Smilax (Smilacaceae) From The Miocene Of Western Eurasia With Caribbean Biogeographic Affinities

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American Journal of Botany 102 ( 3 ): 1 – 16 , 2015 ; http://www.amjbot.org/ © 2015 Botanical Society of America

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

The genus Smilax L. (Smilacaceae) comprises ca. 210 spe-cies of lianas, shrubs, and herbs occurring mainly in the sub-tropics and tropics of both hemispheres with some extensions into temperate regions ( Ferrufi no-Acosta, 2010 ; Qi et al., 2013 ). Smilax is a monocot genus in the order Liliales; it is sister to a clade comprising Philesiaceae with two species in South America and Ripogonaceae with six species in Australia, New Zealand, and New Guinea ( Kim et al., 2013 ). Recent comprehensive

molecular studies identifi ed four major clades within Smilax (including Heterosmilax Kunth; Fig. 1 ). (A) The Eurasian-African-Indian Smilax aspera L. is sister to the remainder of the genus albeit with low support. (B) A clade of American species (the New World clade) consists of fi ve subclades. Notably, three of these subclades have a single or very few Old World representatives that are sister to the American species ( Qi et al., 2013 ; Fig. 2 ). One subclade, B3, comprises species from South America (Brazil, Venezuela), the Caribbean, and southern Flor-ida. This subclade corresponds to the Smilax Havanensis group according to Ferrufi no-Acosta (2010) , which includes ten species with a distinctly dentate leaf margin, and partly to the Smilax Schomburgkiana group according to Ferrufi no-Acosta (2010) . Finally, C and D, the remaining two clades, which include chiefl y Old World species plus one clade of North American herbaceous species. Molecular dating studies have suggested a stem node age of 58 ± 9.9 to 46 ± 8.2 Ma (million years) for the Smilacaceae ( Vinnersten and Bremer, 2001 ) or 90 ± <16 Ma ( Janssen and Bremer, 2004 ) corresponding to Late Creta-ceous to early Cenozoic.

Leaf morphology in Smilax is highly variable within a species and among clades and using patterns of leaf venation and shape

1 Manuscript received 12 November 2014; revision accepted 11 February 2015.

The authors thank: Diane Erwin, UCMP, Berkeley, California, USA; Martin Gross and Reinhold Niederl, Universalmuseum Joanneum, Graz, Austria; Irene Zorn, Geologische Bundesanstalt, Vienna, Austria; and Andreas Kroh, Naturhistorisches Museum, Vienna, Austria for facilitating work in the collections. Benjamin Bomfl eur, Stockholm, Sweden is thanked for help with nomenclatural issues. This work was supported by a grant of the Swedish Research Council to TD. Two reviewers provided helpful comments on the manuscript.

6 Author for correspondence (e-mail: [email protected])

doi:10.3732/ajb.1400495

SMILAX (SMILACACEAE) FROM THE MIOCENE OF WESTERN EURASIA WITH CARIBBEAN BIOGEOGRAPHIC AFFINITIES 1

THOMAS DENK 2,6 , DIMITRIOS VELITZELOS 3 , H. TUNCAY GÜNER 4 , AND LILIAN FERRUFINO-ACOSTA 5

2 Swedish Museum of Natural History, Department of Palaeobiology, Box 50007, 10405 Stockholm, Sweden; 3 Athens University, Department of Geology and Geoenvironment, Section of Historical Geology and Paleontology, Panepistimiopolis,

Athens 15784 Greece; 4 Istanbul University, Faculty of Forestry, Department of Forest Botany, 34473 Bahceköy, Istanbul, Turkey; and 5 Universidad Nacional Autónoma de Honduras, Facultad de Ciencias, Departamento de Biología, Laboratorio de

Histología Vegetal y Etnobot á�nica, Boulevard Suyapa, Tegucigalpa, Honduras

• Premise of the study: Recent molecular studies provide a phylogenetic framework and some dated nodes for the monocot genus Smilax . The Caribbean Havanensis group of Smilax is part of a well-supported “New World clade” with a few disjunct taxa in the Old World. Although the fossil record of the genus is rich, it has been diffi cult to assign fossil taxa to extant groups based on their preserved morphological characters.

• Methods: Leaf fossils from Europe and Asia Minor were studied comparatively and put into a phylogenetic and biogeographic context using a molecular phylogeny of the genus.

• Key results: Fossils from the early Miocene of Anatolia represent a new species of Smilax with systematic affi nities with the Havanensis group. The leaf type encountered in the fossil species is exclusively found in species of the Havanensis group among all modern Smilax . Scattered fossils of this type from the Miocene of Greece and Austria, previously referred to Quercus (Fagaceae), Ilex (Aquifoliaceae), and Mahonia (Berberidaceae) also belong to the new species.

• Conclusions: The new Smilax provides fi rst fossil evidence of the Havanensis group and proves that this group had a western Eurasian distribution during the Miocene. The age of the fossils is in good agreement with the (molecular-based) purported split between the Havanensis and Hispida groups within Smilax . The Miocene Smilax provides evidence that all four subclades within the “New World clade” had a disjunct intercontinental distribution during parts of the Neogene involving trans-Atlantic crossings (via fl oating islands or the North Atlantic land bridge) and the Beringia land bridge.

Key words: biogeography; bird dispersal; disjunct distribution; evolution; fl oating islands; North Atlantic land bridge; Smilacaceae; Smilax Havanensis group; transatlantic crossing.

GALLEY PROOF — AJBD1400495

2 • V O L . 1 0 2 , N O. 3 M A R C H 2 0 1 5 • A M E R I C A N J O U R N A L O F B OTA N Y

alone makes it diffi cult to discriminate infrageneric groups of Smilax or even to distinguish Smilax from other monocot genera ( Daghlian, 1981 ; Wilde, 1989 ; Mai, 1995 ; Ferrufi no-Acosta, 2010 ). This makes the fossil record of foliage resembling Smilax diffi cult to interpret. The oldest leaf remains and reproductive structures assigned to Smilax date back to the Cretaceous in both hemispheres (e.g., Berry, 1911 ; Filippova, 1994 ) but all these records are in strong need of revision ( Daghlian, 1981 ; Greenwood and Conran, 2000 ). Unambiguous fossils of Smilax date back at least to the early middle Eocene ( Wilde, 1989 ) and of Ripogonum to the early Eocene ( Conran et al., 2009 ).

From the middle Eocene and Eocene/Oligocene of North America and Europe several leaf remains with strong similarity to modern Smilax were reported ( Cockerell, 1914 ; Chaney and Sanborn, 1933 ; Wilde, 1989 ; Dilcher and Lott, 2005 ); in some cases, leaf epidermal features provide strong support for the ge-neric assignment of the leaf remains ( Wilde, 1989 ). All the leaf remains recovered conform to two basic leaf types: 1) ovate-elliptic; and 2) (wide) ovate and distinctly cordate-hastate.

