American Journal of Botany 98(8): 13371355. 2011.

PALEOCENE MALVACEAE FROM NORTHERN SOUTH AMERICA

AND THEIR BIOGEOGRAPHICAL IMPLICATIONS1

Mnica R. Carvalho24,7, Fabiany A. Herrera3,5, Carlos A. Jaramillo3, Scott L. Wing6, and Ricardo Callejas2
2Instituto

de Biologa, Universidad de Antioquia, Medelln, Colombia; 3Smithsonian Tropical Research Institute, CTPA, Panama City, Panama; 4Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802 USA; 5Department of Biology and Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 USA; and 6Department of Paleobiology, Smithsonian Museum of Natural History, Washington D.C. 20013 USA

Premise of the study: The clade Bombacoideae + Malvoideae (Malvatheca group sensu Baum et al.) in Malvaceae comprises a mostly tropical lineage with derived taxa that now thrive in higher latitudes. The sparse fossil record, especially for Malvoideae, obscures interpretations of past distributions. We describe fossil leaves of Malvoideae from the middle-late Paleocene Cerrejn Formation in Colombia, which contains evidence for the earliest known neotropical rainforest. Methods: Fifty-six leaf compressions belonging to Malvaceae were collected from the Cerrejn Formation in northern Colombia. Leaf architectural characters were scored and optimized for 81 genera of Malvaceae. Synapomorphic characters and unique character combinations support natural afnities for the fossil leaves. Fossil pollen from the same formation was also assessed. Key results: Despite convergence of overall leaf architecture among many Malvaceae, Malvaciphyllum macondicus sp. nov. can be assigned to the clade Eumalvoideae because of distal and proximal bifurcations of the costal secondary and agrophic veins, a synapomorphy for this clade. Conclusions: The leaf compressions, the oldest fossils for Eumalvoideae, indicate a minimum divergence time of 5860 Ma, older than existing estimates from molecular analyses of living species. The abundance of eumalvoid leaves and of bombacoid pollen in the midlate Paleocene of Colombia suggests that the Malvatheca group (Malvoideae + Bombacoideae) was already a common element in neotropical forests and does not support an Australasian origin for Eumalvoideae. Key words: Colombia; Eumalvoideae; fossil leaves; leaf architecture; Malvaceae; neotropics; paleobiogeography; pollen.

Malvaceae is a diverse tropical to temperate family of more than 4500 species in nearly 250 genera. Nine subfamilies have been recognized as monophyletic, regrouping traditional paraphyletic Sterculiaceae, Tiliaceae, and Bombacaceae within an expanded Malvaceae (Bayer et al., 1999; Kubitzki and Bayer, 2003). This regrouping has been supported by various morphological and anatomical synapomorphies as well as molecular data (Judd and Manchester, 1997; Alverson et al., 1998, 1999; Bayer et al., 1999).
1 Manuscript

received: 30 December 2010; revision accepted: 27 May 2011.

This work was supported by a short-term fellowship at the Smithsonian Tropical Research Institute and a partial Jos Cuatrecasas fellowship in the Department of Botany of the Smithsonian Museum of Natural History (MRC), Carbones del Cerrejn and the Smithsonian Paleobiology Endowment Fund (FAH), a Smithsonian Unrestricted Endowment Grant (CJ, SW), and NSF grants DEB-0733725 (CJ), and DEB-0919071 (MRC), the Fundacin para la Promocin de la Investigacin y la Tecnologa, Banco de la Repblica, the Colombian Petroleum Institute, and Fundacin Ares (CJ, FAH), the Evolving Earth Foundation (FAH), the Geological Society of America Foundation (FAH), the Gary S. Morgan Student Research Award (FAH), and the Lewis & Clark Foundation-American Philosophical Society (FH). The authors thank L. Teicher, F. Chavez, G. Hernndez, C. Montes, A. Rincn, and the geology team at the Cerrejn mine for eldwork support. M.R.C. especially thanks Laurence Dorr for taxonomic discussions and Lisa Barnett, Peter Wilf, Vicky Funk, Emily Wood, Alvaro Idrraga, and curators at US, A, HUA and SCZ herbaria. 7 Author for correspondence (e-mail: moccada@gmail.edu) doi:10.3732/ajb.1000539

Malvaceae is one of the most dominant plant families in neotropical forests, both in terms of abundance and species number (Terborgh and Andresen, 1998; ter Steege et al., 2000; Burnham and Johnson, 2004). The informal but well-supported Malvatheca group (Baum et al., 1998, 2004) combines Bombacoideae and Malvoideae into one of the most speciose clades (ca. 1300 species) within Malvaceae and one of the most conspicuous groups in the neotropics. Malvoideae comprises traditional Malvaceae sensu stricto (Baum et al., 1998, 2004) as well as various tropical lineages traditionally included in the Bombacaceae, namely, Camptostemon, Quararibea, Matisia, and Phragmotheca (Fig. 1). The oldest record for the Malvatheca group is based on pollen from the Maastrichtian of New Jersey attributed to Bombacoideae (Wolfe, 1975), suggesting pre-Cenozoic divergence times for the major clades within this family. Due to the conspicuous palmate venation of many extant Malvaceae, many palmately veined fossil leaves dating back to the Late Cretaceous have been assigned to this family, usually under paraphyletic Sterculiaceae (Table 1) (Ward, 1887; Lesquereux, 1891; Knowlton, 1902,1917, 1923, 1930; Fontaine, 1905; Berry, 1929; Hollick, 1930, 1936; MacGinitie, 1974; Wolfe, 1977); however, high levels of homoplasy and foliar character convergence make it difcult to assess their natural afnities. More reliable taxonomic identications have been supported by the co-occurrence of leaves and associated plant organs (Kvaek et al., 2002; Kvaek, 2004, 2006), preservation of cuticular features (Pan and Jacobs, 2009; Worobiec et al., 2010), whole-plant interpretations (Kvaek, 2008), reproductive structures (Duarte, 1974;

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Here we describe a new species of the Malvatheca group from a middle to late Paleocene (5860 Ma) tropical rainforest in Colombia (Wing et al., 2009). This species is assigned to Malvoideae, based on overall leaf morphology and the identication of shared-derived characters among taxa within this group. To place this species, we explored leaf character distribution across the major lineages of this family as a means to overcome the familys natural variation and identify traits that may have become xed across clades. These fossil leaves document the earliest known megafossil occurrence for the clade Eumalvoideae in the neotropics and predate molecular clock-based divergence estimates by ~30 Myr, and the groups fossil pollen record by at least 9 Myr (Muller, 1981; Pfeil et al., 2002; Koopman and Baum, 2008; Jaramillo et al., 2011). Fossil pollen from the same formation as the leaf fossils demonstrates the occurrence of taxa within Bombacoideae, suggesting a noticeable diversity of the Malvatheca group in the neotropics by the middle-late Paleocene. MATERIALS AND METHODS
The fossil leaves and pollen grains described were collected from the Cerrejn Formation, exposed in the Cerrejn coal mines in the Cesar-Ranchera basin, northern Colombia (11914.58N, 723630.43W; Fig. 2). The Cerrejn Formation is a 700 m thick sequence of coal beds, uvial sandstones, and lacustrine siltstones; these deposits have been dated as mid to late Paleocene based on isotopic and biostratigraphic correlations (Jaramillo et al., 2007). The depositional sequence suggests paleoenvironments that range from coastal plains characterized by deltaic systems at the base of the sequence, to continental environments dominated by oodplains, swamps, and lagoons near the top of the formation (Jaramillo et al., 2007). The 56 specimens assigned to this leaf morphotype (CJ26 of Wing et al., 2009), vary from incomplete to nearly complete foliar compression fossils. Forty-nine specimens were found in a gray siltstone bed near the top of the formation (localities below coal seam 175: FH0705-6-8-11-12, GPS 110749.4N, 723460.5W) that we infer to represent a swampy-lacustrine environment because the bed is very ne grained and laterally extensive; the other seven specimens come from a locality in the middle of the formation (locality below coal seam 100: FH0317, GPS 11.135N, 72.57W) that we infer was deposited in a uvial channel because it is composed of cross-laminated silt and ne sand and has a lenticular cross section. Fossil leaves were described according to shape and venation characters using the terminology of Ellis et al. (2009). Branching of costal secondary and agrophic veins are features of special importance in Malvaceae. We refer to branching of major or minor 2 veins toward the base of the leaf as proximal branching and branching toward the apex as distal branching (Fig. 3A, B). Type specimens were drawn under camera lucida on a Nikon SMZ1500 stereoscope and digitized with Adobe (San Jose, California, USA) Illustrator CS4. Specimens were photographed with a Nikon DS70 and DMX1200F and observed with epiuorescence using a Nikon Eclipse 50i microscope coupled to a mercury lamp, to detect preserved cuticle fragments. When present, leaf fragments were removed from the specimen and treated with Calgon 10% solution for 7 d, rinsed, followed by digestion with 10% HF for 12 h. Loose cuticle fragments were mounted in glycerin and observed under epiuorescence. An exhaustive morphological comparison was performed with numerous angiosperm families similar to Malvaceae using the National Cleared Leaf Collection stored at the Smithsonian Natural History Museum (USNM), and botanical specimens at the Harvard University Herbaria (A), United States National Herbarium (US), Herbario Universidad de Antioquia (HUA), and the Smithsonian Tropical Research Herbarium (SCZ). Over 375 genera of Euphorbiaceae, Moraceae, Bixaceae, Urticaceae, Cucurbitaceae, Sapindaceae, Vitaceae, Eleaeocarpaceae, and other families with palmately veined leaves were examined to establish similarities between the fossils and any of these lineages (Appendix S1; see Supplemental Data with the online version of this article). Once afnities to distantly related lineages were discarded based on consistent morphological differences in overall venation and tooth characters, the fossil leaves were compared to a broad survey of Malvaceae. One hundred and seventy genera of Malvaceae were studied (Appendix 1); 81 of these were scored for 53 leaf morphology characters based on the Ellis et al. (2009) Manual of Leaf Architecture, including features of overall leaf shape, venation, and teeth

Fig. 1. Distribution and phylogenetic relationships of major groups within the Malvatheca group (modied from Baum et al., 2004).

