Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Paliurus Fruits from the Oligocene of South China and Their Phytogeographic Implications

  • Jun-Ling Dong,

    Affiliations School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China, Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology, CAS, Nanjing, 210008, China

  • Bai-Nian Sun ,

    bnsun@lzu.edu.cn

    Affiliations School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China, Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology, CAS, Nanjing, 210008, China

  • Fu-Jun Ma,

    Affiliation School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China

  • Qiu-Jun Wang,

    Affiliation School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China

  • Pei-Hong Jin,

    Affiliation School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China

  • Wen-Jia Wang,

    Affiliation School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China

  • Peng Deng,

    Affiliation School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China

  • Yi Yang,

    Affiliation School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China

  • Xiao-Jing Li

    Affiliation School of Earth Sciences & Key Laboratory of Mineral Resources in Western China (Gansu Province), Lanzhou University, Lanzhou, 730000, China

Paliurus Fruits from the Oligocene of South China and Their Phytogeographic Implications

  • Jun-Ling Dong, 
  • Bai-Nian Sun, 
  • Fu-Jun Ma, 
  • Qiu-Jun Wang, 
  • Pei-Hong Jin, 
  • Wen-Jia Wang, 
  • Peng Deng, 
  • Yi Yang, 
  • Xiao-Jing Li
PLOS
x

Abstract

Paliurus favonii Unger is recognized and described based on fruits from the Oligocene Ningming flora of Guangxi, South China. Characteristics of the present specimens include circular winged fruits that are 10.0–11.5 mm in diameter with a central endocarp at 3.0 to 4.0 mm in diameter. The specimens fall into the morphological range of the fossil species P. favonii, which has been observed in other Cenozoic sites in the Northern Hemisphere. The present discovery represents the lowest latitude distribution of P. favonii in the world, and we are presenting the first P. favonii fossil described with detailed cuticular characteristics from China. Further, this finding demonstrates that the genus existed in the Oligocene Ningming region, South China, and provides new information for understanding the fossil history. The dispersal mode for winged fossils demonstrates that wind dispersal is well-represented in the Oligocene Ningming flora.

Introduction

Paliurus Mill. of the plant family Rhamnaceae contains five extant species of deciduous or evergreen shrubs and trees. The genus is distributed in southern portions of Europe (Northern and Eastern Mediterranean, as well as parts of Northern Africa and eastward to Western Asia) and Asia (China, Korea, Japan, and Vietnam; Fig 1; [1, 2]), and most occurrences are limited to a moist, equable, and temperate climate in tropical to warm temperate regions [3, 4]. P. hirsutus Hemsl., P. orientalis (Franch.) Hemsl. and P. hemsleyanus Rehder ex. Schirarend & Olabi are endemic to China, while P. ramosissimus (Lour.) Poir. occurs in southern China, Korea, Japan and Vietnam. The four species typically grow at elevations below 2000 m [5]. P. spina-christi Mill. is exclusively distributed in the meridional and submeridional regions of southern Europe and western Asia [1] at elevations below 2300 m [4]. P. spina-christi is also cultivated as an ornamental plant or hedge in Qingdao (Shandong Province), China [5] and North Africa [4]. Paliurus has broad ecological tolerance in China and occurs mainly in the southwest, central-south and east regions, with a northernmost extension in Gansu Province [5].

The fossil record for Paliurus is extensive in the Cenozoic of the Northern Hemisphere, including western North America, central Europe and eastern Asia, and its age ranges from the Eocene to Pliocene [4]. Asia includes a long fossil history of Paliurus since the Middle Eocene, which is based on leaves and fruits from Ube flora, Japan [6] and based on leaves from Liaoning, China [7]. Burge and Manchester [4] emended the diagnosis of P. favonii, which was recognized by Unger [8] based on morphological analyses, and it was proposed that all Asia fruit records within the P. favonii morphological variation range were included in this species. Paliurus has been broadly distributed geographically since the Eocene from North America and Asia, became widespread and morphologically diverse through the Miocene. Paliurus fruit fossils are rarely encountered in China, particularly in the Oligocene sediments. Fruit fossils can provide reliable data for deducing the evolutionary and biogeographical history of a genus, even a family.

