observed in several specimens. Seeds are arranged in two rows (Fig. 9), with marginal placentation (Figs. 19, 20). Young ovules are clearly anatropous, as indicated by the micropyle visible in a proximal position near the point of attachment as seen in several ovules in at least one specimen (Fig. 19). Within a carpel, all seeds are nearly the same size and shape (Figs. 3, 6, 8, 9, 10, 13), indicating that they were all at the same stage of maturity (or were all aborted, see discussion below) at the time of preservation. Seeds are elliptic to polygonal in shape, slightly impressed, saddle-shaped with ridges on the surface suggestive of the anticlinal walls of the sclerotesta cells (Fig. 11). Mature dehiscent carpels are often preserved (Figs. 3, 6, 8). The carpels open apically along the adaxial suture, and each carpel is further divided into two valves by loculicidal longitudinal dehiscence along the abaxial or "dorsal" side (Figs. 3, 6, 8, 9).
Pollen grains have been found both on the stigmas and on the peduncles (Figs. 37, 38). Pollen grains on stigmas are partially occluded as though they were preserved in a stigmatic exudate (or the formerly suspended particulate residue of such an exudate). Nonetheless, the overall shape, size, number, and form of apertures and exine ornamentation can be observed (Figs. 37–42). Pollen grains preserved on the peduncle are similar in shape, size, aperture configuration, and exine ornamentation to those found on the stigmas but are more easily observed since they are not preserved in a medium that partially obscures them (Figs. 38, 40, 42). The pollen grains are relatively small, 9–10 µm in polar diameter, only 3.1–3.5 µm in equatorial diameter, perprolate in shape (P/E = 2.9–2.85), and consistently tricolpate. Colpi extend almost the entire length of the grains (Fig. 40). There is no indication of an endoaperture in any of the grains examined with SEM. Exine sculpturing is reticulate with polygonal lumina and somewhat laterally flattened muri (Figs. 38–40).
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morphological data matrix using NONA and Winclada with the parsimony ratchet resulted in significantly shorter trees that had very different patterns of relationship for several groups than those presented by Hufford (1992)
. Differences are relevant to our discussion of Microaltingia and Hamamelidaceae. Hufford reported 56 trees of length 682, but our analyses resulted in 119 trees of length 679. This disparity can be explained by the use of NONA (Goloboff, 1998
) instead of PAUP 3.0 combined with more effective search strategies, including the parsimony ratchet. This has been demonstrated empirically to be several orders of magnitude faster and much more effective at discovering shortest trees than is PAUP (Nixon, 1999
). One of the most significant differences between the actual most parsimonious trees for this data set and those published by Hufford is the position of Platanaceae. In Hufford's published trees, Platanaceae, represented on the tree by the genus, were a sister taxon of Hamamelidaceae, while in the actual shortest trees based on that (Hufford's) data set, Platanaceae have a more basal position in the tricolpate clade and are not a direct sister taxon to Hamamelidaceae. This latter pattern is more consistent with recent molecular analyses. When Microaltingia is included in the matrix, all shortest trees place Microaltingia as a sister taxon to modern Altingioideae, as shown in the strict consensus (Fig. 43). With Microaltingia included, Platanaceae is still not placed as a sister taxon to Hamamelidaceae, and the trees are otherwise identical to those trees found with Microaltingia excluded.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Endress, 1989a, b, 1993
; Endress and Friis, 1991
).
Fossil flowers of hamamelidaceous affinity are uncommon, but, as noted above, at least three have been reported from Cretaceous deposits. Archamamelis is represented by flower fragments and isolated stamens found from the upper Cretaceous (late Santonian or Early Campanian) of Sweden (Endress and Friis, 1991
). Archamamelis resembles the genus Hamamelis and differs from Microaltingia in being 6(7)-merous, completely syncarpous, and bisexual. Archamamelis and Microaltingia apparently represent very different evolutionary lines within Hamamelidaceae. The slightly older hamamelidaceous fossil flower Allonia decandra has been described from Campanian deposits of the southeastern United States. This taxon is represented by pentamerous staminate flowers. They have narrow petals and two whorls of distinctive stamens and have affinities with the subtribe Loropetalinae (Magallon-Puebla, Herendeen, and Endress, 1996
).