In view of several New World-Old World disjunctions within clades of Smilax ( Fig. 2 ) it will be important to link fossil taxa with specifi c infrageneric clades as they might provide crucial biogeographic information. In most, if not all cases, the previ-ous fossil record of Smilax is diffi cult to put into a phylogenetic and historically biogeographic context because the basic leaf

types in Smilax have evolved independently in distantly related infrageneric groups ( Fig. 1 ).

In this study, we describe a new species of Smilax from the Miocene of western Eurasia with a highly diagnostic leaf mor-phology. We refer the fossil species to the modern Havanensis group and discuss the implications of the new fossil fi nd for the evolution of modern disjunct distribution patterns in various subgroups of the New World clade of Smilax .

MATERIALS AND METHODS

The fossil plant material investigated for the current study originates from the following collections: University of California Museum of Paleontology, Berkeley, California, USA (UCMP); Universalmuseum Joanneum [formerly Landesmuseum Joanneum], Graz, Austria (LMJ); Geologische Bundesanstalt, Vienna, Austria (GBA); Naturhistorisches Museum Wien, Vienna, Austria (NHMW); and Istanbul University, Faculty of Forestry, Istanbul, Turkey (ISTO-F). High resolution scans of herbarium material of modern Smilax were provided from the herbaria at Berlin, Germany (B; Röpert, 2000 ), Edinburgh, UK (E; Royal Botanic Garden Edinburgh, 2014 ), Kew, UK (K; Royal Botanic Gardens, Kew , 2014 ), and Paris, France (P; http://science.mnhn.fr/institution/mnhn/search). The terminology for the morphological description of the fossil leaves mainly follows Dilcher (1974) .

The specimens investigated for this study and specimen details are listed in Appendix S1 (see Supplemental Data with the online version of this article). The plant fossils originate from lower to middle Miocene sedimentary formations

Fig. 1. Simplifi ed phylogenetic relationships of Smilax (based on Qi et al., 2013 ). The distribution of characteristic leaf types across the main clades A to D is shown. Clades A and B share ovate to lanceolate leaves with a conspicuous cordate-hastate base (gray). Note that this leaf type is restricted to Smilax aspera (clade A) and Smilax bona-nox and allied species (clade B). White arrowhead indicates presence of spinose-ciliate leaf margin in these species. Ovate to oblong leathery leaves with a spiny margin (dark gray) are confi ned to clade B (Havanensis group). Narrowly elliptic to lanceolate leaves (white) occur in clades B, C, and D. The most common leaf type in clades B, C, and D is ovate (to elliptic and oblong) with a rounded or cordate base (background shading). Drawings of leaves are based on herbarium specimens (herbaria E, K, P, S) and on Flora of China Editorial Committee (2000) , Flora of North America Editorial Committee (2003) , and Ferrufi no-Acosta (2010) . Leaves are not to scale.


D E N K E T A L . — E U R A S I A N M I O C E N E S M I L A X • V O L . 1 0 2 , N O. 3 M A R C H 2 0 1 5 • 3

from Turkey (Güvem, Ankara; Soma-Deniș, Manisa; Yata ğ�an Basin, Mu ğ�la), Greece (Kymi, Euboea), and Austria (Parschlug, Styria; Fig. 3 ).

Güvem area — The plant-bearing sediments are fossil-rich diatomites and lacustrine claystones of the Dereköy pyroclastics forming the basal part of the Güvem Formation ( Wilson et al., 1997 ; Tankut et al., 1998 ; Yavuz-Ișık, 2008 ). The Dereköy pyroclastics unconformably overlie the Çukurviran dacite, for which a Potassium-Argon (K-Ar) age of 19.7 ± 0.6 Ma was obtained ( Wilson et al., 1997 ). Above the Dereköy pyroclastics, the Bakacak andesite yielded a K-Ar age of 17.9 ± 0.5 Ma ( Wilson et al., 1997 ). Hence, the plant fossils from the Güvem area (Beș Konak, Kısilcahaman, Keseköy) are of early to middle Burdigalian age (early Miocene).

Soma-Deniş — Volcanic ash on top of the lower coal seam of the Soma Formation has been radiometrically dated as 17.3 ± 0.4 Ma ( Becker-Platen et al., 1977 ). The small mammal fossils recovered in the basal coal-bearing part of

the Soma Formation (lower coal seam) indicate a Burdigalian age (MN3). Plant fossils are from the marls above the lower coal seam and thus are of late Burdi-galian to early Langhian age (early to middle Miocene).

Yatağan Basin, Muğla — The early to early late Miocene Eskihisar Forma-tion is the lowermost in the Neogene succession of the Yata ğ�an Basin. The fossil-bearing sediments (Eskihisar, Tınaz, Salipașalar) are deposited above the lignite seam of the Sekköy member of the Eskihisar Formation. Based on paly-nological data, radiometric dating, vertebrate fossils and lithostratigraphic cor-relation, a Langhian to Serravallian (middle Miocene) age is suggested (see Güner and Denk, 2012 ).

Kymi, Euboea — Plant fossils in the Aliveri-Kymi Basin originate from the Marmarenia Formation, which is part of the Prinias Group. Small mammal fossils and palynology suggest a Burdigalian age ( Velitzelos, 2002 ; Velitzelos et al., 2014 ).

[AQ1]

Fig. 2. Phylogeny of the “New World Clade” of Smilax showing three New World-Old World disjunctions, two achieved including the North Atlantic land bridge (NALB), one including the Beringian land bridge (BER). E: E. North America, Az: Azores, BA: Balkans, Asia Minor, M: Mesoamerica, CM: Canary Islands, Ma-deira, M/S: Mesoamerica, South America, W: W. North America, E/W: E. North America, W. North America. NALB: North Atlantic Land Bridge, PP: Bayesian posterior probability. Asterisk denotes fully supported clades. Phylogenetic framework for “New World clade” of Smilax from Qi et al. (2013) . Inferred divergence age between Hispida group and remainder of New World clade from Zhao et al. (2013) . Light gray shading denotes group for which the fossil species described here provides a minimum age of ca. 20 Ma. Note that the Glauca and Hispida groups share closely similar, undiagnostic, leaf types. Morphologically recognized infrage-neric “groups” of Smilax from Ferrufi no-Acosta (2010) .



Parschlug, Styria — In the Parschlug basin the main lignite seam is over-lain by claystone and marls. Plant fossils occur in the light claystone and typically in the hard, reddish-blackish marlstone (ironstone; Kovar-Eder et al., 2004 ). Based on biostratigraphic correlation, a Karpatian-early Bad-enian age was suggested ( Kovar-Eder et al., 2004 ). This corresponds to Bur-digalian to Langhian (late early to early middle Miocene; Harzhauser and Piller, 2007 ).

SYSTEMATIC PALEOBOTANY

Family — Smilacaceae Vent., Tabl. Règn. Vég. 2: 146. 1799; nom. cons.

Genus — Smilax L., Sp. Pl. 2: 1028. 1753.

Species — Smilax miohavanensis Denk, D.Velitzelos, T.Güner et Ferrufi no-Acosta, nom. nov.

Basionym — Quercus aspera Unger (in Chloris protogaea: 108. 1847).

