Carvalho Et Al_2011_Malvaceae Cerrejon Flora

1337

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

American Journal of Botany 98(8): 1337–1355, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America

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 para-phyletic Sterculiaceae, Tiliaceae, and Bombacaceae within an expanded Malvaceae ( Bayer et al., 1999 ; Kubitzki and Bayer, 2003 ). This regrouping has been supported by various morpho-logical and anatomical synapomorphies as well as molecular data ( Judd and Manchester, 1997 ; Alverson et al., 1998 , 1999 ; Bayer et al., 1999 ).

Malvaceae is one of the most dominant plant families in neo-tropical 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 Mal-vatheca group ( Baum et al., 1998 , 2004 ) combines Bomba-coideae and Malvoideae into one of the most speciose clades (ca. 1300 species) within Malvaceae and one of the most con-spicuous groups in the neotropics. Malvoideae comprises tradi-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 Phragmotheca ( Fig. 1 ).

The oldest record for the Malvatheca group is based on pol-len from the Maastrichtian of New Jersey attributed to Bomba-coideae ( Wolfe, 1975 ), suggesting pre-Cenozoic divergence times for the major clades within this family. Due to the con-spicuous 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 Ster-culiaceae ( 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 diffi cult to assess their natural affi nities. More reliable taxo-nomic identifi cations have been supported by the co-occurrence of leaves and associated plant organs ( Kva č ek et al., 2002 ; Kva č ek, 2004 , 2006 ), preservation of cuticular features ( Pan and Jacobs, 2009 ; Worobiec et al., 2010 ), whole-plant interpre-tations ( Kva č ek, 2008 ), reproductive structures ( Duarte, 1974 ;

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 é Cuatrecasas fellowship in the Department of Botany of the Smithsonian Museum of Natural History (MRC), Carbones del Cerrej ó n 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 Fundaci ó n para la Promoci ó n de la Investigaci ó n y la Tecnolog í a, Banco de la Rep ú blica, the Colombian Petroleum Institute, and Fundaci ó n 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. Hern á ndez, C. Montes, A. Rinc ó n, and the geology team at the Cerrej ó n mine for fi eldwork support. M.R.C. especially thanks Laurence Dorr for taxonomic discussions and Lisa Barnett, Peter Wilf, Vicky Funk, Emily Wood, Alvaro Id á rraga, and curators at US, A, HUA and SCZ herbaria.

7 Author for correspondence (e-mail: [email protected])

doi:10.3732/ajb.1000539

PALEOCENE MALVACEAE FROM NORTHERN SOUTH AMERICA AND THEIR BIOGEOGRAPHICAL IMPLICATIONS 1

M ó nica R. Carvalho 2 – 4,7 , Fabiany A. Herrera 3,5 , Carlos A. Jaramillo 3 , Scott L. Wing 6 , 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 Cerrej ó 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.

1338 American Journal of Botany [Vol. 98

Kva č ek et al., 1991 , 2002 ; Manchester, 1992 , 1994 ), and ana-tomically preserved wood ( Manchester, 1979 , 1980 ). The fossil record of leaves attributed to Malvaceae or its segregate fami-lies ranges from the Late Cretaceous to the late Neogene, in-cluding reports from the Cretaceous of North America ( Hollick, 1930 , 1936 ), lower Miocene of Europe ( Kva č ek et al., 2002 ; Kva č ek 2008 ), Miocene of Argentina ( Anz ó tegui 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 ; Magall ó n and Castillo, 2009 ). Magall ó n 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 fami-lies within the order ( Magall ó n et al., 1999 ). The underestima-tion 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 diver-gence of crown Malvales actually corresponds to divergences within the order and would thus decrease the “ super high ” di-versifi cation rates estimated for Malvales by Magall ó n and Castillo (2009) .

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

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 be-come fi xed across clades. These fossil leaves document the ear-liest 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-rej ó n Formation, exposed in the Cerrej ó n coal mines in the Cesar-Rancher í a basin, northern Colombia (11 ° 9 ′ 14.58 ″ N, 72 ° 36 ′ 30.43 ” W; Fig. 2 ). The Cerre-j ó 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 continen-tal 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.