Another taxon is represented by unisexual hamamelidaceous fossil inflorescences (both staminate and pistillate) from the same locality as Microaltingia (Crepet et al., 1992
). It differs dramatically from Microaltingia in lacking both phyllomes and hypanthia in both male and female flowers and having a well-developed four-lobed perianth in flowers of both sexes and pollen that, while similar to that of Microaltingia, has smaller lumina (Crepet et al., 1992
). Based on preliminary cladistic analyses (unpublished data) in which the fossils were included in Hufford's (1992)
matrix, Microaltingia is not closely related to these other hamamelidaceous inflorescences, and we must continue to search for possible staminate material of Microaltingia.
Although fossil staminate inflorescences representing the genus Microaltingia are not known, fortunately, staminate material is not necessary to firmly establish the hamamelidaceous affinity of the pistillate inflorescences. It is possible that our failure to find corresponding staminate inflorescences in Microaltingia is due to differential temporal shedding of staminate flowers and mature (pistillate) infructescences. In modern Hamamelidaceae, the characters of the pistillate inflorescences are sufficient to determine their affinities at both the family and subfamily levels, and sometimes, even generic affiliations can be determined on the basis of the characters of the pistillate inflorescences.
Within the Hamamelidaceae, subfamily Hamamelidoideae, comprising 22 genera with 80 species, is the largest of the four subfamilies (Endress, 1993
). The flowers of Hamamelidoideae are predominantly bisexual, but in some genera flowers are andromonoecious or unisexual. Petals are ribbon-like in most genera, but may be short and of different morphologies. Most genera within the Hamamelidoideae have sepals, but they are sometimes missing (e.g., Distylium, Matudaea, etc.). While flowers of most genera in the subfamily have one ovule/carpel, there are three ovules/carpels in Neostraria, Noahdendron, and Corylopsis (Endress, 1993
). Moreover, inflorescences in the Hamamelidoideae are spikes, racemes, or small axillary clusters but not capitate inflorescences. In living Hamamelidoideae, distinctly unisexual inflorescences occur only in Sinowilsonia. All of these characters separate Microaltingia from Hamamelidoideae. Possible affinities of the monogeneric subfamily Rhodoleioideae with Microaltingia can easily be ruled out due to the bisexual and zygomorphic flowers of that subfamily. The subfamily Exbucklandioideae includes four genera (Endress, 1993
) with bisexual flowers. Chunia and Mytilaria have spicate inflorescences, while Disanthus has two-flowered inflorescences and Exbucklandia has capitate inflorescences. Exbucklandia, therefore, is the only genus similar to Microaltingia in Exbucklandioideae. However, Exbucklandia is different from Microaltingia in having bisexual flowers and loosely packed florets in the inflorescence. In addition, Exbucklandia typically has only 6–8 ovules in each carpel, whereas Microaltingia has at least eight and frequently more than eight.
The subfamily Altingioideae includes the genera Liquidambar, Semiliquidambar, and Altingia with 13 extant species (Endress, 1993
). Microaltingia is considered similar to the extant Altingioideae based on a suite of common characters. The gross morphology of the pistillate inflorescences is nearly the same, except that in Microaltingia it is smaller in size. Numerous sessile, tightly packed florets form globose to subglobose inflorescences in both the fossil and the extant taxa. They both have unisexual (or functionally unisexual) inflorescences and both fossil and modern taxa lack a perianth and have phyllomes inserted on the rim of the hypanthium (although there is only one whorl of phyllomes in extant taxa vs. 2–3 in the fossil). In addition, there are several to many ovules per carpel in both the fossil and the extant taxa of the subfamily. Note that, while sterile phyllomes in pistillate flowers are distinctive features of extant Altingioideae, they also occur in some genera of subfamilies Exbucklandioideae and Rhodoleioideae.
Of the three genera of Altingioideae, Microaltingia most closely resembles the genus Altingia. Microaltingia has some unique characters shared only by Altingia. The style of Altingia is shorter than those of the other two genera and is largely or completely lost when the infructescence is mature. Similarly, Microaltingia has short styles present only in young flowers. In contrast to the fossil, the carpels split open only along the inner surface (septicidal dehiscence) in both Liquidambar and Semiliquidambar (Chang, 1958
; Bogle, 1986
; Ferguson, 1989
), while in both Altingia and Microaltingia each carpel further splits abaxially into two separate valves (a feature also found in some Hamamelidaceae outside of Altingioideae and possibly plesiomorphic within the family). The fossil taxon has more characters in common with modern Altingia (and with Altingioideae) than with any other modern taxon (but it does share numerous characters with Exbucklandia).
