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Bisexual from the Coniacian (Late ) of Vancouver Island, Canada: Ambiplatanus washingtonensis gen. et sp. nov. ()

Mindell, R. A., Karafit, S. J., & Stockey, R. A. (2014). Bisexual Flowers from the Coniacian (Late Cretaceous) of Vancouver Island, Canada: Ambiplatanus washingtonensis gen. et sp. nov. (Platanaceae). International Journal of Sciences, 175(6), 651-662. doi:10.1086/676306

10.1086/676306 University of Chicago Press

Version of Record http://cdss.library.oregonstate.edu/sa-termsofuse Int. J. Plant Sci. 175(6):651–662. 2014. ᭧ 2014 by The University of Chicago. All rights reserved. 1058-5893/2014/17506-0002$15.00 DOI: 10.1086/676306

BISEXUAL FLOWERS FROM THE CONIACIAN (LATE CRETACEOUS) OF VANCOUVER ISLAND, CANADA: AMBIPLATANUS WASHINGTONENSIS GEN. ET SP. NOV. (PLATANACEAE)

Randal A. Mindell,* Steven J. Karafit,† and Ruth A. Stockey1,‡

*Department of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada; †Department of Biology, University of Central Arkansas, Conway, Arkansas 72035, USA; and ‡Department of Botany and Plant Pathology, 2082 Cordley Hall, Oregon State University, Corvallis, Oregon 97331, USA

Editor: Patrick S. Herendeen

Premise of research. Anatomically preserved platanaceous inflorescences have been found in rocks of Late Cretaceous (Coniacian) age at the Eden Main locality on Vancouver Island, British Columbia, Canada. Methodology. Specimens occur in calcium carbonate concretions near the base of the Nanaimo Group (Comox Formation) and are studied with the cellulose acetate peel technique and SEM. Pivotal results. Inflorescences are small (!5 mm), pedunculate heads, with fewer than 30 flowers per inflorescence. Both bisexual and unisexual flowers are present on the same inflorescence. Elongate and over- arching tepals enclose the developing and androecium at early stages of development. More mature specimens have individual flowers with at least two whorls of tepals fused toward the base. Flowers have a of five free , each with short filaments and a sclerotic apical connective extension. In situ is small, prolate, tricolpate, 11–13 mm in polar diameter, and 8–9 mm in equatorial diameter. In flowers where it can be observed, the staminal whorl encloses five short, conduplicate, glabrous carpels lacking differentiated styles but bearing broad, flat apices. The ovary of these carpels is occupied by a single . Conclusions. While the Eden Main specimens display a five-parted gynoecial arrangement common in the pistillate flowers of other Cretaceous platanoids, Ambiplatanus washingtonensis gen. et sp. nov. provides the first fossil evidence of functional bisexuality in fossil Platanaceae.

Keywords: Cretaceous, Platanaceae, , .

