American Journal of Botany 91(3): 499±509. 2004. ANATOMICALLY PRESERVED LIQUIDAMBAR (ALTINGIACEAE) FROM THE MIDDLE MIOCENE OF YAKIMA CANYON,WASHINGTON STATE, USA, AND ITS BIOGEOGRAPHIC IMPLICATIONS1 KATHLEEN B. PIGG,2 STEFANIE M. ICKERT-BOND,2,5 AND JUN WEN3,4 2SOLS Faculty & Admin, Arizona State University, Box 874501, Tempe, Arizona 85287-4501 USA; 3Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, Illinois 60605 USA; and 4Laboratory of Systematic and Evolutionary Botany & Herbarium, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, China Liquidambar changii Pigg, Ickert-Bond & Wen sp. nov. (Altingiaceae) is established for anatomically preserved, middle Miocene infructescences from Yakima Canyon, Washington, USA. Specimens are spherical, ;2.5 cm in diameter, and have ;25±30 tightly packed, bilocular fruits per head. Fruits are 3.4±4.7 mm wide 3 2.6±3.5 mm long and wedge shaped, fused at the base, and free distally. Each locule contains 1±2 mature, elongate seeds proximally and 5±9 aborted seeds of more irregular shape distally. Mature seeds are 1.5 mm long 3 1.2 mm wide, elongate, and triangular transversely, with a slight ¯ange. Seeds have a seed coat for which three zones can be well de®ned, a uniseriate outer palisade layer, a middle region of isodiametric cells comprising most of the integument, and a uniseriate inner layer of tangentially elongate cells lining the embryo cavity. Liquidambar changii is most similar to the eastern Asian L. acalycina H.-T. Chang on features of infructescence, fruit, and seed morphology and quite unlike the North American L. styraci¯ua L. and other species. Such a close relationship between these two species supports a Beringian biogeographic track between eastern Asia and western North America during the Miocene. Previous phylogenetic and allozyme analysis of modern Liquidambar demonstrates a close relationship between North American-western Asian taxa and suggests a North Atlantic biogeo- graphic track in the middle Miocene. Together, these biogeographic tracks underscore the complexity of the biogeographic history of the Altingiaceae in the Northern Hemisphere throughout the Neogene. Key words: Altingia; Altingiaceae; biogeography; fossil fruit; infructescence; Liquidambar; Miocene; silici®cation. The Altingiaceae Lindl. consist of three genera (Liquidam- ico to Honduras are sometimes recognized as L. styraci¯ua bar L., Altingia Noronha, and Semiliquidambar H.-T. Chang) var. mexicana Oerst. and L. macrophylla Oerst. (Ernst, 1963; and ;15 species that have an intercontinental disjunct distri- Ferguson, 1989; Zhang et al., 2003). Altingia and Semiliqui- bution in eastern and western Asia and North and Central dambar, exclusively eastern Asian in distribution, have ap- America (Ferguson, 1989; Wen, 1999). Today, Liquidambar proximately eight and three species, respectively (Ferguson, (the sweet gum) is comprised of around ®ve species with two 1989; Zhang et al., 2003), although revisions of these genera occurring in eastern Asia (L. acalycina H.-T. Chang and L. are needed (Endress, 1993). Liquidambar has been distin- formosana Hance), one in western Asia (L. orientalis Mill.), guished from Altingia based on a combination of vegetative, and one in eastern North America extending into central Mex- particularly leaf features, as well as reproductive characters. ico and further into Central America (L. styraci¯ua L.). Mor- Whereas Liquidambar leaves are typically deciduous and pal- phological variants similar to L. styraci¯ua occurring in Mex- mately 3±7 lobed with actinodromous venation, those of Al- tingia are evergreen, commonly obovate and entire with pin- 1 Manuscript received 30 June 2003; revision accepted 30 October 2003. nate venation. Semiliquidambar shows an intermediate mor- The authors thank Wesley C. Wehr (Burke Museum of Natural History and phology between the two other genera and has been suggested Culture, University of Washington, Seattle, Washington), Raymond D. Foisy to possibly represent an intergeneric hybrid (Bogle, 1986). (Yakima, Washington), Walter L. Friedrich (University of Aarhus, Aarhus, With respect to infructescence characters, those of Liquidam- Denmark), Zlatko KvacÏek, (Charles University, Prague, Czech Republic), Ed- bar tend to have been interpreted to have fruits with septicidal uardo Martinetto (University of Turin, Turin, Italy), and William C. Rember (Idaho State University, Moscow, Idaho) for providing specimens for study; dehiscence and persistent styles while in Altingia both septi- Johanna Eder (Natural History Museum, Vienna, Austria), Barbara Ertter, (UC cidal and loculicidal dehiscence are reported, and styles are & JEPS, Berkeley, California), Else Marie Friis (Swedish Museum of Natural typically