Paleocene wind-dispersed fruits and seeds from Colombia and their implications for early Neotropical rainforests

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Abstract

Extant Neotropical rainforests are well known for their remarkable diversity of fruit and seed types. Biotic agents disperse most of these disseminules, whereas wind dispersal is less common. Although wind-dispersed fruits and seeds are greatly overshadowed in closed rainforests, many important families in the Neotropics (e.g., Bignoniaceae, Fabaceae, Malvaceae, Orchidaceae, Sapindaceae) show numerous morphological adaptations for anemochory (i.e. wings, accessory hairs). Most of these living groups have high to moderate levels of plant diversity in the upper levels of the canopy. Little is known about the fossil record of wind-dispersed fruits and seeds in the Neotropics. Six new species of disseminules with varied adaptations for wind dispersal are documented here. These fossils, representing extinct genera of Ulmaceae, Malvaceae, and some uncertain families, indicate that wind-dispersed fruit and seed syndromes were already common in the Neotropics by the Paleocene, coinciding with the early development of multistratal rainforests. Although the major families known to include most of the wind-dispersed disseminules in extant rainforests are still missing from the Paleogene fossil record of South and Central America, the new fossils imply that anemochory was a relatively important product and/or mechanism of plant evolution and diversification in early Neotropical rainforests.

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  • ARDITTI J. & GHANI A.K.A. 2000. Tansley Review No. 110. Numerical and Physical Properties of orchid seeds and their biological implications. New Phytol. 145: 367-421.

  • AUGSPURGER C. 1986. Morphology and dispersal potential of wind-dispersed diaspores of Neotropical trees. Amer. J. Bot. 73: 353-363.

  • BAUM D.A. SMITH S.D. YEN A. ALVERSON W.S. NYFFELER R. WHITLOCK B.A. & OLDHAM R.L. 2004. Phylogenetic relationships of Malvatheca (Bombacoideae and Malvoideae; Malvaceae sensu lato) as inferred from plastid DNA sequences. Amer. J. Bot. 91: 1863-1871.

  • BAYONA G. CORTES M. JARAMILLO C. OJEDA G. ARISTIZABAL J.J. & REYES A. 2008. An integrated analysis of an orogen-sedimentary basin pair: Latest Cretaceous-Cenozoic evolution of the linked Eastern Cordillera orogen and the Llanos foreland basin of Colombia. Bull. Geol. Soc. Amer. 120: 1171-1197.

  • BAYONA G. MONTENEGRO O. CARDONA A. JARAMILLO C. LAMUS F. MORÓN S. QUIROZ L. ET AL. 2012. Estratigrafía procedencia subsidencia y exhumación de las unidades Paleógenas en el Sinclinal de Usme sur de la zona axial de la Cordillera Oriental. Geol. Colomb. 35: 5-35.

  • BERRY E.W. 1929. Tertiary Plants from Colombia South America. Proc. Natl. Acad. Sci. U.S.A. 75: 1-12

  • BRITTON N.L. 1893. Note on a collection of Tertiary fossil plants from Potosi Bolivia. Trans. Am. Inst. Min. 21: 250-257.

  • BROWN R.W. 1946. Alterations in some fossil and living floras. J. Wash. Acad. Sc. 36: 344-355.

  • BURGE D.O. & MANCHESTER S.R. 2008. Fruit morphology fossil history and biogeography of Paliurus (Rhamnaceae). Int. J. Pl. Sci. 169: 1066-1085.

  • BURNHAM R.J. 1986. Foliar morphological analysis of the Ulmoideae (Ulmaceae) from the early Tertiary of western North America. Palaeontographica B 201: 135-167.

  • BURNHAM R.J. 1995. A new species of winged fruit from the Miocene of Ecuador: Tipuana ecuatoriana (Leguminosae). Amer. J. Bot. 82: 1599-1607.

  • BURNHAM R.J. & CARRANCO N.L. 2004. Miocene winged fruits of Loxopterygium (Anacardiaceae) from the Ecuadorian Andes. Amer. J. Bot. 91: 1767-1773.

