Int. J. 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

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 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 as sister taxon to all genera among Humiriaceae. 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, , , 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 en- docarps were recognized in the early 1920s and ’30s (Berry The Humiriaceae is a relatively small flowering plant family 1922a, 1922b; Reid 1933). Unfortunately, little was known of of the , with eight genera and ;50 species (Cua- the family, and comparative collections of extant species were trecasas 1961). It is distributed primarily in lowland to mon- very limited at that time. Many of those pioneering fossil iden- tane rain forests of the Neotropics but has a single species in tifications have been assumed to be systematically accurate rain forests of western Africa (fig. 1). The family has distinc- and therefore cited as indicators of ancient biomes (Burnham tive drupaceous fruits with woody endocarps having longitu- and Johnson 2004), but they remain in need of careful reeval- dinal germination valves and, in some genera, apical foramina uation. and endocarp wall cavities. The fruits are known to be con- We studied the fruit morphology of all extant genera of Hu- sumed and/or dispersed by rodents, tapirs, primates, birds, miriaceae with three objectives: (1) to seek new characters and bats and sometimes inhabited by beetle larvae (Cuatreca- that could allow the recognition of genera, (2) to discuss the sas 1961; Macedo and Prance 1978; Henry et al. 2000; John- characters useful for the identification of fossil remains, and son et al. 2001; Sabatier 2002; Lopes and Faria 2004; Ridgely (3) to consider the utility of the fruits in phylogenetic analyses. et al. 2005). Additionally, the extinct megafauna and Paleo- Finally, we describe a new record of Sacoglottis based on per- Indians of the Amazon rain forest apparently interacted with mineralized endocarps from ;19.5–17-Myr-old deposits from Humiriaceae (Roosevelt et al. 1996; Guimara˜es et al. 2008). the Cucaracha Formation of the Panama Canal and critically Although the family is clearly monophyletic, the precise review previously reported fossil fruits and pollen of the family. phylogenetic position of Humiriaceae relative to other Mal- pighiales is not clear yet (Bove 1997; Wurdack and Davis Material and Methods 2009). An early to middle Cretaceous origin has been inferred from molecular divergence estimates (Davis et al. 2005). The We examined collections from the U.S. National Herbarium oldest fossil record of Humiriaceae, however, dates back to (US) at the Smithsonian Institution in Washington, DC; the the Eocene (Berry 1924a, 1929a; this study). The fossil record Smithsonian Tropical Research Institute (STRI) in Panama; of the family has been recognized on the basis of pollen, the University of Florida Herbarium (FLAS) in Gainesville, wood, and endocarps (Berry 1922a; Lorente 1986; Hoog- Florida; the Missouri Botanical Garden Herbarium (MO); the U.S. National Arboretum Herbarium (BARC); the Natural 1 Author for correspondence; e-mail: fherrera@flmnh.ufl.edu. History Museum, London; and the Universidad Nacional Manuscript received August 2009; revised manuscript received January 2010. (UN) in Bogota´, Colombia. Approximately 100 specimens of

392 HERRERA ET AL.—PHYLOGENY OF THE HUMIRIACEAE 393

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 ferring to specimens deposited at the National Museum of in the online edition of the International Journal of Plant Sci- Natural History (USNM) in Washington, DC; the Florida ences). Transverse and longitudinal sections were cut through Museum of Natural History (UF) in Gainesville, Florida; the the center of the fruits or endocarps. The characters inspected University of Amsterdam (UA); and the Philipps-University are summarized in table 1. Marburg (UMBG), Germany. Newly recovered specimens of A new matrix, modified and expanded from that of Bove Sacoglottis tertiaria from Panama were deposited at STRI. (1997), was prepared for the phylogenetic analysis (fig. 3). Morphological data on extant Humiria pollen were ob- The character descriptions and scoring criteria are available tained from the extensive study of pollen morphology of Hu- in appendix B in the online edition of the International Jour- miriaceae by Bove and Melhem (2000) and the observation nal of Plant Sciences and online at the MorphoBank Web site of two species from the Graham Pollen Collection hosted at (http://www.morphobank.org; project P277, Matrix of Mor- STRI (Humiria balsamifera, slide 17520, Costa Rica, and phological Characters of Humiriaceae). Cladistic analyses Humiria guianensis, slides 5723 and 3011, Brazil). We used were performed using PAUP*, version 4.0 (Swofford 2003), a Nikon I80 camera with Nomarsky microscopy and a Nikon and the examination of character state distributions was com- DXM 1200 camera for the pollen observations. pleted using Mesquite, version 2.6 (Maddison and Maddison The newly recovered fossil endocarps reported in this study 2009). Our analysis was rooted with four outgroups, including (fig. 5) were collected from the Gaillard Cut section (Lirio the three used by Bove (1997), plus Caryocaraceae, in accor- East outcrop) of the southeastern part of the Panama Canal dance with the most recent phylogeny of the Malpighiales (lat. 9°3920N, long. 79°399400W). The fossils were found in (Wurdack and Davis 2009). To avoid assumptions regarding March of 2007 while exploring new temporary exposures cre- character state transitions, the 40 characters were treated as ated during the expansion of the canal. The plant locality is unordered. An exhaustive search with multistate taxa was car- placed in the lowermost part of the Cucaracha Formation. ried out. Morphological characters were evaluated through Lithofacies, sedimentary structures, fossils, and ichnofossils a review of Bove (1997), Bove and Melhem (2000), and refer- suggest that the ;100–140-m-thick Cucaracha Formation ences therein (e.g., Cuatrecasas 1961; Narayana and Rao was deposited in a succession grading from nearshore shallow 1977) and through direct observation of the fruits. Characters marine environments at the base to terrestrial facies in upper were coded as polymorphic when more than one state was levels. Kirby et al. (2008) reconstructed the formation as present, and characters not applicable for a taxon or simply a coastal delta plain consisting of abundant paleosols, chan- not known were coded as missing. Support levels for tree nel, levee, floodplain, marsh, and volcanic deposits. The Cu- nodes were assessed with the bootstrap procedure provided in caracha Formation overlies the Culebra Formation, also PAUP*, version 4.0, using a branch-and-bound search and exposed in the canal, which includes a distinct marine succes- 10,000 bootstrap replicates. sion ranging from neritic environments at the base (coral reef, Eleven of 16 fossil endocarp taxa previously assigned to costal lagoon) to delta and prodelta fronts at the top (Wood- Humiriaceae were physically reexamined (table 2; fig. 4), re- ring and Thompson 1949; Kirby et al. 2008; Moro´ n et al. 394 INTERNATIONAL JOURNAL OF PLANT SCIENCES

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 son and Kirby 2006; MacFadden 2006; Kirby et al. 2008). mammals, pollen, marine invertebrates, magnetostratigraphy, These sources indicate an age of ;19.5–14 Ma for the Cucar- and radiometric dating (Bold 1973; Woodring 1982 [1957]; acha Formation and 23–19 Ma for the underlying Culebra Graham 1988a, 1988b; MacFadden and Higgins 2004; John- Formation (Kirby et al. 2008). These data suggest a late Early HERRERA ET AL.—PHYLOGENY OF THE HUMIRIACEAE 395

