| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
a L. H. Bailey Hortorium, 462 Mann Library, Cornell University, Ithaca, New York 14853-4301 b Department of Plant Biology, Arizona State University, Box 871601, Tempe, Arizona 85287-1601
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
Key Words: acorn • cupule • Fagaceae • fossil • fruit • Middle Miocene • paleobotany • Quercus
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
; Crepet, 1989
). While some authors include the Southern Hemisphere taxon Nothofagus Blume in the Fagaceae, more recent treatments have placed this group of biogeographically important trees in its own monotypic family, Nothofagaceae Kuprianova, based on numerous distinguishing characters (Kuprianova, 1962
; Nixon, 1982
; Jones, 1986
; Romero, 1986
; Hill and Jordan, 1993
; Manos and Steele, 1997
; Rozefelds and Drinnan, 1997
).
An important defining character within the Fagaceae is the presence of a woody subtending structure, called a cupule, around the flower(s). This cupule is sometimes described as an involucre, but cupules are believed to be condensed branching structures rather than involucral bracts (Forman, 1966
; Fey and Endress, 1983
). Flowers in this family have an inferior ovary composed of several fused carpels with two ovules per carpel. After fertilization, the flower develops into a one-seeded, unilocular, indehiscent fruit that is commonly called a nut. Several features, including the mature appearance and dehiscence pattern of the cupule, and the number of fruits enclosed by the cupule are diagnostic for each genus, and numerous authors have addressed the evolutionary significance of these features within Fagaceae (e.g., Berridge, 1914
; Brett, 1963
; Forman, 1966
; Abbe, 1974
; Endress, 1977
; Fey and Endress, 1983
; Nixon, 1989
, 1993
; Crepet and Nixon, 1989a, b
). Two genera of Fagaceae, Quercus and Lithocarpus, form a globose, indehiscent fruit that can be fully to partially enclosed by a non-spiny cupule with a bowl-like shape, and the fruit and cupule described together comprise the acorn. The genus Castanopsis can have globose fruits, but each fruit is typically enclosed within a spiny cupule that opens along sutures to form valves. A few species in Castanopsis develop non-spiny cupules, but suture-like zones are visible, and these cupules also have asymmetric scale-bearing ridges, while almost all acorns have symmetrical scale patterns (Kaul, 1988
). Cupules in Lithocarpus and Quercus are unique in the family as evalvate structures that subtend a single fruit and are thought to be derived within the Fagaceae (Forman, 1966
; Fey and Endress, 1983
; Nixon, 1984
).
Quercus is widely distributed throughout the Northern Hemisphere with its greatest diversity in the southeastern United States, the highlands of Mexico, montane subtropical Eurasia, and east Asia (Nixon, 1993
, 1997
). In contrast, Lithocarpus has its highest diversity in southeast Asia (Soepadmo, 1972
). The leaves, fruits, and growth patterns of Lithocarpus and Quercus are morphologically similar, but the two genera can be distinguished on closer comparison through differences in pollination methods, inflorescences, floral morphology, and number of stamens (see Table 1).
|
; Gregor, 1977
), mentioned in a variety of compression floras as Q. sp. acorns and/or cupules (Newberry, 1898
; Knowlton, 1926
; Berry, 1929
, 1931
, 1934
; Brooks, 1935
; Smith, 1939
; Condit, 1944
; Graham, 1963
, 1965
; Smiley and Rember, 1985
; Manchester and Meyer, 1987
), identified to species based on association with leaves of a particular fossil taxon (Fields, 1990
; Axelrod, 1991
), and some acorns have been formally described and assigned a specific epithet (Daghlian and Crepet, 1983
; Manchester, 1994
). However, these fossils show only morphological detail and are limited in the information they provide. The present study documents the first petrified Quercus acorns to be described on the basis of internal anatomical detail. A suite of morphological, anatomical, and developmental features of the fossil acorns are compared to features in extant Lithocarpus and Quercus and provide a unique opportunity to document the evolutionary status of derived features in the family Fagaceae in the Neogene. |
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
, 1992
; Reidel et al., 1989
; Borgardt and Pigg, 1996
; Pigg, Sophy and Wehr, 1996
). The fossil material occurs in the Museum Flow Package within the interbeds of the Sentinel Bluffs Unit of the central Columbia Plateau N2 Grande Ronde Basalt of the Columbia River Basalt Group (Middle Miocene, Upper Tertiary) dated 15.6 ± 0.2 million years old by Ar/Ar radiometric dating (Swanson et al., 1979
; Long and Duncan, 1982
; Landon and Long, 1989
; Reidel et al., 1989
; Tolan et al., 1989
; Katherine M. Reed, Washington State Department of Natural Resources, Division of Geology and Earth Resources, Olympia, Washington, personal communication, 1994). The specimens were recovered from the "County Line Hole" locality known locally as the "Hi Hole" (R. Foisy, Yakima, Washington, personal communication, 1994). All of the specimens described in this study are part of the T. H. Tuggle-Foisy Collection at the Burke Museum of Natural History and Culture, University of Washington, Seattle (UWBM). Additional material was obtained by the authors during a collecting trip to the locality in June 1994 and is deposited in the Fossil Plant Collections, Arizona State University (ASU).
Previous plants described from these localities include Osmunda wehrii Miller, based on petrified rhizomes and petioles, and Pinus foisyi Miller, based on petrified leaves, pollen, and ovulate cones (Miller, 1982
, 1992
). Additional petrified plant remains at this and adjacent sites include several additional types of filicalian ferns (Rothwell, Arnone, and Pigg, 1996
), members of Taxodiaceae, Hamamelidaceae (Pigg, 1997
), Juglandaceae, Vitaceae, Cornaceae, and Typhaceae and several additional forms (Borgardt and Pigg, 1994
, 1996
; Pigg, Sophy, and Wehr, 1996
). Petrified woods described from Yakima Canyon by Prakash and Barghoorn (1961a,
b
) and nearby sites at Vantage studied by Beck (1945
, 1955)
, Scott, Barghoorn, and Prakash (1962)
, and Prakash (1968)
reveal that Ginkgo, several conifers, and a diverse array of dicots, including three types of Quercus wood, were endemic to the central Washington area in the Middle Miocene. Also nearby and of similar age are the well-known western Latah compression floral outcrops near Grand Coulee and Spokane, Washington (Knowlton, 1926
; Berry, 1929
, 1931
; Brown, 1936
; Fields, 1983
, 1996
).
While some of the specimens in the present study were completely within the chert matrix, others were partially or completely weathered out as individual fruits, cupules, or complete acorns. The chert was initially slabbed with an intermediate-sized diamond blade saw to identify individual specimens. These were then excised out and wafered in serial section on a Buehler Isomet Low-Speed saw. All sections were mounted with a UV-cured adhesive (UV-154, T.H.E. Company, Lakewood, Colorado) onto microscope slides for study and reflected light microphotography. Fragile specimens were stabilized in Bioplastic resin (Ward's, Rochester, New York) and then sectioned with the Buehler Isomet Low-Speed saw and mounted on slides. Anatomical sections of extant Quercus fruits loaned by Mogensen, Northern Arizona University, Flagstaff were studied for comparison (Mogensen, 1965
). Specimens were photographed through a dissecting microscope (SZH, Olympus) and a compound microscope (BH-2, Olympus) with reflected light from fiber optics for anatomical detail. Measurements were made with digital calipers (Digimatic, Mitutoyo Corporation, Japan).
|
SYSTEMATICS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
Genus
Quercus L.
