Icacinaceae from the eocene of Western North America.

AJB Advance Article published on May 21, 2015, as 10.3732/ajb.1400550. The latest version is at http://www.amjbot.org/cgi/doi/10.3732/ajb.1400550 RESEARCH ARTICLE

A M E R I C A N J O U R N A L O F B OTA N Y

ICACINACEAE FROM THE EOCENE OF WESTERN NORTH AMERICA1 SARAH E. ALLEN2,3, GREGORY W. STULL2–4, AND STEVEN R. MANCHESTER3 2Department

of Biology, University of Florida, P.O. Box 118525, Gainesville, Florida 32611 USA; and 3Florida Museum of Natural History, P.O. Box 117800, University of Florida, Gainesville, Florida 32611-7800 USA

• Premise of the study: The Icacinaceae are a pantropical family of trees, shrubs, and climbers with an extensive Paleogene fossil record. Our improved understanding of phylogenetic relationships within the family provides an excellent context for investigating new fossil fruit and leaf material from the Eocene of western North America. • Methods: We examined fossils from early and middle Eocene sediments of western Wyoming, northeastern Utah, northwestern Colorado, and Oregon and compared them with extant species of Iodes and other icacinaceous genera as well as previously described fossils of the family. • Key results: Three new fossil species are described, including two based on endocarps (Iodes occidentalis sp. nov. and Icacinicaryites lottii sp. nov.) and one based on leaves (Goweria bluerimensis sp. nov.). The co-occurrence of I. occidentalis and G. bluerimensis suggests these might represent detached organs of a single species. A new genus, Biceratocarpum, is also established for morphologically distinct fossil fruits of Icacinaceae previously placed in Carpolithus. Biceratocarpum brownii gen. et comb. nov. resembles the London Clay species “Iodes” corniculata in possessing a pair of subapical protrusions. • Conclusions: These fossils increase our knowledge of Icacinaceae in the Paleogene of North America and highlight the importance of the Northern Hemisphere in the early diversification of the family. They also document interchange with the Eocene flora of Europe and biogeographic connections with modern floras of Africa and Asia, where Icacinaceae are diverse today. The present-day restriction of this family to tropical regions offers ecological implications for the Eocene floras in which they occur. Key words: paleotropics.

Biceratocarpum; endocarp; Eocene; fossil; Goweria; Icacinaceae; Icacinicaryites; Iodes; North America;

1 Manuscript received 16 December 2014; revision accepted 16 April 2015. The authors thank J. Barkley, S. Casebolt, T. Lott, and others who assisted with fieldwork at the Blue Rim and Kisinger Lakes sites. J. Landeen is gratefully acknowledged for donating many of the Blue Rim specimens. S. L. Wing and K. R. Johnson provided access to specimens studied at the USNM and the Denver Museum of Nature and Science. M. E. Collinson provided comparative data on related fossils from the London Clay flora. We also thank the herbarium collection managers at Wageningen, Leiden, and especially J. Solomon at the Missouri Botanical Garden for facilitating study of extant material. H. Wang provided careful curation of the FLMNH specimens. Thank you to N. Stull for creating the diagrammatic reconstruction of Biceratocarpum brownii, C. S. Hoyuelos and F. Herrera who provided beam time and guidance at the Advanced Photon Source, Argonne National Laboratory, for x-ray tomography of an extant Iodes fruit, and three anonymous reviewers who provided helpful suggestions on an earlier version of the manuscript. This work was supported by funds from the Ellis L. Yochelson Award of the Paleontological Society and the Riewald-Olowo Memorial Fund from the University of Florida Department of Biology to G.W.S. and from the Evolving Earth Foundation, the Paleontological Society, the University of Florida Department of Biology, and NSF award DEB-1404895 to S.E.A. and EAR 0174295 and EAR 1338285 to S.R.M. 4 Author for correspondence (e-mail: [email protected])

doi:10.3732/ajb.1400550

The early and middle Eocene biota of western Wyoming, partially treated in studies by Lesquereux (1878, 1883), Newberry (1898), Berry (1930), Brown (1929, 1934, 1937), MacGinitie (1974), and Wilf (2000), is characterized by some of its more common floristic elements, including Macginitiea wyomingensis (MacGinitie) Manchester (Platanaceae), Populus cinnamomoides (Lesquereux) MacGinitie (Salicaceae), Cedrelospermum nervosum (Newberry) Manchester (Ulmaceae), and abundant Lygodium kaulfussii Heer (Schizaeaceae). However, many accessory elements of the flora remain poorly known and/ or misidentified. New investigations of the Bridger Formation flora of southwestern Wyoming, in comparison with the previously studied Kisinger Lakes flora of the Aycross Formation in northwestern Wyoming (MacGinitie, 1974), are aimed at a better understanding of the floristic affinities of the biota, which includes a mixture of extinct and extant genera. The Icacinaceae Miers represent a biogeographically and ecologically significant component of the flora, given the family’s present-day confinement to tropical forests. The Icacinaceae are a pantropical family of woody trees, shrubs, and climbers including ca. 34 genera and 200 species, as currently circumscribed (APG III, 2009; Byng et al., 2014), although this likely does not represent a monophyletic assemblage (Kårehed,

American Journal of Botany 102(5): 1–20, 2015; http://www.amjbot.org/ © 2015 Botanical Society of America

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2001; Stevens, 2001 onward; Byng et al., 2014). The family is phylogenetically positioned near the base of the lamiid clade (Kårehed, 2001; Soltis et al., 2011; Refulio-Rodriguez and Olmstead, 2014), close to Garryales, Oncotheca Baill., and Metteniusa Karsten. Traditionally, the family (Icacinaceae s.l.) included around 54 genera and 400 species, which were organized by different authors into either tribes (Icacineae, Iodeae, Phytocreneae, and Sarcostigmateae; Engler, 1893) or informal groups (Bailey and Howard, 1941a, b) based largely on stem and wood anatomical features. Multiple phylogenetic studies (Savolainen et al., 2000; Soltis et al., 2000; Kårehed, 2001) have shown this traditional circumscription to be highly polyphyletic; consequently, approximately 20 genera, from the Icacineae tribe of Engler (1893), or groups I and II of Bailey and Howard (1941b), were removed from the family and transferred to the campanulid families Cardiopteridaceae Blume (Aquifoliales), Pennantiaceae J. Agardh (Apiales), and Stemonuraceae Kårehed (Aquifoliales). Recent analyses based on ca. 73 plastid genes indicate that additional genera (e.g., Apodytes E. Mey. ex Arn., Calatola Standl., Platea Blume, Emmotum Desv.) should be removed from the family and included within a broader circumscription of Metteniusaceae H. Karst. ex Schnizl. (G. W. Stull et al., unpublished manuscript). The remaining 23 genera, including all genera of the traditional Iodeae, Phytocreneae, and Sarcostigmateae tribes, and some genera of the Icacineae (e.g., Cassinopsis Sond., Icacina A. Juss, and Mappia Jacq.), constitute the Icacinaceae s.s. (G. W. Stull et al., unpublished manuscript), which corresponds approximately to the Icacina group of Kårehed (2001). Although the monophyly of the constituent genera has not been investigated comprehensively, recent analyses show that the monotypic genus Polyporandra Becc. is nested within Iodes Blume, and that the genera Polycephalium Engl. and Chlamydocarya Baill. are nested within Pyrenacantha Wight (Byng et al., 2014). The Icacinaceae s.s. have a rich fossil record, primarily from the Paleogene of North America and Europe, although new fossil evidence from South America (Stull et al., 2012), Africa (Manchester and Tiffney, 1993), and Asia (endocarp from the Miocene Wenshan flora of southeastern Yunnan, China; specimen in XTBG collection of Zhekun Zhou) has been emerging. The fossil record of the family consists primarily of endocarps (drupaceous fruits characterize the family). The endocarps are woody, unilocular, lenticular to globose in cross section, and contain a single seed, as only one of the two apical ovules present in each ovary matures (Kårehed, 2001). The ovules are supplied by a vascular bundle that generally runs along one margin of the fruit (usually in the mesocarp) and passes through the endocarp to the locule subapically, below the stylar canal (Reid and Chandler, 1933; Howard, 1942). In the older literature (Reid and Chandler, 1933; Howard, 1942), the main vascular bundle of icacinaceous fruits is referred to, perhaps incorrectly, as a funicle, a term typically used to specifically denote the stalk connecting an ovule to the placenta (Eames, 1961). The overall morphology and surface sculpture of the endocarp vary within the family and, in combination with other internal morphological features, often are useful for recognizing particular genera or putative clades in the fossil record (Stull et al., 2012). The modern genus Iodes (including Polyporandra), for example, is unique within the family in having the marginal/main vascular bundle embedded within the endocarp wall, in addition to having a reticulately ridged endocarp surface (Fig. 1). We describe fossils of Icacinaceae from the Eocene of Wyoming, Utah, Colorado, and Oregon representing three species based on fruits and one based on leaves. Biceratocarpum brownii gen. et comb. nov. accommodates endocarp compressions/