Miocene age (19.5–17 Ma) for the Humiriaceae fossil at the e.g., in Humiria; fig. 2R) to very thick (;8–14 mm, e.g., in Lirio East site. Schistostemon and Sacoglottis; fig. 2L–2O). The thickest me- socarps are found in Endopleura (fig. 2U) and Hylocarpa, where the extra mesocarpic tissue growth corresponds to Results pronounced furrows between the sharp ribs of the endocarp. When the mesocarp contains cavities, it becomes more fi- Fruit Morphology and Habitats of Extant Humiriaceae brous, as in Sacoglottis (table 1; fig. 2L–2N). Neither the The Humiriaceae is characterized by epitropous ovules (one exocarp nor the mesocarp has been reported from any fossil or two); free and thick petals; stamens united at the base in specimen related to Humiriaceae because these soft tissues one to several whorls; thick, fleshy anthers with elongated are easily degraded or decomposed before fossilization. How- connectives; a free disk; and a syncarpous superior ovary of ever, thickness of the mesocarp could be especially helpful three to 10 carpels. The leaves are alternate, simple, and for discriminating fossil species if they are found in the fu- mostly entire margined and coriaceous, and the xylem vessels ture. We found the thickness of the mesocarp to be consistent include scalariform perforation plates (Aublet 1775; Jussieu at the species level; for example, two specimens of Sacoglot- 1829; Urban 1877; Cuatrecasas 1961; Gentry 1975). The dis- tis trychogina collected from distant parts of Amazonia (fig. tinctive drupaceous fruit develops a combination of diagnostic 2N) showed equivalent mesocarp thickness. characters, mainly in the endocarp, that can facilitate identifi- Endocarp shape. The endocarp shape, like overall fruit cation (Cuatrecasas 1961). The endocarps are woody, with shape, is variable at and species levels, as illustrated by a central vascular axis, three to 10 carpels, and one or two Cuatrecasas (1961, p. 94; table 1). Endocarp shape fluctuates seeds per locule. Each carpel is supplied with a germination from oblong, ovoid, or obovate to elliptic or globose, and it valve. The endocarps of some genera also have apical foram- may or may not have an acuminate apex (fig. 2A–2K). We ina. Several genera also have cavities in the wall that have found no preferential shape in any genus of Humiriaceae. been referred to in the literature as resin or oil cavities (Cua- Hence, endocarp shape is of limited value in distinguishing trecasas 1961). fossil species in this family. Among Malpighiales, we do not recognize any other fami- Endocarp surface and structure. The surface and struc- lies with fruits having the same set of characters seen in Hu- ture of the endocarp provide useful characters for the identi- miriaceae. Fruits of the Caryocaraceae are slightly similar, fication of genera and species within Humiriaceae (table 1). with a woody and spinulose/corrugated endocarp, but they A smooth endocarp is the most common type, as in Vantanea lack germination valves, endocarp wall cavities, and foram- (fig. 2G–2I), Humiria, Endopleura, and Humiriastrum (fig. ina, and the seeds are reniform rather than ellipsoidal to 2E). The second type of surface is corrugated, which includes oblong (Prance and Freitas 1973). Here, we present a brainlike surfaces in Vantanea (fig. 2J) and strongly folded or morphological review of the fruit characters for all genera of furrowed surfaces, as in Duckesia (fig. 2P) and some species Humiriaceae: Vantanea, Humiria, Duckesia, Hylocarpa, En- of Humiriastrum (fig. 2F). The monotypic genus Hylocarpa dopleura, Humiriastrum, Sacoglottis, and Schistostemon (ta- has an intermediate, slightly corrugated surface (fig. 2K). Sa- ble 1). coglottis and Schistostemon have bullate or inflated surfaces Drupe size and shape. Among the genera, fruit size varies as a result of the bulges of big cavities in the endocarp (fig. greatly (1.6 to ;10 cm in maximum length; table 1). The lon- 2A–2D). All endocarps in Humiriaceae are woody, although gest drupes occur in Vantanea and Hylocarpa (fig. 2J,2K) and in genera with cavities they tend to be spongy. The endocarp the smallest in Humiria (1.6 cm in length; fig. 2R). Because of Hylocarpa has five external sharp ribs, corresponding to some species of Vantanea and Humiria are very similar in fruit the septa (fig. 2K). Endopleura has perhaps the most striking morphology, size is useful for distinguishing them. The small endocarp, where each of the five septa bifurcates, giving drupes of Humiria seem to be related to dispersal by bats and a 10-radiate shape seen in cross section (fig. 2U). Despite the birds (Cuatrecasas 1961; Macedo and Prance 1978; Ridgely systematic utility of the surface and structure of the endo- et al. 2005). In general, the length of a drupe within an indi- carps in the family, in some cases it will be necessary to use vidual species and even within a genus does not vary more other characters to distinguish genera, as in the case of the than a couple of centimeters. However, we caution that the smooth endocarps of Vantanea and Humiria and the corru- size of the drupe should be used only in combination with gated endocarps of Duckesia and Humiriastrum. other characters for identification of fossil species. Germination valve morphology. The number of valves is The shape of the drupe is variable within genera of Humir- equal to the number of septa. Usually five valves occur, except iaceae and by itself is not a good character for identification in Vantanea and Humiria, where the number may increase to of fossil endocarps (fig. 2). Even within a single species, fruits eight or 10 (fig. 2R,2S); in some very rare cases, we counted vary from ovoid or oblong to elliptic or globose (table 1). three or four valves in Humiriastrum and Sacoglottis. The Cuatrecasas (1961), however, used this character for recogni- shape and length of the valves vary mostly at the generic level. tion of varieties. In Vantanea and Humiria, the valves are short to long and Exocarp and mesocarp. The exocarp is usually thin narrow and oblong (sometimes lingulate or tongue shaped; (<1 mm), with a surface that can be smooth, carnose, gla- fig. 2H–2J); sometimes the valves in Humiria are reniform in brous, or fibrous (table 1). These states are present in almost shape, as an expression of the two superposed seeds inside the all genera; therefore, this character is not diagnostic beyond same locule (fig. 3). In Endopleura, the valves are short, and the family level. However, the mesocarp thickness is system- in Hylocarpa, they are long (fig. 2K), but in both genera, the atically useful. The mesocarp varies from very thin (<1 mm, valves are located at the bottom of the furrow or between the Table 1 Flower and Fruit Characters of Humiriaceae Character Vantanea Duckesia Endopleura Hylocarpa Humiria Humiriastrum Schistostemon Sacoglottis Flower: Stamen no. 50–180 20, 25 20, 30 30 20 20 20 10 Anthers, thecae Bilocular, 2 Unilocular, 4 Unilocular, 4 Unilocular, 2 Unilocular, 2 Unilocular, 2 Unilocular, 2 Unilocular, 2 Ovules per locule 2 1 1 1 2 1 1 1 Drupe: Shape Variable: ovoid, Ovoid Elliptic Elliptic Variable: ovoid, Variable: ovoid, Variable: ovoid, Variable: ovoid, oblong, elliptic globose oblong, globose oblong, globose oblong, globose oblong, elliptic elliptic elliptic elliptic Maximum length (cm) ;10 ;7 ;7 ;10 ;1.6 ;5 ;5 ;6 Exocarp: Texture Carnose, Smooth, Smooth, fibrous, Smooth, Smooth, carnose, Carnose, smooth Carnose, Carnose, coriaceous coriaceous coriaceous noncoriaceous glabrous coriaceous coriaceous, coriaceous, 396 glabrous, glabrous, fibrous fibrous Thickness (mm) <1 ;.5 ;.6 <1 <.1 <.2 <.1 <.1 Mesocarp: Thickness (mm) 1–5 ;6 3–14 3–10 <1 2–5 .5–10 .5–8 Fabric Granulose to Granulose Granulose and Granulose