Cenozoic Plant Diversity of Yunnan: a Review

Plant Diversity xxx (2016) 1e12

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Plant Diversity

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Cenozoic plant diversity of Yunnan: A review

Yong-Jiang Huang a, d, Lin-Bo Jia a, e, Qiong Wang b, Volker Mosbrugger c, * Torsten Utescher c, f, Tao Su b, d, Zhe-Kun Zhou a, b, a Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China b Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China c Senckenberg Research Institute/BiK F (Loewe), Senckenberganlage 25, 60325 Frankfurt am Main, Germany d State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences, Nanjing 210008, China e Graduate University of the Chinese Academy of Sciences, Beijing 100049, China f Steinmann Institute, University of Bonn, Nussallee 8, 53115 Bonn, Germany article info abstract

Article history: Yunnan in southwestern China is renowned for its high plant diversity. To understand how this modern Received 10 October 2016 botanical richness formed, it is critical to investigate the past biodiversity throughout the geological time. Received in revised form In this review, we present a summary on plant diversity, floristics and climates in the Cenozoic of Yunnan 18 November 2016 and document their changes, by compiling published palaeobotanical sources. Our review demonstrates Accepted 21 November 2016 that thus far a total of 386 fossil species of ferns, gymnosperms and angiosperms belonging to 170 genera Available online xxx within 66 families have been reported from the Cenozoic, particularly the Neogene, of Yunnan. Angio- sperms display the highest richness represented by 353 species grouped into 155 genera within 60 Keywords: fi Cenozoic families, with Fagaceae, Fabaceae, Lauraceae and Juglandaceae being the most diversi ed. Most of the Fossil plants families and genera recorded as fossils still occur in Yunnan, but seven genera have disappeared, Floristic change including Berryophyllum, Cedrelospermum, Cedrus, Palaeocarya, Podocarpium, Sequoia and Wataria. The Palaeobiodiversity regional extinction of these genera is commonly referred to an aridification of the dry season associated Palaeoclimate with Asian monsoon development. Floristic analyses indicate that in the late Miocene, Yunnan had three Yunnan floristic regions: a northern subtropical floristic region in the northeast, a subtropical floristic region in the east, and a tropical floristic region in the southwest. In the late Pliocene, Yunnan saw two kinds of floristic regions: a subalpine floristic region in the northwest, and two subtropical floristic regions separately in the southwest and the eastern center. These floristic concepts are verified by results from our areal type analyses which suggest that in the Miocene southwestern Yunnan supported the most Pantropic elements, while in the Pliocene southwestern Yunnan had abundant Tropical Asia (Indo eMalaysia) type and East Asia and North America disjunct type that were absent from northwestern Yunnan. From the late Miocene to late Pliocene through to the present, floristic composition and vegetation types changed markedly, presumably in response to altitude changes and coeval global cooling. An integration of palaeoclimate data suggests that during the Neogene Yunnan was warmer and wetter than today. Moreover, northern Yunnan witnessed a pronounced temperature decline, while southern Yunnan experienced only moderate temperature changes. Summer precipitation was consis- tently higher than winter precipitation, suggesting a rainfall seasonality. This summary on palaeoclimates helps us to understand under what conditions plant diversity occurred and evolved in Yunnan throughout the Cenozoic. Copyright © 2016 Kunming Institute of Botany, Chinese Academy of Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC BY- NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction * Corresponding author. Key Laboratory for Plant Biodiversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Lanhei Road þ Yunnan in southwestern China has long been recognized as a 132#, Kunming 650201, Yunnan, China. Fax: 86 0871 65219932. E-mail address: [email protected] (Z.-K. Zhou). hotspot for plant diversity (Wu, 1988; Lopez-Pujol et al., 2006, Peer review under responsibility of Editorial Ofﬁce of Plant Diversity. 2011; Ruth et al., 2008; Turkington and Harrower, 2016). It is http://dx.doi.org/10.1016/j.pld.2016.11.004 2468-2659/Copyright © 2016 Kunming Institute of Botany, Chinese Academy of Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Huang, Y.-J., et al., Cenozoic plant diversity of Yunnan: A review, Plant Diversity (2016), http://dx.doi.org/ 10.1016/j.pld.2016.11.004 2 Y.-J. Huang et al. / Plant Diversity xxx (2016) 1e12 home to approximately 16,000 higher plant species grouped into 2. Research history of palaeobotany in Yunnan more than 2300 genera within 244 families, representing 6% of the world's total diversity of higher plant species (Wu, 1979), even As a montane region, Yunnan has more than 150 Cenozoic though the region accounts for only 4% of the Chinese land surface. sedimentary basins, many of which have yielded Cenozoic strata Nearly half of these plant species are endemic to Yunnan. In addi- that bear plant fossils (Ge and Li, 1999). The region archives at least tion, almost all ecosystem types within China, including tropical 20 megafossil floras, ranging from the early Oligocene to late seasonal rain forest, evergreen broad-leaved forest, sclerophyllous Pliocene (Fig. 1). However, these fossil floras rarely attracted evergreen broad-leaved forest, deciduous broad-leaved forest, both attention before the beginning of the last century. In 1920, Colani warm and cold temperate coniferous forests, dry and warm valley reported the first plant fossils recovered from Miocene sediments scrubs as well as subalpine and alpine scrubs can be found in along the former railway connecting Kunming and Hanoi (Colani, Yunnan (Writing Group of Yunnan Vegetation, 1987). This high 1920), but interest was transient as no more palaeobotanical diversity of plant taxa and vegetation types qualifies Yunnan as an studies followed for the next 57 years. In 1978, several Chinese outstanding place for botanical research. Yunnan also exhibited paleobotanists, including Tao Jun-Rong, Guo Shuang-Xing and Li exceptional botanical richness in the geological past as revealed by Hao-Ming, jointly published a monograph entitled “Cenozoic Plants the rich fossil record. To date, around 20 megafossil floras are of China” (Writing Group of the Cenozoic Plants of China, 1978). In known from the Cenozoic of Yunnan, and hundreds of fossil spe- that monograph, 301 plant fossil species, covering mosses, ferns, cies, covering ferns, gymnosperms and angiosperms, have been gymnosperms and angiosperms, were described systematically. documented. A summary of past plant diversity based on palae- Among them, 76 species came from five floras in Yunnan: the obotanical data affords a better understanding of the modern Oligocene Jinggu flora, the Miocene Duotan flora, the early Miocene botanical richness in this region. Shuanghe flora, the late Miocene Xiaolongtan flora, and the late In the present review, we compile palaeobotanical data from Pliocene Eryuan flora. In the 1980s, Tao and Chen (1983) described literature to document plant diversity in Yunnan throughout the the late Miocene Bangmai flora, also known as the Lincang flora, Cenozoic. Only fossil taxa represented by megafossils are consid- from southwestern Yunnan which comprised 59 fossil species ered, i.e., leaves, wood, fruits, seeds and flowers. Pollen records are grouped into 48 genera within 28 families; Tao (1986) reported the not considered, because they can be transported to Yunnan from late Pliocene Fudong flora from northwestern Yunnan which yiel- elsewhere and cannot be identified to a fine enough taxonomic ded 17 species grouped into four genera of three families. Unfor- resolution. We first briefly introduce the research history of tunately, published mostly in Chinese, these works have had palaeobotany in Yunnan, then present known fossil families, limited international recognition. genera and species to depict the diversity of Cenozoic plants and During the last two decades, 10 Cenozoic megafossil floras from ecosystems, and analyze the inferred floristic characters and Yunnan have been studied as doctoral or master's research projects, changes. We also summarize the Neogene climate evolution in e.g., the late Miocene Xianfeng flora, the late Pliocene Nanbanbang, Yunnan and related extinction events exemplified for selected Fudong, Longmen and Tuantian floras. A few are still being inves- plant taxa. The present review aims to facilitate access to the rich tigated for the subject of doctoral research, e.g., the middle Miocene palaeobotanical record of Yunnan for both palaeobotanists and Wenshan and Maguan floras (formerly dated as late Miocene, but botanists. recently moved to middle Miocene according to lake geochemical