  • BURNHAM R.J. & JOHNSON K.R. 2004. South American palaeobotany and the origins of Neotropical rainforests. Philos. Trans. Roy. Soc. London B. 359: 1595-1610.

  • CALL V.C. & DILCHER D.L. 1997. The fossil record of Eucommia (Eucommiaceae) in North America. Amer. J. Bot. 84: 798-814.

  • CARVALHO M.R. HERRERA F.A. JARAMILLO C.A. WING S.L. & CALLEJAS R. 2011. Paleocene Malvaceae from Northern South America and their biogeographical implications. Amer. J. Bot. 98: 1337-1355.

  • CORREA E. JARAMILLO C. MANCHESTER S.R. & GUTIERREZ M. 2010. A fruit and leaves of rhamnaceous affinities from the Late Cretaceous (Maastrichtian) of Colombia. Amer. J. Bot. 97: 71-79.

  • DALLWITZ M.J. PAINE T.A. & ZURCHER E.J. 2000. Principles of interactive keys. Available from: http://deltaintkey.com. Accessed January 2013.

  • DENK T. & DILLHOFF R.M. 2005. Ulmus leaves and fruits from the Early-Middle Eocene of northwestern North America: systematics and implications for character evolution within Ulmaceae. Canad. J. Bot. 83: 1663-1681.

  • DILCHER D.L. POTTER F.W. & CREPET W.L. 1976. Investigations of angiosperms from the Eocene of North America: Juglandaceous winged fruits. Amer. J. Bot. 63: 532-544.

  • DORIA G. JARAMILLO C.A. & HERRERA F.A. 2008. Menispermaceae from the Cerrejón Formation middle to late Paleocene Colombia. Amer. J. Bot. 95: 954-973.

  • ENGLEHARDT H. 1895. Über neue Tertiärpflanzen Süd Amerikas. Abhandlungen der Abh. Senckenberg. Naturf. Ges. 19: 1-47.

  • ERIKSSON O. 2008. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence. Int. J. Pl. Sci. 169: 863-870.

  • ERIKSSON O. & KAINULAINEN K. 2011. The evolutionary ecology of dust seeds. Perspect. Pl. Ecol. Evol. Syst. 13: 73-87.

  • ERIKSSON O. FRIIS E.M. & LÖFGREN P. 2000. Seed size fruit size and dispersal systems in angiosperms from the Early Cretaceous to the Late Tertiary. Amer. Naturalist. 156: 47-58.

  • FERNÁNDEZ-ALONSO J.L. 2003. Bombacaceae neotropicae novae vel minus cognitae VI. Novedades en los géneros Cavanillesia Eriotheca Matisia y Pachira. Revista Acad. Colomb. Ci. Exact. 27: 25-37.

  • GAUTIER-HION A. DUPLANTIER J. M. QURIS R. FEER F. SOURD C. DECOUX J.-P. DUBOST G ET AL. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324-337.

  • GENTRY A.H. 1993. Diversity and floristic composition of lowland tropical forest in Africa and South America: 500-547. In: Goldblatt P. (eds) Biological relationships between Africa and South America Yale University Press New Haven USA.

  • GRIZ L.M.S. & MACHADO I.C. S. 2001. Fruiting phenology and seed dispersal syndromes in Caatinga a tropical dry forest in the northeast of Brazil. J. Trop. Ecol. 17: 303-321.

  • HABLY L. & THIÉBAUT M. 2002. Revision of Cedrelospermum (Ulmaceae) fruits and leaves from the Tertiary of Hungary and France. Palaeontographica B 262: 71-90.

  • HERRERA C.M. 1989. Seed dispersal by animals: A role in angiosperm diversification? Amer. Naturalist. 133: 309-322.

  • HERRERA F. MANCHESTER S.R. HOOT S.B. WEFFERLING K.M. CARVALHO M.R. & C. JARAMILLO. 2011. Phytogeographic Implications of fossil endocarps of Menispermaceae from the Paleocene of Colombia. Amer. J. Bot. 98: 2004-2017.