Fibrous, fleshy Granulose to Granulose to Granulose to nongranulose fibrous (two nongranulose, nongranulose, nongranulose, layers) fibrous fibrous fibrous Endocarp: Shape Variable: oblong Ovoid with acute Elliptic Elliptic, acute Variable: ovoid, Variable: ovoid, Variable: ovoid, Variable: ovoid, elliptic, acute apex apex and globose oblong, globose oblong, globose oblong, globose oblong, apex common truncate base elliptic elliptic elliptic elliptic Surface Smooth, strongly Strongly Smooth Slightly corrugated Smooth Smooth, Bullate (inflated) Bullate (inflated) corrugated, corrugated corrugated brainlike Structure Densely woody Spongy-lignose to Densely woody, Densely woody, Densely woody Woody to densely Woody to spongy, Woody to spongy, woody sharp ribs five sharp ribs woody inconspicuously inconspicuously divided into furrowed furrowed two, giving a 10-radiate- shaped section Septa narrowing outward (seen in cross section) No No No No No No/yes Yes Yes; some species show a bulb at the edge of the septa Germination valve no. 5–8 5 5 5 5–10 4–5 5 3–5 Valve shape Short to long- Long-oblong Short, located Long and elliptic Narrow, oblong Oblong and short Long, elliptic, and Long, elliptic, and oblong (lingulate), between the ribs at the bottom of (lingulate), broad broad (lingulate), narrow at the bottom of the furrow bean-shaped narrow furrowed the furrow Valve from apex to base No No No No Yes/no No Yes Yes Valve conspicuous Yes, sometimes Yes No Moderately Yes No to moderately No No with a midfurrow Relative rib- valve width ;Equal or valves ;Equal or valves Valves narrower Valves narrower ;Equal or valves ;Equal or valves Valves wider Valves wider narrower narrower narrower narrower or Foramina: wider Number Absent 5 5 Absent 5 5 Absent Absent 397 Seed: No. fertile seeds Usually 1, 2–3 rare 2 Usually 1–3, 5 rare Usually 1–2, 5 rare 1–4 1–5 Usually 1–3 Usually 1–3 No. per locule 1 1 1 1 2 superposed 1 1 1 No. seminal cavities Up to 6 Up to 4 Up to 5 Up to 5 Up to 10 (all sizes) Up to 9 (all sizes) Up to 4 Up to 5 Seminal cavity shape (seen in cross section) Pentagonal (very Elliptic, ovoid Elliptic Elliptic, ovoid Very variable Elliptic, ovoid, Elliptic, ovoid, Elliptic, ovoid, angular), ovoid circular circular circular

Cavities: Present/absent Absent Present Absent Absent Absent Absent to Present Present moderately Size (mm) .1–.7 .05–.6 .4–4.2 .3–7 Habitat Lowland rain Amazonia rain Amazonia rain Amazonia rain Rain forests to Lowland rain Amazonia rain Lowland to forest (mostly) forest forest forest forested forests forest mountain rain to border of savannas forests savanna Altitude >500 m ;800 ;2300 ;1200–1400 ;800 ;1200 Note. Transverse and longitudinal sections were taken at the center of the fruits or endocarps. 398 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 3 Cladistic analysis of Humiriaceae using 40 morphological characters; one of the two most parsimonious trees obtained by using PAUP*, version 4.0; in both results, the topology did not change among Humiriaceae. Outgroups include Erythroxylaceae, Caryocaraceae, Linaceae, and Ixonanthaceae; eight genera compose Humiriaceae. The cladogram has a consistency index of 0.79 and a retention index of 0.60; several nodes occurred 70% of the time in 10,000 bootstrap replicates for Vantanea, 58% for the remaining seven genera, and 71% for the node Sacoglottis þ Schistostemon. Synapomorphies, autapomorphies, and homoplastic characters (in italics) were placed in the cladogram. Several of the morphological evolutionary trends proposed for Humiriaceae are in bold colors. The complete sequence of characters and states of the matrix are listed in appendix B in the online edition of the International Journal of Plant Sciences and also online at the MorphoBank Web site (http:// www.morphobank.org; project P277, Matrix of Morphological Characters of Humiriaceae). Endocarp drawings modified from Cuatrecasas (1961); seed locules ¼ black, and seeds and cavities ¼ white.

sharp septa. The valves are long in Duckesia, but in Humirias- fig. 2H), Humiria, and Duckesia. The valves are moderately trum they are short and located at the top of the endocarp developed in Humiriastrum but very inconspicuous in Endo- (fig. 2E,2F), although both have corrugated endocarps. Saco- pleura, Sacoglottis, and Schistostemon. glottis and Schistostemon have indistinguishable valves that Foramina. A set of five apical holes or foramina occurs in are unique for the family (fig. 2A–2D); they are long (reaching four genera: Duckesia, Endopleura, Humiria, and Humirias- the apex and the base of the endocarp), elliptic, and consider- trum (table 1; figs. 2E,2F, 3). This is a good character for ably wider than other valves in the family. This correlates the recognition of modern or fossil genera. Some species of with an extreme reduction of the thickness of the septa, as Vantanea and Humiria develop very similar endocarps with seen in cross section (fig. 2L–2O). The expression of the smooth surfaces, yet the presence of foramina in the latter ge- valves at the surface is also variable. The most conspicuous nus can be used to distinguish the two. Although the pres- valves are seen in Vantanea (sometimes with a middle furrow; ence or absence of foramina is useful in distinguishing Table 2 Fossil Fruits of Humiriaceae Vantanea Vantanea Vantanea Humiria Humiriastrum Humiriastrum Sacoglottis Sacoglottis Sacoglottis Sacoglottis Sacoglottis Sacoglottis Sacoglottis Sacoglottis Fossil speciesa cipaconensis cipaconensis cipaconensis bahiensis sp. sp. tertiaria tertiaria tertiaria tertiaria tertiaria tertiaria tertiaria tertiaria

Source Berry 1924a, Berry 1927, Wijninga Selling 1945 Wijninga and Wijninga Berry 1922a, Berry 1924b Reid 1933 Wijninga and Wijninga Wijninga Lott et al., This article 1929d 1929a; 1996a Kuhry 1990 1996a 1922b Kuhry 1990 1996a 1996b forthcoming Selling 1945 (T294) (T197) (T295) (T196) (T296) (T377) Age ? Eocene Middle–late Miocene? Early Pliocene Middle–late Pliocene? ? ? Early Pliocene Middle–late Late Miocene Pleistocene Early-Middle Miocene Pliocene? Miocene Miocene Early Miocene Pliocene Location Colombia, Peru, Belen Colombia, Brazil, state Colombia, Colombia, Bolivia, Colombia, Colombia Colombia, Colombia, Colombia, Costa Rica Panama Canal High Plain Punta High Plain of Bahia High Plain High Plain Pisllypampa High Plain High Plain High Plain High Plain Zone Bogota´ Parin˜ as Bogota´ S. T. Bogota´ Bogota´ S. T. Bogota´ Bogota´ Bogota´ Bogota´,Rı´o Zipaco´ n I–II Subachoque I–II Zipaco´ n Subachoque S. T. I–II Frio Endocarp: Max. length (cm) ;2.4 3.35 3.3 1.4 2.7 2.1 2.2 3 ;3 ;2.8 4 3.8 3.2 ;2.4 Shape Elliptic Elliptic, ovoid Elliptic, ovoid, Ovoid Elliptic Elliptic, ovoid, Elliptic, Elliptic Ovoid Elliptic Elliptic, ovoid, Elliptic, ovoid Elliptic Elliptic globose, globose globose globose obovate Surface Smooth Smooth Glabrous Smooth Corrugated Corrugated Slightly Bullate Bullate? Bullate Bullate Bullate Bullate Bullate? bullate (eroded) Structure Woody Woody Woody Woody Woody Woody Woody Woody Woody Woody Woody Woody Woody Woody Septa narrowing ? No No No ? ? ? ? ? ? Yes ? ? Yes No. valves 5–8 5–6 5–7 5 5 5 5 5 5 5 5 5 5 5 Valve shape Long, Long, Long, oblong Long, Long, narrow Long, narrow Elliptic Elliptic Elliptic Elliptic Elliptic Elliptic Elliptic Elliptic? lingulate lingulate lingulate lingulate to short to short elliptic, elliptic, furrowed furrowed Valve from apex to base No No No No No No Yes Yes Yes Yes Yes Yes Yes ? Valve at surface conspicuous Yes, with Yes, without Yes, with Yes, without Yes Yes No No No No No No No ? midfurrow midfurrow midfurrow midfurrow? Relative rib- valve width ;Equal or ;Equal or ;Equal or Valves Valves Valves Valves Valves Valves Valves Valves Valves Valves ? valves valves valves narrower narrower narrower wider wider wider wider wider wider wider narrower narrower narrower Apical foramina Absent Absent Absent Absent 5 5 Absent Absent Absent Absent Absent Absent Absent Absent No. fertile seeds 1? ? 