impressions, casts, and molds with distinctive subapical hornlike structures from the early–middle Eocene Aycross and Bridger Formations, the Clarno Formation, and the Parachute Creek Member of the Green River Formation. Icacinicaryites lottii sp. nov. is based on endocarp compressions/impressions from the Aycross Formation of northwestern Wyoming. Iodes occidentalis sp. nov. is based on endocarp compressions/impressions from the early–middle Eocene Bridger Formation and the Laney Member of the Green River Formation of southwestern Wyoming and rare, similarly preserved specimens from the Parachute Creek Member of the Green River Formation in northwestern Colorado. Finally, we describe fossil leaves from the Bridger Formation with affinities to Iodes that co-occur at multiple localities with Iodes occidentalis, suggesting that they might belong to the same taxon. However, because numerous other angiosperm groups show leaf architecture similar to Iodes, we describe the leaves as a new species of Goweria Wolfe (G. bluerimensis sp. nov.), a fossil leaf genus attributed to Icacinaceae but with uncertain intrafamilial affinities. We discuss the systematic implications of these fossils and call attention to logical issues surrounding the placement of fossils within the traditional Iodeae tribe, which is likely polyphyletic and defined mainly on plesiomorphic fruit characters. We also discuss the biogeographic significance of the fossils in the context of the broader fossil and modern distribution of the family, focusing in particular on Iodes, which today is restricted to tropical forests of Africa, Madagascar, and Indo-Malesia, and Biceratocarpum brownii, which shows strong morphological similarity to the Eocene London Clay taxon “Iodes” corniculata Reid & Chandler. MATERIALS AND METHODS The fossils examined for this work derive mainly from four Eocene outcrop areas in western Wyoming (Fig. 2). Most specimens (fruits and leaves) were found at sites along the Blue Rim escarpment in southwestern Wyoming (UF localities 15761, 15761N, 15761S, 18288, 19031, 19032, 19225, 19225N, 19337, and 19338). The Blue Rim sites are situated in the lower part of the Bridger Formation (Kistner, 1973; Allen, 2011), representing mostly fluvial and lacustrine environments, and are estimated to be ~49.5 Myr old. Other fruits were collected from the Aycross Formation, from localities constituting the Kisinger Lakes flora of MacGinitie (1974), in northwestern Wyoming (USGS loc. D3532A-D, UCMP loc. PA108 [A], PA121 [B]; UF localities 19376, 19377). This flora is preserved in fluvial to floodplain environments and is estimated to be ~48.5 Myr old. Specimens were also studied from the Tipperary site, investigated by Berry (1930) and MacGinitie (1974; USGS loc. 8785, UCMP PA110). We also collected from the Barrel Springs localities in the Laney Member of the Green River Formation, in southern Wyoming (UF localities 18151, 19335). Other specimens were found in collections from the Parachute Creek Member of the Green River Formation in northwestern Colorado (UF loc. 00582, DMNH loc. 317 and USNM loc. 41142) and near Bonanza, Utah (UF loc. 00583). Specimens from the Clarno Nut Beds site in the Clarno Formation in Wheeler County, Oregon, were also examined (UF loc. 00225). The leaves and fruits were recovered by splitting shales and siltstones in the field with additional fine preparation in the laboratory to expose them more fully. Fossil leaves were photographed with a Nikon D300 camera. Fruits (both macro and close-ups) were photographed with a Canon EOS Digital Rebel XSi camera. Measurements of morphological characters were done by hand or using the program ImageJ (Rasband, 1997–2015). The density of papillae on the fossil and modern fruits was assessed from light microscopy images of the specimens by counting them in the program Adobe Photoshop (San Jose, California, USA), and calculating the distance between adjacent papillae with ImageJ. Herbarium specimens examined for comparison are listed in Appendices 1 and 2. Fossil and modern leaves were described using the terminology described in the Manual of Leaf Architecture (Ellis et al., 2009). The cleared leaves figured for comparison are from the National Cleared Leaf Collection (NCLC) housed at the Smithsonian Museum of Natural History in Washington, D.C.

ALLEN ET AL.—ICACINACEAE FROM THE EOCENE

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Fig. 1. Extant Iodes fruits for comparison with the fossil specimens. (A–D) Iodes klaineana Pierre, Wilde 606 from Gabon. (A) Lateral view showing reticulum of ridges and pubescence. (B) Dorsal view showing prominent keel. (C) Apical view with remnant stigma. (D) Basal view with persistent calyx. (E, F) Iodes cf. madagascariensis Baill, McPherson 18809 from Madagascar. (E) Lateral view with reticulum of ridges. Keel is visible on the left side of the fruit. (F) Dorsal view showing prominent keel. (G) Iodes klaineana Pierre, A. Leonard 154, from Yangambi, Congo, showing prominent vascular bundle within endocarp (arrow). (H) Iodes africana Welw. ex Oliv., Breteler et al., 8231, x-ray section, transverse through the apical 1/4 of the fruit. Vascular bundle within the endocarp indicated with an arrow. Scale bar = 1 mm. (I) Natsiatum herpeticum Buch.-Ham. ex Arn., A.J.C. Grierson & D. G. Long 3775, Bhutan Cross section with arrow indicating vascular bundle in mesocarp rather than endocarp. Scale bars = 5 mm (all except H).

SYSTEMATICS AND RESULTS Family— Icacinaceae Miers 1851. Genus— Biceratocarpum Stull, S.E. Allen, & Manchester, gen. nov.

Diagnosis— Endocarp ellipsoidal in lateral view, lenticular in cross section, unilocular, bivalved. Outer endocarp surface with a reticulum of ridges delimiting polygonal areoles with few or no freely ending ridgelets. Endocarp possessing an eccentric, subapical pair of horn-like protrusions, with one on either face of the endocarp surface.


Type locality— Tipperary flora, Wyoming (USGS loc. 8785). Additional localities—Kisinger Lakes, Wyoming; Blue Rim, Wyoming; Bonanza, Utah; Clarno Nut Beds, Oregon; Douglas Pass, Colorado. Additional specimens— UF 19376-59511, 59512, 59513 (Kisinger Lakes); UF 19225-54569, 54562 (Blue Rim); UF 00583-61314 (Bonanza); UF 00225-6458, 9902 (Clarno Nut Beds); DMNH 317-35557 (Douglas Pass).

Fig. 2. Map showing the fossil localities referenced in the text. Relevant Icacinaceae specimens have been found at the Clarno Nut Beds (NB) locality in Oregon; Kisinger Lakes (KL), Tipperary (TP), Blue Rim (BR), and Barrel Springs (BS) localities in Wyoming; Bonanza, Utah (BZ); and Douglas Pass, Colorado (DP). Base map generated and sites plotted via Map-it (http://woodshole. er.usgs.gov/mapit/).

Etymology— The genus name Biceratocarpum means fruit with two horns (based on the Latin components bi- = two, cerato- = horn, and -carpum = fruit), and refers to the distinct pair of horn-like protrusions shown by the fossils. Species— Biceratocarpum brownii (Berry) Stull, S.E. Allen, & Manchester, comb. nov. Basionym— Carpolithus browni Berry 1930, USGS Prof. Paper 165-B, pp. 78–79, pl. 14, fig. 1. The original specific epithet, browni, was indicated with one “i” at the end. However, we have emended this to brownii following the practice that if a name ending in a consonant is used for a specific epithet, “ii” should be used (Stearn, 2004). Emended diagnosis— Endocarp ellipsoidal in lateral view, lenticular in cross section, 7.5–9.5 mm long, 5–7.5 mm wide, unilocular, bivalved. Outer surface covered with a reticulum of ridges delimiting polygonal areoles (ca. 20–25 total) with few or no freely ending ridgelets. Course of the marginal vascular bundle embedded in the endocarp wall. Endocarp possessing a symmetrical pair of horn-like protrusions, positioned eccentrically and subapically on the outer endocarp faces, each apparently accommodating a central channel. Inner endocarp surface showing shallow mounds corresponding to areoles/depressions of outer endocarp reticulum. Inner endocarp surface densely covered with regularly spaced, minute papillae; papillae average 0.03 mm apart (from 10 measurements done at random from punctae of the locule cast from specimen USNM 316745). Endocarp wall 0.3–0.4 mm thick (cellular detail not preserved as the wall is generally coalified). Holotype— USNM 316745 (pl. 14, fig. 1 in Berry, 1930; Figs. 3D, E, 4A in present article).

Discussion—This species was originally described from a single piece of shale bearing two endocarp specimens, one of them a locule cast showing the papillae, and the other a compression fossil showing the external features of the endocarp (Fig. 3D, E). Our diagnosis expands on that of Berry (1930) to include additional features we observed in the holotype and provides a size range based on subsequently recognized specimens. The type collection from Tipperary has been augmented with a few additional new impression specimens from the Kisinger Lakes flora (Fig. 3G), which is considered to be contemporaneous (MacGinitie, 1974), and from the middle Eocene Parachute Creek Member of the Green River Formation. We also discovered two previously collected specimens from the middle Eocene Clarno Nut Beds belonging to this taxon, both of which document the position of the vascular bundle within the endocarp wall and show a pair of apical protrusions. One specimen (UF 00225-6458) was previously figured by Manchester (1994: pl. 17, figs. 3, 4) but misidentified as Iodes multireticulata Reid & Chandler. The other specimen (UF 00225-9902) is newly figured here (Figs. 3A, B). We prepared a line drawing based on the specimens cited to more clearly present our interpretation of the morphological features shown by this taxon (Fig. 5). Biceratocarpum brownii possesses numerous characters commonly found in endocarps of Icacinaceae: a single locule, a bivalved construction with a reticulum of ridges covering the two endocarp faces, an asymmetrical apex, and (as in some extant genera) a papillate lining on the inner endocarp surface (Fig. 4A). We considered other fossil and extant icacinaceous genera that might accommodate this species—however, the combination of characters exhibited by this fossil precludes placement in any of them. While Hosiea Hemsl. & E.H. Wilson, Iodes, and Miquelia Meisn. all possess (at least in certain species) papillae on the inner endocarp walls, B. brownii differs from these genera by the presence of a pair of horn-like protrusions near the apex of the endocarp, with one on each of the two valves and thus visible in both counterparts of laterally preserved impression specimens (Fig. 3). On impression specimens, the horns appear as depressions, sometimes containing infillings of the channels within the horns (e.g., Fig. 3B, C). These structures possibly represent the point of entry of two vascular bundles into the locule (supplying the two apical ovules characteristic of icacinaceous fruits), although this species also has a marginal vascular bundle similar to other genera of Icacinaceae (Fig. 3A). It is therefore difficult to assess the possible functions of these protuberances, especially since there do not appear to be any homologous structures in modern fruits of Icacinaceae from which to draw inferences. The extant genus Phytocrene Wall. possesses a pair of endocarp channels, but these are more central and apically positioned, and they are not enveloped within protuberances as in Biceratocarpum (Fig. 6).