Kvaek et al., 1991, 2002; Manchester, 1992, 1994), and anatomically preserved wood (Manchester, 1979, 1980). The fossil record of leaves attributed to Malvaceae or its segregate families ranges from the Late Cretaceous to the late Neogene, including reports from the Cretaceous of North America (Hollick, 1930, 1936), lower Miocene of Europe (Kvaek et al., 2002; Kvaek 2008), Miocene of Argentina (Anztegui and Cristalli, 2000) and late Oligocene of Africa (Pan and Jacobs, 2009). Despite the extensive Late Cretaceous and Cenozoic fossil record of Malvaceae, molecular clock approximations infer fairly recent divergence times (Wikstrom et al., 2001; Magalln and Castillo, 2009). Magalln and Castillo (2009) estimated the divergence of crown group Malvales at 33.9 Ma, much younger than the Late Cretaceous/early Cenozoic fossil record of families within the order (Magalln et al., 1999). The underestimation probably results from a combination of low taxon sampling within Malvales and the use of derived fossil taxa as calibration points. The latter may mean that the estimated age for divergence of crown Malvales actually corresponds to divergences within the order and would thus decrease the super high diversication rates estimated for Malvales by Magalln and Castillo (2009).

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Table 1.

Morphological comparison of Malvaceae fossil leaves.

Lamina Primary Secondary dissection venation a veins Unlobed Unlobed Unlobed Unlobed Comp Comp 3 Lobed 3 Lobed 3 Lobed 3 Lobed 3 Lobed 3 Lobed Unlobed Unlobed Unlobed Unlobed Unlobed Unlobed Unlobed 3 Lobed Unlobed Unlobed Unlobed Unlobed Unlobed Unlobed 3 Lobed 3 Lobed 3 Lobed 3 Lobed 3 Lobed Actino Actino 5 Pinnate Pinnate Pinnate Pinnate Actino 5 Actino 5 Actino Actino Actino Actino Actino 7 Actino Actino Actino Actino Pinnate Actino 3 Pinnate Actino 3 Pinnate Actino Pinnate Pinnate Pinnate Actino 3 Actino Actino 3 Actino Pinnate Crasp Brochid Semicrasp Brochid Semicrasp Brochid Semicrasp Semicrasp Brochid Brochid Brochid Crasp Crasp Semicrasp Crasp Crasp Crasp Crasp Crasp Crasp Semicrasp Brochid Crasp Crasp Crasp Crasp Brochid Brochid Brochid Brochid Brochid Minor secondaries Crasp Brochid Semicrasp Brochid Semicrasp Brochid Semicrasp Semicrasp Brochid Brochid Brochid Crasp Crasp Semicrasp Crasp Crasp Crasp Crasp Crasp Brochid Semicrasp Brochid Crasp Crasp Brochid Brochid Brochid Brochid Brochid Brochid Brochid Agrophic Tertiary veins venation Comp Comp Comp S Absent Absent Comp Comp Comp Comp Comp Comp Comp Comp S S Comp S S S S S S S S S S S Comp S S Opp Alt Opp Ret Ret Ret Ret Opp Opp Opp Opp Alt Opp Opp Opp Opp Opp Opp Opp Opp Opp Ret Opp Alt ? Opp Opp Ret Ret Ret Ret Major Quaternary vein Tooth venation branching shape Alt Ret Opp Ret Ret Ret Ret Ret Ret Ret Ret ? ? Ret Opp Ret Opp ? ? ? Opp ? Opp ? ? Ret Ret Ret Ret Ret Ret Prox Prox Prox Pro Prox Prox Prox Prox Prox Prox Prox Prox Prox ? Cv-Cv Cc-Cc Cc-Cc Cv-Cc Cv-Cv Cv-Cv Cc-Cc Cv-Cv Cv-Cc Cv-Cc Cv-Cc Cv-Cv Cv-Cv Cv-Cv Cv-Cc Cv-Cv Cv-Cc Teeth order 1 1 1 2 1 1 1 1 1 1 1 1 1 1 1 1 1 Principal vein Accesory course veins Med-Str Str-prox ? Curv-prox Med, curv Med, curv Curv-prox Str-prox Curv-prox Curv-prox Str-prox ? Str-prox Anastom Absent ? ? ? ? Cv Cv Cv ? ? ? Cv

Taxon Abutilon eakini Hollick Apeiba improvisa MacGinite Apeibopsis atwoodi Hollick Apeibopsis cyclophylla Lesquereux Bombacites eocenicus Berry Bombacites jacksonensis Berry Dombeya novimundi Hickey Dombeyopsis decheni Weber. Dombeyopsis lobata Unger Dombeyopsis obtusa Lesquereux Dombeyopsis ovata Knowlton Dombeyopsis plantanoides Lesquereux Grewia alaskana Hollick Grewia crenata Unger Heer Grewiopsis acuminata Lesquereux Grewiopsis formosa Berry Grewiopsis tiliacea Sap. Grewiopsis tuscaloosensis Berry Grewiopsis wadii Berry Grewiopsis yukonensis Hollick Luehea newberryana Knowlton MacGinite Pterospermites carolinensis Berry Pterospermites dentatus Heer Pterospermites haquei Knowlton Pterospermum conforme Hollick Sterculia atwoodi Hollick Sterculia basiauriculata Hollick Sterculia elegans Fontaine Sterculia labrusca Unger Sterculia reticulata Lesquereux Sterculia subtilis MacGinite

Sinus Angular Angular Angular Angular Angular Angular Angular Angular Curved Angular Angular Curved Angular Curved Curved Curved Curved

Symmetry Sym Asym Asym Asym Sym Asym Asym Sym Asym Asym Asym Asym Sym Sym Asym Sym Asym

Source b 8 18 7, 8 17 4 3 6 19 12, 13, 20 14 11 14 7 19 16 2 19 2 3 7 18 2 19 9 7 7 7 5 8 17

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Curv-prox Anastom Str-prox Str-prox Absent Cv ? Absent

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Notes: Actino = Actinodromous venation, Alt = Alternate percurrent, Anastom = anastomosing, Asym = Asymmetrical, Brochid = Brochidodromous, Cc = Concave, Comp = Compound, Crasp = Craspedodromous, Curv = Curved, Cv = Convex, Med = Medial, Opp = Opposite percurrent, Prox = proximal, Ret = Reticulate, Semicrasp = Semicraspedodromous, Str = Straight, S = Simple, Sym = Symmetrical, ? = uncertain. a Numbers in parentheses correspond to the number of basal veins. b References: 1, Anztegui and Cristalli, 2000; 2, Berry, 1919; 3, Berry, 1924b; 4, Berry, 1930; 5, Fontaine, 1905; 6, Hickey, 1977; 7, Hollick, 1930; 8, Hollick, 1936; 9, Knowlton, 1899; 10, Knowlton, 1917; 11, Knowlton, 1922; 12, Kvaek et al., 2002; 13, Kvaek, 2008; 14, Lesquereux, 1878; 15, Lesquereux, 1883; 16, Lesquereux, 1887; 17, Lesquereux, 1891; 18, MacGinitie, 1974; 19, Schenk, 1890; 20, Unger, 1850

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(Appendix 2; online Appendix S2). The scored genera were chosen based on their inclusion in published phylogenetic analyses and thorough sample availability, taking into consideration that all of the major clades that have been proposed for Malvaceae were equally represented. This was especially an issue for the selection of genera of Malvoideae, given that this group outnumbers all other subfamilies in genera and species. In this case, a few genera of each of the main tribes (Hibisceae, Malveae, and Gossypieae; sensu Kubitzki and Bayer, 2003) were selected to keep a comparable number of representative genera for each subfamily. When possible, the species directly included in these published analyses were scored (see Appendix 3 for taxa and voucher information); otherwise, recent taxonomic treatments of the genera were followed for species selection to avoid misplacement of polyphyletic genera. In each case, several closely related species per genus were studied, and multiple specimens of each species were revised; taxa with multiple character states were coded as polymorphic. Scored characters were optimized as unordered on existing phylogenetic topologies (Seelanan et al., 1997; Alverson et al., 1999; Bayer et al., 1999; Nyffeler and Baum, 2000; Whitlock et al., 2001; Pfeil et al., 2002; Baum et al., 2004; Nyffeler et al., 2005; Tate et al., 2005; Wilkie et al., 2006; Le Pechon et al., 2009) using a Fitch algorithm implemented in the program MacClade v4.06 (Maddison and Maddison, 2003). Topologies were analyzed both independently and by combining them in a supertree topology. Several large genera of Malvoideae are known to be polyphyletic, and their inclusion could potentially add noise to the results of the analyses. However, polyphyletic genera (such as Sida and Hibiscus) generally consist of more than one lineage within the same tribe, and since this character exploration aims to look at a higher hierarchical resolution, the inclusion of polyphyletic genera did not have a major effect on the results. Character optimization did not conict between independent trees and the supertree. Most of the examined leaf features are highly homoplasious within Malvaceae, and for this reason, only characters inferred to be synapomorphic and characters conserved within various clades at various levels are discussed to support taxonomic afnities of the fossil leaves. Fossils are stored in the paleontological collections of the Colombian Geological Institute (INGEOMINAS) in Bogot, Colombia (repository acronym ING).

19 7 3 19 Asym Asym Asym Angular Angular Angular 1 1 1 Cv-Cc Cv-Cc Cv-Cc Prox Prox Prox Opp Opp Opp Opp Ret ? ? ?

Principal vein Accesory course veins

Symmetry

Teeth order

Major Quaternary vein Tooth venation branching shape

Agrophic Tertiary veins venation

Opp Opp Opp

Opp Ret Ret

Prox Prox, Distal

Cv-Cv Cv-Cc Cv-Cv

1 1 2

Angular Angular Curved

Sinus

Asym Asym Sym

Curv-prox ? Curv-prox ? Med? Straight Med, curv Anastom Curv-prox Cv ? ?