Synonym (replaced) — Smilax aspera (Unger) Denk, D.Velitzelos, T.Güner et Ferrufi no-Acosta, comb. nov.

The new combination is a junior homonym of the extant Smi-lax aspera L. (in Sp. Pl. 2: 1028. 1753). In accordance with Articles 6.10, 6.11, and 41 of the International Code of Nomen-clature for Algae, Fungi, and Plants (Melbourne Code, 2011), the replacement name Smilax miohavanensis is proposed.

1847 Quercus aspera Unger, p. 108, pl. 30, fi gs. 1 (right), 2, 3 (right).

?1847 Ilex sphenophylla Unger, p. 148, pl. 50, fi g. 9. 1864 Ilex sphenophylla Unger, p. 12, pl. 3, fi gs. 1-6. 1864 Ilex cyclophylla Unger, p. 13, pl. 3, fi gs. 7, 8. 1864 Ilex neogena Unger, p. 13, pl. 3, fi gs. 9, 10, 13 (? non

11, 12). 1867 Ilex cyclophylla Unger, p. 76, pl. 13, fi g. 14. 1867 Ilex neogena Unger, p. 76, pl. 13, fi gs. 16, 17 (non

15, 18). 2004 Mahonia (?) aspera Kovar-Eder et Kva č�ek, p. 57, pl.

13, fi gs. 3, 4, 6, 8 (?1, 2, 5).

Etymology — The specifi c epithet denotes the morphological similarity of the Miocene species with extant members of the Smilax Havanensis group according to Ferrufi no-Acosta (2010 ; corresponding to clade B3 of Qi et al., 2013 , the Central and South America lineage).

Holotype — Specimen UCMP Kasapligil 6914 ( Fig. 4, A-C ).

Paratypes — Specimens UCMP Kasapligil 5522b, 5524, 5720, 5861, 6072, 6927b, n.n. [ Fig. 4, G, H ] ; GBA 2002_01_0043, GBA 2002_01_0690, GBA 2002_01_0082, GBA BOT 2805; LMJ 76529, LMJ 76532 ; NHMW (Ettingshausen 7137) B.1878 VI 9140, NHMW (Ettingshausen 7173) 1878 VI 9140, NHMW (Ettingshausen 7473) B. 1878 VI 9476, NHMW (Ettingshau-sen) 1876 XVI 80; ISTO-F 01009.

(1) Diatomites of the Dereköy pyroclastics, lower Miocene (Burdigalian; see Güner and Denk, 2012 ), Güvem area (Beș Konak, Kısilcahaman, Keseköy), Anatolia, Turkey. Collection Baki Kasapligil, Museum of Paleontology, University of California (UCMP), Berkeley. (2) Fine-grained lacustrine sediments of the Marmarenia Formation, lower Miocene (Bur-digalian; see Velitzelos et al., 2014 ), Kymi (Kimi), Euboea. Collections GBA, NHMW. (3) Marls of the Soma Formation, Soma coal basin, and Sekköy Member of the Eskihisar Forma-tion, Yata ğ�an Basin, western Turkey (see Güner and Denk, 2012 ). Newly collected material housed at ISTO-F. (4) Reddish marlstone (ironstone), Parschlug basin, middle Miocene; see Kovar-Eder et al. (2004) , Parschlug, Styria, Austria. Collec-tions GBA, LMJ, NHMW.

Specifi c diagnosis — Leaves simple, petiolate, elliptic to ovate, base obtuse, acute or cordate, apex obtuse to acute, mucronate, primary venation acrodromous (3-veined), sec-ondary veins connecting central and lateral primary veins, leaf margin hyaline, deeply spinose or nearly entire margined, dentate axes approximately perpendicular to the tangent of the margin.

Description — Leaves simple, elliptic to ovate to rounded, symmetric; petiolate, petiole fl attened and twisted when inserted

Fig. 3. Map showing localities from which Smilax miohavanensis is known and their stratigraphic positions. Miocene stages follow Cohen et al. (2013) .



into the lamina, 3 to 12 mm long; lamina 15 to 75 mm long, 9 to 40 mm wide, base obtuse, acute or cordate, apex obtuse to acute, mucronate; primary venation acrodromous (3-veined), secondary veins connecting the central and lateral primary veins, departing from the central vein at angles of 15 ° to 45 ° ; secondary veins departing from the lateral primary veins at an-gles of 15 ° to 45 ° and forming irregularly angular loops toward the margin, from which veinlets branch off into the teeth; leaf margin conspicuously hyaline, dentate, deeply spiny, dentate axes approximately perpendicular to the tangent of the margin or slightly inclined to the tangent, number of teeth variable ranging from 0 to 30+ (0 to 18+ in specimens from Parschlug; to 30+ in specimens from Güvem; Figs. 4–7 ; Appendix S2, see Supplemental Data with the online version of this article).

Remarks — The material from Anatolia (Güvem) is consid-ered to represent the same species as slightly younger material from the historical collections of Greece (Kymi [Kumi]) and Austria (Parschlug) described by Unger in various papers be-tween 1847 and 1867 ( Unger, 1847 , 1850a , b , 1864 , 1867 ). Un-ger used various names to describe such leaves ( Quercus aspera , Ilex sphenophylla , Ilex cyclophylla , Ilex stenophylla , Ilex aspera nomen nudum, Ilex neogena , and partly Smilax schmidtii nomen nudum; Appendix S1, see Supplemental Data with the online version of this article). The earliest names used by Unger were Quercus aspera and Ilex sphenophylla . Quercus aspera from the middle Miocene of Austria and the specimens from the early Miocene of Turkey described here are highly similar warranting inclusion in a single species. However, the epithet “ aspera ” is occupied by the extant species Smilax aspera L. Thus the new combination “ Smilax aspera ” would be an illegitimate junior homonym to the extant species. Ilex sphe-nophylla described at the same time ( Unger, 1847 ) is based on much less material, the small size and preservation of which make an unambiguous determination impossible (Appendix S3, see Supplemental Data with the online version of this article). On the original lithographic plate (plate 50, fi g. 9 in Unger, 1847 ), three specimens of I. sphenophylla are shown on a single slab. The actual specimens housed at LMJ are on individual slabs and only in one case (LMJ76515) do they provide a close match to the illustration (Appendix S3, A-C). The second speci-men referred to fi g. 9 by its original label (Appendix S3, D) resembles the two specimens shown on the left half of the il-lustration but does not exactly match either the one or the other. The third specimen could not be located in the collections of LMJ, NHMW or GBA. Noteworthy, the original specimens of Ilex sphenophylla to Unger’s publication from 1864 were also labeled as ”83. Ilex sphenophylla Ung. Chlor. Protog. p. 148. t. 50. f. 9”. Ilex sphenophylla was also described and fi gured by Unger in later publications. The specimen fi gured from Gleichenberg ( Unger, 1850b ) probably is not Smilax , while the leaves fi gured in Unger (1864) most likely belong to Smilax miohavanensis .