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Fig. 3. Fruits of Biceratocarpum brownii gen. et comb. nov. (A, B) Two counterpart halves of an endocarp mold from the Clarno Nut Beds, Oregon, UF 002259902. (A) Blue arrow highlights an infilling of the bottom portion of the vascular canal, which presumably ran within the endocarp wall from the base to the apex, where it entered the locule to supply the ovules. (B) Blue arrows highlight the subapical horns. (C) Impression specimen of this species from Blue Rim, Wyoming, UF 19225-54569. (D) Lectotype, designated here, of Biceratocarpum brownii, comb. nov., USNM 316745a from Tipperary flora, Wyoming. Note the horn toward the apex of the fruit and the absence of freely ending ridges penetrating the areoles on this mold of the endocarp surface. (E) A second specimen, a locule cast, from the same hand sample as the Lectotype, USNM 316745b. (F) Endocarp impression with shadowed protrusion of horn into the sediment indicated by arrow. From the Parachute Creek Member of the Green River Formation, Colorado, USNM 57250 (USNM loc. 41142). (G) Impression of endocarp with horn indicated by arrow, Kisinger Lakes flora, UF 19376-59511. Scale bars = 5 mm.

Furthermore, Phytocrene does not possess a prominent vascular bundle within the endocarp wall. Although the endocarp is missing from the specimen in Fig. 3A, the specimen does show an infilling of the vascular canal positioned within the groove left by the marginal endocarp ridge, indicating that the vascular bundle traveled through the endocarp wall. Given that the vascular bundle is embedded within the endocarp wall, it seems likely that this species is closely related to Iodes. However, as mentioned already, no extant members of Iodes possess subapical protrusions. Additionally, B. brownii is distinct in having well-defined areoles in the endocarp reticulation with few or no freely ending ridgelets. Iodes and other genera in the family with ridged endocarps (e.g., Alsodeiopsis Oliv., Desmostachys Miers., Natsiatum Buch.-Ham. ex Arn., and Rhyticaryum Becc.) usually have at

least a few freely ending ridgelets penetrating the areoles, or a more diffuse ridging pattern without well-defined areoles. Given these distinct attributes, the recognition of a new genus, perhaps related to Iodes, is warranted: Biceratocarpum. This fossil species was widespread, with occurrences at Kisinger Lakes (WY), Tipperary (WY), Blue Rim (WY), Bonanza (UT), Douglas Pass (CO), and Clarno (OR). At Blue Rim, it is known from only a few specimens, in contrast to the abundant endocarps of Iodes occidentalis (described below). At first, we compared Biceratocarpum brownii with specimens of I. occidentalis from Blue Rim to determine whether they might be conspecific, as both are reticulately ridged and have a similarly papillate locule cast. On close inspection, however, a number of differences became apparent. Iodes occidentalis appears to have had more inflated, subglobose endocarps, allowing them to orient in various ways in the


Fig. 4. Papillae of fossil and modern specimens of Icacinaceae. (A–C) Close up of papillae impressions on the surface of locule casts. (A) Biceratocarpum brownii gen. et comb. nov., USNM 316745. (B) Iodes occidentalis sp. nov., UF 15761-22704. (C) Iodes occidentalis sp. nov., UF 19225-57243. (D) Papillae of extant Iodes cf. madagascarensis Baill., McPherson 18809, for comparison. Scale bars = 0.25 mm.

sediment, whereas B. brownii tends to lie flat in the bedding plane reflecting a preferred orientation due to the originally lenticular form of the fruit. Iodes occidentalis has a more complicated ridging pattern on the endocarp, with freely ending ridgelets entering

the areoles, unlike B. brownii. Furthermore, I. occidentalis lacks the pair of horns (one on each endocarp face) shown by B. brownii and instead has a single vascular strand running through the endocarp wall, consistent with the modern genus Iodes (Fig. 1).

Fig. 5. Drawing of Biceratocarpum brownii gen. et comb. nov. emphasizing features observed on fossils and described in text. (A) Lateral view. (B) Dorsal view.


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Etymology— The specific epithet is named for FLMNH paleobotany research assistant and laboratory manager Terry Lott, who collected these specimens in the summer of 2013.

Fig. 6. Phytocrene blancoi (Blanco) Merr., Elmer 15960, Luzon Island, Philippines, MO 833710. (A) Lateral view with arrow showing apical channel in the endocarp. (B) Side view with both apical channels indicated by arrows. Scale bars = 5 mm.

The main diagnostic character for this genus (the pair of horns) is not present in other fossil genera of Icacinaceae, such as Iodicarpa Manchester, Palaeohosiea Kvaček & Bůžek, or Croomiocarpon Stull, Manchester & Moore. However, the combination of characters shown by Biceratocarpum—i.e., reticulately ridged endocarps lacking or nearly lacking freely ending ridgelets, a pair of subapical horns on the endocarp, and papillae on the inner endocarp surface—are seen in the London Clay species described as “Iodes” corniculata by Reid and Chandler (1933). Although Biceratocarpum brownii differs from “Iodes” corniculata in having more numerous areoles on the endocarp surface (20–25 instead of 15–20) and a more densely papillate inner endocarp wall, they are otherwise very morphologically similar and share the unique feature of having a subapical pair of horns. These characters suggest close affinities between these taxa, and, upon further study of the London Clay taxon, perhaps calls for transfer of “Iodes” corniculata to Biceratocarpum. Should further study indicate that the London Clay and Wyoming fossils are conspecific, then the earlier published epithet, brownii, would take priority. Icacinicarya Reid and Chandler (1933) was established to accommodate fossils of Icacinaceae lacking clear affinities to any particular modern genus. Given that Icacinicarya was originally established based on permineralized material, Pigg et al. (2008) established Icacinicaryites to serve a similar function for fossils lacking the anatomical details necessary for a more precise generic assignment. We considered placing this species in the latter genus, but B. brownii is sufficiently preserved and morphologically distinct enough to warrant placement in a separate fossil genus. Genus— Icacinicaryites Pigg, Manchester & DeVore 2008. Species— Icacinicaryites lottii Stull, S.E. Allen, & Manchester, sp. nov. Diagnosis— Endocarp elliptical with a reticulum of ridges forming polygonal areoles with occasional freely ending ridgelets. Apex with a sessile and button-shaped stigma. Fruit subtended by a thick stalk. Holotype hic designatus— UF 19376-59514 (Fig. 7A). Type locality— Kisinger Lakes, Wyoming (UF loc. 19376). Paratype— UF 19376-59515 (Fig. 7B, C).

Description— Endocarp elliptical, 9.8–12.1 mm long, 8.7– 8.8 mm wide. Base and apex relatively symmetrical. Surface covered with a reticulum of ridges forming polygonal areoles (ca. 35 per endocarp face). Areoles penetrated by unbranched (or occasionally once-branched) freely ending ridgelets. Exocarp and mesocarp 0.9–1.1 mm thick, represented by a narrow, darkly stained layer surrounding the endocarp impressions/ compressions, with a sessile, button-shaped stigma evident at the apex. Stigma 1 mm wide. Fruit subtended by a thick stalk, ca. 1.1–1.7 mm wide and 3.3–4.3 mm long. Discussion—This species is represented by two specimens collected from the Kisinger Lakes flora in Fremont County, Wyoming. These fossils are unique in that the exterior portions of the fruit (as opposed to just the endocarp) are at least partially preserved. The endocarp compressions/impressions are surrounded by a dark band, interpreted as the exo/mesocarp, with a buttonlike structure positioned at the apex of the fruit, interpreted as a sessile stigma. At the base of the fruit is a broad, obliquely angled stalk extending down from the dark layer (i.e., exo- and mesocarp) encompassing the fruit (Fig. 7A–C). This stalk probably represents either a pedicel or a stipe, with at least three lines of evidence favoring the latter interpretation: One, this structure is unusually broad compared to the pedicels of modern taxa of Icacinaceae. Two, there is no indication of perianth at the junction of this structure with the rest of the fruit, which would be expected if this structure were indeed a pedicel. Instead, it appears to be continuous with the exocarp, perhaps with a nectar disc or perianth scar at its base (Fig. 7A). It is possible that the perianth could have been lost during fruit development, but the perianth is almost always persistent in mature fruits of Icacinaceae (G. W. Stull, personal observations, based on numerous herbarium specimens across all genera of the family). Three, the oblique orientation of the structure suggests a lack of rigidity, which is unusual for pedicels of Icacinaceae. Although stipes are rare in Icacinaceae, they do occur in species of several genera— e.g., multiple species of Pyrenacantha from Madagascar (e.g., Labat et al., 2006) and Miquelia caudata King (G. W. Stull, personal observations)—and these structures on the fossils resemble the stipes present on modern species of Icacinaceae. The combination of characters exhibited by these fossils clearly suggests affinities with Icacinaceae and calls for the recognition of a new species. However, several key characters are unobservable, making its affinities at the generic level obscure. The reticulately ridged endocarp surface, with numerous areoles penetrated by freely ending ridgelets, closely resembles numerous modern and fossil taxa of Icacinaceae. The presence of a sessile, button-like stigma is also consistent with numerous genera within the family. Although these fossils superficially resemble Iodes, their preservation makes it impossible to determine whether they had vascular bundles inside or outside the endocarp wall and whether they had smooth or papillate inner endocarp surfaces. Furthermore, while the fossils possess structures similar to stipes of some species of the extant genera Pyrenacantha and Miquelia, the surface morphology of the fossils is clearly distinct from those genera in being ridged rather than pitted. Given the unclear generic affinities of these fossils, we place them in the fossil genus Icacinicaryites, which was established by Pigg et al. (2008) to accommodate compression/


Fig. 7. Icacinicaryites lottii sp. nov. fruits from the Kisinger Lakes flora of Wyoming. (A) Well-preserved endocarp and subtending stalk impression, UF 1937659514. Freely ending ridges (preserved as furrows) are present in the majority of the fruit’s areoles. (B) Impression, UF 19376-59515. (C) Counterpart to B; UF 19376-59515’. Scale bars = 5 mm.