15 10 1

SYSTEMATICS Family Malvaceae Juss. Subfamily Malvoideae Morphogenus Malvaciphyllum Anztegui Morphospecies Malvaciphyllum macondicus M. Carvalho sp. nov. Diagnosis Leaves ovate, dentate to crenate, petiole doubly pulvinate. Length to width ratio ~1 : 1, apex shape straight. Base strongly cordate. Laminar surface pubescent. Primary veins actinodromous, 59 basal primary veins; secondary veins craspedodromous, rst pair of costal secondary veins branching proximally and distally. Tertiary veins opposite convex to chevroned percurrent, fourth order veins mixed opposite/alternate percurrent, freely ending veinlets branched. Teeth two to three orders, symmetrical, convex-convex, principle veins of teeth medial and straight, accessory veins looped. Holotype hic designatus ING 1410 (Fig. 4B, C; 5D, E). Paratypes ING 1411; ING 1357 (Fig. 4A); ING 1074; ING 0617; ING 1077 (Fig. 4D); ING 1091 (Fig. 5F) Studied material 56 specimens: ING 06160620, ING 0984, ING 0985, ING 1056, ING 1075 (Fig. 5A), ING 10761078, ING 10801096, ING 1097 (Fig. 5C), ING 1098, ING 10991101, ING 1102 (Fig. 5B), ING 1103 1121, ING 1357, ING 1358, ING 1410, ING 1411.

S S S Comp Brochid Crasp Crasp Crasp Brochid Crasp Crasp Crasp Actino 3 Pinnate Pinnate Actino 3 Lobed Unlobed Unlobed Unlobed Sterculia tenuinervis Heer. Tilia cretacea Hollick Tilia jacksoniana Berry Tilia malmgreni Heer

Minor secondaries

Lamina Primary Secondary dissection venation a veins

Tilia populifolia Lesquereux Unlobed Tilia speciosissima Knowlton Unlobed Unlobed Malvaciphyllum quenquiadensis Anztegui

Table 1.

Continued.

Taxon

Actino Actino Actino

Crasp Crasp Crasp

Crasp Crasp Crasp

Comp Comp Comp

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tooth apex, lacking any type of glandular swelling or projection. Accessory veins are present, looping symmetrically on the principal vein and forming a series of arches that terminate at the tooth apex (Fig. 5F). Source, age, and stratum Colombia, Ranchera Basin, Cerrejn Formation, Cerrejn coal mine; ING 1410, ING 1411, ING 0617, and four other specimens were found at Pit Tabaco 1, locality 0317, placed between coal beds 100 and 102, coordinates 11.14N, 72.57W; ING 1357, ING 1074, ING 0617, ING 1077, and 45 other specimens were collected in ve localities at Pit Tabaco Extensin, between coal beds 170 and 175, coordinates 11.13N, 72.58W. The age of the entire coal-bearing section of the Cerrejn Formation has been estimated as middle to late Paleocene (5860 Ma). This age estimate is based on biostratigraphic correlations and has been described elsewhere (Jaramillo et al., 2007). Systematic afnity within angiosperms Palmate leaf venation, toothed margins, and stellate trichomes are widespread and conspicuous in most Malvaceae (Kubitzki and Bayer, 2003). However, these characters occur in other lineages of angiosperms, reecting the repeated evolution of palmate venation patterns (White, 2005). Despite this evolutionary trend, tooth shape and venation characters exhibit familial and generic level consistency, being useful in taxonomic and phylogenetic studies at different hierarchical levels (Hickey and Wolfe, 1975; Fuller and Hickey, 2005; Doyle, 2007). Teeth of Malvaceae follow a consistent morphological pattern different from that in other palmately veined lineages: they are symmetrical to asymmetrical laminar projections with a medial principal vein and generally have accessory veins forming a series of looping arches that terminate at the tooth apex (Fig. 3G, H); such teeth have been called malvoid (Hickey and Wolfe, 1975). Teeth of this type are observed in Malvaciphyllum macondicus. Principal (and accessory) veins terminate at the tooth margin without any type of glandular thickenings or processes such as mucros, papillae, or foramina found in other palmately veined, toothed angiosperm lineages. Families with similar palmately veined, toothed leaves, such as Euphorbiaceae, Vitaceae, Gunneraceae, Moraceae, Rosaceae, among others (online Appendix S1), show distinctive tooth morphology, including various types of glandular thickenings and accessory veins that differ from those seen in extant Malvaceae and Malvaciphyllum macondicus (For detailed comparison between families, see online Appendix S1). Mucronate and glandular tooth terminations on asymmetrical teeth in Euphorbiaceae (Klucking, 2003) and translucid papillae in Vitaceae distinguish the two most phenetically similar families from M. macondicus. Species of Bixaceae are closely related to Malvaceae, yet differ in having asymmetric teeth with a principal vein that terminates in the sinus and not the apex of the tooth. Eleaocarpaceae, a family that used to be part of Malvales but that is presently thought to be distantly related to Malvaceae, differs in having teeth with principal veins that extend beyond the blade lamina. The combination of characters seen in Malvaciphyllum macondicus: palmately veined leaves, stellate and acicular trichomes, double pulvinus, and the distinctive tooth venation are consistent with and indicative of Malvaceae. There are not any other angiosperm lineages that exhibit this combination of characters.

Fig. 2. Collection site for Malvaciphyllum macondicus sp. nov., Cerrejn coal mines, Guajira, Colombia.

EtymologyThe epithet macondicus refers to the ctional town Macondo, described by Gabriel Garca Mrquez (1970) in One Hundred Years of Solitude. This town epitomizes the lifestyle and culture of the Caribbean coast of Colombia, the area from which these fossils come.

Description The fossil leaves are microphyllous to macrophyllous leaf compressions; the one complete petiole is 5.08 cm long 0.37 cm wide, doubly pulvinate and terete. The laminar shape varies from ovate to elliptic, 9.25 (3.9917.54) cm (measured in 11 specimens) long and 8.85 (3.3416.4) cm (measured in 14 specimens) wide. The leaves exhibit a straight-sided, acute apex, and a base that is cordate, with a basal extension asymmetry and a reex angle (Fig. 4B). The laminar surface is densely pubescent, covered with coalied stellate and acicular trichomes (observed in specimens ING 1410, ING 1411; Fig. 5D, E). The primary vein framework is actinodromous, with 59 veins arising from the base. Costal secondary veins are craspedodromous, excurrent on primary veins, and increasing in spacing proximally. Agrophic veins are compound, with the minor secondaries arising exmedially from the basal veins. The rst pair of costal secondaries and minor secondaries bear a pair of minor secondary veins that branch both proximally and distally close to the margin (Fig. 5B). Tertiary venation is opposite percurrent, concentric to the base of the lamina; costal tertiaries are sinuous to straight; epimedials are admedially perpendicular to the midrib and exmedially parallel to costal tertiaries. Fourth order veins are mixed opposite/alternate percurrent; fth order veins are regular reticulate. Tertiary and fourth order veins are very thick compared to primary veins. Areolation is well developed with branched freely ending veinlets, and the ultimate marginal venation is looped. The teeth are regularly spaced, 5 cm on average (minimum 2, maximum 7), and occur in two to three discrete orders of teeth distinguished by their size and the gauge of the veins that enter them (Fig. 4A). The rst order teeth are generally present and supplied by the rst pair of lateral primaries; they are convexstraight in shape, and their sinuses vary from curved to angular. Second and third order teeth are consistently present and are supplied by second and third order veins, respectively; they have angular sinuses, and their shapes range from convex-convex to exuous-exuous, symmetrical to slightly asymmetrical. All teeth exhibit a medial principal vein that terminates at the

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Character optimizations and afnities within Malvaceae Simple, palmately veined leaves with dentate-crenate margins are common in six of nine subfamilies within Malvaceae, including Byttnerioideae, Grewioideae, Helicteroideae, Tilioidae, Dombeyoideae, and Malvoideae. All leaf architecture characters were optimized on a supertree of Malvaceae as a means to explore for leaf characters that have become xed at various clade levels and could potentially prove to be useful for leaf identication within a family of ~4500 spp. Over 90% of the leaf characters scored and mapped on the supertree compiled for Malvaceae are highly homoplasious at family level (online Appendix S3), reecting the repeated convergence of leaf morphology within this group and the difculty of addressing infrafamilial relations of fossil leaves. However, some character states are conserved at lower hierarchical levels. When combined, conserved characters can help distinguish between leaves of some lineages within the family (Table 2). Malvaciphyllum macondicus exhibits the same character combination that is distinctive to the clade Eumalvoideae of Malvoideae (see Table 2). Eumalvoideae (former Malvaceae sensu stricto) holds the highest number of species in Malvaceae and occurs in a wide variety of habitats (Kubitzki and Bayer, 2003). Habitat variation is reected in a wide range of leaf shape, size, and venation that vary from small, reduced leaves of species growing in desert or upland habitats (Nototriche, Fuertesimalva) to large, deeply cordate leaves of lowland tropical species of genera such as Abutilon and Hibiscus. Despite this variation, the general pattern of leaf venation of Eumalvoids is characterized by simple, dentate leaves with actinodromous venation and more than ve basal veins, compound agrophics, craspedodromous secondary veins, alternate percurrent third and fourth order veins, and branched freely ending veinlets. In particular, two character states that are recovered as restricted to Eumalvoideae and differentiate this group from other subfamilies are also present in the fossil leaves. The proximal and distal branching of secondary veins refers to the orientation of veins of secondary or nearly secondary gauge that branch from the basalmost major or minor secondary veins (Fig. 3A and B). In most Malvaceae, including Eumalvoideae, lateral primaries that innervate the lobes branch both proximally and distally, but only in Eumalvoideae do costal secondaries branch on the distal side near the margin (Figs. 3A, B, 6). The second character state recovered as synapomorphic for Eumalvoideae is the presence of three distinct orders of teeth, reecting differences in the size of the teeth fed by primary, secondary, and tertiary veins. In other lineages in the family that have one or two orders of teeth, the teeth are fed by secondary and tertiary veins (Fig. 3CE). These two charactersthe costal secondary and minor secondary vein branching as well as three orders of teethdistinguish Eumalvoideae from all other lineages of Malvaceae that have similar leaf architecture. The afnity of M. macondicus to