DISCUSSION

Generic affi nity of the fossil species — The foliage described here has previously been attributed to various genera. Of these, Quercus and Ilex never have acrodromous primary veins. Ma-honia Orientales group typically has leafl ets with a primary ve-nation that approaches an acrodromous pattern. However, the

venation in Mahonia is better described as festooned brochido-dromous with secondary veins forming loops followed by ad-ditional lateral loops ( Güner and Denk, 2012 ). In contrast, the primary and lateral primary veins in Smilax are connected by secondary veins that depart from the primary veins at relatively low angles (20 to 55 ° ). The highly variable degree of spiny den-tition, from many teeth to no teeth at all on the same branch, in Smilax Havanensis group (Appendices S4, S5, see Supple-mental Data with the online version of this article) is also seen in the fossil specimens but never in Mahonia . Furthermore, leafl ets of Mahonia , except for the terminal ones, lack a dis-tinct petiole and usually have an asymmetric base. A similar leaf dimorphism (entire to conspicuously dentate) as in Smi-lax Havanensis group is seen in modern species of Ilex but these cannot be confused with Smilax on account of their dif-ferent leaf venation.

The character combination encountered in the fossil leaves described here matches exactly the one in modern members of the Smilax Havanensis group: 3-5 (−7) acrodromous primary veins, central and lateral primary veins originating in one point, deeply spiny leaf margin, dental axes typically perpendicular to the tangent of the leaf margin, co-occurrence of leaves with densely spiny and entire margin. The lateral primary veins in the fossil species commonly are not clearly visible in the upper portion of the lamina (appearing as imperfect-developed acro-dromous). Only few specimens (e.g., Fig. 7B ; Appendix S6, see Supplemental Data with the online version of this article) show that the lateral veins actually go all the way up to the apical part of the leaf lamina. This may be in part due to the preservation of the leaves. However, modern members of Smilax including species of Smilax Havanensis group can also have relatively thin lateral major veins that are prominent only on the upper or lower leaf surface ( Smilax aquifolium Ferrufi no et Greuter, S. cristalensis Ferrufi no et Greuter, S. cuprea Ferrufi no et Greuter, S. ilicifolia Desv. ex Ham.; Ferrufi no-Acosta, 2010 ) and spe-cies with chartaceous leaves commonly have lateral primary veins that do not reach all the way to the leaf apex but instead form a loop toward the primary vein (Appendix S7, see Supple-mental Data with the online version of this article).

Within the Havanensis group according to Ferrufi no-Acosta (2010) , Smilax miohavanensis resembles most closely Smilax aquifolium , S. coriacea Spreng., S. cristalensis , S. havanensis , S. ilicifolia , and S. populnea Kunth, all of which share ovate to elliptic leaves and the deeply spinose leaf margin. In addition, Smilax campestris Griseb. and S. spinosa Mill. of the Spinosa group may have leaves similar to Smilax miohavanensis , but the leaf margin commonly is less deeply spinose. In addition, these two species have highly polymorphic leaves including ovate and elliptic dentate leaves (approaching the Havanensis morphotypes), larger, long ovate ones with entire margin ( Smi-lax Weberi group morphotype), and narrowly elliptic to lanceo-late leaves with entire margin (Petiolata group morphotype). This may suggest that different morphotypes encountered in a fossil assemblage originated from the same species. For exam-ple, it cannot be ruled out that the foliage of Smilax mioha-vanensis from the early Miocene of Kimi ( Fig. 7 ) and S. weberi from the same locality (Appendix S8, right, see Supplemental Data with the online version of this article), may actually have been produced by the same species. However, the lanceolate leaves commonly co-occurring with ovate-elliptic ones in mod-ern species of the Spinosa group have never been found to-gether with foliage of Smilax miohavanensis .



Fig. 4. Smilax miohavanensis nom. nov. from the early Miocene of Anatolia. (A) Leaf with distinct petiole and acrodromous venation. UCMP, Kasapligil 6914. (B, C) Details of A showing hyaline spiny margin and leaf base. (D) Small leaf. UCMP, Kasapligil 5524. (E) Detail of (D). (F) Imprint of an elliptic leaf. UCMP, Kasapligil 6072. (G, H) UCMP, Kasapligil n.n. (I) Basal half of a small leaf. UCMP, Kasapligil 6927b. Scale bar = 3 cm in A, F, G; 2 cm in B, C, D, and 1 cm in E, H, I.



Fig. 5. Smilax miohavanensis nom. nov. from the early Miocene of Anatolia. (A) Large leaf with distinct petiole. UCMP, Kasapligil 5861. (B) Detail of (A) showing hyaline spiny margin. (C) UCMP, Kasapligil 5522b. (D) Detail of (C) showing secondary veins departing from lateral primary vein. (E) Leaf fragment. UCMP, Kasapligil 5720. (F, G) Details of (E) showing hyaline, spiny leaf margin and secondaries connecting the central and lateral primary veins. Scale bar = 3 cm in A, B, C, E, and 2 cm in D, F, G.



Fig. 6. Smilax miohavanensis nom. nov. from the middle Miocene of Austria. (A) Coarsely dentate leaf. GBA 2002_01_0090. (B) LMJ 76532, as Quercus aspera , Unger 1847, pl. 30, fi g. 1 . (C) Broadly ovate leaf. NHMW (Ettingshausen 7137), B. 1878 VI 9140. (D) Entire-margined leaf. NHMW (Ettingshausen 7473), B. 1878 VI 9476. Scale bar = 1 cm in A-D.



Smilax in the Cenozoic of Eurasia and North America — A large number of species of Smilax have been described from Cenozoic sediments of Eurasia and North America comprising a range from ovate to distinctly hastate foliage. The latter has commonly been compared to the modern Eurasian-African-In-dian Smilax aspera and the eastern North American Smilax bona-nox L.

Oldest reliable fossils of Smilax are from the Paleocene and Eocene of Europe and North America. Paleocene records are diffi cult to assign to a particular genus with certainty. For ex-ample, Heer (1859 , p. 106, plate 133, fi g. 24) fi gured the basal part of a small leaf from the middle Paleocene of Ménat (Se-landian, ca. 61 Ma) which he referred to Smilax sagittifera Heer. This leaf fragment may belong to Smilax but is insuffi -cient for a conclusive generic assignment. A leaf fragment from the Paleocene of western Greenland ( Heer, 1874 ) assigned to Smilax lingulata Heer lacks the basal and apical lamina and cannot be assigned to any modern genus. Another leaf from the Paleocene of Atanikerluk assigned by Heer (1871) to Smilax grandifolia Unger is closely similar to modern Smilax by its leaf shape and venation. Lesquereux (1888) and Cockerell (1914) described Smilax carbonensis (Lesq.) Cockerell from the Paleocene/Eocene of Wyoming. The lamina lacks the apical part but might well belong to Smilax .