0–3 2, superposed ? ? ? ? ? ? 1 ? ? 2? Seminal cavities per endocarp Up to 3? Up to 6 Up to 3 1 ? ? ? ? ? ? 1? ? ? 2 Seed shape, cross section ;Pentagonal, ;Pentagonal, ;Pentagonal Ovoid ? ? ? ? ? ? Ovoid ? ? Ovoid ovoid ovoid Cavities, size (cm) No No No No Present? ? Present, .1–2 Present, .1–3 Present, 1–2 Present, 1–3 Present, Present, 2–4 Present, .5–2 Present, .4–2 <1–2.5 Paleohabitat ? Costal rain Tropical ? Tropical Tropical Subandean, Tropical Tropical Subandean Lowland rain Lowland rain forest lowland lowland lowland warm ? ? lowland lowland warm forest forest Paleoaltitude (m) ? ? Up to 1200 ? Up to 1000 Up to 1200 ? ? ? Up to 1000 Up to 1200 Up to 1000 ;Sea level 1000? a Species names are based on the present revision. Original published names may differ and are presented in the synonymy herein. 400 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 4 Fossil endocarps belonging to or rejected from Humiriaceae. A, Sacoglottis tertiaria Berry emend. Herrera (USNM 320660), Pliocene of Bolivia. B, Sacoglottis tertiaria Berry emend. Herrera (USNM 320710), Zipaco´ n (Colombia), previously classified as Vantanea; note the characteristic cavities as seen in living Sacoglottis. C, Vantanea cipaconensis (Berry) comb. nov. Herrera (USNM 320720), Zipaco´ n (Colombia), previously classified as Sacoglottis. D, Vantanea cipaconensis Berry comb. nov. Herrera, Eocene of Peru. Left specimen (USNM 318013) shows outlines of germination valves, and right specimen (USNM 318020) is a thin section of an endocarp (Berry 1927) showing a vascular strand at the center of the axis, five locules, and probably five valves, although only two are preserved in the upper part of the section. The fossil was originally attributed to Sacoglottis. E, Incertae sedis (USNM 316829); after reexamination, this specimen from Ecuador is rejected from Humiriaceae. F, Incertae sedis (USNM 317919); after reexamination, this specimen from Peru is rejected from Humiriaceae.

genera, we found high variation in the morphology of the fo- in buoyancy, were observed in Sacoglottis, Schistostemon, ramina at the genus and species levels, indicating that this Duckesia, and occasionally Humiriastrum (table 1). In Ducke- character should not be used to discriminate fossil species. sia and Humiriastrum (fig. 2P,2Q), the cavities are small, Seed morphology. Morphology of the seed—a double 0.1–0.7 mm in diameter, whereas in Sacoglottis and Schisto- testa, a straight or slightly curved embryo, with oblong or stemon (fig. 2A–2D,2L–2O), they are usually much larger, ovate cotyledons, and a fleshy and oily endosperm—is very 0.3–7 mm in diameter. The density and distribution of these constant within the family (Cuatrecasas 1961). We searched cavities can be useful to distinguish living or fossil species. For for additional distinguishing features of the testa using SEM example, in Sacoglottis cydonioides the cavities are consis- but did not find any significant differences among the mod- tently concentrated in the inner part of the endocarp, whereas ern genera studied. The oblong to elliptic seed shape corre- in Sacoglottis trichogyna there are fewer cavities and they are sponds to that of the surrounding seminal cavity. In cross mainly confined to the border of the endocarp (fig. 2N). Al- section, the shapes of the seminal cavity and the seed are though the cavities are sometimes observed to be empty, con- highly variable (fig. 2L–2U), from elliptic to ovoid to circu- tents are commonly observed; these have been reported as oil lar; only in Vantanea we do see an unequal pentagon (fig. and resin (Cuatrecasas 1961), but we are not aware of any 2T). The number of seminal cavities is commonly four to six. chemical investigations to verify their composition. However, in Humiria and Humiriastrum we found up to 10 Habitat. All genera are tropical and have species in low- seminal cavities of different sizes, mostly without seeds (figs. land to montane rain forests (table 1). Some species of Vanta- 2Q,2R, 3). The number of fertile seeds also varies from one nea and Humiria are also found on the border between rain to five. Humiria, with two seeds per locule, is readily differ- forests and forested savannas, mainly in the Guianas and Ven- entiated from the rest of the genera, which have single-seeded ezuela (fig. 1). In these countries, Humiria is found up to locules (Cuatrecasas 1961). ;2300 m in high-altitude savannas of the Tepuyes. Other Endocarp wall cavities. Although not present in all gen- genera such as Vantanea, Humiriastrum, Sacoglottis,andSchis- era, cavities within the endocarp wall are one of the charac- tostemon are found in montane rain forests up to ;1400 m. teristic features for the family. Such cavities, which aid Judging from these modern habitats of Humiriaceae, fossil en- Fig. 5 New occurrence of Sacoglottis tertiaria Berry emend. Herrera from the Miocene Cucaracha Formation from Panama. A–D, Specimen FH5964. A and B show endocarps before sectioning; the arrow points out cavities. C, Cross section of the endocarp; upper arrow shows seminal cavity space; lower arrow shows a seed. D, Seed or seminal cavity filling that breaks off from the endocarp. E–G, Specimen FH5965. E, Endocarp showing cavities. F, Endocarp wall adhered to the rock. G, Cross section of the endocarp; arrow points out a seminal cavity filled with calcite. H, I, Specimen FH5966. H, Elliptic endocarp still immersed in the rock; the arrow indicates the unique locule. I, Section of the endocarp showing cavities and a seminal cavity filled with calcite. J, Specimen FH5967; endocarp showing sediment that filled the exterior cavities of the wall. 402 INTERNATIONAL JOURNAL OF PLANT SCIENCES docarps may be indicators of tropical rain forests in the paleo- provided some ideas about the sister families to Humiriaceae botanical record. However, this assumes that the fossil species and generic relationships but did not include important char- had ecological requirements similar to those of the living acters of the flowers and the endocarps, and the results were counterparts. Because of the altitude where some genera grow presented without indicating statistical support values of the today and the buoyant properties seen in some fruits, it is pos- tree. The cladogram by Bove (1997) gave support to Cuatre- sible that the endocarps are transported downstream to lower casas’s (1961) hypothesis of Vantanea as the most ancestral elevations and even to the ocean, where they may be carried genus, followed by Humiria; among the rest of the genera, great distances by sea currents (Gunn and Dennis 1976). the relationships do not coincide clearly with the trends pro- posed by Cuatrecasas. Using PAUP* with Bove’s (1997) unmodified published Phylogenetic Analysis matrix, we tried to replicate her cladogram, but we were un- After our reexamination of morphology, the only genera able to reproduce her result. We obtained four (rather than that are indistinguishable by their fruits are Sacoglottis and one) most parsimonious trees, whose consensus gave poor Schistostemon. Cuatrecasas (1961) elevated Schistostemon to resolution. Our new analysis (fig. 3) yielded two most parsi- the generic level; originally, it was treated as a subgenus of monious cladograms differing only in relationships between Sacoglottis (Urban 1877). The main differences occur in the two of the outgroup families, Caryocaraceae and Linaceae. flowers; Sacoglottis has 10 undivided stamens, whereas Schis- The resulting cladogram has a tree length of 109 steps, a con- tostemon contains 20 