Bogotá, D.C. 2011

UNIVERSIDAD DE LOS ANDES FACULTAD DE CIENCIAS DEPARTAMENTO DE CIENCIAS BIOLÓGICAS PIPER FOSSIL FROM A NEOTROPICAL FOREST OF THE LATE CRETACEOUS OF COLOMBIA : INFERRED AGES OF ORIGIN AND PATTERNS OF DIVERSIFICATION OF THE GENUS CAMILA MARTÍNEZ AGUILLÓN BOGOTÁ , D.C. 2011 UNIVERSIDAD DE LOS ANDES FACULTAD DE CIENCIAS DEPARTAMENTO DE CIENCIAS BIOLÓGICAS PIPER FOSSIL FROM A NEOTROPICAL FOREST OF THE LATE CRETACEOUS OF COLOMBIA : INFERRED AGES OF ORIGIN AND PATTERNS OF DIVERSIFICATION OF THE GENUS CAMILA MARTÍNEZ AGUILLÓN TESIS DE POSGRADO PARA OPTAR AL TÍTULO DE MAGÍSTER EN CIENCIAS BIOLÓGICAS DIRECTOR : SANTIAGO MADRIÑÁN (U NIANDES ) CODIRECTOR : CARLOS JARAMILLO (STRI) BOGOTÁ , D.C. 2011 ABSTRACT • Premise of study: The description of the new fossil Chavicoides schilleriphyllum from the late Cretaceous of Colombia is not only the first record associated with Piperaceae, but one of the oldest angiosperm macrofossils from the Neotropics. The study of C. schilleriphyllum within a phylogenetic framework allows an approach to understand the evolutionary history of Piper . • Methods: Leaf architecture characters of the fossil were compared to extant angiosperms. The phylogenetic position of C. schilleriphyllum was established based on a combined analysis of a molecular topology and a morphological matrix in order to make an internal calibration of the phylogeny of extant species. • Key Results: The dated phylogeny estimates that the genus Piper was originated in the Early Cretaceous. The diversification events started since the Late Cretaceous and continued gradually increasing until end of the Paleogene when the diversification rates turned exponential. • Conclusions : Chavicoides schilleriphyllum suggest that the habitat of Piper in the Late Cretaceous was an understory of a warm and wet forest. The genus seems to have originated in the Early Cretaceous and its actual distribution, may be a result of vicariance events. The incredible number of Piper species can be explained by a long history that is intensified during the end of the Paleogene when the uplift of the Andes together with development of the Amazon forest caused exponential rates of diversification. MARTÍNEZ , C. –– Piper fossil record from the Late Cretaceous 2 Key words: Colombia; dated phylogeny; fossil leaves; fossil record; Guaduas Formation; Late Cretaceous; Maastrichtian; paleobotany; Piper; Piperaceae.. AKNOWLEDGMENTS I would like to thank to Drs. S. Madriñán and C. Jaramillo for their help as advisors of this work; Dr. R. Callejas for valuable commentaries along the study; M. Gutierrez who collected the fossils from the Guaduas Formation, for allow me to work with them; the herbaria US, HUA, COL for let me visit the collection; the Paleobotanical Collection from the United States National Museum of Natural History for let me visit the collection; the herbarium HUA for provide me cuticle samples. This project was supported by the Cuatrecasas Fellowship Award from the Smithsonian Institution; the University of Missouri Columbia through the collaboration of Dr. A. Jaramillo; and the Universidad de los Andes through the Proyecto Semilla. MARTÍNEZ , C. –– Piper fossil record from the Late Cretaceous 3 INTRODUCTION The tropical rainforest can be documented in the fossil record based on reliable and accessible characteristics that fall into three broad categories, climatic indicators, taxonomic lineage indicators, physiognomic features of leaves and multistratification (Burnham and Johnson, 2004). The climatic conditions are defined as an annual rainfall of 1800 mm or greater, and a mean annual temperature (MAT) between 18ºC and 28ºC. The taxonomic indicators are principally the dominance of angiosperms, where more than 80% of individuals belong to the palm family or dicotyledonous angiosperm families. The physiognomy of leaves is characterized by the presence of entire margins, drip tips and large leaf size (Burnham and Johnson, 2004). The multistratification of the forest refers to tree crowns forming different strata that react different to light and other factors (Grubb et al., 1963; Morley, 2000). The earliest record of a Neotropical rainforest has recently been documented from the Paleocene of Colombia (Doria et al., 2008; Herrera et al., 2008; Gomez-Navarro et al., 2009). The similar family-level flora composition of Paleocene and modern Neotropical rainforests suggests that these plant groups have dominated the tropics for a long time (Doria et al., 2008; Herrera et al., 2008; Gomez- Navarro et al., 2009; Wing et al., 2009). Pre-Paleocene evidence for an angiosperm- biomass dominated, multistratified rainforest in South America is neither supported nor rejected by the scant data available (Jaramillo et al., 2010b). Almost no macrofossils from tropical floras of