Subgenus
Quercus Hickel et Camus.
Section
Quercus Hickel et Camus.
Type species
Quercus hiholensis Borgardt et Pigg sp. nov. (Figs. 5–12, 14, 19–40).
|
|
|
Holotype
University of Washington, Burke Museum of Natural History and Culture (UWBM) collection B4101; specimen number: 45-I (Figs. 5, 31, 38, 40).
|
|
|
Type locality
The "Hi Hole", known locally as one of the "County Line Holes" ("Hi Hole", "Lo Hole", and "Ho Hole") is ~7.3 km north off the Interstate 82 Firing Center Exit, Yakima County, on Yakima Canyon Road (T14N, R19E, NE 1/4 of NW 1/4 of Sec 3).
Age
15.6 ± 0.2 million years old (Middle Miocene, Upper Tertiary).
Stratigraphy
Museum Flow Package, Sentinel Bluffs Unit, central Columbia Plateau N2, Grande Ronde Basalt member, Columbia River Basalt Group.
Etymology
The specific name, hiholensis, refers to the "Hi Hole" locality in Yakima Canyon, Washington.
Quercus sp.
UWBM collection B4101; specimen numbers (in numerical order): 42 (Fig. 16); 68 (Fig. 18); 55104 (Fig. 15); 55401 (Fig. 13); 56468-19 (Fig. 17).
|
DESCRIPTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
|
In specimens with external scale morphology, the cupule scales measure up to 2.8 x 2.8 mm and are helically arranged. A papery tip on the distal end of the scales can extend the length of the scales by 1.4 mm (Fig. 9) when present. Cupule scales vary in their morphology from base to apex. Basal scales appear highly raised and tuberculate (Fig. 7–10). In contrast, the apical scales assume a more regular morphology and are slightly keeled. The most apical scales appear papery and undulate. In paradermal section, all scales show a regular, helical arrangement under the surface of the cupule (Fig. 14). Lateral scales show a gradual change in morphology from the contorted basal scales to the more regular apical scales. Sclereid patches are scattered throughout the cupule (Figs. 8, 39) and are sometimes organized into white star-shaped clusters associated with the interior appressed edges of the scales (Figs. 6, 11, 36).
Almost all of the specimens are fruits and enclose a single seed in a surviving locule. The ovule enlargement that follows fertilization can be seen in some of the smallest specimens (e.g., Figs. 24–26), but embryos could not be confirmed in all young specimens. One specimen (not illustrated) shows no ovule enlargement and is designated a flower. Because of the rare occurrence of flowers, all specimens in this study will be described as fruits. The wall layers in all of the fruits are intact with no compression or disruption, indicating that none of the fruits were fully mature when they were preserved. The fruits range in sizes from 2.7 x 2.6 mm (Fig. 24) up to 9 x 10.9 mm (Fig. 8), and in shape from ovoid-conical (Fig. 12) to ovoid (Figs. 5–6, 8–11). The youngest fruits show best the features of the perianth and styles with the perianth lobes closely appressed to the styles (Figs. 6, 12, 17–22). The styles, when present, are short, and have a broadly expanding apex (Figs. 18–19).
The fruit wall can be seen in two stages of maturation. In the youngest fruits, the layers are subtle, with only the palisade layer and abscission zone clearly visible (Figs. 12, 18, 23–26, 28–30). In more mature specimens, the fruit wall, except for the abscission zone, can be divided into five distinct layers (Figs. 5, 11, 33, 36), which conform to the layers described by Soepadmo (1968)
. The outer epidermis is uniseriate and is composed of tabular cells. Just inside the outer epidermis, the palisade layer is up to 0.3 mm thick with cells radially elongate and densely packed, forming a visible band. The central layer, the outer parenchymatous layer, comprises the bulk of the fruit wall and is up to 2.5 mm. In this layer, discrete patches of isodiametric sclereids are visible and scattered within parenchymatous tissue. The fourth layer, the inner parenchymatous layer, is up to 0.1 mm thick with cells longitudinally elongate and lacks sclereids. The inner epidermis is uniseriate and composed of tabular cells and unicellular trichomes (Figs. 23, 40). The apical portion of the palisade and outer parenchymatous layers in the fruit wall becomes sclerified early in development (Fig. 19). Basally, a disc-shaped abscission zone is present even in the most immature specimens (Figs. 24, 27–28, 30, 35), and was useful in orienting the specimens. In more mature fruits, this layer becomes quite prominent because of the large, discrete, rectangular sclereid patches (Figs. 33–34).
Some of the youngest fruits show the septa and associated basal aborted ovules that characteristically occur in section Quercus (Figs. 25–26, 30). The umbilical complex, which is a compound structure that includes the funiculus of the ovule, the surviving septum, and the placenta, is present at the base of all the specimens, and can be seen as either a post-like structure (Fig. 29), or as a longer, recurved structure (Figs. 33–34). The abortive ovules are basal (Figs. 31, 34), found between the seed coat and fruit wall, and are either filled with tissue (Figs. 31, 34) or appear hollow (Fig. 32).
The seeds in the very youngest fruits are irregularly-shaped and do not completely fill the surviving locule (Figs. 12, 29–30). The seeds in more mature fruits completely fill the locular cavity and become appressed to the fruit wall (Figs. 5–6, 8, 11, 19–20, 33, 35–36). The seed coat consists of rectangular cells that are compressed along their longitudinal plane (Fig. 32).
Embryos are present in many of the specimens with varying degrees of preservation. Embryos are up to 6 x 6.9 mm in size. The specimens that are the best preserved show two cotyledons (Fig. 11), and even the radicle of the embryo axis (Figs. 37–38). Embryos that have undamaged cotyledons (Figs. 5, 11, 33, 36) are smooth externally with no grooves, are not fused to each other, and assume a symmetrical axial orientation in the seed. In a few specimens, the tissue of the cotyledons became partially transparent while being preserved (Figs. 5, 31, 36) and can be studied with transmitted light. One exceptionally preserved specimen shows a young embryo suspended within endosperm (Fig. 27).
Some of the embryos contain foreign materials that either appear as solid masses or loosely associated clumps (Figs. 5, 36). These acorns are similar in appearance to modern forms damaged by beetle larvae and may represent a similar situation for Q. hiholensis.
Several specimens that show a contrasting cupule scale morphology are designated as Quercus sp. (e.g., Figs. 13, 16). Unlike Q. hiholensis, these forms have cupule scales that are regular in their helical arrangement on the cupule and are distinctly keeled with little surface ornamentation in either the apical or distal portions of the cupule.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
|
; Tillson and Muller, 1942
; Tucker, 1980
), and in one extreme case, as multiple genera (Schwarz, 1936
). Camus (1934–1954)
recognized two subgenera, Cyclobalanopsis and Quercus, within the genus Quercus, and recent phylogenetic analyses indicate that these two form monophyletic groups, supporting her classification over other treatments (Nixon, 1984,
1993
). This study will follow a modification of the classification system of Camus for the subgenus Quercus (Nixon, 1993,
1997
) (Table 3). The subgenus and section name Euquercus is updated to Quercus in accordance with the International Code of Botanical Nomenclature (Voss et al., 1983
), and the section name Lobatae has priority over the better known name Erythrobalanus for the black or red oaks. The floral and fruit taxonomic differences among the three North American sections (Lobatae, Protobalanus, and Quercus) have been investigated thoroughly in the literature and are well established (Table 2). The black or red oaks of section Lobatae are native only to the New World, present in North America and Central America, with one species extending its range into Colombia, South America. The oaks in the smallest section, Protobalanus, are currently restricted to western North America and possess a mosaic of features in leaves, wood, flowers, and fruit found in the sections Lobatae and Quercus. Section Quercus, the white oaks, has the greatest number of species and has the widest distribution with occurrences in Asia, Europe, North Africa, and North and Central America. Information about floral and fruit anatomy and development of the other sections established by Camus (Cerris, Macrobalanus, and Mesobalanus) is less well known. They are included in section Quercus according to Nixon (1984,
1993
), and further phylogenetic studies are needed to reveal intra-sectional relationships within this group of oaks.