stamens, five of them episepalous, lon- sistency index of 0.79 (0.68 excluding autapomorphies), a re- ger, and trifurcate at the apex (triantheriferous). The striking tention index of 0.60, 27 parsimony-informative characters, similarity of their endocarps causes us to question again and 13 parsimony-uninformative characters. This topology is whether the characters of Schistostemon are sufficient to sep- three steps more parsimonious than that presented by Bove arate it at the generic level from Sacoglottis. (1997), 58 steps versus 61 steps in MacClade, version 4.08. Cuatrecasas (1961) regarded Vantanea as the most ancestral Our analysis of 40 morphologic characters for four poten- genus of the family and Sacoglottis as the most derived. From tial outgroups and the eight genera yielded a well-constrained the extreme characters observed in these two genera, he pro- hypothesis of relationships for Humiriaceae (fig. 3). The ge- posed several trends of evolution within the family. The first nus Vantanea is placed as sister to all genera (bootstrap ¼ hypothesized trend is the reduction of stamens (table 1), from 70%), followed by Humiria and the remaining genera (boot- Vantanea having an indefinite number of stamens (50–180) in strap ¼ 58%). several whorls (three or four) to Sacoglottis having 10 stamens The new hypothesis of relationships for Humiriaceae (fig. in a single whorl; the rest of the genera oscillate between 20 3) allows us to discuss the evolutionary trends proposed by and 30 stamens in either one or two whorls. Other trends oc- Cuatrecasas (1961). (a) The number of whorls and their sta- cur in the anther sacs from bilocular to unilocular and in the mens do not follow a linear pattern of reduction. The three thecae from four to two (table 1). Cuatrecasas also proposed or four whorls seen in Vantanea appear as an autapomorphy, several trends of morphological evolution in the ovary and the and there is an equivocal reconstruction of the two whorls endocarps (table 1). Vantanea and Humiria have two ovules for Duckesia and Hylocarpa. A reduction in stamen num- per locule, whereas the other genera hold one ovule. Endocarp bers, from >50 in Vantanea to 20 in Humiria and descen- surface ranges from smooth in Vantanea and Humiria to dants, may be inferred but with the appearance of new sharply ribbed and corrugated in Hylocarpa and Endopleura. synapomorphies in Duckesia (20 or 25 stamens) and Hylo- The germination valves show disjunctive patterns: a reduction carpa (30) and autapomorphies in Endopleura (20 or 30) of length but accompanied by the appearance of apical foram- and Sacoglottis (10). (b) Our topology supports Cuatrecasas’s ina (Humiria, Humiriastrum, and Endopleura) and an in- suggestion that bilocular anthers are ancestral and the uniloc- crease of the length and width of the valves (extreme ular ones are derived. (c) The reduction in ovule number reduction of the thickness of the septa), accompanied by the from two per locule (Vantanea and Humiria) to one per loc- appearance of cavities (Sacoglottis and Schistostemon). ule (remaining genera) is upheld here. (d) The transition On the basis of these hypothesized evolutionary trends, from smooth endocarp, as in Vantanea, to corrugated, as in Cuatrecasas (1961) deduced relationships and formed a classi- Duckesia and Hylocarpa, and to bullate, in a more derived fication for the Humiriaceae. Vantanea was included as the node with Sacoglottis and Schistostemon, is supported. (e) only genus in the tribe Vantaneoideae. The remaining seven Our cladogram does not support a single origin of sharp en- genera compose the tribe Humirioideae; within this tribe, docarp ribs; this character occurs independently in both Hy- Humiria remains the closest genus to Vantanea. The mono- locarpa and Endopleura.(f) A reduction of valve length typic genera Duckesia, Hylocarpa, and Endopleura were occurs in the Endopleura/Humiriastrum clade, and there is considered to be more advanced than Vantanea and Humiria a widening of the valves together with the presence of cavi- on account of anthers and the endocarp morphology. Humir- ties in the derived clade Sacoglottis/Schistostemon (fig. 3). (g) iastrum displays an intermediate condition between the Cuatrecasas also indicated that the presence of foramina was proposed ancestral genera and the most derived ones, Schis- coupled with reduction of valve size. However, in our results tostemon and Sacoglottis. these characters seem to have evolved independently. In addi- In another effort to understand the phylogenetic relation- tion, our analysis indicates a derived clade, Endopleura/ ships among Humiriaceae, Bove (1997) used a cladistic Humiriastrum þ Sacoglottis/Schistostemon, which is well sup- method with Hennig86 and a matrix of 24 characters, which ported by having five traces in carpels and the inconspicuous produced a single most parsimonious cladogram. The study germination valves. In conclusion, the addition of new char- HERRERA ET AL.—PHYLOGENY OF THE HUMIRIACEAE 403 acters in our cladistic analysis strongly supports some of the to 4 mm in diameter. One seed per locule. Seminal cavities evolutionary trends anticipated by Cuatrecasas (1961) but up to two per fruit and shape seen in cross section ovoid. Fo- also suggests that other trends are more complicated than ramina absent. Vascular strand at the central axis of the en- previously thought. It is also possible that as a result of docarp, sometimes difficult to distinguish from cavities in extinction or unidentified genera among Humiriaceae, our cross section. topology does not reflect the complete history of the family. New occurrence. Location: Panama; Lirio East (North) out- Several synapomorphies, all of them related to the endo- crop of the Panama Canal (lat. 9°3920N, long. 79°399400W). carps, support the sister position of Sacoglottis and Schisto- Age and formation: late Early Miocene, ;19.5–17 Ma; base of stemon (fig. 3): bullate endocarps, valves extending from the Cucaracha Formation. apex to base and wider than the septa, and cavities up to 7 Cited specimens. FH5964, FH5965, FH5966, FH5967, mm in diameter. Cuatrecasas (1961) elevated the subgenus FH5968, hosted at STRI (fig. 5). Schistostemon from Sacoglottis because of the difference in Description. Endocarps range from 24.2 to 15.7 mm in the number of stamens (character 4 in the matrix) and the length and from 15.4 to 12.2 mm in width. Endocarp shape presence of trifurcate stamens (character 7). However, the elliptic (fig. 5H), but in most of the specimens, the original number of stamens is not always constant for other genera, shape has been lost as a result of taphonomic processes or dis- e.g., Vantanea, Duckesia, and Endopleura. Another autapo- integration after recovering the fossils from the sediment. morphic state for Sacoglottis is related to the number of Septa five, very thin, and narrowing outward (fig. 5C,5G). valves (character 21); however, we found that three valves Foramina absent; we made several sections of the endocarps are very rare instead of the five prevalent for the node in search of foramina at the base and apex without finding Sacoglottis/Schistostemon. We did not find any additional any evidence of them. The shape, length, and prominence of characters to separate these as genera. In view of their the valves are not evident. Number of fertile seeds and seminal indistinguishable endocarps (fig. 2), we consider that Schisto- cavities one or two; figure 5C is a cross section of the endocarp stemon should be reduced to a subgenus of Sacoglottis. One showing a seed with several layers that may represent portions of the arguments for this suggestion is also based on the of the seed coat. A second seed broke off during sectioning (fig. strength of the endocarp characters in our cladistic analysis 5D), although it is possible that this seed represents a seminal to differentiate all of the remaining genera. cavity instead filled with calcium carbonate, as in figure 5G and 5I. One seed per locule (fig. 5C,5H). The seeds and/or seminal cavities are 3.5 mm wide and range from 17.5 to 9.5 Fossil Record of Humiriaceae mm in length. Seminal cavity shape ovoid in cross section. Cav- ities abundant, ranging from 0.4 to 2 mm in diameter. Fossil endocarps treated before Cuatrecasas’s (1961) mono- Systematic position of S. tertiaria Berry emend. Herrera. graph have not been appropriately revised yet. Here, we After our reexamination of the endocarp morphology (table present a review of the humiriaceous fossil record. 