eumalvoids is supported by the occurrence of the two characters that are unique to Eumalvoideae as well as the similarity in overall leaf architecture. Given that most other features are highly homoplasious, we consider that the costal secondary and minor secondary vein branching, and the number of orders of teeth evolved only once within the Malvaceae and support the relationship between M. macondicus and stem group Eumalvoideae. Even though most taxa in this group are known to have small leaves markedly different from the mesophyll and macrophyll leaf blades of M. macondicus, large leaves are commonly found in tropical and subtropical genera such as Hibiscus, Wercklea, and Malvaviscus. These genera share the same set of characters and show the greatest overall similarity to M. macondicus. Comparison to fossil Malvaceae The conspicuous palmate venation and double pulvini in most Malvaceae have been prevalent in fossil leaves that date back to the Late Cretaceous, such as Tilia populifolia (Lesquereux, 1883), Tilia cretacea, Pterospermum conforme, and Apeibopsis atwoodii (Hollick, 1930), among others. Many fossil leaves have been described as related or similar to Malvaceae, although the accuracy of the systematic assignments is questionable. The diagnostic characters, in particular the distal and proximal branching of secondary veins in Malvaciphyllum macondicus, are not found in most of the fossil leaves previously described as Malvaceae (Table 1). The fossil genus Malvaciphyllum Anztegui was described from two species of fossil leaves from Miocene and Pliocene deposits of Argentina and Brazil, respectively, and was initially related to extant Abutilon (Anztegui and Cristalli, 2000). This morphogenus is the only malvalean fossil to exhibit the same proximal and distal branching patterns as M. macondicus. Given that this character suggests afnities to the Eumalvoideae clade, we consider Malvaciphyllum as part of the stem group of this clade, and we include the fossils described here as a new species of this fossil genus. The consistently smaller (notophyll) size, prominent rounded lobes, mostly crenate margins, opposite-percurrent fourth order venation, and lack of pulvini in M. quenquiadensis (Anztegui and Cristalli, 2000) differs from the mostly mesophyll-sized, unlobed, markedly dentate or crenate and pulvinate M. macondicus leaves. These features are used to support species delimitation. In examining fossil leaves described as Malvaceae, we did not nd a special afnity of Dombeya novi-mundi to extant Dombeya or the clade that includes this genus. Dombeya novimundi, described by Hickey (1977), is known from Eocene deposits of Wyoming and North Dakota, and is one of the few fossil leaf taxa assigned to a modern genus of Malvaceae. As with most fossil leaves attributed to this family, D. novi-mundi is characterized by having 57 actinodromous primary veins, a toothed margin, a pulvinulus at the base of the leaf blade, and concentric, opposite percurrent tertiary veins with well-developed

Fig. 3. Leaf morphology of extant Malvaceae. (A) Major vein branching proximally; exmedial branches of secondary veins are directed to the base of the leaf only (arrows). Dombeya dawei Sprague (A, Dummer NA). Scale = 4 cm. (B) Major vein branching proximally and distally. Exmedial branches of secondary veins are directed to the base (proximal) and to the apex (distal) of the leaf (arrows). Wercklea tulipiora (Hook.) Fryxell (A, Webster #12383). Scale = 5 cm. (C) One order of teeth. Helmiopsiella poissonii (Arnes) Capuron ex L.C. Barnett. (US, #3504977). Scale = 2 cm. (D) Two orders of teeth as determined by two discrete tooth sizes (arrows indicate two different sizes). Dombeya ciliata Cordem. (A, Friedmann # 2745). Scale = 2 cm. (E) Three orders of teeth. Hibiscus mutabilis L. (A, Hassler # 42593). Scale = 2 cm. (F) Cleared leaf of Kydia calycina Roxb. Arrow indicates apical pulvinulus (NMNH, Cleared Leaf Collection). Scale = 1 cm. (G) Tooth size differentiation. Arrowheads show two teeth orders. Urena lobata L. (NMNH, Cleared Leaf Collection). Scale = 0.5 cm. (H) Malvoid tooth venation detail. Arrowheads show looping accessory veins. Byttneria dentata Pohl. (NMNH, Cleared Leaf Collection). Scale = 1 mm.

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Fig. 4. Malvaciphyllum macondicus sp. nov. (A) Paratype ING 1357 (STRI-9364). Arrows indicate three orders of teeth associated with primary (a), secondary (b) and tertiary (c) veins. Scale = 2 cm. (B) Holotype ING 1410. Scale = 1 cm. (C) Holotype venation sketch; drawn with camera lucida. (D) Paratype ING 1077 (STRI-9731). Scale = 3 cm.

areolation. Most of the leaf character states of this taxon are recovered as plesiomorphic for the family as a whole, so that leaves with morphologies similar to that of D. novi-mundi are

widespread across various lineages of Malvaceae. The tooth morphology of D. novi-mundi, however, is not very common in Malvaceae: the teeth are markedly asymmetrical, concave-convex

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Fig. 5. Malvaciphyllum macondicus sp. nov. (A) Paratype ING 1075 (STRI-9734). Arrows indicate double pulvini. Scale = 3 cm. (B) Specimen ING 1102 (STRI-9755); arrows indicate major vein branching distally and proximally. Scale = 2 cm. (C) Specimen ING 1097 (STRI-9775); teeth order differentiation. Arrows indicate different sizes of teeth fed by secondary (a) and tertiary veins (b). Scale = 5 mm. (D, E) Holotype ING 1410; epiuorescence of in situ cuticle. (D) Arrows indicate acicular tricome remains. Scale = 50 m. (E) Arrows indicate acicular and stellate trichome remains. Scale = 200 m. (F) Paratype ING 1091 (STRI-9751); tooth detail, arrows indicate accessory veins looping against primary tooth vein. Scale = 1 mm.

in shape, seeming almost hook-shaped, and are fed by secondary veins (rarely tertiary veins) that curve as they enter the tooths laminar projection. Teeth of D. novi-mundi are similar to those of some taxa in Grewioideae (such as species of Heliocarpus and Luehea) and Byttnerioideae (Abroma spp.), which used to be included in former Tiliaceae and Sterculiaceae, respectively, and might have directed the original designation proposed by Hickey (1977). As former Sterculiaceae have been shown to be polyphyletic and are now included in various subfamilies of Malvaceae, this leaf morphology is more widespread than previously thought. Dombeya novi-mundi is probably related to Malvaceae, but subfamily-level designations cannot be fully resolved with the existing characters, and afnities to extant Dombeya need further support from other features. Pollen record The fossil pollen Bombacacidites annae (Van der Hammen, 1954; Germeraad et al., 1968) is very common in sediments of the Cerrejn Formation (Fig. 7) (Jaramillo et al., 2007). The pollen is a monad, radial, isopolar, with amb triangular-obtuse-convex to almost circular; aperture tricolporate, ectocolpi costate, very short, colpi slightly protruding, costae 3 m wide, endopore lalongate, pores indistinct; semi-

tectate, exine 2 m thick, nexine 0.5 m thick, columellae 1 m thick, tectum 0.5 m thick, columellae distinct, long, present only under muri of reticulum, tectum reduced to reticula; sculpture reticulate, heterobrochate, lumina 13 m wide at apocolpia and surrounding the colpi, almost foveolate (lumina 0.5 m wide) at mesocolpia, muri pluricolumellate, 1 m wide, the transition from reticula to foveolae is gradual although in short distance, sometimes a pseudo-line separates foveolae from reticula. Dimensions: equatorial diameter 25 (38.5) 50 m, SD 4.9, N = 40; equatorial diameter length/width 1.1. The pollen morphology of Bombacacidites annae is very similar to the Bombax-subtype of Nilsson and Robyns (1986), that is characteristic of several genera including Aguiaria, Bernoullia, Bombacopsis, Bombax, Eriotheca, Pseudobombax, and Spirotheca (Nilsson and Robyns, 1986) within the clade Bombacoideae. DISCUSSION Leaf character considerations Leaf architecture characters were optimized on pre-existing phylogenetic hypotheses as a means to assess within-group character variation and

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Notes: Actino = Actinodromus, Alt = Alternate percurrent, Branch = Branched, Brochid = Brochidodromous, Comp = Compound, Crasp = Craspedodromous, FEVS = Freely ending veinlets, Opp = Opposite percurrent, Prox = Proximal, Pubesc = Pubescent, Retic = Reticulate, S = Simple. Boldfaced states indicate reconstructed character states shared with Malvaciphyllum macondicus sp. nov
Absent Absent Prox, distal Absent Prox, distal

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Third Primary No. of Agrophic Secondary Minor Intersecondary order venation basal veins veins venation secondaries venation venation

Combination of foliar characters interpreted as synapomorphic at subfamily level within Malvaceae.

