Qi Wang 2,3,6 , Steven R. Manchester 3,5 , and David L. Dilcher 4

American Journal of Botany 97(12): 1982–1998. 2010.

F RUITS AND FOLIAGE OF P UERARIA (LEGUMINOSAE, PAPILIONOIDEAE) FROM THE NEOGENE OF EURASIA AND THEIR BIOGEOGRAPHIC IMPLICATIONS 1

Qi Wang2,3,6 , Steven R. Manchester 3,5 , and David L. Dilcher4

2 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, P. R. China; 3 Paleobotany and Palynology Laboratory, Florida Museum of Natural History, the University of Florida, Gainesville, Florida 32611-7800 USA; and 4 Department of Biology, Indiana University, Bloomington, Indiana 47405 USA

• Premise of the study : Pueraria (Leguminosae, Papilionoideae) is native in East Asia, South Asia, Southeast Asia, and Oceania and is well known as a rampant invasive weed in the southeastern United States (P. montana; better known as kudzu ), but relatively little is known about its early evolution and biogeographic origin. • Methods : On the basis of comparative analyses of the fruit and leafl et architecture of closely related extant and fossil taxa, we studied the fossil history and biogeography of Pueraria . • Key results : Fossil Pueraria is recognized on the basis of distinctive fruit and foliage from the Mio-Pliocene of middle latitudes in China, Japan, Abkhazia, and Croatia. Recognition of P. miothunbergiana from the Mio-Pliocene of China and Japan is re- inforced by a trifoliolate leaf as well as isolated lateral and terminal leafl ets. Pueraria shanwangensis sp. nov. represents the fi rst recognition of fossil Pueraria fruits. This fruit species co-occurs with P. miothunbergiana in the Middle Miocene Shan- wang fl ora and possibly represents the same population. Pueraria maxima (Unger) comb. nov., previously named as Dolichites maximus or Desmodium maximum , is recognized on the basis of leafl ets from the Miocene of Croatia and Abkhazia. Other prior fossil reports of Pueraria and Dolichites are reevaluated. • Conclusions : Pueraria had begun to diversify by at least the Middle Miocene and had spread into the Mio-Pliocene subtropical and temperate fl oras of the Balkan Peninsula, the Caucasus, and eastern Asia, which suggests the present diversity of this genus in tropical Asia and Oceania might have originated from the mid-latitudes of Eurasia.

Key words: biogeography; Dolichites ; kudzu; Leguminosae; Miocene; Neogene; paleobotany; Pueraria .

Pueraria DC. is the largest papilionoid legume genus of the climbers, lianas, or rarely shrubs distributed in East Asia, South subtribe Glycininae in the tribe Phaseoleae. D e Candolle (1825) Asia, Southeast Asia, and Oceania ( Lackey, 1981 ; van der named it after Marc Nicolas Puerari (1766– 1845), a Swiss pro- Maesen, 1985 , 1994 , 2002 ; Niyomdham, 1992 ; Lock and fessor of botany at the University of Copenhagen. Pueraria Heald, 1994; Wu et al., 1994; Lee, 1995; Zhang and Chen, contains about 15– 20 living species, which are usually strong 1995; Schrire, 2005; Le, 2007, 2008 ). Some species are used as ornamentals, for food (edible tubers), medicinal preparations, 1 Manuscript received 10 May 2010; revision accepted 7 October 2010. thickening agents, fi ber, pasture, fodder, erosion control, and The authors thank two anonymous reviewers for their invaluable green manure ( van der Maesen, 1994 , 2002 ; Wu et al., 1994 ; suggestions; K. Uemura (National Science Museum, Tokyo), W. Piller and Zhang and Chen, 1995 ; Schrire, 2005 ). Because of these benefi - M. Gross (Landesmuseum Joanneum, Graz), D. M. Erwin (the University of cial properties, Pueraria was introduced to many places of the California Museum of Paleontology, Berkeley), and W. A. DiMichele and world outside its native range. Puerari montana (Lour.) Merr. J. G. Wingerath (Smithsonian Institution, Washington, DC) for access to the (kudzu) was introduced into the United States at the Philadel- fossil collections; Y. B. Sun (Institute of Botany, the Chinese Academy of phia Centennial Exposition in 1876, but now it has become a Sciences [CAS], Beijing), for his excellent line drawings; and H. S. Wang rampant, invasive species or weed in the southeastern United and T. A. Lott (Florida Museum of Natural History), D. M. Wang (Peking University), L. J. G. van der Maesen (Wageningen Agricultural University), States, covering and outcompeting the native vegetation (Pap pert Y. V. Mosseichik (Russian Academy of Sciences), S. M. Snigirevsky et al., 2000 ; Forseth and Innis, 2004 ). Pueraria thus has at- (St. Petersburg State University), J. Kovar-Eder (Staatliches Museum f ü r tracted extensive attention from botanists, ecologists, and con- Naturkunde), A. Momohara (Chiba University), M. Long and E. Antobam servation biologists. However, relatively little is known about (New York Botanic Garden), J. Y. Guo (the Claremont Colleges), X. Q. Liu its early evolution, diversity, and biogeographic history. (Huazhong Agricultural University, Wuhan), H. H. Xu (Nanjing Institute of Pueraria fossils provide an historical perspective for the Geology and Palaeontology, Nanjing, CAS), and J. R. Tao, X. Y. Zhu, Y. F. early evolution, diversity, and biogeography of the genus. Hu Du, Z. F. Le, B. Liu, and J. Zhang (Institute of Botany, Beijing, CAS) for and Chaney (1938) described the fi rst fossil species of Pueraria their important help. This work was supported by the National Natural (i.e., P. miothunbergiana Hu et Chaney) on the basis of two Science Foundation of China (grant no. 40830209), Institute of Botany, CAS leafl ets from the Middle Miocene Shanwang Formation of (grant no. 110100P008), and a visiting scholar fellowship program from the Chinese Academy of Sciences to Q.W. Shandong Province, eastern China. On the basis of a comparison 5 Author for correspondence (e-mail: steven@fl mnh.ufl .edu ) with fossil leafl ets from the Kodor fl ora of Abkhazia, however, 6 E-mail: [email protected] Kolakovsky (1959 , 1964 ) considered P. miothunbergiana to be synonymous with a previously described legume fossil, doi:10.3732/ajb.1000167 Dolichites maximus Unger (1850, 1864 ), from the Miocene of