Introduction 2010; Carpenter et al. 2005), these three families remain dis- parate when interpreted only through extant representatives. The 10 living of Platanaceae show relatively little Fortunately, Platanaceae are an ancient, diverse group with morphological variation when compared to the extensive and an extensive fossil record reaching well into the Early Creta- diverse fossil record for the (Crane 1989; Magallo´n- ceous (Hickey and Doyle 1977; Crane 1989; Friis et al. 2011). Puebla et al. 1997; Maslova 2003, 2010; Nixon and Poole Significant differences in morphology (Hickey and Doyle 2003; Friis et al. 2011; Denk et al. 2012). Living representa- 1977; Maslova 2010), biology (Crane 1989), floral tives are generally united by palinactinodromous , glo- arrangement (Manchester 1986; Magallo´ n-Puebla et al. 1997), bose, unisexual inflorescences that are typically borne on a pollen ultrastructure (Pedersen et al. 1994; Denk and Tekleva peduncle, and mature with a persistent style (Nixon 2006), and dispersal mechanisms (Manchester 1986) have all and Poole 2003). This anomalous suite of characters has lent been revealed by these fossils. Specifically of interest for this itself to various interpretations as to the systematic placement work are numerous specimens from the Cretaceous and Ter- of the family (Griggs 1909; Schwarzwalder and Dilcher 1991; tiary that suggest the presence of bisexual flowers and inflo- Hoot et al. 1999; Hilu et al. 2003). Current interpretations of rescences (Friis 1985; Magallo´ n-Puebla et al. 1997; Mindell the higher- phylogeny based on molecular data place the et al. 2006). Living Platanaceae have predominantly unisexual family as sister to and in the order inflorescences and flowers (Nixon and Poole 2003), although Proteales (APG III 2009; Barniske et al. 2012). Although some rare bisexual inflorescences and flowers are observed (Booth- efforts have been made to find morphological synapomorphies royd 1930; Schwarzwalder and Dilcher 1981; Floyd et al. within this group (Hoot et al. 1999; Doyle and Endress 2000, 1999). Thus, it is expected that the stratigraphic record would preserve bisexual flowers and inflorescences (Mindell et al. 1 Author for correspondence; e-mail: [email protected] 2006). .edu. The Late Cretaceous (Coniacian) Eden Main Quarry locality Manuscript received October 2013; revised manuscript received February 2014; provides three-dimensional, cellular preservation for the study electronically published May 28, 2014. of fossil . Anatomically preserved fossils from this age

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This content downloaded from 128.193.163.187 on Fri, 18 Jul 2014 14:00:01 PM All use subject to JSTOR Terms and Conditions 652 INTERNATIONAL JOURNAL OF PLANT SCIENCES are uncommon (Nishida 1991; Takahashi et al. 1999; Karafit in two alternating cycles overarching gynoecium and androe- and Stockey 2008; Jud et al. 2010), and thus Eden Main offers cium. Stamens five, in single whorl; filaments short; thecae a rare view into the reproductive biology of Mesozoic Platan- elongate, apical connective dome shaped. Pollen prolate, tri- aceae. This article provides the first formal description of an colpate; exine semitectate, reticulate. Carpels five, condupli- angiosperm from the locality and reveals a new genus with cate, wedge shaped in cross section; styles undifferentiated; implications for the evolution of the family. apical platform broad. one per carpel.