Brochid Brochid Brochid Brochid

Brochid Crasp

co-occurring, clade-xed traits that were reliable for developing hypotheses of natural afnities. Two characters were recovered as co-occurring and restricted to clade Eumalvoideae: the number of orders of teeth and the branching pattern of major secondary veins (Fig. 6). Despite the association of leaf traits with environmental factors, the restriction of these to a particular clade may reect the expression of underlying developmental factors. Major veins have been shown to function as long-distance distribution lines of water through the leaf (Roth-Nebelsick et al., 2001; Sack and Holbrook, 2006) as well as biomechanical support for the leaf blade (Niklas, 1999). Likewise, theoretical modeling of biomechanical responses in leaves has shown that the local structure of venation networks responds to mechanical stress and tensile forces (Corson et al., 2009, 2010). The increased size of the teeth fed by secondary veins relative to teeth fed by tertiary veins, and the resulting exmedial demand for biomechanical support and/or water supply, may thus explain the presence of the proximal and distal branching in Eumalvoideae. Another possibility is that the major vein branching and increased size of the teeth fed by secondary veins relates to the need to release excess water that is common in the riparian environments inferred for Malvaciphyllum macondicus (see Paleoecological insights). This, however, is not the case for some of the extant species that show this trait, such as Wercklea and Malvaviscus, which can inhabit more xeric habitats (Fryxell, 1981; Turner and Mendenhall, 1993). Whether the difference in tooth size reects a change in the overall construction of these leaves cannot be determined simply by observing patterns of correlated evolution. The co-occurrence and restrictedness of these two traits, however, offers a recognizable distinction between the leaves of Eumalvoideae and all other Malvaceae that supports natural afnities for the fossil here described. Malvoideae fossil record The macrofossil record for Malvoideae is sparse when compared to the extensive fossil record for other subfamilies within Malvaceae (Manchester, 1992). Macrofossils related to Malvoideae include leaf compressions of Malvaciphyllum quenquiadensis, which Anztegui associated with Abutilon (see Comparison to fossil Malvaceae), and several fruit compressions assigned to Hibiscus and Malva from the Miocene and Eocene of the United States (Berry, 1929; Brown, 1934), and the Eocene of Patagonia, (formerly dated as Miocene; Berry, 1925, 1929, 1938; Wilf et al., 2005). However, these fossils were initially described based on morphological resemblance, and natural afnities for most of them remain untested. The distinctive echinate, multiporate pollen morphology of Malvoideae has been used as evidence for tracing back this group in the fossil record; however, no detailed SEM studies have proven the afnity of these pollen grains. The earliestdispersed pollen remains include Echiperiporites estelae, from the early Eocene (51 Ma) of Colombia (Jaramillo et al., 2011) and Malvacearumpollis bakonyensis, known from the late Eocene/early Oligocene sedimentary sequences of the Murray Basin of Australia (ca. 3537 Ma; MacPhail and Truswell, 1989; MacPhail, 1999). Based on Eocene pollen from Venezuela (3740 Ma) and the records from the Murray Basin, Koopman and Baum (2008) estimated a divergence age for Eumalvoideae of 29.732.5 Ma. Malvaciphyllum macondicus shows that this group occurred in northern South America by 5860 Ma, predating the earliest reliable pollen record by ~9 Ma (see Jaramillo et al., 2011) and arguing for a much earlier origin than that suggested by molecular

Absent Absent Retic Retic Retic Opp Opp Opp 1 1 2, 3

Fourth order venation FEVS

Opp Retic Opp Opp Retic Alt Alt Present Present Absent Absent Absent Brochid Brochid Brochid Crasp Absent Comp 1 3 59 S Comp S S S S Pubesc Entire Acute Dentate Entire Obtuse Smooth Entire Acute Dentate Reex Pubesc Actino

Pinnate Pubesc Pinnate Pubesc

Leaf Amgle Pube complexity Margin of base scence

Bombacoideae Malvaciphyllum macondicus sp. nov.

Byttnerioideae Grewioideae Tilioideae Helicteroideae Helictereae Durioneae Dombeyoideae Brownlowioideae Sterculioideae Malvoideae Eumalvoideae

Subfamily

Table 2.

Comp S

S S

Entire Acute Smooth Pinnate Dentate Reex Pubesc Actino

Dentate Dentate

1 59

Absent Comp

Absent Crasp

Present Absent

Alt

Retic Retic Retic Alt Retic Hibiscieae: Alt Alt

Absent 1 Absent Absent 1 1, 2 Absent Absent Absent 1 1, 2 Branch Hibiscieae: Hibisceae: 3 1, 2, 3 Branch 2-3 1, 2, 3

Teeth: no. of orders

Vein order on teeth

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Fig. 6. Character optimizations on one of the supertrees compiled for Malvaceae. Arrows indicate Eumalvoideae clade (based on Seelanan et al., 1997; Alverson et al., 1999; Bayer et al., 1999; Whitlock et al., 2001; Pfeil et al., 2002; Baum et al., 2004; Nyffeler et al., 2005; Tate et al., 2005; Wilkie et al., 2006; Le Pchon et al., 2009). (A) Number of orders of teeth. One order = Kokia rockii Lewton (NMNH, Cleared Leaf Collection); Two orders = Dombeya cincinnata K. Schum. (NMNH, Cleared Leaf Collection); Three orders = Urena lobata L. (NMNH, Cleared Leaf Collection). (B) Branching of major veins. Unbranched = Scaphium linearicarpum (Mast.) Pierre (US, # 2888505, Sinclair 8562); proximal = Dombeya dawei Sprague (A, Dummer NA.); proximal/distal = Wercklea tulipiora (Hook.) Fryxell (A, Webster #12383).

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Malvaciphyllum macondicus in northern South America during the late Paleocene requires that either dispersals from Australasia into South America occurred before 60 Ma or the earlydiverging Eumalvoideae had a different distribution than previously thought. Malvaciphyllum macondicus and the record of Bombacacidites annae in Cerrejn imply that both Eumalvoideae and Bombacoideae were present in South America by the middle Paleocene. The oldest pollen of Bombacoideae is found in Maastrichtian (~70 Ma) deposits of the Gulf Coast (Wolfe, 1975), and it appears in tropical South America by mid-Paleocene (60 Ma; Jaramillo et al., 2011). Given that the oldest fossil record of Bombacoideae is centered in North and South America, and since Eumalvoideae (as well as the Australasian genera Lagunaria, Howittia, and Radyera; see Fig. 1) should have diverged before 60 Ma, we consider that present-day distribution interpretations do not need to rely on long-distance dispersals across the Pacic into South America. It is possible that these taxa had a much broader distribution in the past, favored by warmer climatic conditions and continental landmasses at closer proximity than today. Several scenarios could be proposed for explaining current and past distributions for Eumalvoideae, none of which are fully falsiable with present data.
Fig. 7. Bombacacidites annae, slide 547, EF = E20 2/4, Palynological Collection Colombian Petroleum Institute, grain in polar view, mid focus. See the subcircular amb and the heterobrochate reticula, ornamentation changing from reticulate at apocolpia and around colpi to almost foveolate at mesocolpia.

clock inferences (Koopman and Baum, 2008). The low number of calibration points and the derived nature of fossil taxa available for this group make molecular clock estimation of divergence dates susceptible to possible underestimations. Evidence for divergence earlier than 40 Ma for Eumalvoideae is not surprising and has been suggested elsewhere, based on the derived nature of the earliest fossil pollen attributed to the group (Pfeil et al., 2002). Pollen of Eumalvoideae seems to be lacking from the Paleocene deposits of South America. The Paleocene occurrence of eumalvoid leaves is consistent with the idea that the pollen morphology of eumalvoids evolved later than the distinctive leaf morphology, supporting Malvaciphyllum as a stem group of this clade. Biogeographical considerations The sparse fossil evidence for Malvoideae has led various authors to advocate for biogeographical scenarios mostly based on extant distribution. The basalmost lineage of Malvoideae is a clade of neotropical trees: Quararibea, Matisia, and Phragmotheca. Sister to this clade is Eumalvoideae, nested within a grade of Australasian genera including Lagunaria, Howittia, and Radyera (Figs. 1 and 6). The restricted distribution of this grade has been interpreted by Baum et al. (2004) as suggestive of an Australasian origin for Eumalvoideae, in which case, the neotropical lineages within the group would have arrived via trans-Pacic dispersal. There is little doubt that dispersal has played an important role in the history of Malvoideae, and colonization events have been reported for various lineages within this group (Fuertes-Aguilar et al., 2002; Koopman and Baum, 2008; Wagstaff et al., 2010) as well as for closely related Bombacoideae (Dick et al., 2007; Tsy et al., 2009). However, the presence of

Scenario 1Eumalvoideae could have originated in the neotropics and remained present there ever since; dispersal across the Pacic or through Antarctica (see Scenario 2) and regional extinction of basal genera in the neotropics would explain extant distributions of the Australasian genera. This would be consistent with the occurrences of Eumalvoideae and phylogenetically related Bombacoideae in the northern South American fossil record. The extensive pollen record of Bombacoideae shows the earliest occurrences for the group in the Gulf Coast of the United States during the Maastrichtian and an earliest appearance in South America by the middle Paleocene. Under this scenario, Bombacoideae and Malvoideae could have originated in North America by the Late Cretaceous, and further dispersion of both groups would explain the fossil record in northern South America and the proposed origin of eumalvoids in the neotropics during the Paleocene. This opens the possibility of a dispersal route from North to South America during the middle Paleocene, possibly through a Caribbean volcanic arch that briey connected North and South America at this time (Bayona et al., 2011; Cardona et al., 2011). This same dispersal pattern has been proposed for Ulmaceae (Jaramillo and Dilcher, 2001). Scenario 2Eumalvoideae reached South America from Australia before the opening of the Tasman Strait and the Drake Passage. Evidence of biotic interchange between Australia and South America has been found in the Eocene of Argentina (Zamaloa et al., 2006), and globally warm climates are thought to have permitted migration of thermophilic plants and animals among high latitude southern continents (Wilf et al., 2005, 2009). The Drake Passage opened in the late Eocene (~41 Ma), ending the land connection between Australia and South America (Kennett, 1977; Scher and Martin, 2006). The hypothesized movement of eumalvoids across high southern latitude land bridges would agree with earlier ideas for the biogeography of the lineage (Baum et al., 2004) and implies the occurrence of late Cretaceous or early Paleocene Malvoideae in Australia and/or southern South America; however, no fossils of this age