Radoboj, Croatia, and he transferred them to the extant legume Prague personal communication, 2010). Recently, the geological age of the Kodor genus Desmodium Desv. as D. maximum (Unger) Kolakovsky. fl ora has been specifi ed as Late Miocene (Mai, 1995, p. 414). (2) Kabutoiwa, Japan. Shakryl (1992) followed this taxonomic viewpoint; however, other The published photograph and line drawing of a leafl et specimen described under the name P. miothunbergiana by Ozaki (1991) from Mount Kabutoiwa in the bor- authors accepted P. miothunbergiana as a valid representative of der area of Nagano and Gunma Prefectures, Japan, was consulted. Recent radio- extant kudzu in the Mio-Pliocene of China, Japan, and Alaska metric dating indicates that the Kabutoiwa fl ora is middle Pliocene, about 3.5 Ma ( Tanai and Suzuki, 1972 ; Hayashi, 1975 ; WGCPC, 1978 ; Wolfe ( Kohei, 2007 ). (3) Inkyoyama, Japan. The published photographs of two leafl et and Tanai, 1980 ; Ozaki, 1991 ; Tao et al., 1999 ). Additional fossil fossils named P. tanaii Ozaki (1974) from the Miocene Inkyoyama hill of Gifu species of Pueraria also were described from the Oligo-Miocene Prefecture, Japan, were examined. (4) Siziman, Russia. The published photographs of China, Japan, and Russia (Akhmetiev, 1972; Ozaki, 1974; Tao of two leafl et fossils named P. sizimanica Akhmetiev (1972) from the Nitusi Cape, the northern end of the Siziman Bay of far eastern Russia, were consulted. Recent and Chen, 1983 ; van der Maesen, 1985 , 1994 , 2002 ; Uemura, radiometric data corroborate an Oligocene age for the Siziman fl ora (Akhmetiev et 1988; Tao et al., 2000; Akhmetiev et al., 2009). Nevertheless, it has al., 2009 ). (5) Lincang, China. The published photographs of two leafl et fossils remained uncertain whether all these Pueraria fossils were reliably named P. prethomsonii Tao et Chen and P. yunnanensis Franchet from the identifi ed. Therefore, the previously reported fossil leafl ets of Pu- Lincang region of Yunnan Province, southwestern China (Tao and Chen, 1983), eraria and Dolichites Unger desperately need reinvestigation. were consulted. The age for this locality is the Late Miocene (Tao et al., 2000). In this paper, we aim to investigate the fossil record of Puer- The macrofossils used in this study are preserved as impressions lacking cuti- cle. The systematic relations of the fruits and leafl ets were evaluated indepen- aria and to consider its biogeographic implications. On the ba- dently. An Internet identifi cation system for the legume fruits (INTKEY, available sis of a comparative analyses of the fruit and leafl et architecture at http://nt.ars-grin.gov/SBMLWeb/OnlineResources/Fabaceae/; Kirkbride et al., of closely related extant and fossil taxa, we corroborate the pre- 2003) was used to narrow the fi eld of candidate genera in the identifi cation pro- vious identifi cation of P. miothunbergiana from the Mio-Plio- cess. The fruit morphology of Pueraria was compared with that of related genera cene of China and Japan, and we reject prior reports of Pueraria (see Lee and Hymowitz, 2001 ). Cultivated kudzu vines at the Institute of Botany from the Oligo-Miocene of far eastern Russia and Alaska. (Beijing, CAS) were observed, and fresh leafl ets were collected. Herbarium specimens with closely similar leafl ets and fruits were examined at the China National Pueraria shanwangensis sp. nov. is instituted for the fruit fossils Herbarium (PE). Cleared leaf collections deposited at the University of California from the Middle Miocene Shanwang fl ora of eastern China, Museum of Paleontology, Berkeley, were examined online (available at http:// representing the fi rst discovery of Pueraria fruits in the fossil bscit.berkeley.edu/ucmp/). record. The leafl ets of D. maximus from the Middle Miocene of Photographs were taken with a digital camera (Panasonic DMC-FZ30, Radoboj in Croatia and Desmodium maximum from the Kodor Secaucus, New Jersey, USA). Figures were made with CorelDraw 10 program fl ora of Abkhazia are transferred to Pueraria as P. maxima (Corel, Ottawa, Ontario, Canada). Terminology used in the specimen descriptions follows Dilcher (1974), Herendeen (1992), and Ellis et al. (2009). (Unger) comb. nov., and the nomenclatural history of Dolichites is briefl y reviewed.

RESULTS MATERIALS AND METHODS The taxonomy of living Pueraria is mainly based on growth The macrofossils presented here were collected from the following localities. habit, leafl et form, characteristics of fl ower and infl orescence (1) Shanwang, China. The leafl et and fruit fossils were collected from diatoma- (e.g., number of fl owers per node, types of stipule and calyx, cal- ceous shale of the Shanwang Formation at Linqu County, Shandong Province, losities on the vexillum), pod morphology (e.g., shape, size, tex- in eastern China (lat. 36 ° 54 ´ N, long. 118 ° 20´ E). The specimens are deposited at the Institute of Botany, the Chinese Academy of Sciences (CAS), Beijing ture, pubescence, dehiscence and curling of valves), and seed (specimen numbers prefi xed with “ PE ” ); the Florida Museum of Natural History, number and morphology (e.g., shape, size, seed-coat ornamenta- University of Florida, Gainesville (UF); and the University of California Museum tion, shape and size of hilum) (Lackey, 1981; van der Maesen, of Paleontology, Berkeley (UCMP). The Shanwang Basin includes a famous 1985, 1994 , 2002 ; Wu et al., 1994; Lee, 1995; Zhang and Chen, fossil deposit with exquisitely preserved animals and plants that have been 1995; Le, 2008). Despite the putatively complex phylogenetic re- studied since the 1930s ( Hu and Chaney, 1938 ; Liu and Leopold, 1992 ; Yang lations within Pueraria (Lackey, 1981; Lee and Hymowitz, 2001; and Yang, 1994; Yang and Sun, 2000). The geological age of the Shanwang fl ora has been accepted as Middle Miocene (Li, 1981; Wang et al., 2006, 2007 ). Doyle et al., 2003 ), its characteristic leafl ets and fruits are very (2) Ch ōjabaru, Japan. A leafl et specimen deposited at the National Science Mu- useful for recognition of the genus. seum, Tokyo (NSM), and a trifoliolate specimen deposited at the Geological Museum of the Geological Survey of Japan, Tsukuba (GSJ), were examined. Family — Leguminosae Juss. They were collected from the Middle Miocene Chō jabaru Formation of Iki Is- Subfamily — Papilionoideae L. ex DC. land, Nagasaki Prefecture, Japan ( Hayashi, 1975 ; Takahashi, 1981 ). (3) Tribe — Phaseoleae DC. Takamine, Japan. A lobed leafl et specimen deposited at the National Science Museum, Tokyo, was examined. It was collected from the Late Miocene Takamine Subtribe — Glycininae Benth. Formation in the western marginal area of the Yonezawa Basin, Yamagata Pre- Genus — Pueraria DC. fecture, Japan ( Uemura, 1988 ). (4) Tyonek, Alaska, United States. A leafl et spec- Species — Pueraria shanwangensis Qi Wang, Manchester et imen from the Middle Miocene Tyonek Formation of Seldovia Point, Alaska Dilcher, sp. nov. (Fig. 1– 4, 6, 9) ( Wolfe and Tanai, 1980 ), was examined. It is deposited at the Smithsonian Insti- tution, Washington, DC. (5) Radoboj, Croatia. Five leafl et specimens and six fruit Specifi c diagnosis— Fruits linear-oblong or narrowly oblong, specimens deposited at Landesmuseum Joanneum (LMJ), the University of Graz, Austria, were examined. These specimens were collected from Radoboj, 2.4 – 5.1 cm long and 0.5 – 0.7 cm wide. Marginal sutures slightly Croatia, a classic Miocene locality ( Unger, 1838 , 1847 ; Brongniart, 1850 ). The thickened, constricted, and nonwinged. Unilocular and charta- geological age of the Radoboj fl ora recently has been accepted as Middle Mio- ceous. Seeds about 2– 5 in number, oblong, about 3.5– 4.5 mm cene ( Pantic, 1992 ; Kovar-Eder, 2003 ). long and 2.5– 3.0 mm wide, attached along the placental suture, Additional localities were included from the published literature, though we with seed length slightly oblique or parallel to fruit length. Fruit did not have access to the original specimens: (1) Kodor, Abkhazia. The pub- apex acute, acuminate or attenuate, with a straight or curved lished fi ve photographs and three line drawings of the leafl et specimens described under the name Desmodium maximum by Kolakovsky (1959 , 1964 ) from the early beak, 0.8 – 1.8 mm long. Base rounded or tapered, sessile or sub- Pliocene of the Kodor River, Abkhazia, were consulted because the original spec- sessile. Calyx and androecial sheath persistent. Calyx campan- imens unfortunately were destroyed by fi re (Zlatko Kvač ek, Charles University, ulate, 2.0 – 3.0 mm long, with teeth 2.0 – 2.5 mm long, pedicellate, 1984 American Journal of Botany [Vol. 97

Figs. 1 – 4, 9. Pueraria shanwangensis sp. nov. from the Middle Miocene Shanwang Formation of Shandong Province, eastern China. 1. Holotype, UF15839-54195. 2. Showing a persistent calyx and long, spreading hairs. PE 20000708. 3. Arrow points to an androecial sheath. PE 20000707. 4. Showing the contour and orientation of seeds. UF 15839-54193. 5. Two fruits of extant species P. montana (Lour.) Merr. Arrow points to an androecial sheath. PE 0929181 and PE 0936696. 6. Detail from Fig. 2 showing dense trichomes. 7 . Detail of upper part of a fruit in extant species P. montana with a portion of pericarp removed to show a nephroid seed (arrow). 8. Enlargement of the seed in Fig. 7. 9. Detail of upper part of the fossil fruit in Fig. 4 showing a longi- tudinally oriented, oblong seed, slightly oblique to the fruit length (arrow). Bars = 1 cm, except in Fig. 8, which is 0.5 cm. December 2010] Wang et al. — Fossil history and biogeography of P UERARIA 1985

Table 1. Comparisons between Pueraria shanwangensis and other taxa with similar fruit morphology in the tribe Phaseoleae (sensu Lee and Hymowitz, 2001 ).

