Paleocene Malvaceae from Northern South America

Home , Commersonia, Entelea, Eriotheca, Fremontodendron, Glossostemon, Glyphaea

American Journal of Botany 98(8): 1337–1355. 2011.

P ALEOCENE MALVACEAE FROM NORTHERN SOUTH AMERICA AND THEIR BIOGEOGRAPHICAL IMPLICATIONS 1

M ó nica R. Carvalho2 – 4,7 , Fabiany A. Herrera 3,5 , Carlos A. Jaramillo3 , Scott L. Wing6 , and Ricardo Callejas 2

2 Instituto de Biolog í a, Universidad de Antioquia, Medell í n, Colombia; 3 Smithsonian Tropical Research Institute, CTPA, Panama City, Panama; 4 Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802 USA; 5 Department of Biology and Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 USA; and 6 Department 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 Malvoid- eae, obscures interpretations of past distributions. We describe fossil leaves of Malvoideae from the middle-late Paleocene Cerrej ó n Formation in Colombia, which contains evidence for the earliest known neotropical rainforest. • Methods: Fifty-six leaf compressions belonging to Malvaceae were collected from the Cerrejó n Formation in northern Colom- bia. Leaf architectural characters were scored and optimized for 81 genera of Malvaceae. Synapomorphic characters and unique character combinations support natural afﬁ nities 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 58– 60 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 Malvaceae is one of the most dominant plant families in neo- than 4500 species in nearly 250 genera. Nine subfamilies have tropical forests, both in terms of abundance and species number been recognized as monophyletic, regrouping traditional para- ( Terborgh and Andresen, 1998 ; ter Steege et al., 2000 ; Burnham phyletic Sterculiaceae, Tiliaceae, and Bombacaceae within an and Johnson, 2004). The informal but well-supported Mal- expanded Malvaceae ( Bayer et al., 1999 ; Kubitzki and Bayer, vatheca group ( Baum et al., 1998 , 2004 ) combines Bomba- 2003 ). This regrouping has been supported by various morpho- coideae and Malvoideae into one of the most speciose clades logical and anatomical synapomorphies as well as molecular (ca. 1300 species) within Malvaceae and one of the most con- data (Judd and Manchester, 1997; Alverson et al., 1998, 1999 ; spicuous groups in the neotropics. Malvoideae comprises tradi- Bayer et al., 1999 ). tional Malvaceae sensu stricto ( Baum et al., 1998 , 2004 ) as well as various tropical lineages traditionally included in the Bom- bacaceae, namely, Camptostemon , Quararibea , Matisia , and 1 Manuscript received: 30 December 2010; revision accepted: 27 May 2011. Phragmotheca ( Fig. 1 ). This work was supported by a short-term fellowship at the Smithsonian The oldest record for the Malvatheca group is based on pol- Tropical Research Institute and a partial Jos é Cuatrecasas fellowship in the len from the Maastrichtian of New Jersey attributed to Bomba- Department of Botany of the Smithsonian Museum of Natural History (MRC), Carbones del Cerrejó n and the Smithsonian Paleobiology coideae (Wolfe, 1975), suggesting pre-Cenozoic divergence Endowment Fund (FAH), a Smithsonian Unrestricted Endowment Grant times for the major clades within this family. Due to the con- (CJ, SW), and NSF grants DEB-0733725 (CJ), and DEB-0919071 (MRC), spicuous palmate venation of many extant Malvaceae, many the Fundació n para la Promoció n de la Investigació n y la Tecnologí a, palmately veined fossil leaves dating back to the Late Cretaceous Banco de la Rep ú blica, the Colombian Petroleum Institute, and Fundaci ó n have been assigned to this family, usually under paraphyletic Ster- Ares (CJ, FAH), the Evolving Earth Foundation (FAH), the Geological culiaceae ( Table 1 ) ( Ward, 1887 ; Lesquereux, 1891 ; Knowlton, Society of America Foundation (FAH), the Gary S. Morgan Student 1902 , 1917 , 1923 , 1930 ; Fontaine, 1905 ; Berry, 1929 ; Hollick, Research Award (FAH), and the Lewis & Clark Foundation-American 1930 , 1936 ; MacGinitie, 1974 ; Wolfe, 1977 ); however, high Philosophical Society (FH). The authors thank L. Teicher, F. Chavez, G. levels of homoplasy and foliar character convergence make it Hern á ndez, C. Montes, A. Rinc ó n, and the geology team at the Cerrej ó n diffi cult to assess their natural affi nities. More reliable taxo- mine for fi eldwork support. M.R.C. especially thanks Laurence Dorr for taxonomic discussions and Lisa Barnett, Peter Wilf, Vicky Funk, Emily nomic identifi cations have been supported by the co-occurrence Wood, Alvaro Id á rraga, and curators at US, A, HUA and SCZ herbaria. of leaves and associated plant organs (Kva č ek et al., 2002; 7 Author for correspondence (e-mail: [email protected]) Kva ček, 2004, 2006 ), preservation of cuticular features (Pan and Jacobs, 2009; Worobiec et al., 2010), whole-plant interpre- doi:10.3732/ajb.1000539 tations ( Kvač ek, 2008 ), reproductive structures ( Duarte, 1974 ;

Here we describe a new species of the Malvatheca group from a middle to late Paleocene (58 – 60 Ma) tropical rainforest in Co- lombia (Wing et al., 2009). This species is assigned to Malvoid- eae, based on overall leaf morphology and the identiﬁ cation 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 family ’ s natural variation and identify traits that may have become ﬁ 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 group’s 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 Cer- rejó n Formation, exposed in the Cerrejó n coal mines in the Cesar-Rancherí a basin, northern Colombia (11° 9 ′ 14.58 ″ N, 72° 36 ′ 30.43 ” W; Fig. 2 ). The Cerre- jó n Formation is a 700 m thick sequence of coal beds, fl 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 fl 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 11° 07 ′ 49.4 ° N, − 72 ° 34 ′ 60.5 °W) that we infer to represent a swampy-lacustrine environment because the bed is very fi 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, − 72.57 ° W) that we infer was deposited in a fl uvial channel because it is composed of cross-laminated silt and fi ne sand and has a lenticular cross section. Fig. 1. Distribution and phylogenetic relationships of major groups Fossil leaves were described according to shape and venation characters within the Malvatheca group (modifi ed from Baum et al., 2004 ). 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 Kva č ek et al., 1991 , 2002 ; Manchester, 1992 , 1994 ), and ana- branching and branching toward the apex as distal branching ( Fig. 3A, B ). tomically preserved wood ( Manchester, 1979 , 1980 ). The fossil Type specimens were drawn under camera lucida on a Nikon SMZ1500 record of leaves attributed to Malvaceae or its segregate fami- stereoscope and digitized with Adobe (San Jose, California, USA) Illustrator lies ranges from the Late Cretaceous to the late Neogene, in- CS4. Specimens were photographed with a Nikon DS70 and DMX1200F and cluding reports from the Cretaceous of North America (Hollick, observed with epifl uorescence using a Nikon Eclipse 50i microscope coupled to 1930 , 1936 ), lower Miocene of Europe ( Kvač ek et al., 2002 ; a mercury lamp, to detect preserved cuticle fragments. When present, leaf fragments were removed from the specimen and treated with Calgon 10% solution Kva ček 2008), Miocene of Argentina (Anz ó tegui and Cristalli, for 7 d, rinsed, followed by digestion with 10% HF for 1 – 2 h. Loose cuticle 2000 ) and late Oligocene of Africa ( Pan and Jacobs, 2009 ). fragments were mounted in glycerin and observed under epifl uorescence. Despite the extensive Late Cretaceous and Cenozoic fossil An exhaustive morphological comparison was performed with numerous record of Malvaceae, molecular clock approximations infer angiosperm families similar to Malvaceae using the National Cleared Leaf Col- fairly recent divergence times (Wikstrom et al., 2001; Magall ó n lection stored at the Smithsonian Natural History Museum (USNM), and bo- and Castillo, 2009). Magall ó n and Castillo (2009) estimated the tanical specimens at the Harvard University Herbaria (A), United States National Herbarium (US), Herbario Universidad de Antioquia (HUA), and the divergence of crown group Malvales at 33.9 Ma, much younger Smithsonian Tropical Research Herbarium (SCZ). Over 375 genera of Euphor- than the Late Cretaceous/early Cenozoic fossil record of fami- biaceae, Moraceae, Bixaceae, Urticaceae, Cucurbitaceae, Sapindaceae, Vita- lies within the order ( Magall ó n et al., 1999 ). The underestima- ceae, Eleaeocarpaceae, and other families with palmately veined leaves were tion probably results from a combination of low taxon sampling examined to establish similarities between the fossils and any of these lineages within Malvales and the use of derived fossil taxa as calibration (Appendix S1; see Supplemental Data with the online version of this article). points. The latter may mean that the estimated age for diver- Once affi nities to distantly related lineages were discarded based on consistent morphological differences in overall venation and tooth characters, the fossil gence of crown Malvales actually corresponds to divergences leaves were compared to a broad survey of Malvaceae. One hundred and sev- within the order and would thus decrease the “ super high” di- enty genera of Malvaceae were studied (Appendix 1); 81 of these were scored versifi cation rates estimated for Malvales by Magall ó n and for 53 leaf morphology characters based on the Ellis et al. (2009) Manual of Castillo (2009) . Leaf Architecture, including features of overall leaf shape, venation, and teeth August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1339

b 20 veins Source Accesory Anastom 19 vein vein course Principal Curv-prox Teeth Teeth order Sinus Symmetry Tooth Tooth shape vein vein Major branching Quaternary venation Tertiary Tertiary venation veins Agrophic Minor secondaries veins Secondary

