AMERICAN JOURNAL OF

BotanyDecember 2011 ◆ Volume 98 ◆ Number 12 Vol. 98, No. 12, 1911–xxxx—AMERICAN JOURNAL OF BOTANY—DECEMBER 2011

Offi cial Publication of the Botanical Society of America, Inc. www.amjbot.org American Journal of Botany 98(12): 2004–2017. 2011.

P HYTOGEOGRAPHIC IMPLICATIONS OF FOSSIL ENDOCARPS OF MENISPERMACEAE FROM THE PALEOCENE OF COLOMBIA 1

Fabiany Herrera2,3,6 , Steven R. Manchester2 , Sara B. Hoot4 , Keir M. Wefferling4 , M ó nica R. Carvalho3,5 , and Carlos Jaramillo 3

2 Department of Biology – Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 USA; 3 Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Anc ó n, Rep ú blica de Panam á ; 4 Department of Biological Sciences, P. O. Box 413, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53201 USA; and 5 Department of Geosciences, Pennsylvania State University, University Park, Pennsylvania 16802 USA

• Premise of the study: Fossil leaves of Menispermaceae were previously described from the Paleocene of Colombia. Because of strong homoplasy of leaf characters, the fossils could not be placed more specifi cally within recognized clades, and additional data were needed to specify intrafamilial and paleogeographic relationships during the Paleocene. • Methods: Fossil endocarps of Menispermaceae were collected from the Cerrej ó n Formation, the recently discovered Bogot á fl ora, and Wyoming (~60 Ma). We surveyed the endocarp morphology of almost all extant genera, conducted character optimization, a molecular scaffold analysis, and critically reviewed the related fossil genera. • Key results: Parallel syndromes of fruit characters have appeared in unrelated clades of the family according to current phylo- genetic reconstructions. However, mapping selected endocarp characters across those clades that contain horseshoe-shaped endocarps facilitates identifi cation and phylogenetic assessment of the fossils. Three fossil species are recognized. One of them belongs to the extant genus Stephania , which today grows only in Africa and Australasia. Palaeoluna gen. nov. is placed within the pantropical clade composed of extant Stephania , Cissampelos , and Cyclea ; this morphogenus is also recognized from the Paleocene of Wyoming. Menispina gen. nov. shows similarity with several unrelated clades. • Conclusions: The new fossils from Colombia reveal a complex paleobiogeographic history of the recognized clades within Menispermaceae, suggesting a more active exchange among neotropical, paleotropical, North American, and European paleo- forests than previously recognized. In addition, the new fossils indicate that neotropical forests were an important biome for the radiation and dispersal of derived lineages in Menispermaceae after the Cretaceous – Paleogene boundary.

Key words: Cissampelos ; Colombia; endocarps; fossils; paleobiogeography; Paleocene; rainforest; Stephania .

Menispermaceae are a pantropical angiosperm family within family include liana or vine growth habit, fl owers unisexual, Ranunculales with approximately 71 genera and 450– 500 spe- plants usually dioecious, petioles often swollen at the base, cies ( Thanikaimoni, 1984 ; Kessler, 1993 ). Species of the family ovules two (but one aborting), fruits in aggregates of drupes, are most common in tropical lowland rainforests although sev- endocarps with a condyle and seeds with a large, usually curved eral genera have species adapted to cooler or drier biomes. embryo (Diels, 1910; Kessler, 1993; Ortiz et al., 2007; Hoot Some of the morphological synapomorphies recognized for the et al., 2009 ; Jacques, 2009a ). Historically, Menispermaceae were divided into fi ve or eight tribes based largely on endocarp and seed characters (Miers, 1 Manuscript received 15 November 2010; revision accepted 12 September 1851; Diels, 1910; Kessler, 1993). However, the recent boom in 2011. molecular analyses has resulted in revised hypotheses of tribal This research was made possible through support from the Evolving relationships, morphological evolution, and classifi cation for Earth Foundation, the Geological Society of America Foundation, the this family (Jacques et al., 2007, 2011 ; Ortiz et al., 2007; Wang Asociació n Colombiana de Geó logos y Geofí sicos del Petroleo-ARES, et al., 2007 ; Jacques and Bertolino, 2008 ; Hoot et al., 2009 ). The The Smithsonian Institution, the Gary S. Morgan Student Research Award, endocarp types (i.e., boat-shaped, horseshoe-shaped, hairpin- and the Lewis & Clark Foundation-American Philosophical Society to F.H., National Science Foundation (NSF) grants EF-0431266 and BSR- shaped) that were used for the traditional classifi cation within 0743474 to S.R.M., NSF DEB-0919071 to M.R.C., NSF DEB-0733725 to the family appear to be highly homoplasious, and several tradi- C.J., and NSF DEB-0542679 to S.B.H. The authors thank L. Teicher, F. tional tribes and genera based on these characters are poly- Chavez, and the geology team at Minas Cerrej ó n. J. Moreno, E. Cadena, A. phyletic or paraphyletic when superimposed on a molecular Rincon, S. Moron, G. Bayona, S. L. Wing, J. Bloch, M. I. Barreto, G. phylogeny ( Jacques et al., 2007 ; Ortiz et al., 2007 ; Hoot et al., Doria, and A. Rojas for their assistance with the Bogot á and Cerrej ó n fi eld 2009 ). These new hypotheses of intrafamilial relationships trips; C. A. Mu ñ oz for his hospitality during fi eldwork in Bogotá . D. Bell in Menispermaceae indicate the need for caution in identifying (US) granted access to modern Menispermaceae collections, R. C. Ortiz affi nities for fossil taxa. Nonetheless, fossil endocarps are in- and F. Jacques provided helpful discussions about the systematics of the valuable for understanding the evolution and paleobiogeography fossils, and G. Bedoya provided nomenclatural suggestions. Two of the family. Furthermore, their identifi cation to the tribe or ge- anonymous reviewers and T. Lott provided helpful reviews of the manuscript. F.H. thanks B. Himschoot for support. nus level will require a combination of fruit characters instead of 6 Author for correspondence (e-mail: fherrera@fl mnh.ufl .edu) relying on the historical endocarp types (Jacques et al., 2011). As recently listed in Doria et al. (2008) and Jacques (2009b), doi:10.3732/ajb.1000461 dozens of leaf, wood, fl ower, pollen, and endocarp fossils