Fruit morphology Surface Seed Taxa Size (cm) Shape Base Apex Marginal suture pubescence number

Pueraria shanwangensis Qi 2.4 – 5.1 × 0.5 – 0.7 Linear-oblong or Rounded or Acute, acuminate, Slightly constricted, Dense, spreading, 2 – 5 Wang, Manchester et Dilcher1 narrowly oblong tapered or attenuate slightly thickened long hairs Pueraria montana (Lour.) 4 – 13 × 0.6 – 1.3 Linear or narrowly Rounded or Acute, acuminate, Slightly constricted, Dense, spreading, 2 – 10 Merr. 2 – 4,7 – 8 oblong tapered or attenuate slightly thickened long hairs Glycine max (L.) Merr. 3,6,8 4 – 7.5 × 0.8 – 1.5 Oblong or slightly Narrowly Acute Constricted Dense, long hairs 2 – 5 falcate cuneate Vigna marina (Burm.) Merr.3,8 3.5 – 6 × 0.8 – 0.9 Linear-oblong Rounded or Acute or Slightly constricted, Sparse, soft hairs 2 – 6 tapered acuminate thickened Neonotonia wightii (Arn.) 1.5 – 3.5 × 0.2 – 0.6 Slightly moniliform Tapered Acuminate Constricted, slightly Spreading hairs 2 – 10 J. A. Lackey3 to linear thickened Ophrestia pinnata (Merr.) 2.5 – 4 × 0.6 – 0.8 Linear-oblong Tapered Acute or No constriction, Long, spreading 2 – 5 Verdc.3,8 acuminate slightly thickened hairs Shuteria involucrata 3 – 5 × 0.2 – 0.6 Linear Rounded Acute No constriction Long, soft hairs 5 – 6 (Wall.) Walp.3,8 Dunbaria rotundifolia 3 – 5 × 0.6 – 0.8 Linear-oblong Narrowly Acute No constriction, Short, soft hairs 6 – 8 (Lour.) Merr.5,8 cuneate slightly thickened Kennedia rubicunda Vent.3 3 – 7 × 0.7 – 1.2 Linear Short tapered Acuminate No constriction, Spreading hairs 4 – 9 to tapered slightly thickened Nogra guangxiensis 4.5 – 5 × 0.5 – 0.6 Narrowly oblong Rounded Acute No constriction Thick, long hairs 6 – 8 C. F. Wei3,8 or linear Sinodolichos lagopus 5 – 6.5 × 0.6 – 0.75 Linear Short tapered Acute No constriction Thick, long hairs 7 – 10 (Dunn) Verdc. 3,8 to rounded Teyleria koordersii 3 – 4 × 0.4 – 0.5 Linear or slightly Short tapered Short tapered to No constriction Long, compressed 4 – 8 (Backer) Backer3,8 falcate to rounded rounded or spreading hairs References: 1 fossil fruit specimens used in this paper; 2 van der Maesen, 1985; 3 Kirkbride et al., 2003; 4 Le, 2008; 5 specimen PE-1112697; 6 specimen PE-01840115; 7 specimens PE-0929181 and PE-0936696; 8 Lee, 1995.

3.0– 4.0 mm long. Fruit surface with dense, spreading, simple 2.0 – 3.0 mm long with lobes 2.0 – 2.5 mm long, and pedicel 3.0 – hairs, 2.0 – 3.0 mm long. 4.0 mm long ( Fig. 2 ). Androecial sheath about 3 mm long, less than 1 mm wide (Fig. 3). Surface covered with dense, spreading, Etymology— The specifi c epithet refers to the type locality, simple hairs, 2.0– 3.0 mm long (Figs. 1– 4, 6, 9). Shanwang. Comparison and discussion— These fossils obviously rep- Holotype— UF15839-54195 (Fig. 1) (designated here; de- resent a type of legume fruit. On the basis of nine key characters posited at Florida Museum of Natural History, the University of (i.e., fruit shape, length, width, apex, base, marginal suture, sur- Florida, Gainesville). face pubescence, calyx, and seed number) entered in INTKEY for legume fruits (see Materials and Methods), we were able to Paratypes — PE 20000708 (Figs. 2, 6), 20000707 (Fig. 3), narrow the fossil identifi cation to taxa within the subfamily 9901060, 9901910, 20000700, 20000701, 20000702, and Papilionoideae. Most of the candidates fell into the tribe Phase- 20000710 (Institute of Botany, CAS, Beijing); UF15839- oleae, subtribe Glycininae, so we further concentrated on the 54190, 15839-54191, 15839-54192, 15839-54193 (Figs. 4, 9), taxa within this subtribe as presented in the phylogenetic analy- and 15839-54194. ses of Lee and Hymowitz (2001). The set of fruit characters highlighted in Table 1 indicates these fossils conform well with Description— Fruits linear-oblong or narrowly oblong, 2.4– a group of genera in the tribe Phaseoleae, having linear to nar- 5.1 cm long ( x = 3.9 cm, excluding associated calyx and pedi- rowly oblong, nonwinged, multiseeded, pubescent pods with cel), 0.5 – 0.7 cm wide ( x = 0.6 cm, excluding the length of hairs persistent calyces. Although there are numerous instances of on both margins), straight or curved, and with no wings along convergence and parallelism in the pods of extant Legumino- the placental suture (Figs. 1– 4 ). Sutures slightly thickened and sae, the suite of characters seen in these fossils, particularly in- constricted, or strongly constricted because of abortive ovule. cluding the dense covering of long hairs (compare Figs. 6, 7), Fruits preserved with carbonaceous remnants indicate that orig- lends confi dence in the identifi cation to a subset of genera in- inal texture appears unilocular and chartaceous. Seeds oblong, cluding Pueraria . Our identifi cation of these fruits is also infl u- about 3.5– 4.5 mm long and 2.5– 3.0 mm wide, attached along enced by their co-occurrence with the leafl et fossils identifi able the placental suture, about 2 – 5 in number, oriented with their as Pueraria at the Shanwang locality discussed later. Among length slightly oblique or parallel to the fruit length ( Figs. 4, 9 ). previously published legume genera based on leafl ets from the Fruit apex acute, acuminate, or attenuate, with a straight or diverse Shanwang assemblage (Hu and Chaney, 1938; WGCPC, curved beak, 0.8– 1.8 mm long. Base rounded or tapered, sessile 1978 ; Tao et al., 1999 ; Wang et al., 2006 , 2007 ), Pueraria is the or with a very short stipe, 1.0 – 1.5 mm long, and associated with only genus with pods of this kind; i.e., these fruits are clearly a persistent calyx and an androecial sheath. Calyx campanulate, distinct from those of Albizia Durazz., Cercis L., Gleditsia L., 1986 American Journal of Botany [Vol. 97

Figs. 10 – 13. Pueraria miothunbergiana Hu and Chaney emend. from the Middle Miocene Shanwang Formation of Shandong Province, eastern China. 10. A line drawing from Hu and Chaney (1938, Pl. 28, Fig. 1). 11 . Holotype, UCMP 410001. This is the counterpart of the specimen fi gured by Hu and Chaney (1938, Pl. 28, Fig. 1). 12. A larger lateral leafl et. PE 52961 (WGCPC, 1978, Pl. 91, Fig. 5). 13. A smaller, somewhat scalloped lateral leafl et. PE 52297 ( WGCPC, 1978 , Pl. 85, Fig. 3 ). Bars = 2 cm. December 2010] Wang et al. — Fossil history and biogeography of P UERARIA 1987