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 epifl uorescence using a Nikon Eclipse 50i microscope coupled to a mercury lamp, to detect preserved cuticle fragments. When present, leaf frag-ments were removed from the specimen and treated with Calgon 10% solution for 7 d, rinsed, followed by digestion with 10% HF for 1 – 2 h. Loose cuticle fragments were mounted in glycerin and observed under epifl uorescence.

An exhaustive morphological comparison was performed with numerous angiosperm families similar to Malvaceae using the National Cleared Leaf Col-lection stored at the Smithsonian Natural History Museum (USNM), and bo-tanical 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 Euphor-biaceae, Moraceae, Bixaceae, Urticaceae, Cucurbitaceae, Sapindaceae, Vita-ceae, 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 affi nities 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 sev-enty 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

1339A

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arvalho et al. —

Neotropical fossil M

alvaceae Table 1. Morphological comparison of Malvaceae fossil leaves.

TaxonLamina

dissectionPrimary

venation a Secondary

veinsMinor

secondariesAgrophic

veinsTertiary venation

Quaternary venation

Major vein

branchingTooth shape

Teeth order Sinus Symmetry

Principal vein

courseAccesory

veins Source b

“ Abutilon ” eakini Hollick Unlobed Actino Crasp Crasp Comp Opp Alt Prox Cv-Cv 1 Angular Sym Med-Str Anastom 8 “ Apeiba ” improvisa

MacGiniteUnlobed Actino 5 Brochid Brochid Comp Alt Ret – – – – – – – 18

Apeibopsis atwoodi Hollick Unlobed Pinnate Semicrasp Semicrasp Comp Opp Opp – – – – – – – 7, 8 Apeibopsis cyclophylla

LesquereuxUnlobed Pinnate Brochid Brochid S Ret Ret – – – – – – – 17

Bombacites eocenicus Berry

Comp Pinnate Semicrasp Semicrasp Absent Ret Ret – Cc-Cc 1 Angular Asym Str-prox Absent 4

Bombacites jacksonensis Berry

Comp Pinnate Brochid Brochid Absent Ret Ret – – – – – – – 3

“ Dombeya ” novimundi Hickey

3 Lobed Actino 5 Semicrasp Semicrasp Comp Ret Ret – Cc-Cc 1 Angular Asym ? ? 6

Dombeyopsis decheni Weber. 3 Lobed Actino 5 Semicrasp Semicrasp Comp Opp Ret Prox Cv-Cc 2 Angular Asym Curv-prox ? 19 Dombeyopsis lobata Unger 3 Lobed Actino Brochid Brochid Comp Opp Ret Prox – – – – – – 12, 13,

20 Dombeyopsis obtusa

Lesquereux3 Lobed Actino Brochid Brochid Comp Opp Ret Pro – – – – – – 14

Dombeyopsis ovata Knowlton

3 Lobed Actino Brochid Brochid Comp Opp Ret Prox – – – – – – 11

Dombeyopsis plantanoides Lesquereux

3 Lobed Actino Crasp Crasp Comp Alt ? Prox – – – – – – 14

“ Grewia ” alaskana Hollick Unlobed Actino 7 Crasp Crasp Comp Opp ? Prox Cv-Cv 1 Angular Sym Med, curv ? 7 “ Grewia ” crenata Unger

HeerUnlobed Actino Semicrasp Semicrasp Comp Opp Ret Prox Cv-Cv 1 Angular Asym Med, curv ? 19

Grewiopsis acuminata Lesquereux

Unlobed Actino Crasp Crasp S Opp Opp – Cc-Cc 1 Angular Asym Curv-prox Cv 16

Grewiopsis formosa Berry Unlobed Actino Crasp Crasp S Opp Ret Prox Cv-Cv 1 Angular Sym Str-prox Cv 2 Grewiopsis tiliacea Sap. Unlobed Actino Crasp Crasp Comp Opp Opp – Cv-Cc 1 Curved Asym Curv-prox Cv 19 Grewiopsis tuscaloosensis