Rhamnaceae is a cosmopolitan family that tends to be observed in xeric regions and may be classified as mesothermal [9]. Paliurus fossils have been frequently observed in mesic ecological settings from tropical to warm temperate regions [4], which is consistent with the ecological requirements of the extant species. In Asia, the geographical distribution of Paliurus macrofossils indicates that the genus has grown in a warm temperate climate since the mid-Eocene [10]. The winged fruits of Paliurus are well-adapted for wind dispersal and are important to the reproductive ecology and early diversification of the genus.

In this paper, we identify and describe a new occurrence of Paliurus favonii Unger from the Oligocene Ningming Formation of Ningming Basin, Guangxi Province, South China based on the distinctive fruit features; this is the lowest latitude distribution for the species. Our finding provides additional fossil evidence for understanding the evolution of Paliurus. Moreover, the phytogeographic history of Paliurus is discussed.

Materials and Methods

Geological setting

Three Paliurus fruit fossils were collected from the shallow lacustrine deposits of the Ningming Formation in the Ningming Basin (at 22°09′15.77″N, 107°01′23.11″E), Guangxi Zhuang Autonomous Region, South China (Fig 2). The Ningming Formation is composed primarily of gray-dark gray mudstone with light yellow shaly siltstone and fine-grained sandstone. The precise age remains unknown due to a lack of volcanic rocks and mammals in the Ningming Formation stratum. Presently, scholars consider two hypotheses for the age of the Ningming Formation. On the one hand, the Ningming Formation is considered to be Miocene based on fish and bivalve fossils [11]; on the other hand, it is also considered to be of the Late Eocene to Oligocene based on the palynological assemblages [12]. Although the Ningming Formation age is hotly debated, previous studies on plant and fish fossils from the same stratum (e.g., Palaeocarya [13, 14], Bauhinia [15, 16], Cephalotaxus [17], Cupressus [18], Calocedrus [19], Ailanthus [20], Laurophyllum [21], Buxus [22], Chuniophoenix, Livistona [23], Ecocarpia [24] and Huashancyprinus [25]) support the notion that the Ningming Formation belongs to the Oligocene age, which is adopted in this paper.

thumbnail
Fig 2. Fossil locality showing Ningming County of Guangxi, South China.

https://doi.org/10.1371/journal.pone.0140653.g002

Material and preparation

These specimens were preserved as compression fossils. Photographs were collected using a Sony DSC-T70 digital camera and examined in detail under a Leica MZ 12.5 stereomicroscope. The extant specimens for morphological comparison are from the herbarium of the School of Life Sciences, Lanzhou University and the South China Institute of Botany, Chinese Academy of Sciences. All specimens are preserved at the Laboratory of Paleontology in Lanzhou University.

The fossil specimen cuticles were prepared by removing residual mineral matrix with 30% HCl and HF, successively, and bleaching with 65% HNO3 followed by treating with 5% KOH to obtain the cuticle. After washing several times, a portion of the cuticle samples was dyed and then mounted on thin slides for observation by light microscopy. The other cuticles were dehydrated and mounted on stubs for examination by SEM. The extant specimens’ cuticles were prepared using a 1:1 solution of glacial acetic acid and 30% H2O2. The prepared cuticles for both the fossil and extant specimens were observed and photographed using a Leica DM4000B multifunctional biological microscope.

The maps of the modern distribution and fossil locality were drawn using CorelDraw X6 software. The palaeogeographic map that shows the Paliurus macrofossil distribution was plotted using ODSN software. The fruit morphology terms are from Harris and Harris [26] and Burge and Manchester [4]; Conover [27] was used for the fruit cuticle term. The fruit dimensions were calculated in accordance with Burge and Manchester [4]: A fruit diameter, the average distance across the fruit wing based on two perpendicular measurements; B wing width, the average width of the wing measured at four points 90°; and C receptacle diameter, the average distance across the receptacle based on two perpendicular measurements.