Figs. 14 – 17. Pueraria miothunbergiana Hu and Chaney emend. from the Middle Miocene Shanwang Formation of Shandong Province, eastern China. 14. A larger lateral leafl et with a short, pulvinate petiolule. UF15839-54198. 15. A smaller lateral leafl et with a short, pulvinate petiolule and a cleft on right margin. UF15839-54197. 16, 17. Two larger lateral leafl ets. UF15839-54196 and UF15839-54199. Bars = 2 cm. 1988 American Journal of Botany [Vol. 97

Gymnocladus Lam., Indigofera L., Sophora L., Wisteria Nutt., veins alternate and predominantly opposite percurrent, convex, and Podocarpium A. Braun ex Stizenberger (formerly Podogo- straight or sinuous, close, with 2– 4 mm intervals, and oblique, nium Heer). maintaining an approximately constant angle of ca. 120 ° with Extant Pueraria species, e.g., P. montana and P. yunnanensis , the midvein, almost perpendicular to the secondary veins, more usually bear a persistent calyx, an androecial sheath, and lon- or less parallel to each other, and interconnected by transverse gitudinally oriented seeds (van der Maesen, 1985; Lee, 1995; anastomoses. Quaternary veins forming a regular polygonal Kirkbride et al., 2003; Le, 2008; Le and Zhu, 2009; Figs. 5, 7). reticulum. Areolation well developed. Marginal ultimate veins Some of the fossil specimens preserve the seed outlines within the looped and sometimes fi mbrilate at the laminar base. pod, indicating that the seeds were oriented as in the extant species, with their long axes obliquely longitudinal with respect to the Comparison and discussion— The fossil leafl ets presented pod axis ( Figs. 4, 9 , cf. Figs. 7, 8). Pueraria shanwangensis repre- here are characterized by their markedly large asymmetrical sents the fi rst recognition of Pueraria fruits in the fossil record (lateral) and symmetrical (terminal) leafl ets with eucamptodro- and provides corroboration for the prior reports based on leafl ets. mous and strong basal secondary veins and a short, pulvinate petiolule. Although mostly known only from isolated leafl ets, a Species— Pueraria miothunbergiana Hu and Chaney, emend. specimen from the Middle Miocene Chō jabaru Formation of (Fig. 10–21, 23) Iki Island, Japan (Hayashi, 1975), shows a relatively complete Pueraria miothunbergiana Hu and Chaney in Carnegie Inst. leaf with three leafl ets and a pulvinus at the base of the petiole Washington Publ. 507: 52, Pl. 28, Fig. 1. 1938 (Fig. 10 herein); ( Fig. 21 ). The fossil leafl ets are extremely similar to those of the Hayashi, Fossils from Chō jabaru, Iki Island, Japan, 25, Pl. 17, trifoliolate genera in the papilionoid legume tribe Phaseoleae Fig. 4, & Pl. 18, Fig. 5. 1975 (Figs. 20– 21 herein); WGCPC, Fos- and allies, for example, several species of the extant genera sil Plants of China 3: Cenozoic Plants from China, 109, Pl. 85, Desmodium ( Figs. 25 – 26 ), Dolichos L. (Fig. 27), Erythrina L., Fig. 3 , Pl. 91, Fig. 5, & Pl. 92. 1978 ( Figs. 12 – 13 herein); Ozaki Mucuna Adans., Pueraria ( Fig. 22 ), and Rhynchosia Lour. in Bull. Kanagawa Pref. Mus. Nat. Sci. Special Issue: 133, Fig. Leaf/leafl et architecture serves to distinguish Pueraria from 29– 2 , Pl. 5, Fig. 11. 1991; Tao et al., Shanwang Plant Fossils, 41 these other genera (Table 2, Figs. 24– 27 ). In particular, our & 70, Pl. 28, Figs. 2 – 3 . 1999. leafl et fossils, like modern kudzu, have a distinctive eucamptodromous pattern of secondary veins, i.e., the veins arch toward Synonymy— Pueraria tanaii Ozaki in Sci. Rep. Yokohama Nat. the margin and merge gradually into a marginal vein, without Univ. Sect. 2 Biol. Geol. Sci. 21: 15, Pl. 2, Fig. 11, Pl. 3, Fig. 3. forming a series of subordinate loops (Fig. 24), whereas other 1974; Pueraria sp. in Uemura, Late Miocene Floras in Northeast genera tend to have brochidodromous secondary veins, as doc- Honshu, Japan, 149, Fig. 34, Pl. 9, Fig. 8. 1988 ( Fig. 19 herein). umented in Dolichos ( Fig. 27 ), Erythrina, and most species of Mucuna ( Ettingshausen, 1854 ; Wilmot-Dear, 1984 ; Yu and Holotype— UCMP 410001 (Fig. 11) [the counterpart of the Chen, 1991 ). Although Mucuna prurien DC. bears eucampto- specimen fi gured by Hu and Chaney (1938 , Pl. 28, Fig. 1 ), depos- dromous secondary veins, its tertiary and quaternary veins are ited at the University of California Museum of Paleontology, noticeably different from those of Pueraria ( Table 2 ). Seven Berkeley]. species of Desmodium differ by their camptodromous-reticulo- dromous, semicraspedodromous, craspedodromous-cladodro- Other specimens examined— PE 52961 (Fig. 12), 52297 (Fig. mous, to craspedodromous venation (Deokule and Kate, 2001). 13), 09512 (Fig. 18), 09513, 09514, 081023 and 081024; Size can also help in distinguishing taxa. For example, many UF15839-54198 ( Fig. 14 ), 15839-54197 ( Fig. 15 ), 15839-54196 species of Desmodium ( Ohashi, 1973 ; Lee, 1995 ; Krings, 2004 ; ( Fig. 16 ), 15839-54199 ( Figs. 17, 23 ); NSM-PP 15691 ( Fig. 19 ) Figs. 25 – 26 ) and Rhynchosia ( Meikle, 1951 ; Thulin, 1981 ) usu- and PP 11094b ( Fig. 20 ); GSJ-F7732 ( Fig. 21 ). ally bear smaller leafl ets that would not compare well with these fossils. The terminal leafl ets are easily distinguished from Cer- Emended description (new characters are italicized)— Leaf pin- cis foliage with basal actinodromous venation (e.g., Cercis nately trifoliolate, up to 18 cm long, with a thickened pulvinus at miochinensis Hu and Chaney, 1938, from the Shanwang fl ora). petiolar base; leafl et 5.2 – (8.5) – 18.5 cm long, 4.8 – (5.5) – 16.0 cm The lateral leafl ets are superfi cially similar to leaves of some wide, and; petiolule 3.0 – 9.0 mm long, with a thickened pulvinus; nonlegume genera (e.g., Alangium Lam., Byttneria Loefl ., and terminal leafl ets grossly symmetrical, suborbicular, rhomboid-ovate fossil Plafkeria Wolfe) with largely asymmetrical foliage, but or wide ovate, with acuminate apex, and convex, obtusely cuneate these usually bear a longer petiole ( > 1 cm long) and/or a promi- or obtusely rounded base; lateral leafl ets strongly asymmetrical, nent cordate base ( Tanai, 1989 ; Yu and Chen, 1991 ; Table 2 ). In ovate, wide ovate to very wide ovate, rarely scalloped or lobed, with addition, this leafl et fossil shares with extant Pueraria a series of an acuminate, acute or rarely rounded apex, and obtusely cuneate, prominent external branches to the secondary veins (agrophic, or broadly rounded, truncate or even slightly cordate base. Margin pectinal veins), that are particularly well developed in the lower entire, slightly undulate or entire with a cleft on the larger side of the portion of the lamina. These compound agrophic veins, along lamina, or palmately lobed with a shallow, rounded sinus and a with predominantly opposite percurrent tertiaries, and polygonal medium, acuminate sinus; texture chartaceous . reticulate quaternaries support the identifi cation of these fossils Venation pinnate. Primary vein (i.e., midvein) moderately to Pueraria . Modern Pueraria leafl ets sometimes have well-de- thick, straight or slightly curved. Secondary veins in 5– 7 pairs, veloped intersecondaries, which have not been observed in this including 1 – 2 strong basal veins, alternate or opposite, diverg- fossil species. Perhaps this is because of the relatively small num- ing from the midvein at 30 ° – (40 ° – 45 ° ) – 60 ° , eucamptodromous, ber of fossil leafl ets available for study, limiting our knowledge curving slightly then arching abruptly upward along the margin of the full range of variation in the leafl et architecture. and becoming a fi mbrial vein, without higher-order vein loops. Hu and Chaney (1938) fi rst described this species under the Compound agrophic veins, 1 – 5, arising on the exmedial side of name P. miothunbergiana from the Shanwang Formation on the secondaries at 30 ° – 90 ° . Intersecondary veins absent. Tertiary basis of a well-preserved terminal leafl et (i.e., holotype, no. 184, December 2010] Wang et al. — Fossil history and biogeography of P UERARIA 1989