|
; Muller, 1942a
; Soepadmo, 1972
; Nixon, 1997
) (Table 3). Acorns within genus Quercus are morphologically distinct between the two subgenera. The cupule scales of subgenus Cyclobalanopsis are concentric, fused lamellae and are easily differentiated from the cupule scales of subgenus Quercus and Q. hiholensis which are imbricate and helically arranged (Soepadmo, 1972
; Kaul, 1985
).
In addition to their presence in the genus Quercus, acorns are also found in one other member of the Fagaceae, the genus Lithocarpus. Because the fossil fruits of Q. hiholensis are not found in association with leaves, it is necessary to compare them to both genera. Lithocarpus is almost entirely restricted to Asia, but one species, L. densiflora (Hook & Arn.) Rehder, is present today in California, hinting at a once wider distribution for members of this genus. Lithocarpus leaves that have been compared favorably with extant L. densiflora have been reported from at least five Tertiary localities from the American Northwest (Knowlton, 1926
; MacGinitie, 1933
; Brooks, 1935
; LaMotte, 1952
; Graham, 1963,
1965,
Smiley and Rember, 1985
; Axelrod, 1964
; Fields, 1990,
1996
; Axelrod and Schorn, 1994
), as well as acorns (Axelrod, 1966
; Smiley and Rember, 1985
). Although the extant American Lithocarpus species has a strikingly different cupule morphology (recurved, thin, papery scales) when compared to Quercus cupules, some extant Asian Lithocarpus species have cupules similar to Quercus, and two Northwest localities have leaves assigned to Lithocarpus that are comparable to forms found today in Asia. Axelrod (1966)
compared L. coatsi from the Eocene Copper Basin flora to Asian forms. In the Miocene Oviatt Creek flora, Boyd (1985)
described L. oviattensis leaves with entire margins and drip tips, a morphology found today only in Asia. Comparison of Q. hiholensis to extant American and Asian Lithocarpus acorns reveals several differences such as the basal position of the abortive ovules and umbilical complex, the absence of staminodia in the persistent perianth of the young fruits, cotyledons that are not grooved, and the solitary nature of the fossil fruit (see Table 1) that demonstrate stronger affinities of the fossil acorns to Quercus.
A few fossil acorns have been illustrated in Tertiary fruit and seed or leaf compression floras (Eocene: Manchester, 1994
; Oligocene: Daghlian and Crepet, 1983
; Manchester and Meyer, 1987
; Miocene: Newberry, 1898
; Knowlton, 1926
; Smith, 1939
; Axelrod, 1991
; Taylor and Taylor, 1993
; Pliocene/Miocene: Condit, 1944
). The best-documented occurrences include those from the Eocene of Oregon (Manchester, 1994
), the Oligocene of Tennessee (Daghlian and Crepet, 1983
) and the Miocene of Idaho (Fields, 1990,
1996
; written communication, 1994; Taylor and Taylor, 1993
).
Quercus paleocarpa Manchester was described from the Middle Eocene Clarno Nut Beds of Oregon based on several specimens including a complete acorn with fruit and cupule. The complete acorns are prolate, 22 x 15.5–21.8 mm, with a bowl-shaped cupule covering one-third to one-half the length of the fruit. The cupule is characterized by seven conspicuous concentric transverse ribs, which decrease in size from base to apex. Although cupules with symmetrical concentric rings can be found in both Quercus and Lithocarpus (Kaul, 1985
), Manchester (1994)
interpreted this specimen as assignable to Quercus, on the basis of the relatively coarse appearance of the cupular lamellae. Additional specimens of this type, particularly those showing such features as persistent perianth parts and style morphology, would aid greatly in determining the affinities of these interesting forms.
Quercus huntsvillensis Daghlian et Crepet was described from the Oligocene Catahoula Formation near Huntsville, Tennessee, based on a single, crushed fruit 17 x 15 mm with a peduncle 17 mm long (Daghlian and Crepet, 1983
). They placed this specimen in the subgenus Lepidobalanus (Endl.) Oersted sensu Trelease (=subgenus Quercus, section Quercus), on the criteria of basally thickened cupule scales. Although basally thickened cupule scales are characteristic of section Quercus, they are also found in section Protobalanus, which, although currently restricted to several areas of western North America, was more widespread in the Tertiary (Chaney and Axelrod, 1959
; Wolfe, 1980
; Axelrod, 1983
).
A third interesting occurrence is that of two different species of compressed acorns found in attachment to corresponding leaf-bearing stems from the Middle Miocene Succor Creek flora of the Sucker Creek Formation of southwestern Idaho (Fields, 1990
, 1996,
written communication, 1994; Taylor and Taylor, 1993
). The first specimen with acorns attached to a stem bears leaves of the fossil leaf taxon Q. hannibili Dorf (Fields, Michigan State, East Lansing, written communication, 1994), which has been compared to the modern oak Q. chrysolepis of section Protobalanus (Axelrod, 1964
; Graham, 1965
). The acorns found associated with this leaf taxon have helically arranged cupule scales that are keeled and are morphologically similar to the acorns found associated with the second leaf taxon in such a way that these acorns cannot be distinguished from one another without corresponding attached leaves (Fields, Michigan State University, East Lansing, written communication, 1994). The second specimen has three cupules, 15–21 mm wide, attached to the stem and two of them envelop fruits, which measure 20 x 18 mm, by half their length. The leaf attached to the stem is assignable to Quercus simulata Knowlton, a fossil taxon that, interestingly, has been compared to every taxonomic group in the genus Quercus. Knowlton (1898)
described and compared it to an extant black oak (section Lobatae) with entire leaf margins, and many authors have also compared Q. simulata to black oaks (Chaney, 1920
; Berry, 1929,
1931,
1934
; Axelrod, 1964
, 1992
). This fossil leaf has also been compared to leaves from Lithocarpus densiflora (Chaney, 1927
), oaks in section Protobalanus (Berry, 1929
; Wolfe, 1960,
1964
), and oaks of subgenus Cyclobalanopsis (MacGinitie, 1933
; Chaney and Axelrod, 1959
; Axelrod, 1964
). A dramatic shift in comparison occurred when Niklas and Giannasi (1978)
published a paleobiochemistry study that found leaves of Q. simulata had the most affinity with white oaks (section Quercus) from Japan and Korea. Wolfe (1980)
commented on this study and also recommended comparing Q. simulata to an extant western North American white oak, Q. sadleriana, which appears to be a relictual species with strong similarities to eastern North American and Asian species of Quercus (Nixon, 1997)
.