Ethics statement

All necessary permits were obtained for the described sampling sites in verbal or written form. Three Paliurus fossils were collected in Ningming County, Guangxi Province, South China. The field work was permitted by the local government. For the extant plant sampling sites, permits were verbally obtained from the herbarium office of the School of Life Sciences, Lanzhou University, China and the South China Institute of Botany, Chinese Academy of Sciences. The extant plant materials did not involve endangered or protected species.

Results

Family

Rhamnaceae Jussieu

Tribe

Paliureae Reissek ex Endl.

Genus

Paliurus Miller

Species

Paliurus favonii Unger

Figs 3A–3G; 4A–4F;

thumbnail
Fig 3. Morphological characteristics of Paliurus favonii and similar extant species for morphological comparison.

A–G. Morphological characteristics of Paliurus favonii. A. Specimen no. LDGSW-2014-222. D. Specimen no. LDGSW-2014-223. G. Specimen no. LDGSW-2014-224. B, E. Showing the distinctly domed and indehiscent endocarp (arrow). C, F. Showing obvious persistent receptacular rim (arrow). H. Extant Paliurus hemsleyanus. I. Extant Paliurus orientalis. J. Extant Cyclocarya paliurus (Juglandaceae). A, D, G. Scale bars = 5.0 mm. B, C, E, F. Scale bars = 1.0 mm. H–J. Scale bars = 10.0 mm.

https://doi.org/10.1371/journal.pone.0140653.g003

thumbnail
Fig 4. Anatomical characteristics of Paliurus favonii and Paliurus hemsleyanus.

A–C. Endocarp epidermal characteristics of Paliurus favonii under light micrographs, showing undulate cell walls. C. Magnification of stomatal apparatus (arrow) from B (arrow), showing anomocytic stoma. D. Epidermal characteristics of Paliurus favonii under SEM. E, F. Internal anatomy of Paliurus favonii under SEM, showing three layers structure of the endocarp. G–I. Wing epidermal characteristics of extant Paliurus hemsleyanus, showing anomocytic stoma (arrow). A–C, G–I. Scale bars = 50.0 μm.

https://doi.org/10.1371/journal.pone.0140653.g004

Specimen No

LDGSW-2014-222, LDGSW-2014-223, LDGSW-2014-224.

Lectotype

LMJ (Landesmuseum Joanneum, Graz) 76518, designated by Kovar-Eder et al. [28], pl. 11, fig.7. Same specimen figured by Unger [8], p. 147, pl. 50, fig. 6.

Age

Oligocene

Number of specimens studied

Three

Description

The fruit is a winged drupe in which the indehiscent endocarp is encircled by the orbicular wing with an irregular undulate margin and 10.0–11.5 mm in diameter. The endocarp in the apical view is distinctly domed, 5.0–6.0 mm in diameter and 1.0 mm deep. The pedicel is not preserved; only a round attachment scar remains on the base of the ovary (Fig 3C and 3F). The receptacle is flat with a pronounced rim surrounding a round pedicel scar; the receptacle is 3.0–4.0 mm in diameter. The vascular ridges radiating from base of the pedicel to the edge of the receptacle form a persistent scar on the basal side of the ovary that can be observed but is not inconspicuous in fossils (Fig 3C). The wing is typically thin with fine radiating, dichotomizing, and anastomosing venation, 2.5–3.0 mm in width, chartaceous, and oriented perpendicular to the main axis of the fruit. The edges of the wing show obvious lobes (Fig 3A). Structurally, the fruit pericarp is composed of three distinctive layers (Fig 4E and 4F). The epicarp is glabrous, and the two-layered mesocarp is thickest and composed of spongy and palisade parenchyma. Due to the lignified endocarp, the inner structure was not preserved.

The epidermal cells of the endocarp are quadrilateral with oblique end walls, have an irregular shape, are somewhat elongate and are typically arranged in longitudinal files. The size is more or less uniform, 11.0–40.0 μm long and 3.0–18.0 μm wide with a length/width ratio up to 9.0 (Fig 4A–4D). The periclinal walls are even, have wax ornamentations on the surface, are mostly rectangular and are slightly elongate or polygonal. The anticlinal walls appear distinctly deep-sinuous with a U shape (Fig 4D) and are thickened. The stomata are sparse, elliptic, and approximately 13.0 μm long and 8.5 μm wide. The stomata are anomocytic, and the guard cells are slightly sunken (Fig 4C).