Figs. 18 – 21. Pueraria miothunbergiana Hu and Chaney emend. from the Miocene of China and Japan. 18. A trilobate leafl et from the Middle Miocene Shanwang Formation of Shandong Province, eastern China. PE 09512. 19. A trilobate leafl et from the Late Miocene Takamine Formation of Yamagata Prefecture, Japan. NSM-PP15691 ( Uemura, 1988 , Pl. 9, Fig. 8). Figs. 20, 21. A leafl et and a leaf from the Middle Miocene Chō jabaru Formation of Iki Island, Nagasaki Prefecture, Japan. 20. The leafl et showing obtuse apex and a short pulvinate petiolule. NSM-PP 11094b ( Hayashi, 1975 , Pl. 17, Fig. 4 ). 21. The leaf showing the organic connections of three leafl ets, with a long, pulvinate petiole. GSJ-F7732 ( Hayashi, 1975 , Pl. 18, Fig. 5). Bars = 2 cm. 1990 American Journal of Botany [Vol. 97

Fig. 22. The leafl et morphology of living kudzu Pueraria montana (Lour.) Merr. from a cultivated vine at the Institute of Botany, the Chinese Academy of Sciences, Beijing. Bar = 2 cm. reillustrated here in Fig. 10 ) and a fragmentary lateral leafl et, lar leafl ets described as P. tanaii (see Pl. 2, Fig. 11, Pl. 3, Fig. 3, which have been lost. Fortunately, the holotype’ s counterpart in Ozaki, 1974) from the Miocene Inkyoyama fl ora survives at the University of California Museum of Paleon- of Japan are relatively small (5.2– 8.2 × 4.8– 6.0 cm) and bear tology ( Fig. 11 ). Additional specimens of P. miothunbergiana eucamptodromous secondary veins, compound agrophic veins were collected more recently from the same Shanwang (1 – 4), and a short petiolule (2.4 – 4 mm long); these salient fea- locality( WGCPC, 1978 ; Tao et al., 1999 ; this paper) and from tures agree with the diagnostic characters of P. miothunbergi- the Middle Miocene Chō jabaru Formation of Iki Island, Japan ana . From the Late Miocene Takamine fl ora of Japan, Uemura ( Hayashi, 1975 ; Figs. 20 – 21 ). The three rhombic to suborbicu- (1988) described Pueraria sp. on the basis of an incompletely December 2010] Wang et al. — Fossil history and biogeography of P UERARIA 1991

Figs. 23– 27. Lateral leafl et architecture in Pueraria miothunbergiana Hu et Chaney and other taxa. 23. Partial enlargement of the upper part of P. miothunbergiana in Fig. 17 showing the fi ne venation. UF15839-54199. 24. Partial enlargement of the upper part of living P. montana leafl et from a cultivated kudzu vine at the Institute of Botany, the Chinese Academy of Sciences. 25, 26. Two lateral leafl ets of Desmodium elagans DC. showing craspedodromous secondary veins that are basal or suprabasal. PE-544507. 27. A lateral leafl et of Dolichos lablab L. showing brochidodromous secondary veins. PE-01838780. Bars = 2 cm. preserved leafl et lacking the lower part (Fig. 19). The lobed men identifi ed as P. miothunbergiana was reported from the shape and venation pattern from the upper part of the leafl et middle Pliocene of Mount Kabutoiwa, Japan (see Fig. 29– 2 , Pl. resemble those of P. miothunbergiana ( Fig. 18 ), so we include 5, Fig. 11, in Ozaki, 1991 ); it shows very similar architectural it in the same species. The geologically youngest leafl et speci- features to the Miocene leafl ets of China and Japan. 1992 American Journal of Botany [Vol. 97 Areole Yu Yu and 6 development Good Good Good Good Poor Poor Poor Good Poor or moderate Good Good Good Good vein ° reticulate Irregular Irregular reticulate Irregular reticulate Irregular reticulate Irregular reticulate or freely ramifying Irregular reticulate ramifying Irregular Irregular reticulate Irregular Irregular reticulate Irregular reticulate Regular Regular reticulate Regular reticulate Regular reticulate ed ed Ettingshausen, 1854; 5 vein 4 ed Irregular ed Freely ° ed ed Ramifi Alternate percurrent or ramifi Percurrent or ramifi Ramifi Alternate percurrent, sinuous or convex Opposite percurrent, straight Opposite percurrent, straight or convex Percurrent or ramifi Percurrent or ramifi Opposite percurrent, straight Alternate and predominantly opposite percurrent Alternate and opposite percurrent Alternate and mainly opposite percurrent vein 3 ° 12 – 14, basal no Eucamptodromous, 14 – 16, basal 2 – 3 8 – 10, basal 2 Brochidodromous, 8 – 10, basal 2 14 – 20, basal 2 8 – 12, basal 2 – 4 14 – 18, basal 4 Brochidodromous, 6 – 8, basal 2 eucamptodromous, 12 – 14, basal 2 – no or 1 12 – 16 basal 4 10 – 14, basal 1 – 2 10 – 14, basal 2 12 – 14, basal 1 – 2 vein 2 ° moderate or weak Moderate Eucamptodromous, moderate Moderate Craspedodromous or Stout Eucamptodromous, Moderate Eucamptodromous, Moderate Eucamptodromous, Moderate Eucamptodromous, Entire Moderate Craspedodromous, Entire Stout or EntireEntire Moderate Brochidodromous, Moderate Entire, crenate or rarely trilobed Entire Moderate Brochidodromous, Entire Stout or Entire or slightly undulate Entire, somewhat revolute Entire, slightly undulate, entire with a cleft or trilobed Entire, sometimes undulate slightly Entire, slightly undulate, bilobed to trilobed specimens PE-01838778, PE-01838780, and PE-01838781; 4 acuminate Acute or acuminate Long acuminate or acute. mucronate Acuminate or caudate- acuminate Acute or obtuse Short acuminate or acute Rounded, obtuse, acute, acuminate, or mucronate Acuminate with drip tip Acuminate, acute, or rarely rounded Acuminate or acute Acuminate, acute, or obtuse et/leaf architecture. et/leaf Deokule and Kate, 2001; truncate or slightly cordate wide cuneate or truncate or cordate cordate wide cuneate, or truncate or cuneate cuneate, truncate, or slightly cordate concavo-convex, wide cuneate, truncate or slightly cordate cuneate, truncate or slightly cordate 3 1 – 1.5 Rounded 2 – 8 Strongly direct observation from a cultivated vine at the Institute of Botany, the Chinese Academy of Sciences, Beijing. the Chinese vine at the Institute of Botany, from a cultivated direct observation (cm) Base Apex Margin 1 0.2 – 0.3 Rounded, 0.2 – 0.4 Rounded, 0.5 – 0.7 Wide cuneate Acuminate Entire Stout Brochidodromous, 0.3 – 0.4 Rounded, 0.2 – 0.3 Wide cuneate 1.3 – 3.0 Rounded 0.3 – 0.9 Convex, wide 0.3 – 0.6 Convex, slightly 0.4 – 1.0 Narrow to wide Petiole 10 0.08 – 0.1 Rounded Acute or short et UCMP-ACL506; et UCMP-ACL506; Tanai, 1989; 9 and other taxa with similar leafl Ovate, wide ovate or wide ovate Ovate, obliquely ovate elliptical triangular-ovate, Wide ovate-rhombic Rhombic-ovate Rhombic-ovate or wide ovate ovate, Narrow oblong or lanceolate ovate, Wide cordate or orbicular Wide ovate, ovate, Wide or rhombic-ovate wide ovate very Ovate-elliptical, Ovate-elliptical, rhombic, wide ovate, orbicular-rhombic ovate, Narrow or wide ovate ovate, Obliquely ovate, Obliquely ovate, rhomboid-ovate, rarely wide ovate, suborbicular or scalloped or Obliquely ovate wide ovate, or rhomboid-ovate rhomboid-orbicular obliquely ovate, Wide suborbicular ovate, or rhombic cleared leafl 2