impression fossils of Icacinaceae lacking the preservation necessary for assignment to a more natural (i.e., presumably monophyletic) extant or fossil genus. These fossils are distinct from Biceratocarpum brownii in lacking the pair of subapical horns on the endocarp surface and in the presence of numerous freely ending ridgelets on the endocarp surface. They are distinct from Iodes occidentalis both in their larger size (9.8–12.1 mm long in Icacinicaryites lottii vs. 7.1 mm long on average in Iodes occidentalis) and their possession of a large stipe (I. occidentalis appears to lack stipes and have relatively narrow pedicels, consistent with modern species of Iodes). The combination of a ridged endocarp surface with a prominent stipe is also a unique combination of characters not known in any other modern or fossil species of Icacinaceae. Genus— Iodes Blume 1825. Species— Iodes occidentalis S.E. Allen, Stull, & Manchester, sp. nov. Diagnosis— Endocarp bivalved, globose to lenticular, with a reticulum of ridges forming irregular areoles that are regularly penetrated by freely ending ridgelets. Endocarp inner surfaces or locule casts, when preserved, densely covered with minute papillae. Vascular bundle embedded in the endocarp wall. Holotype hic designatus— UF 19225-57242 (Fig. 8D, E). Type locality— Blue Rim, Wyoming (UF loc. 19225). Paratypes— UF 19225-57241 (Fig. 8F), UF 19225-57243 (Fig. 8G, H). Additional specimens examined for species description— UF 15761-22676 to 22679, 22689, 22692, 22694, 22697,

30925, 31009, 48449, 48450, 48453, 48454, 48457, 48591, 48603; UF 15761S-57858; UF 19032-39002, 39007; UF 1922551995, 51997, 54563, 54564, 54566; UF 19337-58058; UF 19338-58269, 58271. Etymology— The specific epithet occidentalis (Latin = western), refers to the occurrence of this species in the western hemisphere, contrasting with the modern distribution of the genus in Africa and Asia. Description— Endocarp globose to lenticular (may be partially due to compression), averaging 7.1 mm long by 6.2 mm wide with an average length to width ratio of 1.2:1 (based on measurements from 28 specimens), unilocular, bivalved. Base and apex usually symmetrical, rarely slightly asymmetrical (Figs. 8, 9). If asymmetrical usually at the apex. Outer surface covered with a reticulum of ridges, forming polygonal areoles (average of 25.9 areoles on each lateral face based on 19 specimens). Areoles irregular in size and shape, often penetrated by freely ending, usually unbranched, ridgelets. Longitudinal ridges present in many specimens, although commonly only moderately well developed (e.g., only run 3/4 the length of the endocarp or follow an irregular course). Specimens have an average of 3.8 longitudinal ridges (including partial length ridges) per valve. Inner endocarp surface reflects ridging pattern of the external surface (visible on the locule casts). Locules, when well preserved, densely covered with minute papillae; spacing of papillae varied between the two specimens that are well preserved (the papillae are most obviously represented by little holes densely covering the locule casts). Ninty-nine papillae were counted in 0.25 mm2 on specimen UF 19225-57243 (Fig. 4C), while 188 papillae were observed in 0.25 mm2 on specimen UF 15761-22704 (Fig. 4B). Correspondingly, spacing between adjacent papillae (measured from the center of one hole to another) varied with an average


of 0.05 mm for specimen UF 19225-57243 and 0.03 mm for specimen UF 15761-22704 (from 10 measurements at random). Endocarp wall averaged 0.64 mm thick on specimen UF 19225-57242 (widest near the apex; cellular detail not preserved as the wall is generally coalified). Vascular bundle running through the thickness of the endocarp wall from the base to the apex, where it abruptly turns and enters to the locule (rarely preserved, but documented by an infilling of the vascular canal within the width of the endocarp wall in specimen UF 19225-57242; Fig. 8D, E). Pedicel occasionally preserved. On specimen UF 19225-57241 (Fig. 8F), the incomplete length of the pedicel is 3.3 mm, while the width is ~0.6 mm. Discussion— The suite of characters shown by these fossils indicates that they belong to family Icacinaceae and more specifically to the extant genus Iodes. Numerous genera in the family (e.g., Alsodeiopsis, Desmostachys, Hosiea, Iodes, Natsiatum, Rhyticaryum) have woody, bivalved, unilocular endocarps, covered by a reticulum of ridges on the external surface, with an asymmetrical apical bulge marking the entry of the main vascular bundle into the locule (Stull and Manchester, 2012). This vascular bundle is called the funicle in earlier literature on fossil and modern Icacinaceae (e.g., Reid and Chandler, 1933; Howard, 1942). This suite of fruit characters has generally been associated with the Iodeae (Engler, 1893; Sleumer, 1942), including the genera Hosiea, Iodes, Mappianthus Hand.-Mazz, and Natsiatum, and paleobotanists have generally placed fossil fruits with this set of characters in this tribe (e.g., Reid and Chandler, 1933). However, molecular data (Byng et al., 2014; G. W. Stull et al., unpublished manuscript) indicate that the Iodeae are not monophyletic. Additionally, several genera outside the tribe (e.g., Alsodeiopsis, Desmostachys, Rhyticaryum) have fruit characters similar to genera within the Iodeae tribe (Stull and Manchester, 2012). These findings suggest that certain “Iodeae” fruit characters may be plesiomorphic or homoplasious and consequently unreliable for generic identification. Paleobotanists should therefore no longer assign fossils to this tribe because it does not seem to represent a natural group. Despite issues surrounding the monophyly of the Iodeae and their recognition in the fossil record, several genera historically placed within this tribe appear themselves to represent monophyletic lineages and possess unique character combinations allowing identification in the fossil record. Iodes, for instance, is unique among icacinaceous genera in that the main vascular bundle of the fruit—which, as mentioned earlier, runs from the base of the fruit to the apex, where it enters the locule to provide nutritional supply to the apical ovules—is embedded within the endocarp wall (Fig. 1). All other extant genera within the family possess vascular bundles that run through the mesocarp, along the outside of the endocarp. Fruits of Iodes also commonly have papillae lining the inner wall of the endocarp, as do the fossil specimens described here. However, not all extant species of Iodes possess papillae on the inner endocarp wall surfaces [G. W. Stull, personal observations: Iodes balansae Gagnep., papillae absent, KUN 0647596; Iodes seguinii (H. Lév.) Rehder, papillae absent, KUN 0649120]. It is also important to recognize that several other genera of Icacinaceae possess species with papillate inner endocarp walls (e.g., Miquelia, Hosiea). Therefore, this character alone does not permit definitive identification of Iodes, although in combination with others characters (especially an embedded vascular bundle) it appears useful for identifying this genus.

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On the basis of an examination of modern fruits of Iodes (Appendix 1), the fossil fruits described here are somewhat more similar to the African species. The fruits of modern African species, like Iodes occidentalis, tend to be smaller ( 90°. Primary venation pinnate, secondaries brochidodromous, ≥5 prominent veins radiating from the base of the laminae. Intersecondaries absent, tertiary veins percurrent. Holotype hic designatus— UF 15761N-57228 (Fig. 10A). Type locality— Blue Rim, Wyoming (UF loc. 15761N). Paratype— UF 15761-55239 (Fig. 10C). Additional specimens examined for species description—UF 15761-22732, 48468, 55240, 55241, 55242, 55243, 55244, 55253; UF 15761N-61357; UF 19032-39006; UF 1922551975, 57111. Etymology— The specific epithet bluerimensis refers to the escarpment in the Bridger Formation of southwestern Wyoming where these leaves have been found. Description—Petiole 2 to 7.5 mm long (when preserved, often incomplete) and ~1.5 to 2.5 mm wide, frequently showing a darker strand of tissue down the center of the petiole (see Fig. 8A, I). Lamina (leaf blade) varies from nanophyllous to mesophyllous (1.3 to 8.5 cm long and 0.6 to 5.0 cm wide) with length usually longer than width. Lamina relatively wide; length to width ratio on six mostly complete specimens from 1.35:1 to 1.92:1 (mean 1.68:1). One especially broad specimen has a length to width ratio of 0.82:1 (Fig. 10E). Shape is usually ovate but varies to elliptic. Laminae are generally symmetrical (occasionally base is slightly asymmetrical) and are unlobed and untoothed. Apex



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angle to the midvein that averages to 43.9° (based on three measurements each on eight leaves), while the basalmost vein measured averaged to a significantly larger 74.8°. Attachment of major secondaries to midvein excurrent (no deflection of course). Intersecondary veins absent. Tertiary veins percurrent, mostly opposite, rarely alternate, variable in course, most frequently straight. Tertiary vein angle generally consistent, but varying from increasing exmedially, basally concentric, to increasing proximally. Epimedial tertiaries (intersect primary vein) opposite percurrent, rarely alternate, and perpendicular to the midvein. Exterior tertiaries looped. Higher order venation rarely well preserved but 4th and 5th order venation appears reticulate.