Fig. 1. Map showing the distribution of Cenozoic fossil ﬂoras in Yunnan, southwestern China.

Please cite this article in press as: Huang, Y.-J., et al., Cenozoic plant diversity of Yunnan: A review, Plant Diversity (2016), http://dx.doi.org/ 10.1016/j.pld.2016.11.004 Y.-J. Huang et al. / Plant Diversity xxx (2016) 1e12 3 evidence; Lebreton-Anberree et al., 2016). To the best of our and the late Miocene Shuitangba flora, and tens of fossil species knowledge, at least eight doctoral and two master's theses are have been described (e.g., Wen et al., 2013; Jacques et al., 2013; freely accessible at universities or institutions in China, e.g., Lanz- Wang et al., 2013; Meng et al., 2014, 2015; Xie et al., 2014; Zhang hou University, Kunming Institute of Botany, Chinese Academy of et al., 2015a, 2015b; Liang et al., 2016; Su et al., 2016; Fig. 2). It Sciences (Zhao, 2002; Xie, 2007; Wu, 2010; Su, 2010; Xing, 2010; seems that the recent decades have witnessed an upward surge in Huang, 2012; Hu, 2013; Li, 2015; Wang, 2016; Zhu, 2016). Such palaeobotanical research in Yunnan. theses usually present a full list of identified plant taxa that more or less reflects a given fossil flora (Wu, 2010; Huang, 2012; Zhu, 2016). 3. Families, genera and species of fossil plants Some of the authors have also interpreted the palaeovegetation or palaeoclimate accordingly (Wu, 2010; Su, 2010; Xing, 2010). Based Up to now, approximately 386 plant species (including mor- on detailed palaeobotanical research, hundreds of fossil species phospecies) belonging to 170 genera within 66 families have been have been published in a variety of international journals (e.g., Zhao documented from the Cenozoic of Yunnan and most of them are et al., 2004; Xie et al., 2010; Xing et al., 2010, 2013; Su et al., 2011, from the Neogene (see the Appendix). They include ferns, gym- 2013b; Huang et al., 2012, 2013; Wu et al., 2012; Hu et al., 2014; nosperms and angiosperms, of which ferns and gymnosperms are Jia et al., 2015; Li et al., 2015; Zhu et al., 2015, 2016; Huang et al., relatively few. 2016a; Fig. 2). In addition to those targeted within doctoral or Fossil ferns from Yunnan comprise only nine species placed in master's projects, research has begun on other fossil floras, such as five genera of four families: Davalliaceae, Equisetaceae, Osmunda- the Oligocene Jinggu flora, the middle Miocene Sanzhangtian flora, ceae and Polypodiaceae. The genus Drynaria in Polypodiaceae is the