American Journal of Botany 98(12): 2004–2017, 2011; http://www.amjbot.org/ © 2011 Botanical Society of America 2004 December 2011] Herrera et al. — Fossil endocarps of Menispermaceae from South America 2005 have been attributed to Menispermaceae ranging from the Formation had accumulated in the lowlands (Bayona et al., 2008). Pollen as- lower Cretaceous to the Pliocene. In South America, Paleo- semblages from the Bogot á Formation belong to the zone T-03b-Foveotricol- pites perforatus of Jaramillo et al. (2011), indicating a middle to late Paleocene gene fossil leaves have been attributed to Menispermaceae age. The formation varies from extensive and thick siltstones, claystones, and from the Paleocene of Colombia and Argentina ( Iglesias et al., paleosols to interbedded sandstones and sporadic conglomerates and breccias. 2007; Doria et al., 2008) and the Eocene of Brazil (Dolianiti, Contrary to the Cerrej ó n Formation, the Bogot á sequence lacks coal deposits. 1949; Mello et al., 2000). Of these fossil records, just those Initial sedimentological analyses from the Bogotá Formation indicate deposi- reported from the Paleocene of Colombia ( Doria et al., 2008 ) tion in fl uvial environments. The specimen BF18-ING-0017 was found in a have been fully described and compared with extant leaves of massive yellowish lacustrine claystone bed, about 40 cm thick underneath a thick red paleosol. The specimens BF19-ING-0012-0016 and BF18-ING-0023 the family; the remaining reports of Menispermaceae in South are from grayish, laminated, and fi ne-grained sandstones that suggest deposi- America still require a detailed examination to confi rm their tion in overbank deposits. The specimens BF20-ING-0019-0020, BF20- affi nity. Because of the homoplasy found in leaf characters in ING-0024, and BF20-ING-0026 were found along with abundant crocodile Menispermaceae (see Hoot et al., 2009 ), the four Paleocene teeth and turtle shells in an ~20 cm reddish breccia with very angular grains and fossil species from the Cerrejó n Formation of Colombia could iron oxide cementing material. This bed may have been deposited during an not be placed more specifi cally within recognized clades of aqueous debris fl ow. Some of the plant families and genera already identifi ed from the Bogotá fl ora include Annonaceae, Arecaceae, Fabaceae, Lauraceae, the family (Doria et al., 2008). Future comparative studies on Malvaceae, Salicaceae, Theaceae, and the fl oating-aquatic fern Salvinia . cuticle and leaf architectural patterns among living Menisper- The Colombian fossils are stored at the paleontological collections of the maceae might provide stronger evidence for placing such Colombian Geological Institute (INGEOMINAS) in Bogot á , Colombia. fossils. The specimen from Linch, Wyoming (UF18257-21872; Fig. 17 ) was recov- Jacques et al. (2011) recently used a molecular scaffold ered from a Paleocene (Tiffanian) locality of the Fort Union Formation (Pow- analysis for the placement of 26 taxa of fossil menisperma- der River Basin), exposed at the west side of the highway 192 at the southern end of the road cut in Pine Ridge, WY quadrangle 7.5′ series, GPS 43° 37.800 ′ N ceous endocarps. In general, their consensus tree agreed with 106 ° 12.371 ′W. Pollen samples from the Fort Union Formation have corrobo- the previous suggested affi nities of the fossil taxa, except in rated a middle-late Paleocene age for the stratigraphic sequence where the fossil the case of some fossil species placed within the genera Coc- was found ( Nichols, 1994). The menispermaceous endocarp is found together culus and Parabaena. Despite the drawbacks of the molecular with predominantly deciduous taxa including Metasequoia , Aesculus , Cranea , scaffold approach (relatively low number of fossilizable char- Corylites , Fagopsiphyllum , and Juglandicarya simplicarpa . acters compared to DNA data, the lack of interaction among We studied modern fruits representing 68 of the 71 extant genera recognized for Menispermaceae with materials from the U. S. National Herbarium (US) at data partitions, homoplasy, and the limited topology of the the Smithsonian Institution in Washington, D.C., the Smithsonian Tropical Re- resulting trees), this method seems feasible for hypothesizing search Institute (STRI) in Panama, the University of Florida Herbarium (FLAS) the placement of extinct species within a given topology of in Gainesville, Florida, the U. S. National Seed Herbarium housed at the Na- extant taxa (Manos et al., 2007). tional Arboretum, Washington, D. C. (BARC), the Herbarium of the Arnold Here, we describe three Paleocene fossil taxa based on en- Arboretum (A) at Harvard University in Boston, Massachusetts, the Field Mu- seum of Natural History Herbarium (F) in Chicago, Illinois, and the University docarps collected from north and central Colombia (Cerrejó n of Wisconsin-Milwaukee (UWM) Herbarium in Milwaukee, Wisconsin (Figs. and Bogot á paleofl oras) and Wyoming (USA). A molecular 18 – 48 ). To fully examine the endocarp morphology of the extant taxa (species scaffold analysis was implemented for the placement of the listed in Appendix 1) and prepare them for photography, the mesocarp tissue fossil taxa. The menispermaceous fossil endocarps comple- was removed after hydration with boiling water or by soaking the fruits in tap ment the earlier report based on foliage from the Cerrej ó n water for 8 – 24 h, depending on their size and mesocarp thickness. The endo- fl ora ( Doria et al., 2008 ) and provide greater resolution of in- carps were cleaned with a nylon toothbrush and rinsed until free of soft tissues. Photographs were taken using a Retiga 2000R digital camera with QCapturePro trafamilial relationships. In particular, these new fossil spe- 5.1 software, attached to an Olympus SZX16 microscope in the UWM micros- cies suggest a wider biogeographic distribution for the copy laboratory. For the grayscale photos, exposures were adjusted and back- ancestors of extant African and Australasian lineages and sug- grounds removed in Photoshop CS2 (Adobe, San Jose, California, USA). Fully gest a Paleocene connection with extinct menispermaceous mature endocarps and drupes were measured with calipers; the average size taxa from North America. was recorded when multiple specimens were examined. These studies were supplemented by consideration of published images and descriptions (e.g., Thanikaimoni, 1986; Jacques, 2009a). Terminology for the description of fruits partly follows Jacques (2009a). See Appendix 2 for a complete defi nition of MATERIALS AND METHODS endocarp characters. To assess affi nities of the fossil endocarps with living genera within The newly recovered South American endocarps are from two widely sepa- Menispermaceae, we searched for extant morphological synapomorphies based rated Paleocene fl oras from northern (Cerrej ó n fl ora) and central (Bogot á fl ora) on the characters that are preserved in the fossil remains. Scoring criteria are Colombia ( Figs. 1 – 16 ). Three specimens were collected from the upper levels of available in Appendix 3, also at the MorphoBank web site [http://www. the Cerrej ó n Formation, an ca. 700-m-thick stratigraphic sequence, composed of morphobank.org; Project (P407): Herrera et al_Endocarp Morphological abundant and thick coals, fl uvial sandstones, and lacustrine siltstones that were Matrix Menispermaceae]. Character optimization was conducted with the pro- deposited in a succession of tidal fl ats to coastal fl oodplains crossed by channels gram Mesquite 2.74 ( Maddison and Maddison, 2009 ). The morphological char- (Bayona et al., 2004, 2008 ). The Cerrejó n Formation has been dated as middle acters were superimposed on a simplifi ed DNA tree topology for Menispermaceae to late Paleocene (~60 Ma) based on pollen zonation, correlations with stable (only those extant clades with high support of PP ≥ 95 and BS ≥ 80 were main- carbon isotopic data, and marine microfossils ( Jaramillo et al., 2007 ; 2011 ). The tained; Hoot et al., 2009). This simplifi ed DNA tree was then used as the “ back- Cerrejó n endocarp fossils (CJ85-ING-1412 to CJ85-ING-1414) were found bone constraint” for a molecular scaffold analysis (Springer et al., 2001; Manos along with angiosperm leaf remains in an extensive gray siltstone bed around et al., 2007 ). Sagittaria sagittifolia (Alismataceae) and Fumaria indica (Papav- 60– 90 cm thick that was deposited in a swampy-lacustrine environment. The eraceae) were used to root the tree. The morphological matrix included 25 char- local fl ora was dominated by Araceae, Arecaceae, Fabaceae, Lauraceae, Malva- acters, 17 of them referring to the endocarp, the remaining eight characters ceae, Zingiberales, and several unidentifi ed ferns (Herrera et al., 2008; G ó mez- were taken from Hoot et al. (2009) and correspond to habit, leaf and pollen Navarro et al., 2009 ; Wing et al., 2009 ; Carvalho et al., 2011 ). features (Appendix 3). A heuristic search was carried out with 1000 replicates Eleven endocarps were collected from a recently discovered fossil fl ora of random taxon addition and tree-bisection-reconnection (TBR) branch swap- from the eastern Colombian Andes. The plant localities are from the Bogot á ping in the program PAUP* 4.0b10 (Swofford, 2003). Bootstrap analyses were Formation, an outcropping at the Sabana de Bogotá between 2700– 3000 m performed on the morphological data without enforcing the backbone con- a.s.l. During the Paleocene, the Andes had not been uplifted, and the Bogotá straint, using 100 replicates and full heuristic searches. 2006 American Journal of Botany [Vol. 98