Material and Methods Type Species—Ambiplatanus washingtonensis Mindell, Karafit & Stockey sp. nov. (Figs. 1–5) Floral features are preserved in four inflorescences. Three Specific diagnosis. Receptacular head parenchymatous. other inflorescences show only abraded receptacular tissues. Peduncle at least 1.5 mm long. Flowers fewer than 30 per These specimens are anatomically preserved in three dimen- inflorescence; up to 0.5 mm in diameter; unisexual and bisex- sions in calcareous marine concretions collected from the ual flowers present in same inflorescence. Tepal whorls two or quarry at the Eden Main fossil locality (Karafit and Stockey more, extending above gynoecium and androecium. Flowers Њ 2008). The Eden Main quarry (lat. 49 49 52.04 N, long. pentamerous; stamens bithecate; thecae elongate; anther with Њ 125 25 10.41 W, universal transverse Mercator 10N 325999 sclerenchymatous apical connective. Pollen prolate, tricolpate, 5522663) is 35 km northwest of Courtenay, British Columbia, 11–13 mm polar diameter, 8–9 mm equatorial diameter. Carpels Canada (Karafit and Stockey 2008). The concretions are em- glabrous, apices broad, flattened. Styles glabrous. one bedded in a sandstone matrix in the Dunsmuir Member of the seeded. Comox Formation (Nanaimo Group) and are thought to have Holotype, hic designatus. UAPC-ALTA P14460 Ebot, formed in a nearshore marine environment (Mustard 1994; Ftop (figs.1A–1C,2,3,4,5A–5C). Haggart et al. 2003; Johnstone et al. 2006). The locality is Locality. Eden Main Quarry, Vancouver Island, British dated as early Coniacian on the basis of bivalves, gastropods, Columbia, Canada. and ammonites (Haggart et al. 2003, 2005). Fossil decapods Stratigraphic position and age. Comox Formation, Con- have been described from material found at the locality iacian, Late Cretaceous. (Schweitzer et al. 2003, 2009). Mosses, lycophytes, ferns, cy- Etymology. The genus Ambiplatanus is named in recog- cadeoids, conifers, and angiosperms are abundant in the con- nition of the bisexuality of the flowers and inflorescences. The cretions (Karafit 2008; Jud et al. 2010). One species of fertile specific epithet washingtonensis is given in reference to the schizaeaceous fern has been recognized and described (Karafit proximity of Mount Washington to the fossil sites on Van- and Stockey 2008). couver Island, British Columbia, Canada. Concretions bearing plant fossils were cut into serial sections and studied with the cellulose acetate peel technique (Joy et Description al. 1956). Peels were mounted on slides with Eukitt mounting medium (O. Kindler, Freiberg, Germany). Images were cap- Seven inflorescences, three containing flowers and four tured with a Powerphase One scanner (Phase One, Copen- showing only an abraded , are present in the Eden hagen) mounted to a compound microscope and were pro- Main collection. Inflorescences are globose heads, 4–5 mm in cessed with Adobe Photoshop 10.0 (Adobe Systems). Pollen diameter and borne on short peduncles (fig. 1A–1C). Since samples were prepared with a modified Daghlian and Taylor peduncles are