  • HICKEY L.H. 1977. Stratigraphy and paleobotany of the Golden Valley Formation (early Tertiary) of western North Dakota. Geol. Soc. Amer. Mem. 150: 1-183.

  • HLADIK A. & MIQUEL S. 1990. Seedling types and plant establishment in an African rain forest: 261-281. In: Bawa K. S. Hadley M. (eds) Reproductive ecology of tropical forest plants. The Parthenon Publishing Group Paris France.

  • HOWE H.F. & SMALLWOOD J. 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Evol. S. 13: 221-228. HUERTAS G. 1960. De la flora fossil de la Sabana. Boletín de Geología 5: 53-57.

  • JANSON C.H. 1983. Adaptation of fruit morphology to dispersal agents in a Neotropical forest. Science 219: 187-189.

  • JANSON C.H. 1992. Measuring evolutionary constraints: A Markov model for phylogenetic transitions among seed dispersal syndromes. Evolution 46: 136-158.

  • JARA-GUERRERO A. DE LA CRUZ M. & MÉNDEZ M. 2011. Seed dispersal spectrum of woody species in south Ecuadorian dry forests: Environmental correlates and the effect of considering species abundance. Biotropica 43: 722-730.

  • JARAMILLO C. & DILCHER D.L. 2001. Middle Paleogene palynology of central Colombia South America: A study of pollen and spores from tropical latitudes. Palaeontogr. Abt. B 285: 87-213.

  • JARAMILLO C. RUEDA M. & TORRES V. 2011. A palynological zonation for the Cenozoic of the llanos foothills of Colombia. Palynology 35: 46-84.

  • JARAMILLO C. BAYONA G. PARDO-TRUJILLO A. RUEDA M. TORRES V. HARRINGTON G.J. & MORA G. 2007. The palynology of the Cerrejón Formation (upper Paleocene) of northern Colombia. Palynology 31: 153-189.

  • KEAY R.W.J. 1957. Wind-dispersed species in a Nigerian forest. J. Ecol. 45: 471-478.

  • KOVAR-EDER J. KNÖRR U.C. & MAZOUCH P. 2012. Fruit ecology of Eocene and Neogene plant assemblages in Europe: Tracing shifts in dispersal syndromes. Palaios 27: 887-903.

  • KOVAR-EDER J. KVAČEK Z. & STRÖBITZER-HERMANN M. 2004. The Miocene Flora of Parschlug (Styria Austria) - Revision and Synthesis. Ann. Naturhist. Mus. Wien. 105: 45-159.

  • KVAČEK Z. MANCHESTER S.R. & AKHMETIEV M.A. 2005. Review of the fossil history of Craigia (Malvaceae s.l.) in the northern hemisphere based on fruits and co-occurring foliage: 114-140. In: Herman B. (eds) Modern problems of Palaeofloristics Palaeophytogeography and Phytostratigraphy. GEOS Moscow.

  • KVAČEK Z. MANUM S.B. & BOULTER M.C. 1994. Angiosperms from the Paleogene of Spitsbergen including an unfinished work by A.G. Nathorst. Palaeontographica B 232: 103-128.

  • LOHMANN L.G. BELL C.D. CALIÓ M.F. & WINKWORTH R.C. 2013. Pattern and timing of biogeographical history in the Neotropical tribe Bignonieae (Bignoniaceae). Bot. J. Linn. Soc. 171: 154-170.

  • LÓPEZ M. & RAMÍREZ N. 1989. Características morfológicas de frutos y semillas y su relación con los síndromes de dispersión de una comunidad arbustiva en la Guayana Venezolana. Ecologia 40: 354-371.

  • LORTS C.M. BRIGGEMAN T. & SANG T. 2008. Evolution of fruit types and seed dispersal: A phylogenetic and ecological snapshot. J. Syst. Evol. 46: 396-404.

  • MAGALLÓN-PUEBLA S. & CEVALLOS-FERRIZ S. R.S. 1994. Latest occurrence of the extinct genus Cedrelospermum (Ulmaceae) in North America: Cedrelospermum manchesteri from Mexico. Rev.