Foliage with preserved epidermal features from the early Eo-cene of Australia ( Conran et al., 2009 ) unequivocally belongs to Ripogonium and ovate and deeply cordate leaves with pre-

served epidermal features from early middle Eocene (ca. 47 Ma) sediments of Messel, Germany, belong to Smilax ( Wilde, 1989 ). From the middle Eocene of Hungary, Erdei and R á�kosi (2009) described ovate foliage with obtuse leaf base and from the middle Eocene Clairborne Formation, Tennessee, Sun and Dilcher (1988) and Dilcher and Lott (2005) described ovate and cordate-hastate Smilax foliage, the latter of which they com-pared to the modern Smilax bona-nox Noteworthy, the two types of foliage encountered in the Clairborne Formation are morphologically very similar to the foliage from Messel. From East Asia, Ding et al. (2011) list a single Paleocene leaf record that probably needs to be reconfi rmed (leaf dimensions are 1.6 × 1.1 cm) and one Eocene record. Overall, this suggests that Smilax was established at the latest by the early Eocene (late Ypresian, ca. 47 Ma) and possibly already by the middle Pa-leocene (Selandian, ca. 61 Ma; Ménat) or early/middle Paleo-cene (Danian/Selandian, ca. 62 Ma; Greenland), and would be in good agreement with the inferred Cretaceous stem age for the Smilacaceae ( Vinnersten and Bremer, 2001 ; Janssen and Bremer, 2004 ).

From Oligocene and Miocene sediments many species of Smilax were described from North America and Europe ( Table. 1 ). All these records can be attributed to four morphotypes (“ For-menkreis ” according to Weyland, 1937 ). The “Sagittifera mor-photype” comprises foliage with ovate to lanceolate leaves with a conspicuous cordate-hastate base and corresponds to the leaf type found in species belonging to clades A and B of modern

Fig. 7. Smilax miohavanensis nom. nov. Broadly ovate leaf types. (A) Middle Miocene of the Yata ğ�an Basin, western Turkey. ISTO-F 01009. (B) Early Miocene of Kymi, Euboea, Greece. NHMW (Ettingshausen), 1876 XVI 80. Scale bar = 1 cm in A, B.



TABLE 1. The Cenozoic record of Smilax .

Origin Age Reference Leaf shape and base

Morphotype (MT) according to Weyland (1937) amended

by present study Taxon name

EU Paleocene Heer, 1859 Ovate, deeply cordate “Sagittifera MT” Smilax sagittifera HeerNALB Paleocene Heer, 1871 Ovate, cordate No MT assigned Smilax grandifolia Heer a NALB Paleocene Heer, 1874 Lanceolate (fragment) “Petiolata MT” Smilax lingulata HeerAM Paleocene/Eocene Lesquereux, 1878 ;

Cockerell, 1914 Broadly ovate, cordate No MT assigned Smilax carbonensis

CockerellEU Early middle Eocene Wilde, 1989 Ovate, obtuse-decurrent “Weberi MT” cf. Smilax sp. 1EU Early middle Eocene Wilde, 1989 Narrowly ovate-elliptic to

broadly ovate, shallowly cordate-hastate

“Petiolata MT” to widespread unspecifi c type

cf. Smilax sp. 2

EU Early middle Eocene Wilde, 1989 Elliptic to lanceolate, obtuse to acute

No MT assigned ? Smilax sp. 3

N Eur Middle Eocene Heer, 1869 Broadly ovate, obtuse-hastate

“Weberi MT” Smilax paliformis Heer

N Eur Middle Eocene Heer, 1869 Ovate, obtuse “Weberi MT” Smilax reticulata Heer a N Eur Middle Eocene Heer, 1869 Ovate, otuse-decurrent No MT assigned Smilax convallium HeerN Eur Middle Eocene Heer, 1869 Narrowly ovate-elliptic “Petiolata MT” Smilax lingulata HeerEU Middle Eocene Erdei and R á�kosi, 2009 Ovate, obtuse “Weberi MT” Smilax sp. 1EU Middle Eocene Erdei and R á�kosi, 2009 Ovate, obtuse “Weberi MT” ? Smilax sp.AM Middle Eocene Dilcher and Lott, 2005 Ovate, obtuse-decurrent No MT assigned Smilax sp. 1AM Middle Eocene Dilcher and Lott, 2005 Ovate, deeply

cordate-hastate“Sagittifera MT” Smilax sp. 2

EU Late Eocene Knobloch et al., 1996 Ovate-elliptic, acute No MT assigned Smilax sp. 1EU Late Eocene Knobloch et al., 1996 Elliptic, acute No MT assigned Smilax sp. 2AM Late Eocene Cockerell, 1914 Ovate, truncate-decurrent No MT assigned Smilax labidurommae

CockerellAM Late Eocene Knowlton, 1899 Broadly ovate-elliptic,

shallowly cordateNo MT assigned Smilax lamarensis

KnowltonAM Late Eocene Chaney and Sanborn,

1933 Ovate, acute No MT assigned Smilax goshensis

Chaney and SanbornEA Eocene Ding et al., 2011 Ovate, round No MT assigned Smilax sp.AM Eocene/Oligocene Meyer, 2003 Broadly ovate, truncate No MT assigned Smilax labidurommae

CockerellEU Oligocene Kva č�ek and

Walther, 1995 Ovate, oblong,

slightly hastate“Weberi MT” Smilax sp.

EU Early Oligocene Saporta, 1863 Narrowly ovate, shallowly cordate

“Petiolata MT” Smilax linearis Saporta

EU Early Oligocene Saporta, 1863 Narrowly ovate, shallowly sagittate

“Sagittifera MT” Smilax sagittiformis Saporta

EU Early Oligocene Saporta, 1863 Lanceolate, auriculate No MT assigned Smilax elongata SaportaEU Early Oligocene Walther and

Kva č�ek, 2007 Ovate, oblong,

slightly hastate“Weberi MT” Smilax weberi Wessel

AM Early Oligocene Becker, 1969 Ovate, shallowly cordate No MT assigned Smilax trinervis MoritaEU Middle Oligocene Mai and Walther, 1978 Narrowly ovate-elliptic “Petiolata MT” Smilax petiolata

WeylandEU Middle Oligocene Saporta, 1888 Ovate, deeply

cordate-hastate“Sagittifera MT” Smilax coquandi Saporta

EU Middle Oligocene Saporta, 1888 Narrowly ovate, shallowly cordate

“Sagittifera MT” Smilax philiberti Saporta

EU Late Oligocene Wessel and Weber, 1856 Ovate-elliptic to oblong “Weberi MT” Smilax weberi WesselEU Late Oligocene Wessel and Weber, 1856 Ovate-elliptic “Weberi MT” Smilax ovata Wessel a EU Late Oligocene Wessel and Weber, 1856 Ovate, deeply

cordate-hastate“Sagittifera MT” Smilax remifolia Wessel

EU Late Oligocene Saporta, 1862 ; 1873 Roundish, deeply cordate and notched

No MT assigned Smilax rotundilobus Saporta

EU Late Oligocene Saporta, 1865a Broadly ovate, hastate-truncate

“Weberi MT” Smilax garguieri Saporta

EU Late Oligocene Saporta, 1865a Lanceolate, auriculate No MT assigned Smilax abscondita Saporta

EU Late Oligocene Kovar-Eder, 1982 Long ovate, deeply cordate

“Sagittifera MT” Smilax sp.