Primary venation venation Comp PinnateComp Semicrasp Pinnate Semicrasp Brochid Absent Brochid Ret Absent Ret Ret Ret – Cc-Cc – 1 Angular – Asym Str-prox – Absent – 4 – – – 3 Lamina 3 Lobed3 Lobed Actino 3 Actino3 Lobed Brochid Pinnate Brochid Brochid Brochid Brochid Comp Brochid S Ret S Ret Ret Ret Ret – Ret – – – – – Cv-Cc 1 – – Curved – Asym – Absent Absent – – 18 – – – 8 17 3 Lobed Actino Brochid Brochid S Ret Ret ? – – – – – – 5 3 Lobed Actino Brochid Brochid Comp Opp Ret Prox – – – – – – 12, 13, 3 Lobed Actino 3 Brochid Brochid S Opp Ret – – – – – – – 7 3 Lobed Actino Crasp Crasp Comp Alt ? Prox – – – – – – 14 3 Lobed Actino3 Lobed Brochid Actino Brochid Brochid Brochid Comp Comp Opp Opp Ret Ret Pro Prox – – – – – – – – – – – – 14 11 3 Lobed Actino 5 Semicrasp Semicrasp Comp Opp Ret Prox Cv-Cc 2 Angular Asym Curv-prox ? 19 3 Lobed Pinnate Crasp Brochid S Opp ? Prox Cv-Cv 1 Curved Asym ? ? 7 3 Lobed Actino 5 Semicrasp Semicrasp Comp Ret Ret– Cc-Cc 1 Angular Asym ? ? 6 UnlobedUnlobed Actino Actino Crasp Crasp Crasp Crasp S Comp Opp Opp Opp Ret – Prox Cv-Cv Cv-Cc 1 1 Angular Curved Sym Asym Str-prox Curv-prox Cv Cv 19 2 Unlobed PinnateUnlobed Actino 3 Crasp Crasp Crasp Crasp S S Opp Opp ? ? Prox Cv-Cc– 1 Cv-Cc Angular 1 Asym Angular Curv-prox Asym ? Str-prox ? 2 3 Unlobed Pinnate Crasp Brochid S Opp Ret – – – – – – – 7 Unlobed Actino 7 Crasp Crasp Comp Opp ? Prox Cv-Cv 1 Angular Sym Med, curv ? 7 Unlobed ActinoUnlobed Semicrasp Actino Semicrasp Crasp Comp Opp Crasp Ret S Prox Opp Cv-Cv 1 Opp Angular Asym – Med, curv Cc-Cc ? 1 Angular 19 Asym Curv-prox Cv 16 Unlobed Actino 3Unlobed Semicrasp Pinnate SemicraspUnlobed Brochid ActinoUnlobed S Brochid Pinnate CraspUnlobed Opp Pinnate Crasp S Crasp Crasp Opp Crasp Ret Brochid S– S S ? Opp Cv-Cv 1 Alt Opp Prox ? Angular ? Sym – – ? Str-prox – Cv-Cv Cv – 1 Prox – Cv-Cc Curved 18 Cv-Cv 1 Sym 1 – Curved Curved Asym Sym Str-prox – Str-prox Cv ? – 9 7 2 UnlobedUnlobed Actino Actino 5Unlobed CraspUnlobed Brochid Pinnate Pinnate Semicrasp Brochid Crasp Semicrasp Brochid Comp Comp Brochid Comp Alt Opp Opp S Opp Ret Alt Ret – – Prox Ret Cv-Cv – – 1 – Angular – – Sym – – – Med-Str Anastom – 8 – – – – – – – – – 7, 8 18 – 17 dissection

Weber.

Unger Unger Berry Hollick

Hollick

Sap. Fontaine Hollick

Unger Hollick Berry novimundi reticulata subtilis labrusca basiauriculata elegans atwoodi eakini ” alaskana crenata newberryana ” ” ” ” ” ” improvisa ” ” ” ” ” 1. fossil leaves. Morphological comparison of Malvaceae Lesquereux MacGinite Berry Hollick Lesquereux Lesquereux Knowlton Heer Lesquereux Knowlton Knowlton MacGinite Knowlton Heer Hollick Berry Hollick Lesquereux Berry MacGinite Berry Hickey Sterculia Sterculia Sterculia Sterculia Sterculia Grewia Grewia Sterculia Luehea Abutilon Apeiba Dombeya “ “ “ Grewiopsis tiliacea Grewiopsis tuscaloosensis Grewiopsis Grewiopsis wadii Grewiopsis yukonensis Grewiopsis “ “ “ “ Dombeyopsis obtusa Dombeyopsis ovata Dombeyopsis plantanoides Dombeyopsis Grewiopsis acuminata Grewiopsis formosa Grewiopsis Dombeyopsis lobata Dombeyopsis Table Taxon Pterospermites haquei Pterospermites Pterospermites carolinensis Pterospermites dentatus Pterospermites conforme Pterospermum “ “ “ “ Apeibopsis atwoodi Apeibopsis cyclophylla Bombacites eocenicus Bombacites jacksonensis “ decheni Dombeyopsis 1340 American Journal of Botany [Vol. 98

b (Appendix 2; online Appendix S2). The scored genera were chosen based on 74 ; their inclusion in published phylogenetic analyses and thorough sample avail- ability, 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

?19 other subfamilies in genera and species. In this case, a few genera of each of the

veins Source main tribes (Hibisceae, Malveae, and Gossypieae; sensu Kubitzki and Bayer, Accesory 2003 ) were selected to keep a comparable number of representative genera for each subfamily. When possible, the species directly included in these published analyses

vein vein were scored (see Appendix 3 for taxa and voucher information); otherwise, re- course Straight Principal cent 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 romous, Cc = Concave, Comp = Compound, Crasp romous, Cc = Concave, ( Maddison and Maddison, 2003 ). Topologies were analyzed both indepen-

asp = Semicraspedodromous, Str Straight, S Simple, dently and by combining them in a supertree topology.

Teeth Teeth order Sinus Symmetry 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

y, y, 1977; 7, Hollick, 1930 ; 8, Hollick, 1936 ; 9, Knowlton, 1899 ; 10, one lineage within the same tribe, and since this character exploration aims to Tooth Tooth shape Cv-Cv 2 Curved Sym ? ?look at 1 a higher hierarchical resolution, the inclusion of polyphyletic genera did not have a major effect on the results. Character optimization did not conﬂ ict between independent trees and the ‘ supertree ’ . Most of the examined leaf fea- vein vein Distal Major tures are highly homoplasious within Malvaceae, and for this reason, only char- branching acters inferred to be synapomorphic and characters conserved within various clades at various levels are discussed to support taxonomic afﬁ nities of the fossil leaves. Fossils are stored in the paleontological collections of the Colombian Geo- logical Institute (INGEOMINAS) in Bogotá , Colombia (repository acronym Quaternary venation ING).

Tertiary Tertiary venation SYSTEMATICS

Family— Malvaceae Juss. veins

Agrophic Subfamily— Malvoideae

Morphogenus— Malvaciphyllum Anz ó tegui ek, 2008 ; 14, Lesquereux, 1878 ; 15, Lesquereux, 1883 ; 16, Lesquereux, 1887 ; 17, Lesquereux, 1891 ; 18, MacGinitie, 19 ; 18, Lesquereux, 1891 ; 17, Lesquereux, 1887 ; 16, Lesquereux, 1883 ; 15, Lesquereux, 1878 ; 14, ek, 2008 č Minor

secondaries Morphospecies— Malvaciphyllum macondicus M. Carvalho sp. nov.

Diagnosis— Leaves ovate, dentate to crenate, petiole doubly veins

Secondary pulvinate. Length to width ratio ~1 : 1, apex shape straight. Base

a strongly cordate. Laminar surface pubescent. Primary veins ac-

ek et al., 2002 ; 13, Kva Kva ; 13, ek et al., 2002 tinodromous, 5 – 9 basal primary veins; secondary veins craspe- č dodromous, ﬁ rst pair of costal secondary veins branching Primary venation venation proximally and distally. Tertiary veins opposite convex to chev- roned percurrent, fourth order veins mixed opposite/alternate percurrent, freely ending veinlets branched. Teeth two to three orders, symmetrical, convex-convex, principle veins of teeth Lamina 3 Lobed Actino 3 Brochid Brochid S Opp Ret – – – – – – – 19 UnlobedUnlobed PinnateUnlobed Pinnate Crasp Actino Crasp Crasp Crasp Crasp Crasp S S Comp Opp Opp Opp ? ? ? Prox Prox Prox Cv-Cc Cv-Cc Cv-Cc 1 1 1 Angular Angular Angular Asym Asym Asym Curv-prox Curv-prox Med- ? ? 7 3 UnlobedUnlobed ActinoUnlobed Actino Actino Crasp Crasp Crasp Crasp Crasp Crasp Comp Comp Comp Opp Opp Opp Opp Ret Ret – Prox Prox, Cv-Cv Cv-Cc 1 1 Angular Angular Asym Asym Med, Curv-prox curv Anastom Cv 15 10 dissection medial and straight, accessory veins looped.