Fig. 2. Selected fossil taxa comprising leaves, wood, fruits and seeds from the Cenozoic of Yunnan. Scale bars ¼ 10 mm for images 1e3, 5 and 8e10; 0.5 mm for images 4, 7, 11 and 12.1. Drynaria callispora (Polypodiaceae) from the late Pliocene Longmen flora (Su et al., 2011). 2. Calocedrus shengxianensis (Cupressaceae) from the middle Miocene Wenshan flora (Zhang et al., 2015b). 3. Tsuga xianfengensis (Pinaceae) from the late Miocene Xianfeng flora (Xing et al., 2013). 4. Fossil wood of Pinus uniseriata (Pinaceae) from the Xianfeng flora (Wang et al., in press). 5. Mahonia mioasiatica (Berberidaceae) from the Wenshan flora (Huang et al., 2016a). 6. Quercus tenuipilosa (Fagaceae) from the late Pliocene Hunshuitang flora (Hu et al., 2014). 7. A fossil seed of Ranunculus (Ranunculaceae) from the Nanbanbang flora (unpublished data). 8. Rosa fortuita (Rosaceae) from the Wenshan flora (Su et al., 2016). 9. Celastrus caducidentatus (Celastraceae) from the middle Miocene Sanzhangtian flora (Liang et al., 2016). 10. Bauhinia wenshanensis (Fabaceae) from the Wenshan flora (Meng et al., 2014). 11. Eurya stigmosa (Theaceae) from the late Pliocene Nanbanbang flora (Zhu et al., 2016). 12. Aralia stratosa (Araliaceae) from the late Pliocene Fudong flora (Zhu et al., 2015).

Please cite this article in press as: Huang, Y.-J., et al., Cenozoic plant diversity of Yunnan: A review, Plant Diversity (2016), http://dx.doi.org/ 10.1016/j.pld.2016.11.004 4 Y.-J. Huang et al. / Plant Diversity xxx (2016) 1e12 most diverse and has four different fossil species, which all came species). Most families, however, have only one or two fossil from the Neogene of western Yunnan (Su et al., 2011; Wu et al., species, e.g., Euphorbiaceae, Oleaceae, Nymphaeaceae and Celas- 2012; Wen et al., 2013; Huang et al., 2016b). This may from a his- traceae (Table 1). Based on the above summary, Fabaceae, Faga- torical view explicate the establishment of the modern Drynaria ceae, Lauraceae, Juglandaceae and Rosaceae were among the most diversity in the Hengduan Mountains, western Yunnan (Huang diversified families in the Cenozoic of Yunnan either at the generic et al., 2016b). Fossil gymnosperms from Yunnan fall into 24 spe- level or at the species level. Today, Fagaceae and Lauraceae are two cies grouped into 10 genera of two families, Pinaceae and Cupres- of the major families contributing to evergreen broad-leaved saceae. The former has 15 fossil species belonging to four genera forests in Yunnan as well as in other parts of southern China (Cedrus, Picea, Pinus and Tsuga), while the latter has nine fossil (Writing Group of Yunnan Vegetation, 1987), and Fabaceae is species belonging to six genera (Calocedrus, Cephalotaxus, Cupres- among the most common families in tropical and subtropical sus, Platycladus, Sequoia and Taiwania). forests in Yunnan. Rich fossil records of Fabaceae, Fagaceae and Similar to modern Yunnan, angiosperms were the most diverse Lauraceae suggest that their dominance in the present evergreen plant group throughout the Cenozoic. A total of 353 fossil species broad-leaved forests of Yunnan seems to have been largely of angiosperms grouped into 155 genera within 60 families are established at least by the Neogene. In addition, many other known from megafossil remains. At the family level, Fabaceae has families that are widely seen in the modern broad-leaved forests 23 genera with fossil records and represents the most genus-rich were also found as fossils, e.g., Juglandaceae, Ulmaceae, Sapin- family in the fossils, followed by Lauraceae which has 11 fossil daceae, Salicaceae, Betulaceae and Rosaceae. This suggests that genera (Table 1). Other angiosperm families having at least five the modern floristic composition at the family level in Yunnan was genera of fossil plants are Rosaceae (8 genera), Fagaceae (7 probably formed in the Neogene or before. Interestingly, some genera), Juglandaceae (6 genera), Malvaceae (6 genera) and families such as Magnoliaceae and Theaceae that are important Rutaceae (5 genera). Angiosperm families having four genera of and frequent components today are not well represented in the fossil plants include Anacardiaceae, Betulaceae, Hamamelidaceae, fossil record (Table 1). Poaceae and Rhamnaceae. Most families are represented by only With respect to the species diversity of genera, six angiosperm one genus with fossil evidence, e.g., Buxaceae, Caryophyllaceae, genera have more than 10 fossil species, i.e., Quercus, Castanopsis, Elaeagnaceae and Moraceae (Table 1). Further fossil finds will no Lithocarpus, Acer, Cyclobalanopsis and Cinnamomum (Table 2; Fig. 3). doubt reveal more. For their diversity at the species level, Faga- Among them, Quercus is obviously the richest and has 36 fossil ceae having 79 fossil species is the most species-rich family, fol- species; Castanopsis, Lithocarpus and Acer have 14, 13 and 11 fossil lowed by Fabaceae and Lauraceae with 38 and 33 fossil species, species, respectively; and Cyclobalanopsis and Cinnamomum each respectively. There are seven other families having 10 or more has 10 fossil species. It is worth explaining that different classifi- fossil species, namely Juglandaceae (14 species), Ulmaceae (13 cations of Quercus and Cyclobalanopsis exist. Some botanists species), Sapindaceae (13 species), Salicaceae (12 species), Betu- consider Quercus and Cyclobalanopsis as two separate genera laceae (11 species), Anarcardiaceae (11 species) and Rosaceae (10 distinguished by the imbricate-scaled or lamellate structure of the

Table 1 Known families of fossil plants from the Cenozoic of Yunnan, and the numbers of their fossil genera and species.