BerryUnlobed Pinnate Crasp Crasp S Opp ? Prox Cv-Cc 1 Angular Asym Curv-prox ? 2

Grewiopsis wadii Berry Unlobed Actino 3 Crasp Crasp S Opp ? – Cv-Cc 1 Angular Asym Str-prox ? 3 Grewiopsis yukonensis

Hollick3 Lobed Pinnate Crasp Brochid S Opp ? Prox Cv-Cv 1 Curved Asym ? ? 7

“ Luehea ” newberryana Knowlton MacGinite

Unlobed Actino 3 Semicrasp Semicrasp S Opp Opp – Cv-Cv 1 Angular Sym Str-prox Cv 18

Pterospermites carolinensis Berry

Unlobed Pinnate Brochid Brochid S Ret ? Prox – – – – – – 2

Pterospermites dentatus Heer

Unlobed Actino Crasp Crasp S Opp Opp – Cv-Cv 1 Curved Sym Curv-prox Anastom 19

Pterospermites haquei Knowlton

Unlobed Pinnate Crasp Crasp S Alt ? – Cv-Cc 1 Curved Asym Str-prox Cv 9

Pterospermum conforme Hollick

Unlobed Pinnate Crasp Brochid S ? ? Prox Cv-Cv 1 Curved Sym Str-prox ? 7

“ Sterculia ” atwoodi Hollick Unlobed Pinnate Crasp Brochid S Opp Ret – – – – – – – 7 “ Sterculia ” basiauriculata

Hollick3 Lobed Actino 3 Brochid Brochid S Opp Ret – – – – – – – 7

“ Sterculia ” elegans Fontaine 3 Lobed Actino Brochid Brochid S Ret Ret ? – – – – – – 5 “ Sterculia ” labrusca Unger 3 Lobed Actino 3 Brochid Brochid Comp Ret Ret – – – – – – – 8 “ Sterculia ” reticulata

Lesquereux3 Lobed Actino Brochid Brochid S Ret Ret – – – – – – – 17

“ Sterculia ” subtilis MacGinite

3 Lobed Pinnate Brochid Brochid S Ret Ret – Cv-Cc 1 Curved Asym Absent Absent 18


(Appendix 2; online Appendix S2). The scored genera were chosen based on 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 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, re-cent taxonomic treatments of the genera were followed for species selection to avoid misplacement of polyphyletic genera. In each case, several closely re-lated 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 indepen-dently 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 confl ict between independent trees and the ‘ supertree ’ . Most of the examined leaf fea-tures are highly homoplasious within Malvaceae, and for this reason, only char-acters inferred to be synapomorphic and characters conserved within various clades at various levels are discussed to support taxonomic affi nities of the fos-sil leaves.

Fossils are stored in the paleontological collections of the Colombian Geo-logical Institute (INGEOMINAS) in Bogot á , Colombia (repository acronym ING).

SYSTEMATICS

Family — Malvaceae Juss.

Subfamily — Malvoideae

Morphogenus — Malvaciphyllum Anz ó tegui

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 ac-tinodromous, 5 – 9 basal primary veins; secondary veins craspe-dodromous, fi rst pair of costal secondary veins branching 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 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 0616 – 0620, ING 0984, ING 0985, ING 1056, ING 1075 ( Fig. 5A ), ING 1076 – 1078, ING 1080 – 1096, ING 1097 ( Fig. 5C ), ING 1098, ING 1099 – 1101, ING 1102 ( Fig. 5B ), ING 1103 – 1121, ING 1357, ING 1358, ING 1410, ING 1411. T

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1341August 2011] Carvalho et al. — Neotropical fossil Malvaceae

tooth apex, lacking any type of glandular swelling or projec-tion. 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 ( Jaramillo et al., 2007 ).