  • Palaeobot. Palynol. 81: 115-128.

  • MANCHESTER S.R. 1987. Extinct ulmaceous fruits from the Tertiary of Europe and western North America. Rev. Palaeobot. Palynol. 52: 119-112.

  • MANCHESTER S.R. 1989A. Systematics and fossil history of the Ulmaceae: 221-252. In: Crane P.R. Blackmore S. (eds) Evolution Systematics and fossil history of the Hamamelidae vol. 2: Higher Hamamelidae. Systematics Association Special vol. 40B Clarendon Press Oxford.

  • MANCHESTER S.R. 1989B. Attached reproductive and vegetative remains of the extinct American- European genus Cedrelospermum (Ulmaceae) from the early Tertiary of Utah and Colorado USA. Amer. J. Bot. 76: 256-276.

  • MANCHESTER S.R. & DONOGHUE M. 1995. Winged fruits of Linnaeeae (Caprifoliaceae) in the Tertiary of western North America: Diplodipelta gen. nov. Int. J. Pl. Sci. 156: 709-722.

  • MANCHESTER S.R. & O’LEARY E. 2010. Phylogenetic Distribution and Identification of Fin-winged Fruits. Bot. Rev. 76: 1-82.

  • MANCHESTER S.R. & TIFFNEY B.H. 2001. Integration of paleobotanical and neobotanical data in the assessment of phytogeographic history of holarctic angiosperm clades. Int. J. Pl. Sci. 162: S19-S27.

  • MARTINEZ C. JARAMILLO C. & CREPET W. 2014. Neotropical Cretaceous-Paleogene fossil macrofloras and its affinities with temperate America. Abstract of the 10th North American Paleontological Convention Gainesville USA Vol. 13.

  • MINAKI M. NOSHIRO S. & SUZUKI M. 1988. Hemiptelea mikii sp. nov. (Ulmaceae) Fossil Fruits and Woods from the Pleistocene of Central Japan. Bot. Mag. (Tokyo) 101: 337-351.

  • MIRLE C. & BURNHAM R.J. 1999. Identification of asymmetrically winged samaras from the Western Hemisphere. Brittonia 51: 1-14.

  • MORI S.A. & BROWN J. L. 1994. Report on wind dispersal in a lowland moist forest in central French Guiana. Brittonia 46: 105-125.

  • MULLER J. 1981. Fossil pollen records of extant angiosperms. Bot. Rev. 47: 1-142.

  • NEUBIG K. HERRERA F. MANCHESTER S.R. & ABBOTT J.R. 2012. Fossils biogeography and dates in an expanded phylogeny of Ulmaceae. Botany 2012: Annual Meeting of the Botanical Society of America in Columbus Ohio USA.

  • NYFFELER R. BAYER C. ALVERSON W.S. YEN A. WHITLOCK B.A. CHASE M.W. & BAUM D.A. 2005. Phylogenetic analysis of the Malvadendrina clade (Malvaceae s.l.) based on plastid DNA sequences. Org. Divers. Evol. 5: 109-123.

  • OLMSTEAD R.G. 2013. Phylogeny and biogeography in Solanaceae Verbenaceae and Bignoniaceae: a comparison of continental and intercontinental diversification patterns. Bot. J. Linn. Soc. 171: 80-102.

  • PAN A.D. CURRANO E.D. JACOBS B.F. FESEHA M. TABOR N. & HERENDEEN P.S. 2012. Fossil Newtonia (Fabaceae: Mimoseae) seeds from the early Miocene (22-21 Ma) Mush Valley in Ethiopia. Int. J. Pl. Sci. 173: 290-296.

  • PELL S.K. MITCHELL J.D. MILLER A.J. & LOBOVA T.A. 2011. Anacardiaceae: 7-50. In: Kubitzki K. (eds) Flowering Plants. Eudicots. The Families and Genera of Vascular Plants vol. 10 Springer New York.

  • PHILLIPS O. JAMES M. & GENTRY A. 2002. Global patterns of plant diversity: Alwyn H. Gentry’s Forest Transect Data Set. Missouri Botanical Garden Press St. Louis. MO.

