Int. J. Plant Sci. 171(4):392–408. 2010. Ó 2010 by The University of Chicago. All rights reserved. 1058-5893/2010/17104-0005$15.00 DOI: 10.1086/651229
PHYTOGEOGRAPHIC HISTORY AND PHYLOGENY OF THE HUMIRIACEAE Fabiany Herrera,1 ,*,y Steven R. Manchester,* Carlos Jaramillo,y Bruce MacFadden,*,z and Silane A. da Silva-Caminhay *Department of Biology, Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, U.S.A.; ySmithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Ancon, Panama´, Repu´blica de Panama´; and zDivision of Research on Learning (EHR/DRL), National Science Foundation, 4201 Wilson Boulevard, Arlington, Virginia 22031, U.S.A.
To place a new fossil occurrence of Sacoglottis in a broader context, we surveyed the fruit morphology of all extant genera of the Humiriaceae, conducted a cladistic analysis, and critically reviewed the fossil record for this family. Living and fossil fruits of Humiriaceae are recognized by a woody endocarp, germination valves, and, in some genera, wall cavities. The phylogenetic analysis based on 40 morphological characters yielded two most parsimonious trees indicating Vantanea as sister taxon to all genera among Humiriaceae. Schistostemon is indistinguishable from Sacoglottis in fruit morphology and is recovered as sister to Sacoglottis in the topology; we recommend restoring Schistostemon to the rank of subgenus within Sacoglottis. A review of prior published reports of fossil fruits attributed to Humiriaceae led to the rejection and/or reattribution of some records but supports recognition of Vantanea, Humiria, Humiriastrum, and Sacoglottis. The available characters do not support recognition of multiple fossil species of Sacoglottis. We recognize the occurrence of Sacoglottis tertiaria Berry emend. Herrera from Peru, Ecuador, Colombia, and a newly collected Miocene site from Panama. The Cenozoic fossil record of Humiriaceae in South and Central America, together with discreditation of former reports from Europe, strongly supports a Neotropical origin for this family. Keywords: fossils, Humiriaceae, phylogeny, morphology, Miocene, Panama. Online enhancements: appendixes.
Introduction
hiemstra et al. 2006; Pons and Franceschi 2007). The first endocarps were recognized in the early 1920s and ’30s (Berry 1922a, 1922b; Reid 1933). Unfortunately, little was known of the family, and comparative collections of extant species were very limited at that time. Many of those pioneering fossil identifications have been assumed to be systematically accurate and therefore cited as indicators of ancient biomes (Burnham and Johnson 2004), but they remain in need of careful reevaluation. We studied the fruit morphology of all extant genera of Humiriaceae with three objectives: (1) to seek new characters that could allow the recognition of genera, (2) to discuss the characters useful for the identification of fossil remains, and (3) to consider the utility of the fruits in phylogenetic analyses. Finally, we describe a new record of Sacoglottis based on permineralized endocarps from ;19.5–17-Myr-old deposits from the Cucaracha Formation of the Panama Canal and critically review previously reported fossil fruits and pollen of the family.
The Humiriaceae is a relatively small flowering plant family of the Malpighiales, with eight genera and ;50 species (Cuatrecasas 1961). It is distributed primarily in lowland to montane rain forests of the Neotropics but has a single species in rain forests of western Africa (fig. 1). The family has distinctive drupaceous fruits with woody endocarps having longitudinal germination valves and, in some genera, apical foramina and endocarp wall cavities. The fruits are known to be consumed and/or dispersed by rodents, tapirs, primates, birds, and bats and sometimes inhabited by beetle larvae (Cuatrecasas 1961; Macedo and Prance 1978; Henry et al. 2000; Johnson et al. 2001; Sabatier 2002; Lopes and Faria 2004; Ridgely et al. 2005). Additionally, the extinct megafauna and PaleoIndians of the Amazon rain forest apparently interacted with Humiriaceae (Roosevelt et al. 1996; Guimara˜es et al. 2008). Although the family is clearly monophyletic, the precise phylogenetic position of Humiriaceae relative to other Malpighiales is not clear yet (Bove 1997; Wurdack and Davis 2009). An early to middle Cretaceous origin has been inferred from molecular divergence estimates (Davis et al. 2005). The oldest fossil record of Humiriaceae, however, dates back to the Eocene (Berry 1924a, 1929a; this study). The fossil record of the family has been recognized on the basis of pollen, wood, and endocarps (Berry 1922a; Lorente 1986; Hoog1
Material and Methods We examined collections from the U.S. National Herbarium (US) at the Smithsonian Institution in Washington, DC; the Smithsonian Tropical Research Institute (STRI) in Panama; the University of Florida Herbarium (FLAS) in Gainesville, Florida; the Missouri Botanical Garden Herbarium (MO); the U.S. National Arboretum Herbarium (BARC); the Natural History Museum, London; and the Universidad Nacional (UN) in Bogota´, Colombia. Approximately 100 specimens of
Author for correspondence; e-mail:
[email protected].