SYSTEMATICS Description — Impressions and casts of fi ve horseshoe- shaped endocarps; outline of endocarp obovate in lateral view Fruits of Menispermaceae are single-seeded drupes with an with a smooth and broad-rounded dorsal crest and an asym- ornamented to smooth endocarp; the shape of the endocarp and metrical and acute base; length 4.5 – 6.5 mm, mean 5.65 mm its seed varies strongly from completely straight, boat-shaped, (SD = 0.89, N = 4), width 3.5– 4.3 mm, mean 3.9 mm (SD = to horseshoe-shaped as found in many extant genera (Figs. 18– 0.43, N = 4); endocarp wall thickness ~0.6– 0.7 mm (measured 48 ). The curved-seeded endocarps result from an outgrowth of from the locule cast to the apex of the endocarp); the dorsal the ovary wall into the placental region; this outgrowth is known crest with one side broader (toward putative stylar end) than the as the condyle ( Hoot et al., 2009 ). Curved seeds are not unique other; lateral crest decorated with spine-like structures (from 10 for Menispermaceae; for example, some genera in Schisan- to 13); condyle outline obovate; a straight ventral vascular tube draceae, Cochlospermaceae, and Alismataceae may resemble ascends (from base of condyle area) and approaches the locule the typical horseshoe shape of some Menispermaceae. How- forming a strong curvature at the connection point (preserved ever, the combination of characters mentioned already (orna- only in one specimen CJ85-ING-1413; Figs. 3, 4 ); locule cast mented to smooth endocarp and condyle) makes the drupes of apically positioned within the outline of the endocarp, with un- Menispermaceae unique within angiosperms. The three new equal limbs and rimmed by the lateral crest, beset with radially species from the Paleocene of Colombia and Wyoming reported aligned ribs (from 10 to 13); locule cast limbs widely spaced, in this study present a unique combination of characters diag- ~0.7 mm (measured from tip of the short limb to tip of the lon- nostic for the family. ger limb); longer limb of locule cast appears to be at seed radi- The morphological characters mapped over the simplifi ed cal end (also stylar end of fruit); ventral notch straight; a tiny, topology of Menispermaceae corroborate other recent studies narrow (length ~1 mm, wide ~0.2 mm), and obovate perfora- indicating homoplasy among endocarp morphology features tion piercing the endocarp near the base. within this family ( Fig. 49 ; Appendix 3). Although we did not fi nd any strong synapomorphies for the simplifi ed clades Derivation of specifi c epithet — From the prefi x “ palaeo ” for in Menispermaceae, the character mapping provides hypoth- ancient and “sudamericana ” from the continent where the fos- eses for the placement of the fossils. The three fossil taxa sils originate. studied are very similar to the endocarps found in the follow- ing clades and genera (Fig. 49): (a) Sinomenium -Menisper- Age, source, and stratum — Middle to late Paleocene. Holo- mum , (b) Pericampylus (c) Stephania -Cissampelos -Cyclea type and paratypes CJ85-ING-1413 and CJ85-ING-1414 from ( S -C -C ). Morphological characters shared between these Guajira Peninsula, Rancherí a Basin, Cerrejó n coal mine, Cer- clades and the fossils treated here include horseshoe-shaped rejó n Formation, Tabaco Extensió n localities 0705 and 0712, endocarps, the endocarps being less than 10 mm in length, 11 ° 07 ′ 49.8N, 72° 34 ′60.5W, localities placed below coal bed the presence or absence of a basal sculpturing, the presence 175. Paratypes BF18-ING-0017 and BF18-ING-0023 from of lateral crests, and a spiny ornamentation on both dorsal Cundinamarca state, Cogua locality FH0903, Bogotá Forma- and lateral crests. tion; 5 ° 04 ′ 36.1N, 73 ° 57 ′ 18.9W. The molecular scaffold analysis yielded 152 trees of 76 steps (CI 0.447, RI 0.548, RC 0.245). The resulting strict consensus Systematic affi nity within Menispermaceae — Among mod- tree was similar to the backbone constraint generated from the ern genera of the S-C-C clade ( Fig. 50 ), the fossil shows closest DNA data ( Fig. 49 ), but placed the three fossil species within morphological similarity to Stephania . Some of the characters the extant S - C - C clade (Fig. 50). A more detailed comparison that support this affi nity include the horseshoe-shaped endo- of the fossil endocarps with modern genera is discussed follow- carp, the length of the endocarp considerably less than 10 mm, ing the taxonomic descriptions. a thin endocarp wall ( < 1 mm), only one lateral crest on each side of the endocarp, a straight ventral vascular tube, a long Order — Ranunculales Dumortier radical limb, conspicuous locule ribs, a straight ventral notch, and the lack of protrusions in the locule chamber (Figs. 18– 28 ). Family — Menispermaceae A. L. de Jussieu Although none of these traits by itself is synapomorphic for Stephania (Fig. 49), the combination of all the characters men- Genus — Stephania Loureiro tioned makes it possible to recognize endocarps of this genus and facilitates identifi cation of the Paleocene endocarps. Steph- Type species — Stephania palaeosudamericana Herrera, ania exhibits a signifi cant amount of intrageneric variation in Manchester, Hoot, Wefferling, Carvalho et Jaramillo sp. nov. ornamentation (ribs and spines), perforation (presence/absence and size), endocarp shape (from obovate to rounded), number Diagnosis —Endocarp thin-walled; dorsal crest broad- of dorsal crests (one or two), and spiny or nonspiny dorsal and rounded, base asymmetrical and acute; with one lateral crest lateral crests (Figs. 18– 28 ) and the Cerrejó n and Bogotá endo- on each side of the plane of symmetry; lateral crests spiny; carps fi t well within this natural morphological variation. Cis- locule cast apically positioned and with unequal and closely sampelos and Cyclea are closely related to Stephania ( Hoot spaced limbs and 10 to 13 ribs; straight ventral vascular tube; et al., 2009 ; Jacques et al., 2011 ), but their endocarps are easily endocarp with a tiny perforation in the condylar area, near the distinguished (Figs. 29– 33, 35– 39 ). In these two genera, there base. are always two lateral crests per side, usually two dorsal crests (rather than one as in this fossil), and their endocarps are often Holotype hic designatus — CJ85-ING-1412 ( Figs. 1, 2 ). imperforate. Stephania palaeosudamericana also resembles members of Paratypes — CJ85-ING-1413 ( Figs. 3, 4 ); CJ85-ING-1414 the Sinomenium - Menispermum clade, but in these two genera ( Fig. 5 ); BF18-ING-0017 ( Fig. 6 ); BF18-ING-0023 ( Fig. 7 ). the endocarps do not have a complete perforation (but rather December 2011] Herrera et al. — Fossil endocarps of Menispermaceae from South America 2007