abraded, the length of 1.5 mm is a minimum, (1979) technique by dissolving an acetate peel bearing anthers with acetone on filter paper over a 1-mm mesh filter in a Mil- and they might have been longer in life. Fewer than 30 sessile lipore filter, then mounting the filter paper to an SEM stub. flowers are attached to a parenchymatous receptacular head The pollen grains obtained were coated with 15 nm of gold (fig. 1C). Individual flowers, up to 0.5 mm in diameter, are by a Nanotek sputter-coater and examined with a Japan Elec- either unisexual (fig. 2A) or bisexual (fig. 2C,2D), with both tronics Optics (JEOL 6301F) scanning electron microscope types of flowers present on a single inflorescence (fig. 1B,1C). (SEM) at 5 kV. All specimens are housed in the University of At least two whorls of overarching tepals enclose the re- Alberta Paleobotanical Collections, Edmonton, Alberta productive organs early in development (fig. 1D,1E). When (UAPC-ALTA). the inflorescences are abraded, it is difficult to interpret tepal length and extent. However, in the best-preserved specimens, Systematic Description the tepals extend above the level of the stamens and carpels at maturity and are up to 1.25 mm long (figs. 2A,2C,2D, Order—Proteales de Jussieu ex Berchtold & J. Presl 3A,3B). Unisexual flowers bear either carpels or stamens in whorls of five (figs. 1C,1E,3C,5A,5C). Family—Platanaceae T. Lestiboudois Five stamens in a single whorl are bithecate and up to 1.0 mm long, with short filaments and large, sclerenchymatous, Genus—Ambiplatanus Mindell, Karafit & Stockey gen. dome shaped, apical connective extensions up to 230 mmin nov. (Figs. 1–5) width and 380 mm high (fig. 3A–3C). Thecae are elongate, up Generic diagnosis. Inflorescences bisexual, globose, pe- to 400 mm long. Microsporangial walls are 1 cell thick (fig. 3D). dunculate heads, containing fewer than 30 flowers. Flowers Pollen grains are small, prolate, tricolpate, 11–13 mm in polar bisexual, some appearing unisexual; well developed diameter, and 8–9 mm in equatorial diameter (figs. 3D,4A,4C).

This content downloaded from 128.193.163.187 on Fri, 18 Jul 2014 14:00:01 PM All use subject to JSTOR Terms and Conditions Fig. 1 Inflorescence anatomy of Ambiplatanus washingtonensis gen. et sp. nov. A, Longitudinal section showing flowers in inflorescence. Note central receptacular tissue and flower with both stamens and carpels at bottom. Holotype P14460 Ftop 2. Scale bar p 1 mm. B, Longitudinal section through inflorescence, showing peduncle (P) attachment and numerous pentamerous flowers. Holotype P14460 Ebot 2. Scale bar p 1 mm. R p receptacle. C, Section showing flowers in longitudinal (top left) and transverse (center right) view. Note receptacular tissue (R). Holotype P14460 Ebot 3. Scale bar p 0.5 mm. D, Section of immature inflorescence, showing numerous flowers on head. Note overarching tepals. Paratype P14320 Ebot 2b. Scale bar p 0.5 mm. E, Oblique tangential section through flower of immature inflorescence. Note five carpels and whorls of tepals. Paratype P14320 Ebot 25b. Scale bar p 250 mm.