Family Number of genera Number of species Family Number of genera Number of species

Fabaceae 23 38 Schisandraceae 1 1 Lauraceae 11 33 Piperaceae 1 1 Rosaceae 8 10 Magnoliaceae 1 3 Fagaceae 7 79 Annonaceae 1 3 Cupressaceae 6 9 Dioscoreaceae 1 1 Juglandaceae 6 14 Typhaceae 1 1 Malvaceae 6 7 Menispermaceae 1 1 Rutaceae 5 8 Buxaceae 1 1 Pinaceae 4 15 Cercidiphyllaceae 1 1 Poaceae 4 7 Elaeagnaceae 1 1 Hamamelidaceae 4 5 Cannabaceae 1 2 Rhamnaceae 4 7 Moraceae 1 4 Betulaceae 4 11 Myricaceae 1 6 Anacardiaceae 4 11 Celastraceae 1 1 Ulmaceae 3 13 Clusiaceae 1 1 Salicaceae 3 12 Hypericaceae 1 1 Sapindaceae 3 13 Passiﬂoraceae 1 1 Meliaceae 3 3 Euphorbiaceae 1 2 Cornaceae 3 5 Myrtaceae 1 3 Polypodiaceae 2 5 Simaroubaceae 1 1 Smilacaceae 2 4 Capparaceae 1 1 Berberidaceae 2 3 Schoepﬁaceae 1 1 Combretaceae 2 3 Loranthaceae 1 1 Lythraceae 2 4 Caryophyllaceae 1 1 Sapotaceae 2 2 Aizoaceae 1 1 Styracaceae 2 2 Hydrangeaceae 1 1 Oleaceae 2 2 Pentaphylacaceae 1 1 Adoxaceae 2 3 Theaceae 1 1 Araliaceae 2 2 Symplocaceae 1 1 Equisetaceae 1 2 Ericaceae 1 4 Osmundaceae 1 1 Plantaginaceae 1 1 Davalliaceae 1 1 Aquifoliaceae 1 2 Nymphaeaceae 1 1 Pittosporaceae 1 1

Table 2 Known genera of fossil plants from the Cenozoic of Yunnan, and the numbers of their fossil species.

Genus Number of species Genus Number of species Genus Number of species Genus Number of species

Quercus 36 Bambusium 2 Typha 1 Passiﬂora 1 Castanopsis 14 Mahonia 2 Graminites 1 Sabia 1 Lithocarpus 13 Exbucklandia 2 Phragmites 1 Lumnitzera 1 Acer 11 Cassia 2 Cyclea 1 Lagerstroemioxylon 1 Cinnamomum 10 Dalbergia 2 Berberis 1 Pistacioxylon 1 Cyclobalanopsis 10 Gleditsia 2 Buxus 1 Dodonaea 1 Ulmus 9 Podocarpium 2 Corylopsis 1 Koelreuteria 1 Pinus 8 Robinia 2 Distylium 1 Citrus 1 Phoebe 7 Sophora 2 Rhodoleia 1 Evodia 1 Albizzia 6 Rosa 2 Cercidiphyllum 1 Murraya 1 Myrica 6 Sorbus 2 Abarema 1 Toddalia 1 Salix 6 Celtis 2 Acacia 1 Ailanthus 1 Rhus 6 Fagus 2 Bauhinia 1 Aphanamixis 1 Machilus 5 Pterocarya 2 Cercis 1 Chukrasia 1 Palaeocarya 5 Mallotus 2 Erythrophleum 1 Toona 1 Populus 5 Terminalia 2 Gymnocladus 1 Firmiana 1 Drynaria 4 Pistacia 2 Indigofera 1 Helicteres 1 Tsuga 4 Toxicodendron 2 Leguminosites 1 Reevesia 1 Berchemia 4 Burretiodendron 2 Lespedeza 1 Tilia 1 Ficus 4 Alangium 2 Maackia 1 Wataria 1 Juglans 4 Nyssa 2 Millettia 1 Capparis 1 Betula 4 Ilex 2 Mucuna 1 Schoepﬁa 1 Zanthoxylum 4 Viburnum 2 Pithecellobium 1 Loranthus 1 Rhododendron 4 Palaeosorum 1 Shuteria 1 Cucubalus 1 Magnolia 3 Osmunda 1 Amelanchier 1 Tetragonia 1 Smilax 3 Humata 1 Crataegus 1 Hydrangea 1 Bambusiculmus 3 Cedrus 1 Photinia 1 Cornus 1 Desmodium 3 Cephalotaxus 1 Prunus 1 Ternstroemia 1 Ormosia 3 Platycladus 1 Rubus 1 Chrysophyllum 1 Zelkova 3 Taiwania 1 Stranvaesia 1 Sinosideroxylon 1 Berryophyllum 3 Euryale 1 Hippophae 1 Schima 1 Alnus 3 Schisandra 1 Paliurus 1 Symplocos 1 Carpinus 3 Piper 1 Rhamnella 1 Rehderodendron 1 Trapa 3 Annona 1 Ventilago 1 Styrax 1 Syzygium 3 Desmos 1 Cedrelospermum 1 Fraxinus 1 Equisetum 2 Uvaria 1 Castanea 1 Jasminium 1 Picea 2 Alseodaphne 1 Carya 1 Plantago 1 Calocedrus 2 Laurus 1 Engelhardia 1 Sambucus 1 Cupressus 2 Neocinnamomum 1 Platycarya 1 Pittosporum 1 Sequoia 2 Oreodaphne 1 Corylus 1 Aralia 1 Lindera 2 Sassafras 1 Celastrus 1 Oreopanax 1 Litsea 2 Dioscorea 1 Garcinia 1 Nothaphoebe 2 Heterosmilax 1 Hypericum 1

e.g., Betula and Ficus both with four fossil species, Alnus and Car- pinus with three, and Lindera and Mahonia with two (Table 2). Most of the genera have only one fossil species, e.g., Buxus, Citrus, Cornus and Sambucus. Notably, the genera that were species diverse in the Cenozoic mainly belong to Fagaceae (Querucs, Castanopsis, Lith- ocarpus and Cyclobalanopsis) and Lauraceae (Cinnamomum, Phoebe and Machilus), and as already mentioned, they are still diverse in modern forests of Yunnan. Other genera that have good fossil records are also important components of modern broad-leaved forests in Yunnan, e.g., Acer, Ulmus, Myrica, Rhus and Salix. This therefore suggests the idea that the composition of Neogene evergreen broad-leaved forests in this region was already similar to that today at the generic level.