Fig. 9. Impressions of fruits of Iodes occidentalis sp. nov. from the Barrel Springs locality (Green River Formation) in Wyoming (A–C) and the Douglas Pass Radar Site II locality in Colorado (D). (A) UF 18151-62097. (B) UF 19335-56837. (C) UF 19335-56836. (D) UF 00582-57564. Scale bars = 5 mm.

generally acute, rarely obtuse; apex shape varies from straight (the most common condition) to convex to rounded. Base convex to rounded to cordate, with basal angle ranging consistently from obtuse to reflex. Well-preserved specimens with a complete apex display a mucronate-like projection of the midvein at the apical termination (Fig. 10A). Some specimens have numerous evenly spaced pigmented dots scattered across the leaf surface that may be interpreted as laminar glands or trichome bases. Primary venation pinnate, with a straight, moderately thick midvein. Naked basal veins present with at least five basal veins. Agrophic veins simple. Secondaries brochidodromous, but loop so close to the margin they can easily be mistaken for craspedodromous. Interior secondaries absent, while minor secondaries are simple brochidodromous. Leaves have a marginal secondary vein (which is a vein of secondary gauge running on the leaf margin, not to be confused with a fimbrial vein, which is a marginal vein of tertiary gauge, Ellis et al., 2009). Secondary veins are spaced closer together proximally (toward the base) with occasional irregular variations in spacing. The angle of departure of secondary veins from the midvein ranges from ~30 to over 90° with higher values near the base. Secondary angle varies from smoothly to abruptly increasing proximally (toward the base of the lamina). The center and apical portions of the leaf have a secondary vein ←

Comparison to extant Icacinaceae leaf morphology—Leaves of Icacinaceae are simple, usually borne in spiral arrangement, but opposite phyllotaxy occurs in a few genera including Cassinopsis Sond., Iodes, and Mappianthus. Most genera have unlobed elliptical leaves (although there are some ovate and occasionally obovate species); however, some species of Phytocrene and Pyrenacantha [e.g., Pyrenacantha lobata (Pierre) Byng & Utteridge; Byng et al., 2014] are palmately lobed. Icacinaceous leaves typically have untoothed margins but are rarely minutely toothed (e.g., Natsiatopsis Kurz, Hosiea; Kårehed, 2001). When teeth are present, they are usually nonglandular, enervated by minor veins that extend to, or slightly beyond, the margin. Primary venation is usually pinnate, but is palmate in a few genera (e.g., Natsiatopsis, Natsiatum, Phytocrene, Pyrenacantha; Kårehed, 2001). The secondary veins are typically brochidodromous. Tertiaries and higher order venation are generally regular and well organized across the family (Fig. 11). We reviewed herbarium specimens of extant Iodes species and found many features are consistent with the fossils. From the specimens examined (Appendix 2), most species are notophyllous to mesophyllous in size, while Iodes liberica Stapf (MO 05005469) is microphyllous. Length to width ratios included the range observed in the fossils, but there are also examples with more slender leaves such as Iodes velutina King (MO 4018700) whose ratio is consistently over 2.0:1. Shape is usually elliptic with a few specimens that are slightly basally or medially asymmetrical. Apex angle and shape are more variable in the extant species; some have an obtuse angle and convex, obtuse, or emarginate shape, while many others share a generally acute apex with the fossil species. Base shape of extant Iodes varies from acute to obtuse to reflex with overall laminar shape varying accordingly. The fossils also seem to show signs of pubescence, which is consistent with leaves of extant Iodes. All extant Iodes examined have pinnate primary venation. Basal veins are usually naked (forming the leaf margin) and vary from one to seven. Secondary veins are festooned brochidodromous with no intersecondary veins. The spacing between adjacent secondary veins usually decreases proximally, while the angle of divergence of secondaries from the midvein increases smoothly or abruptly as seen on the fossils. Secondaries have an excurrent attachment to the midvein, while tertiaries

Fig. 8. Selection of Iodes occidentalis sp. nov. fruits from the Blue Rim flora (Bridger Formation) in southwestern Wyoming showing notable characteristics. These are impressions unless otherwise indicated. (A) UF 19225-51993. (B) UF 19225-51996. (C) UF 15761-22683. (D) Specimen (cast) showing an infilling of the vascular bundle (arrow) positioned within the space left by endocarp wall, UF 19225-57242. (E) Close up of the cast in D. Scale bar = 2.5 mm. (F) Fruit with rare pedicel, UF 19225-57241. (G) Ridge impressions of the endocarp visible on the locule cast. This locule cast also shows numerous small, densely spaced holes (more greatly enlarged in 4C), which are impressions of the papillae originally lining the inner endocarp surface of the fruit, UF 19225-57243’. Scale bar = 2.5 mm. (H) Impression counterpart of the endocarp in G. These are shown at the same magnification to show the relative endocarp wall thickness, UF 19225-57243. Scale bar = 2.5 mm. (I) Example of a typically preserved endocarp mold, UF 19225-51997. Scale bars = 5 mm (except E, G, and H: scale bars = 2.5 mm as noted).



Fig. 11. Extant Iodes leaves for comparison with the fossil specimens. Each specimen is identified with its name and authority, collector, locality, and herbarium if available. Original slides are part of the National Cleared Leaf Collection housed at the Smithsonian Museum of Natural History in Washington, D.C. (A) Iodes philippinensis Merr. (det. Sleumer), M. S. Clemens 32172, Mt. Kinabalu, Brit. N. Borneo, Leiden. Arrows indicate areas where the original slide mounting medium has discolored, partially obscuring the leaf. (B) Iodes reticulata King., Yates 1342, Sumatra, USNH 1551286. Arrow indicates area where the original slide mounting medium has discolored, partially obscuring the leaf. (C) Iodes trichocarpa Mild., Linder 1886, unknown, Arnold Arboretum. The single vascular bundle in the petiole is visible as a dark line (arrow). (D) Iodes seguini (Léul.) Rehd. (det. Sleumer), Liang 69753, Kwangsi, Arnold Arboretum. Scale bars = 10 mm.

are opposite to rarely alternate percurrent. Tertiary vein angle varies from relatively consistent to basally concentric, while epimedial tertiaries are opposite percurrent. Exterior tertiaries are looped; fourth and fifth order venation is reticulate. Areoles are present with moderate to good development and branched ←

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freely ending veinlets that are often obscured by excessive pubescence especially on the abaxial leaf surface. Marginal ultimate venation is looped (Fig. 11). Iodes scandens (Becc.) Utteridge & Byng (previously in its own genus, Polyporandra) also has morphological similarities to the Blue Rim specimens. We examined two herbarium specimens of I. scandens (MO 3487929 and MO 6178926) for comparison with the fossils. The specimens had a relatively long length to width ratio of up to 2.49:1. Leaves were elliptic and symmetrical with acute acuminate apices and acute slightly convex to convex bases. Secondaries were slightly different than the fossil specimens in that they were eucamptodromous becoming brochidodromous distally. The higher order venation was comparable with other species of Iodes. Goweria bluerimensis is known only from isolated leaves, and the source twigs are unknown, so the arrangement and organization, whether opposite as in extant Iodes (and its sister genus, Mappianthus) or alternate as in most other genera of the family, cannot be determined. If these leaves do indeed belong to Iodes, we can hypothesize that the leaves of this extinct taxon were opposite. The petiole preservation suggests it has a resistant strand of vascular tissue preserved in the center. This feature seems taxonomically significant because the petioles of other angiosperm leaves preserved in the same sediments at Blue Rim do not show such a distinct central dark band. When we examined the petiole of an Iodes ovalis Blume herbarium specimen (MO 4255558) with focused transmitted light we observed a single, dark, vascular trace running the length of the petiole. A vascular strand is also visible in the petiole of the cleared leaf of Iodes trichocarpa Mild. (see Fig. 11C). Icacinaceae s.s. (except for Cassinopsis) have a single vascular strand leading to each leaf, but it is not known if expanded petioles with a narrow, resistant vascular strand are found across the family. As the arrangement and number of vascular strands within petioles varies across families and genera (figs. 9.1–9.5 of Howard, 1979 illustrate a classification of the vasculature of nonmonocot petioles), we consider this feature to be informative for the recognition of leaves of Icacinaceae. The mucronate-like projection at the apex of well-preserved specimens (e.g., Fig. 10A) corresponds to a projection of the midvein past the laminar tissue on the apex of many extant Iodes taxa, but this feature is also found in other genera of Icacinaceae. Comparison with other leaf fossils—Goweria bluerimensis sp. nov. has been found at several localities at Blue Rim, but so far has not been observed in other fossil floras. Fossil leaves from other Eocene localities including the Green River (WY, UT, CO), Yellowstone-Absaroka (WY), and Clarno (OR) were examined to see whether any corresponded with the Blue Rim material. MacGinitie (1969) documented three leaves from the Green River flora that look superficially similar to G. bluerimensis. Aristolochia mortua Cockerell has a similar overall shape and looping secondary venation, but differs in both the number of primary basal veins and tertiaries. Erythrina roanensis MacGinitie shares a thick petiole and looping secondaries with G. bluerimensis, but has an emarginate apex and a different pattern of higher order

Fig. 10. Selection of leaves of Goweria bluerimensis sp. nov. from the Blue Rim flora (Bridger Formation) in southwestern Wyoming. (A) Composite image of the part and counterpart of UF 15761N-57228. Apical protuberance and vascular strand in the petiole are visible. (B) Cordate base and looping secondary venation are visible, UF 19225-51975. (C) Note overall cordate shape, UF 15761-55239. (D) Ladder-like tertiaries, UF 15761-55241. (E) Unusual rounded shape, UF 1922557111. (F) Intact acute apex, UF 15761-55240. (G) Leaf fragment adjacent to fruit of Iodes occidentalis sp. nov., UF 19337-57978’. (H) One of the smallest leaves of Goweria bluerimensis, UF 15761N-57271’. (I) Well-defined vascular strand in the petiole, UF 15761S-57861. Scale bars = 10 mm.