EU Early Miocene Brongniart, 1828 Narrowly ovate, deeply cordate

“Sagittifera MT” Smilacites hastata Brongniart a

EU Early Miocene Heer, 1855 Broadly ovate, shallowly cordate

“Weberi MT” Smilax grandifolia Heer a

EU Early Miocene Saporta, 1865b Narrowly ovate, deeply cordate

“Sagittifera MT” Smilax hastata Saporta a

EU Early Miocene Saporta, 1865b ? No MT assigned Smilax appendiculata Saporta

[AQ18]

[AQ19]

[AQ20]



TABLE 1. Continued.




EU Early Miocene Saporta, 1865b Broadly ovate, shallowly cordate

No MT assigned Smilax asperula Saporta

EU Early Miocene Knobloch and Kva č�ek, 1976

Broadly ovate, shallowly cordate

“Weberi MT” Smilax weberi Wessel

EU Early Miocene Hably, 1983 Ovate, acute-decurrent to truncate

“Weberi MT” Smilax weberi Wessel

EU Early Miocene Hably, 1983 Ovate-oblong, cordate-hastate

No MT assigned Smilax aspera L. fossilis

EU Early Miocene Hably, 1983 ovate-elliptic, obtuse No MT assigned Smilax borsodensis Andre á�nszky

EU Early Miocene Bůžek et al., 1996 Broadly ovate, deeply cordate

“Sagittifera MT” Smilax sagittifera Heer

EU Early Miocene Knobloch and Kva č�ek, 1996

Broadly ovate, deeply cordate-hastate

“Sagittifera MT” Smilax sagittifera Heer

EU Early Miocene This study Ovate-elliptic, acute, obtuse to cordate

“Havanensis MT” Smilax miohavanensis nom. nov.

AM Early Miocene Chaney, 1920 Ovate, shallowly cordate-hastate

“Sagittifera MT” Smilax magna Chaney

EA Early/middle Miocene Huzioka,1963 Ovate, cordate No MT assigned Smilax minor MoritaEA Early/middle Miocene Huzioka,1963 Ovate, acute-obtuse No MT assigned Smilax trinervis MoritaEU Middle Miocene This study Ovate-elliptic,

acute, obtuse to cordate“Havanensis MT” Smilax miohavanensis

nom. nov.EU Middle Miocene Unger, 1847 Broadly ovate,

deeply cordate“Sagittifera MT” Smilacites grandifolia

Unger a EU Middle Miocene Unger, 1847 Narrowly ovate,

deeply cordate“Sagittifera MT” Smilacites sagittata

Unger a EU Middle Miocene Heer, 1855 Ovate, deeply cordate “Sagittifera MT” Smilax sagittifera HeerEU Middle Miocene Heer, 1855 Broadly ovate, hastate “Weberi MT” Smilax obtusiloba HeerEU Middle Miocene Heer, 1855 Broadly ovate,

shallowly cordateNo MT assigned Smilax parvifolia Heer b

EU Middle Miocene Heer, 1855 Narrowly ovate, shallowly cordate

“Sagittifera MT” Smilax angustiloba Heer

EU Middle Miocene Heer, 1859 Ovate, deeply cordate-hastate

“Sagittifera MT” Smilax obtusangula Heer

EU Middle Miocene Heer, 1859 Ovate, deeply cordate-saggitate

No MT assigned Smilax auriculata Heer

EU Middle Miocene Unger, 1869 ovate-elliptic, obtuse No MT assigned Smilax hyperborea Unger

EU Middle Miocene Hantke, 1954 Broadly ovate, deeply cordate-hastate

“Sagittifera MT” Smilax sagittifera Heer emend. Hantke

EU Middle Miocene Andreanszky, 1959 ovate-elliptic, obtuse No MT assigned Smilax borsodensis Andre á�nszky

EU Middle Miocene Andreanszky, 1959 ovate-elliptic, obtuse No MT assigned Smilax hyperborea Unger

EU Middle Miocene Andreanszky, 1959 Broadly ovate, deeply cordate

“Sagittifera MT” Smilacites grandifolia Unger a

EU Middle Miocene Andreanszky, 1959 Broadly ovate, deeply cordate

“Sagittifera MT” Smilax praeaspera Andre á�nszky

EU Middle Miocene Andreanszky, 1959 Narrowly ovate, obtuse-acute

No MT assigned Smilax cf. oldhamii Miq.

EU Middle Miocene Iljinskaja, 1964 Broadly ovate, deeply cordate

No MT assigned Smilax grandifolia Heer a

EU Middle Miocene Ferguson, 1971 Ovate, acute-obtuse No MT assigned Taxon LXXIIEU Middle Miocene Ferguson, 1971 Narrowly ellipitc “Petiolata MT” Taxon LXXIIIN Eur Middle Miocene Christensen, 1975 Ovate, obtuse-decurrent “Weberi MT” Smilax weberi WesselAM Middle Miocene Lesquereux, 1888 Narrowly ovate,

deeply cordate“Sagittifera MT” Smilax wardii

LesquereuxAM Middle Miocene Hollick, 1936 Ovate, obtuse “Weberi MT” Smilax reticulata Heer a AM Middle Miocene Smiley et al., 1975 Ovate, obtuse-decurrent “Weberi MT” Smilax (cf. S. magna

Chaney)NALB Middle Miocene Denk et al., 2005 Ovate, obtuse-decurrent No MT assigned Smilax sp.EA Middle Miocene Tanai and Suzuki, 1963 Ovate-roundish, obtuse No MT assigned Smilax trinervis MoritaEU Late Miocene Weyland, 1957 Narrowly ovate-elliptic “Petiolata MT” Smilax petiolata

WeylandEU Late Miocene Massalongo , 1859 Elliptic No MT assigned Smilacites cocchiana

MassalongoEU Late Miocene Massalongo, 1859 Ovate-oblong,

slightly hastate“Weberi MT” Smilacites spadaeana

Massalongo

[AQ21]

[AQ22]

[AQ23]



TABLE 1. Continued.