This content downloaded from 128.193.163.187 on Fri, 18 Jul 2014 14:00:01 PM All use subject to JSTOR Terms and Conditions Fig. 2 Anatomy of flowers and inflorescences of Ambiplatanus washingtonensis gen. et sp. nov. A, Longitudinal section through flowers. at left shows carpels. Note ovules (O), undifferentiated styles, and broad stigmatic platform (S). Flower at right shows with apical connective tissue (C). Holotype P14460 Ebot 5. Scale bar p 250 mm. B, Oblique longitudinal section of flower, showing stamens with broad, overarching, apical connectives (C) and light-colored anthers (A) with pollen. Holotype P 14460 Ebot 25. Scale bar p 360 mm. C, Oblique transverse section through single bisexual flower with central whorl of five carpels enclosed by androecium and at least two whorls of tepals. Holotype P14460 Ftop 30. Scale bar p 500 mm. D, Oblique transverse section of flower in C, showing carpels (red), tepals (green), and stamens (blue). P14460 Ebot 5. Scale bar p 500 mm.

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This content downloaded from 128.193.163.187 on Fri, 18 Jul 2014 14:00:01 PM All use subject to JSTOR Terms and Conditions Fig. 3 Androecium anatomy of Ambiplatanus washingtonensis gen. et sp. nov. A, Longitudinal section through single flower, showing stamens with apical connective tissue and elongate anthers. Note apical connective tissue (C), anthers (A), basal carpels (Ca), and elongate tepals at right. Holotype P14460 Ftop 2. Scale bar p 250 mm. B, Transverse section of flower in area of stamens, showing stamens (numbers). Note apical connective tissue (C) and filament (F). Holotype P14460 Ftop 35. Scale bar p 250 mm. C, Slightly oblique transverse section of flower showing five stamens (numbers), three represented by apical connective tissue and two showing anther tissue. Holotype P14460 Ebot 37. Scale bar p 100 mm. D, Transverse section through anther. Note cluster of tricolpate pollen. P14460 Ebot 62. Scale bar p 50 mm.

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Fig. 4 SEM images of Ambiplatanus washingtonensis gen. et sp. nov. pollen. Holotype specimen P14460 Ebot 70. A, Cluster of pollen grains. Scale bar p 2 mm. B, Pollen grain in polar view, showing three colpi and microreticulate ornamentation. Scale bar p 2 mm. C, Pollen grain in equatorial view, showing elongate colpi, prolate shape, and microreticulum. Scale bar p 2 mm. D, Detail of microreticulate exine ornamentation, showing high muri. Scale bar p 200 nm. E, Detail of colpus, showing granular ornamentation. Scale bar p 200 nm. F, Section through pollen wall, showing thick tectum and elongate columellae. Scale bar p 1nm.

The exine is semitectate and reticulate, and the muri are high served to contain a single ovule that in some sections appears (fig. 4). The nexine is up to 240 nm thick, the columellae up to to have a wing-like extension (fig. 5C,5D). It is difficult to 550 nm tall, and the tectum up to 340 nm thick (fig. 4F). determine ovule attachment because of preservation; therefore, Carpels (up to 720 mm long and 240 mm in diameter) are and ovule curvature are currently unknown. glabrous, conduplicate, and triangular in transverse section, Discussion with a very prominent median suture (fig. 5). Styles are un- differentiated, and carpel apices are broad and flattened, pro- These fossils show pentamerous, sessile flowers with a well- viding a broad stigmatic platform (fig. 5A). Carpels are ob- developed perianth, arranged on small, pedunculate, globose