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have been yet recovered, and the Gulf Coast-centered record for its sister group, Bombacoideae, seems to conict with this view. Scenario 3A third possible dispersion route, neither transPacic (Baum et al., 2004) nor Antarctic (as in scenario 2), could have been across high northern latitudes. There are multiple examples of animal and plant taxa moving across high latitude land bridges and into South America in the Paleogene, including arctostylopid mammals (Missiaen et al., 2006), Salvinia (Wing et al., 2009), and Anacardiaceae (Manchester et al., 2007). Even though no fossil Malvaceae from Asia or Europe support this hypothesis, the earliest fossil record of Bombacoideae does occur in North America; more material from other areas may help test this possibility. Divergence time estimates and evidence for past distribution for eumalvoids remain elusive, such that hypotheses of origin and diversication at its basalmost nodes are still poorly supported. The pre-late Paleocene divergence suggested here for eumalvoids sets this group in a time when warm climates seem to have favored thermophilic plant and animal dispersal at high latitudes (Wolfe, 1978; Tiffney and Manchester, 2001; Missiaen et al., 2006). New calibration points for molecular clock approaches are still needed within Malvoideae to have a better understanding of the times of origin and radiation of this group, however, as the nodes for this group are pushed further back in time, the effects of past extinctions, radiations and dispersals become greater, and the explanatory power of extant distributions decreases. Paleoecological insights The Cerrejn ora resembles extant neotropical rainforests in terms of rankorder abundance and oristic composition, mean annual temperature and precipitation (Wing et al., 2009). This ora has been interpreted to represent tropical wetland vegetation, preserved in low-energy depositional environments. The abundance of small, young leaves, as well as large blades of Malvaciphyllum macondicus in ne-grained sediments suggests little predepositional transport and therefore that the plants grew in the local setting of lower delta plain lakes, ponds, and swamps. In these environments, a large number of leaves could have been deposited and buried. The Eumalvoideae include a large number of herbaceous and woody species occurring in diverse habitats from tropical to temperate environments. In lowland tropical forests, eumalvoids are frequently associated with naturally disturbed habitats such as forest gaps, riverbanks, and along deltas (i.e., Talipariti spp.). These plants tend to grow in dense populations along river margins and swamps (Smith et al., 2004), consistent with sedimentological evidence for the sites where we recovered Malvaciphyllum macondicus fossils. Other fossil plants with similar inferred habitats and ecological characteristics co-occur with M. macondicus, including the heliophyte Montrichardia aquatica (Herrera et al., 2008) and various species of palms (Gmez-Navarro et al., 2009). The occurrence of Malvaciphyllum macondicus, along with two other malvalean fossil leaves from Cerrejn ora not described in this study (morphotypes CJ25 and CJ36; see Wing et al., 2009, Supporting Information), and the high pollen abundance of Bombacoideae suggest that derived lineages of Malvaceae were already a diverse element of neotropical rainforests of the late Paleocene. This adds specicity to previous observations that the middle-late Paleocene rainforests of South Amer-

ica already harbored the plant lineages that dominate neotropical forests in the present. LITERATURE CITED
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Appendix 1. List of genera of Malvaceae studied. Genera Adansonia L. Abelmoschus Medik. Abutilon Mill. Acaulimalva Krapov. Acropogon Schltr. Aguiaria Ducke Allosidastrum (Hochr.) Krapov., Fryxell & D. M. Bates Althaea L. Althofa K. Schum. Andeimalva J. A. Tate Anisodontea C. Presl Anoda Cav. Apeiba Aubl. Ayenia L. Bastardia Kunth Bastardiopsis (K. Schum.) Hassl. Batesimalva Fryxell Bernoullia Oliv. Berrya Roxb. Bombacopsis Pittier Bombax L. Bombycidendron Zoll. & Moritzi Brachychiton Schott & Endl. Briquetia Hochr. Brownlowia Roxb. Burretiodendron Rehder Byttneria Loe. Camptostemon Mast. Carpodiptera Griseb. Ceiba Mill. Christiana DC. Cienfuegosia Cothen. Clappertonia Meisn. Coelostegia Benth. Cola Schott & Endl. Commersonia J. R. Forst. & G. Forst. Corchoropsis Siebold & Zucc. Corchorus L. Corynabutilon (K. Schum.) Kearney Craigia W. W. Sm. & W. E. Evans Cristaria Cav. Cullenia Wight Cuningia S. Vidal Decastichia Rchb. Dendrosida Fryxell Dicraspidia Standl. Dombeya Cav. Durio Adans. Entelea R. Br. Eremalche Greene Eriolaena DC. Eriotheca Schott & Endl. Firmiana Marsili Fremontodendron Coville Fryxelia D. M. Bates Fuertesimalva Fryxell Gaya Kunth

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Genera Glossostemon Desf. Glyphaea Hook. f. Goethalsia Pittier Gossampinus Schott & Endl. Gossypium L. Grewia L. Guazuma Mill. Gyranthera Pittier Hainania Merr. Helicteres L. Heliocarpus L. Helmiopsiella Arenes Helmiopsis H. Perrier Heritiera Aiton Herrania Goudot Hibiscus L. Hildegardia Schott & Endl. Hoheria A. Cunn. Horsfordia A. Gray Howittia F. Muell. Huberodendron Ducke Jarandersonia Kosterm. Kearnemalvastrum D. M. Bates Keraudrenia J. Gay Kleinhovia L. Kokia Lewton Krapovickasia Fryxell Kydia Roxb. Lagunaria Rchb. Lasiopetalum Smith Lavatera L. Lawrencia Hook. Lecanophora Speg. Leptonychia Turcz. Luehea Willd. Malachra L. Malacothamnus Greene Malvastrum A. Gray Malvaviscus Fabr. Malvella Jaub. & Spach Malva L. Mansonia J. R. Drummond ex D. Prain Matisia Bonpl. Melhania Forssk. Melochia L. Meximalva Fryxell Microcos L. Modiola Moench Modiolastrum K. Schum. Mollia Mart. Monteiroa Krapov. Montezuma Moc, & Sesse ex DC. Mortoniodendron Standl. & Steyerm. Neobrittonia Hochr. Neobuchia Urb. Nesogordonia Baill. Nototriche Turcz.

Genera Octolobus Welw. Pachira Aubl. Palaua Cav. Paradombeya Stapf Patinoa Cuatrec. Pavonia Cav. Peltaea (C. Presl) Standl. Pentace Hassk. Pentapetes L. Pentapteris Haller Periptera DC. Phragmocarpidium Krapov. Phymosia Desv. ex Ham. Physodium C. Presl Pterygota Schott & Endl. Quararibea Aubl. Radyera Bullock Reevesia Lindl. Rhodognaphalopsis A. Robyns Rhyncosida Fryxell Robinsonella Rose & Baker f. Ruizia Cav. Rulingia R. Br. Scaphium Schott & Endl. Scaphopetalum Mast. Schoutenia Korthals Senra Cav. Septotheca Ulbr. Sida L. Sidalcea A. Gray Sidastum Baker f. Plagianthus J. R. Forst. & G. Forst. Pseudabutilon R. E. Fr. Pseudobombax Dugand Pterocymbium R. Br. Sitella L. H. Bailey Sphaeralcea A. St.-Hil. Spirotheca Ulbr. Sterculia L. Tarasa Phil. Tetralix Griseb. Tetrasida Ulbr. Theobroma L. Thomasia J. Gay Triplochiton K. Schum. Triumfetta L. Trochetia DC. Urena L. Waltheria L. Wercklea Pitter & Standl. Wissadula Medik.

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Appendix 2. Characters and character states used for optimization. Based on Ellis et al. (2009). Character 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 Leaf complexity Petiole insertion Leaf size Length: Width Ratio Shape of the lamina Medial symmetry of the lamina Basal symmetry of the lamina Lobation Margin Special features of the margin Base angle Base shape Apex angle Apex shape Terminal apex features Surface texture Surcial Glands Primary venation network Number of basal veins Agrophic veins Major secondary vein framework Interior secondaries Minor secondary course Perimarginal veins Major secondary spacing Variation of major secondary angle to midvein Major secondary attachment to midvein Intersecondary veins Intersecondary veinscourse Intersecondary veinslength Intersecondary veinstermination Intercostal tertiary venation framework Intercostal tertiary angle variability Epimedial tertiaries Exterior tertiary course Quaternary vein fabric Quinternary vein fabric Areolation Freely ending veinlets Marginal ultimate venation Tooth spacing Number of orders of teeth Veins forming teeth Number of teeth per cm Tooth sine Tooth shape Principal vein termination Principal vein course Principal vein curvature Accesory veins Course of major accesory veins Special features of the tooth apex Branching of major veins Character states 0: Simple; 1: Compound 0: Marginal; 1: Peltate 0: Microphyll; 1: Notophyll; 2: Mesophyll; 3: Macrophyll 0: 1-1; 1: 2-1; 2: 3-1; 3: 3-2; 4: 5-4 0: Elliptic; 1: Ovate; 2: Obovate 0: Strictly asymmetric; 1: Symmetric 0: Strictly asymmetric; 1: Symmetric 0: Non lobed; 1: Palmately lobed 0: Entire; 1: Dentate 0: Absent; 1: Thickened margin; 2: Sinuous margin; 3: Revolute margin 0: Reex; 1: Acute; 2: Obtuse 0: Cordate; 1: Convex; 2: Decurrent; 3: Cuneate; 4: Rounded; 5: Lobed; 6: Complex 0: Acute; 1: Obtuse 0: Acuminate; 1: Straight; 2: Convex; 3: Rounded 0: Non distinctive; 1: Mucronate; 2: Spinose 0: Smooth; 1: Pubescent 0: Absent; 1: Laminar; 2: On veins 0: Actinodromous; 1: Pinnate 0: 1; 1: 3; 2: 5; 3: 79 0: Absent; 1: Simple; 2: Compound 0: Basal eucamptodromous; 1: Craspedodromous; 2: Semicraspedodromous; 3: Brochidodromous 0: Absent; 1: Present 0: Semicraspedodromous; 1: Craspedodromous; 2: Brochidodromous 0: Absent; 1: Fimbrial veins 0: Consistent; 1: Inconsistent; 2: Abruptly increasing basally; 3: Gradually increasing basally 0: Consistent; 1: Inconsistent; 2: Gradually decreasing basally; 3: One pair of acute basal secondaries; 4: Gradually increasing basally 0: Excurrent; 1: Decurrent; 2: Deected 0: Absent; 1: Present 0: Parallel to secondaries; 1: Perpendicular to midvein 0: Same as subjacent secondaries; 1: Less than half of subjacent secondaries; 2: More than half of subjacent secondaries 0: With subjacent secondaries; 1: Basiexed; 2: Reticulate 0: Reticulate; 1: Alternate percurrent; 2: Opposite percurrent 0: Consistent; 1: Inconsistent; 2: Increasing exmedially; 3: Increasing proximally 0: Reticulate; 1: Alternate percurrent; 2: Opposite percurrent 0: Looped; 1: Terminating at the margin; 2: Looped with teeth 0: Alternate percurrent; 1: Opposite percurrent; 2: Reticulate 0: Irregular reticulate; 1: Regular reticulate 0: Good development; 1: Moderate development; 2: Poor development 0: Absent; 1: Non ramied; 2: Ramied 0: Ramied; 1: Anastomosing; 2: Fimbrial vein 0: Regular; 1: Irregular 0: 1; 1: 2; 2: 3 0: Primaries; 1: Secondaries; 2: Primaries and secondaries; 3: Secondaries and tertiaries; 4: Tertiaries; 5: Primaries, secondaries and tertiaries 0: One to two; 1: Three to ve; 2: Six to eight; 3: Nine to eleven 0: Curved; 1: Angular 0: Concave-concave; 1: Convex-concave; 2: Convex-convex; 3: Convex-exuous; 4: Flexuousconcave; 5: Flexuous-convex; 6: Flexuous-exuous; 7: Retroexed-straight; 8: Straight-straight; 9: Flexuous-straight 0: At tooth sine; 1: Submarginal; 2: At apex 0: Medial; 1: Closer to proximal ank; 2: Closer to distal ank 0: Straight; 1: Curved 0: Absent; 1: Present 0: Looped; 1: Convex; 2: Straight 0: Marginal; 1: Mucronate; 2: Spinose 0: Absent; 1: Only proximal; 2: Proximal and distal