However, several characters found in Microaltingia are not found in extant Altingia or Altingioideae. The most significant differences are related to pollen morphology. The pollen grains of extant Altingioideae are spherical and periporate with circular pores and fine reticulate ornamentation (Bogle and Philbrick, 1980
; Zavada and Dilcher, 1986
), whereas pollen of Microaltingia is perprolate and tricolpate with coarsely reticulate exine. Pollen like that of Microaltingia is common in other subfamilies of the Hamamelidaceae, particularly Exbucklandioideae and Hamamelidoideae, and the tricolpate-reticulate type is common among other families considered to be basal tricolpates (Cronquist, 1981
). Other differences between the fossil and extant taxa include floret structure and morphology. In extant Altingioideae, the gynoecium is surrounded by a single cycle of fleshy, sterile phyllomes, and outside of the phyllomes there sometimes is a cycle of stamens (Bogle, 1986
). In Microaltingia there are 2–3 cycles of the phyllomes and no apparent stamens. However, sometimes stamens fail to develop in extant Altingioideae. While the morphology of the phyllomes of the fossil is similar to phyllome morphology of the modern taxa, the phyllomes in modern Altingia, like the carpels, are covered by dense hairs, but they are glabrous in the fossils. There are also differences in the numbers of seeds. Although both Microaltingia and extant Altingioideae have numerous ovules per carpel, only a few ovules mature in the modern taxa (Mohana Rao, 1974
; Endress, 1993
). In further contrast to the fossil, the ovules mature as winged seeds in modern Altingioideae and Exbucklandioideae (Endress, 1993
). None of the seeds in Microaltingia are winged and, in fact, they have testal sculpturing similar to that in the aborted ovules of modern Altingia, introducing the possibility that we do not have any fossil specimens with carpels containing mature ovules.
The inflorescences of Microaltingia exhibit a mosaic of characters found in the subfamilies of modern Hamamelidaceae, particularly in Altingioideae, Exbucklandioideae, and Hamamelidoideae. The combination of features in the fossils (capitate-spheroidal inflorescences, tricolpate, reticulate pollen, unisexuality, sterile phyllomes surrounding the gynoecium, gynoecium partially inferior, bilocular, and an ovary with multiple nonwinged seeds) is not found in any single extant subfamily or genus of Hamamelidaceae. Most of these features are concentrated in Altingioideae (except pollen morphology/ornamentation and a gynoecium that is partially inferior), but many are also found in Exbucklandioideae (including pollen characters and sterile phyllomes) and a few (also including pollen characters) in Hamamelidoideae.
Some features of Microaltingia are similar to those of modern and fossil members of Platanaceae, but that family can be removed from consideration because of the numerous apomorphic features of the fossil not found in Platanaceae, such as syncarpous bicarpellate flowers (Cronquist, 1981
; Endress, 1993
; Kubitziki, 1993a, b
). Although Microaltingia possesses a mixture of characters now distributed among modern Hamamelidaceae and Platanaceae, the characters that Microaltingia shares with the platanoids are also shared with putatively more basal members of the Hamamelidaceae. As noted above, the set of characters found in Microaltingia is not found in any single genus or subfamily of Hamamelidaceae. Thus, it can be concluded that Microaltingia represents an extinct hamamelidaceous taxon which is closest to Altingioideae, particularly Altingia, that retains ancestral characters (particularly pollen morphology) reflecting its relationships with basal Hamamelidaceae (especially Exbucklandia; Bogle, 1986
). This conclusion is consistent with the preliminary phylogenetic analysis. When Microaltingia is included in the broad rosid matrix of Hufford (1992)
, in all parsimonious trees Microaltingia is a sister taxon to the subfamily Altingioideae. This strongly supports our placement of Microaltingia, especially given that Hufford's (1992)
matrix does not include some additional characters discussed above that support the placement of Microaltingia near Altingioideae (e.g., phyllomes, nature of the inflorescence, unisexual florets).