Holotype hic designatus— ING 1410 ( Fig. 4B, C ; 5D, E ). Heer. Knowlton Berry Lesquereux Heer Anz ó tegui Paratypes — ING 1411; ING 1357 ( Fig. 4A ); ING 1074; ING 0617; ING Hollick 1077 ( Fig. 4D ); ING 1091 ( Fig. 5F ) tenuinervis ” Actino = Actinodromous venation, Alt = Alternate percurrent, Anastom = anastomosing, Asym = Asymmetrical, Brochid = Brochidod Asym = Anastom = anastomosing, Alternate percurrent, Alt = Actinodromous venation, Actino = Studied material— 56 specimens: ING 0616– 0620, ING 0984, ING cretacea jacksoniana malmgreni populifolia speciosissima 1. Continued. ” ” ” ” ” 0985, ING 1056, ING 1075 ( Fig. 5A ), ING 1076 – 1078, ING 1080 – 1096, ING References: 1, Anz ó tegui and Cristalli, 2000; 2, Berry, 1919; 3, Berry, 1924b; 4, Berry, 1930; 5, Fontaine, 1905; 6, Hicke 1930; 5, Fontaine, 1924b; 4, Berry, 1919; 3, Berry, and Cristalli, 2000; 2, Berry, tegui ó Anz 1, References: Numbers in parentheses correspond to the number of basal veins. Notes: a b

quenquiadensis 1097 ( Fig. 5C ), ING 1098, ING 1099 – 1101, ING 1102 ( Fig. 5B ), ING 1103 – Tilia Tilia Tilia Sterculia Tilia Tilia Knowlton, 1917 ; 11, Knowlton, 1922 ; 12, Kva Kva ; 12, 1922 Knowlton, ; 11, 1917 Knowlton, 19, Schenk, 1890 ; 20, Unger, 1850 Unger, ; 20, Schenk, 1890 19, “ “ “ Table Taxon “ “ “ Malvaciphyllum Craspedodromous, Curv = Curved, Cv = Convex, Med = Medial, Opp Opposite percurrent, Prox proximal, Ret Reticulate, Semicr Cv = Convex, Craspedodromous, Curv = Curved, Sym = Symmetrical, ? uncertain. 1121, ING 1357, ING 1358, ING 1410, ING 1411. August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1341

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, Rancher í a Basin, Cerrej ó n Formation, Cerrej ó n 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, coordi- nates 11.14° N, 72.57 ° W; ING 1357, ING 1074, ING 0617, ING 1077, and 45 other specimens were collected in fi ve localities at Pit Tabaco Extensi ó n, between coal beds 170 and 175, coordi- nates 11.13° N, 72.58 °W. The age of the entire coal-bearing section of the Cerrej ó n Formation has been estimated as middle to late Paleocene (58– 60 Ma). This age estimate is based on biostratigraphic correlations and has been described elsewhere Fig. 2. Collection site for Malvaciphyllum macondicus sp. nov., Cer- ( Jaramillo et al., 2007 ). rej ó n coal mines, Guajira, Colombia. Systematic affi nity within angiosperms — Palmate leaf venation, toothed margins, and stellate trichomes are wide- Etymology— The epithet “ macondicus ” refers to the fi ctional town Ma- spread and conspicuous in most Malvaceae ( Kubitzki and condo, described by Gabriel Garc í a M á rquez (1970) in One Hundred Years of Bayer, 2003). However, these characters occur in other line- Solitude . This town epitomizes the lifestyle and culture of the Caribbean coast ages of angiosperms, refl ecting the repeated evolution of of Colombia, the area from which these fossils come. palmate venation patterns (White, 2005). Despite this evolutionary trend, tooth shape and venation characters exhibit fa- Description— The fossil leaves are microphyllous to mac- milial and generic level consistency, being useful in taxonomic rophyllous leaf compressions; the one complete petiole is 5.08 and phylogenetic studies at different hierarchical levels cm long × 0.37 cm wide, doubly pulvinate and terete. The ( Hickey and Wolfe, 1975 ; Fuller and Hickey, 2005 ; Doyle, laminar shape varies from ovate to elliptic, 9.25 (3.99 – 17.54) 2007 ). cm (measured in 11 specimens) long and 8.85 (3.34– 16.4) cm Teeth of Malvaceae follow a consistent morphological pat- (measured in 14 specimens) wide. The leaves exhibit a tern different from that in other palmately veined lineages: they straight-sided, acute apex, and a base that is cordate, with a are symmetrical to asymmetrical laminar projections with a basal extension asymmetry and a refl ex angle (Fig. 4B). The medial principal vein and generally have accessory veins form- laminar surface is densely pubescent, covered with coalifi ed ing a series of looping arches that terminate at the tooth apex stellate and acicular trichomes (observed in specimens ING (Fig. 3G, H); such teeth have been called malvoid (Hickey and 1410, ING 1411; Fig. 5D, E). The primary vein framework is Wolfe, 1975 ). Teeth of this type are observed in Malvaciphyl- actinodromous, with 5– 9 veins arising from the base. Costal lum macondicus . Principal (and accessory) veins terminate at secondary veins are craspedodromous, excurrent on primary the tooth margin without any type of glandular thickenings or veins, and increasing in spacing proximally. Agrophic veins processes such as mucros, papillae, or foramina found in other are compound, with the minor secondaries arising exmedially palmately veined, toothed angiosperm lineages. from the basal veins. The fi rst pair of costal secondaries and Families with similar palmately veined, toothed leaves, such minor secondaries bear a pair of minor secondary veins that as Euphorbiaceae, Vitaceae, Gunneraceae, Moraceae, Rosa- branch both proximally and distally close to the margin (Fig. ceae, among others (online Appendix S1), show distinctive 5B ). Tertiary venation is opposite percurrent, concentric to tooth morphology, including various types of glandular thick- the base of the lamina; costal tertiaries are sinuous to straight; enings and accessory veins that differ from those seen in extant epimedials are admedially perpendicular to the midrib and ex- Malvaceae and Malvaciphyllum macondicus (For detailed com- medially parallel to costal tertiaries. Fourth order veins are parison between families, see online Appendix S1). Mucronate mixed opposite/alternate percurrent; fi fth order veins are reg- and glandular tooth terminations on asymmetrical teeth in ular reticulate. Tertiary and fourth order veins are very thick Euphorbiaceae ( Klucking, 2003 ) and translucid papillae in compared to primary veins. Areolation is well developed with Vitaceae distinguish the two most phenetically similar families branched freely ending veinlets, and the ultimate marginal ve- from M. macondicus . Species of Bixaceae are closely related to nation is looped. Malvaceae, yet differ in having asymmetric teeth with a princi- The teeth are regularly spaced, 5 cm on average (minimum 2, pal vein that terminates in the sinus and not the apex of the maximum 7), and occur in two to three discrete orders of teeth tooth. Eleaocarpaceae, a family that used to be part of Malvales distinguished by their size and the gauge of the veins that enter but that is presently thought to be distantly related to Malva- them (Fig. 4A). The fi rst order teeth are generally present and ceae, differs in having teeth with principal veins that extend supplied by the fi rst pair of lateral primaries; they are convex- beyond the blade lamina. straight in shape, and their sinuses vary from curved to angular. The combination of characters seen in Malvaciphyllum ma- Second and third order teeth are consistently present and are condicus: palmately veined leaves, stellate and acicular supplied by second and third order veins, respectively; they trichomes, double pulvinus, and the distinctive tooth venation have angular sinuses, and their shapes range from convex-convex are consistent with and indicative of Malvaceae. There are not to fl exuous-fl exuous, symmetrical to slightly asymmetrical. any other angiosperm lineages that exhibit this combination of All teeth exhibit a medial principal vein that terminates at the characters. 1342 American Journal of Botany [Vol. 98 August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1343

Character optimizations and affi nities within Malva- eumalvoids is supported by the occurrence of the two charac- ceae— Simple, palmately veined leaves with dentate-crenate ters that are unique to Eumalvoideae as well as the similarity in margins are common in six of nine subfamilies within Malva- overall leaf architecture. Given that most other features are ceae, including Byttnerioideae, Grewioideae, Helicteroideae, highly homoplasious, we consider that the costal secondary and Tilioidae, Dombeyoideae, and Malvoideae. All leaf architec- minor secondary vein branching, and the number of orders of ture characters were optimized on a supertree of Malvaceae as teeth evolved only once within the Malvaceae and support the a means to explore for leaf characters that have become fi xed at relationship between M. macondicus and stem group Eumal- various clade levels and could potentially prove to be useful for voideae. Even though most taxa in this group are known to have leaf identifi cation within a family of ~4500 spp. Over 90% of small leaves markedly different from the mesophyll and macro- the leaf characters scored and mapped on the supertree com- phyll leaf blades of M. macondicus , large leaves are commonly piled for Malvaceae are highly homoplasious at family level found in tropical and subtropical genera such as Hibiscus , Wer- (online Appendix S3), refl ecting the repeated convergence of cklea , and Malvaviscus . These genera share the same set of leaf morphology within this group and the diffi culty of address- characters and show the greatest overall similarity to M. ing infrafamilial relations of fossil leaves. However, some char- macondicus . acter states are conserved at lower hierarchical levels. When combined, conserved characters can help distinguish between Comparison to fossil Malvaceae— The conspicuous palmate leaves of some lineages within the family ( Table 2 ). venation and double pulvini in most Malvaceae have been prev- Malvaciphyllum macondicus exhibits the same character alent in fossil leaves that date back to the Late Cretaceous, such combination that is distinctive to the clade Eumalvoideae of as “Tilia ” populifolia ( Lesquereux, 1883 ), “Tilia ” cretacea , Malvoideae (see Table 2). Eumalvoideae (former Malvaceae sensu “ Pterospermum ” conforme , and Apeibopsis atwoodii ( Hollick, stricto) holds the highest number of species in Malvaceae and 1930), among others. Many fossil leaves have been described occurs in a wide variety of habitats (Kubitzki and Bayer, 2003). as related or similar to Malvaceae, although the accuracy of the Habitat variation is refl ected in a wide range of leaf shape, size, systematic assignments is questionable. and venation that vary from small, reduced leaves of species The diagnostic characters, in particular the distal and proximal growing in desert or upland habitats (Nototriche , Fuertesi- branching of secondary veins in Malvaciphyllum macondicus, malva ) to large, deeply cordate leaves of lowland tropical spe- are not found in most of the fossil leaves previously described cies of genera such as Abutilon and Hibiscus . Despite this as Malvaceae (Table 1). The fossil genus Malvaciphyllum variation, the general pattern of leaf venation of Eumalvoids is Anz ó tegui was described from two species of fossil leaves from characterized by simple, dentate leaves with actinodromous Miocene and Pliocene deposits of Argentina and Brazil, respec- venation and more than fi ve basal veins, compound agrophics, tively, and was initially related to extant Abutilon ( Anz ó tegui and craspedodromous secondary veins, alternate percurrent third Cristalli, 2000 ). This morphogenus is the only malvalean fossil to and fourth order veins, and branched freely ending veinlets. exhibit the same proximal and distal branching patterns as M. In particular, two character states that are recovered as re- macondicus. Given that this character suggests affi nities to the stricted to Eumalvoideae and differentiate this group from other Eumalvoideae clade, we consider Malvaciphyllum as part of the subfamilies are also present in the fossil leaves. The proximal stem group of this clade, and we include the fossils described and distal branching of secondary veins refers to the orientation here as a new species of this fossil genus. The consistently smaller of veins of secondary or nearly secondary gauge that branch (notophyll) size, prominent rounded lobes, mostly crenate mar- from the basalmost major or minor secondary veins (Fig. 3A gins, opposite-percurrent fourth order venation, and lack of pul- and B). In most Malvaceae, including Eumalvoideae, lateral vini in M. quenquiadensis ( Anz ó tegui and Cristalli, 2000 ) differs primaries that innervate the lobes branch both proximally and from the mostly mesophyll-sized, unlobed, markedly dentate or distally, but only in Eumalvoideae do costal secondaries branch crenate and pulvinate M . macondicus leaves. These features are on the distal side near the margin ( Figs. 3A, B, 6 ). The second used to support species delimitation. character state recovered as synapomorphic for Eumalvoideae In examining fossil leaves described as Malvaceae, we did is the presence of three distinct orders of teeth, refl ecting differ- not fi nd a special affi nity of Dombeya novi-mundi to extant ences in the size of the teeth fed by primary, secondary, and Dombeya or the clade that includes this genus. Dombeya novi- tertiary veins. In other lineages in the family that have one or mundi , described by Hickey (1977) , is known from Eocene de- two orders of teeth, the teeth are fed by secondary and tertiary posits of Wyoming and North Dakota, and is one of the few veins ( Fig. 3C – E ). fossil leaf taxa assigned to a modern genus of Malvaceae. As These two characters — the costal secondary and minor sec- with most fossil leaves attributed to this family, D. novi-mundi ondary vein branching as well as three orders of teeth— distinguish is characterized by having 5– 7 actinodromous primary veins, a Eumalvoideae from all other lineages of Malvaceae that have toothed margin, a pulvinulus at the base of the leaf blade, and similar leaf architecture. The affi nity of M. macondicus to 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 tulipiﬂ ora (Hook.) Fryxell (A, Webster #12383). Scale = 5 cm. (C) One order of teeth. Helmiopsiella poissonii (Ar è nes) 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. 1344 American Journal of Botany [Vol. 98