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Appendix 3. List of collection vouchers used for leaf character coding and leaf character optimizations. Taxon. Voucher, locality, year, herbarium. HUA = Herbario Universidad de Antioquia, USNM = Smithsonian Natural History Museum, US = United States National Herbarium. Malvaceae Abelmoschus sagittifolius (Kurz) Merr. USNM Cleared leaf collection 10426. Abutilon asiaticum (L.) Sweet. Fosberg, 24827, Mariana Islands, 1946, US 2639870; USNM Cleared leaf collection 10427. Abroma augusta (L.) L. f. Forsberg 25828, Ngeanges Island, Caroline Islands, 1946, US 2431324; USNM Cleared leaf collection 1915. Adansonia digitata L. USNM Cleared leaf collection 3657. Aguiaria excelsa Ducke Ducke 25188, Province of Amazonas, Brazil, 1932, US 1618767. USNM Cleared leaf collection 9147. Apeiba aspera Aubl. Albert de Escobar 2154, Choc, Colombia, 1982, HUA 15905; Rudas A 3259, Amazonas, Colombia, 1992, HUA 119287; David H 2925, Caldas, Colombia, 2009, HUA 171951; USNM Cleared leaf collection 8037. Ayenia wygodzinskyi Cristbal USNM Cleared leaf collection 11448. Bastardia viscosa (L.) Kunth Albert de Escobar 729, El Oro Province, Ecuador, 1978, HUA 10280; Fonnegra 1400, La Guajira, Colombia, February 1980, HUA 11889; Bunch s.n., La Guajira, Colombia, HUA 14936; Bunch 187, La Guajira, Colombia, HUA 14039; Bunch 746, La Guajira, Colombia, HUA 14178; USNM Cleared leaf collection 6205, 10205. Berrya cordifolia (Willd.) Burret Britton 415, St. ChristopherNevis, 1901, US 428789; Robyns 6994, Sri Lanka, 1969, US 2612298; Pipoly JJ 7336, Guyana, 1986, US 3131458; USNM Cleared leaf collection 404. Bombax ceiba L. Specht 1175, Northern territory, Australia, 1948, US 2125226; USNM Cleared leaf collection 10055. Brachychiton populneus (Schott & Endl.) R. Br. Camp WH E-2898, Azuay Province, Ecuador, 1945, US 2167393; USNM Cleared leaf collection 3617. Brownlowia helferiana Pierre USNM Cleared leaf collection 3590. Brownlowia tersa (L.) Kosterm. USNM Cleared leaf collection 2171. Burretiodendron esquirolii (H. Lv.) Rehder USNM Cleared leaf collection 8041. Byttneria ancistrodonta Mildbr. Palacios 8140, Provincia de Sucumbos, Ecuador, 1991, US 3290270; Palacios 9021, Province of Sucumbos, Ecuador, 1991, US 3299287; USNM Cleared leaf collection 11516. Byttneria dentata Pohl. USNM Cleared leaf collection 11517. Ceiba pentandra (L.) Gaertn. Gentry 24534, Choc, Colombia, 1979, HUA 11125; Rodrguez W 144, Magdalena, Colombia, 1996, HUA 109211; Fonnegra 7369, Magdalena, Colombia, 2001, HUA 125723; USNM Cleared leaf collection 13357, 1912. Christiana africana DC. Albert de Escobar 1171, Provincia de El Oro, Ecuador, 1979, HUA 10213; USNM Cleared leaf collection 4593. Cienfuegosia drummondii (A. Gray) Lewton USNM Cleared leaf collection 10461. Cola nitida (Vent.) Schott & Endl. Vigne 1176, Gold Coast, Ghana, 1928, US 1429974; Cooper 336, Liberia, 1929, US 1378506; USNM Cleared leaf collection 14435. Commersonia bartramia (L.) Merr. Dietrich s.n., Queensland, Australia, US 205778; Hosakawa 6938, Palau Islands, 1933, US 2932222; Soejarto DD 14221, Quang Tri Province, Vietnam, 2008, US 3581477. USNM Cleared leaf collection 3623. Corchorus aestuans L. Irwin 21115, Gois Province, Brazil, US 2833229; Elias 751, Atlntico, Colombia, 1929, US 1443072; Tamayo 971, Falcn Province, Venezuela, 1938, US 1801830; Dugand 5000, Atlantico, Colombia, 1956, US 2252591; Koch 87271, Guerrero Province, Mexico, 1987, US 3363583; USNM Cleared leaf collection 1389. Cullenia ceylanica (Gardner) Wight ex K. Schum. USNM Cleared leaf collection 8054. Diplodiscus paniculatus Turcz. Clemens 616, Lanao del Sur, Philippines, 1907, US 3415457; Elmer 13267, Philippines, 1912, US 3415454; USNM Cleared leaf collection 3600. Dombeya burgessiae Gerard ex Harv. Soejarto DD 2328, Antioquia, Colombia, 1970, HUA 3025; Soejarto DD 2564, Antioquia, Colombia, 1970, HUA 2564; USNM Cleared leaf collection 9623. Durio grifthii (Mast.) Bakh, USNM Cleared leaf collection 11453. Durio lanceolatus Mast. USNM Cleared leaf collection 3666. Entelea arborescens R. Br. Fosberg 22563, Chimborazo, Ecuador, 1945, US 2109622; USNM Cleared leaf collection 3602. Eriolaena spectabilis (DC.) Planch. Ex Mast. Rock JF 1663, Chiengmai Province, Siam, 1922, US 1214561. Eriotheca globossa (Aubl,) A. Robyns Nuez 19422, Cusco, Peru, 1997; USNM Cleared leaf collection 9149. Firmiana colorata (Roxb.) R. Br. USNM Cleared leaf collection 8048. Fremontodendron decumbens R.M. Lloyd Gankin 737, California, US, 1966, US 3082463; USNM Cleared leaf collection 3629. Gaya gaudichaudiana A. St.-Hil. Gaudichaud-Breaupr, s.n., Rio de Janeiro, Brazil, US 2599921; USNM Cleared leaf collection 10464 (led as Gaya gracilipes). Glyphaea grewioides Hook. F. USNM Cleared leaf collection 4596.Goethalsia meiantha (Donn. Sm.) Burret Soejarto DD 3251, Antioquia, Colombia, 1972, HUA 3071; Loaiza 62, Antioquia, Colombia, 1980, HUA 12264; Giraldo LF 08, Antioquia, Colombia, 1994, HUA 91125; Snchez-Gmez JC 163, Antioquia, Colombia, 2006, HUA 168563; USNM Cleared leaf collection 3881. Grewia bicolor Juss. USNM Cleared leaf collection 11350. Grewia paniculata Roxb. Ex DC. USNM Cleared leaf collection 11503 (led as Microcos tomentosa). Guazuma ulmifolia Lam. White 481, Magdalena, Colombia, 1977, HUA 8083; Fonnegra 797, Antioquia, Colombia, 1978, HUA 7572; Palacio M s.n., Antioquia, Colombia, 1984, HUA 24133; Zardini 8478, Guaira Province, Paraguay, December 1988, HUA 69967; USNM Cleared leaf collection 3633. Gyranthera caribensis Pittier USNM Cleared leaf collection 10053. Helicteres guazumifolia Kunth USNM Cleared leaf collection 11402. Heliocarpus palmeri S. Watson Palmer 191, Chihuahua, Mexico, 1885, US 13314; USNM Cleared leaf collection 3606, 11371 (Filed under Heliocarpus glaber and Heliocarpus polyandrous). Heritiera ornithocephala Kosterm. USNM Cleared leaf collection 11408. Herrania purpurea (Pittier) R.E. Schult. Cogollo A 1415, Antioquia, Colombia, 1984, HUA 322473; Rentera 10899, Choc, Colombia, 1995, HUA 99400; Idrraga A 2901, Choc, Colombia, 2004, HUA 170332; Benavides JC 3027, Antioquia, Colombia, HUA 154282; USNM Cleared leaf collection 5567. Hibiscus ribifolius A. Gray Xantus 11, Baja California, Mexico, 1859, US 42462; USNM Cleared leaf collection 6215. Hildegardia barteri Mast. USNM Cleared leaf collection 7592, 14440. Huberodendron allenii Standl. & L.O.Williams Allen 6014, Puntarenas Province, Costa Rica, 1951, US 2215856; USNM Cleared leaf collection 3671. Jarandersonia paludosa Kosterman USNM Cleared leaf collection 8035. Keraudrenia collina Domin USNM Cleared leaf collection 3635. Kleinhovia hospita L. Unknown collector s.n., Canal zone, Panama, US 2800262. USNM Cleared leaf collection 1921. Kokia rockii Lewton USNM Cleared leaf collection s.n. Lagunaria patersonia (Andrews) G. Don USNM Cleared leaf collection 6213. Malvastrum spicatum (L.) A. Gray Sintenis 2996, Puerto Rico, 1886; Sintenis 3574, Puerto Rico, 1886; USNM Cleared leaf collection 10481. Malvaviscus arboreus Cav. Busch, s.n., Texas, US, 1900, US 386842; Molina 560, Bolivar, Colombia, HUA 16630; Marulanda 2149, La Guajira, Colombia, August 1990, HUA 75866; USNM Cleared leaf collection 6191, 6192, 6211, 16806. Mortoniodendron vestitum Lundell Contreras 7327, Petn Province, Guatemala, 1967, US 2558505; Lundell 18153, Petn Province, Guatemala, 1964, US 2479936; USNM Cleared leaf collection 3880. Neoregnellia cubensis Urb. Ekman Pl.ind.Occ.16692, Pinar del Ro, Cuba, 1923, US 2225018; Leonard 13142, La Hispaniola, 1929, US 1451820; USNM Cleared leaf collection 3646. Nesogordonia dewevrei (De Wild. & T. Durand) Capuron ex R. Germ. USNM Cleared leaf collection 3593, 4599. Ochroma pyramidale (Cav. Ex Lam.) Urb. Fonnegra 2187, Antioquia, Colombia, 1987, HUA 38291; Duque A 2382, Caldas, Colombia, 2001, HUA 134824; David H 1214, Caldas, Colombia, 2005, HUA 149414; USNM Cleared leaf collection 10233. Octolobus angustatus Hutch. USNM Cleared leaf collection 4616, 14443.