venation. Aleurites glandulosa (Brown) MacGinitie has an acute apex, looping venation, and ladder-like percurrent tertiaries, but has an acute base and three strong basal veins that were not seen on G. bluerimensis. Furthermore, MacGinitie (1974) noted three other taxa from his Yellowstone-Absaroka flora that could be initially mistaken for G. bluerimensis. Aristolochia solitaria MacGinitie shares a similar overall shape and looping venation, but contrasts with its three strong basal veins and very polygonal reticulate higher order venation. Canavalia diuturna MacGinitie is pinnate with looping venation with secondaries diverging at a higher angle near the leaf base. The overall shape is similar to G. bluerimensis, but the tertiary venation is more reticulate and the petiole is slender. Finally, Luehea newberryana (Knowlton) MacGinitie displays some looping venation and distinct opposite percurrent tertiaries that are perpendicular to the midrib, but differs in having multiple strong basal veins and having teeth. No specimens from the Clarno Formation (OR) have leaf architecture that matches with G. bluerimensis. Comparison with other Icacinaceae leaf fossils— Fossil leaves previously assigned to Icacinaceae are rare, perhaps due in part to the difficulty in finding diagnostic characters, i.e., features that are not also present in other plant families. In North America, the middle Eocene Chalk Bluffs flora preserves leaves from near You Bet, CA, in the Sierra Nevada Mountains, assigned to Phytocrene sordida (Lesquereux) MacGinitie (1941). One of MacGinitie’s Chalk Bluffs species, Ficus densifolia Knowlton, was later transferred to Icacinaceae as Miquelia californica Wolfe (1977). Wolfe (1968) initially placed Goweria in Menispermaceae, but later (Wolfe, 1977) reassigned it to Icacinaceae. Many of the characters in Wolfe’s diagnosis of Goweria apply to the leaves presented here including the ovate shape, multiple basal veins, straight secondaries that loop near the margin, percurrent tertiaries that loop near the margin, a thick petiole, and reticulate higher order venation. Wolfe (1968) described the primary venation of Goweria as palmate with five primaries, many of these only extending halfway to the apex. In examining the specimens Wolfe assigned to Goweria and taking into account the changes in standard leaf terminology since 1968 (other basal veins are at least 75% of the thickness of the midvein to be considered primaries, Ellis et al., 2009), we assigned these fossils to Goweria. There are no characters in Wolfe’s (1968) diagnosis of the genus that preclude the assignment of the Blue Rim species to this genus as G. bluerimensis. However, in 1977, when Wolfe transferred Goweria to Icacinaceae, he emended his initial diagnosis of this genus from having a marginal vein to just a thickened margin. Goweria bluerimensis has a marginal secondary vein. Sometimes it is obscured and seems to diminish toward the apex, but it is always present near the base. Wolfe (1968, 1977) described three species of Goweria: G. dilleri, G. lineraris, and G. alaskana. Both G. dilleri and G. lineraris are described as having common intersecondary veins, which are not present in G. bluerimensis. The presence or absence of intersecondaries was not mentioned in the description of G. alaskana but was not observed on the type specimen. Wolfe (1977) also described leaves of Phytocrene acutissima Wolfe, Phytocrene sordida, and Pyrenacantha sp. While many of the characters of Wolfe’s Phytocrene species, including the ovate shape, rounded to cordate base, and acuminate apex, align with G. bluerimensis, the leaves have small, irregular teeth, which are not seen on any of the Blue Rim specimens. Other leaves assigned to Icacinaceae include five species in five genera from the middle Eocene of Hokkaido, Japan (Tanai,

1990). The taxa assigned to Icacinaceae from this locality include Goweria bibaiensis Tanai, Huziokaea eoutilus (Endo) Tanai, Merrilliodendron ezoanum Tanai, Phytocrene ozakii Tanai, and Pyrenacantha sp. Goweria bibaiensis shares some features with G. bluerimensis, including a similar size and frequent ovate shape. Tanai (1990) noted that G. bibaiensis is palmately veined with five primary veins, camptodromous secondaries, and the marginal tertiaries terminate in small bumps. In contrast, G. bluerimensis has an untoothed margin, brochidodromous secondaries, and is pinnate with five or more basal veins (it is possible that Tanai interpreted some of the basal veins as primaries). Assessing whether these other previously published fossil leaf occurrences still fall within our current understanding of Icacinaceae is outside the scope of this paper. Although the genus Icaciniphyllum was established for fossil leaves from the Paleogene of Europe once thought to represent Icacinaceae (Kvaček and Bužek, 1995), the type species was later recognized as Sloanea L. (Elaeocarpaceae; Kvaček et al., 2001), so the genus Icaciniphyllum is not available for icacinaceous fossils. Paleoecological implications—Broadleaved evergreen leaves tend to be thicker than broadleaved deciduous leaves (Chaloner and Creber, 1990). Leaf thickness is difficult to estimate directly from fossil leaf impressions, but the positive correlation between petiole thickness and laminar thickness (quantified as mass per area) documented in modern angiosperm leaves allows for estimation of leaf thickness when petioles are preserved (Royer et al., 2007). A leaf mass per area (MA) analysis was completed on the specimens of Goweria bluerimensis with intact petioles following the methods outlined by Royer et al. (2007). Petiole width (PW) and leaf area (A) were measured in millimeters and squared millimeters, respectively, using ImageJ. There were 19 G. bluerimensis specimens (Appendix 3) with an intact petiole near the base of the leaf. The resulting MA using the formula from Royer et al. [log MA = 3.070 + 0.382 × log (PW2/A); Royer et al., 2007] was 119.45 g/m2. In a more conservative approach, MA was recalculated using only those specimens where most of the leaf was intact (therefore excluding the specimens where more than 1/3 of the leaf area had to be estimated with ImageJ). This calculation was completed with 11 specimens for an MA of 109.09 g/m2. Both of these numbers fall within the range of 87 to 129 g/m2, which suggests the fossil G. bluerimensis leaves had an approximately 1 year lifespan and were likely deciduous. An MA of 129 g/m2 indicates a lifespan greater than 1 year (Royer et al., 2007). It is important to note that the petioles on the fossils may be slightly wider due to taphonomic alteration (Royer et al., 2007). Therefore, these estimates for MA on the fossil G. bluerimensis are likely slightly higher than they would be if fresh material were measured. However, leaf lifespan would likely still be in the range of 1 year. This estimate of MA for G. bluerimensis can be compared with other Eocene fossil floras in North America. MA averaged 76.8 g/m2 with a range of 57 to 87 g/m2 for the Republic fossil flora (WA) in the Klondike Mountain Formation (~49 Ma; Royer et al., 2007). These estimates of this lacustrine flora suggest leaf lifespans under 12 months. These leaves also showed high levels of herbivory. A different fossil lake flora preserved in the Green River Formation of Bonanza, UT (~47 Ma), had a mean MA of 113.2 g/m2 with a range from 70 to 157 g/m2 (Royer et al., 2007). This flora’s higher leaf mass per area suggests more taxa with longer living leaves and generally different ecological strategies. The Bonanza site had correspondingly


less herbivory than the Republic site (Royer et al., 2007). The estimate of MA using G. bluerimensis is in the middle of these two floras. However, estimating the MA from multiple species at Blue Rim (rather than just one) is warranted for a more accurate comparison. Despite these results, the applicability of estimating MA using fossil leaves from vine or liana taxa has not been examined in detail. The original data set used by Royer et al. (2007) to create the formula to estimate MA from fossil leaves contained only ~12 taxa with a vine habit of the 667 species-site pairs. Studies on modern forests have shown that lianas tend to have both a lower leaf mass per area and leaf lifespan than trees growing in the same location (Wright et al., 2004; Cai et al., 2009; Zhu and Cao, 2010; Kazda, 2015). Furthermore, unless a confident taxonomic assignment has been applied to a fossil leaf morphotype, as was done with Goweria bluerimensis, the habit (e.g., tree, vine, shrub) of the original plant is usually not known. In addition, a few fossil specimens of G. bluerimensis (notably UF 19338-58273, UF 15761N-57274, and UF 1922556970) had larger circular structures randomly arranged across the leaf surface. Initial interpretation suggested that these marks were small galls, but upon closer inspection they are more closely aligned with fungal damage (E. Currano, University of Wyoming, personal communication, May 2013). Final remarks on G. bluerimensis—While many of the characters of Goweria bluerimensis seem convergent with those of other tropical eudicot families, the co-occurrence of these leaves and the fruits of Iodes occidentalis at several sites along the Blue Rim escarpment provided strong evidence for assignment to Icacinaceae. If the hypothesis that the G. bluerimensis leaves were produced by the same species as the Iodes occidentalis fruits is correct, then these leaves would belong to the extant genus Iodes. However, by themselves, the leaves do not provide sufficient characters for definitive placement in this modern genus, particularly in view of the fact that a related, but extinct, icacinaceous fruit type, Biceratocarpum brownii, also occurs at Blue Rim. Specimens of B. brownii are rare at Blue Rim, but their presence argues for caution in assumptions about co-occurring organs especially since there are shared morphological features among the leaves of different genera in Icacinaceae. DISCUSSION Overview of Icacinaceae fossil record— Paleobotanists have typically placed fossil fruits of Icacinaceae into either the Iodeae or Phytocreneae based on the general fruit characters displayed by these two tribes (e.g., Reid and Chandler, 1933; Pigg et al., 2008; Rankin et al., 2008). Genera of the Phytocreneae—Miquelia, Phytocrene, Pyrenacantha (including Chlamydocarya Baill. and Polycephalium Engl.; Byng et al., 2014), and Stachyanthus Engl.—for example, have endocarps with pitted surfaces, generally corresponding to tuberculate protrusions into the locule. The size and spacing of the pits, as well as the morphology of the tubercles, are potentially diagnostic for particular genera within the tribe. Fossil fruits of the Phytocreneae are known primarily from the Paleogene of North America (e.g., Manchester, 1994; Rankin et al., 2008; Stull et al., 2012) and Europe (e.g., Reid and Chandler, 1933; Collinson et al., 2012), although records are also known from the Paleocene of South America (Stull et al., 2012) and the Oligocene of Africa (Manchester and Tiffney, 1993).