Several traditional morphological works and recent cladistic analyses based on morphology suggest a close systematic relationship between Platanaceae and Hamamelidaceae (Takhtajan, 1969
; Hickey and Wolfe, 1975
; Cronquist, 1981
; Zavada and Dilcher, 1986
; Lu, Li, and Xu, 1991
; Schwarzwalder and Dilcher, 1991
; Hufford, 1992
; however, it appears that Hufford's published trees were not actually most parsimonious and misplaced Platanaceae, as discussed below). In contrast to many morphological analyses, recent published cladograms based on molecular DNA sequences place modern Platanus more basally within the tricolpate clade, with the "ranunculids" (e.g., Chase et al., 1993
). When the matrix of Hufford (1992)
is reanalyzed with NONA (Goloboff, 1998
), shorter trees than those found with PAUP 3.0 resulted, and these trees place Platanaceae in a position more similar to that found with molecular analyses, i.e., as an early branch on the tricolpate lineage subtending the divergence of Hamamelidaceae and not a sister taxon to that family. This is true without the addition of Microaltingia as well as with the fossil included (Fig. 43). Based on these more careful morphological analyses, the most parsimonious interpretation is that any platanoid features (e.g., capitate inflorescences, pollen morphology) of Microaltingia and other hamamelid fossils from the Turonian (Crepet et al., 1992
) are retained plesiomorphic features common to a possibly platanoid ancestor in terms of morphology, but that is not phylogenetically related to modern Platanaceae. In other words, the ancestral tricolpate plexus was "platanoid" in general morphology, but modern Platanaceae are derived and more closely related to families other than Hamamelidaceae. Fossils with platanoid features ("Platanaceae") date back to the Lower Cretaceous (e.g., Friis and Crane, 1989
), but these fossils do not have unequivocal synapomorphies with modern Platanaceae, as discussed by Nixon (1996)
. The oldest Hamamelidaceae are Turonian (this report, and Crepet et al., 1992
). The mosaics of platanoid features found in both fossil and modern Hamamelidaceae support the interpretation that Hamamelidaceae was derived from a Platanus-like ancestor, but that modern Platanaceae have independently retained similar features and are not a sister taxon of Hamamelidaceae lineage. While this distinction is subtle, it is important to keep in mind when interpreting characters and assigning names to fossil taxa. Much of the confusion exists because of the designation of platanoid fossils as Platanaceae without reference to any conclusive synapomorphies (e.g., Friis and Crane, 1989
).
Phyllomes are distinctive characters of Microaltingia, modern Altingioideae, Exbucklandia, and Rhodoleioideae. The nature and function of the phyllomes have always been in question. There are several different interpretations of these structures: as bracteoles surrounding the pistillate flowers (Guillaumin, 1920
); as styles of sterile carpels (Harms, 1930
); as staminodia (Tong, 1930
); as disk lobes (Vink, 1957
; Bogle, 1986
); and as rudimentary scales (Endress, 1993
). No stigmatic surfaces, ovules, or pollen have been observed on or as part of phyllomes in any fossil or extant plants (Bogle, 1986
). There is no convincing evidence that they are derived from reproductive structures. The proliferated system of procambial strands observed in the bases of the sterile phyllomes and the stomata on phyllome epidermis of Liquidambar, L. styraciflua (Wisniewski and Bogle, 1982
), might indicate a glandular or secretory function (and therefore the possibility that they are attractants/rewards to pollinators), but confirmation based on field observation is called for (Bogle, 1986
), and such information is needed before making inferences on the function of similar stomata found on phyllomes of Microaltingia (Figs. 21–22).
Modern Altingioideae are wind-pollinated with typical anemophilous characters such as naked unisexual flowers with long, widely decurrent stigmas (Bogle, 1986
; Endress, 1989a, 1993
) and spheroidal pollen grains in the size range 32–55 µm (Bogle and Philbrick, 1980) that are characteristic of wind-pollinated angiosperms (Whitehead, 1969
; Friis and Crane, 1989
). Microaltingia also exhibits unisexual flowers, but these florets have very small perprolate pollen grains 9–10 µm in size and stigmas restricted to apical regions, characters only found in entomophilous Hamamelidaceae (Endress, 1989c
). In combination with the well-developed phyllomes of Microaltingia, these characters suggest that Microaltingia may have been insect pollinated as has been suggested for early platanoids (Friis and Crane, 1989
), a possibility consistent with derived entomophily in Hamamelidaceae as suggested above.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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