Quercus hiholensis differs from these previously described acorns in several ways. Cupule scales of Q. hiholensis are helically arranged, in contrast to the concentric lamellae of Q. paleocarpa from the Eocene Clarno Nut Beds. While both Q. hiholensis and the Oligocene Q. huntsvillensis have helically arranged cupule scales, scales of Q. hiholensis vary in morphology from base to apex, and scales of Q. huntsvillensis have basally thickened scales that are keeled and of uniform shape throughout. The acorns attached to leaf-bearing twigs from the Sucker Creek Formation also have a regular keeled morphology from the base to the apex of the fruit.
Morphological features of fossil acorns are usually the only information available, but anatomical characters such as those found inside the fruits of Q. hiholensis are necessary for unambiguous descriptions and taxonomic assignment. Features such as the final position of the abortive ovules and the umbilical complex, cupule scale ornamentation, and details of the persistent perianth and styles are the result of developmental processes that occur in extant Quercus fruits as they mature (Figs. 1–4). The resulting combination of character states are unique to each section of subgenus Quercus (Table 2). The fossil Q. hiholensis acorns documented in this study show several stages of maturation and development that conform most closely to those of section Quercus, and will be used to illustrate the development of the fruits and cupules for this extant section.
Development of reproductive structures in subgenus Quercus
In subgenus Quercus, inflorescence primordia are initiated at the end of the growing season, remaining quiescent in terminal buds until the next flush of growth. The continued development and enlargement of these primordia in temperate climates occur in response to ambient conditions, such as warm temperatures in the spring or adequate rainfall in desert areas (Turkel, 1950
; Rebuck, 1952
; Sharp and Sprague, 1967
). The staminate flowers are borne on catkins and emerge first, sometimes maturing weeks before the pistillate flowers are fully formed and receptive for pollination (Sharp and Chisman, 1961
; Stairs, 1964
). The pistillate inflorescences emerge from leaf axils distal to the leaf axils that produce staminate inflorescences (Trelease, 1924
; Muller, 1942a
). Each pistillate inflorescence has only a few floral primordia produced, and the cupules in subgenus Quercus do not become deformed from crowding. In contrast, the cupules from some species of Lithocarpus and rarely of Quercus subgenus Cyclobalanopsis can show compressed scales or lamellae from the pressure of adjoining cupules (Kaul, 1985,
1987
). The inflorescence axis, which bears the acorns until they are fully mature, can remain short (subsessile) or elongate to form a peduncle up to several centimetres long (Trelease, 1924
; Soepadmo, 1968,
1972
; Kaul, 1985
; Nixon, 1997
). The cupules of Q. hiholensis that show external morphological detail are not deformed from crowding (Figs. 9–10). Several specimens are pedunculate, but of indeterminate length (Fig. 9).
With development of the pistillate flower, individual scale primordia of the cupule emerge at the base of the ovary (Sattler, 1973
). These primordia fuse into a ring and continue to produce cupule scales in an extremely complex helical pattern (Forman, 1966
), enveloping the ovary. The fusion of the primordia results in cupule scales that are accrescent at their base, but loosely or closely imbricate at their apex. The scales can appear papery and flattened (common in section Lobatae), or are basally thickened and appear keeled in profile and/or tuberculate with a variously thickened surface (common in sections Quercus, Protobalanus) (Trelease, 1924
; Muller, 1942a
; Kaul, 1985
). The cupules of Q. hiholensis have a morphology that conforms more closely to sections Quercus or Protobalanus. All scales are thickened basally. Basal scales of the cupule are tuberculate and irregular, and apical scales are smaller with a keeled morphology and less ornamentation (Figs. 5–6, 9–10).
In extant Quercus, the floral apex of the pistillate flower flattens and usually produces two cycles of three perianth members in a ring on the margin of the floral apex. Gynoecial primordia (usually three) appear to the inside of this perianth ring in the ovary wall. As the flower elongates, the gynoecial primordia grow inward to form the septa and delimit locular spaces. Simultaneously, these gynoecial primordia also elongate acropetally through the perianth to form the styles (Sattler, 1973
). These styles are glabrous distal to the perianth with a spreading stigmatic surface on the adaxial groove in subgenus Quercus (Trelease, 1924
; Muller, 1942a;
Nixon, 1984
). In section Lobatae, each style is elongate and gradually spreading (see Fig. 2). In comparison, those of sections Protobalanus and Quercus are shorter and can appear blunt (see Fig. 1), and are most similar to the morphology seen in Q. hiholensis (Figs. 6, 18–20).
The perianth of the pistillate oak flower is urceolate, usually with six lobes. In the sections Quercus and Protobalanus and in Q. hiholensis, these lobes are reduced and are often tightly appressed to the styles (Figs. 6, 17–22
), while in section Lobatae, most of the species have enlarged perianth lobes, and the apical cupule scales become entrapped under them early in development (see Fig. 2) (Ørsted, 1871
; Trelease, 1924
; Muller, 1942a
; Nixon, 1984
).
Previous authors have described the region of the extant Quercus flower and fruit that is located between the base of the perianth to the apex of the ovary as a stylopodium (Trelease, 1924
; Muller, 1942a
). The term stylopodium actually refers to fused styles that form an enlarged structure above the perianth at the apex of the ovary, such as in the family Apiaceae (Lawrence, 1951
; Kearney, Peebles, and Collaborators, 1960). In subgenus Quercus, the perianth is raised above the cupule scales after fertilization by a column formed by the elongation of the apex of the ovary. This pattern can be recognized clearly in Q. hiholensis (Figs. 17, 19–20), where the perianth is above the cupule at even the earliest stages of fruit development. In extant oaks, this column of ovary tissue is persistent on the mature fruit as an apical mucronate umbo, and may be subtended in some species by either a hemispherical swelling or depression in the apical end of the fruit wall (Trelease, 1924
; Muller, 1942a
; Kaul, 1985
). Quercus hiholensis has a depression around the umbo in more developmentally mature fruits (Fig. 5).
Styles, stigmas, perianth, carpels, immature ovules, and the first few rows of cupule scales are all present at the time of pollination in extant subgenus Quercus (Hjelmqvist, 1953
; Stairs, 1964
; Mogensen, 1965
, 1972
). Because the development of the gynoecial primordia is delayed for a time after the floral apex begins to elongate, the locules are incomplete with an open space at the base of the ovary (Figs. 25–26). Prior to fertilization, the collateral, anatropous ovules finish development of the double integument and embryo sac, and most of the ovules are similar in size. Although all six ovules have an equal possibility of developing into the single seed, only one survives. The other five ovules undergo either embryo sac disintegration, zygote or embryo abortion, or fail to develop a coherent embryo sac prior to pollen tube penetration (Brown, 1971
; Brown and Mogensen, 1972
; Mogensen, 1975a
, b
). After fertilization, which can be delayed one year in oaks with the biennial fruiting habit (Mogensen, 1965
), the seed enlarges quickly and fills the locular spaces. Septa in some members of section Lobatae may persist and become imbedded in and/or create grooves in the seed coat and cotyledons (Ørsted, 1871
; Trelease, 1924
; Muller, 1942a
; Nixon, 1984
, 1993
). In sections Protobalanus and Quercus, the cotyledons and seed coat appear smooth. All examined specimens of Q. hiholensis have smooth cotyledons (Figs. 5–6, 8, 11, 20, 33, 36), suggesting greater affinity to sections Protobalanus or Quercus.