4. Disappearance of some plant taxa Fig. 3. Species diversity of the fossil-richest genera from the Cenozoic of Yunnan. Molecular studies have been repeatedly interpreted as meaning that numerous plant groups in Yunnan experienced species diver- cupule (Hjelmquist, 1948; Huang et al., 1999), whereas others treat siﬁcation as a result of increasing environmental complexity (e.g., them as two subgenera of Quercus (Forman, 1966; Manos et al., Wang et al., 2005; Yu et al., 2015). The other side of the historical 2001). Here we follow the former taxonomic treatment. For the emergence of new lineages, however, is species extinction. remaining genera of angiosperms, nine have 5e10 fossil species, Although most families and genera recorded as fossils still exist, namely Ulmus, Phoebe, Albizzia, Myrica, Salix, Rhus, Machilus, some genera disappeared from Yunnan after the Neogene. To date, Palaeocarya and Populus. Nearly 40 genera have 2e4 fossil species, there are seven genera with fossil evidence we do not encounter in

Please cite this article in press as: Huang, Y.-J., et al., Cenozoic plant diversity of Yunnan: A review, Plant Diversity (2016), http://dx.doi.org/ 10.1016/j.pld.2016.11.004 6 Y.-J. Huang et al. / Plant Diversity xxx (2016) 1e12 the natural vegetation of the region. They are Cedrus, Sequoia, dry conditions after autumn may prevent their seeds from germi- Berryophyllum, Cedrelospermum, Palaeocarya, Podocarpium and nating or their seedlings from developing new leaves. In contrast to Wataria (Fig. 4). modern climates, in the Neogene Yunnan had relatively humid Cedrus is a small genus of four extant species restricted to conditions in the dry season (Xia et al., 2009; Sun et al., 2011; Xing Mediterranean regions and the western Himalayas (Maheshwari et al., 2012; Su et al., 2013a; Huang et al., 2015a). Humid and suit- and Biswas, 1970). In modern Yunnan, no Cedrus grows as a natu- able habitats might explain the historical existence of the two ral population. However, a recent fossil discovery of seeds and cone genera in this region. As precipitation in the dry season decreased, scales indicate that Cedrus occurred in northwestern Yunnan dur- likely linked to the Asian monsoon intensification, as is elaborated ing the late Pliocene (Su et al., 2013b). The genus must have dis- below, the dry winter and spring ultimately led to the regional appeared from this region soon after (Su et al., 2013b), as is also extinction of species that require a moister dry season (Su et al., evidenced by the decline in its pollen occurrences (Tong et al., 1990; 2013b; Zhang et al., 2015a). Wang and Shu, 2004; Xiao et al., 2010). Sequoia is a genus now Unlike Cedrus and Sequoia that have no living relatives in endemic only to the western coast of North America (Waston and Yunnan but survive in other regions, the remaining five genera only Eckenwalder, 1993). Like the situation with Cedrus, Sequoia also have fossil representatives; in other words, they have gone extinct has a fossil representative in Yunnan. Fossils of cones and leafy globally. Berryophyllum is an extinct genus morphologically similar shoots discovered from the middle Miocene Maguan flora in to extant Lithocarpus, Canstanopsis and Cyclobalanopsis of Fagaceae southeastern Yunnan closely resemble modern Sequoia, indicating (Zhou, 1996). The genus was widely distributed in Europe and its occurrence in the region at that time (Zhang et al., 2015a). The North America from the Paleocene to Miocene (Jones and Dilcher, genus probably disappeared from Yunnan after the middle 1988; Zhou, 1996). In Yunnan, it has been described only from the Miocene. This raises the question as to why Cedrus and Sequoia Oligocene Jinggu flora in southern Yunnan. Cedrelospermum went extinct in Yunnan but survive in other regions. Investigations (Ulmaceae) is another extinct genus that was well represented in by Su et al. (2013b) and Zhang et al. (2015a) have demonstrated that Europe (Hably and Thiebaut, 2002; and references therein) and the aridification of the dry season, associated with monsoon North America (Manchester, 1987, 1989; Manchester and Tiffney, intensification, might have played a major role. Today, Yunnan has 2001). In Yunnan, one fossil species described as Cedrelospermum dry conditions from late autumn to early spring, whereas Medi- asiaticum has been reported from the middle Miocene Maguan terranean regions and the western coast of North America both flora in southeastern Yunnan (Jia et al., 2015). This species repre- have wet winters and springs. As seeds of Cedrus and Sequoia are sents the first record of Cedrelospermum in Asia (Jia et al., 2015). recalcitrant, they germinate immediately upon their maturity in Palaeocarya is morphologically similar to two modern genera, the autumn (Olson et al., 1990; Kumar et al., 2011). Unfortunately, namely Engelhardia and Oreomunnea of Juglandaceae (Manchester,

Fig. 4. Selected fossil taxa now extinct in Yunnan. Scale bars ¼ 10 mm for all images. 1. Seed scale of Cedrus angusta (Pinaceae) from the late Pliocene Longmen flora (Su et al., 2013b). 2, 3. Winged fruits of Cedrelospermum asiaticum (Ulmaceae) from the middle Miocene Maguan flora (Jia et al., 2015). 4. Leafy shoot of Sequoia maguanensis (Cupressa- ceae; Zhang et al., 2015a) from the middle Miocene Wenshan flora.