Affinities

Affinities with extant taxa.

The morphological characteristics of Paliurus fruit include a circular or orbicular wing encircling a central endocarp with a superficial similarity to Cyclocarya Iljinskaya (Juglandaceae), Asteranthos Desfontaines (Lecythidaceae) and Dioncophyllum Baillon (Dioncophyllaceae) [4, 10, 29, 30]. However, the Paliurus fruit can be distinguished by its bi- or tri-locular endocarp and persistent receptacular rim or its persistent scar around the base of the ovary [4, 30, 31]. However, for Cyclocarya paliurus (Batal.) Iljinsk., the receptacular rim is lacking, and a single locule is partitioned at its base into 2 or 4 compartments [30, 31]. The wing venation is mainly subparallel (radiating), occasionally anastomoses and does not dichotomize before the medial part [30, 32]. Asteranthos Desf. is a Neotropical genus and contains a single species, A. brasiliensis, which is a species native to Amazonian Brazil and Venezuela [33]. Its fruit is globose to ovate, monospermous and indehiscent; the wing is membranaceous, and the calyx is persistent on the fruit as a circular rim [10, 34, 35]. Dioncophyllum thollonii Baill. is a member of the family Dioncophyllaceae, which is predominantly restricted to western Africa tropical rainforests. Its ovary is unilocular [36], and the fruit shape is disk-shaped with a larger ellipsoidal wing that is approximately 5.0–12.0 cm in diameter (Table 1; [10, 37]).

thumbnail
Table 1. Comparision between Paliurus and other taxa with similar fruit morphology.

https://doi.org/10.1371/journal.pone.0140653.t001

Five extant Paliurus species can be partitioned into two groups based on their fruit morphology and dimensions. The first group is the P. spina-christi group, which is comprised of P. spina-christi, P. orientalis and P. hemsleyanus, and the second group is the P. ramosissimus group, which consists of P. ramosissimus and P. hirsutes [4, 5]. In the P. spina-christi group, the wing is thin, chartaceous, 2.0–10.0 mm in width, and equatorially extended with limited development of spongy parenchyma in the mesocarp [4]. The fruit dimensions are much larger than the fossil specimens (Table 2). However, the wing index is 0.2–0.3, which is similar to our specimens. In the P. ramosissimus group, the wing is thick, robust, and wedge-shaped at the longitudinal section with a well-developed spongy parenchyma in the mesocarp, and the fruit is pubescent. By comparing the fossil specimens with the two extant groups, the present specimens are more similar to the first group based on the wing texture, fruit morphology and dimensions, and wing/fruit and receptacle/fruit indexes.

To more precisely assign the present fossils, we compared our specimens with the cuticular characteristics of the extant species. The fossil species are almost identical to the extant species in orientation and stomata type (Fig 4C and 4I), but they differ in the epidermal cell wall morphology. The anticlinal walls of the present specimens are distinctly deep-sinuous (Fig 4D) and thickened, which differ from the extant species that feature almost straight anticlinal walls (Fig 4G–4I).

thumbnail
Table 2. Morphological characteristics of extant and fossil Paliurus species (characteristic data from Burge and Manchester [4]).

https://doi.org/10.1371/journal.pone.0140653.t002

Affinities with fossil taxa.