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 widespread across various lineages of Malvaceae. The tooth recovered as plesiomorphic for the family as a whole, so that morphology of D. novi-mundi, however, is not very common in leaves with morphologies similar to that of D. novi-mundi are Malvaceae: the teeth are markedly asymmetrical, concave-convex August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1345

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; epiﬂ uorescence of in situ cuticle. (D) Arrows indicate acicular tricome remains. Scale = 50 µ m. (E) Arrows indicate acicular and stellate trichome remains. Scale = 200 µ 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 second- tectate, exine 2 µ m thick, nexine 0.5 µ m thick, columellae 1 µ m ary veins (rarely tertiary veins) that curve as they enter the thick, tectum 0.5 µ m thick, columellae distinct, long, present tooth ’ s laminar projection. Teeth of D. novi-mundi are similar only under muri of reticulum, tectum reduced to reticula; sculp- to those of some taxa in Grewioideae (such as species of Helio- ture reticulate, heterobrochate, lumina 1– 3 µ m wide at apocol- carpus and Luehea ) and Byttnerioideae (Abroma spp.), which pia and surrounding the colpi, almost foveolate (lumina 0.5 µ m used to be included in former Tiliaceae and Sterculiaceae, re- wide) at mesocolpia, muri pluricolumellate, 1 µ m wide, the spectively, and might have directed the original designation transition from reticula to foveolae is gradual although in short proposed by Hickey (1977). As former Sterculiaceae have been distance, sometimes a pseudo-line separates foveolae from re- shown to be polyphyletic and are now included in various sub- ticula. Dimensions: equatorial diameter 25 (38.5) 50 µ m, SD families of Malvaceae, this leaf morphology is more widespread 4.9, N = 40; equatorial diameter length/width 1.1. The pollen than previously thought. Dombeya novi-mundi is probably re- morphology of Bombacacidites annae is very similar to the lated to Malvaceae, but subfamily-level designations cannot be Bombax -subtype of Nilsson and Robyns (1986) , that is charac- fully resolved with the existing characters, and afﬁ nities to ex- teristic of several genera including Aguiaria , Bernoullia , Bom- tant Dombeya need further support from other features. bacopsis , Bombax , Eriotheca , Pseudobombax , and Spirotheca ( Nilsson and Robyns, 1986 ) within the clade Bombacoideae. Pollen record— The fossil pollen Bombacacidites annae ( Van der Hammen, 1954 ; Germeraad et al., 1968 ) is very common in sediments of the Cerrejó n Formation (Fig. 7) (Jaramillo DISCUSSION et al., 2007 ). The pollen is a monad, radial, isopolar, with amb triangular-obtuse-convex to almost circular; aperture tricolpo- Leaf character considerations— Leaf architecture charac- rate, ectocolpi costate, very short, colpi slightly protruding, ters were optimized on pre-existing phylogenetic hypotheses costae 3 µ m wide, endopore lalongate, pores indistinct; semi- as a means to assess within-group character variation and 1346 American Journal of Botany [Vol. 98

co-occurring, clade-ﬁ xed traits that were reliable for develop- ing hypotheses of natural afﬁ nities. Two characters were recov- vein vein Prox, distal distal Mayor ered as co-occurring and restricted to clade Eumalvoideae: the branching 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 particu- Vein Vein order 1, 2, 3 on teeth

Hibisceae: lar clade may reﬂ ect the expression of underlying develop- mental factors. Major veins have been shown to function as long-distance distribution lines of water through the leaf 3 Malvaciphyllum macondicus ( Roth-Nebelsick et al., 2001 ; Sack and Holbrook, 2006 ) as well of orders Teeth: no. Teeth: 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

Branch Hibiscieae: responds to mechanical stress and tensile forces ( Corson et al., 2009, 2010 ). The increased size of the teeth fed by secondary

spedodromous, FEVS = Freely ending veinlets, spedodromous, FEVS = Freely ending veinlets, veins relative to teeth fed by tertiary veins, and the resulting

Alt exmedial demand for biomechanical support and/or water sup- venation FEVS

Fourth order Fourth ply, 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 second-

order ary veins relates to the need to release excess water that is Third structed character states shared with venation common in the riparian environments inferred for Malvaciphyl- lum 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 xe- venation ric habitats ( Fryxell, 1981 ; Turner and Mendenhall, 1993 ). Intersecondary Whether the difference in tooth size reﬂ ects a change in the overall construction of these leaves cannot be determined sim- ply by observing patterns of correlated evolution. The co-oc- Minor currence and restrictedness of these two traits, however, offers secondaries a recognizable distinction between the leaves of Eumalvoideae and all other Malvaceae that supports natural afﬁ nities for the fossil here described. venation Secondary Malvoideae fossil record — The macrofossil record for Mal- voideae is sparse when compared to the extensive fossil record

veins for other subfamilies within Malvaceae (Manchester, 1992).

Agrophic Macrofossils related to Malvoideae include leaf compressions of Malvaciphyllum quenquiadensis , which Anz ó tegui associated with Abutilon (see Comparison to fossil Malvaceae ), and

No. of several fruit compressions assigned to Hibiscus and Malva from basal veins 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, Primary venation these fossils were initially described based on morphological resemblance, and natural affi nities for most of them remain un- tested. The distinctive echinate, multiporate pollen morphology Pube scence of Malvoideae has been used as evidence for tracing back this group in the fossil record; however, no detailed SEM studies ex Pubesc Actino 5 – 9 Comp – Crasp Absent Alt Hibiscieae: ex Pubesc Actino 5 – 9 Comp Crasp Crasp Absent Alt Alt Branch 2-3 1, 2, 3 Prox, have proven the affi nity of these pollen grains. The earliest- Amgle of base dispersed 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. 35– 37 Ma; MacPhail and Truswell, S Dentate Refl

Leaf 1989 ; MacPhail, 1999 ).

complexity Margin Based on Eocene pollen from Venezuela (37– 40 Ma) and the

records from the Murray Basin, Koopman and Baum (2008) sp. estimated a divergence age for Eumalvoideae of 29.7– 32.5 Ma.

Actino = Actinodromus, Alt = Alternate percurrent, Branch = Branched, Brochid Brochidodromous, Comp Compound, Crasp Cra Alt = Actinodromus, Actino = Malvaciphyllum macondicus shows that this group occurred in

2. within Malvaceae. level Combination of foliar characters interpreted as synapomorphic at subfamily northern South America by 58 – 60 Ma, predating the earliest

Notes: reliable pollen record by ~9 Ma (see Jaramillo et al., 2011) and macondicus nov. Table Subfamily ByttnerioideaeGrewioideaeTilioideaeHelicteroideae – S Helictereae Dentate DurioneaeDombeyoideae SBrownlowioideae Dentate – Sterculioideae S Comp – Malvoideae S S – – Entire Pubesc Eumalvoideae – Dentate Pinnate Acute – Pinnate – – S S – Entire – 3 – Obtuse Pubesc Smooth Dentate Entire – – Reﬂ Pubesc – – Acute – – – – – – – 1 – – – – – – – – Absent – Brochid – – 3 – – – – Absent Brochid – – Present Brochid – – – – – Present Brochid Retic Brochid – Brochid Brochid – Retic Opp – Retic Opp Absent Absent Retic – – Retic Retic – – Absent – Alt Absent Absent Opp Opp – 1 1 Opp Opp – – Retic Alt Retic 2, – 3 Retic Absent Absent – Absent – Absent Absent 1 – – – 1 – 1 – 1, 2 – 1, – 2 – Absent – – – – Bombacoideae Malvaciphyllum Comp Entire Acute Smooth Pinnate 1 Absent Brochid Absent Present – – – – – Absent Opp = Opposite percurrent, Prox = Proximal, Pubesc = Pubescent, Retic = Reticulate, S = Simple. Boldfaced states indicate recon Opp = Opposite percurrent, Prox Proximal, Pubesc Pubescent, Retic Reticulate, S Simple. Boldfaced sp. nov arguing for a much earlier origin than that suggested by molecular August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1347