Cretaceous age have been placed in modern angiosperm orders (Burnham and Johnson, 2004). A recently found fossil flora, from the Guaduas Formation, a Maastrichtian (Late Cretaceous) assemblage from the central Andes of MARTÍNEZ , C. –– Piper fossil record from the Late Cretaceous 4 Colombia represents a good opportunity to explore the tropical forests of the Cretaceous (Gutierrez and Jaramillo, 2007). Preliminary analyses show that leaf physiognomy of Guaduas fossils was dominated by mesophyll-macrophyll leaf sizes with brochidodromous-eucamptodromous venation and entire margins, suggesting a warm and wet palaeoclimate, as is seen in today’s tropical rainforest (Jaramillo et al., 2010b). However, the Guaduas flora lacks key floristic elements that are present in modern Neotropical floras (e.g., Fabaceae, Menispermaceae, Moraceae) (Jaramillo et al., 2010b). Estimations of leaf margin and leaf area, for paleoprecipitation and paleotemperature based on Wilf equations (1997), indicate that this locality presented a MAT of 22 ± 3.4ºC and a mean annual precipitation (MAP) of 2400 mm/year (range 1800–3500 mm) that falls within the modern ranges of tropical rainforests (Gutierrez and Jaramillo, 2007). Nevertheless, is worth noting that new insights into paleo-estimations of MAT and MAP based on that multivariate and phylogenetic approaches are more accurate and precise (Little et al., 2010; Pepper et al., 2011). The Eastern Cordillera of Colombia, where the Guaduas Formation is located, is the easternmost branch of a retroarc fold- and- thrust belt related to the Late Cretaceous– Cenozoic shortening, resulting from the interaction between the Nazca, Caribbean and South American plates (e.g. Cooper et al., 1995; Gomez et al., 2009; Parra et al., 2009; Parra et al., 2010). The Guaduas Formation is a mudstone succession, with sand and coal levels accumulated in different depositional environments that ranges from a supratidal zone to a coastal floodplains and swamps (Sarmiento-Rojas et al., 2006; Amaya et al., 2010). The Guaduas Flora contains approximately 1200 specimens and 45 morphotypes. MARTÍNEZ , C. –– Piper fossil record from the Late Cretaceous 5 Although the taxonomic affinities of all the morphotypes has not been yet established, is known that, angiosperms dominated the floodplain environment, with 32 morphotypes described as dicotyledonous, 10 as monocotyledonous, and only two as ferns (pers. comm. Mauricio Gutierrez, 2009). Rhamnaceae has been documented in this flora, based on well preserved leaves and fruits (Correa et al., 2010). Other possible families like Araceae, Arecaceae, Lauraceae, Zingiberaceae, Fabaceae, Moraceae, and Menispermaceae are absent. This study describes one of the most abundant morphotypes of the Guaduas flora, the morphotype GD5, which resembles the genus Piper (Piperaceae) based on leaf megafossil impressions and compressions. The Piperaceae are an emblematic family of tropical rainforests. Piper is one of the most diverse genera within the angiosperms, with approximately 2,000 species distributed pantropically (Fig. 1) (Jaramillo and Manos, 2001; Quijano-Abril et al., 2006). Piper reaches its highest diversity in the lowlands of the Neotropics, is often a dominant element in the understory and has been found as one of the five most species-rich genera in Neotropical forests (Gentry, 1990). The elevation range for the genus is 0–2500 m, with a few species occurring above 3000 m. The abundance and morphological diversity of Piper have been proposed as a model of evolution of Neotropical secondary vegetation (Gomez-Pompa, 1971). Piper species have been considered key species on the basis of its relation with frugivorous bats (Fleming, 1985; Bizerril and Raw, 1998; Jaramillo and Manos, 2001). Synapomorphies of Piper are their swollen nodes and perianthless flowers arranged in condensed terminal spikes (Jaramillo et al., 2008). Growth habits ranges from mid-size shrubs to treelets and vines (Jaramillo and Callejas, 2004). Small shrubs are MARTÍNEZ , C. –– Piper fossil record from the Late Cretaceous 6 more associated to the understory of very wet lowlands in the Neotropical forest suggesting more tolerance to shade conditions, while the other habits mentioned are more characteristic of dryer and exposed conditions (Jaramillo and Callejas, 2004). Leaf architecture characters, which are of great importance in this study, present high variation along the genus. Flower presentation may be correlated with their pollination system (Jaramillo and Manos, 2001) that has been identified as ambophilous (wind and small insects) (De Figueiredo and Sazima, 2000). Recent molecular phylogenetic studies of Piperaceae have described Piper as monophyletic and sister to Peperomia (Jaramillo and

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