1) and the new cladistic analysis (fig. 3), we suggest that Schistostemon should be subsumed within Sacoglottis and Humiriaceae Juss 1829 treated as a subgenus. The above fossils belong to the Saco- glottis/Schistostemon clade, and under this concept, Berry’s Sacoglottis tertiaria Berry emend. Herrera name, S. tertiaria, remains appropriate. Saccoglottis tertiaria Berry (1922a, 1922b, pp. 129–130, We found no differences to justify the application of multi- pp. 178–180 [basionym; Bolivia, Pliocene]; fig. 4A); Sacco- ple fossil names historically reported. The size and shape of glottis pliocenica Berry (1922a, pl. 8, figs. 5–11 [nomen nu- the fossil endocarps, the five valves or septa, and the diameter dum; Bolivia, Pliocene]); Vantanea colombiana Berry (1924b, of the cavities are approximately constant among all these p. 259; fig. 3 [Zipaco´n, high plain of Bogota´, Colombia; age specimens (table 2). We cannot rule out the possibility that the unknown; cited specimen: USNM 320710]; fig. 4B); Saco- reports of Sacoglottis represent multiple species, taking into glottis costata Reid (1933, pp. 210–212, pl. 14, figs. 1–2 account the differences in age and geographic distribution, [SIC ¼ Saccoglottis; Colombia, specific location unspecified, but, morphologically, all of them are undistinguishable or fall age unknown]); Sacoglottis sp. Wijninga (1996a, p. 144, pl. within the range of variability known to occur within individ- 11, fig. T296 [Salto del Tequendama, high plain of Bogota´, ual extant species. Colombia, Middle-Late Miocene]); Sacoglottis sp. Wijninga The fossil described as Vantanea colombiana (Berry 1924b) (1996b, pp. 348–349, pl. 4, fig. T377 [Rı´o Frio, high plain of from the Zipaco´ n Province in the high plain of Bogota´ (fig. Bogota´, Colombia, Late Miocene–Early Miocene]). 4B) does not resemble Vantanea at all. We transfer this endo- Lectotype hic designatus. USNM 320660 (fig. 4A; from carp to S. tertiaria, as was informally suggested by Wijninga Berry 1922a, 1922b). (1996a). Berry (1924b) recognized the similarity of its cavities Emended diagnosis. Endocarps elliptic, ovoid, to globose, to those of modern Sacoglottis yet assigned the fossil to Vanta- slightly bullate to bullate. Five septa, very thin (narrowing nea, which lacks cavities and has conspicuous valves. Berry outward), seen at the surface as longitudinal lines. Five valves (1924b) suggested the age of the fossil as Oligocene based on (in the original report, Berry [1922a, p. 178] described the the state of preservation and correlations with other localities, valves as seeds: ‘‘the stone has imbedded in it five large but we consider the age to be uncertain. The precise geograph- seeds’’), elliptic in surface shape, wider than septa, inconspic- ical and stratigraphic position of the fossil is unknown. uous and elongate, reaching the apex and base of the endo- Reid (1933) named another fossil endocarp from Colombia carp. Wall and septa containing abundant cavities, from 0.1 as Sacoglottis costata. Although well preserved, the geo- 404 INTERNATIONAL JOURNAL OF PLANT SCIENCES graphic and stratigraphic provenance of the fossil is unknown. ever, judging from the characters of Humiria recognized by The fossil does not present any novel character to distinguish it Cuatrecasas (1961; table 1), it is clear that the fossils were er- as a separate species from S. tertiaria. Although we did not reex- roneously transferred. The fossil endocarps exceed 1.6 cm in amine the specimen directly, it seems that the endocarp has evi- length, lack foramina, and have only one seed per locule. dence of abrasion or erosion, which formed external furrows. The endocarps clearly resemble those of Vantanea instead. Other fossil endocarps from Miocene and Pliocene deposits The Berry (1924a, 1927, 1929d) collection of Vantanea fos- from the high plain of Bogota´ in Colombia were identified as sil endocarps exceeded 100 specimens; however, it has been Sacoglottis sp. (Wijninga 1996a, 1996b). Most of these speci- reduced drastically. Of the original 76 specimens of Vantanea mens could not be relocated for this study (V. M. Wijninga, cipaconensis from Peru, just 40 specimens were accessible for personal communication, 2009), but five specimens from the this study; of 46 specimens of V. cipaconensis from Colombia Salto de Tequendama locality (Wijninga 1996a) were made (Zipaco´ n), only one specimen was observed directly (three available; our reexamination of these specimens corroborates others were analyzed just from photographs; Berry 1929d). their assignment to S. tertiaria. Most of the numerous specimens of Vantanea reported by Distribution. Fossil endocarps of S. tertiaria (table 2; fig. Wijninga (1996a) from Miocene deposits of Colombia (Salto 1) have been reported mostly from Bolivia and Colombia, de Tequendama) have been lost (V. M. Wijninga, personal with two exceptions from Costa Rica and Panama (Lott communication, 2009), but 18 surviving specimens were ana- et al., forthcoming; this study). The oldest fossil confirmed so lyzed. In reviewing all of the fossil endocarps, we did not find far comes from the newly reported Panamanian specimen, sufficient morphological characters to separate them as differ- dated as Early Miocene (19.5–17 Ma). ent fossil species (table 2). Berry (1929d) separated the endo- carps from Colombia and Peru taxonomically, mainly on the basis of the number of valves, but this character is very vari- Vantanea cipaconensis (Berry) comb. nov. Herrera able, even within a single species in modern Vantanea (Cuatre- Saccoglottis cipaconensis Berry (1924a, 1929d, p. 64–65, casas 1961; table 1). The Miocene endocarps reported by p. 6, figs. 20–22, pl. 1; figs. 1–5 [basionym]; S. cipaconensis Wijninga (1996a) also have the same number of valves as the (Berry) Weyland (1938b; p. 161); Humiria peruviana (Berry) specimens from Zipaco´ n and Peru. Endocarp shape is the Selling (1945, pp. 264–265, figs. 13–17 [Zipaco´ n, high plain most variable character seen in the three reports, but again of Bogota´, Colombia, age unknown]; fig. 4C); Saccoglottis this is highly variable within individual extant species. Hence, sp. Berry (1924a, p. 65 [Belen and La Brea, Peru, Eocene]; it seems reasonable to place all reports within V. cipaconensis. fig. 4D); S. cipaconensis Berry (1927, pp. 124–126, pl. 20, figs. The oldest confirmed fossil of Humiriaceae, V. cipaconensis 8–16); S. cipaconensis peruvianus Berry (1929a, pp. 155–157, from the Eocene of Peru, coincides with the most basal genus pl. 1, figs. 14–18); S. cipaconensis peruvianus (Berry) Weyland as proposed by Cuatrecasas (1961) and supported by our (1938b,p.161);H. peruviana (Berry) Selling (1945, pp. 264– phylogenetic analysis (fig. 3). The specimens from Peru are 265, figs. 18–22 [Belen and La Brea, Peru, Eocene]); Vantanea permineralized, with excellent anatomical preservation. A trans- sp. Wijninga (1996a, pp. 143–144, pl. 10, fig. T294 [Salto verse section published by Berry (1929a) illustrates many of del Tequendama, high plain of Bogota´, Colombia, Middle- the characters contributing to our generic determination (fig. Late Miocene]). 