EU Late Miocene Massalongo, 1859 Broadly ovate, shallowly cordate

“Weberi MT” Smilacites orsiniana Massalongo

EU Late Miocene Massalongo, 1859 Ovate, cordate No MT assigned Smilacites nestiana Massalongo

EU Late Miocene Massalongo, 1859 Ovate, deeply cordate “Sagittifera MT” Smilacites pulchella Massalongo

EU Late Miocene Massalongo, 1859 Ovate, deeply cordate “Sagittifera MT” Smilacites sagittifera Massalongo

EU Late Miocene Massalongo, 1859 Broadly ovate, slightly hastate

No MT assigned Smilacites proxima Massalongo

EU Late Miocene Laurent, 1908 Broadly ovate, cordate-hastate

No MT assigned Smilax mauritanica Desf. fossilis

EU Late Miocene Berger, 1957 Ovate, hastate- to saggitate-cordate

“Sagittifera MT” Smilax hastata Brongniart a

EU Late Miocene Berger, 1957 Elliptic, acute No MT assigned Smilax cf. ovata WesselEU Late Miocene Kolakovski, 1964 Ovate to ovate-oblong,

truncate, cordate to hastate

No MT assigned Smilax aspera L. fossilis

EU Late Miocene Knobloch, 1969 Ovate, cordate-hastate No MT assigned Smilax hastata Brongniart a

AM Late Miocene Brown, 1937 Ovate, shallowly cordate-hastate


AM Late Miocene Chaney and Axelrod, 1959

Ovate, shallowly cordate-hastate


EA Late Miocene Uemura, 1988 Ovate, elliptic No MT assigned Smilax trinervis MoritaEA Late Miocene Ding et al., 2011 Ovate, acute-obtuse No MT assigned Smilax tiantaiensis

Ding et al.AM Early Pliocene Axelrod, 1980 Broadly ovate, deeply

cordateNo MT assigned Smilax remingtonii

AxelrodEU Early Pliocene Pop, 1936 Broadly ovate to

ovate-oblong, hastateNo MT assigned Smilax aspera L.

Notes: a Invalid homonym of: Smilax auriculata Walter 1788; S. grandifolia Buckley 1843; S. hastata Jacq. 1760; S. ovata Duhamel 1803; S. reticulata Desv. 1825; S. sagittata Desv. ex Ham. 1825. Taxonomic treatment based on World Checklist of Monocotyledons, website http://apps.kew.org/wcsp/home.do .

Plant name not in italics = probably not belonging to Smilax . EU = Europe and Asia Minor, NALB = involving the North Atlantic land bridge, AM = North America, N Eur = North Europe, EA = East Asia.

Smilax ( Fig. 1 ). The “Weberi morphotype” encompasses ovate (to elliptic and oblong) foliage with a rounded or cordate to slightly hastate base and corresponds to the most widespread leaf type in modern Smilax found in all four main clades of the genus. These two morphotypes were also recognized in previ-ous work (e.g., Weyland, 1937 ; Christensen, 1975 ). A further morphotype detected in the fossil record comprises distinctly narrowly elliptic to lanceolate leaves, hereafter called “Petio-lata morphotype” based on the foliage of Smilax petiolata Wey-land ( Fig. 1 , Table 1 ). This morphotype, again, is also recognized among modern species of Smilax and occurs in clades B, C, and D both in New World and Old World species. The last morpho-type is here called “Havanensis morphotype” referring to the early and middle Miocene Smilax miohavanensis and corre-sponding to the Caribbean to South American species of the Smilax Havanensis group according to Ferrufi no-Acosta (2010 ; Fig. 2 ). While the fi rst three morphotypes are not diagnostic for a particular modern clade of Smilax , the Havanensis morphot-ype is restricted to clade B ( Qi et al., 2013 ; Fig. 1 ).

For the remaining (fossil) morphotypes, the high degree of parallel evolution of leaf morphology observed in the modern species of Smilax is also seen in the fossil record. Nevertheless, it is striking that identical leaf types are recorded both from North American and from European sedimentary formations.

For example, broadly ovate foliage with leaf bases ranging from hastate to hastate-cordate was reported from the Eocene/Oligocene Florissant beds of Colorado ( Cockerell, 1914 ; Meyer, 2003 ) and from the Oligocene fl ora of Suletice-Berand of Bohemia ( Kva č�ek and Walther, 1995 ). A leaf referred to as Smilax labidurommae Cockerell from the Eocene/Oligocene Florissant Formation ( Meyer, 2003 , fi g. 117) is virtually identi-cal to specimens described as Smilacites garguieri Saporta from the lower Oligocene of France ( Saporta, 1865a ).

To our knowledge, the fossil record of Smilax from East Asia is not as rich as that for Europe and North America. Miocene leaf remains described by Morita (1931 ) , Chaney and Axelrod (1959) , Tanai and Suzuki (1963) , Huzioka (1963) , and Ding et al. (2011) all belong to the general leaf type found in all four major clades of Smilax. Also from Central and South America little is known about the fossil history of Smilax , which may to some extent explain why the Smilax Havanensis group has no fossil record in the New World. According to Graham (2010) , pollen referred to as Smilacites has been reported from late Eocene to Pliocene sedimentary formations of Mexico and Argentina.

In Parschlug, Smilax miohavanensis (Havanensis group) co-occurs with S. sagittifera (Sagittifera group morphotype; Kovar-Eder et al., 2004 ). In Kymi, Smilax miohavanensis co-occurs with S. weberi (as S. schmidtii Unger nom. nud. in Un-

[AQ2]



ger, 1867 ; Appendix S8, see Supplemental Data with the online version of this article).

Integrating plant fossils in time-calibrated phylogenetic studies — In a recent study, Chen et al. (2014) used fossils to constrain nodes of intrageneric groups/species of Smilax . Two fossil species, Smilax trinervis Morita and S. tiantaiensis Ding et al. were used to constrain the ages of a S. davidiana A.DC., -S. china L. clade and of S. glaucochina Warb. ex Diels. Chen et al. (2014) indicated an age of 6 Ma for S. trinervis based on material from the late Miocene Takamine fl ora (Honshu, Japan; Uemura, 1988 ). This is problematic as Smilax trinervis (includ-ing S. minor Morita) was a common element in the late early and middle Miocene of Japan (e.g., late early Miocene Utto fl ora, Huzioka, 1963 ; see also Uemura, 1988 ). Hence, a node age constrained with S. trinervis would more appropriately be around 17-16 Ma. Furthermore, the leaf morphology of Smilax trinervis cannot be used to place this fossil taxon close to the living S. china . Instead, the fossil resembles several species of the clade comprising the species S. glabra Roxb. to S. ferox Wall. ex Kunth ( fi g. 3a in Chen et al., 2014 ; see also Morita, 1933 ).

The second fossil, Smilax tiantaiensis , resembles the modern S. china , S. davidiana , S. glaucochina , S. cyclophylla Warb., and S. stans Maxim. according to the original paper by Ding et al. (2011) , and therefore cannot be used to constrain the age of a single species.

A third fossil species used to constrain an intrageneric node in the study by Chen et al. (2014) was S. magna Chaney de-scribed from early and middle Miocene deposits of western North America ( Table 1 ; Chaney, 1920 ; Chaney and Axelrod, 1959 ; Smiley et al., 1975 ). Smilax magna was used to constrain the age of the S. hispida lineage to 18.5 Ma. Smilax magna shows a characteristic variability in leaf morphology (Weberi morphotype, Sagittifera morphotype, and unspecifi c leaf mor-phology) that includes leaf types encountered in various species of clade B of Qi et al. (2013 ; e.g., S. bona-nox , S. glauca Wal-ter, S. hispida Raf., and S. rotundifolia L., cf. Chaney and Axel-rod, 1959 ). Therefore, the fossil species could just as well have been used to constrain the age of the clade comprising S. glauca to S. rotundifolia , or the entire New World Smilax -clade of Chen et al. (2014 , fi g. 3a). Alternatively, fossils displaying very similar leaf variability to S. magna are also known from Eocene and Oligocene sediments of North America and Central Europe ( Dilcher and Lott, 2005 ; Wessel and Weber, 1856 ). In other words, the three fossil taxa selected by Chen et al. (2014) cannot convincingly be assigned to a particular in-group node or their stratigraphic age was misinformed. This calls for caution when fossil are included in time-calibrated phylogenetic studies.