Paliurus fossil fruits were reported as abundant in the Cenozoic deposits of the Northern Hemisphere and presented varied morphologies and dimensions. Burge and Manchester [4] made a detailed summary and emended the diagnosis of P. favonii. They concluded that, except for P. clarnensis, most Paliurus fruits including European, Asian, and North American records ranging from the Eocene to Pleistocene, should be considered the P. favonii that was described by Unger [8] based on both the fruits and leaves from the Miocene deposits near Parschlug, Austria. All Asian fruit dimensions and wing widths fall within the P. favonii morphological continuum. The morphological analysis data (e.g., wing width, fruit diameter, receptacle diameter, wing index, receptacle index, and endocarp depth) of the present fossil fruits fall within the P. favonii morphological continuum (Table 3), thus the present specimens should be considered P. favonii species. P. favonii spans and even exceeds the entire range of modern species [4].

thumbnail
Table 3. Morphological characteristics of present and other known fossil specimens (characteristic data from Burge and Manchester [4], Li et al. [10] and Correa et al. [30]).

https://doi.org/10.1371/journal.pone.0140653.t003

The present specimens are similar to Paliurus clarnensis, P. microcarpa and Archaeopaliurus boyacensis in morphological characteristics. However, certain additional characteristics are distinctive [4, 10, 30]. The Archaeopaliurus boyacensis was found in the late Cretaceous (Maastrichtian) of Colombia, northern South America [30]. The endocarp is 12.0 mm in width and 4.0 mm in depth; the fruit is 35.0 mm in diameter. The fruit dimensions are larger than those of the present specimens. P. clarnensis was reported from the Middle Eocene of Red Gap, Jefferson County, Oregon and overlaps with P. favonii in fruit and endocarp dimensions [4]. However, the receptacle index of P. clarnensis is smaller than the present specimens. P. clarnensis has a larger fruit (i.e., 18.5–23.5 mm) with a narrower receptacle rim (i.e., 1.2–1.8 mm). P. microcarpa from the Miocene of Tiantai County in Zhejiang Province of China was documented by Li et al. [10] and exhibits clear differences in wing index and endocarp depth (Table 3). The P. microcarpa endocarp is 3.0–4.0 mm in depth, and the wing index is 0.1–0.2 mm, which is outside the range of the present specimens. Table 3 includes an outline of the fruit characteristics that differentiate the fossil representatives of Paliurus.

Discussion

Currently, Paliurus is widely distributed in Asia and Eastern Europe [1], but abundant fossil data, including fruits, endocarps, and leaves, indicate a broader distribution in the Cenozoic (Fig 5). The earliest reliable Paliurus fruit fossil evidence is from the Early Eocene Wind River Formation of Wyoming, North America [31], and most recent occurrences are from the Pleistocene of Yamashiro Province, Japan [38]. In North America, the Paliurus fruits and leaves are from the western and southeastern United States, and the age spans from the Early Eocene to Middle Miocene [31, 39]. In Europe, the Paliurus fruits and leaves have been reported from the Czech Republic, Austria, Germany, France, and Poland, and the age spans from the Oligocene to Pliocene [8, 28, 40]. In Asia, Paliurus fossil records are from Japan, China, Siberia, and Kazakhstan from the Middle Eocene to Pleistocene [6, 7, 10, 38]. The fossils are well-represented in the Miocene localities, but the Pliocene and Pleistocene records were limited to Europe and Asia [4]. In addition, they were widely distributed in the middle latitudes of the Northern Hemisphere during a large portion of its history.

thumbnail
Fig 5. Palaeogeographic distribution of Paliurus macrofossils (including fruits, leaves and endocarps) [4, 10, 41].

A. Eocene, at 41.2 Ma. B. Oligocene, at 28.1 Ma. C. Miocene, at 13.82 Ma. D. Pliocene, at 3.6 Ma.

https://doi.org/10.1371/journal.pone.0140653.g005

In China, Paliurus fossil records are rare compared with fossil records elsewhere in the world. The earliest report of Paliurus was published based on leaves from the Middle Eocene of Fushun, Liaoning [7, 42], and other fossil records including leaves or fruits, were reported from the Early Miocene of Yunnan and Shandong [42], and from the late Middle Miocene to early Late Miocene of Tiantai, Zhejiang [10]. The fossil records are undoubtedly incomplete in China, and, previously, such records from the Oligocene strata of this country did not exist. Our finding reveals the lowest latitude distribution of Paliurus favonii and provides a new fossil record, which is the first fossil described with detailed cuticular characteristics in the Oligocene sediment from south China. This recognition of Paliurus demonstrates that this genus existed in the Ningming region, South China, where it is currently distributed–by the Oligocene. It further aids in understanding the radiation process of the genus.