Figs. 1– 17. Fossil taxa from Paleocene of Colombia and Wyoming, USA. Figs. 1– 7. Stephania palaeosudamericana Herrera, Manchester, Hoot, Wef- ferling, Carvalho et Jaramillo sp. nov. Figs. 1, 2. Holotype (CJ85-ING-1412), part and counterpart; from upper to lower arrows: 1. Locule ribs, seed radical end, straight ventral vascular tube, stylar end; 2. lateral ridges. Figs. 3, 4. Paratype (CJ85-ING-1413), part and counterpart; from upper to lower arrows: 3. Dorsal crest, entry of vascular tube into seed locule; 4. lateral ridges, perforation. 5. Paratype (CJ85-ING-1414), from upper to lower arrows: broader dorsal crest, straight ventral notch. 6. Paratype (BF18-ING-0017), arrow: lateral spines. 7. Paratype (BF18-ING-0023), locule cast showing a longer limb. Figs. 8– 11. Menispina evidens Herrera, Manchester, Hoot, Wefferling, Carvalho et Jaramillo gen. nov. sp. nov. 8. Holotype (BF19-ING-0014), upper arrow: conspicu- ous dorsal spine, lower arrow: basal sculpturing. 9. Paratype (BF19-ING-0015), arrow: basal sculpturing. 10. Paratype (BF19-ING-0012), arrow: broader dorsal crest. 11. Paratype (BF19-ING-0016), left arrow: pedicel, middle arrow: basal sculpturing, right arrow: broader dorsal crest. Figs. 12 – 17. Palaeoluna bogotensis Herrera, Manchester, Hoot, Wefferling, Carvalho et Jaramillo gen. nov. sp. nov. 12. Holotype (BF20-ING-0020), upper arrow: conical pits of spines, lower arrow: locule ribs. 13. Paratype (BF20-ING-0019), upper arrow: locule inner protrusions, lower arrow: thick endocarp wall. 14. Paratype (BF20-ING-0024), arrow: locule inner protrusions. 15. Paratype (BF20-ING-0026), showing thick endocarp wall and locule inner protrusions. 16. Paratype (BF2-ING-0018), arrow: putative stylar end. 17. Palaeoluna sp. (UF18257-21872), Paleocene of Wyoming, endocarp impression. Scale bars = 2 mm. 2008 American Journal of Botany [Vol. 98 lateral apertures that do not traverse the endocarp) and are usu- Systematic affi nity within Menispermaceae — No living ge- ally rounded in outline, the dorsal crest is more or less spiny nus coincides fully with the morphology of Menispina evidens . (more in Sinomenium ), and the locule ribs are inconspicuous Nevertheless, this fossil shares characters with three unrelated ( Figs. 42 – 48 ). clades within the Menispermaceae ( Fig. 49 ; Appendix 3): S - C - Fossil endocarps of Stephania have been reported from the C clade, Sinomenium - Menispermum , and Pericampylus . early Miocene of Kenya ( Chesters, 1957 ) and the late Pleisto- Menispina evidens is similar to the Sinomenium - Menisper- cene of Nepal (Bhandari et al., 2009). Both fossil species have mum clade and shares some characters (i.e., horseshoe-shaped prominent ornamentation on the dorsal crest, which is quite dif- endocarps, length signifi cantly less than 10 mm, thin endocarp ferent from S. palaeosudamericana; the species from Nepal wall ( < 1 mm), and the lack of locule inner protrusions; Fig. 49 ); also has a larger perforation. however, the extant genera differ from the Paleocene species in the presence of a vasculature channel on the lateral crests, the Morphogenus — Menispina Herrera, Manchester, Hoot, absence or poor development of dorsal spines, and inconspicu- Wefferling, Carvalho et Jaramillo gen. nov. ous locule ribs ( Figs. 42 – 49 ). On the other hand, Menispina evidens resembles the extant Generic diagnosis — Endocarp thin-walled; endocarp outline genus Pericampylus in having endocarps with limbs of equal elliptic, circular and obovate in lateral view with single rows of length, basal sculpturing, a horseshoe-shaped endocarp, length conspicuous acute spines on the dorsal and lateral crests; locule signifi cantly less than 10 mm, a thin endocarp wall (< 1 mm), cast extending near to the base, more or less smooth with equal conspicuous locule ribs, a straight ventral notch, and lack of and closely spaced limbs and marked with 11 to 14 radial ribs locule inner protrusions (Figs. 40, 41, 49). Pericampylus dif- that are more or less aligned with the dorsal and lateral spines; fers, however, from Menispina in having two dorsal and lateral apparently lacking a perforation, but with a basal sculpturing crests on each side of the endocarp, and in the presence of very near the shorter limb; pedicel short. thick spines ( Fig. 40 ). The molecular scaffold analysis places Menispina within Derivation of generic name — From the Greek word “Meni- the S - C- C clade together with the two other fossil genera from skos” for crescent-shaped and the Latin word “ spina ” for the Paleocene of Colombia ( Fig. 50 ). Within this clade, spine. Menispina is placed as sister to Palaeoluna , but without boot- strap support. Characters shared with the S - C- C clade include: Type species — Menispina evidens Herrera, Manchester, the horseshoe-shaped endocarp, length signifi cantly less than Hoot, Wefferling, Carvalho et Jaramillo sp. nov. 10 mm, thin endocarp wall (< 1 mm), conspicuous locule ribs, a straight-margined ventral notch, and the lack of locule inner Holotype hic designatus — BF19-ING-0014 ( Fig. 8 ). protrusions ( Fig. 49 ). Notable differences between M . evidens and other members of the S - C- C clade, namely the absence of Paratypes — BF19-ING-0012 ( Fig. 10 ), BF19-ING-0015 endocarps with limbs of equal length and basal sculpturing, as ( Fig. 9 ), BF19-ING-0016 ( Fig. 11 ). well as the lack of synapomorphic endocarp characters to re- late this fossil genus to any other extant clade, lead us to con- Description —Impressions and casts of four crescent and sider M. evidens as of uncertain placement within the extant horseshoe-shaped endocarps; length 3.0– 4.3 mm, mean 3.7 mm Menispermaceae topology. (SD = 0.53, N = 4), width 2.5 – 4.3 mm, mean 3.4 mm (SD = 0.8, N = 4); endocarp wall thickness ~0.6– 1.0 mm (measured from Morphogenus — Palaeoluna Herrera, Manchester, Hoot, the locule cast to the apex of the endocarp); outline of endo- Wefferling, Carvalho et Jaramillo gen. nov. carp elliptic, circular and obovate in lateral view with 13 to 16 conspicuous, stiff, acute spines on the dorsal and lateral crests; Generic diagnosis — Endocarp thick-walled; dorsal crest or- the longest dorsal spines are at least 1.5 mm in length; the namented with inconspicuous narrow spines; one lateral crest; thickest dorsal spine bases are mostly located near the stylar locule cast with unequal and widely spaced limbs, and 15 to 16 and pedicel ends (best seen in the holotype and paratype prominent ribs; locule chamber with inner protrusions. BF19-ING-0015, Figs. 8, 9 ); dorsal crest with one side broader (toward stylar end) than the other; condyle outline obovate Derivation of generic name — From the prefi x “ palaeo ” for and elliptic; central locule cast extending to the base and with ancient and the Latin “ luna” for moon, because of the resem- equal limbs, marked with 11 to 14 radially aligned ribs and blance to a crescent moon-like shape. with rounded pits or grooves (probably spine bases); locule cast limbs closely spaced; apparently lacking a perforation, Type species — Palaeoluna bogotensis Herrera, Manchester, but with a basal sculpturing (manifested as a small concavity) Hoot, Wefferling, Carvalho et Jaramillo sp. nov. near shorter limb; ventral notch straight-margined; pedicel short (~0.5 mm). Holotype hic designatus — BF20-ING-0020 ( Fig. 12 ).