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 Pé chon 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 tulipiﬂ ora (Hook.) Fryxell (A, Webster #12383). 1348 American Journal of Botany [Vol. 98

Malvaciphyllum macondicus in northern South America during the late Paleocene requires that either dispersals from Austral- asia into South America occurred before 60 Ma or the early- diverging Eumalvoideae had a different distribution than previously thought. Malvaciphyllum macondicus and the record of Bombacacid- ites annae in Cerrejó n imply that both Eumalvoideae and Bom- bacoideae 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-Paleo- cene (60 Ma; Jaramillo et al., 2011). Given that the oldest fossil record of Bombacoideae is centered in North and South Amer- ica, and since Eumalvoideae (as well as the Australasian genera Lagunaria , Howittia , and Radyera ; see Fig. 1) should have di- verged before 60 Ma, we consider that present-day distribution interpretations do not need to rely on long-distance dispersals across the Pacifi c 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 falsifi able with present data. Fig. 7. Bombacacidites annae , slide 547, EF = E20 2/4, Palynological Collection Colombian Petroleum Institute, grain in polar view, mid focus. Scenario 1 — Eumalvoideae could have originated in the neo- See the subcircular amb and the heterobrochate reticula, ornamentation tropics and remained present there ever since; dispersal across changing from reticulate at apocolpia and around colpi to almost foveolate the Pacifi c or through Antarctica (see Scenario 2) and regional at mesocolpia. 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 phyloge- clock inferences (Koopman and Baum, 2008). The low number netically related Bombacoideae in the northern South American of calibration points and the derived nature of fossil taxa avail- fossil record. able for this group make molecular clock estimation of diver- The extensive pollen record of Bombacoideae shows the ear- gence dates susceptible to possible underestimations. Evidence liest occurrences for the group in the Gulf Coast of the United for divergence earlier than 40 Ma for Eumalvoideae is not sur- States during the Maastrichtian and an earliest appearance in prising and has been suggested elsewhere, based on the derived South America by the middle Paleocene. Under this scenario, nature of the earliest fossil pollen attributed to the group ( Pfeil Bombacoideae and Malvoideae could have originated in North et al., 2002). Pollen of Eumalvoideae seems to be lacking from America by the Late Cretaceous, and further dispersion of both the Paleocene deposits of South America. The Paleocene occur- groups would explain the fossil record in northern South Amer- rence of eumalvoid leaves is consistent with the idea that the ica and the proposed origin of eumalvoids in the neotropics dur- pollen morphology of eumalvoids evolved later than the dis- ing the Paleocene. This opens the possibility of a dispersal route tinctive leaf morphology, supporting Malvaciphyllum as a stem from North to South America during the middle Paleocene, group of this clade. possibly through a Caribbean volcanic arch that briefl y con- nected North and South America at this time ( Bayona et al., Biogeographical considerations— The sparse fossil evi- 2011; Cardona et al., 2011). This same dispersal pattern has dence for Malvoideae has led various authors to advocate for been proposed for Ulmaceae ( Jaramillo and Dilcher, 2001 ). biogeographical scenarios mostly based on extant distribution. The basalmost lineage of Malvoideae is a clade of neotropical Scenario 2— Eumalvoideae reached South America from trees: Quararibea , Matisia, and Phragmotheca . Sister to this Australia before the opening of the Tasman Strait and the Drake clade is Eumalvoideae, nested within a grade of Australasian Passage. Evidence of biotic interchange between Australia and genera including Lagunari a, Howittia, and Radyera ( Figs. 1 South America has been found in the Eocene of Argentina and 6 ). The restricted distribution of this grade has been inter- (Zamaloa et al., 2006), and globally warm climates are thought preted by Baum et al. (2004) as suggestive of an Australasian to have permitted migration of thermophilic plants and animals origin for Eumalvoideae, in which case, the neotropical lin- among high latitude southern continents ( Wilf et al., 2005 , eages within the group would have arrived via trans-Pacifi c 2009 ). The Drake Passage opened in the late Eocene (~41 Ma), dispersal. ending the land connection between Australia and South Amer- There is little doubt that dispersal has played an important ica (Kennett, 1977; Scher and Martin, 2006). The hypothesized role in the history of Malvoideae, and colonization events movement of eumalvoids across high southern latitude land have been reported for various lineages within this group bridges would agree with earlier ideas for the biogeography of ( Fuertes-Aguilar et al., 2002 ; Koopman and Baum, 2008 ; the lineage (Baum et al., 2004) and implies the occurrence of Wagstaff et al., 2010 ) as well as for closely related Bombacoideae late Cretaceous or early Paleocene Malvoideae in Australia (Dick et al., 2007; Tsy et al., 2009). However, the presence of and/or southern South America; however, no fossils of this age August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1349 have been yet recovered, and the Gulf Coast-centered record ica already harbored the plant lineages that dominate neotropical for its sister group, Bombacoideae, seems to confl ict with this forests in the present. view. LITERATURE CITED Scenario 3— A third possible dispersion route, neither trans- Pacifi c (Baum et al., 2004) nor Antarctic (as in scenario 2), Alverson , W. S. , K. G. Karol , D. A. Baum , M. W. Chase , S. M. could have been across high northern latitudes. There are mul- Swensen , R. McCourt , and K. J. Sytsma . 1998 . Circumscription of the Malvales and relationships to other Rosidae: Evidence from tiple examples of animal and plant taxa moving across high lati- rbcL sequence data. American Journal of Botany 85 : 876 – 887 . tude land bridges and into South America in the Paleogene, Alverson , W.S. , B.A. Whitlock , R. Nyffeler , C. Bayer , and D.A. including arctostylopid mammals (Missiaen et al., 2006), Sal- Baum. 1999 . Phylogeny of the core Malvales: Evidence from ndhF vinia (Wing et al., 2009), and Anacardiaceae (Manchester et al., sequence data. American Journal of Botany 86 : 1474 – 1486 . 2007). Even though no fossil Malvaceae from Asia or Europe Anz ó tegui , L. , and P. Cristalli . 2000 . Primer registro de hojas de support this hypothesis, the earliest fossil record of Bomba- Malvaceae en el Ne ó geno de Argentina y Brasil. Ameghiniana 37 : coideae does occur in North America; more material from other 169 – 180 . areas may help test this possibility. Baum , D. A. , W. S. Alverson , and R. L. Nyffeler . 1998 . A Durian by Divergence time estimates and evidence for past distribution any other name: Taxonomy and nomenclature of the core Malvales. for eumalvoids remain elusive, such that hypotheses of origin Harvard Papers in Botany 3 : 315 – 330 . Baum , D. A. , S. D. Smith , A. Yen , W. S. Alverson , R. Nyffeler , B. A. and diversifi cation at its basalmost nodes are still poorly sup- Whitlock , and R. L. Oldham . 2004 . Phylogenetic relationships of ported. The pre-late Paleocene divergence suggested here for Malvatheca (Bombacoideae and Malvoideae; Malvaceae sensu lato) eumalvoids sets this group in a time when warm climates seem as inferred from plastid DNA sequences. American Journal of Botany to have favored thermophilic plant and animal dispersal at high 91 : 1863 – 1871 . latitudes ( Wolfe, 1978 ; Tiffney and Manchester, 2001 ; Missi- Bayer , C. , M. Fay , P. De Bruijn , V. Savolainen , C. Morton , K. aen et al., 2006 ). New calibration points for molecular clock Kubitzki , W.S. Alverson , and M.W. Chase . 1999 . Support for approaches are still needed within Malvoideae to have a better an expanded family concept of Malvaceae within a recircumscribed understanding of the times of origin and radiation of this group, order Malvales: A combined analysis of plastid atpB and rbcL DNA however, as the nodes for this group are pushed further back in sequences. Botanical Journal of the Linnean Society 129 : 267 – 303 . time, the effects of past extinctions, radiations and dispersals Bayona , G. , C. Montes , A. Cardona , C. Jaramillo , G. Ojeda , V. Valencia, and C. Ayala-Calvo . 2011 . Intraplate subsidence and become greater, and the explanatory power of extant distribu- basin fi lling adjacent to an oceanic arc– continent collision: a case from tions decreases. the southern Caribbean-South America plate margin . Basin Research 23: 403 – 422 . Paleoecological insights— The Cerrej ó n fl ora resembles ex- Berry , E . W. 1919 . Upper Cretaceous fl oras of the Eastern Gulf region tant neotropical rainforests in terms of rank – order abundance in Tennessee, Mississippi, Alabama, and Georgia. U.S. Geological and fl oristic composition, mean annual temperature and pre- Survey Professional Paper 112: 116p. cipitation (Wing et al., 2009). This fl ora has been interpreted to Berry , E. W. 1924a . Fossil plants and Unios in the Red Beds of Wyoming. represent tropical wetland vegetation, preserved in low-energy Journal of Geology 32 : 488 – 497 . depositional environments. The abundance of small, young Berry , E . W. 1924b . The Middle and Upper Eocene fl oras of southeast- leaves, as well as large blades of Malvaciphyllum macondicus ern North America. U.S. Geological Survey Professional Paper 92. in fi ne-grained sediments suggests little predepositional trans- Berry , E. W. 1925 . A Miocene fl ora from Patagonia. The Johns Hopkins University Studies in Geology 6 : 183 – 251 . port and therefore that the plants grew in the local setting of Berry , E .W. 1929 . A revision of the fl ora of the Latah Formation. U.S. lower delta plain lakes, ponds, and swamps. In these environ- Geological Survey Professional Paper : 225-265. ments, a large number of leaves could have been deposited and Berry , E .W. 1930 . Revision of the Lower Eocene Wilcox fl ora of the south- buried. eastern states: With descriptions of new species, chiefl y from Tennessee The Eumalvoideae include a large number of herbaceous and and Kentucky. U.S. Geological Survey Professional Paper 156. woody species occurring in diverse habitats from tropical to Berry , E. W. 1938 . Tertiary fl ora from the Rio Pichileufu, Argentina. temperate environments. In lowland tropical forests, eumal- Geological Society of America Special Papers 12. voids are frequently associated with naturally disturbed habitats Brown , R. 1934 . The recognizable species of the Green River Flora. U.S. such as forest gaps, riverbanks, and along deltas (i.e., Talipariti Geological Survey Professional Paper Series 185C: 45-77. spp.). These plants tend to grow in dense populations along Burnham , R. J. , and K. R. Johnson . 2004 . South American palaeobotany and the origins of neotropical rainforests. Philosophical Transactions river margins and swamps ( Smith et al., 2004 ), consistent with of the Royal Society, B , Biological Sciences 359 : 1595 – 1610 . sedimentological evidence for the sites where we recovered Cardona , A. , V. A. Valencia , G. Bayona , J. Duque , M. Ducea, G. Malvaciphyllum macondicus fossils. Other fossil plants with Gehrels, C. Jaramillo , et al . 2011 . Early-subduction-related similar inferred habitats and ecological characteristics co-occur orogeny in the northern Andes: Turonian to Eocene magmatic and with M. macondicus, including the heliophyte Montrichardia provenance record in the Santa Marta Massif and Rancheria Basin, aquatica (Herrera et al., 2008) and various species of palms northern Colombia . Terra Nova 23: 26 – 34 . ( G ó mez-Navarro et al., 2009 ). Corson , F. , M. Adda-Bedia , and A. Boudaoud . 2009 . In silico leaf The occurrence of Malvaciphyllum macondicus, along with venation networks: Growth and reorganization driven by mechanical two other malvalean fossil leaves from Cerrej ó n fl ora not de- forces. Journal of Theoretical Biology 259 : 440 – 448 . scribed in this study (morphotypes CJ25 and CJ36; see Wing et Corson , F. , H. Henry , and M. Adda-Bedia. 2010 . A model for hierarchical patterns under mechanical stresses. Philosophical Magazine 9 0 : al., 2009 , Supporting Information), and the high pollen abun- 357 – 373 . dance of Bombacoideae suggest that derived lineages of Mal- Dick , C. W. , E. Bermingham , M. R. Lemes , and R. Gribel . 2007 . Extreme vaceae were already a diverse element of neotropical rainforests long-distance dispersal of the lowland tropical rainforest tree Ceiba of the late Paleocene. This adds specifi city to previous observa- pentandra L. (Malvaceae) in Africa and the Neotropics. 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Appendix 1 . List of genera of Malvaceae studied.