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Fig. 5 Gynoecium anatomy of Ambiplatanus washingtonensis gen. et sp. nov. A, Longitudinal section of carpels (from fig. 2A). Note ovules (O), undifferentiated styles, and broad stigmatic surfaces at top. Holotype P14460 Ebot 5. Scale bar p 250 mm. B, Oblique transverse section of flower (from fig. 2C), showing a single whorl of five carpels. Holotype P14460 Ftop 30. Scale bar p 500 mm. C, Mature carpels/fruits in transverse section. Note deltoid shape and coat remnants at arrow. Holotype P14460 Ebot 62. Scale bar p 500 mm. D, Longitudinal section through mature fruits, showing winged . Paratype P14468 Cbot 74b. Scale bar p 250 mm. heads. Single-seeded carpels have undifferentiated styles and Living Plantanaceae are represented by ∼10 species in the are commonly encircled by an overarching whorl of stamens genus Platanus L. (Nixon and Poole 2003). Platanus, like the with short filaments, a large apical connective extension, and fossil described here, has dome-shaped apical connectives in situ tricolpate, reticulate pollen. These characters clearly above the anthers and can have stalked inflorescences (Nixon place the fossil within the Platanaceae (Boothroyd 1930; Denk and Poole 2003). Furthermore, some species of Platanus have and Tekleva 2006; APG III 2009; von Balthazar and Scho¨- been observed to occasionally bear rudimentary to functionally nenberger 2009; Maslova 2010; Friis et al. 2011). However, bisexual flowers or inflorescences (Boothroyd 1930; Schwarz- the Eden Main heads bear bisexual and possibly unisexual walder and Dilcher 1981; Floyd et al. 1999; von Balthazar flowers (see floral diagrams in fig. 6). This is evidenced by and Scho¨ nenberger 2009). The two mature Eden Main inflo- well-developed in situ pollen co-occurring in the flowers along- rescences show both bisexual and unisexual flowers and differ side mature ovule-bearing carpels and seed-bearing fruits. markedly from extant Platanus in having a well-developed

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Fig. 6 Bisexual flowers and inflorescences of Ambiplatanus washingtonensis gen. et sp. nov. (Platanaceae). A, Floral diagram through basal portion of an individual flower. Note staminal tube uniting androecium and pentamery of floral whorls. B, Floral diagram showing stamens opposite carpels. C, Floral diagram representing distal portions of flower, showing five large masses of apical connective tissues above anthers. D, Inflorescence diagram showing possible arrangement of uniformly bisexual flowers. E, Inflorescence diagram showing alternate possible arrangement of mixed staminate, carpellate, and perfect flowers. overarching perianth, fixed pentamerous organ arrangement, developed (Tschan et al. 2008). A second species, Platanus and short carpels with undifferentiated styles that mature into laevis Velenovsky´ (1882), from the Cretaceous (Cenomanian) glabrous fruits (see table 3 in Tschan et al. 2008; table 2 in of Germany, is described from impression fossils of pistillate Maslova 2010). inflorescences; however, as in specimens of P.quedlinburgensis, Circumscription of the family Platanaceae is best understood details of floral organization are lacking, and it is uncertain through the fossil record, as extant species represent only a whether either of these fossil taxa belong to Platanus or one fraction of the known diversity (Hickey and Doyle 1977; Man- of the extinct genera (Friis et al. 2011). chester 1986; Crane 1989; Magallo´ n-Puebla et al. 1997). It is While the earliest reports of the genus Platanus may be Late thought that the genus Platanus had possibly appeared as early Cretaceous, the earliest known fossils of the family Platanaceae as the Cretaceous, as evidenced by the fossil species Platanus are from the lower Cretaceous (Hickey and Doyle 1977; Friis quedlinburgensis (Pacltova´) Tschan, Denk & von Balthazar et al. 1988, 2011; Crane et al. 1993; Wang et al. 2011) of (Tschan et al. 2008). This taxon is known from compression . The oldest platanaceous inflorescences are rep- fossils of staminate and pistillate inflorescences from the Upper resented by pistillate heads of Friisicarpus brookensis (Friis, Cretaceous (Santonian) of Germany (Pacltova´ 1982; Knobloch Crane, Pedersen & Drinnan) Maslova & Herman (Maslova and Mai 1986). The unisexual inflorescences are stalked but and Herman 2006) and staminate inflorescences of Aquia are ∼10 mm in diameter, making them twice the diameter of brookensis Friis, Crane, Pedersen & Drinnan (Crane et al. the Eden Main fossils (Tschan et al. 2008). The pistillate in- 1993), from mesofossils in sediments of the Patapsco For- florescences of P. quedlinburgensis have long styles, and the mation (middle Albian) of Virginia (Friis et al. 1988, 2011). staminate inflorescences contain prolate to subovate pollen, Species of Friisicarpus Maslova & Herman (pPlatanocarpus while the Eden Main fossils have only prolate pollen that is Friis, Crane & Pedersen [Friis et al. 1988]), like the Eden Main much smaller than that reported in P. quedlinburgensis (Tschan fossils, have five-parted flowers with stout carpels and undif- et al. 2008). Like that of the Eden Main fossils and unlike that ferentiated styles, but they differ in having only unisexual flow- of most extant taxa, the perianth of P. quedlinburgensis is well ers and sessile inflorescences (Friis et al. 1988; Crane et al.