Derivation of specifi c epithet — From the Latin “ evidens ” : Paratypes — BF20-ING-0019 ( Fig. 13 ); BF20-ING-0018 evident, clear. (Fig. 16); BF20-ING-0024 (Fig. 14); BF20-ING-G0026 (Fig. 15 ). Age, source, and stratum — Middle to late Paleocene. Bo- got á Formation, Cundinamarca state, Nemoc ó n locality, Checua Species description — Molds and casts of fi ve horseshoe- mine. Holotype and paratypes BF19-ING-0014-16, locality shaped endocarps; endocarp outline obovate in lateral view with FH0801, 5 ° 0.8 ′ 24.9N, 73° 50 ′80.4W. Paratype BF19-ING-0012, broad-rounded dorsal side; length ~6.2– 9.0 mm, mean 7.2 mm locality FH0806, 5 ° 0.8 ′ 14.5N, 73 ° 50 ′ 80.2W. (SD = 1.2, N = 4), width 5.0 – 7.0 mm, mean 5.9 mm (SD = 0.9, December 2011] Herrera et al. — Fossil endocarps of Menispermaceae from South America 2009

Figs. 18– 48. Extant Menispermaceae endocarps. Figs. 18– 20. Stephania brevipes Craib (A96-895). 18. Lateral view (LV), endocarp shape obovate with a prominent perforation, arrow: ornamentation. 19. Sagittal view (SV), arrow: apical locule/seed. 20. Sagittal view empty (SVE), arrow: straight ventral vascular tube. Figs. 21 – 23. S. delavayi Diels (US599329). 21. LV, arrow: broad dorsal crest. 22. SV, endocarp with an apical locule/seed (arrow). 23. SVE, arrow: tiny perforation. Figs. 24– 27. S. japonica (Thunb) Miers (US3461000, A3485). 24. LV, arrow: ornamentation. 25. SV, arrow: longer locule limb of the stylar end. 26. SVE, arrow: straight ventral vascular tube. 27. LV of the seed, arrow: conspicuous ribs. 28. S . hernandiifolia (Willd.) Walp. (US3345848), arrow: straight ventral notch. Figs. 29, 30. Cissampelos andromorpha DC (US1997934, US2575572). 29. LV, endocarp exhibiting typical morphology for this genus, arrow: outermost lateral crest. 30. SV, arrow: longer seed/locule limb. Figs. 31 – 33. C . pareira L. (F2742). 31. LV, arrow: lateral crest spines. 32. SVE, arrow: inner locule ribs. 33. LV of the seed, notice longer limb and arrow: conspicuous ribs. 34. Diploclisia glaucescens (Blume) Diels (A1501), SV, hairpin-shaped endocarp, arrow: inner locule protrusions derived from intense exterior ribbing. 35. Cyclea atjehensis Forman (A90-33), LV, notice two lateral and two dorsal crests, arrow: conspicuous spines. 36. Cy. hypoglauca (Schauer) Diels (US1754790), SV, left arrow: longer locule/seed limb, right arrow: straight ventral vascular tube. 37. Cy. peltata Diels (US2616394), LV, arrow: ornamentation of outermost lateral crest. 38. Cy. polypetala Dunn (US458824), LV, endocarp showing two dorsal and two lateral crests, arrow: one of the lateral crests. 39. Cy. racemosa Oliv. (A663), SVE, arrow: straight ventral vascular tube. Figs. 40, 41. Pericampylus glaucus (Lam.) Merr. (A96-662). 40. LV, arrow: broad dorsal crest, also notice conspicuous spines. 41. LV of the seed ex- hibits conspicuous ribs (arrow) and two limbs of equal length. Figs. 42– 45. Menispermum canadense L. (UWM15599, US371274). 42. LV, arrow: vasculature channel. 43. SV, notice central seed. 44. SVE, notice smooth locule chamber wall; arrow: entry of lateral vascular tube. 45. LV of the seed exhibiting two limbs of equal length and without ribs. Figs. 46 – 48. Sinomenium acutum (Thunb.) Rehder & Wilson (A24889, US1990264). 46. LV, arrow: spines on the dorsal crest. 47. SVE, notice smooth locule chamber wall; arrow: entry of vascular tube. 48. LV of the seed shows inconspicuous ribs. Scale bars = 0.5 mm.

N = 4); endocarp wall thickness ~1.0 – 2.1 mm (measured from 5 ° 0.8 ′ 41.5N, 73 ° 50 ′ 58.3W. Paratype BF20-ING-0018 comes the locule cast to the apex of the endocarp); impression speci- from GPS location 5° 0.8 ′ 23.44N, 73 ° 50 ′ 27.54W. mens of the interior side of the dorsal crest preserve conical pits indicating the presence of narrow, spine-like structures; one lat- Systematic affi nity within Menispermaceae — In the molec- eral crest on each side; condyle outline ovate in shape; central ular scaffold analysis, Palaeoluna bogotensis is placed within locule cast with unequal limbs (appearing as a J-shaped locule), the S - C - C clade (Fig. 50). One of the main morphological char- ornamented by 15 to 16 radially aligned ribs; opposite to the acters supporting this placement is the presence of strongly un- locule ribs are spine-like structures that correspond to inner equal locule limbs ( Fig. 49 ). Although this character is not protrusions of the locule chamber; locule cast limbs widely synapomorphic for the S - C - C clade, it appears to be diagnostic spaced, ~1.1 mm (measured from tip of the short limb to tip of in comparison with the remaining clades in the family that ex- the longer limb). hibit horseshoe-shaped endocarps with conspicuous locule ribs. The strongly unequal limbs combined with other characters Derivation of specifi c epithet — From the Bogot á Formation, (e.g., conspicuous locule ribs, endocarp length less than 10 mm, where the fossils were found. etc.) make this group recognizable. Within the S - C - C clade, Cissampelos has the closest morphological similarity with the Age, source, and stratum — Middle to late Paleocene. Bo- fossil taxon (Figs. 29– 33 ); the almost J-shaped locules in this got á Formation, Cundinamarca State, Nemoc ó n locality, Checua extant genus are very similar to those in P . bogotensis ( Figs. 30, mine. Holotype and paratypes BF20-ING-0019, BF20- 33 ). On the basis of these morphological similarities, we sup- ING-0024, and BF20-ING-G0026 are from locality FH0918, port Palaeoluna as an extinct genus within the S - C - C clade. 2010 American Journal of Botany [Vol. 98

Fig. 49. Morphological characters superimposed on a simplifi ed tree topology of Menispermaceae (only those extant clades with high support PP ≥ 95 and BS ≥ 80 were maintained, modifi ed from Hoot et al., 2009). See Appendix 2 and 3 for a complete list of the genera and characters states. *Cocculus appears paraphyletic. This simplifi ed DNA tree was then used as the “ backbone constraint ” for a molecular scaffold analysis. Photos of endocarps correspond to Stepha- nia brevipes Craib (A96-895); lowercase letters indicate some of the morphological characters mapped. Gray boxes highlight the extant genera that show the closest similarity to the new Paleocene endocarps from Colombia and Wyoming. Fossil taxa ( † ) included at the bottom of the fi gure for comparison. December 2011] Herrera et al. — Fossil endocarps of Menispermaceae from South America 2011

Figs. 50, 51. 50. Strict consensus tree of morphological data analyzed under the backbone constraint shown in Fig. 49 , bootstrap values given for nodes > 50%; fossil taxa († ) are highlighted with a gray shaded box, solid circles correspond to the backbone constraint. See Appendix 3 for a complete list of the genera. *Cocculus appears paraphyletic. 51. Fossil locations and geographic distribution of three extant genera in Menispermaceae that are related to the Paleocene endocarps. Modern distribution based on literature (e.g., Thanikaimoni, 1986 ) and biodiversity occurrence data accessed through GBIF Data Portal, data.gbif.org, 2010-10-15. Base map courtesy of National Aeronautics and Space Administration Jet Propulsion Laboratory, California Institute of Technology.