Systematic affi nity within angiosperms — Palmate leaf ve-nation, toothed margins, and stellate trichomes are wide-spread and conspicuous in most Malvaceae ( Kubitzki and Bayer, 2003 ). However, these characters occur in other line-ages of angiosperms, refl ecting the repeated evolution of palmate venation patterns ( White, 2005 ). Despite this evolu-tionary trend, tooth shape and venation characters exhibit fa-milial 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 pat-tern 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 form-ing 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 Malvaciphyl-lum 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, Rosa-ceae, among others (online Appendix S1), show distinctive tooth morphology, including various types of glandular thick-enings and accessory veins that differ from those seen in extant Malvaceae and Malvaciphyllum macondicus (For detailed com-parison 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 princi-pal 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 Malva-ceae, differs in having teeth with principal veins that extend beyond the blade lamina.

The combination of characters seen in Malvaciphyllum ma-condicus : 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., Cer-rej ó n coal mines, Guajira, Colombia.

Etymology — The epithet “ macondicus ” refers to the fi ctional town Ma-condo, described by Gabriel Garc í a M á rquez (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 mac-rophyllous 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 (3.99 – 17.54) cm (measured in 11 specimens) long and 8.85 (3.34 – 16.4) 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 refl ex angle ( Fig. 4B ). The laminar surface is densely pubescent, covered with coalifi ed stellate and acicular trichomes (observed in specimens ING 1410, ING 1411; Fig. 5D, E ). The primary vein framework is actinodromous, with 5 – 9 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 fi 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 ex-medially parallel to costal tertiaries. Fourth order veins are mixed opposite/alternate percurrent; fi fth order veins are reg-ular 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 ve-nation 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 fi rst order teeth are generally present and supplied by the fi rst pair of lateral primaries; they are convex-straight 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 fl exuous-fl exuous, symmetrical to slightly asymmetrical. All teeth exhibit a medial principal vein that terminates at the


eumalvoids is supported by the occurrence of the two charac-ters 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 Eumal-voideae. Even though most taxa in this group are known to have small leaves markedly different from the mesophyll and macro-phyll leaf blades of M. macondicus , large leaves are commonly found in tropical and subtropical genera such as Hibiscus , Wer-cklea , 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 prev-alent 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 Anz ó tegui was described from two species of fossil leaves from Miocene and Pliocene deposits of Argentina and Brazil, respec-tively, and was initially related to extant Abutilon ( Anz ó tegui 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 affi nities 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 mar-gins, opposite-percurrent fourth order venation, and lack of pul-vini in M. quenquiadensis ( Anz ó tegui 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 fi nd a special affi nity of Dombeya novi-mundi to extant Dombeya or the clade that includes this genus. Dombeya novi-mundi , described by Hickey (1977) , is known from Eocene de-posits 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 5 – 7 actinodromous primary veins, a toothed margin, a pulvinulus at the base of the leaf blade, and concentric, opposite percurrent tertiary veins with well-developed

Character optimizations and affi nities within Malva-ceae — Simple, palmately veined leaves with dentate-crenate margins are common in six of nine subfamilies within Malva-ceae, including Byttnerioideae, Grewioideae, Helicteroideae, Tilioidae, Dombeyoideae, and Malvoideae. All leaf architec-ture characters were optimized on a supertree of Malvaceae as a means to explore for leaf characters that have become fi xed at various clade levels and could potentially prove to be useful for leaf identifi cation within a family of ~4500 spp. Over 90% of the leaf characters scored and mapped on the supertree com-piled for Malvaceae are highly homoplasious at family level (online Appendix S3), refl ecting the repeated convergence of leaf morphology within this group and the diffi culty of address-ing infrafamilial relations of fossil leaves. However, some char-acter 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 refl ected 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 , Fuertesi-malva ) to large, deeply cordate leaves of lowland tropical spe-cies 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 fi 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 re-stricted 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, refl ecting differ-ences 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. 3C – E ).

These two characters — the costal secondary and minor sec-ondary vein branching as well as three orders of teeth — distinguish Eumalvoideae from all other lineages of Malvaceae that have similar leaf architecture. The affi nity of M. macondicus to

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.