Several distinct fruit wall layers are visible in even the youngest fruits (Figs. 5, 8, 11–12, 24–26, 30, 33, 36). Regions of the fruits that are heavily sclerified at maturity, such as the abscission zone, the palisade layer, and the outer parenchymatous layer at the fruit apex, are especially prominent. In extant oaks, the wall layers become compressed and/or break down at the time of fruit maturity, forming the hard "shell" of the acorn. Mogensen (1965)
noted that the fruit wall sclerenchyma in section Lobatae remained thick at maturity, while the fruit wall layers in section Quercus became thin and undefined. All of the Q. hiholensis fruits examined in this study have coherent wall layers with no compression, so this character cannot be resolved.
Historically, a character that has been used to distinguish between extant sections Lobatae and Quercus is the pubescence of the inner epidermis of the fruit wall, or endocarp (Trelease, 1924
; Tillson and Muller, 1942
; Mogensen, 1965
; Tucker, 1980
; Nixon, 1984
). However, presence or absence of trichomes is only relevant in the mature fruit. The endocarp of all three sections of subgenus Quercus is pubescent until the final stages of acorn maturation. The endocarp pubescence of section Lobatae ranges from usually very pubescent to rarely patchy at maturity (see Fig. 4), and can be patchy in section Protobalanus (Nixon, 1984
, 1997
; Landrum, 1993
). The endocarp pubescence of section Quercus can also appear patchy when the seed is removed, but in most cases, the "glabrous" endocarp of section Quercus is actually the inside of the seed coat that detaches from the embryo at maturity and becomes attached to the fruit wall (see Fig. 3). If the seed coat is peeled from the endocarp, trichomes are still visible on the endocarp (Nixon, 1984
, 1997
). Although Q. hiholensis has trichomes present with no fusion of seed coat and fruit wall in all specimens studied, none of the fruits are completely mature, so the significance of these characters in the fossils is unclear.
The embryo axis can also be used as a taxonomic character. In sections Lobatae and Protobalanus, the shoot apex lacks leaf primordia until after germination, but the embryo of section Quercus can possess one to a few whorls of leaf primordia while still in the seed (Mogensen, 1965
; Sutton and Mogensen, 1970
). In the few fossil specimens of Q. hiholensis that contain suitably preserved embryo axes, the shoot apex is out of the plane of section (Figs. 37–38), so this character could not be verified.
The final position of the aborted ovules in acorns is a very important taxonomic character in subgenus Quercus. In almost all of section Lobatae, these aborted ovules occur above the seed, attached at the apex of the fruit (see Fig. 4). A few black oak species have been described with what appears to be basal or lateral abortive ovules (Muller, 1942a
), but whether these are developmentally similar to the white oaks is unknown at this time (Nixon, Cornell University, Ithaca, New York, personal communication, 1998). In section Protobalanus, the aborted ovules are found laterally, while section Quercus has basal abortive ovules (see Fig. 3). These patterns hold in general for the sections of subgenus Quercus, but exceptions are well known (Trelease, 1924
; Muller, 1942a
, b
). The apical abortive ovules in section Lobatae can shift down and appear lateral, while the basal abortive ovules in section Quercus can shift upward and also appear lateral. Although this abortive ovule position character can be misleading if examined superficially, the underlying basis for this character is a more consistent feature that has received little or no attention in the past.
The final position of the aborted ovules for each section of subgenus Quercus is due to fruit wall and umbilical complex development. The term "umbilical complex" is used in this study to indicate the compound structure that vascularizes the developing seed and includes the placenta, the funiculus of the ovule, and the surviving septum (referred to as the columella in Nixon, 1984
, 1993
, 1997
). Because all the ovules begin development on septa that are extensions of the fruit wall, changes that occur in the fruit wall also affect the final position of the abortive ovules and the umbilical complex. In section Lobatae, attachment of the seed occurs at the apex of the fruit, near the apical abortive ovules. The umbilical complex is either part of one of the sclerified septal ridges that groove the cotyledons or one of the thin, papery "strings" along the inside wall of the fruit, and is therefore present from the apex to the base of the fruit. In section Protobalanus, the surviving septum is present on the inside of the fruit wall from the base to the apex of the fruit as a papery string. The position of the umbilical complex and the attachment of the seed to the fruit have yet to be determined for section Protobalanus, but the lateral abortive ovules may provide a clue. In contrast to the previous two sections and all other genera of the family Fagaceae, the seed attachment, abortive ovules, and the umbilical complex for section Quercus are present solely at the base of the fruit (Nixon, 1984
, 1993
). The umbilical complex can appear in longitudinal section as a recurved structure or as a post, and both of these conformations can be seen in Q. hiholensis (Figs. 29, 33–34). An umbilical complex that persists only at the basal portion of the fruit is unique to subgenus Quercus, section Quercus, and emphasizes the affinity of these fossils that were preserved over 15 million years ago to extant Quercus.
Interesting evidence of predation exists in many of the Q. hiholensis acorns. The cotyledonary tissues are disrupted by what appears to be cavities or channels containing foreign material. Figure 5 shows an oblong structure indicated by an arrow within a cavity at the base of the seed that resembles an insect larva. Cotyledonary tissue is missing, and there appears to be frass (insect excrement) in the cavity and the surrounding tissue. In a second example, an unusual circular object is found within the seed that is not a normal developmental feature of oak cotyledons (Fig. 36, at arrow). This circular structure may represent a larval body or the cavity it formed in a cross-sectional view. Several other seeds in the collection (not illustrated) appear to have been consumed entirely, for the seed cavity is completely filled with insect remains and/or frass. This suggests that plant–animal interactions among oaks and their predators in the Miocene were similar to those found today.
|
CONCLUSIONS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
; Nixon, 1993
). Leaves attributed to Quercus from Eocene strata such as those in the Republic flora may provide earlier evidence for Quercus, but need to be re-evaluated (Gandolfo, 1996
). The leaf floras (Trelease, 1918
; Knowlton, 1926
; MacGinitie, 1941
, 1962
, 1969
; Lakhanpal, 1958
; Chaney and Axelrod, 1959
; Wolfe, 1980
; Crepet, 1981
; Axelrod, 1983
; Manchester and Meyer, 1987
; Axelrod and Schorn, 1994
), fruit and seed floras (Manchester, 1994
), petrified woods (Beck, 1945
, 1955
; Prakash and Barghoorn, 1961a
, b
; Prakash, 1968
) and pollen record (e.g., Elsik, 1978
) of the Tertiary show that the distribution and abundance of the genus Quercus changed dramatically during the Eocene–Oligocene transition in North America. The cooler, drier, and more variable climates that developed in the Oligocene are believed to have encouraged the evolution and migration of the oaks. The stabilization into the modern sections that are present today in North America occurred during this time (Wolfe, 1980
; Daghlian and Crepet, 1983
). By the Middle Miocene, the Quercus fossil taxa that are comparable to eastern North American and Asian Quercus species (in addition to their many associated taxa) are absent from western North America, while the diversification and radiation of the lobed-leaved oaks had accelerated throughout the Northern Hemisphere (Knowlton, 1926
; Berry, 1929
; Brown, 1936
; Chaney and Axelrod, 1959
; Smiley, 1963
; Raven and Axelrod, 1974
; Axelrod, 1983
; Axelrod and Schorn, 1994
; Wehr, 1995
).