Palaeoluna bogotensis also resembles species of the fossil Chandler (1961) suggested Sinomenium and Menispermum as genus Palaeosinomenium Chandler, originally described from the extant genera most closely related to Palaeosinomenium . How- the early Eocene of England (Chandler, 1961). Palaeosinome- ever, after examining these two extant genera we question this af- nium is typifi ed by a horseshoe-shaped endocarp with one loc- fi nity. In the Sinomenium -Menispermum clade, the locule ribs are ule limb much longer than the other, radial ridges that continue fairly inconspicuous (Figs. 42– 48 ). Also, in Palaeosinomenium the over the lateral crest toward the perforation, and the presence of radial ridges may continue over the lateral crest toward the perfora- abundant and conspicuous ribs. The new fossil morphogenus tion, not characteristic of Sinomenium or Menispermum . In addi- Palaeoluna can be differentiated from Palaeosinomenium by tion, the locule area is completely smooth and unribbed as observed the thick endocarp wall, the lack of radial ridges that continue in living and fossil taxa ( Figs. 42 – 48 ; Liu and Jacques, 2010 ). over the lateral crest, and the presence of inner protrusions in We also placed an endocarp from the middle-late Paleocene the locule chamber. This last character is only found in the un- (Tiffanian) Fort Union Formation near Linch, Wyoming, within related hairpin-shaped endocarps of modern Diploclisia (Fig. 34). the new genus Palaeoluna ( Fig. 17 ). The endocarp shows a strong Affi nity with extant Diploclisia can be ruled out, however, similarity to the Colombian taxon, having an outline obovate in based on differences in endocarp size, the shape of the locule lateral view, strongly unequal (J-shaped) and widely spaced limbs, chamber, and the ornamentation. and the locule chamber has abundant inner protrusions. 2012 American Journal of Botany [Vol. 98

Fig. 52. Hypothesized routes of dispersal for the Paleocene endocarps from Colombia and North America. Black star indicates the Bogota and Cer- rej ó n fl oras from Colombia; white star indicates the Fort Union Formation, Linch, Wyoming, USA. Paleocene map modifi ed from Scotese (2001) .

DISCUSSION AND IMPLICATIONS FOR seem to explain better the current distribution for some clades of MENISPERMACEAE Menispermaceae. Here, we propose four hypothetical scenarios that explain the occurrence of these fossil taxa: The new menispermaceous endocarp taxa described in this study augment the list of fossils recently identifi ed from the Pa- (1) Dispersal via Laurasia— The former presence of the genus leocene forests of northern South America. Other components of Stephania, which grows today in equatorial Africa and Australasia the Cerrej ó n fl ora identifi ed to extant taxa below the family level ( Fig. 51 ), in Paleocene neotropical rainforests, indicates a broader include the aroid Montrichardia ( Herrera et al., 2008 ), members distribution of this genus in the past. It is possible that this genus of the palm subtribes Euterpeinae and Attaleinae (G ó mez- reached the neotropics by dispersal from Africa and/or Asia via Navarro et al., 2009 ), and leaves of Eumalvoideae, Malvaceae Laurasia ( Fig. 52 ). The absence of Stephania endocarps of Paleo- (Carvalho et al., 2011). The new fossils reconfi rm the presence cene age or older ages from Old World fl oras could also support a and diversity of Menispermaceae in the middle-late Paleocene of neotropical origin with subsequent local extinction of this genus. Colombia. Lianas are the predominant habit for extant Menisper- Paleobotanical localities of Paleocene age are too poorly repre- maceae and are typical of rainforests. The Cerrej ó n and Bogot á sented in Africa and Southeast Asia to refute the Laurasian hypoth- paleofl oras have all the characteristics representative of this esis. However, the presence of Stephania endocarps in the Messel biome ( Herrera et al., 2008 ; Head et al., 2009 ; Wing et al., 2009 ); fl ora (~47 Ma) from the middle Eocene of Germany (Collinson hence, it is not surprising to recover this family in the fl ora. et al., in press) supports this route of dispersion. The fossil leaves and endocarps from the Paleocene of Co- lombia constitute the earliest known record of this family in (2) Transpacifi c dispersal of Stephania between South northern South America. The distinctive endocarps of this fam- America and Australasia ( Fig. 52 ) — There is increasing evi- ily seem to be lacking from the fl ora of the late Cretaceous dence supporting transpacifi c dispersal events in several extant (Maastrichtian) Guaduas Formation, which is stratigraphically plant groups ( Michalak et al., 2010 ; Renner et al., 2010 ), which beneath the Bogot á Formation (currently under study, C. Jaramillo makes this route seem plausible. Another fossil from the Cer- and F. Herrera, unpublished data), so it is possible that the fam- rej ó n Formation assigned to the modern palm genus Nypa ily was introduced to this region later toward the end of the shows a connection with southeastern Asia (G ó mez-Navarro Cretaceous or in the Paleocene during the interval immediately et al., 2009 ). Also, new fossil fruits from a late Eocene locality preceding the time in which the Cerrej ó n and Bogota fossils of Panama (Tonos í , Azuero Peninsula) show affi nities with ex- were deposited. tant Australasian genera (F. Herrera and S. Manchester, per- Modern neotropical rainforests are distinctive in family compo- sonal observation). sition ( Gentry, 1988 ; Terborgh and Andresen, 1998 ) and Menisper- maceae is one of the common elements in this biome. How (3) Exchange of Stephania via Antarctica ( Fig. 52 ) — A Pa- Menispermaceae originated or reached South America is still un- leocene dispersal event via Antarctica is also probable. This known. There is little doubt that vicariance may have played an route of exchange lasted until the opening of the Drake Passage important role in the history of the family; however, based on the and the resulting glaciation in the late Eocene ( Scher and available fossil record, dispersal events and/or local extinctions Martin, 2006 ). This is also supported by several plant lineages of December 2011] Herrera et al. — Fossil endocarps of Menispermaceae from South America 2013 extant Australasian affi nity (e.g., Eucalyptus, Gymnostoma, and Bayona , G. , C. Jaramillo , M. Rueda , A. Pardo , A. Christie , and G. Papuacedrus ) together with menispermaceous leaves and endo- Herná ndez . 2004 . Important paleotectonics and chronostratigraphic carps found in Eocene fl oras of Argentina (Zamaloa et al., 2006; considerations of the Late Paleocene in the northernmost Andes as con- Iglesias et al., 2007 ; Wilf et al., 2009 ; Gandolfo et al., 2011 ). strained by Paleocene rocks in the Cerrejó n coal mine. In Proceedings of the Tercera Convenció n Té cnica de la Asociació n Colombiana de (4) Caribbean exchange — Menispermaceae was also pres- Geó logos y Geofí sicos de el Petró leo, Bogotá , Colombia; Memorias ent in mid-latitude North America at about the same time as the [lecture]. Bayona , G. , C. Montes , A. Cardona , C. Jaramillo , G. Ojeda, V. Valencia, deposition of the Colombian endocarps. Examples include cf. and C. Ayala . 2010. Intraplate subsidence and basin fi lling adjacent to Canticocculus Chandler from the upper Paleocene of North an oceanic arc-continent collision: A case from the southern Caribbean – Dakota, United States ( Crane et al., 1990 ), and the aforementioned South America plate margin. Basin Research 10.1111/j.1365-2117. specimen of Palaeoluna from the middle-late Paleocene of the 2010.00495.x . Fort Union Formation, Wyoming (Fig. 17). The morphological Bhandari , S. , A. Momohara , and K. N. Paudayal . 2009 . Late similarity between the latter specimen and those of Palaeoluna Pleistocene plant macro-fossils from the Gokarna Formation of the bogotensis is striking and suggests that phytogeographic ex- Kathmandu Valley, Central Nepal. Bulletin of the Department of change occurred between these two regions during or perhaps Geology, Tribhuvan University, Kathmandu, Nepal 12 : 75 – 88 . immediately prior to the middle-late Paleocene. This phytogeo- Buchs , D. M. , R. J. Arculus , P. O. Baumgartner , and A. Ulianov . graphic exchange could have been favored when the Caribbean 2011 . Oceanic intraplate volcanoes exposed: Example from sea- volcanic arc briefl y connected South and North America during mounts accreted in Panama. Geology 39 : 335 – 338 . the Paleocene ( Fig. 52 ; Bayona et al., 2010 ; Cardona et al., Cardona , A. , V. A. Valencia , G. Bayona , J. Duque , M. Ducea , G. Gehrels , C. Jaramillo , et al . 2010 . Early-subduction-related orogeny in the 2010 ; Buchs et al., 2011 ). Palaeoluna is placed within the ex- northern Andes: Turonian to Eocene magmatic and provenance record tant S - C - C clade (Fig. 50), and it shows close similarity to ex- in the Santa Marta Massif and Rancheria Basin, northern Colombia. tant Cissampelos ; this modern genus has a very widespread Terra Nova 10.1111/j.1365-3121.2010.00979.x . distribution ranging from North America, the neotropics, Af- Carvalho , M. R. , F. A. Herrera , C. A. Jaramillo , S. L. Wing , and R. rica, and Australasia (Fig. 51). If Palaeoluna represents the an- Callejas . 2011 . Paleocene Malvaceae from Northern South America cestor of Cissampelos , South and North America rise as and their biogeographical implications. American Journal of Botany candidates for the ancestral area of this lineage. 98 : 1337 – 1355 . As yet, the place of origin of the Menispermaceae remains Chandler , M. E. J. 1961 . The lower tertiary fl oras of southern England I. uncertain, although Thanikaimoni (1984 , 1986 ) suggested the Paleocene fl oras. In London Clay fl ora (supplement). British Museum Cretaceous lowland forests of Africa. Interestingly, Cretaceous (Natural History), London, UK. fossil records for Menispermaceae remain unsubstantiated. The Chesters , K. I. M. 1957 . The Miocene fl ora of Rusinga Island, Lake fossil genus Prototinomiscium Knobloch and Mai (Knobloch Victoria. Kenya. Palaeontographica, B 101 : 30 – 71 . and Mai, 1986 ) from the upper Cretaceous of Europe has been Collinson , M. E. , S. R. Manchester , and V. Wilde. 2011 . Fossil fruits and seeds of the Middle Eocene Messel biota, Germany. Abhandlungen uncritically accepted as a valid record of Menispermaceae for der Senckenberg Gesellschaft für Naturforschung . In press. molecular dating analyses (e.g., Anderson et al., 2005), although Crane , P. R. , S. R. Manchester , and D. L. Dilcher . 1990 . A preliminary the endocarp fossil shows a surface cell pattern unlike any known survey of fossil leaves and well-preserved reproductive structures for the family. In our opinion, the assignment of this fossil to from the Sentinel Butte Formation (Paleocene) near Almont, North Menispermaceae is dubious. Also, many fossil leaves called Dakota. Fieldian a , Geology 20 : 1 – 63 . Menispermites from Cretaceous fl oras of North America and Diels , L. 1910 . Menispermaceae. In A. 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Appendix 1. Extant species of Menispermaceae photographed and analyzed for endocarp morphology.