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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

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

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.


tectate, exine 2 µ m thick, nexine 0.5 µ m thick, columellae 1 µ m thick, tectum 0.5 µ m thick, columellae distinct, long, present only under muri of reticulum, tectum reduced to reticula; sculp-ture reticulate, heterobrochate, lumina 1 – 3 µ m wide at apocol-pia and surrounding the colpi, almost foveolate (lumina 0.5 µ m wide) at mesocolpia, muri pluricolumellate, 1 µ m wide, the transition from reticula to foveolae is gradual although in short distance, sometimes a pseudo-line separates foveolae from re-ticula. Dimensions: equatorial diameter 25 (38.5) 50 µ 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 charac-teristic of several genera including Aguiaria , Bernoullia , Bom-bacopsis , Bombax , Eriotheca , Pseudobombax , and Spirotheca ( Nilsson and Robyns, 1986 ) within the clade Bombacoideae.

DISCUSSION

Leaf character considerations — Leaf architecture charac-ters were optimized on pre-existing phylogenetic hypotheses as a means to assess within-group character variation and

in shape, seeming almost hook-shaped, and are fed by second-ary veins (rarely tertiary veins) that curve as they enter the tooth ’ s laminar projection. Teeth of D. novi-mundi are similar to those of some taxa in Grewioideae (such as species of Helio-carpus and Luehea ) and Byttnerioideae ( Abroma spp.), which used to be included in former Tiliaceae and Sterculiaceae, re-spectively, 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 sub-families of Malvaceae, this leaf morphology is more widespread than previously thought. Dombeya novi-mundi is probably re-lated to Malvaceae, but subfamily-level designations cannot be fully resolved with the existing characters, and affi nities to ex-tant Dombeya need further support from other features.

Pollen record — The fossil pollen Bombacacidites annae ( Van der Hammen, 1954 ; Germeraad et al., 1968 ) is very com-mon in sediments of the Cerrej ó n Formation ( Fig. 7 ) ( Jaramillo et al., 2007 ). The pollen is a monad, radial, isopolar, with amb triangular-obtuse-convex to almost circular; aperture tricolpo-rate, ectocolpi costate, very short, colpi slightly protruding, costae 3 µ m wide, endopore lalongate, pores indistinct; semi-

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 differ-entiation. 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.

1346 American Journal of Botany [Vol. 98 T

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co-occurring, clade-fi xed traits that were reliable for develop-ing hypotheses of natural affi nities. Two characters were recov-ered 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 particu-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 ( 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 sup-ply, may thus explain the presence of the proximal and distal branching in Eumalvoideae. Another possibility is that the ma-jor vein branching and increased size of the teeth fed by second-ary veins relates to the need to release excess water that is 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-ric habitats ( Fryxell, 1981 ; Turner and Mendenhall, 1993 ). 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-currence and restrictedness of these two traits, however, offers a recognizable distinction between the leaves of Eumalvoideae and all other Malvaceae that supports natural affi nities for the fossil here described.

Malvoideae fossil record — The macrofossil record for Mal-voideae 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 Anz ó tegui associ-ated 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 affi nities for most of them remain un-tested. 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 affi nity of these pollen grains. The earliest-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, 1989 ; MacPhail, 1999 ).

Based on Eocene pollen from Venezuela (37 – 40 Ma) and the records from the Murray Basin, Koopman and Baum (2008) estimated a divergence age for Eumalvoideae of 29.7 – 32.5 Ma. Malvaciphyllum macondicus shows that this group occurred in northern South America by 58 – 60 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


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 P é 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).


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 Cerrej ó 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.

Scenario 1 — Eumalvoideae could have originated in the neo-tropics and remained present there ever since; dispersal across the Pacifi c or through Antarctica (see Scenario 2 ) and regional extinction of basal genera in the neotropics would explain ex-tant distributions of the Australasian genera. This would be consistent with the occurrences of Eumalvoideae and phyloge-netically related Bombacoideae in the northern South American fossil record.