Quercus hiholensis demonstrates a suite of features that places it in the genus Quercus, subgenus Quercus, section Quercus, and shows that these unique characters, thought to be highly derived within the Fagaceae (Forman, 1966
; Daghlian and Crepet, 1983
; Nixon, 1984
, 1993
) are present in the Middle Miocene of western North America. Quercus hiholensis has several morphological features that are correlated with features present in extant species that exhibit annual-fruiting habits in subgenus Quercus, such as the reduced perianth and basal abortive ovules. The annual fruiting habit may have been a significant ecological factor in the successful radiation of the white oaks in the Neogene. The level of predation on acorns is another important ecological factor for Quercus, and evidence of damage on these Miocene acorns, which appears similar to patterns seen today, suggests that present plant–animal interactions were occurring in the Neogene. Supplementing well-known wood and leaf floras, Q. hiholensis represents a third independent confirmation based on anatomical, morphological, developmental, and ecological evidence that the white oaks, section Quercus, were well established in western North America by the Middle Miocene.
|
FOOTNOTES |
|---|
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDESCRIPTIONDISCUSSIONCONCLUSIONSREFERENCES |
|---|
Axelrod, D. I. 1964 The Miocene Trapper Creek Flora of southern Idaho. University of California Publications in Geological Science 51: 1–181.
———. 1966 The Eocene Copper Basin flora of northeastern Nevada. University of California Publications in Geological Science 59: 1–125.
———. 1983 Biogeography of oaks in the Arcto-Tertiary Province. Annals of the Missouri Botanical Garden 70: 629–657.
[ISI]
———. 1991 The Early Miocene Buffalo Canyon Flora of Western Nevada. University of California Publications in Geological Science 135: 1–76.
———. 1992 The Middle Miocene Pyramid Flora of Western Nevada. University of California Publications in Geological Science 137: 1–50.
———, and H. Schorn. 1994 The 15 Ma floristic crisis at Gillam Spring, Washoe County, northwestern Nevada. PaleoBios 16: 1–10.
Beck, G. F. 1945 Ancient forest trees of the sagebrush area in central Washington. Journal of Forestry 43: 334–338.
———. 1955 Fossil wood of the Far West. Walnut and oak-like woods of the Russell Forests. Northwest Mineral News October–November: 16–19.
Berridge, E. M. 1914 The structure of the flower of Fagaceae, and its bearing on the affinities of the group. Annals of Botany 28: 509–526.
Berry, E. W. 1929 A revision of the flora of the Latah formation. U.S. Geological Survey Professional Paper 140: 1–81.
———. 1931 A Miocene flora from Grand Coulee, Washington. U.S. Geological Survey Professional Paper 170-C: 31–42.
———. 1934 Miocene plants from Idaho. U.S. Geological Survey Professional Paper 185-E: 97–125.
Borgardt, S. J., and K. B. Pigg. 1994 Anatomically preserved Miocene plants from Yakima Canyon, Washington. American Journal of Botany 81 (supplement 6): 100 (Abstract).
———, and ———. 1996 Petrified acorns from the Miocene of North America and their significance to the evolution of Quercus L. (Fagaceae). Abstract Volume: Fifth Quadrennial Conference of the International Organisation of Palaeobotany 11 (Abstract).
Boyd, A. E. 1985 A Miocene flora from the Oviatt Creek Basin, Clearwater County, Idaho. Master's thesis, University of Idaho, Moscow, ID.
Brett, D. W. 1963 The inflorescence of Fagus and Castanea, and the evolution of the cupules of the Fagaceae. New Phytologist 63: 96–118.
Brooks, B. W. 1935 Fossil plants from Sucker Creek, Idaho. Annals of the Carnegie Museum 24: 275–336.
Brown, R. C. 1971 The developmental anatomy of the abortive and young functional embryo in Quercus gambelii Nutt. Master's thesis, Northern Arizona University, Flagstaff, AZ.
———, and H. L. Mogensen. 1972 Late ovule and early embryo development in Quercus gambelii. American Journal of Botany 59: 311–316.
[ISI]
Brown, R. W. 1936 Additions to some fossil floras of the western United States. U.S. Geological Survey Professional Paper 186J: 163–206.
Camus, A. 1934–1954 Les chênes. Monographie du Genre Quercus (et Lithocarpus). Encyclopédie Économique de Sylviculture, vols. 6–8. Académie des Sciences, Paris.
Chaney, R. W. 1920 The Flora of Eagle Creek formation. Contributions to the Walker Museum, vol. 2, 5: 115–181.
———. 1927 Geology and palaeontology of the Crooked River Basin, with special reference to the Bridge Creek flora. Carnegie Institution of Washington Publication 346: 45–138.
———, and D. I. Axelrod. 1959 Miocene floras of the Columbia Plateau. Carnegie Institution of Washington Publication 617: 1–231.
Condit, C. 1944 The Remington Hill Flora Carnegie Institution of Washington Publication 553: 21–55.
Crepet, W. L. 1981 The status of certain families of the Amentiferae during the Middle Eocene and some hypotheses regarding the evolution of wind pollination in dicotyledonous angiosperms. In K. J. Niklas [ed.], Paleobotany, paleoecology, and evolution, vol. 1, 103–128. Praeger Scientific, New York, NY.
———. 1989 History and implications of the early North American fossil record of Fagaceae. In P. R. Crane and S. R. Blackmore [eds.], Evolution, systematics, and fossil history of the Hamamelidae, vol. 2, `Higher' Hamamelidae. Systematic Association Special Volume Number 40B, 45–66. Clarendon, Oxford.
———, and K. C. Nixon. 1989a Earliest megafossil evidence of Fagaceae: phylogenetic and biogeographic implications. American Journal of Botany 76: 842–855.
[ISI]
———, and ———. 1989b Extinct transitional Fagaceae from the Oligocene and their phylogenetic implication. American Journal of Botany 76: 1493–1505.
[ISI]
Daghlian, C. P., and W. L. Crepet. 1983 Oak catkins, leaves and fruits from the Oligocene Catahoula Formation and their evolutionary significance. American Journal of Botany 70: 639–649.
[ISI]
Elsik, W. L. 1978 Palynology of Gulf Coast lignites: the stratigraphic framework and depositional environments. In W. R. Kaiser [ed.], Proceedings of the Gulf Coast lignite conference: geology, utilization and environmental aspects. University of Texas Bureau of Economy Geological Report Investigation 90: 21–32.
Endress, P. K. 1977 Evolutionary trends in the Hamamelidales-Fagales-Group. Plant Systematics Evolutionary Supplement 1: 321–347.
Fey, B. S., and P. K. Endress. 1983 Development and morphological interpretation of the cupule in Fagaceae. Flora 173: 451–468.
[ISI]
Fields, P. F. 1983 A review of the Miocene stratigraphy of southwestern Idaho, with emphasis on the Payette formation and associated floras. Master's thesis, University of California, Berkeley, CA.
———. 1990 A Quercus simulata with attached acorns! American Journal of Botany 77 (supplement 6): 218 (Abstract).
———. 1996 The Succor Creek flora of the Middle Miocene Sucker Formation, southwestern Idaho and eastern Oregon; systematics and paleoecology. Ph.D. dissertation, Michigan State University, East Lansing, MI.
Forman, L. L. 1966 On the evolution of cupules in the Fagaceae. Kew Bulletin 18(3): 385–419.
Gandolfo, M. 1996 The presence of Fagaceae (Oak Family) in sediments of the Klondike Mountain Formation (Middle Eocene), Republic, Washington. Washington Geology 24: 20–21.
Graham, A. K. 1963 Systematic revision of the Sucker Creek and Trout Creek Miocene floras of southeastern Oregon. American Journal of Botany 50: 921–936.