Le, 2008; 8

× × ×

× × × ×

Pueraria × × × × 0.8 or ovate- Ovate 4.1 Ovate 0.3 – 0.4 Rounded Obtuse or × × 8.0 – 8.2 3.8 – 5.9 1.4 6.0 – 10.0 5.0 – 8.0 6.0 4 – 10 2.5 – 7.0 7 – 14 2 – 3.5 7 – 23 5.5 – 6 2.5 – 2.7 2.4 – 4.5 2.0 – 7.0 1.5 – 5.0 2.7 – 11 2 – 10.0 5.2 – 18.5 4.8 – 16 8.3 – 15.0 5.5 – 12.0 7 – 26 5 – 22

9 1,2

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DC.

6,9

L. this paper L. 5 specimen PE-544507;

1 7 – 8,10, this paper van der Maesen, 1985; van 7

5 this paper

6 2. Comparisons between 5 3 References: miothunbergiana Hu and Chaney Tanai (Oishi et Huzioka) Klein ex Willd. Willd. Klein ex Oliv. Roxb. ex Colebr. Spreng. corallodendron DC. (Unger) Qi Wang, Wang, (Unger) Qi Manchester et Dilcher Merr. (Lour.) DC. Table Taxa Size (cm) Shape Dolichos lablab Chen, 1991; Pueraria Leguminosae Juss. (Leaﬂ Leguminosae Desmodium elegans Dolichos ciliatus Alangiaceae DC. (Leaf) Alangium faberi (Leaf) Sterculiaceae Vent. Byttneria aspera Juss. (Leaf) Tiliaceae Plafkeria basiobliqua Erythrina humeana Erythrina Desmodium laxiﬂ orum Pueraria maxima Pueraria montana Mucuna pruriens December 2010] Wang et al. — Fossil history and biogeography of P UERARIA 1993

Bearing in mind the characters typical of living and fossil Puer- Figs. 1– 2 . 1959 (Fig. 31 herein); Kolakovsky in Pliocenovaya aria , we rejected some leafl et fossils previously identifi ed as Pu- fl ora Kodora, 114, Pl. 43, Figs. 8 – 10 , Pl. 44, Figs. 1 – 2 . 1964; eraria from the Oligo-Miocene of China, Japan, Russia, and the Shakryl in Herendeen et Dilcher, Advances in Legume System- United States. Three leafl et specimens identifi ed as P. miothun- atics 4: the Fossil Record, 201, Fig. 3, text-fi gs. 4 – 5, Fig. 4 . bergiana (see Pl. 15, Fig. 3, Pl. 16, Figs. 2, 6, in Hayashi, 1975) 1992. from the Middle Miocene Ch ō jabaru Formation of Japan bear a longer petiolule (> 1 cm long) or lack strong basal secondary veins, Lectotype— LMJ 76781 (Fig. 28) (designated here. Unger ’ s so we excluded these specimens from Pueraria. A lobed lamina Pl. 8, Fig. 3 , 1864, deposited at Landesmuseum Joanneum, the described as P. miothunbergiana (see Pl. 4, Fig. 14 in Tanai and University of Graz, Austria). Suzuki, 1972) from the Miocene of Ogawa, Japan bears brochidodromous secondary veins and a prominent cordate base, so it can- Other specimens examined— LMJ 76782 and 76785 (Figs. not be accepted as Pueraria. The lamina identifi ed as a leafl et of 29 – 30 ) (Unger ’ s Pl. 7, Figs. 1, 3 , 1864). P. miothunbergiana (see Pl. 15, Fig. 3, in Wolfe and Tanai, 1980 ; USNM 208461) from the Middle Miocene Tyonek Formation of Description— Leaf inferred to be pinnately trifoliolate from Alaska is very small (5.4 × 4.2 cm), with a weak midvein, fewer the symmetry of individual leafl ets. Leafl ets 8.3 – 15.0 cm long, secondary veins (fewer than 4 pairs), and irregularly percurrent 5.5 – 12.0 cm wide, with thickened petiolules, 3.0 – 6.0 mm tertiary veins, which do not conform to Pueraria . The laminae long. Terminal leafl ets more or less symmetrical, rhomboid- described as P. sizimanica (see Pl. 75, Fig. 7, in Akhmetiev, 1972 ; orbicular or rhomboid-ovate, with acuminate apex, and con- Pl. 4, Fig. 11, in Akhmetiev et al., 2009) from the Oligocene Siz- vex or somewhat concavo-convex base; lateral leafl ets strongly iman fl ora of far eastern Russia are 8 – 12 × 6 – 11 cm in size. They asymmetrical, ovate or wide ovate, with short acuminate or bear brochidodromous secondary veins, however, so we dismissed acute apex, and broadly rounded, truncate, or even slightly this species from Pueraria . Two leafl et specimens described as P. cordate base. Margin entire, sometimes undulate slightly; tex- prethomsonii and P. yunnanensis (see Pl. 17, Fig. 2 , Pl. 18, Fig. 9, ture chartaceous. Venation pinnate with a moderately thick, in Tao and Chen, 1983 ; Pl. 71, Fig. 3 , Pl. 56, Fig. 5, in Tao et al., straight or slightly curved primary vein (midvein) and 5 – 7 2000) from the Late Miocene Lincang region of Yunnan Prov- pairs of secondary veins, including a strong basal pair. Sec- ince, southwestern China, are relatively small (5.8 – 6.8 × 4 – 5 cm) ondary veins alternate or opposite, diverging from the mid- and lack strong basal secondary veins, so we rejected these two vein at 30 ° – 60 ° , eucamptodromous, curving slightly then fossil species from Pueraria . arching abruptly upward along the margin and becoming a Pueraria miothunbergiana occurrences from the Mio-Plio- fi mbrial vein, lacking higher-order vein loops. Compound cene of China and Japan share salient characters of leafl et archi- agrophic veins, 1 – 5, arising on the exmedial side of secondar- tecture, but it is possible these leafl ets represent only an ies at 30 ° – 90 ° . Intersecondary veins present. Tertiary veins extremely similar morphotype borne by multiple species, as it alternate and opposite percurrent, convex, straight or sinuous, is also the case that some living Pueraria species are almost usually branching, with 2– 6 mm intervals, almost perpendicu- indistinguishable on only the basis of leafl et architecture. On lar to the secondary veins, more or less parallel to each other, the other hand, they may truly represent a single biological spe- and interconnected by transverse anastomoses. Quaternary cies. We have observed in the fi eld that leafl ets, even from the veins form a regular polygonal reticulum. Areolation well de- same vine of modern kudzu, exhibit considerable variation veloped. Marginal ultimate veins looped and often fi mbrilate from entire to scalloped, bilobed, or palmately lobed ( Fig. 22 ), at the laminar base. as do the fossil leafl ets presented here. Therefore, leafl et lobes of Pueraria may refl ect developmental variation. Such devel- Comparison and discussion— Unger (1838) published a opmental variations in the lamina margin also occur in some monotypic legume fossil genus Dolichites on the basis of D. non-legume taxa, such as Sassafras albidum (Nutt.) Nees europaeus Unger for a pod that he considered to be similar to (Lauraceae Juss.) and Alangium faberi Oliv. (Alangiaceae DC.) those of the extant legume genus Dolichos. Later, Unger ( Table 2 ). (1850 , 1864 ) emended Dolichites to include leafl ets as well as Pueraria miothunbergiana (leafl ets) and P. shanwangensis fruits from the Middle Miocene of Radoboj, Croatia, and rec- (fruits) presented here were both collected from the Middle ognized two species: D. europaeus , for the fruits previously Miocene Shanwang Formation. It is probable these leafl ets described, and D. maximus , for both isolated fruit and leafl et were detached from the same plant species that produced these specimens. Both species were fi rst illustrated by Unger (1864) , fruits, representing the same Pueraria population in the Middle and the original specimens are deposited at the Landesmu- Miocene Shanwang fl ora. seum Joanneum, Graz, Austria. We reexamined these specimens and concluded that Dolichites should be used only for Species— Pueraria maxima (Unger) Qi Wang, Manchester the fruit fossils originally named as D. europaeus because the et Dilcher, comb. nov. (Fig. 28–31) specimens later placed in D. maximus appear to be generically distinct. Further, D. maximus included heterogeneous ele- Basionym— Dolichites maximus Unger in Genera et Species ments that may belong to at least 3 different taxa. Among the Plantarum Fossilium, 489. 1850; this name was not validly pub- fi gured original material of D. maximus ( Unger, 1864 ), three lished in Unger, Chloris Protogaea, 85. 1847 (nomen nudum ), leafl et specimens (i.e., LMJ-76781, 76782, and 76785) should and was fi rst illustrated by Unger in Denkschr. K. Akad. Wiss. be transferred to Pueraria ( Figs. 28 – 30 ), whereas other leaf- Math.-Naturwiss. Cl. 22: 25, Pl. 7, Figs. 1– 6 , Pl. 8, Figs. 3– 4. lets and fruits need taxonomic reconsideration. The fruits that 1864 (leafl ets in Figs. 28 – 30 herein). Unger (1864) described as D. maximus are quite different from those of the type species D. europaeus and may belong Synonym— Desmodium maximum (Unger) Kolakovsky in to another legume genus. Remarkably, abundant other legume Trudy Sukhumskogo Bot. Sada 12: 240, Pl. 12, Fig. 1, Pl. 13, fruits also were described from the Middle Miocene of Radoboj 1994 American Journal of Botany [Vol. 97