Manuscript received August 2009; revised manuscript received January 2010.
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Fig. 1 Distribution of modern genera and location of fossil endocarps of the Humiriaceae. Base map courtesy of National Aeronautics and Space Administration Jet Propulsion Laboratory, California Institute of Technology.
46 species were measured and photographed (fig. 2; table A1 in the online edition of the International Journal of Plant Sciences). Transverse and longitudinal sections were cut through the center of the fruits or endocarps. The characters inspected are summarized in table 1. A new matrix, modified and expanded from that of Bove (1997), was prepared for the phylogenetic analysis (fig. 3). The character descriptions and scoring criteria are available in appendix B in the online edition of the International Journal of Plant Sciences and online at the MorphoBank Web site (http://www.morphobank.org; project P277, Matrix of Morphological Characters of Humiriaceae). Cladistic analyses were performed using PAUP*, version 4.0 (Swofford 2003), and the examination of character state distributions was completed using Mesquite, version 2.6 (Maddison and Maddison 2009). Our analysis was rooted with four outgroups, including the three used by Bove (1997), plus Caryocaraceae, in accordance with the most recent phylogeny of the Malpighiales (Wurdack and Davis 2009). To avoid assumptions regarding character state transitions, the 40 characters were treated as unordered. An exhaustive search with multistate taxa was carried out. Morphological characters were evaluated through a review of Bove (1997), Bove and Melhem (2000), and references therein (e.g., Cuatrecasas 1961; Narayana and Rao 1977) and through direct observation of the fruits. Characters were coded as polymorphic when more than one state was present, and characters not applicable for a taxon or simply not known were coded as missing. Support levels for tree nodes were assessed with the bootstrap procedure provided in PAUP*, version 4.0, using a branch-and-bound search and 10,000 bootstrap replicates. Eleven of 16 fossil endocarp taxa previously assigned to Humiriaceae were physically reexamined (table 2; fig. 4), re-
ferring to specimens deposited at the National Museum of Natural History (USNM) in Washington, DC; the Florida Museum of Natural History (UF) in Gainesville, Florida; the University of Amsterdam (UA); and the Philipps-University Marburg (UMBG), Germany. Newly recovered specimens of Sacoglottis tertiaria from Panama were deposited at STRI. Morphological data on extant Humiria pollen were obtained from the extensive study of pollen morphology of Humiriaceae by Bove and Melhem (2000) and the observation of two species from the Graham Pollen Collection hosted at STRI (Humiria balsamifera, slide 17520, Costa Rica, and Humiria guianensis, slides 5723 and 3011, Brazil). We used a Nikon I80 camera with Nomarsky microscopy and a Nikon DXM 1200 camera for the pollen observations. The newly recovered fossil endocarps reported in this study (fig. 5) were collected from the Gaillard Cut section (Lirio East outcrop) of the southeastern part of the Panama Canal (lat. 9°3920N, long. 79°399400W). The fossils were found in March of 2007 while exploring new temporary exposures created during the expansion of the canal. The plant locality is placed in the lowermost part of the Cucaracha Formation. Lithofacies, sedimentary structures, fossils, and ichnofossils suggest that the ;100–140-m-thick Cucaracha Formation was deposited in a succession grading from nearshore shallow marine environments at the base to terrestrial facies in upper levels. Kirby et al. (2008) reconstructed the formation as a coastal delta plain consisting of abundant paleosols, channel, levee, floodplain, marsh, and volcanic deposits. The Cucaracha Formation overlies the Culebra Formation, also exposed in the canal, which includes a distinct marine succession ranging from neritic environments at the base (coral reef, costal lagoon) to delta and prodelta fronts at the top (Woodring and Thompson 1949; Kirby et al. 2008; Moro´n et al.