4D, right). According to Berry (1929b), the floristic affinity of Lectotype hic designatus. USNM 320720 (fig. 4C). Addi- the whole fossil assemblage indicates that this species grew in tional cited specimens: USNM 318013, USNM 318020 (fig. tropical rain forests. Another endocarp reported by Berry 4D). (1924a) from Zipaco´n in the high plain of Bogota´ (Colombia) Emended diagnosis. Endocarp woody, elliptic, ovoid, ob- was suggested to be from the Guaduas Formation, either Eo- ovate to globose. Surface smooth (not corrugated). Apex of cene or Oligocene in age. Today this formation is recognized endocarp obtuse, rounded to acute. Septa or valve number as Late Cretaceous (Sarmiento 1994). However, according to from five to eight, radially arranged. Septa enlarging outward, the geological map of Colombia (Go´ mez et al. 2006), Zipaco´ n as seen in cross section. Valves conspicuous, having a median and its surrounding area lie on Neogene deposits. Given the furrow on the surface, lingulate to oblong, but never reaching close geographic proximity, it is possible that the fossils re- the top or the base of the endocarp; valves generally narrower ported from Zipaco´ n (Berry 1924a) are correlated in age with than septa, rarely equal in width to the septa. Seeds one per those reported by Wijninga (1996a) from Late Miocene de- locule. Up to six seminal cavities per fruit; pentagonal to posits. Another Colombian fossil reported by Berry (1925) to ovoid as viewed in cross section. Cavities and foramina ab- have been from the Cretaceous, near the eastern border of the sent. Vascular strand at the central axis of the endocarp. Sabana of Bogota´, was later determined by C14 dating to be Comments. Wijninga (1996a) briefly reviewed the fossil only ;300 yr old (Manchester and Kress 1993). So far, the record of Vantanea and suggested appropriate assignments of age of the lectotype of V. cipaconensis remains unknown, and the endocarps without formal reassignments. Here, we present it is unlikely that the locality where the collection was made the corrected systematic descriptions and revised nomencla- can be found on the basis of the limited information provided ture and, finally, discuss the justification for the assignment of by Berry (1924a, 1929d). each fossil to Vantanea. Initially, Berry (1924a, 1927, 1929a, 1929d) described many humiriaceous specimens from Colombia and Peru as Other Humiriaceous Endocarps S. cipaconensis and S. cipaconensis peruvianus. Later, Selling A carbonized endocarp from the state of Bahia, Brazil, of (1945) transferred these two fossil taxa to Humiria. How- Miocene or Pliocene age was assigned by Selling (1945) to HERRERA ET AL.—PHYLOGENY OF THE HUMIRIACEAE 405

Humiria (table 2). Selling based this classification mainly on and Moreno 1991). Alangiaceae (Alangium) has larger pollen what he interpreted as impressions of two seeds in a locule; grains (>50 mm), amb is circular, and columellae are distinct. the size of the endocarp also favors its classification (;14 Caprifoliaceae (Abelia) has larger pollen grains (>60 mm), mm of length). However, as also noted by Cuatrecasas lacks pores, and has a zonosulcus. Clethraceae (Clethra) has (1961, p. 33), the fossil endocarp lacks foramina and has a protruding aperture, and columellae are indistinct. Pyrola- only one seminal cavity, indicating that this fossil greatly re- ceae (Monotropa) is oblate and lacks columellae. Hyppocra- sembles the genus Vantanea as well. We did not have the op- teaeae (Tontelea) is oblate, and pores are lalongate. portunity to examine the specimen directly and cannot settle The fossil record of P. devriesii is widely distributed in the its affinity. If Selling (1945) interpreted the impressions of the Neotropics (Hoorn 1994; app. A). It has been observed since two seeds wrongly, which seems probable, given the frag- the Early Miocene in Panama, Colombia, Venezuela, and mentary nature of the endocarp, the fossil would more likely western Amazonia. belong to Vantanea. Both of these genera have two ovules per locule in the ovary, but only in Humiria are both ovules known to develop into seeds. It is not difficult to infer that Fossils Excluded from Humiriaceae early representatives of Vantanea could also have developed two seeds per locule. Incertae sedis Fossil endocarps related to Humiriastrum have also been re- Rejected. Vantanea sheppardi Berry (1929c; pp. 300–301, ported from Colombia (Wijninga and Kuhry 1990; Wijninga figs. 4–5 [Point sandstone at Ancon Point, Sta Elena Peninsula, 1996a), but unfortunately the specimens have been lost (V. M. Ecuador; Eocene; cited specimen: USNM 316829]; fig. 4E). Wijninga, personal communication, 2009). The authors rec- Berry (1929c) described this species from the Eocene de- ognized the similarity of the corrugated endocarps to those of posits of Ecuador. He correlated the locality in age and floris- extant Duckesia (table 1; fig. 2P). According to their descrip- tic affinity with the Belen localities of Peru. The fossil species tions, the valves are generally short and located above the was discriminated from the others species of Vantanea mainly middle part of the endocarp, in agreement with the morphol- by the shape and size of the specimen. The exterior of the fos- ogy of modern species of Humiriastrum. However, the pub- sil does not show any characters to relate it to Vantanea or lished pictures of the fossils show that the valves seem to even to the Humiriaceae (fig. 4E, top). The specimen lacks extend fully from the apex to the base of the endocarps, in valves, septa, foramina, and cavities. In search of internal conformity with Duckesia. If additional specimens can be lo- characters, we made an equatorial transverse cut (fig. 4E, bot- cated, it would be important to examine cross sections to con- tom), but this also failed to reveal any internal structure, lead- firm the generic placement. ing us to assign this specimen as incertae sedis. Rejected. Vantanea compressiformis Berry (1929a, pp. 157–158, pl. I, figs. 25–26 [Belen and La Brea from Peru; Eo- Pollen of Psilabrevitricolporites devriesii cene; cited specimen: USNM 317919]; fig. 4F). Lorente emend. Silva-Caminha et al. This species was described from Eocene deposits of Peru. Psilabrevitricolporites devriesii (Lorente) Silva-Caminha et al. The main character used by Berry to discriminate it from V. ci- (2010) is a fossil pollen taxon very similar to extant Humiria- paconensis was the size, 4.5 versus 3.35 cm in length (longest type pollen (Bove and Melhem 2000; fig. 6). Fossil pollen of P. endocarp seen in V. cipaconensis). We reexamined the original devriesii was analyzed from five sites (table A2 in the online specimen and found no evidence such as valves, septa, or seeds edition of the International Journal of Plant Sciences) in Co- that would relate this species to Vantanea or even to the Hu- lombia and Brazil. Both P. devriesii and extant Humiria-type miriaceae (fig. 4F). We therefore assign this specimen as incer- pollen are prolate (fig. 6D,6H) and have a radial symmetry, tae sedis. amb circular to triangular-obtuse-convex (fig. 6A–6C,6F, Rejected. Sacoglottis kayseri (Schindehu¨ tte) Kirchheimer 6G), polar area large, and apocolpium index 0.6. The grains (1951, pp. 76–79, figs. 1–2 [Eichelskopfes tuff, Homberg in are tricolporate, with costate colpi; costae slightly developed, lower Hesse, Germany; Miocene; cited specimens: UMBG ;2 mm thick; colpi very short, having straight borders and 3155–3156]). rounded ends; and pores simple, circular, and 3 mm wide (fig. The fruit assigned to S. kayseri (Schindehu¨ tte) Kirchheimer 6D,6E,6H). The exine is tectate, thick (;3 mm), with barely from the Middle Miocene Eichelskopfes Tuff in lower Hesse, distinct columellae, and the sexine and nexine are well defined Germany (Kirchheimer 1951), was considered a valid record and dense (fig. 6A,6F); the surface sculpture is psilate (fig. 6B, of Humiriaceae by Mai (1995). However, our reexamination 6G). In P. devriesii, the polar diameter is ;28–30 mm, and the of the original specimens indicates that their morphology does equatorial diameter is ;25–27 mm, whereas in extant Humi- not correspond to this family. The illustrated fossil is a locule ria, the range of size is larger, from 23 to 45 mm. The humiria- cast of a unilocular, six- to seven-carpellate fruit bearing parie- ceous affinity of P. devriesii was originally proposed by tal scars of numerous seeds. Accompanying the locule casts Lorente (1986) and is reconfirmed here. illustrated by Kirchheimer, the collection also includes the The combination of the following characters is typical of external molds/impressions of the same fruit, indicating a Humiria: medium size (28–30 mm), prolate, and triangular- smooth rather than a punctate outer surface. This species has obtuse-convex amb; tricolporate, with a brevicolpus; costate, been reassigned to an extinct genus of Salicaceae (Manchester with a circular pore; columellae barely distinct; and psilate and Hottenrott 2009). ornamentation. Similar morphology can be found in several Sacoglottis germanica (Sacoglottis smythii [F. Mueller] families but with some differences (Erdtman 1952; Roubik Weyland [1938a, 1938b]) was assigned to Humiriaceae. This 406 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 6 Morphological details of Psilabrevitricolporites devriesii and Humiria. Scale bar ¼ 10 mm. A–E, Psilabrevitricolporites devriesii. A, Slide AM27–31, Amazon, England Finder (EF) X30/4; grain in polar view showing the tectate exine and narrow costae. B, Slide 63, Rio Cobugon ORC-28, Colombia, EF S18/2; grain in polar view showing the psilate ornamentation and triangular-obtuse-convex amb. C, Slide 176, Gibraltar- 1, 2509–2609, Colombia, EF G11/3; grain in polar view showing the brevicolporate aperture. D, Slide 87, Arauca-2, 160709–160809, Colombia, EF V22/2; grain in equatorial view showing the brevicolporate aperture and the prolate outline. E, Slide 889, Tocoragua-1, 14740R, Colombia, EF R40; plain view of a short colpus, slightly costate, and a circular, simple pore. F, Humiria balsamifera, Graham Pollen Collection, slide 5723, Brazil, EF P30/1–2; grain in polar view showing the tectate exine and narrow costae. G, Humiria balsamifera, Graham Pollen Collection, slide 17520, Costa Rica, EF G32/1; grain in polar view showing the psilate ornamentation and triangular-obtuse-convex amb. H, Humiria guianensis, Graham Pollen Collection, slide 3011, EF K32/2–4; grain in equatorial view showing the brevicolporate aperture and the prolate outline. species was initially thought to be from Germany and at- Our morphologic phylogenetic analysis yielded a well- tracted attention because of its paleogeographic implications constrained hypothesis of relationships for Humiriaceae, with for the family. Nevertheless, it was later clarified that the fos- a consistency index of 0.79 and a retention index of 0.60 sil was actually from Australia (Spondylostrobus smythii V. (fig. 3). Vantanea is placed as the most ancestral genus of Mueller; Kirchheimer 1938); it was recently reexamined and the family (bootstrap ¼ 70%), followed by Humiria. The assigned to Anacardiaceae (Dettmann and Clifford 2002). remaining genera form a clade of two pairs, Duckesia þ Hylocarpa, and a larger clade containing Endopleura þ Discussion Humiriastrum and Sacoglottis þ Schistostemon. Our mor- phological analysis of the endocarps and the cladistic hypoth- Reexamination of the fruit characters within Humiriaceae esis corroborated the close relationship between Sacoglottis reinforces the systematic value of the endocarps for the iden- and Schistostemon (bootstrap ¼ 71%) as proposed (Urban tification of living and fossil genera, as suggested earlier by 1877; Cuatrecasas 1961). On the other hand, we did not find Cuatrecasas (1961). Characters commonly preserved in the any additional characters to separate these genera that share fossil record, such as the surface and structure of the endo- indistinguishable endocarps (fig. 2A–2D,2L–2O), leading to carp, the morphology of the germination valves, and the our suggestion that Schistostemon should be reduced to a sub- presence of foramina and cavities, appear to be the most re- genus of Sacoglottis. liable features for the identification of fossil genera (fig. 2; In total, 15 reports of fossil endocarps and pollen are up- table 1). Other characters, such as the thickness of the held as valid for Humiriaceae (table 2; figs. 4–6; app. A): mesocarp and the distribution, size, and abundance of cavi- Vantanea (Eocene and Miocene), Sacoglottis (Early Miocene ties, may emerge as trustworthy for the identification of fossil and Late Pliocene), Humiria (Miocene and Pliocene), Humir- species. Endocarp shape was widely used to discriminate fos- iastrum (Miocene and Early Pliocene). We found no differ- sil species in Humiriaceae, but this character fails to support ences to justify most of the fossil species published in the the distinction of multiple species. We emphasize that the literature. The rejection of former reports of fossil Humiria- naming of new species should be justified if on a combination ceae from Germany and Australia reduces the accepted re- of characters and not on features observed to be highly vari- cord of this family to Central and South America, thus able within extant species (table 1). supporting a Neotropical origin for this family. The only spe- HERRERA ET AL.—PHYLOGENY OF THE HUMIRIACEAE 407 cies of Humiriaceae identified outside the Neotropics is the ex- grant 0824299), and the Paleobiology STRI endowment to tant Sacoglottis gabonensis from West African rain forests (fig. C. Jaramillo; NSF grant EF-0431266 to S. R. Manchester; 1). This species probably was dispersed by ocean currents and a UF 2007 Research Opportunity Grant and NSF grants from the Neotropics (Renner 2004). This study highlights the OISE-0638810, EAR-0642528, and EAR-0824299 to B. importance of reviewing historical reports of Neotropical MacFadden. We thank C. Montes, N. Strong, M. Carvalho, genera before they can be accepted as taxonomically accurate. A. Rincon, and the paleontology team at STRI for help with The living distribution and ecological requirements indicate fieldwork; J. Bloch and J. Chen for help with the cladistic that fossil endocarps of Humiriaceae may offer a clue for the analysis; S. Wing (SI) and V. Wijninga and H. Hooghiem- reconstruction of ancient biomes and paleoclimates. stra (UA) for providing access to the fossil collections; D. Bell (US), C. Galdames (STRI), K. Perkins (FLAS), and F. Acknowledgments Gonzalez (UN) for access to modern Humiriaceae collec- tions; D. Jarzen, T. Lott, and E. Moreno for helpful discus- This research was made possible through the collaboration sions about the systematics of the fossils; and N. Atkins for and funding of the Autoridad del Canal de Panama and R. improving the grammar. F. Herrera thanks B. Himschoot, Perez for donating the Toyota vehicles used in the fieldwork. M. I. Barreto, and family for support. Any opinions, find- The work was also supported by a graduate research fellow- ings, conclusions, or recommendations expressed in this arti- ship of the University of Florida (UF) to F. Herrera; the M. cle are those of the authors and do not necessarily reflect the Tupper Fellowship, the National Science Foundation (NSF; views of the NSF.

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