Biogeographic patterns-multiple intercontinental disjunctions — The molecular phylogeny of Smilax can be used as a phylogenetic framework for assessing the evolution of basic leaf types in Smilax and the importance of fossils for bio-geographic reconstructions. As discussed in the previous sec-tion most leaf types in Smilax are shared by all major clades ( Figs. 1, 2 ). Therefore, leaf fossils assigned to Smilax may be of limited value for biogeographic reconstructions.

However, the contemporaneous presence of highly similar leaf types in European and North American sediments in the Eocene and possible already in the Paleocene (see above) sug-gests that the North Atlantic might have played an important

[AQ3]

role for range expansion in the early Cenozoic. This is in agree-ment with the phylogenetic framework, in which the fi rst di-verging clades A and B of Qi et al. (2013) represent (western) Eurasian and American taxa.

In this study, the focus is on the New World clade of Smilax (clade B). This clade comprises three New World—Old World disjunctions that must have been achieved independently in the Neogene ( Qi et al., 2013 ; Zhao et al., 2013 ). Zhao et al. (2013) inferred a divergence age between the Hispida group and the remainder of the New World clade of Smilax of ca. 25 Ma ( Fig. 2 ). Hence, the divergence ages of the three New World—Old World disjunctions in clades B4 and B5, and in the Smilax Ha-vanensis group (B3) must be younger. From the early and mid-dle Miocene of Central Europe, northern Europe and North America closely similar leaf types have been referred to as Smi-lax weberi and S. cf. magna , respectively ( Knobloch and Kva č�ek, 1976 ; Christensen, 1975 ; Smiley et al., 1975 ). These leaves clearly belong to the Weberi morphotype and possess the same type of epidermal characteristics. Although it cannot be determined whether these similarities evolved in parallel it is noteworthy that the Miocene fossils are highly similar to the modern species of clade B5 and B4 involving North American-western Eurasian disjunctions ( Fig. 2 ). The same is true for the fossil taxon pair Smilax sp. from the middle Miocene of Iceland ( Denk et al., 2005 , 2011 ) and leaf fossils from the Miocene of Alaska assigned to S. lingulata Heer by Hollick (1936) . The paleobotanical records and modern trans-Atlantic sister group relationships are strongly suggestive of migration across the North Atlantic. The Greenland-Scotland Transverse Ridge con-sisting of a chain of islands might have acted as a corridor (the so-called North Atlantic land bridge) for temperate plants with different dispersal modes until the latest Miocene ( Grímsson and Denk, 2007 ; Denk et al., 2010 , 2011 ). The modern species of clades B4 and B5 displaying New World-Old World disjunc-tions thrive in humid warm temperate climates ( Denk et al., 2001 ; Flora of North America Editorial Committee, 2003 ) com-parable to the middle Miocene conditions in the northern North Atlantic ( Denk et al., 2011 ). This may imply that the modern distribution of some members of these clades in tropical regions (e.g., Smilax velutina Killip et C.V.Morton) represents a more recent adaptation.

The fossil Smilax described here provides evidence that also clade B3 of Qi et al. (2013) that exclusively consists of New World species today had a wider distribution during the Neo-gene. Given the modern range of species of clade B3 and the divergence ages reconstructed by Zhao et al. (2013) , a more southern route than the North Atlantic land bridge could be as-sumed. Trans-Atlantic dispersal at tropical latitudes has been invoked for numerous angiosperm lineages ( Thorne, 1973 ; Renner, 2004 ) and for animals (platyrrhine monkeys, rodents; Houle, 1999 ; Poux et al., 2008 ; Rowe et al., 2010 ) based on fos-sil data and molecular phylogenetic studies. Dispersal across the tropical Atlantic could have happened in both directions based on the available wind and sea currents (cf. Fratantoni, 2001 ; Renner, 2004 ). The most likely means for crossing of the tropical Atlantic during the Early Cenozoic until the Miocene appears to be so-called fl oating islands ( Houle, 1998 ). Based on the geographical and stratigraphic distribution of Smilax mio-havanensis (Appendix S9, see Supplemental Data with the online version of this article), two dispersal scenarios can be inferred. First, migration across the Atlantic could have been achieved via Africa south of 30 ° N and crossing of the Atlantic by means of fl oating islands. Alternatively, as in the more tem-

[AQ4]



perate members of clade B4 and B5, crossing could have been via the North Atlantic land bridge, although temperatures at higher latitudes probably were too cool for subtropical-tropical plants (see Denk et al., 2011 , for an assessment of the paleotem-peratures across the North Atlantic land bridge during the Neo-gene). If the present distribution of the Smilax Havanensis group is the result of a niche shift similar to the one seen in Smilax velutina (see above in previous paragraph) then its (tem-perate) ancestors may have been able to cross the North Atlan-tic via the North Atlantic land bridge.

Smilax is mainly dispersed by birds ( Riddley, 1930 ). Im-portant dispersers of seeds of Smilax are crows (Corvidae), thrushes (Turdidae; e.g., Turdus , Sialis ), woodpeckers (Pici-dae), and ducks (Anatidae). A dated phylogeny of Corvus (crows) suggested that the genus originated in the Palearctic in the early Miocene and that the Eurasian-North American genus Pica (magpies) is their modern sister group. Within crows, early phylogenetic splits involve Palearctic-Nearctic/Caribbean disjunctions dated to middle Miocene ( Jønsson et al., 2012 ). These authors explained the modern distribution pattern by trans-Atlantic dispersal. This scenario, if correct, would be closely similar to the pattern seen in the Miocene-Recent distribution of the Smilax Havanensis group. Various Caribbean-Nearctic sister group relationships in Corvus may also support the statement by Qi et al. (2013) that Caribbean members of the Smilax Havanensis group might be derived from mainland lineages.

Similarly, thrushes appear to have crossed the Atlantic sev-eral times during the late Neogene ( Voelker et al., 2009 ) and ducks underwent a global diversifi cation also during the Mio-cene ( Gonzalez et al., 2009 ). Although it is clear that these birds disperse Smilax , it is not clear how the fruits traveled across the Atlantic. For example, fruit-eating birds are unlikely to retain the seeds across the Atlantic ( Renner, 2004 ). The most likely explanations for the trans-Atlantic crossings of Smilax and other plants during the Neogene are a combination of bird dis-persal and transport on fl oating islands (southern North Atlan-tic) or of bird dispersal and island hopping (via the northern North Atlantic).

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Smilax (Smilacaceae) From The Miocene Of Western Eurasia With Caribbean Biogeographic Affinities

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