1999). It has an excellent fossil record in the Northern Hemisphere, still below the minimum level (60%) that defines a tropical floristic extending from the Pliocene deeply into the Eocene (Tanai and region (Zhu, 2013). Therefore, the Xianfeng and Xiaolongtan floras Uemura, 1983; Jahnichen€ et al., 1984; Manchester, 1987; Guo and represent two subtropical floras. By contrast, the late Miocene Zhang, 2002; Jin, 2009; Meng et al., 2015). In Yunnan, Palaeocarya Bangmai flora in southwestern Yunnan contains more tropical has been reported from the middle Miocene Wenshan flora in genera, accounting for 60% of the fossil assemblage (Guo, 2011). southeastern Yunnan (Meng et al., 2015) and the late Pliocene Moreover, several genera are mainly or even merely distributed in Tuantian flora in southwestern Yunnan (Xie et al., 2010). Podo- tropical regions, such as Mucuna, Murraya, Neocinnamomum, carpium of Fabaceae is one of the most common legumes recorded Ormosia, Piper and Terminalia (Guo, 2011). According to the defi- from the Eocene to Pliocene (Xu et al., 2015). In Yunnan, the genus nition of a tropical floristic region by Zhu (2013), the late Miocene has one fossil species named P. poocarpum from the late Miocene Bangmai flora would qualify as tropical. Thus we conclude that in Xiaolongtan flora in southern Yunnan (Guo and Zhou, 1992). The the late Miocene three known floristic regions occurred in extinct genus Wataria, established by Terada and Suzuki (1998),is Yunnan: a northern subtropical floristic region in the northeast, a anatomically similar to Reeveia of Malvaceae. In Yunnan, Wateria subtropical floristic region in the east, and a tropical floristic re- yunnanica has been described from the middle Miocene Shengli gion in the southwest (Fig. 5A). flora in southern Yunnan on the basis of fossil wood (Li et al., 2015). For the late Pliocene, seven fossil floras are known from Yunnan, This wood species represents the first fossil occurrence of the genus i.e., the Nanbanbang, Fudong, Eryuan, Longmen, Tuantian, Yuan- in China (Li et al., 2015). mou and Hunshuitang floras. The first four floras from the southern Hengduan Mountains in northwestern Yunnan are fairly distin- 5. Floristic characters and changes guished by the dominance of mountain oaks, Quercus sect. Heter- obalanus, suggesting sclerophyllous evergreen broad-leaved forests Of the 20 megafossil floras from Yunnan considered here, those during the late Pliocene. This is well supported by the fact that of late Miocene and late Pliocene age have been well studied and seven out of the 20 fossil species from the Fudong flora belong to they are relatively abundant (Fig. 1). Hence these floras may readily Quercus sect. Heterobalanus (Huang, 2012), and 1275 out of around reflect floristic characters of the two time slices in the region as well 1500 fossil specimens from the Longmen flora belong to this sec- as their changes. Fossil floras of other stratigraphical phases are not tion (Su, 2010). Today, sclerophyllous evergreen broad-leaved for- considered in the present analyses, as they have been insufficiently ests dominated by Quercus sect. Heterobalanus are widely studied from a formal systematic viewpoint. distributed in northwestern Yunnan (Writing Group of Yunnan There are four late Miocene floras known from Yunnan on the Vegetation, 1987). This pattern might have been largely estab- basis of which we look at the late Miocene floristic characteristics: lished by the late Pliocene. Distinct from these four floras, the the Shuitangba, Xianfeng, Bangmai and Xiaolongtan floras. The contemporary Tuantian flora in southwestern Yunnan was shown late Miocene Shuitangba florainnortheasternYunnanisdomi- to contain many tropical to subtropical elements, accounting for nated by subtropical representatives of Quercus as revealed by the about 53% of the recognized fossil taxa (Wu, 2010). They include pollen record (Chang et al., 2015), and Euryale in the aquatic Castanposis, Cyclobalanopsis and Quercus of Fagaceae, and Cinna- ecosystem as reflected by recently recovered carpological remains momum, Lindera and Machilus of Lauraceae (Wu, 2010), which (Huang et al., 2015b). The flora contains several temperate ele- collectively characterize a subtropical evergreen broad-leaved for- ments such as Corylus and Staphylea, and only a few pantropical est. The late Pliocene Hunshuitang flora in eastern central Yunnan ones such as Zanthoxylum. Thus the Shuitangba flora might is dominated by Cyclobalanopsis (Hu, 2013; Hu et al., 2014), also represent a northern subtropical flora. The late Miocene Xianfeng suggesting a subtropical evergreen broad-leaved forest. Hence in and Xiaolongtan floras in eastern Yunnan are both dominated by the late Pliocene of Yunnan, at least two kinds of floristic regions the evergreen fagaceous elements such as Cyclobalanopsis, Lith- existed: sclerophyllous evergreen broad-leaved forests in the ocarpusandQuercus, as well as Lauraceae (Xia et al., 2009; Xing northwest that represented a subalpine floristic region, and sub- et al., 2012). In the Xiaolongtan flora, tropical and subtropical tropical evergreen broad-leaved forests in the southwest and Fabaceae are relatively abundant (Guo and Zhou, 1992; Xia et al., eastern center that in each case represented a subtropical floristic 2009), but the percentage of tropical components (30e50%) is region (Fig. 5B).