[ISI]
———. 1965 The Succor Creek and Trout Creek Miocene floras of southeastern Oregon. Kent University Bulletin (Research Series IX) 53: 9–147.
Gregor, H. J. 1977 Sutopische Elemente in europaischen Tertiar II (Fruktifikationen). Palaeontologische Zeitschrift 51: 199–226.
Hill, R. S., and G. J. Jordan. 1993 The evolutionary history of Nothofagus (Nothofagaceae). Australian Systematic Botany 6: 111–126.
Hjelmqvist, H. 1953 The embryo sac development of Quercus robur L. Phytomorphology 3: 377–384.
[ISI]
Jones, J. J. 1986 Evolution of the Fagaceae: the implication of foliar features. Annals of the Missouri Botanical Garden 73: 228–275.
[ISI]
Kaul, R. B. 1985 Reproductive morphology of Quercus (Fagaceae). American Journal of Botany 72: 1962–1977.
[ISI]
———. 1987 Reproductive structure of Lithocarpus sensu lato (Fagaceae): cymules and fruits. Journal of the Arnold Arboretum 68: 73–104.
[ISI]
———. 1988 Cupular structure in paleotropical Castanopsis (Fagaceae). Annals of the Missouri Botanical Garden 75: 1480–1498.
[ISI]
Kearney, T. H., R. H. Peebles, and Collaborators. 1960 Arizona Flora. University of California Press, Berkeley, CA.
Knowlton, F. H. 1898 The fossil plants of the Payette formation. U.S. Geological Survey Eighteenth Annual Report part 3: 721–744.
———. 1926 Flora of the Latah formation of Spokane, Washington, and Coeur D'Alene, Idaho. U.S. Geological Survey Professional Paper 140A: 17–39.
Kuprianova, L. A. 1962 Palynological data and the systematics of the Fagales and Urticales [translated from Russian by J. H. Jones]. In Soviet Reports from the First International Palynological Conference, 17–25. U.S.S.R. Academy of Science, Moscow.
Lakhanpal, R. N. 1958 The Rujada flora of west central Oregon. University of California Publications in Geological Science 35: 1–66.
LaMotte, R. S. 1952 Catalogue of Cenozoic plants of North America through 1950. Memoirs of the Geological Society of America 51: 1—381.
Landon, R. D., and P. E. Long. 1989 Detailed stratigraphy of the N2 Grande Ronde Basalt, Columbia River Basalt Group, in the central Columbia Plateau. In S. P. Reidel and P. R. Hooper [eds.], Volcanism and tectonism in the Columbia River flood-basalt province. Geological Society of America Special Paper 239, 55–66. Boulder, CO.
Landrum, L. R. 1993 Vascular plants of Arizona: Fagaceae. Journal of the Arizona-Nevada Academy of Science 27: 203–214.
Lawrence, G. H. M. 1951 Taxonomy of vascular plants. MacMillan, New York, NY.
Long, P. E., and R. A. Duncan. 1982 Ar/Ar ages of the Columbia River basalt from deep bore holes in south-central Washington. Proceedings of the 33rd Alaska Science Conference: 119.
MacGinitie, H. D. 1933 The Trout Creek flora of Southeastern Oregon. Carnegie Institution of Washington Publication 416 II: 21–68.
———. 1941 A Middle Eocene flora from the central Sierra Nevada. Carnegie Institution of Washington Publication 534: 1–178.
———. 1962 The Kilgore flora: a Late Miocene Flora from northern Nebraska. University of California Publications in Geological Science 35: 67–158.
———. 1969 The Eocene Green River flora of northwestern Colorado and northeastern Utah. University of California Publications in Geological Science 83: 1–203.
Manchester, S. R. 1994 Fruits and seeds of the Middle Eocene Nut Beds Flora, Clarno Formation, Oregon. Palaeontographica Americana 58: 1–205.
———, and H. W. Meyer. 1987 Oligocene fossil plants of the John Day Formation, Fossil, Oregon. Oregon Geology 49: 115–127.
Manos, P. S., and K. P. Steele. 1997 Phylogenetic analyses of "higher" Hamamelididae based on plastid sequence data. American Journal of Botany 84: 1407–1419.
[ISI]
Miller, C. N., Jr. 1982 Osmunda wehrii, a new species based on petrified rhizomes from the Miocene of Washington. American Journal of Botany 69: 116–121.
[ISI]
———. 1992 Silicified Pinus remains from the Miocene of Washington. American Journal of Botany 79: 754–769.
[ISI]
Mogensen, H. L. 1965 A contribution to the anatomical development of the acorn in Quercus L. Iowa State Journal of Science 40: 221–255.
———. 1972 Fine structure and composition of the egg apparatus before and after fertilization in Quercus gambelii: the functional ovule. American Journal of Botany 59: 931–941.
[ISI]
———. 1975a Fine structure of the unfertilized, abortive egg apparatus in Quercus gambelii. Phytomorphology 25: 19–30.
[ISI]
———. 1975b Ovule abortion in Quercus (Fagaceae). American Journal of Botany 62: 160–165.
[ISI]
Muller, C. H. 1942a The Central American species of Quercus. U.S. Department of Agriculture Miscellaneous Publications 477, 1–95.
———. 1942b The problem of genera and subgenera in the oaks. Chronica Botanica 7: 2–14.
Newberry, J. S. 1898 The later extinct floras of North America. Monographs of the U.S. Geological Survey 35: 1–295.
Niklas, K. J., and D. E. Giannasi. 1978 Angiosperm paleobiochemistry of the Succor Creek flora (Miocene) Oregon, USA. American Journal of Botany 65: 943–952.
[ISI]
Nixon, K. C. 1982 In support of recognition of the family Nothofagaceae Kuprianova. Botanical Society of America Miscellaneous Publications 169: 102 (Abstract).
———. 1984 A biosystematic study of Quercus series Virentes (the live oaks) with phylogenetic analyses of Fagales, Fagaceae and Quercus. Ph. D. dissertation, University of Texas, Austin, TX.
———. 1989 Origins of Fagaceae. In P. R. Crane and S. R. Blackmore [eds.], Evolution, systematics, and fossil history of the Hamamelidae, vol. 2, `Higher' Hamamelidae. Systematic Association Special Volume Number 40B, 23–43. Clarendon, Oxford.
———. 1993 Infrageneric class of Quercus (Fagaceae) and typification of sectional names. Annales de Sciences Forestieres 50 (supplement 1): 255–345.
———. 1997 Fagaceae. In Flora of North America Editorial Committee [ed.], Flora of North America north of Mexico 3, 436–506. Oxford University Press, New York, NY.
Ørsted, A. S. 1871 Bidrag til Kundshab om Egefamilien i Fortid og Nutid. Kongelige Danske Videnskabernes Selskabs Skrifter 9: 331–538.
Pigg, K. B. 1997 Anatomically preserved Liquidamber-like infructescences (Hamamelidaceae) from the Middle Miocene Yakima Canyon flora of Washington, USA. American Journal of Botany 84 (supplement 6): 140 (Abstract).
———, J. Sophy, and W. C. Wehr. 1996 Petrified Miocene flora from Yakima Canyon, Washington, USA. Abstract Volume: Fifth Quadrennial Conference of the International Organisation of Palaeobotany 80 (Abstract).
Prakash, U. 1968 Miocene fossil woods from the Columbia basalts of central Washington, III. Palaeontographica 122: 183–200.