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Genera of the Iodeae (as traditionally circumscribed, including Hosiea, Iodes, Mappianthus, Natsiatum, and Polyporandra) have bivalved endocarps encircled by a keel in the plane of bisymmetry (within which, or upon which, the main vascular bundle runs, along one side of the endocarp). The keel terminates in an asymmetrical apical bulge (marking the entrance of the vascular bundle into the endocarp to supply the ovules). The endocarp surface bears a prominent reticulum of ridges. Fossil fruits attributed to the Iodeae have been described from numerous localities ranging from the late Cretaceous (Knobloch and Mai, 1986) to the Oligocene (Kvaček and Bužek, 1995), with the majority being from the Paleogene of North America (e.g., Manchester, 1994; Pigg et al., 2008; Stull et al., 2011) and Europe (Reid and Chandler, 1933; Collinson et al., 2012). However, the attribution of fossil fruits to the Iodeae tribe is now seen to be highly problematic. Some of the fruit features considered characteristic of the tribe are not unique to it. For example, the reticulately ridged endocarp surfaces and asymmetrical apical bulges also occur in some genera of the traditional Icacineae tribe (e.g., Alsodeiopsis, Desmostachys, Rhyticaryum). In addition, phylogenetic analyses show that the Iodeae, in their traditional circumscription, are polyphyletic (Byng et al., 2014; G. W. Stull et al., unpublished manuscript). Additional phylogenetic and morphological work is necessary to ascertain fruit characters useful for diagnosing broader clades within the family—particularly among genera of the traditional Iodeae and Icacineae. However, among the traditional Iodeae genera, Iodes, a Paleotropical genus containing ~16 spp., appears monophyletic (Byng et al., 2014) and clearly diagnosable based on morphological grounds. In fruits of Iodes, the main vascular bundle (which runs from the base of the fruit to the apex) is embedded within the endocarp wall; in all other Iodeae and “Iodeae”-like fruits of the Icacineae, the vascular bundle runs outside the endocarp wall, through the mesocarp. In addition, many species of Iodes also bear papillae on the inner endocarp surface, which is a rare character among other icacinaceous genera. These characters, when sufficiently preserved, may allow confident identification of Iodes in the fossil record. Iodes fossil record— Fossils fruits of Iodes, representing three taxa (I. multireticulata, “I.” corniculata Reid & Chandler, and I. eocenica Reid & Chandler), have been described from the early Eocene London Clay flora (Reid and Chandler, 1933). These fossils were noted to display considerable similarity in particular with African species of Iodes (e.g., I. africana Welw. ex Oliv.). One of these fossil species, I. multireticulata, has also been documented from the early Eocene Fisher/Sullivan site of Virginia (Tiffney, 1999) and the middle Eocene Clarno Nut Beds of Oregon (Manchester, 1994), from which an additional species of Iodes, I. chandlerae Manchester, was also described. In addition to these four species, several other fossil species have been placed in extinct genera that may represent Iodes or closely related stem taxa. Croomiocarpon mississippiensis Stull, Manchester et Moore shows a prominent reticulum of ridges as well as a vascular bundle embedded within the endocarp wall (Stull et al., 2011), suggesting affinities with Iodes. Although this fossil lacks papillae on its inner endocarp surface, papillae are also apparently absent from several extant species of Iodes. Additionally, this species has a cleft at the base of the endocarp similar to multiple extant Asian species of Iodes (e.g., I. cirrhosa, I. seguinii). Iodicarpa Manchester also has an embedded vascular bundle and papillate inner endocarp


surfaces (Manchester, 1994), suggesting affinities with Iodes, with the main difference apparently being the much larger size of Iodicarpa (length 26–56 mm, width 20–35 mm, endocarp wall thickness 2–4 mm), although several Asian species of Iodes have relatively large fruits (e.g., endocarps of Iodes balansae Gagnepain are up to 38 mm long; Hua and Howard, 2008). Finally, Palaeohosiea might also represent the extant genus Iodes. Palaeohosiea (Kvaček and Bužek, 1995) includes three species: P. suleticensis Kvaček & Bůžek, P. bilinica (Ettingshausen) Kvaček & Bůžek, and P. marchiaca (Mai) Kvaček & Bůžek. The genus is similar to Iodes in having keeled endocarps covered with a reticulum of ridges, with a papillate lining on the inner endocarp surface, and a vascular bundle that enters the endocarp at the base and runs in the keeled margin toward the apex. The similarity between Palaeohosiea and Iodes was noted by Kvaček and Bůžek (1995), but they distinguished Palaeohosiea from the modern genus based on the prominent keel found in Palaeohosiea, which they deemed absent from Iodes. However, prominent marginal keels are in fact present on practically all extant species of Iodes (e.g., Fig. 1). Kvaček and Bůžek also distinguished Palaeohosiea from Iodes and other known genera of Icacinaceae based on the foliage associated with the fossils, which they interpreted as icacinaceous but distinct from known genera. However, these fossil leaves have since been recognized to represent a separate family, Elaeocarpaceae (Kvaček et al., 2001). Therefore, no major characters distinguish Palaeohosiea from Iodes. These three taxa—one of which, P. bilinica, was also documented at Messel, alongside a possible new species, informally described as Palaeohosiea sp. (Collinson et al., 2012)—possibly should be transferred to the genus Iodes unless other distinguishing characters can be identified. Iodes occidentalis is distinct from previously described fossils in its overall shape (globose vs. more lenticular in the other species of Iodes) and in its endocarp reticulation pattern (it has more frequent freely ending ridgelets). “Iodes” corniculata, which has rare freely ending ridgelets, also possesses a pair of subapical horn-like protrusions (discussed more below), distinguishing it from I. occidentalis. Collectively, however, these fossils are perhaps more similar to fruits of modern African species than fruits of modern Asian species. The African species tend to have smaller, more globose endocarps with a denser reticulation including relatively frequent freely ending ridgelets. These features contrast with those of the Asian ones, which typically have much larger fruits, lenticular in cross section, with a more diffuse reticulation pattern, and often, an asymmetrical cleft near the base of the fruit. Iodes biogeography— Iodes is presently confined to rainforests of Africa, Madagascar, and Indo-Malesia (Fig. 12). However, based on the fossil record described here, the genus had a much broader historical distribution during the Eocene, when thermophilic forests extended well into the Northern Hemisphere (Tiffney, 1985). This fossil record suggests that the Northern Hemisphere may have played an important role in the diversification and global spread of Iodes across the tropics. Reid and Chandler (1933) noted the close similarity of I. multireticulata with modern species from Africa, especially I. africana. Iodes occidentalis is also more morphologically similar to fruits of African species (Fig. 1). Croomiocarpon mississippiensis, however, is considerably larger and possesses a cleft at the base of the endocarp, similar to modern species in Asia. The presence of fruit morphologies similar to both extant Asian and African species in the Eocene of the Northern Hemisphere provides even more clear evidence that the high-latitude

thermophilic forests present during the Paleogene played an important role in the early evolution of this genus. The shared presence of I. multireticulata in Europe and North America during the early–middle Eocene suggests that the North Atlantic Land Bridge (NALB) facilitated migration between these regions (Reid and Chandler, 1933; Manchester, 1994). However, while the Northern Hemisphere seemed to play an important role in the early evolution of the genus, its place of origin remains uncertain. The oldest records are from the early Eocene of Europe and North America (Reid and Chandler, 1933; Tiffney, 1999; present paper), but the Paleogene fossil record of Africa and Asia, where the genus occurs today, is more poorly known, especially based on well-preserved fruit and seed fossils (Jacobs, 2004). Thus, the absence of older records from Africa/Asia might represent a sampling artifact. However, older fossils of the family in general are known from North America (Paleocene: Pigg et al., 2008; Stull et al., 2012) and Europe (Maastrichtian: Knobloch and Mai, 1986), suggesting that the family itself might have originated in the Northern Hemisphere. Systematic and biogeographic significance of Biceratocarpum— Although Biceratocarpum brownii is similar to Iodes in several important respects (embedded vascular bundle, papillate inner endocarp surfaces), it is distinctive in having a subapical pair of horns and in having a closed reticulum of ridges lacking freely ending ridgelets. The former feature—the pair of horns— is particularly distinctive and not known in another extant genus of Icacinaceae. The similarities with Iodes suggest a close relationship, but the differences suggest that this taxon might fall outside the Iodes crown group. We therefore placed this species in a new genus to reflect its morphological distinctness (and perhaps phylogenetic isolation). Interestingly, the London Clay species “Iodes” corniculata also displays a pair of subapical horns (Reid and Chandler, 1933). Work is currently in progress on revising the systematics of Icacinaceae from the London Clay flora (G. W. Stull et al., unpublished manuscript) and will likely involve the transfer of “I.” corniculata to Biceratocarpum. Furthermore, given the morphological similarity of the London Clay fossils with B. brownii, these fossils may be conspecific, in which case the older name (brownii) would take priority (as Biceratocarpum brownii) and encompass both the London Clay and western North American fossils. The disjunction of B. brownii and “I.” corniculata (given their putative close relationship) is possibly the result of migration across the NALB, which seems to have served an important role in facilitating the migration of tropical taxa between North America and Europe during the early Eocene (Tiffney, 1985). The pattern of one species or two closely related species disjunct between North America and Europe during the Eocene is relatively common (Manchester, 1999), and B. brownii and “I.” corniculata thus provide another piece of evidence supporting the Eocene biogeographic connection of North America and Europe, presumably facilitated by the NALB. Biceratocarpum (and “I.” corniculata) also further highlight the importance of the Northern Hemisphere in the early diversification of the family. Biceratocarpum appears to have represented a distinctive lineage within the family, with a relatively wide distribution (North America and Europe), that presumably went extinct due to climate deterioration during the late Eocene–Oligocene. Overview of Icacinicarya and Icacinicaryites—Both Icacinicarya and Icacinicaryites function as repositories for icacinaceous fossils of uncertain generic placement, although the former is


Fig. 12.