The extensive pollen record of Bombacoideae shows the ear-liest 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 Amer-ica and the proposed origin of eumalvoids in the neotropics dur-ing 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 briefl y con-nected 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 2 — Eumalvoideae 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 Amer-ica ( 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

clock inferences ( Koopman and Baum, 2008 ). The low number of calibration points and the derived nature of fossil taxa avail-able for this group make molecular clock estimation of diver-gence dates susceptible to possible underestimations. Evidence for divergence earlier than 40 Ma for Eumalvoideae is not sur-prising 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 occur-rence of eumalvoid leaves is consistent with the idea that the pollen morphology of eumalvoids evolved later than the dis-tinctive leaf morphology, supporting Malvaciphyllum as a stem group of this clade.

Biogeographical considerations — The sparse fossil evi-dence 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 Lagunari a, Howittia , and Radyera ( Figs. 1 and 6 ). The restricted distribution of this grade has been inter-preted by Baum et al. (2004) as suggestive of an Australasian origin for Eumalvoideae, in which case, the neotropical lin-eages within the group would have arrived via trans-Pacifi c 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

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.


ica already harbored the plant lineages that dominate neotropical forests in the present.

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have been yet recovered, and the Gulf Coast-centered record for its sister group, Bombacoideae, seems to confl ict with this view.

Scenario 3 — A third possible dispersion route, neither trans-Pacifi c ( Baum et al., 2004 ) nor Antarctic (as in scenario 2), could have been across high northern latitudes. There are mul-tiple examples of animal and plant taxa moving across high lati-tude land bridges and into South America in the Paleogene, including arctostylopid mammals ( Missiaen et al., 2006 ), Sal-vinia ( 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 Bomba-coideae 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 diversifi cation at its basalmost nodes are still poorly sup-ported. 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 ; Missi-aen 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 distribu-tions decreases.

Paleoecological insights — The Cerrej ó n fl ora resembles ex-tant neotropical rainforests in terms of rank – order abundance and fl oristic composition, mean annual temperature and pre-cipitation ( Wing et al., 2009 ). This fl 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 fi ne-grained sediments suggests little predepositional trans-port and therefore that the plants grew in the local setting of lower delta plain lakes, ponds, and swamps. In these environ-ments, 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, eumal-voids 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 ( G ó mez-Navarro et al., 2009 ).

The occurrence of Malvaciphyllum macondicus , along with two other malvalean fossil leaves from Cerrej ó n fl ora not de-scribed in this study (morphotypes CJ25 and CJ36; see Wing et al., 2009 , Supporting Information), and the high pollen abun-dance of Bombacoideae suggest that derived lineages of Mal-vaceae were already a diverse element of neotropical rainforests of the late Paleocene. This adds specifi city to previous observa-tions that the middle-late Paleocene rainforests of South Amer-


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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 Pittier Pentace 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. Perrier Phymosia Desv. ex Ham. Ayenia L. Heritiera Aiton Physodium C. Presl Bastardia Kunth Herrania Goudot Pterygota 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 Ducke Robinsonella Rose & Baker f. Bombycidendron Zoll. & Moritzi Jarandersonia Kosterm. Ruizia Cav. Brachychiton Schott & Endl. Kearnemalvastrum D. M. Bates Rulingia R. Br. Briquetia Hochr. Keraudrenia J. Gay Scaphium Schott & Endl. Brownlowia Roxb. Kleinhovia L. Scaphopetalum Mast. Burretiodendron Rehder Kokia Lewton Schoutenia Korthals Byttneria Loefl . Krapovickasia Fryxell Senra 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. Evans Malvella Jaub. & Spach Tarasa Phil. Cristaria Cav. Malva L. Tetralix Griseb. Cullenia Wight Mansonia 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 Marsili Mortoniodendron Standl. & Steyerm.Fremontodendron Coville Neobrittonia Hochr. Fryxelia D. M. Bates Neobuchia Urb. Fuertesimalva Fryxell Nesogordonia Baill. Gaya Kunth Nototriche Turcz.