Winged fruits that represent various angiosperm families are frequently found in many Cenozoic fossil localities [43, 44]. Fruits that fall from the mother plants may be dispersed by wind with a potential dispersal distance that depends on the tree size, but the dispersal distance rarely exceeds one hundred to a few hundred meters [45, 46]. The Paliurus fruit, with a single surrounding wing, facilitates wind dispersal by gliding and undulating but not with significant cumulative forward motion [47]. Many fossil winged fruits that are functionally similar to the winged drupe of Paliurus have been reported from low latitude, moist forests in the Ningming Basin, such as Palaeocarya (Juglandaceae) [13, 14] and Ailanthus (Simarubaceae) [20], which might be associated with wind dispersal. Further, other wind diaspores, such as scattered winged seeds of Pinaceae, Chaneya (Rutaceae), Burretiodendron (Tiliaceae), Acer (Anacardiaceous) Ulmus (Ulmaceae) and Fraxinus (Oleaceae), have also been found from the Ningming Flora. Furthermore, genera with winged fossils may compose a certain proportion of the pollen sum from the Ningming microflora [12], e.g., Fraxinoipollenites 0–2.0%; Platycaryapollenites 0–1.9%; Momipites, 0.4–2.8%; and Ulmipollenites, 1.2–4.6%. The presence of wind-dispersed species suggests that sufficient winds were present in Ningming flora during the Oligocene.

Acknowledgments

We thank Zheng-Jie Liu, Ling-Wei Wu (Lanzhou University) for collecting fossil specimens in fieldwork. Thanks to De-Fei Yan, San-Ping Xie, Jing-Yu Wu, Ke-Nan Liu (School of Earth Science, Lanzhou University, China) for offering relevant literature and suggestions, to Jun-Lin Chen for drawing the geographic distribution maps; to Jian-Bin Pan (School of Life Sciences, Lanzhou University, China) for providing extant specimens.

Author Contributions

Conceived and designed the experiments: JD BS FM QW. Performed the experiments: JD PJ WW PD. Analyzed the data: JD BS FM QW. Contributed reagents/materials/analysis tools: JD BS FM QW PJ WW PD YY XL. Wrote the paper: JD.