  • PRANCE G.T. 1978. Notes on the vegetation of Amazonia I. A preliminary note on the origin of the open white sand campinas of the lower Rio Negro. Brittonia 30: 60-63.

  • RAMÍREZ R.S. GRAVENDEEL B. SINGER R.B. MARSHALL C.R. & PIERCE N.E. 2007. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448: 1042-1045.

  • RAPINI A. VAN DEN BERG C. & LIEDE-SCHUMANN S. 2007. Diversification of Asclepiadoideae (Apocynaceae) in the new world. Ann. Missouri Bot. Gard. 94: 407-422.

  • SINHA A. & DAVIDAR P. 1992. Seed dispersal ecology of a wind dispersed rain forest tree in the Western Ghats India. Biotropica 24: 519-526.

  • SMITH N. MORI S.A. HENDERSON A. STEVENSON D. Wm. HEALD S.V. 2004. Flowering Plants of the Neotropics. Princeton University Press Princeton New Jersey.

  • STULL G.W. HERRERA F. MANCHESTER S.R. JARAMILLO C. & TIFFNEY B.H. 2012. Fruits of an “Old World” tribe (Phytocreneae; Icacinaceae) from the Paleogene of North and South America. Syst. Bot. 37: 784-794.

  • STULTS D.Z. & AXSMITH B.J. 2011. First Macrofossil record of Begonia (Begoniaceae). Amer. J. Bot. 98: 150-153.

  • TAKAHASHI M. 1989. Pollen morphology of Celtidaceae and Ulmaceae: a reinvestigation: 253-265. In: Crane P.R. Blackmore S. (eds) Evolution Systematics and fossil history of the Hamamelidae vol. 2: Higher Hamamelidae. Systematics Association Special vol. 40B Clarendon Press Oxford.

  • TIFFNEY B.H. 1984. Seed size dispersal syndromes and the rise of the angiosperms: evidence and hypothesis. Ann. Missouri Bot. Gard. 71: 551-576.

  • TODZIA C.A. 1989. A revision of Ampelocera (Ulmaceae). Ann. Missouri Bot. Gard. 76: 1087-1102.

  • TODZIA C.A. 1992. A reevaluation of the genus Phyllostylon (Ulmaceae). SIDA. 15: 263-270.

  • VAN DER PIJL L. 1969. Principles of dispersal in higher plants. Springer Verlag Berlin - Heidelberg - New York.

  • WANG Y. & MANCHESTER S.R. 2000. Chaneya a new genus of winged fruit from the Tertiary of North America and eastern Asia. Int. J. Pl. Sci. 161: 167-178.

  • WANG Q. MANCHESTER S.R. LI C. & GENG B. 2010. Fruits and leaves of Ulmus from the Paleogene of Fushun northeastern China. Int. J. Pl. Sci. 171: 221-226.

  • WIEGREFE S.J. SYTSMA K. J. & GURIES R.P. 1994. Phylogeny of elms (Ulmus Ulmaceae): molecular evidence for a sectional classification. Syst. Bot. 19: 590-612.

  • WILDE V. & MANCHESTER S.R. 2003. Cedrelospermum fruits (Ulmaceae) and related leaves from the Middle Eocene of Messel (Hesse Germany). Cour. Forsch.-Inst. Senckenberg 241: 147-153.

  • WING S.L. & BOUCHER L.D. 1998. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Pl. Sc. 26: 379-421.

  • WING S.L. HERRERA F. JARAMILLO C. GÓMEZNAVARRO C. WILF P. & LABANDEIRA C.C. 2009. Late Paleocene fossils from the Cerrejón Formation Colombia are the earliest record of Neotropical Rainforest. Proc. Natl. Acad. Sci. U.S.A. 106: 18627-18632.

  • ZAVADA M.S. 1983. Pollen morphology of Ulmaceae. Grana 22: 23-30.

  • ZAVADA M.S. & KIM M. 1996. Phylogenetic analysis of Ulmaceae. Pl. Syst. Evol. 200: 13-20.

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