Genera Genera Genera

Adansonia L. Glossostemon Desf. Octolobus Welw. Abelmoschus Medik. Glyphaea Hook. f. Pachira Aubl. Abutilon Mill. Goethalsia Pittier Palaua Cav. Acaulimalva Krapov. Gossampinus Schott & Endl. Paradombeya Stapf Acropogon Schltr. Gossypium L.Patinoa Cuatrec. Aguiaria Ducke Grewia L. Pavonia Cav. Allosidastrum (Hochr.) Krapov., Fryxell & D. M. Bates Guazuma Mill. Peltaea (C. Presl) Standl. Althaea L. Gyranthera PittierPentace Hassk. Althofﬁ a K. Schum. Hainania Merr. Pentapetes L. Andeimalva J. A. Tate Helicteres L. Pentapteris Haller Anisodontea C. Presl Heliocarpus L. Periptera DC. Anoda Cav. Helmiopsiella Arenes Phragmocarpidium Krapov. Apeiba Aubl. Helmiopsis H. PerrierPhymosia Desv. ex Ham. Ayenia L. Heritiera AitonPhysodium C. Presl Bastardia Kunth Herrania GoudotPterygota Schott & Endl. Bastardiopsis (K. Schum.) Hassl. Hibiscus L. Quararibea Aubl. Batesimalva Fryxell Hildegardia Schott & Endl. Radyera Bullock Bernoullia Oliv. Hoheria A. Cunn. Reevesia Lindl. Berrya Roxb. Horsfordia A. Gray Rhodognaphalopsis A. Robyns Bombacopsis Pittier Howittia F. Muell. Rhyncosida Fryxell Bombax L. Huberodendron DuckeRobinsonella Rose & Baker f. Bombycidendron Zoll. & Moritzi Jarandersonia Kosterm. Ruizia Cav. Brachychiton Schott & Endl. Kearnemalvastrum D. M. Bates Rulingia R. Br. Briquetia Hochr. Keraudrenia J. GayScaphium Schott & Endl. Brownlowia Roxb. Kleinhovia L. Scaphopetalum Mast. Burretiodendron RehderKokia Lewton Schoutenia Korthals Byttneria Loeﬂ . Krapovickasia FryxellSenra Cav. Camptostemon Mast. Kydia Roxb. Septotheca Ulbr. Carpodiptera Griseb. Lagunaria Rchb. Sida L. Ceiba Mill. Lasiopetalum Smith Sidalcea A. Gray Christiana DC. Lavatera L.Sidastum Baker f. Cienfuegosia Cothen. Lawrencia Hook.Plagianthus J. R. Forst. & G. Forst. Clappertonia Meisn. Lecanophora Speg. Pseudabutilon R. E. Fr. Coelostegia Benth. Leptonychia Turcz. Pseudobombax Dugand Cola Schott & Endl. Luehea Willd. Pterocymbium R. Br. Commersonia J. R. Forst. & G. Forst. Malachra L.Sitella L. H. Bailey Corchoropsis Siebold & Zucc. Malacothamnus Greene Sphaeralcea A. St.-Hil. Corchorus L. Malvastrum A. Gray Spirotheca Ulbr. Corynabutilon (K. Schum.) Kearney Malvaviscus Fabr. Sterculia L. Craigia W. W. Sm. & W. E. EvansMalvella Jaub. & SpachTarasa Phil. Cristaria Cav. Malva L.Tetralix Griseb. Cullenia WightMansonia J. R. Drummond ex D. Prain Tetrasida Ulbr. Cuningia S. Vidal Matisia Bonpl. Theobroma L. Decastichia Rchb. Melhania Forssk. Thomasia J. Gay Dendrosida Fryxell Melochia L. Triplochiton K. Schum. Dicraspidia Standl. Meximalva Fryxell Triumfetta L. Dombeya Cav. Microcos L. Trochetia DC. Durio Adans.Modiola Moench Urena L. Entelea R. Br. Modiolastrum K. Schum. Waltheria L. Eremalche Greene Mollia Mart. Wercklea Pitter & Standl. Eriolaena DC. Monteiroa Krapov. Wissadula Medik. Eriotheca Schott & Endl. Montezuma Moc, & Sesse ex DC. Firmiana MarsiliMortoniodendron Standl. & Steyerm. Fremontodendron Coville Neobrittonia Hochr. Fryxelia D. M. Bates Neobuchia Urb. Fuertesimalva Fryxell Nesogordonia Baill. Gaya Kunth Nototriche Turcz. August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1353

Appendix 2. Characters and character states used for optimization. Based on Ellis et al. (2009) .

Character Character states

1 Leaf complexity 0: Simple; 1: Compound 2 Petiole insertion 0: Marginal; 1: Peltate 3 Leaf size 0: Microphyll; 1: Notophyll; 2: Mesophyll; 3: Macrophyll 4 Length: Width Ratio 0: 1-1; 1: 2-1; 2: 3-1; 3: 3-2; 4: 5-4 5 Shape of the lamina 0: Elliptic; 1: Ovate; 2: Obovate 6 Medial symmetry of the lamina 0: Strictly asymmetric; 1: Symmetric 7 Basal symmetry of the lamina 0: Strictly asymmetric; 1: Symmetric 8 Lobation 0: Non lobed; 1: Palmately lobed 9 Margin 0: Entire; 1: Dentate 10 Special features of the margin 0: Absent; 1: Thickened margin; 2: Sinuous margin; 3: Revolute margin 11 Base angle 0: Refl ex; 1: Acute; 2: Obtuse 12 Base shape 0: Cordate; 1: Convex; 2: Decurrent; 3: Cuneate; 4: Rounded; 5: Lobed; 6: Complex 13 Apex angle 0: Acute; 1: Obtuse 14 Apex shape 0: Acuminate; 1: Straight; 2: Convex; 3: Rounded 15 Terminal apex features 0: Non distinctive; 1: Mucronate; 2: Spinose 16 Surface texture 0: Smooth; 1: Pubescent 17 Surfi cial Glands 0: Absent; 1: Laminar; 2: On veins 18 Primary venation network 0: Actinodromous; 1: Pinnate 19 Number of basal veins 0: 1; 1: 3; 2: 5; 3: 7 – 9 20 Agrophic veins 0: Absent; 1: Simple; 2: Compound 21 Major secondary vein framework 0: Basal eucamptodromous; 1: Craspedodromous; 2: Semicraspedodromous; 3: Brochidodromous 22 Interior secondaries 0: Absent; 1: Present 23 Minor secondary course 0: Semicraspedodromous; 1: Craspedodromous; 2: Brochidodromous 24 Perimarginal veins 0: Absent; 1: Fimbrial veins 25 Major secondary spacing 0: Consistent; 1: Inconsistent; 2: Abruptly increasing basally; 3: Gradually increasing basally 26 Variation of major secondary angle to midvein 0: Consistent; 1: Inconsistent; 2: Gradually decreasing basally; 3: One pair of acute basal secondaries; 4: Gradually increasing basally 27 Major secondary attachment to midvein 0: Excurrent; 1: Decurrent; 2: Defl ected 28 Intersecondary veins 0: Absent; 1: Present 29 Intersecondary veins — course 0: Parallel to secondaries; 1: Perpendicular to midvein 30 Intersecondary veins — length 0: Same as subjacent secondaries; 1: Less than half of subjacent secondaries; 2: More than half of subjacent secondaries 31 Intersecondary veins — termination 0: With subjacent secondaries; 1: Basifl exed; 2: Reticulate 32 Intercostal tertiary venation framework 0: Reticulate; 1: Alternate percurrent; 2: Opposite percurrent 33 Intercostal tertiary angle variability 0: Consistent; 1: Inconsistent; 2: Increasing exmedially; 3: Increasing proximally 34 Epimedial tertiaries 0: Reticulate; 1: Alternate percurrent; 2: Opposite percurrent 35 Exterior tertiary course 0: Looped; 1: Terminating at the margin; 2: Looped with teeth 36 Quaternary vein fabric 0: Alternate percurrent; 1: Opposite percurrent; 2: Reticulate 37 Quinternary vein fabric 0: Irregular reticulate; 1: Regular reticulate 38 Areolation 0: Good development; 1: Moderate development; 2: Poor development 39 Freely ending veinlets 0: Absent; 1: Non ramifi ed; 2: Ramifi ed 40 Marginal ultimate venation 0: Ramifi ed; 1: Anastomosing; 2: Fimbrial vein 41 Tooth spacing 0: Regular; 1: Irregular 42 Number of orders of teeth 0: 1; 1: 2; 2: 3 43 Veins forming teeth 0: Primaries; 1: Secondaries; 2: Primaries and secondaries; 3: Secondaries and tertiaries; 4: Tertiaries; 5: Primaries, secondaries and tertiaries 44 Number of teeth per cm 0: One to two; 1: Three to fi ve; 2: Six to eight; 3: Nine to eleven 45 Tooth sine 0: Curved; 1: Angular 46 Tooth shape 0: Concave-concave; 1: Convex-concave; 2: Convex-convex; 3: Convex-fl exuous; 4: Flexuous- concave; 5: Flexuous-convex; 6: Flexuous-fl exuous; 7: Retrofl exed-straight; 8: Straight-straight; 9: Flexuous-straight 47 Principal vein termination 0: At tooth sine; 1: Submarginal; 2: At apex 48 Principal vein course 0: Medial; 1: Closer to proximal fl ank; 2: Closer to distal fl ank 49 Principal vein curvature 0: Straight; 1: Curved 50 Accesory veins 0: Absent; 1: Present 51 Course of major accesory veins 0: Looped; 1: Convex; 2: Straight 52 Special features of the tooth apex 0: Marginal; 1: Mucronate; 2: Spinose 53 Branching of major veins 0: Absent; 1: Only proximal; 2: Proximal and distal 1354 American Journal of Botany [Vol. 98