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Fig. 2 Extant fruits of Humiriaceae. A, B, Endocarps of Sacoglottis guianensis Benth (US 3335606); note wide valves and five thin septa. C, Sacoglottis amazonica Mart (US 2279927); big cavities exposed in the endocarp wall. D, Schistostemon retusum (Ducke) Cuatr. (US 3084949); globose endocarp. E, Humiriastrum excelsum (Ducke) Cuatr. (US 2436147); valves short and five apical foramina. F, Endocarp of Humiriastrum piroparanense Cuatr. (US 2909057). G, Vantanea bahiaensis Cuatr. (US 3258568); apical view of endocarp showing six conspicuous valves. H, Vantanea depleta McPherson (STRI 5741); endocarp with acute apex, valves long and lingulate. I, Vantanea obovata (Nees & Mart.) Benth (US 2949961); ovoid endocarp with lingulate valves. J, Vantanea guianensis Aublet (US 2450957); endocarp with prominent brainlike surface and very dark narrow valves. K, Hylocarpa heterocarpa (Ducke) Cuatr. (US 30137); the endocarp shows five sharp ribs corresponding to the septa, and a valve is present at the bottom of the furrow. L, Sacoglottis amazonica Mart (UN 1745); cross section of endocarp showing thin septa, one seed, and big cavities. M, Sacoglottis ovicarpa Cuatr. (STRI 1296); thin exocarp, five carpels, and one seed in the endocarp. N, Sacoglottis trichogyna Cuatr. (US 3086758); note thick exocarp, five septa, and few cavities located at the border of the endocarp. O, Schistostemon fernandezii Cuatr. (US 2486757); thin septa and big cavities in the endocarp. P, Duckesia verrucosa Cuatr. (US 143); note four locules and intense furrowing and corrugation at the border of the endocarp and tiny cavities in the endocarp. Q, Humiriastrum excelsum (Ducke) Cuatr. (US 2941101); two seeds are surrounded by small cavities in the endocarp. R, Humiria crassifolia Mart. ex Urb. (US 3012820); five septa and two seminal cavities present in the endocarp. S, Vantanea deniseae Rodriguez (US 8613); seven septa and seven valves; note septa engrossing outward in the endocarp. T, Vantanea minor Benth (US 3065783); corrugated endocarp; note five locules with a pentagonal shape. U, Endopleura uchi (Huber) Cuatr. (US 2271080); note five sharp septa divided into two, giving a 10-radiate-shaped section of the endocarp.
2008). The ages of these formations have been obtained from mammals, pollen, marine invertebrates, magnetostratigraphy, and radiometric dating (Bold 1973; Woodring 1982 [1957]; Graham 1988a, 1988b; MacFadden and Higgins 2004; John-
son and Kirby 2006; MacFadden 2006; Kirby et al. 2008). These sources indicate an age of ;19.5–14 Ma for the Cucaracha Formation and 23–19 Ma for the underlying Culebra Formation (Kirby et al. 2008). These data suggest a late Early
HERRERA ET AL.—PHYLOGENY OF THE HUMIRIACEAE Miocene age (19.5–17 Ma) for the Humiriaceae fossil at the Lirio East site.
Results Fruit Morphology and Habitats of Extant Humiriaceae The Humiriaceae is characterized by epitropous ovules (one or two); free and thick petals; stamens united at the base in one to several whorls; thick, fleshy anthers with elongated connectives; a free disk; and a syncarpous superior ovary of three to 10 carpels. The leaves are alternate, simple, and mostly entire margined and coriaceous, and the xylem vessels include scalariform perforation plates (Aublet 1775; Jussieu 1829; Urban 1877; Cuatrecasas 1961; Gentry 1975). The distinctive drupaceous fruit develops a combination of diagnostic characters, mainly in the endocarp, that can facilitate identification (Cuatrecasas 1961). The endocarps are woody, with a central vascular axis, three to 10 carpels, and one or two seeds per locule. Each carpel is supplied with a germination valve. The endocarps of some genera also have apical foramina. Several genera also have cavities in the wall that have been referred to in the literature as resin or oil cavities (Cuatrecasas 1961). Among Malpighiales, we do not recognize any other families with fruits having the same set of characters seen in Humiriaceae. Fruits of the Caryocaraceae are slightly similar, with a woody and spinulose/corrugated endocarp, but they lack germination valves, endocarp wall cavities, and foramina, and the seeds are reniform rather than ellipsoidal to oblong (Prance and Freitas 1973). Here, we present a morphological review of the fruit characters for all genera of Humiriaceae: Vantanea, Humiria, Duckesia, Hylocarpa, Endopleura, Humiriastrum, Sacoglottis, and Schistostemon (table 1). Drupe size and shape. Among the genera, fruit size varies greatly (1.6 to ;10 cm in maximum length; table 1). The longest drupes occur in Vantanea and Hylocarpa (fig. 2J, 2K) and the smallest in Humiria (1.6 cm in length; fig. 2R). Because some species of Vantanea and Humiria are very similar in fruit morphology, size is useful for distinguishing them. The small drupes of Humiria seem to be related to dispersal by bats and birds (Cuatrecasas 1961; Macedo and Prance 1978; Ridgely et al. 2005). In general, the length of a drupe within an individual species and even within a genus does not vary more than a couple of centimeters. However, we caution that the size of the drupe should be used only in combination with other characters for identification of fossil species. The shape of the drupe is variable within genera of Humiriaceae and by itself is not a good character for identification of fossil endocarps (fig. 2). Even within a single species, fruits vary from ovoid or oblong to elliptic or globose (table 1). Cuatrecasas (1961), however, used this character for recognition of varieties. Exocarp and mesocarp. The exocarp is usually thin (