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Pachira quinata (Jacq.) W.S. Alverson Gmez A 566, Antioquia, Colombia, 1992, HUA 81387; Callejas 12230, Antioquia, Colombia, 1990, HUA 116541; Velsquez-R 5762, Antioquia, Colombia, 2009, HUA 168121; USNM Cleared leaf collection 2546. Paradombeya rehderiana Hu USNM Cleared leaf collection 8063 Patinoa sphaerocarpa Cuatr. Krukoff 4656, Amazonas, Brazil, 1933, US 1691072; USNM Cleared leaf collection 10059. Pavonia rmiora Schery Pringle 5447, Jalisco, Mxico, 1893, US 305777; USNM Cleared leaf collection 6209, 16924. Pentace curtisii King USNM Cleared leaf collection 11504. Phymosia rosea (DC.) Kearney Skutch 1025, Department of Huehuetenagi, Guatemala, 1934, US 1644029; USNM Cleared leaf collection 16811, 10484. Pseudobombax septenatum (Jaq.) Dugand Vargas WG 6377, Caldas, Colombia, 1999, HUA 117332; Prez J 964, Santander, Colombia, 1999, HUA 12724, Fernndez-Alonso 22521, Santander, Colombia, 2004, HUA 169531; USNM Cleared leaf collection 3660. Pterocymbium tinctorium Merr. USNM Cleared leaf collection 8051. Pterospermum acerifolium Willd. USNM Cleared leaf collection 1150. Pterygota forbesii Muell. USNM Cleared leaf collection 8047. Quararibea (Matisia) ochrocalyx (K. Schum.) Vischer USNM Cleared leaf collection 3674. Quararibea turbinata (Sw.) Poir Sintenis 6289, Puerto Rico, 1886; Axelrod 8270, Puerto Rico, 1994; USNM Cleared leaf collection 3677. Reevesia thyrsoidea Lindl. USNM Cleared leaf collection 1925. Rulingia madagascariensis Baker Hildebrandt 3662, Madagascar, 1880, US808373; USNM Cleared leaf collection 3651. Scaphium macropodum Beumee ex K. Heyne USNM Cleared leaf collection 8049. Schoutenia hypoleuca Pierre Pierre 659, Cambodia, US 2913962; USNM Cleared leaf collection 518, 519. Spirotheca rivieri (Decne.) Ulbr. USNM Cleared leaf collection 3668. Sterculia apetala (Jacq.) H. Karst. Palacios 8948, Sucumbos Province, Ecuador, 1991, US 3258986; Little 671, Morona-Santiago, Ecuador, US 2972702; Ortega 36, MoronaSantiago, Ecuador, 1976, US 3003289; USNM Cleared leaf collection 11428. Theobroma cacao L. Hoyos Marin S 156, Antioquia, Colombia, 1983, HUA 18169; Santa J 1053, Valle del Cauca, Colombia, 1984, HUA 22480; Fonnegra 2721, Antioquia, Colombia, 1989, HUA 60730;Vlez JG 5444, Valle del Cauca, Colombia, April 2003, HUA 138678; Hoyos-Gmez SE 521, Choc, Colombia, 2005, HUA 160504; David H 1184, Caldas, Colombia, 2005, HUA 148970; USNM Cleared leaf collection 3884. Thespesia cubensis (Britton & P. Wilson) J.B.Hutch USNM Cleared leaf collection 3847, 16930. Tilia cordata Mill. Steinle s.n., Maryland, US, 1958, US 2262316; Allard 20508, Virginia, US, 1952, US 2098497; Ward, s.n., District of Columbia, US, 1884, US 136368; USNM Cleared leaf collection 120. Triplochiton scleroxylon K. Schum. Chevalier 16105, Cte-dIvoire, 1907, US 2543376; USNM Cleared leaf collection 3656, 4609, 14449. Triumfetta speciosa Seem. USNM Cleared leaf collection 11510, 17093. Trochetia parviora Bojer USNM Cleared leaf collection 4612. Wercklea ferox (Hook. f.) Fryxell Nuez 23921, Cusco, Peru, 1998, US. Euphorbiaceae Acalypha cinta Mll. Arg. USNM Cleared leaf collection 11463. Acalypha macrostachya Jacq. USNM Cleared leaf collection 11471. Alchornea triplinervia (Spreng.) Mll. Arg. USNM Cleared leaf collection 11481. Croton euryphyllus W.W. Sm. USNM Cleared leaf collection 11588 (Filed as Croton caudatiformis). Croton gossypiifolius Vahl. USNM Cleared leaf collection 11571, 15198 (Filed as Croton draco). Dalechampia tiliifolia Lam. USNM Cleared leaf collection 11596. Dalechampia aristolochiifolia Kunth USNM Cleared leaf collection 11598. Discocleidian rufescens

(Franch.) Pax & K. Hoffm. USNM Cleared leaf collection 3022. Givotia rottleriformis Griff. ex Wight USNM Cleared leaf collection 9046. Jatropha gossypiifolia L. USNM Cleared leaf collection 3061. Mallotus japonicus (L. f.) Mll. Arg. USNM Cleared leaf collection 38, 9090, 11720. Melanolepis multiglandulosa (Reinw. Ex Blume) Rchb. F. & Zoll. USNM Cleared leaf collection 871. Vitaceae Cissus caesis Afzel. USNM Cleared leaf collection 4948. Vitis betulifolia Diels & Gilg USNM Cleared leaf collection 261, 262. Vitis vinifera L. Field 761, Iraq, 1939, US 1741428; Unknown collector s.n., Italy, US 17449. Hamamelidaceae Corylopsis veitchiana Bean. USNM Cleared leaf collection 528. Liquidambar stryraciua L. USNM Cleared leaf collection 60, 928, 11912, 14582, 14583. Parrotiopsis jacquemontiana (Decne.) Rehder USNM Cleared leaf collection 1128 (led as Parrotia jacquemontiana). Moraceae Bagassa guianensis Aubl. USNM Cleared leaf collection 9102. Morus insignis Bureau Dorr 8749, Trujillo Province, Venezuela, 2000, US 3406012. Morus alba L. USNM Cleared leaf collection 10900. Sapindaceae Acer opalus Mill. USNM Cleared leaf collection 9622. Acer pensylvanicum L.USNM Cleared leaf collection 1176b. Urticaceae Boehmeria nivea (L.) Gaudich. USNM Cleared leaf collection 10911. Boehmeria spicata (Thunb.) Thunb USNM Cleared leaf collection 10912. Cucurbitaceae Sechium edule (Jacq.) Sw. Degener 12753, Kuai County, Hawaii, United States, 1940, US 1864564; Wagner 5680, Maui, Hawaii, United States, 1986, US 3283040. Calycophysum spectabile (Cogn.) C. Jeffrey & Trujillo Dorr 8719, Trujillo Province, Venzuela, 2000, US 3406431; Stergios 18927, Trujillo Province, Venzuela, 2001, US 3403467. Cercidiphyllaceae Cercidiphyllum japonicum Siebold & Zucc. USNM Cleared leaf collection 26, 148 150, 397. Cochlospermaceae Cochlospermum vitifolium (Willd.) Spreng. USNM Cleared leaf collection 3236. Platanaceae Platanus orientalis L. USNM Cleared leaf collection 1545. Platanus occidentalis L. USNM Cleared leaf collection 729 732. Cannabaceae Humulus lupulus L. USNM Cleared leaf collection 6042. Rosaceae Stephanandra chinensis Hance USNM Cleared leaf collection 1540. Crataegus douglasii Lindl. USNM Cleared leaf collection 1436, 1437. Elaeocarpaceae Aristotelia chilensis (Molina) Stuntz USNM Cleared leaf collection 3187. Muntingia calabura L. USNM Cleared leaf collection 3193.