Species name Herbarium no. Region Altitude (m a.s.l.)

Antizoma calcarifera Miers US1991350 South Africa — Cissampelos andromorpha DC. Coll. Fernandez, A. US1997934 Colombia — Cissampelos andromorpha DC. Coll. Mexia, Y. BARC13596 Ecuador — Cissampelos andromorpha DC. Det. Barneny, R. US2575572 Suriname 350 Cissampelos fasciculata Bentham. Coll. Maxon, W. US1181670 Costa Rica 1600 Cissampelos grandifolia Tr & Pl. Coll. Mexia, Y. US1663781 Ecuador 650 Cissampelos grandifolia Tr & Pl. Coll. Skutch A US1642714 Costa Rica 1040 Cissampelos pareira L. Coll. Cook, F. & Griggs, R. US407831 Guatemala — Cissampelos pareira L. Coll. George, P. BARC G011 Guatemala — Cissampelos pareira L. Coll. Morales, J. F2742 Costa Rica — Cissampelos tropaeolifolia DC. Coll. Mexia, Y. & Yaveo, T. BARC130993 Mexico — Cissampelos tropaeolifolia DC. Coll. Encarnaci ó n, F. US3011876 Peru — Cocculus carolinus L. (DC). BARC19889 US — Cocculus hirsutus Diels L. Coll. Barakrishnan, A. US2686633 Sri Lanka — Cyclea atjehensis Forman. Coll. Maxwell, J. A(90-33) Thailand — Cyclea hypoglauca (Schauer) Diels. Coll. Tsui, T.M. US1754790 China — Cyclea hypoglauca Diels. Coll. Tsui, T.M. BARC652 China — Cyclea peltata Diels. Coll. Saldanha C.J. US2616394 India — Cyclea polypetala Dunn. Coll. Henry, A. US458824 China — Cyclea racemosa Oliv. Chow, H. A(663) China — Dioscoreophyllum cumminsii (Stapf) Diels. BARC1970 Nigeria — Diploclisia affi nis Diels. Coll. Wilson, E.H. US599510 China — Diploclisia glaucescens (Blume) Diels. Coll. Chan, K. A(1501) Hong Kong — Jateorhiza macrantha Hooker. Coll. Fernandez, C. US3264726 Equatorial Guinea 240 Limaciopsis loangensis Engl, Coll. Louis, J. BARC7750 Belgian Congo — Menispermum canadense L. Coll. Harrisonburg. BARC94 DR US — Menispermum canadense L. Coll. Rhodes, D. US371274 US — Menispermum canadense L. Coll. Sylvester, C. UWM15599 US — Menispermum dauricum DC. BARC061791 — — Menispermum dauricum DC. Coll. Dorsett, M. BARC89750 China — Pericampylus glaucus (Lam.) Merr. Coll. Maxwell, J. A(96-662) Thailand — Pericampylus glaucus (Lam.) Merr. Coll. Wang, C. US1670049 China — Pericampylus incanus Lamk (Merr). Coll. Merril, E. & McC., F. BARC20102 — — Sinomenium acutum (Thunb.) Reh. & Wi. Coll. Bo. D. & Bart, B. A(24889) China — Sinomenium acutum (Thunb.) Rehder & Wilson. Coll. Lee, C. US1990264 China — Sinomenium acutum R. & W. Coll. Yat-Sen, C. & Szechwan. BARC114802 China — Stephania brevipes Craib. Coll. Maxwell, J. A(96-895) Thailand — Stephania capitata (Blume) Spreng. Coll. King. BARC5239 Malay Peninsula — Stephania delavayi Diels. Coll. Wilson, E.H. US599329 China 200 Stephania epigaea H.S Lo. Coll. Bartholomew, B. US3043598 China — Stephania hernandiifolia (Willd.) Walp. Coll. Huq. A. US3345848 Bangladesh — Stephania japonica (Thunb) Miers. Coll. Hartley, T. US3461000 New Guinea 1220 Stephania japonica (Thunb) Miers. Coll. Schodde, R. A(3485) Australia — Stephania rotunda Lour. Coll. SPI. BARC47804 India — Stephania rotunda Lour. Cur. Bot. Gard. Darjeeling. BARC94085 India — Tiliacora acuminata (Lam.) Miers. Coll. Jayasuriya, M. US2721394 Sri Lanka — Although we studied 68 of the 71 extant genera, we only include here those for which the mesocarp tissue was removed to reveal endocarp characters. Herbarium acronyms follow Index Herbariorium ( http://sweetgum.nybg.org/ih/ ). Specimens from A include collector number in parentheses. 2016 American Journal of Botany [Vol. 98

Appendix 2. List of morphological characters and states.