Fig. 5. Floristic regions in the late Miocene (A) and late Pliocene (B) of Yunnan (grey areas: no data). I. Tropical floristic region. II. Subtropical floristic region. III. Northern subtropical floristic region. IV. Subalpine floristic region.

Based on the above discussions, Yunnan possibly witnessed only on the late Miocene and late Pliocene floras, because of their different floristic features between the late Miocene and late Plio- relative abundance in Yunnan (Tables 3 and 4). cene. This allows us to observe floristic changes from the late The late Miocene Shuitangba flora is represented by seven areal Miocene to late Pliocene through to today. In northern Yunnan, the types at the generic level, the Old World Temperate type of which proportion of temperate elements at the generic level has increased being the most abundant, followed by the North Temperate type. since the late Miocene (Jacques et al., 2014). This is best exemplified The late Miocene Xianfeng flora is dominated by the North by the fact that sclerophyllous evergreen broad-leaved forests were Temperate type followed by the Tropical Asia and Tropical America apparently absent during the late Miocene, but were well estab- disjunct type and the East Asia and North America disjunct type lished in the late Pliocene and are still seen today. In southern (Fig. 6). The late Miocene Bangmai and Xiaolongtan floras comprise Yunnan, the percentage of tropical elements declined significantly, several areal types with each including various genera. The as was previously noticed by Jacques et al. (2014). Today, Yunnan is Pantropic type frequently occurred in both floras, with the number covered mainly by subtropical evergreen broad-leaved forests, with of genera being 16 and 9, respectively. Other important areal types tropical forests being restricted to its southern most parts. Overall, are the East Asia and North America disjunct type, the Tropical Asia it appears that thermophylic floras have moved southward since (IndoeMalaysia) type and the North Temperate type. It is inter- the late Miocene, purportedly in response to elevation changes esting that the Pantropic type and Tropical Asia (IndoeMalaysia) (Jacques et al., 2014). type are best to well represented in the Bangmai and Xiaolongtan floras in southern Yunnan, whereas they are rare to absent in the 6. Areal type analyses of seed plants Shuitangba and Xianfeng floras in northern Yunnan (Fig. 6). Because these two areal types of seed plants reflect a tropical Research into spatial distribution patterns of plants can help floristic composition, the Bangmai and Xiaolongtan floras may have botanists to better understand the origin of a flora and its rela- a higher percentage of tropical elements than the Shuitangba and tionship with others. In China, this kind of study began in 1965 Xianfeng floras. Moreover, it should be noted that the Bangmai and (Wu, 1965). In 1991, Wu (1991) summarized the results of previous Xiaolongtan floras have similar compositions of areal types. This studies and proposed a term named “areal type” to reveal the seems to disagree with the suggested subdivision of floristic re- distribution of a genus of seed plants. In that summary, 15 areal gions, namely that the late Miocene Bangmai flora represented a types of seed plants distributed in China were defined and tropical floristic region while the late Miocene Xiaolongtan flora described (Wu, 1991). They are 1. Cosmopolitan, 2. Pantropic, 3. represented a subtropical floristic region. However, the Pantropic Tropical Asia and Tropical America disjunct, 4. Old World Tropic, 5. type of the former is considerably richer than the latter, which Tropical Asia and Tropical Australasia, 6. Tropical Asia to Tropical apparently supports our floristic region division. Hence it can be Africa, 7. Tropical Asia (IndoeMalaysia), 8. North Temperate, 9. East concluded that in the late Miocene southern Yunnan had far more Asia and North America disjunct, 10. Old World Temperate, 11. Pantropic type elements than northern Yunnan. Temperate Asia, 12. Mediterranean, West Asia to Central Asia, 13. To reconstruct the situation in the late Pliocene, four fossil floras Central Asia, 14. East Asia, and 15. Endemic to China (Wu, 1991; Wu can be used: the Fudong, Eryuan, Longmen and Tuantian floras. As et al., 2003). In the present review, we apply the definitions by Wu is shown, the first three floras from northwestern Yunnan have only (1991) to analyze the areal types of seed plant genera from the a few areal types, meaning low diversity of areal types (Fig. 7). Cenozoic of Yunnan. To achieve the best spatial resolution, we focus Interestingly, they are all dominated by the North Temperate type,

Table 3 Areal types of four late Miocene ﬂoras from Yunnan, following the deﬁnition of 15 areal types by Wu (1991).

Areal type Shuitangba Xianfeng Bangmai Xiaolongtan

1 Chenopodium, Nymphaea / Sophora Sophora, Typha 2 Zanthoxylum / Albizzia, Capparis, Celtis, Albizzia, Cassia, Dalbergia, Chrysophyllum, Dalbergia, Ficus, Helicteres, Dodonaea, Ficus, Indigofera, Ilex, Millettia, Mucuna, Piper, Smilax, Jasminum, Passiﬂora, Smilax Terminalia, Ternstroemia, Tetragonia, Zanthoxylum 3/ Litsea, Nothaphoebe, Phoebe Cinnamomum,Litsea, Ormosia, Schoepﬁa, Cinnamomum, Litsea, Ormosia, Styrax Pithecellobium 4 Cayratia Alangium, Albizzia Lumnitzera, Pittosporum, Syzygium Alangium, Erythrophleum 5/ Cinnamomum Toona Desmos, Rhamnella 6/ 7/ Cyclobalanopsis, Machilus Aphanamixis, Cyclobalanopsis, Murraya, Cyclobalanopsis, Distylium, Exbucklandia, Neocinnamomum, Reevesia, Shuteria, Machilus, Nothaphoebe, Phoebe Sinosideroxylon, Stranvaesia 8 Alnus, Corylus, Staphylea Acer, Alnus, Carpinus, Pinus, Betula, Populus, Quercus, Rhus, Sorbus, Acer, Castanea, Juglans, Myrica, Quercus, Salix Quercus, Rhododendron, Rhus Viburnum 9 Carya, Ampelopsis Castanopsis, Lithocarpus, Tsuga Berchemia, Castanopsis, Desmodium, Gleditsia, Berchemia, Castanopsis, Desmodium, Hydrangea, Lithocarpus, Photinia, Schisandra, Gleditsia, Lespedeza, Magnolia, Toxicodendron Lithocarpus, Robinia, 10 Aldrovanda, Cucubalus, / Loranthus, Trapa / Ligustrum, Trapa 11 / / / Pterocarya 12 / Pistacia Pistacia Laurus 13 / / / 14 Euryale Platycarya Maackia / 15 / / / /