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 1922, US 1214561 . Eriotheca globossa (Aubl,) A. Robyns Nu ñ ez 19422 , Cusco, Peru, 1997; USNM Cleared leaf collection 9149. Abelmoschus sagittifolius (Kurz) Merr. USNM Cleared leaf collection 10426. Abutilon asiaticum (L.) Sweet . Fosberg, 24827, Mariana Islands, 1946, Firmiana colorata (Roxb.) R. Br. USNM Cleared leaf collection 8048. US 2639870; USNM Cleared leaf collection 10427. Abroma augusta Fremontodendron decumbens R.M. Lloyd Gankin 737 , California, US, (L.) L. f. Forsberg 25828, Ngeanges Island, Caroline Islands, 1946, US 1966, US 3082463; USNM Cleared leaf collection 3629. 2431324; USNM Cleared leaf collection 1915. Adansonia digitata L. Gaya gaudichaudiana A. St.-Hil. Gaudichaud-Breaupr é , s.n., Rio de Janeiro, USNM Cleared leaf collection 3657. Aguiaria excelsa Ducke Ducke Brazil, US 2599921; USNM Cleared leaf collection 10464 (fi led as 25188, Province of Amazonas, Brazil, 1932, US 1618767. USNM Gaya gracilipes) . Glyphaea grewioides Hook. F. USNM Cleared leaf Cleared leaf collection 9147. Apeiba aspera Aubl. Albert de Escobar collection 4596. Goethalsia meiantha (Donn. Sm.) Burret Soejarto DD 2154, Chocó , Colombia, 1982, HUA 15905; Rudas A 3259 , Amazonas, 3251, Antioquia, Colombia, 1972, HUA 3071; Loaiza 62, Antioquia, Colombia, 1992, HUA 119287; David H 2925, Caldas, Colombia, 2009, Colombia, 1980, HUA 12264; Giraldo LF 08 , Antioquia, Colombia, HUA 171951; USNM Cleared leaf collection 8037. Ayenia wygodzinskyi 1994, HUA 91125; S á nchez-G ó mez JC 163, Antioquia, Colombia, 2006, Crist ó bal USNM Cleared leaf collection 11448. HUA 168563; USNM Cleared leaf collection 3881. Grewia bicolor Juss. Bastardia viscosa (L.) Kunth Albert de Escobar 729, El Oro Province, USNM Cleared leaf collection 11350. Grewia paniculata Roxb. Ex DC. Ecuador, 1978, HUA 10280; Fonnegra 1400 , La Guajira, Colombia, USNM Cleared leaf collection 11503 (fi led as Microcos tomentosa ). February 1980, HUA 11889; Bunch s.n., La Guajira, Colombia, HUA Guazuma ulmifolia Lam. White 481 , Magdalena, Colombia, 1977, HUA 14936; Bunch 187, La Guajira, Colombia, HUA 14039; Bunch 746 , La 8083; Fonnegra 797 , Antioquia, Colombia, 1978, HUA 7572; Palacio Guajira, Colombia, HUA 14178; USNM Cleared leaf collection 6205, M s.n. , Antioquia, Colombia, 1984, HUA 24133; Zardini 8478 , Guaira 10205. Berrya cordifolia (Willd.) Burret Britton 415, St. Christopher- Province, Paraguay, December 1988, HUA 69967; USNM Cleared leaf Nevis, 1901, US 428789; Robyns 6994, Sri Lanka, 1969, US 2612298; collection 3633. Gyranthera caribensis Pittier USNM Cleared leaf Pipoly JJ 7336, Guyana, 1986, US 3131458; USNM Cleared leaf collection 10053. collection 404. Bombax ceiba L. Specht 1175 , Northern territory, Helicteres guazumifolia Kunth USNM Cleared leaf collection 11402. Australia, 1948, US 2125226; USNM Cleared leaf collection 10055. Heliocarpus palmeri S. Watson Palmer 191 , Chihuahua, Mexico, Brachychiton populneus (Schott & Endl.) R. Br. Camp WH E-2898 , 1885, US 13314; USNM Cleared leaf collection 3606, 11371 (Filed Azuay Province, Ecuador, 1945, US 2167393; USNM Cleared leaf under Heliocarpus glaber and Heliocarpus polyandrous ). Heritiera collection 3617 . Brownlowia helferiana Pierre USNM Cleared leaf ornithocephala Kosterm. USNM Cleared leaf collection 11408. collection 3590. Brownlowia tersa (L.) Kosterm. USNM Cleared leaf Herrania purpurea (Pittier) R.E. Schult. Cogollo A 1415 , Antioquia, collection 2171. Burretiodendron esquirolii (H. L é v.) Rehder USNM Colombia, 1984, HUA 322473; Renter í a 10899 , Choc ó , Colombia, 1995, Cleared leaf collection 8041. Byttneria ancistrodonta Mildbr. Palacios HUA 99400; Id á rraga A 2901 , Choc ó , Colombia, 2004, HUA 170332; 8140, Provincia de Sucumbí os, Ecuador, 1991, US 3290270; Palacios Benavides JC 3027, Antioquia, Colombia, HUA 154282; USNM Cleared 9021, Province of Sucumbí os, Ecuador, 1991, US 3299287; USNM Hibiscus ribifolius A. Gray Xantus 11 Cleared leaf collection 11516. Byttneria dentata Pohl. USNM Cleared leaf collection 5567. , Baja leaf collection 11517. California, Mexico, 1859, US 42462; USNM Cleared leaf collection 6215. Hildegardia barteri Mast. USNM Cleared leaf collection 7592, Ceiba pentandra (L.) Gaertn. Gentry 24534, Chocó , Colombia, 1979, HUA 14440. Huberodendron allenii Standl. & L.O.Williams Allen 6014, 11125; Rodr í guez W 144, Magdalena, Colombia, 1996, HUA 109211; Puntarenas Province, Costa Rica, 1951, US 2215856; USNM Cleared leaf Fonnegra 7369 , Magdalena, Colombia, 2001, HUA 125723; USNM collection 3671. Cleared leaf collection 13357, 1912. Christiana africana DC. Albert de Jarandersonia paludosa Kosterman USNM Cleared leaf collection 8035. Escobar 1171, Provincia de El Oro, Ecuador, 1979, HUA 10213; USNM Cleared leaf collection 4593. Cienfuegosia drummondii (A. Gray) Keraudrenia collina Domin USNM Cleared leaf collection 3635. Kleinhovia Lewton USNM Cleared leaf collection 10461. Cola nitida (Vent.) Schott hospita L. Unknown collector s.n., Canal zone, Panama, US 2800262. & Endl. Vigne 1176 , Gold Coast, Ghana, 1928, US 1429974; Cooper USNM Cleared leaf collection 1921. Kokia rockii Lewton USNM Cleared 336, Liberia, 1929, US 1378506; USNM Cleared leaf collection 14435. leaf collection s.n. Commersonia bartramia (L.) Merr. Dietrich s.n., Queensland, Australia, US 205778; Hosakawa 6938, Palau Islands, 1933, US 2932222; Soejarto Lagunaria patersonia (Andrews) G. Don USNM Cleared leaf collection 6213. DD 14221 , Quang Tri Province, Vietnam, 2008, US 3581477. USNM Malvastrum spicatum (L.) A. Gray Sintenis 2996, Puerto Rico, 1886; Cleared leaf collection 3623. Corchorus aestuans L. Irwin 21115, Goi á s Sintenis 3574, Puerto Rico, 1886; USNM Cleared leaf collection 10481. Province, Brazil, US 2833229; Elias 751 , Atl á ntico, Colombia, 1929, US Malvaviscus arboreus Cav. Busch, s.n., Texas, US, 1900, US 386842; 1443072; Tamayo 971, Falcó n Province, Venezuela, 1938, US 1801830; Molina 560, Bolivar, Colombia, HUA 16630; Marulanda 2149 , La Dugand 5000 , Atlantico, Colombia, 1956, US 2252591; Koch 87271 , Guajira, Colombia, August 1990, HUA 75866; USNM Cleared leaf Guerrero Province, Mexico, 1987, US 3363583; USNM Cleared leaf collection 6191, 6192, 6211, 16806. Mortoniodendron vestitum Lundell collection 1389. Cullenia ceylanica (Gardner) Wight ex K. Schum. Contreras 7327 , Pet é n Province, Guatemala, 1967, US 2558505; Lundell USNM Cleared leaf collection 8054. 18153 , Pet é n Province, Guatemala, 1964, US 2479936; USNM Cleared leaf collection 3880. Diplodiscus paniculatus Turcz. Clemens 616, Lanao del Sur, Philippines, 1907, US 3415457; Elmer 13267, Philippines, 1912, US 3415454; USNM Neoregnellia cubensis Urb. Ekman Pl.ind.Occ.16692, Pinar del Rí o, Cuba, Cleared leaf collection 3600. Dombeya burgessiae Gerard ex Harv. 1923, US 2225018; Leonard 13142 , La Hispaniola, 1929, US 1451820; Soejarto DD 2328 , Antioquia, Colombia, 1970, HUA 3025; Soejarto USNM Cleared leaf collection 3646. Nesogordonia dewevrei (De Wild. DD 2564 , Antioquia, Colombia, 1970, HUA 2564; USNM Cleared leaf & T. Durand) Capuron ex R. Germ. USNM Cleared leaf collection collection 9623. Durio griffi thii (Mast.) Bakh, USNM Cleared leaf 3593, 4599. collection 11453. Durio lanceolatus Mast. USNM Cleared leaf collection 3666. Ochroma pyramidale (Cav. Ex Lam.) Urb. Fonnegra 2187, Antioquia, Colombia, 1987, HUA 38291; Duque A 2382, Caldas, Colombia, 2001, Entelea arborescens R. Br. Fosberg 22563, Chimborazo, Ecuador, 1945, US HUA 134824; David H 1214 , Caldas, Colombia, 2005, HUA 149414; 2109622; USNM Cleared leaf collection 3602. Eriolaena spectabilis USNM Cleared leaf collection 10233. Octolobus angustatus Hutch. (DC.) Planch. Ex Mast. Rock JF 1663, Chiengmai Province, Siam, USNM Cleared leaf collection 4616, 14443. August 2011] Carvalho et al. — Neotropical fossil Malvaceae 1355