———, and E. S. Barghoorn. 1961a Miocene Fossil Woods from the Columbia basalts of central Washington. Journal of the Arnold Arboretum 42: 165–195.
———, and ———. 1961b Miocene Fossil Woods from the Columbia basalts of central Washington, II. Journal of the Arnold Arboretum 42: 347–362.
Raven, P. H., and D. I. Axelrod. 1974 Angiosperm biogeography and past continental movements. Annals of the Missouri Botanical Garden 61: 539–673.
[ISI]
Rebuck, A. L. 1952 An ontogenetic study of the pistillate flower and inflorescence of Quercus alba. Master's thesis, Pennsylvania State College, State College, PA.
Reidel, S. P., T. L. Tolan, P. R. Hooper, M. H. Beeson, K. R. Fecht, R. D. Bently, and J. L. Anderson. 1989 The Grande Ronde basalt, Columbia River Basalt Group; Stratigraphic descriptions and correlations in Washington, Oregon, and Idaho. In S. P. Reidel and P. R. Hooper [eds.], Volcanism and tectonism in the Columbia River flood-basalt province. Geological Society of America, Special Paper 239, 21–53. Boulder, CO.
Romero, E. J. 1986 Fossil evidence regarding the evolution of Nothofagus Blume. Annals of the Missouri Botanical Garden 73: 276–283.
[ISI]
Rothwell, G. W., A. E. Arnone, and K. B. Pigg. 1996 Miocene ferns from central Washington state: anatomy and systematics. American Journal of Botany 83: (supplement 6): 131 (Abstract).
Rozefelds, A. C., and A. N. Drinnan. 1997 Pistillate inflorescence architecture and morphology of the southern beeches (Nothofagus). American Journal of Botany 84 (supplement 6): 156 (Abstract).
Sattler, R. 1973 The organogenesis of flowers. University of Toronto Press, Toronto.
Schwarz, O. 1936 Entwurf zu einen Naturlichen System der Cupuliferen und der Gattung Quercus L. Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem 8: 1–22.
Scott, R. A., E. S. Barghoorn, and U. Prakash. 1962 Wood of Ginkgo in the Tertiary of western North America. American Journal of Botany 49: 1095–1101.
[ISI]
Sharp, W. M., and H. H. Chisman. 1961 Flowering and fruiting in the white oaks. I. Staminate flowering through pollen dispersal. Ecology 42: 365–372.
[ISI]
———, and V. G. Sprague. 1967 Flowering and fruiting in the white oaks. Pistillate flowering, acorn development. weather and yields. Ecology 48: 243–251.
[ISI]
Smiley, C. J. 1963 The Ellensburg Flora of Washington. University of California Publications in Geological Science 35: 159–275.
———, and W. C. Rember. 1985 Composition of the Miocene Clarkia Flora. In C. J. Smiley, A. E. Leviton, and M. Berson [eds.], Late Cenozoic History of the Pacific Northwest: Interdisciplinary Studies on the Clarkia Fossil Beds of Northern Idaho, 95-112. Pacific Division of the American Association for the Advancement of Science, San Francisco, CA.
Smith, H. V. 1939 Additions to the fossil flora of Sucker Creek, Oregon. Michigan Academy of Science Arts and Letters 24: 107–120.
Soepadmo, E. 1968 A revision of the genus Quercus. Gardens' Bulletin (Singapore) 22: 355–428.
———. 1972 Fagaceae. In C. G. G. J. Van Steenis [ed.], Flora Malesiana, Series I, 7, 265–403. P. Noordhoff, Leyden.
Stairs, G. R. 1964 Microsporogenesis and embryogenesis in Quercus. Botanical Gazette 125: 115–121.
Sutton, D. D. and H. L. Mogenson. 1970 Systematic implications of leaf primordia in the mature embryo of Quercus. Phytomorphology 20: 88–91.
[ISI]
Swanson, D. A., T. L. Wright, P. R. Hooper, and R. D. Bently. 1979 Revisions in stratigraphic nomenclature of the Columbia River Basalt Group. United States Geological Survey Bulletin 1457-G, Contributions to Stratigraphy. United States Government Printing Office, Washington.
Szafer, W. 1954 Pliocene flora from the vicinity of Czorsztyn (West Carpathians) and its relationship to the Pleistocene. Instytut Geologiczny (Warszawa, Poland). Prace 11: 183–234.
Taylor, T. N., and E. L. Taylor. 1993 The biology and evolution of fossil plants. Prentice Hall, Englewood Cliffs, NJ.
Tillson, A. H., and C. H. Muller. 1942 Anatomical and taxonomic approaches to subgeneric segregation in American Quercus. American Journal of Botany 29: 523–529.
Tolan, T. L., S. P. Reidel, M. H. Beeson, J. L. Anderson, K. R. Fecht, and D. A. Swanson. 1989 Revisions to the estimates of the area extent and volume of the Columbia River Basalt Group. In S. P. Reidel and P. R. Hooper [eds.], Volcanism and tectonism in the Columbia River flood-basalt province. Geological Society of America, Special Paper 239, 1–20. Boulder, CO.
Trelease, W. 1918 The ancient oaks of America. Memoirs of the Brooklyn Botanical Garden 1: 492–501.
———. 1924 The American oaks. Memoirs of the National Academy of Sciences 20: 1–255.
Tucker, J. M. 1980 Taxonomy of California oaks. In T. R. Plumb [technical coordinator], Proceedings of the Symposium on the Ecology, Management and Utilization of California Oaks, June 26–28, Claremont, California. General Technical Report PSW-44, 19–29. Pacific Southwest Forestry and Range Experimental Station, Berkeley, CA.
Turkel, H. S. 1950 An ontogenetic study of the inflorescences of Quercus alba to the time of pollination. Master's thesis, Pennsylvania State College, State College, PA.
Voss, V. G., H. M. Burdet, W. G. Chalomer, V. Demoulin, P. Hiepko, J. McNiell, R. D. Meikle, D. H. Nicolson, R. C. Rollins, and P. C. Silva [eds.]. 1983 International Code of Botanical Nomenclature adopted by the Thirteenth International Botanical Congress, Syndey. August 1981. Dr. W. Junk, Boston, MA.
Wehr, W. C. 1995 Early Tertiary flowers, fruits, and seeds of Washington state and adjacent areas. Washington Geology 23: 3–16.
Wolfe, J. A. 1960 Early Miocene Floras of Northwest Oregon. Ph.D. dissertation, University of California, Berkeley, CA.
———. 1964 Miocene floras from Fingerrock Wash, southwestern Nevada. U.S. Geological Survey Professional Paper 454N: 1–36.
———. 1980 Neogene history of the California oaks. In T. R. Plumb [technical coordinator], Proceedings of the Symposium on the Ecology, Management and Utilization of California Oaks, June 26–28, Claremont, California. General Technical Report PSW-44, 3–6. Pacific Southwest Forestry and Range Experimental Station, Berkeley, CA.
Abstract of this Article
Reprint (PDF) Version of this Article
Similar articles found in:
American Journal of Botany Online
ISI Web of Science
PubMed
PubMed Citation
Search Medline for articles by:
Borgardt, S. J.
||
Pigg, K. B.
Search for citing articles in:
ISI Web of Science (1)
Search Agricola for articles by:
Borgardt S. J.
||
Pigg K. B.
Download to Citation Manager
HOME
HELP
FEEDBACK
SUBSCRIPTIONS
ARCHIVE
SEARCH
TABLE OF CONTENTS