References

  1. 1. Schirarend C, Olabi MN. Revision of the genus Paliurus Tourn. ex. Mill. (Rhamnaceae). Botanische Jahrbucher fur Systematik, Pflanzengeschichte und Pflanzengeographie 1994; 116: 333–359.
  2. 2. Schirarend C. Pollen morphology of the genus Paliurus (Rhamnaceae). Grana 1996; 35: 347–356.
  3. 3. Richardson JE, Fay MF, Cronk QCB, Chase MW. A revision of the tribal classification of Rhamnaceae. Kew Bulletin 2000; 55: 311–340.
  4. 4. Burge DO, Manchester SR. Fruit Morphology, Fossil History, and Biogeography of Paliurus (Rhamnaceae). International Journal of Plant Sciences 2008; 169: 1066–1085.
  5. 5. Chen YL, Schirarend C. Rhamnaceae. In: Wu ZY, Raven P. eds. Flora of China 12. Beijing: Science Press and St Louis Missouri Botanical Garden Press; 2007. p. 115–168.
  6. 6. Huzioka K, Takahasi E. The Eocene flora of the Ube coal-field, southwest Honshu, Japan. Journal of the Mining College, Akita University, series A 1970; 4: 1–88.
  7. 7. WGCPC. Cenozoic Plants from China, Fossil Plants of China: Beijing. 1978.
  8. 8. Unger F. Chloris Protogaea. Engelmann, Leipzig 1847.
  9. 9. Richardson JE, Chatrou LW, Mols JB, Erkens RHJ, Pirie MD. Historical biogeography of two cosmopolitan families of flowering plants: Annonaceae and Rhamnaceae. Philosophical Transactions of the Royal Society of London Series B, Biological sciences 2004; 359: 1495–1508. pmid:15519968
  10. 10. Li XC, Wang HF, Leng Q, Xiao L, Guo JF, He WL. Paliurus (Paliureae, Rhamnaceae) from the Miocene of East China and its Macrofossil–based Phylogenetic and Phytogeographical History. Acta Geologica Sinica (English Edition) 2014; 88: 1364–1377.
  11. 11. Chen GJ, Chen YF, Kuang GD, Zhu QP. Biostratigraphy of Tertiary fossil fishes from Ningming Basin, Guangxi Vertebrata Palasiatica 2004; 42: 81–85.
  12. 12. Wang WM, Chen GJ, Chen YF, Kuang GD. Tertiary palynostratigraphy of the Ningming basin, Guangxi. Journal of Stratigraphy 2003; 27: 324–327.
  13. 13. Li HM, Chen YF, Chen GJ, Kuang GD, Huang ZT. Tertiary fossil winged fruits of Palaeocarya from Ningming of Guangxi. S China. Acta Palaeontologica Sinica 2003; 42: 537–547.
  14. 14. Chen YF, Manchester SR, Song ZQ, Wang HS. Oligocene fossil winged fruits of tribe Engelhardieae (Juglandaceae) from the Ningming Basin of Guangxi province, South China. International Journal of Latest Research in Science and Technology 2014; 3: 13–17.
  15. 15. Chen YF, Zhang DX. Bauhinia larsenii, a fossil legume from Guangxi, China. Botanical Journal of the Linnean Society 2005; 147: 437–440.
  16. 16. Wang Q, Song ZQ, Chen YF, Sen S, Li ZY. Leaves and fruits of Bauhinia (Leguminosae, Caesalpinioideae, Cercideae) from the Oligocene Ningming Formation of Guangxi, South China and their biogeographic implications. BMC Evolutionary Biology 2014: 1–16. pmid:24758153
  17. 17. Shi GL, Zhou ZY, Xie ZM. A new Cephalotaxus and associated epiphyllous fungi from the Oligocene of Guangxi, South China. Review of Palaeobotany and Palynology 2010; 161: 179–195.
  18. 18. Shi GL, Zhou ZY, Xie Z. Cupressus foliage shoots and associated seed cones from the Oligocene Ningming Formation of Guangxi, South China. Review of Palaeobotany and Palynology 2011; 166: 325–334.
  19. 19. Shi GL, Zhou ZY, Xie ZM. A new Oligocene Calocedrus from South China and its implications for transpacific floristic exchanges. American Journal of Botany 2012; 99: 108–120. pmid:22223689
  20. 20. Song ZQ, Shi GL, Chen YF, Wang Q. Winged fruits of Ailanthus (Simaroubaceae) from the Oligocene Ningming Formation of Guangxi, and Their Taxonomic and Biogeogrephic Implications. Acta Palaeontologica Sinica 2014; 53: 191–200.
  21. 21. Shi GL, Xie ZM, Li HM. High diversity of Lauraceae from the Oligocene of Ningming, South China. Palaeoworld 2014; 23: 336–356.
  22. 22. Ma FJ, Sun BN, Wang QJ, Dong JL, Yang GL, Yang Y. A new species of Meliolinites associated with Buxus leaves from the Oligocene of Guangxi, South China. Mycologia 2015: pmid:26432806