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1993; Wang et al. 2011), rather than bisexual, pedunculate opposed to flowers of Gynoplatananthus, which have only inflorescences, as seen in the Eden Main fossils. rudimentary carpels. Staminate inflorescences with characters similar to those of Manchester (1986) described pistillate from the Eden Main fossil are common in the fossil record. Plata- the of Oregon as Macginicarpa glabra Manchester, nanthus synandrus Manchester has staminate inflorescences which includes flowers with five carpels and elongate, recurved with pentamerous flowers; the five stamens are interconnected styles not unlike those observed in extant Platanus. Another by dome-shaped, apical connective extensions (Manchester species of Macginicarpa, Macginicarpa manchesteri Pigg et 1986). While the type specimen was described from the Eocene Stockey, was reported from the of Alberta, Canada of Oregon, the generic diagnosis was amended to accommo- (Pigg and Stoockey 1991). Like the Eden Main specimens, all date staminate inflorescences of Platananthus hueberi from the species of Macginicarpa lack a tuft of trichomes at the base late Albian of Maryland/Santonian-Campanian of North Car- of the mature fruits, unlike the fruits of extant Platanus (Man- olina and Platananthus scanicus Friis, Crane and Pedersen chester 1986; Pigg and Stockey 1991). However, Macginicarpa from the late Santonian-Campanian of Sweden (Friis et al. differs in having persistent, elongate, recurved styles (Man- 1988). Platananthus speirsiae Pigg & Stockey is known from chester 1986; Pigg and Stockey 1991) instead of the undiffer- staminate inflorescences from the Palaeocene of Canada (Pigg entiated stout carpels seen in the Eden Main fossils. Macgin- and Stockey 1991). Platananthus synandrus, P. hueberi, and icarpa also differs from Ambiplatanus as it has unisexual, P. scanicus are similar to the Eden Main specimens in being pistillate flowers and wingless seeds dispersed as an elongate five-parted with a well-developed perianth and having dome- , although some specimens seem to show some remnant shaped apical connective extensions and small, prolate pollen staminal tissues. with granular aperture sculpture (Friis et al. 1988). All Pla- tananthus species, like all previously described Platanaceae, Bisexuality have unisexual flowers and inflorescences, while the Eden Living Platanus represents a very narrow range of the di- Main specimens have bisexual flowers and inflorescences. versity within the family Platanaceae as it has existed through Quadriplatanus georgianus Magallo´ n-Puebla, Herendeen & time. If familial circumscription was based solely on mor- Crane was described from the Coniacian-Santonian (Upper phology of living species, the Eden Main specimens, along with Cretaceous) sediments of Georgia in the United States. The many other fossil species, would not fit within the limited pistillate flowers in these specimens bear carpels similar to taxonomic boundaries of Platanaceae as deduced using solely those found in the flowers at Eden Main. These lack differ- extant taxa. Specifically, their bisexual flowers, fixed merosity, entiated styles, having broad stigmatic platforms with prom- fruits that lack trichomes, and winged seeds form a unique inent sutures along the length of the carpel (Magallo´ n-Puebla combination of characters. However, the fossil record for the et al. 1997). Furthermore, flowers of Quadriplatanus have eas- family accommodates, or at least suggests, a wide range of ily distinguished , fruits that lack trichomes, and pro- variation in the family during the Cretaceous and early Paleo- late pollen (Magallo´ n-Puebla et al. 1997), as in the specimens gene, including bisexuality, pentamerous flowers, and winged described in this article. Ovules in Quadriplatanus were ob- seeds. Many of these characters recur in numerous fossils of served to have a median longitudinal flap of tissue that was disparate ages (Manchester 1986; Friis et al. 1988; Crane interpreted as either a raphe or a wing (Magallo´ n-Puebla et 1989; Magallo´ n-Puebla et al. 1997; Mindell et al. 2006; al. 1997). Ovules/seeds in the Eden Main specimens also have Tschan et al. 2008). The clear presence and co-occurrence of a crest or wing-like projection in longitudinal section. These these characters within a single inflorescence does not fit any projections could be wings, or they may be a taphonomic ar- known generic diagnosis, extinct or extant. Thus, we have tifact. Like other Cretaceous platanoids, Q. georgianus inflo- designated the specimens Ambiplatanus washingtonensis gen. rescences had flowers with a fixed merosity, but this species et sp. nov. to accommodate the novel suite of inflorescence, differs in being tetramerous. Furthermore, unlike those of the floral, and seed morphologies. Eden Main specimens, the inflorescences of Quadriplatanus were unisexual. It should be noted that an inner whorl of Proteales protruding tissues was found within the staminate flowers of Quadriplatanus. This was interpreted as possibly representing Platanaceae were historically placed among the wind-pol- pistillodes (Magallo´ n-Puebla et al. 1997), as opposed to the linated plants artificially grouped together in Hamamelidae Eden Main flowers, where this whorl is fully developed into (Thorne 1973; Cronquist 1981; Schwarzwalder and Dilcher functional carpels. 1991). Phylogenetic analyses utilizing molecular data have of- Gynoplatananthus oysterbayensis Mindell, Stockey & fered a novel hypothesis placing the family in the order Pro- Beard, based on staminate inflorescences from the Eocene of teales as sister group to Proteaceae in a clade with Nelum- British Columbia, is similar to Platananthus but differs in the bonaceae (Chase et al. 1993; Hoot et al. 1999; Doyle and presence of rudimentary carpels (Mindell et al. 2006). Like the Endress 2000; Hilu et al. 2003; APG III 2009). However, few Eden Main fossils, Gynoplatananthus is five-parted with a morphological synapomorphies have been found in extant rep- well-developed perianth and apical connective extensions resentatives to support this grouping; those that have been (Mindell et al. 2006). Pollen in Gynoplatananthus is larger described include ovule, , and characters (16-mm average polar diameter) and spheroidal, while the pol- (Doyle and Endress 2000), flower merosity (Hoot et al. 1999), len from the Eden Main platanoids is prolate and significantly and cuticular features (Carpenter et al. 2005). The fossil record smaller (11–13 mm in polar diameter). Furthermore, the Eden provides evidence as to the validity of this relationship between Main inflorescences and many of the flowers are bisexual, as such geographically disjunct and morphologically distinct