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Modern distribution of Iodes in central Africa, Madagascar, southeastern Asia, and the central Indo-Pacific Islands.

reserved for anatomically preserved specimens and the latter for compression/impression material. Over 20 species of Icacinicarya have been described, ranging from Maastrichtian to Eocene in age (reviewed in Pigg et al., 2008). Two species of Icacinicaryites have been previously described from the late Paleocene of western North America (Pigg et al., 2008). Icacinicaryites lottii, described here, is considerably smaller than the two previously described Icacinicaryites species [I. linchensis Pigg, Manchester, & DeVore and I. corruga (Brown) Pigg, Manchester, & DeVore]; it also appears to have smaller, more regularly sized areoles in the endocarp reticulation. The broad stipe of I. lottii is also distinctive, but the absence of similar structures on the other species of Icacinicaryites could be an artifact of preservation. Since Icacinicarya and Icacinicaryites do not necessarily represent natural/monophyletic groups (but rather repositories for fossils of Icacinaceae of uncertain generic placement), it is not really reasonable to draw any biogeographic conclusions for these genera as a whole based on the distributions of their constituent fossil taxa. Paleoecological implications— We discuss the paleoecology of these taxa in relation to the Blue Rim flora. This locality has been the most extensively studied of the sites discussed here and has both Iodes fruits and associated leaves preserved. Many Icacinaceae taxa, including Iodes, are lianas (Kårehed, 2001). Today, lianas, which have a very large leaf mass for their

stem diameter, account for a quarter of woody stems in lowland tropical forests (Putz and Chai, 1987; Gentry, 1991; Andrade et al., 2005; Schnitzer, 2005). Lianas are more common in areas with marked seasonality (longer dry seasons) and less common in areas with high mean annual rainfall (Schnitzer, 2005; DeWalt et al., 2010; DeWalt et al., 2015). In addition, most lianas are found in tropical latitudes as their anatomy of both wide and long water vessels makes them very susceptible to freezing and harmful embolisms (Gentry, 1991; Schnitzer, 2005). However, this anatomy enables them to efficiently transport water to their extensive crown even with a narrow stem. Lianas take advantage of deep and extensive root systems to survive during the dry season (Andrade et al., 2005; Schnitzer, 2005). The leaf mass per area (MA) calculation suggested that the Goweria bluerimensis leaves at the Blue Rim site have a lifespan of approximately 1 year and were likely deciduous. This aspect is discussed in more detail in the discussion in the previous systematics section. However, it is important to note that most modern species of Icacinaceae tend to occur in predominately evergreen rather than deciduous forests. The estimate that Goweria bluerimensis is deciduous may relate to the fact that lianas tend to drop their lower leaves as the canopy closes (Rowe et al., 2004). Furthermore, deciduous lianas are most likely to lose their leaves during the driest time of the year, but lianas are often more resistant to seasonal dryness than the tree species they are growing on (Kalácska et al., 2005; Schnitzer and Bongers, 2011).


There is little literature on the ecology of extant Icacinaceae. In a study of all taxa with a liana habit in Lambir National Park, Sarawak, Malaysia, three species of Icacinaceae lianas including Iodes were documented (Putz and Chai, 1987). After Fabaceae, Icacinaceae had the most individual lianas in this forest survey. In addition, Putz and Chai (1987) found that liana taxa were more common in valley rather than ridge plots. The high prevalence of Iodes endocarps in addition to associated leaves at the Blue Rim site suggests this was a common taxon in that area. If Iodes had similar ecological preferences in the Eocene of Wyoming as compared with Southeast Asia today, this site likely represents a lowland. This inference is corroborated by the fluvial depositional environment at Blue Rim. Many of the other taxa preserved at the Blue Rim site, including Populus L. (Salicaceae) and Acrostichum L. (Pteridaceae), support the interpretation of an environment with high soil moisture or nearby water bodies. Icacina oliviformis (Poir.) J. Raynal, an extant species in a different clade of the family, has been extensively studied. The fruits (the mesocarp only) of this taxon were observed as a food source for both baboons and monkeys in northern Central African Republic (Fay, 1993). Primate fossils are present in other parts of the Bridger Formation (e.g., Gunnell, 1998). It is inferred that primates in the Eocene also lived in forested environments like primates today and likely ate icacinaceous taxa. Iodes and other taxa (e.g., Lygodium kaulfussi and Vitis L.) inferred to be climbers at Blue Rim based on nearest living relatives are also strong indicators that this area was at least partially forested as vines and lianas rely on trees for support. In sum, the presence of Icacinaceae in the Blue Rim flora, specifically their liana habit, suggests a low chance of frost and a multistratified forest structure in a local or regional lowland. LITERATURE CITED ALLEN, S. E. 2011. Paleobotanical diversity at the Blue Rim sites of the Eocene Bridger Formation, southwestern Wyoming. GSA Annual Meeting Abstract Paper No. 120-15, Minneapolis, Minnesota, USA. ANDRADE, J. L., F. C. MEINZER, G. GOLDSTEIN, AND S. A. SCHNITZER. 2005. Water uptake and transport in lianas and co-occurring trees of a seasonally dry tropical forest. Trees 19: 282–289. APG III [ANGIOSPERM PHYLOGENY GROUP III]. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105–121. BAILEY, I. W., AND R. A. HOWARD. 1941a. The comparative morphology of the Icacinaceae. I. Anatomy of the node and internode. Journal of the Arnold Arboretum 22: 125–132. BAILEY, I. W., AND R. A. HOWARD. 1941b. The comparative morpholgy of the Icacinaceae. II. Vessels. Journal of the Arnold Arboretum 22: 171–187. BERRY, E. W. 1930. A flora of Green River age in the Wind River Basin of Wyoming, 55–81. U. S. Geological Survey Professional Paper 165-B, Washington, D.C., USA. BROWN, R. W. 1929. Additions to the flora of the Green River Formation, 279–299. U. S. Department of the Interior Professional Paper 154-J, Washington, D.C., USA. BROWN, R. W. 1934. The recognizable species of the Green River flora, 45–68. U. S. Department of the Interior Professional Paper 185-C, Washington, D.C., USA. BROWN, R. W. 1937. Additions to some fossil floras of the Western United States, 163–186. U. S. Department of the Interior Professional Paper 186-J, Washington, D.C., USA. BYNG, J. W., B. BERNARDINI, J. A. JOSEPH, M. W. CHASE, AND T. M. A. UTTERIDGE. 2014. Phylogenetic relationships of Icacinaceae focusing

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APPENDIX 1.

List of herbarium specimens examined for fruit comparative work. Herbarium code “MO” = Missouri Botanical Garden, St. Louis, Missouri, USA.

Taxon – Voucher, Locality, Country, Year, Herbarium sheet number. IODES africana Welw. ex Oliv. – Breteler, Lemmens, Nzabi 8231, between Mouila and Yeno, Gabon, 1987, MO 4314613. Iodes klaineana Pierre – de Wilde et al. 606, SE of Tchibanga, Gabon, 1986, MO 4302002. Iodes ovalis Blume – Hiep et al. HLF203, Na Hang Nature Reserve, Vietnam, 2002, MO 6243998; Lau 148, Ngai District, Hainan, China, 1932, MO 1098159. Iodes perrier Sleumer – Jongkind 3696, Toliara, Madagascar,

APPENDIX 2.

1997, MO 6243553. Iodes seretii (DeWild) Boutique – Ekwuno, Fagbemi, and Osanyinlusi PFO.370, Edondon Forest Res., Nigeria, 1978, MO 2730593. Iodes usambarensis Sleumer – Luke 10774, Tana River District, Kenya, 2004, MO 5989989. Polyporandra scandens Becc. – Takeuchi 9320, Morobe Province, Atzera Range, Paupa New Guinea, 1994, MO 6178926.

List of herbarium specimens examined for leaf comparative work. Herbarium code “MO” = Missouri Botanical Garden, St. Louis, Missouri, USA.

Taxon – Voucher, locality, country, year, herbarium sheet number. ICACINACEAE Iodes cf. cirrhosa – Zhanhuo 91-324, Jinghon Xian, S. Yunnan, China, 1991, MO 4255558. Iodes africana Welw. ex Oliv. – Carvalho 5626, Bata-Senge, Equatorial Guinea, 1994, MO 5165184. Iodes kamerunensis Engl. – Bos 5170, 31 km from Kribi, Lolodorf Road, Cameroon, 1969, MO 5660279. Iodes klaineana Pierre – de Wilde et al. 606, SE of Tchibanga, Gabon, 1986, MO 4302002. Iodes liberica Staph

APPENDIX 3.

– Jongkind and Abbiw 2177, outside Ankasa Game Reserve, Ghana, 1995, MO 05005469. Iodes velutina King var. velutina – Maxwell 82-30, Botanic Gardens “Jungle”, Singapore, 1982, MO 4018700. Polyporandra scandens Becc. – Takeuchi 9320, Morobe Province, Atzera Range, Paupa New Guinea, 1994, MO 6178926; Van Balgooy 5060, NW Buru, Maluku Islands, Indonesia, 1984, MO 3487929.

Specimens of Goweria bluerimensis included in the leaf mass per area (MA) analysis.

UF 15761-22732, 48468, 55240, 55241, 57271; UF 15761N-57228, 57278; UF 15761S-57861, 57865; UF 19032-38992, 38996, 39001; UF

19225-56980, 57111, 59595; UF 19225N-57958; UF 19337-58054; UF 19338-58375.

A New Eocene Casquehead Lizard (Reptilia, Corytophanidae) from North America.

A Ceratopsian Dinosaur from the Lower Cretaceous of Western North America, and the Biogeography of Neoceratopsia.

Why Do the Boreal Forest Ecosystems of Northwestern Europe Differ from Those of Western North America?

Performance of salmon fishery portfolios across western North America.

A new large-bodied oviraptorosaurian theropod dinosaur from the latest Cretaceous of western North America.

Correction: A new large-bodied oviraptorosaurian theropod dinosaur from the latest Cretaceous of western North America.

Bird community conservation and carbon offsets in western North America.

Lead and mercury in fall migrant golden eagles from western North America.

North America.

North America.

North America.

Direct evidence of trophic interactions among apex predators in the Late Triassic of western North America.

A new Early Oligocene toothed 'baleen' whale (Mysticeti: Aetiocetidae) from western North America: one of the oldest and the smallest.

Plague bacterium as a transformer species in prairie dogs and the grasslands of western North America.

Multiscale perspectives of fire, climate and humans in western North America and the Jemez Mountains, USA.

Millennium Development Goals: update from North America.

A primitive fish from the Cambrian of North America.

Cheek tooth morphology and ancient mitochondrial DNA of late Pleistocene horses from the western interior of North America: Implications for the taxonomy of North American Late Pleistocene Equus.

Genome Sequence of Borrelia parkeri, an Agent of Enzootic Relapsing Fever in Western North America.

First Detection of Bat White-Nose Syndrome in Western North America.

Blood parasites of blue grouse (Dendragapus Obscurus) in western North America.

Medicine in North America.

Genetic analysis of cabbage loopers, Trichoplusia ni (Lepidoptera: Noctuidae), a seasonal migrant in western North America.

Three Centuries of Synchronous Forest Defoliator Outbreaks in Western North America.