Figs. 28 – 31. Pueraria maxima (Unger) comb. nov. from the Miocene of Croatia and Abkhazia. Figs. 28 – 30. P. maxima from the Middle Miocene of Radoboj, Croatia. 28. Lectotype, LMJ-76781 ( Unger, 1864 , Pl. 8, Fig. 3 ). Showing a lateral leafl et with an intersecondary vein. 29, 30. Showing two terminal leafl ets. LMJ-76782 and 76785 (Unger, 1864, Pl. 7, Figs. 1, 3). 31. P. maxima from the Late Miocene of Kodor, Abkhazia. Showing a lateral leafl et redrawn from Kolakovsky ’ s (1959 , Pl. 12, Fig.1 ) line-drawing. Bars = 2 cm. December 2010] Wang et al. — Fossil history and biogeography of P UERARIA 1995

Fig. 32. Map showing modern and fossil distribution of Pueraria DC. Gray area refers to the geographic distribution of living species (after van der Maesen, 1985). From left to right, black dots refer to the following fossil localities: Radoboj, Croatia (Unger, 1864; Pant ic, 1992); Kodor, Abkhazia (Ko- lakovsky, 1959, 1964 ; Shakryl, 1992); Shanwang, China (Hu and Chaney, 1938; Tao et al., 1999; Wang et al., 2006, 20 07 ); Chō jabaru, Japan (Hayashi, 1975 ; Takahashi, 1981 ); Inkyoyama, Japan ( Ozaki, 1974 ); Kabutoiwa, Japan ( Ozaki, 1991 ); and Takamine, Japan ( Uemura, 1988 ).