deciduous. Features of Semiliquidambar are inter- History, Stockholm, Sweden), and Jiri KvacÏek (The National Museum, mediate. Prague, Czech Republic) for providing access to fossils and herbarium spec- Historically, these genera have comprised a subfamily of the imens; A. Linn Bogle (NHA), Charlotte M. Christy (Augusta College, Au- Hamamelidaceae, recognized as either the Liquidambaroideae gusta, Georgia), Donald J. Pinkava (ASU), Suhua Shi (SYS), and Emily Wood (GH) for providing comparative living anatomical material; Maria Tcherepova or the Altingioideae on the basis of traditional taxonomic char- for Russian translation; and A. Linn Bogle, Melanie L. DeVore, Steven R. acters including morphology and biochemistry (Harms, 1930; Manchester, Wesley C. Wehr, and an anonymous reviewer for their helpful Chang, 1979; Bogle, 1986; Endress, 1989a, b; Ferguson, 1989; comments on the manuscript. This study was funded by National Science Qui et al., 1998; Zhang et al., 2003). The most recent phylog- Foundation EAR-9980388, and an International Travel Grant and a Minigrant, enies based on combined morphological and molecular data College of Liberal Arts and Sciences, Arizona State University (K. B. P.) and National Science Foundation DEB-0108536 (J. W.). place this group within the order Saxifragales of the rosid 5 Current address: Field Museum of Natural History, 1400 S. Lake Shore clade of core eudicots (MagalloÂn et al., 1999; Judd et al., Drive, Chicago, Illinois 60605 USA. E-mail: sbond@®eldmuseum.org. 2002). 499 500 AMERICAN JOURNAL OF BOTANY [Vol. 91 Within the genus Liquidambar, two sections have been tra- ey, 1991). Altingiaceae fruits dehisce to release seeds, while ditionally delimited on the basis of fruiting head ornamenta- platanaceous carpels develop into single-seeded achenes that tion (Harms, 1930; Chang, 1979). Sect. Cathayambar Harms are dispersed. Sparganium infructesences bear single-seeded (one species, L. formosana) is characterized by the presence drupaceous fruits (Manchester, 1986). of elongate structures (``Borsten'' or ``setae'' of Harms, 1930) Although Liquidambar compressed leaf and infructescence positioned between fruits while in sect. Liquidambar (4±5 spe- remains are widespread in the Northern Hemisphere during the cies) comparable structures are either lacking or inconspicu- Neogene, until recently there has been little pre-Tertiary record ous. Species of sect. Liquidambar are distinguished from one of this group. The earliest fossil reproductive structures as- another by additional features of infructescence morphology signed to the family are in¯orescences from the Late Turonian including thickness and ornamentation of the outer hypanthial (Late Cretaceous) Lower Magothy Formation of New Jersey tissues that comprise the areas between adjacent fruits, result- (Zhou et al., 2001) and the Late Santonian (Late Cretaceous) ing in a honeycomb-like appearance, which is sometimes Allon ¯ora of central Georgia (Herendeen et al., 1999). These called the ``peripheral rim'' (Gregor, 1978 p. 34±35; Ferguson, tiny spherical heads are 1.6±7.0 mm in diameter, each with 1989). Recent phylogenetic analyses (Li et al., 1997, 1999), ;20 apetalous ¯orets. Each ¯oret is bilocular, with carpels that however, do not support this traditional classi®cation. The are fused basally and free distally. There are numerous ovules main distinguishing character of the two sections, the presence per carpel and phyllophores surrounding the gynoecia. Zhou of elongate structures, is thus an autapomorphy for L. formo- et al. (2001) interpret the stratigraphically older of these, Mi- sana. Liquidambar formosana of sect. Cathayambar is most croaltingia Zhou, Crepet & Nixon, as most similar to the Al- closely related to L. acalycina of sect. Liquidambar. Isozyme tingiaceae; however, these fossils have a mosaic of characters studies of Liquidambar (Hoey and Parks, 1991, 1994) showed including tricolpate rather than polyporate pollen typical of that the genetic similarity of extant forms is greater between Altingiaceae. eastern North American L. styraci¯ua and western Asian L. A Paleocene fruit with possible altingioid af®nities, Eva- orientalis than it is between eastern North American and east- carpa polysperma Maslova & Krassilov was described from a ern Asian forms. More recently, DNA molecular phylogenetic compression ¯ora from western Kamchatka (Maslova and studies have con®rmed this same pattern (Li et al., 1997, 1999; Krassilov, 1997). This taxon is based on a single reproductive Shi et al., 1998, 2001; Li and Donoghue, 1999). Today the axis bearing a cluster of pedunculate spherical fruiting heads, center of diversity of the Altingiaceae is eastern Asia, with 4±5 mm in diameter that are composed of approximately 16