1. Endocarp type: horseshoe-shaped (0); straight (1); hairpin-shaped (2); reniform (3). 2. Endocarp Length (mm): small ( < 10 mm) (0); large ( > 10 mm) (1). 3. Endocarp wall thick: yes ( > 1 mm) (0); no ( < 1 mm) (1). 4. Outline endocarp shape: obovate (0); ovate (1); elliptic (2); rounded (3); other (4). 5. Dorsal crest no.: 0 (0); 1 (1); 2 (2); ≥ 3 (3). 6. Lateral crest no.: 0 (0); 1 (1); 2 (2); ≥ 3 (3). 7. One dorsal crest broader: yes (0); no (1). 8. Spiny dorsal crest a : yes (0); no (1). 9. Spiny lateral crest a : yes (0); no (1). 10. Vascular tube course b : enters ventrally (0); enters laterally (1). 11. Locule chamber position: apical (0); central (1); basal (2); along endocarp exterior (3). 12. One limb noticeably longer: yes (0); no (1). 13. Locule ribs conspicuous: yes (0); no (1). 14. Ventral notch straight c : yes (0); no (1). 15. Perforation present d : yes (0); no (1). 16. Basal sculpturing e : yes (0); no (1). 17. Locule inner protrusions: yes (0); no (1). 18. Arborescent habit: liana or herbaceous vine (0); shrub or tree (1). 19. Leaf venation: pinnate (0); actinodromous (1); acrodromous (2). 20. Leaf peltate: yes (0); no (1). 21. Leaf lobed: yes (0); no (1). 22. Endosperm present: yes (0); no (1). 23. Endosperm ruminate: yes (0); no (1). 24. Stamen fusion: all stamens free (0); fi laments fused-anthers free (1); some stamens fused-others free (2); fusion of all stamens, anthers at least partially fused and forming a ring-like structure (3). 25. Pollen type: tricolpate (0); tricolporate (1); triporate (2); inaperturate (3). a Characters 8, 9. Spines are defi ned here as a type of ornamentation that exceed or extend beyond the dorsal or lateral crests. b Character 10. Vascular tube course: direction of entry of the vascular tube into the locule; for example, in Stephania , the vascular tube enters ventrally ( Fig. 20 ), appearing as a straight tube. On the other hand, a lateral vascular tube enters the seed chamber/locule with some curvature either laterally or sublaterally; see Menispermum ( Fig. 44 ). c Character 14. Ventral notch straight: lower ventral line of the endocarp that does not present any indentation or curvature ( Fig. 28 ). d Character 15. Defi ned as a complete perforation of the endocarp. This character is different from lateral apertures which are openings that do not completely traverse the endocarp. e Character 16. Basal sculpturing. This character refers to basal concavities (observed on inner faces of the endocarp) and/or convex sculpturing (observed on outer faces of the endocarp). Because of the uncertainty of the presence of either one of these characters in the fossil genus Menispina Herrera gen. nov. we have scored and combined them as basal sculpturing. Characters in boldface are also presented in Fig. 49 . December 2011] Herrera et al. — Fossil endocarps of Menispermaceae from South America 2017 . cters: . . . . 1011/200111 — — 11111110100122 — — — 30111111111010 — 001000111 1011/200111 001311100131111010100/11001 00131110/1113011101010/111001 001311011130/1110/1110/1000/11001 00010220/10000/30000/11101101031 0000101101000000011???????? 1 0000001100??100?110???????? 0/3 0/1 0 1/2 0/3 1 1 2 0/2/3 0/1 2 1 0/1 0 1 0/1 0 0 0 0/3 0 0 0 0 0 0 0/3 ? 0 0 1/2 0/1 0 1 1 0 0 1 0/1 0 0 1 1 1 1 0 1 0 1 0 1 ? 0/1 1 ? 0 0 ? 1 3 ? 0 2 ? 3 ? 1 ? ? 110200? — — 01 — — — — 1110001100 — — — — 01 — — 110200? 21101101113100/111001001001 001322000001011010100100/11 01031001 — 00/113100111311111100/1001001 1311011101001?01 — 01031001 010311011110111111200??10 1/3 0/1 0/1 3 0/1 0 10/2 0/1 1 1 — 2/3 ? 0/1 1/3 0/1/2 0/1 — 1 — — 1 — 0/1 1/3 1 0/1 1 1 0 0/1 0/1 0/1 0 1 0/1 1 1 0/1 0/1/2 0/1 0/1/2 0 1/2 0/1 0/1 0 0 1 0/2/3 0/10/2/3 0/1 0/1 2/3 1 0/1 2/3 0/1/2 0/1 0/1 0/1 0 0/1 0 0/1 1/3 1 0/1 — 0/1 1 0/1 — 3 1 0/1 1 1 0/1 0 1 0/1/2 0 1 0 1 0/1 0 1 0 0/1 0/1/3 0 0 0 ? 0 1 0/1/2 0/1 1 2/3 0/1/2 0/1/2 0/1 0/1 0/1 0 0/1/3 0/1 — 0/1 1 1 1 0/1 0/1/2 0/1 0 1 0/1 0/1 1

† †

† etc.

etc. appears paraphyletic. etc.

etc.

3. Taxa and matrix of morphological characters (1 – 25, described in Appendix 2). 25, described in – and matrix of morphological characters (1 Taxa 3.

*

Parabaena, Tinomiscium, Borismene, Fibraurea, Penianthus, Dioscoreophyllum, Tinospora, Chasmanthera, Odontocarya, Syntriandrium Chasmanthera, Tinospora, Dioscoreophyllum, Penianthus, Fibraurea, Borismene, Tinomiscium, Parabaena, Calycocarpum, Coscinium, Anamirta, Arcangelisia Sarcopetalum, Abuta, Orthomene, Legnephora, Parapachygone Legnephora, Orthomene, Abuta, Sarcopetalum, Haematocarpus, Cocculus, Hyperbaena Sciadotenia Curarea, Chondrodendron, Carronia, Triclisia, Albertisia, Tiliacora, Pycnarrhena, Cocculus taxa. Fossil

• Complete list of genera for backbone constraint and strict consensus trees (Figs. 49 50), matrix morphological chara • * † • • • Appendix Taxon sagittifolia Sagittaria Fumaria indica Sinomenium Menispermum Calycocarpum 1 2 3 Haematocarpus 4 5 Cyclea Cissampelos 6 Stephania palaeosudamericana Menispina evidens 7 bogotensis Palaeoluna 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 Parabaena Parabaena etc. Burasaia 1 Pycnarrhena 0/1 Pachygone 1 Stephania 2/3 0/1/2 0/1/3 1 0/1 — ? 1 — — — — 1 1 0/1 0/1 0 0/1 0/1 0/1 0/1/3 0/1/2 Diploclisia Pericampylus Sarcopetalum Hypserpa Limacia Strychnopsis Cocculus