( Unger, 1864 ), but their accurate systematic affi nities still 1888 ), and Italy ( Massalongo, 1851 ; Meschinelli and Squinabol, need additional confi rmation. It is possible that further study 1892; Principi, 1926), but these identifi cations are very may lead to Pueraria-type fruit fossils from Radoboj and ad- doubtful because of poor descriptions or illustrations. Nev- jacent regions in the future. ertheless, we expect there may be additional fossil Pueraria Kolakovsky (1959, 1964 ) reduced D. maximus and P. mi- from midlatitude regions of Europe. So far, no fruits of this othunbergiana to Desmodium maximum, which he described genus have been recognized from Europe. from the Late Miocene Kodor fl ora, Abkhazia ( Fig. 31 ). Shakryl (1992) agreed with this reclassifi cation. We compared these fossil leafl ets from the Miocene of Abkhazia, BIOGEOGRAPHIC IMPLICATIONS Croatia, China, and Japan as well as the leafl ets of extant Desmodium, Dolichos , and Pueraria ( Table 2 ) and found Modern species of Pueraria are usually strong climbers and that the fossil leafl ets from Croatia and Abkhazia are quite lianas, only rarely shrubs, which inhabit seasonally dry tropical distinct from Desmodium (see explanation in P. miothunber- and subtropical to warm temperate forests, rain forests, and giana) and should be reclassifi ed into Pueraria. Hence, we scrub vegetation with various moisture regimes ( van der Maesen, made a new combination, i.e., P. maxima (Unger) comb. 1985 , 1994 , 2002 ; Schrire, 2005 ; Le, 2008 ). They mainly rely nov. This species differs from P. miothunbergiana in having on other self-supporting plants, climbing them to increase their no lobation in the lamina margin. One terminal leafl et of P. exposure to higher light levels present at the top of the forest maxima (see Pl. 43, Fig. 8, in Kolakovsky, 1964 ) shows a canopy, and they are highly sensitive to cold temperatures and slightly undulate margin, which is also a feature that can increased CO2 levels (Forseth and Innis, 2004). Therefore, tem- be seen in living kudzu leafl ets (Table 2). We also expect to perature, moisture, and interactions with supporting trees are fi nd Pueraria-type fruit fossils from Kodor and adjacent important ecological factors affecting the physiology, metabo- regions. lism, growth, development, and dispersal of Pueraria . The ex- Leafl et fossils of Dolichites have been previously reported istence of some large lianas such as Pueraria , Wisteria , and from the Tertiary of Europe, North America, and Australia. Vitis L. in the Miocene Shanwang fl ora of eastern China ( Hu However, the identifi cations of this genus from the Eocene and Chaney, 1938 ; WGCPC, 1978 ; Tao et al., 1999 ; Wang of North America ( Berry, 1916 ; Ball, 1931 ) and Australia et al., 2006 ) indicates this fl ora most probably lived in subtropical (Ettingshausen, 1887) are untenable because these leafl ets or warm temperate, humid conditions. The climate conditions either have an obviously cordate base or are narrowly ovate that Pueraria populations experienced in Shanwang are, more in shape. Dolichites also was reported on the basis of leafl ets or less, similar to those of the Middle to Late Miocene Pueraria - from the Eocene of France ( Watelet, 1866 ), the Oligocene of bearing fl oras in Inkyoyama, Japan ( Ozaki, 1974 ); Chō jabaru, Hungary ( Andre á nszky and Nov á k, 1957 ), and the Miocene Japan (Hayashi, 1975, p. 12; Takahashi, 1981 ); Takamine, Japan of Georgia (Palibin, 1937), but these identifi cations are un- (Uemura, 1988, p. 69); Kodor, Abkhazia (Kolakovsky, 1964, p. reliable because the leafl ets either lack eucamptodromous 200; Shakryl, 1992, p. 204); and Radoboj, Croatia (Mai, 1995, secondary and basal agrophic veins or are triangular and nar- p. 438). In contrast, the middle Pliocene Pueraria -bearing fl ora rowly ovate in shape. Moreover, Dolichites was mentioned, but from Kabutoiwa of Japan primarily refl ected cool temperate not fi gured, from the Late Eocene diatomite of Kuclin, Czech aspect ( Ozaki, 1991 , p. 44). Therefore, these results imply that Republic ( Ettingshausen, 1869 ). Also, it was reported from the Pueraria populations during the Neogene, like modern kudzus, post-Eocene of Slovenia ( Pilar, 1883 ), Austria ( Ettingshausen, may have been closely associated with a range of temperate or 1996 American Journal of Botany [Vol. 97 subtropical conditions, participating in moist forests, deciduous Andre á nszky , G. , and É . Nov á k . 1957 . Neue und interessante terti ä re forests, or gallery forests. Pfl anzenarten aus Ungarn 3. Annales Historico-Naturales Musei Leafl et and fruit fossils presented here demonstrate that Pu- Nationalis Hungarici , series nova 8 : 43 – 55 . eraria had begun to diversify by at least the Miocene and had Ball , O. M. 1931 . A contribution to the paleobotany of the Eocene of spread into the Mio-Pliocene fl oras of the Balkan Peninsula, the Texas. Bulletin of the Agricultural and Mechanical College of Texas, Caucasus, and eastern Asia (China and Japan) ( Fig. 32 ). The Series 4 2 : 1 – 173 . Berry , E. W. 1916 . The Lower Eocene fl oras of southeastern North America. eastern Asian P. miothunbergiana appears to have existed from United States Geological Survey Professional Paper 91: 1– 481. the middle Miocene to the middle Pliocene, an interval of about Brongniart , M. A. 1850 . Chronological exposition of the periods of veg- 12.5 Myr. The southeastern European and Caucasian Pueraria etation and the different fl oras which have successively occupied the populations apparently disappeared after the Miocene – early surface of the Earth. Annals and Magazine of Natural History, Series Pliocene with the uplift of the Himalayan – Tibetan plateau and 2 6 : 248 – 270 . the retreat of the Tethys ( An et al., 2001 ), the desertifi cation in the Crame , J. A. , and B. R. Rosen . 2002 . Cenozoic palaeogeography and the Asian interior (Guo et al., 2002), the establishment of the Asian rise of modern biodiversity patterns. In J. A. Crame and A. W. Owen monsoon system (Sun and Wang, 2005), and the desiccation of [eds.], Palaeobiogeography and biodiversity change: The Ordovician the Mediterranean Sea (Messinian salinity crisis) (Fauquette and Mesozoic-Cenozoic radiations, special publications 194, 153– et al., 2006). Therefore, the occurrence of fossil Pueraria in the 168. Geological Society, London, UK. Balkan Peninsula, the Caucasus region, and eastern Asia may De Candolle , M. 1825 . Notice sur quelques genres et esp è ces nou- represent refugia of moisture-loving elements in the Neogene velles de l é gumineuses, extradite de M é moires pr é sent é s à la Soci é t é d’ Histoire naturelle de Genè ve, pendant le cours des annè es 1823 et subtropical and warm temperate fl oras of the northern hemi- 1824. Annales des Sciences Naturelles (Paris) 4 : 90 – 103 . sphere. To some extent, our results support Kovar-Eder ’ s (2003 , Denk , T. , and G. W. Grimm . 2005 . Phylogeny and biogeography of p. 387) viewpoint that the Mediterranean region increasingly Zelkova (Ulmaceae sensu stricto) as inferred from leaf morphology, constituted a refuge suitable for the Late Miocene – Pliocene ITS sequence data and the fossil record. Botanical Journal of the broad-leaved evergreen forests. The pattern of disjunction in Linnean Society 147 : 129 – 157 . the Miocene Pueraria populations is still seen today, for ex- Deokule , S. S. , and S. S. Kate . 2001 . Foliar architecture of some medici- ample, with Pterocarya Kunth (Manchester, 1987; Manchester nally important plants of genus Desmodium Desv. In J. K. Maheshwari et al., 2009 ) and Zelkova Spach ( Manchester, 1989 ; Denk and and A. P. Jain [eds.], Recent researches in plant anatomy and mor- Grimm, 2005 ), and it may have been even more obvious in the phology, 87 – 92. Scientifi c Publishers (India), Jodhpur, India. Miocene, including, for example, the extinct legume genus Dilcher , D. L. 1974 . Approaches to the identifi cation of angiosperm leaf Podocarpium ( Liu et al., 2001 ; Wang et al., 2007 ). remains. Botanical Review 40 : 1 – 157 . Major collision of India with Southeast Asia in the early Doyle , J. J. , J. L. Doyle , and C. Harbison. 2003 . Chloroplast-expressed Cenozoic enlarged the land-area connected to Eurasia, and sub- glutamine synthetase in Glycine and related Leguminosae: Phylogeny, gene duplication, and ancient polyploidy. Systematic Botany 28 : 567 – 577 . sequent linkage with Australasia during the Miocene led to im- Ellis , B. , D. C. Daly , L. J. Hickey , K. R. Johnson , J. D. Mitchell , P. proved connections between Eurasia and Oceania ( Morley, Wilf , and S. L. Wing . 2009 . Manual of leaf architecture, 1 – 190. 1998 ; Hall, 2001 ; Crame and Rosen, 2002; Metcalfe, 2002). Cornell University Press, Ithaca, New York, USA. Recent paleobotanical studies have suggested that temperate Ettingshausen , C. F. 1854 . Ü ber die Nervation der Blä tter der Papiliona- and subtropical fl oras of Yunnan and Tibet in southwestern ceen. Sitzungsberichte der Mathematisch-Naturwissenschaftlichen China began to enter northeast India during the Middle Mio- Classe 12 : 600 – 663 . cene ( Tao et al., 2000 ; Mehrotra et al., 2005 ), implying that the Ettingshausen , C. F. 1869 . Die fossile Flora des Terti ä r-Beckens von expansion of Pueraria from warm temperate and subtropical Bilin. Denkschriften der Kaiserlichen Akademie der Wissenschaften . East Asia to tropical Asia and Oceania might have taken place Mathematisch-Naturwissenschaftlichte Classe 29 : 1 – 110 . after the mid-Miocene with the northward drift and collision of Ettingshausen , C. F. 1887 . Beitr ä ge zur Kenntniss der Terti ä rfl ora southern landmasses into Eurasia. Although the modern diver- Australiens. Denkschriften der Kaiserlichen Akademie der sity center of Pueraria is situated in Indo-Malesia (van der Wissenschaften . Mathematisch-Naturwissenschaftlichte Classe 5 3 : 81 – 142 . Maesen, 1985; Niyomdham, 1992; Lock and Heald, 1994; Ettingshausen , C. F. 1888 . Die fossile Flora von Leoben in Steiermark Schrire, 2005 ; Le, 2008 ; Fig. 32 ), and the genus was classifi ed 2. Denkschriften der Kaiserlichen Akademie der Wissenschaften. as one of the tropical Asian areal-types (Wu, 1991), the fossil Mathematisch-Naturwissenschaftlichte Classe 54 : 319 – 384 . occurrences indicate Pueraria was established earlier in midlat- Fauquette , S. , J.-P. Suc , A. Bertini , S. M. Popescu , S. Warny , N. Bachiri itude regions of Eurasia. Hence, its present distribution may Taoufiq , M.-J. Perez Villa , et al. 2006 . How much did climate refl ect secondary dispersal during or since the Neogene. force the Messinian salinity crisis? 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