This content downloaded from 128.193.163.187 on Fri, 18 Jul 2014 14:00:01 PM All use subject to JSTOR Terms and Conditions 660 INTERNATIONAL JOURNAL OF PLANT SCIENCES taxa. Carpel and stamen number is highly variable in the uni- preservation that is sometimes affected by the presence of py- sexual flowers and inflorescences of extant Platanaceae (Nixon rite, probably due to bacterial degradation before preservation. and Poole 2003). This is in contrast to Proteaceae, where bi- Extant Platanus has a ventral suture (Endress and Igersheim sexual flowers typically feature four stamens and one carpel 1999), but the achene functions as the dispersal unit. It appears (Cronquist 1981). In the fossil record, there is abundant evi- that there has been a change in dispersal vectors through time dence of a fixed pentamerous merosity in Platanaceae (Man- that can be proposed in light of the structure seen in Ambi- chester 1986; Friis et al. 1988, 2011; Crane 1989; Crane et platanus and other presumed wind-dispersed seeds in the Cre- al. 1993; Pedersen et al. 1994; Maslova 2003, 2010; Mindell taceous, water-dispersed fruits in the Paleogene, and wind- et al. 2006), with the exception of one taxon having tetram- dispersed fruits in the present, but this requires further erous flowers (Magallo´n-Puebla et al. 1997). Bisexual flowers investigation. also have been strongly suggested in the fossil record Ambiplatanus provides another line of support for the an- (Magallo´n-Puebla et al. 1997; Mindell et al. 2006). Ambipla- cient relationship between families of Proteales. The genus is tanus washingtonensis provides clear evidence of bisexual the first reported instance of functionally bisexual flowers in flowers in the Late Cretaceous (early Coniacian), perhaps a the fossil record of Platanaceae. Contemporaneous Cretaceous relict of ancestral Platanaceae. Living Proteaceae commonly localities predominantly feature other modes of preservation have winged seeds (Cronquist 1981; Watson and Dallwitz (i.e., compression/impression, charcoalification; Bell 1957; 1992; Schurr et al. 2005), a feature hitherto unknown in fossil Crane and Herendeen 1996; Takahashi et al. 1999; Craggs and living Platanaceae. However, Ambiplatanus and Quadri- 2005; Maslova 2010; Friis et al. 2011). Only the Turonian- platanus (Magallo´n-Puebla et al. 1997) show what may be a Santonian of Hokkaido, Japan, has comparable fossils of an winged seed or possibly a raphe. If these are winged seeds, age and state of preservation similar to those of the Eden Main this evidence would be consistent with the relationship between locality (Nishida 1991). Permineralized fossils like those found Proteaceae and Platanaceae within the order Proteales (APG at Eden Main allow for the identification and description of III 2009; Doyle and Endress 2010). fine structural details. The description of A. washingtonensis Extant Platanus fruits are achenes, which act as the dispersal should provide an impetus for the reevaluation of platanaceous unit. They are subtended by a tuft of trichomes that aid in compression material, where the mode of preservation could wind dispersal (Kubitzki 1993). This tuft of trichomes is absent obscure winged seeds, short carpels within elongate stamens, from many fossil fruits of Platanaceae (Manchester 1986; Pigg and other delicate tissues. and Stockey 1991; Mindell et al. 2006) and has resulted in speculation as to the ancient dispersal of seeds in the family (Manchester 1986; Tiffney 1986). Macginicarpa fruits from the Eocene of Oregon share achene morphology with extant Acknowledgments Platanaceae; however, their fruits lack the basal trichome tuft and, consequently, it was suggested that the fruits were dis- We thank Dr. Dirk Meckert (Courtenay, BC) and Rick Ross persed by water (Manchester 1986). We suggest that the prom- (Vancouver Island Paleontological Society) for their help col- inent and extensive sutures on the carpels in Cretaceous Pla- lecting in the field; Dr. Peter R. Crane (Yale University), Dr. tanaceae flowers reported from charcoalified mesofossils (Friis Else-Marie Friis (Swedish Museum of Natural History), Dr. et al. 1988; Pedersen et al. 1994; Magallo´n-Puebla et al. 1997) Kai R. Pedersen (University of Aarhus), and Dr. James A. Doyle may represent dehiscence lines for the release of winged seeds. (University of California, Davis) for helpful discussion and Fruits of Ambiplatanus lacked trichomes and had clear suture critical review of the manuscript; and Gar W. Rothwell (Ohio lines, suggesting that the seed may have been the dispersal unit. University) for technical assistance and use of laboratory fa- However, empty achenes showing open carpels cannot be dem- cilities. This work was supported in part by NSERC grant A- onstrated in these fossils because of abrasion and because of 6908 to R. A. Stockey.

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