  23. 23. Wang QJ, Ma FJ, Dong JL, Yang Y, Jin PH, Sun BN. Coryphoid palms from the Oligocene of China and their biogeographical implications. Comptes rendus Palevol 2015:
  24. 24. Chen GJ, Fang F, Chang M-M. A new cyprinid closely related to cultrins+xenocyprinins from the mid-Tertiary of South China. Journal of Vertebrate Paleontology 2005; 25: 492–501.
  25. 25. Chen GJ, Chang MM. A new early cyprinin from Oligocene of South China. Science China Earth Sciences 2011; 54: 481–492.
  26. 26. Harris JG, Harris MW. Plant identification terminology: Payson Utah. 2001.
  27. 27. Conover MV. Epidermal patterns of the reticulate-veined Liliiflorae and their parallel-veined allies. Botanical Journal of the Linnean Society 1991; 107: 295–312.
  28. 28. Kovar-Eder J, Kvaček Z, Ströbitzer-Hermann M. The Miocene Flora of Parschlug (Styria, Austria): revision and synthesis. Annalen Naturhistorisches Museum Wien 2004; 105 A: 45–159.
  29. 29. Manchester SR, O’Leary EL. Phylogenetic Distribution and Identification of Fin-winged Fruits. The Botanical Review 2010; 76: 1–82.
  30. 30. Correa E, Jaramillo C, Manchester S, Gutierrez M. A fruit and leaves of Rhamnaceous affinities from the late Cretaceous (Maastrichtian) of Colombia. American Journal of Botany 2010; 97: 71–79. pmid:21622368
  31. 31. Manchester SR. Biogeographical relationships of North American Tertiary floras. Annals of the Missouri Botanical Garden 1999; 86: 472–522.
  32. 32. Manchester SR. The fossil history of the Juglandaceae. 21. Monographs in Systematic Botany, Missouri Botanical Garden: Allen Press, Inc., lawrence, Kansas; 1987. p. 91–98.
  33. 33. de Moraes de Potascheff C, Mori SA, Lombardi JA. Pollination ecology of the Cerrado species Eschweilera nana (Lecythidaceae subfam. Lecythidoideae). Brittonia 2013; 66: 191–206.
  34. 34. Prance GT, Mori SA. Observations on the fruits and seeds of neotropical Lecythidaceae. Brittonia 1978; 30: 21–33.
  35. 35. Morton CM, Mori SA, Prance GT, Karol KG, Chase MW. Phylogenetic relationships of Lecythidaceae: A cladistic analysis using rbcL sequence and morphological data. American Journal of Botany 1997; 84: 530–540. pmid:21708605
  36. 36. Sprague TA. Dioncophyllum Bulletin of Miscellaneous Information (Royal Gardens, Kew) 1916; 4: 89–92.
  37. 37. Shaw HKA. On the Dioncophyllaceae, a Remarkable New Family of Flowering Plants. Kew Bulletin 1951; 6: 327–347.
  38. 38. Miki S. On the Pleistocene flora in Prov. Yamashiro with the Descriptions of 3 New Species and 1 New Varity. The Botanical Magazine 1933; XLVII: 619–631.
  39. 39. Pigg KB, Wehr WC. Tertiary flowers, fruits, and seeds of Washington state and adjacent areas. III. Washington Geology 2002; 30: 3–16.
  40. 40. Mai DH, Walther H. Die oligozänen und untermiozänen Floren Nordwest-Sachsens und des Bitterfelder Raumes. Abh Staatlichen Mus Mineral Geol Dresden 1991; 38: 1–230.
  41. 41. Available: http://www.odsn.de/odsn/services/paleomap/adv_map.html.
  42. 42. Zhang ZC. Angiospermae. Shenyang Institute Geology and Mineral Resources (Eds), Paleontological Atlas of Northest China. Part 2, Volume of Mesozoic and Cenozoic. Beijing: Geological Publishing House; 1980. p. 308–400.
  43. 43. Wilde V, Frankenhäuser H. The Middle Eocene plant taphocoenosis from Eckfeld (Eifel, Germany). Review of Palaeobotany and Palynology 1998; 101: 7–28.
  44. 44. Manchester SR. Update on the megafossil flora of Florissant, Colorado. Fossil flora and stratigraphy of the Florissant Formation, Colorado Proceedings of the Denver Museum of Nature & Science Series 2001; 3: 137–162.
  45. 45. Augspurger CK. Morphology and Dispersal Potential of Wind-Dispersed Diaspores of Neotropical Trees. American Journal of Botany 1986; 73: 353–363.
  46. 46. Wilde V, Frankenhäuser H. A new species of four-winged fruits (Trilobium maii sp. nov.) from the middle Eocene of Eckfeld (Eifel, Germany). Review of Palaeobotany and Palynology 2010; 159: 143–151.
  47. 47. Augspurger CK. Mass Allocation, Moisture Content, and Dispersal Capacity of Wind-Dispersed Tropical diaspores. New Phytologist 1988; 108: 357–368.