Pachira quinata (Jacq.) W.S. Alverson G ó mez A 566 , Antioquia, Colombia, (Franch.) Pax & K. Hoffm. USNM Cleared leaf collection 3022. Givotia 1992, HUA 81387; Callejas 12230, Antioquia, Colombia, 1990, HUA rottleriformis Griff. ex Wight USNM Cleared leaf collection 9046. Jatropha 116541; Vel á squez-R 5762, Antioquia, Colombia, 2009, HUA 168121; gossypiifolia L. USNM Cleared leaf collection 3061. Mallotus japonicus (L. USNM Cleared leaf collection 2546. Paradombeya rehderiana Hu USNM f.) Mü ll. Arg. USNM Cleared leaf collection 38, 9090, 11720. Melanolepis Cleared leaf collection 8063 Patinoa sphaerocarpa Cuatr. Krukoff 4656 , multiglandulosa (Reinw. Ex Blume) Rchb. F. & Zoll. USNM Cleared leaf Amazonas, Brazil, 1933, US 1691072; USNM Cleared leaf collection collection 871. 10059. Pavonia fi rmifl ora Schery Pringle 5447 , Jalisco, M é xico, 1893, Vitaceae US 305777; USNM Cleared leaf collection 6209, 16924. Pentace curtisii King USNM Cleared leaf collection 11504. Phymosia rosea (DC.) Cissus caesis Afzel. USNM Cleared leaf collection 4948. Vitis betulifolia Diels Kearney Skutch 1025, Department of Huehuetenagi, Guatemala, 1934, US & Gilg USNM Cleared leaf collection 261, 262. Vitis vinifera L. Field 1644029; USNM Cleared leaf collection 16811, 10484. Pseudobombax 761 , Iraq, 1939, US 1741428; Unknown collector s.n., Italy, US 17449. septenatum (Jaq.) Dugand Vargas WG 6377, Caldas, Colombia, 1999, HUA 117332; P é rez J 964, Santander, Colombia, 1999, HUA 12724, Hamamelidaceae Fern á ndez-Alonso 22521 , Santander, Colombia, 2004, HUA 169531; Corylopsis veitchiana Bean. USNM Cleared leaf collection 528. Liquidambar USNM Cleared leaf collection 3660. Pterocymbium tinctorium Merr. stryracifl ua L. USNM Cleared leaf collection 60, 928, 11912, 14582, USNM Cleared leaf collection 8051. Pterospermum acerifolium Willd. 14583. Parrotiopsis jacquemontiana (Decne.) Rehder USNM Cleared USNM Cleared leaf collection 1150. Pterygota forbesii Muell. USNM leaf collection 1128 (fi led as Parrotia jacquemontiana ). Cleared leaf collection 8047. Moraceae Quararibea (Matisia) ochrocalyx (K. Schum.) Vischer USNM Cleared leaf collection 3674. Quararibea turbinata (Sw.) Poir Sintenis 6289, Puerto Bagassa guianensis Aubl. USNM Cleared leaf collection 9102. Morus insignis Rico, 1886; Axelrod 8270, Puerto Rico, 1994; USNM Cleared leaf Bureau Dorr 8749, Trujillo Province, Venezuela, 2000, US 3406012. collection 3677. Morus alba L. USNM Cleared leaf collection 10900. Reevesia thyrsoidea Lindl. USNM Cleared leaf collection 1925. Rulingia Sapindaceae madagascariensis Baker Hildebrandt 3662, Madagascar, 1880, Acer opalus Mill. USNM Cleared leaf collection 9622. Acer pensylvanicum US808373; USNM Cleared leaf collection 3651. L. USNM Cleared leaf collection 1176b. Scaphium macropodum Beumee ex K. Heyne USNM Cleared leaf collection Urticaceae 8049. Schoutenia hypoleuca Pierre Pierre 659, Cambodia, US 2913962; USNM Cleared leaf collection 518, 519. Spirotheca rivieri (Decne.) Boehmeria nivea (L.) Gaudich. USNM Cleared leaf collection 10911. Boehmeria Ulbr. USNM Cleared leaf collection 3668. Sterculia apetala (Jacq.) H. spicata (Thunb.) Thunb USNM Cleared leaf collection 10912. Karst. Palacios 8948, Sucumb í os Province, Ecuador, 1991, US 3258986; Cucurbitaceae Little 671, Morona-Santiago, Ecuador, US 2972702; Ortega 36, Morona- Santiago, Ecuador, 1976, US 3003289; USNM Cleared leaf collection Sechium edule (Jacq.) Sw . Degener 12753 , Kuai County, Hawaii, United 11428. States, 1940, US 1864564; Wagner 5680 , Maui, Hawaii, United States, Theobroma cacao L. Hoyos Marin S 156 , Antioquia, Colombia, 1983, HUA 1986, US 3283040. Calycophysum spectabile (Cogn.) C. Jeffrey & 18169; Santa J 1053 , Valle del Cauca, Colombia, 1984, HUA 22480; Trujillo Dorr 8719, Trujillo Province, Venzuela, 2000, US 3406431; Fonnegra 2721 , Antioquia, Colombia, 1989, HUA 60730;V é lez JG 5444 , Stergios 18927, Trujillo Province, Venzuela, 2001, US 3403467. Valle del Cauca, Colombia, April 2003, HUA 138678; Hoyos-G ó mez Cercidiphyllaceae SE 521, Chocó , Colombia, 2005, HUA 160504 ; David H 1184 , Caldas, Colombia, 2005, HUA 148970; USNM Cleared leaf collection 3884. Cercidiphyllum japonicum Siebold & Zucc . USNM Cleared leaf collection Thespesia cubensis (Britton & P. Wilson) J.B.Hutch USNM Cleared 26, 148 – 150, 397. leaf collection 3847, 16930. Tilia cordata Mill. Steinle s.n., Maryland, Cochlospermaceae US, 1958, US 2262316; Allard 20508 , Virginia, US, 1952, US 2098497; Ward, s.n., District of Columbia, US, 1884, US 136368; USNM Cleared Cochlospermum vitifolium (Willd.) Spreng. USNM Cleared leaf collection leaf collection 120. Triplochiton scleroxylon K. Schum. Chevalier 16105, 3236. Cô te-d ’ Ivoire, 1907, US 2543376; USNM Cleared leaf collection 3656, Platanaceae 4609, 14449. Triumfetta speciosa Seem. USNM Cleared leaf collection 11510, 17093. Trochetia parvifl ora Bojer USNM Cleared leaf collection Platanus orientalis L. USNM Cleared leaf collection 1545. Platanus 4612. occidentalis L. USNM Cleared leaf collection 729 – 732. Wercklea ferox (Hook. f.) Fryxell Nu ñez 23921 , Cusco, Peru, 1998, US. Cannabaceae Euphorbiaceae Humulus lupulus L. USNM Cleared leaf collection 6042. Acalypha cinta Mü ll. Arg. USNM Cleared leaf collection 11463. Acalypha Rosaceae macrostachya Jacq. USNM Cleared leaf collection 11471. Alchornea triplinervia (Spreng.) Mü ll. Arg. USNM Cleared leaf collection 11481. Stephanandra chinensis Hance USNM Cleared leaf collection 1540. Crataegus Croton euryphyllus W.W. Sm. USNM Cleared leaf collection 11588 (Filed douglasii Lindl. USNM Cleared leaf collection 1436, 1437. as Croton caudatiformis). Croton gossypiifolius Vahl. USNM Cleared leaf Elaeocarpaceae collection 11571, 15198 (Filed as Croton draco). Dalechampia tiliifolia Lam. USNM Cleared leaf collection 11596. Dalechampia aristolochiifolia Aristotelia chilensis (Molina) Stuntz USNM Cleared leaf collection 3187. Kunth USNM Cleared leaf collection 11598. Discocleidian rufescens Muntingia calabura L. USNM Cleared leaf collection 3193.