Character Character states

1 Leaf complexity 0: Simple; 1: Compound2 Petiole insertion 0: Marginal; 1: Peltate3 Leaf size 0: Microphyll; 1: Notophyll; 2: Mesophyll; 3: Macrophyll4 Length: Width Ratio 0: 1-1; 1: 2-1; 2: 3-1; 3: 3-2; 4: 5-45 Shape of the lamina 0: Elliptic; 1: Ovate; 2: Obovate6 Medial symmetry of the lamina 0: Strictly asymmetric; 1: Symmetric7 Basal symmetry of the lamina 0: Strictly asymmetric; 1: Symmetric8 Lobation 0: Non lobed; 1: Palmately lobed9 Margin 0: Entire; 1: Dentate10 Special features of the margin 0: Absent; 1: Thickened margin; 2: Sinuous margin; 3: Revolute margin11 Base angle 0: Refl ex; 1: Acute; 2: Obtuse12 Base shape 0: Cordate; 1: Convex; 2: Decurrent; 3: Cuneate; 4: Rounded; 5: Lobed; 6: Complex13 Apex angle 0: Acute; 1: Obtuse14 Apex shape 0: Acuminate; 1: Straight; 2: Convex; 3: Rounded15 Terminal apex features 0: Non distinctive; 1: Mucronate; 2: Spinose16 Surface texture 0: Smooth; 1: Pubescent17 Surfi cial Glands 0: Absent; 1: Laminar; 2: On veins18 Primary venation network 0: Actinodromous; 1: Pinnate19 Number of basal veins 0: 1; 1: 3; 2: 5; 3: 7 – 920 Agrophic veins 0: Absent; 1: Simple; 2: Compound21 Major secondary vein framework 0: Basal eucamptodromous; 1: Craspedodromous; 2: Semicraspedodromous; 3: Brochidodromous22 Interior secondaries 0: Absent; 1: Present23 Minor secondary course 0: Semicraspedodromous; 1: Craspedodromous; 2: Brochidodromous24 Perimarginal veins 0: Absent; 1: Fimbrial veins25 Major secondary spacing 0: Consistent; 1: Inconsistent; 2: Abruptly increasing basally; 3: Gradually increasing basally26 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 basally27 Major secondary attachment to midvein 0: Excurrent; 1: Decurrent; 2: Defl ected28 Intersecondary veins 0: Absent; 1: Present29 Intersecondary veins — course 0: Parallel to secondaries; 1: Perpendicular to midvein30 Intersecondary veins — length 0: Same as subjacent secondaries; 1: Less than half of subjacent secondaries; 2: More than half of

subjacent secondaries31 Intersecondary veins — termination 0: With subjacent secondaries; 1: Basifl exed; 2: Reticulate32 Intercostal tertiary venation framework 0: Reticulate; 1: Alternate percurrent; 2: Opposite percurrent33 Intercostal tertiary angle variability 0: Consistent; 1: Inconsistent; 2: Increasing exmedially; 3: Increasing proximally34 Epimedial tertiaries 0: Reticulate; 1: Alternate percurrent; 2: Opposite percurrent35 Exterior tertiary course 0: Looped; 1: Terminating at the margin; 2: Looped with teeth36 Quaternary vein fabric 0: Alternate percurrent; 1: Opposite percurrent; 2: Reticulate37 Quinternary vein fabric 0: Irregular reticulate; 1: Regular reticulate38 Areolation 0: Good development; 1: Moderate development; 2: Poor development39 Freely ending veinlets 0: Absent; 1: Non ramifi ed; 2: Ramifi ed40 Marginal ultimate venation 0: Ramifi ed; 1: Anastomosing; 2: Fimbrial vein41 Tooth spacing 0: Regular; 1: Irregular42 Number of orders of teeth 0: 1; 1: 2; 2: 343 Veins forming teeth 0: Primaries; 1: Secondaries; 2: Primaries and secondaries; 3: Secondaries and tertiaries; 4:

Tertiaries; 5: Primaries, secondaries and tertiaries44 Number of teeth per cm 0: One to two; 1: Three to fi ve; 2: Six to eight; 3: Nine to eleven45 Tooth sine 0: Curved; 1: Angular46 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 apex48 Principal vein course 0: Medial; 1: Closer to proximal fl ank; 2: Closer to distal fl ank49 Principal vein curvature 0: Straight; 1: Curved50 Accesory veins 0: Absent; 1: Present51 Course of major accesory veins 0: Looped; 1: Convex; 2: Straight52 Special features of the tooth apex 0: Marginal; 1: Mucronate; 2: Spinose53 Branching of major veins 0: Absent; 1: Only proximal; 2: Proximal and distal

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


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 ó , 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 Crist ó bal 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. Christopher-Nevis, 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. L é v.) Rehder USNM Cleared leaf collection 8041. Byttneria ancistrodonta Mildbr. Palacios 8140, Provincia de Sucumb í os, Ecuador, 1991, US 3290270; Palacios 9021 , Province of Sucumb í os, Ecuador, 1991, US 3299287; USNM Cleared leaf collection 11516. Byttneria dentata Pohl. USNM Cleared leaf collection 11517.

Ceiba pentandra (L.) Gaertn. Gentry 24534, Choc ó , Colombia, 1979, HUA 11125; Rodr í guez 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, Goi á s Province, Brazil, US 2833229; Elias 751 , Atl á ntico, Colombia, 1929, US 1443072; Tamayo 971 , Falc ó n 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 griffi thii (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 Nu ñ ez 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 é , s.n., Rio de Janeiro, Brazil, US 2599921; USNM Cleared leaf collection 10464 (fi 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; S á nchez-G ó mez 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 (fi 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; Renter í a 10899 , Choc ó , Colombia, 1995, HUA 99400; Id á rraga A 2901 , Choc ó , 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 , Pet é n Province, Guatemala, 1967, US 2558505; Lundell 18153 , Pet é n Province, Guatemala, 1964, US 2479936; USNM Cleared leaf collection 3880.

Neoregnellia cubensis Urb. Ekman Pl.ind.Occ.16692, Pinar del R í o, 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.


(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.) M ü ll. 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 stryracifl ua L. USNM Cleared leaf collection 60, 928, 11912, 14582, 14583. Parrotiopsis jacquemontiana (Decne.) Rehder USNM Cleared leaf collection 1128 (fi 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.

Pachira quinata (Jacq.) W.S. Alverson G ó mez A 566 , Antioquia, Colombia, 1992, HUA 81387; Callejas 12230 , Antioquia, Colombia, 1990, HUA 116541; Vel á squez-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 fi rmifl ora Schery Pringle 5447 , Jalisco, M é xico, 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; P é rez J 964, Santander, Colombia, 1999, HUA 12724, Fern á ndez-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, Sucumb í os Province, Ecuador, 1991, US 3258986; Little 671 , Morona-Santiago, Ecuador, US 2972702; Ortega 36, Morona-Santiago, 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; V é lez JG 5444 , Valle del Cauca, Colombia, April 2003, HUA 138678; Hoyos-G ó mez SE 521 , Choc ó , 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, C ô te-d ’ Ivoire, 1907, US 2543376; USNM Cleared leaf collection 3656, 4609, 14449. Triumfetta speciosa Seem. USNM Cleared leaf collection 11510, 17093. Trochetia parvifl ora Bojer USNM Cleared leaf collection 4612.

Wercklea ferox (Hook. f.) Fryxell Nu ñ ez 23921 , Cusco, Peru, 1998, US.

Euphorbiaceae

Acalypha cinta M ü ll. Arg. USNM Cleared leaf collection 11463. Acalypha macrostachya Jacq. USNM Cleared leaf collection 11471. Alchornea triplinervia (Spreng.) M ü ll. 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

Carvalho Et Al_2011_Malvaceae Cerrejon Flora

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