Note: 1. Cosmopolitan; 2. Pantropic; 3. Tropical Asia and Tropical America disjunct; 4. Old World Tropic; 5. Tropical Asia and Tropical Australasia; 6. Tropical Asia to Tropical Africa; 7. Tropical Asia (IndoeMalaysia); 8. North Temperate; 9. East Asia and North America disjunct; 10. Old World Temperate; 11. Temperate Asia; 12. Mediterranean, West Asia to Central Asia; 13. Central Asia; 14. East Asia; 15. Endemic to China.

Table 4 Tropical Asia to Tropical Africa type, which are found mainly in Areal types of four late Pliocene floras from Yunnan, with the areal type number tropical zones. Therefore, the Tuantian flora is closer to a tropical following Table 3. flora than the remaining three, as is also indicated by our floristic Areal Fudong Eryuan Longmen Tuantian analyses. In short, late Pliocene plant assemblages in northwestern type Yunnan were dominated exclusively by the North Temperate type, 1 / // / while in southwestern Yunnan the Tropical Asia (IndoeMalaysia) 2 / Celtis / Dioscorea, Ilex type and the East Asia and North America disjunct type also played 3/ / / Cinnamomum, important roles. Ormosia 4 / / / Mallotus, Syzygium 5/ / / Evodia 7. Palaeoclimates reflected by the fossil floras 6/ / Garcinia 7 Cyclobalanopsis / / Cyclea, Because plants only exist in a climate zone that they can tolerate, Cyclobalanopsis, fl Exbucklandia, they re ect climate characteristics of their distributional ranges. Heterosmilax, Although a fossil flora can tell us the general climate situation (e.g., Machilus, Rhodoleia the late Miocene Bangmai flora dominated by tropical elements 8 Acer, Berberis, Acer, Pinus, Acer, Cupressus, Betula, Carpinus, indicates a warm climate), quantitative climate results allow a Picea, Pinus, Populus, Pinus, Populus, Castanea, Cornus, better understanding of past climate. As methodologies develop, Populus, Quercus, Quercus, Fraxinus, Juglans, fl Quercus, Salix Viburnum Rhododendron, Myrica, Ulmus fossil oras become valuable proxies for quantitative re- Salix constructions of palaeoclimates by using appropriate approaches. 9 Desmodium, / Lithocarpus Berchemia, In Yunnan, 10 megafossil floras have been investigated quantita- Lithocarpus Castanopsis, tively regarding their palaeoclimates. They are exclusively Neogene Lindera, fl Mahonia, Robinia in age, i.e., the early Miocene Shuanghe ora (Sun et al., 2011), the 10 / Trapa Trapa / early to middle Miocene Mangdan flora (Zhao et al., 2004), the 11 / / / / middle Miocene Tuantian flora (Sun et al., 2011), the late Miocene 12 / // / Xianfeng, Xiaolongtan and Bangmai floras (Xia et al., 2009; Jacques 13 / / // et al., 2011; Xing et al., 2012), and the late Pliocene Fudong, Long- 14 //// fl 15 / / / / men, Eryuan and Tuantian oras (Sun et al., 2011; Xie et al., 2012; Su et al., 2013a; Huang et al., 2015a). The reconstructed palaeoclimate results provide insights into climate changes and suggesting temperate floristic features. This is in line with results of monsoon development in Yunnan throughout the Neogene, and our floristic analyses that northwestern Yunnan represented a thus help us to better understand the environmental conditions subalpine floristic region. Different from the Fudong, Eryuan and under which plant diversity evolved. Longmen floras, the Tuantian flora in southwestern Yunnan is In the Miocene, estimated temperatures indicate that northern much more diverse with regards to areal types (Fig. 7). Although Yunnan was much warmer than it is now, suggesting a significant the North Temperate type is also dominant, the Tropical Asia cooling trend to the present (Sun et al., 2011; Xing et al., 2012). For (IndoeMalaysia) type and the East Asia and North America disjunct example, the mean annual temperature (MAT) of the early Miocene type are frequent. Other areal types include the Pantropic type, the Shuanghe flora was estimated to be 13.8e21.7 C by Coexistence Tropical Asia and Tropical America disjunct type, the Old World Approach (CA) and 18.2 ± 3.6 C by Leaf Margin Analysis (LMA), Tropic type, the Tropical Asia and Tropical Australasia type, and the compared to 12.3 C today (Sun et al., 2011). By contrast,

Fig. 6. Composition of areal types for four late Miocene ﬂoras from Yunnan.

Fig. 7. Composition of areal types for four late Pliocene floras from Yunnan. temperatures in southern Yunnan have changed only moderately palaeoclimate results also demonstrate that summer precipitation since the Miocene (Zhao et al., 2004; Xia et al., 2009). For example, has increased while winter precipitation has decreased since the the MAT estimated from the early to middle Miocene Mangdan late Miocene (Jacques et al., 2011; Xing et al., 2012; Su et al., 2013a; flora using the CA was 18.8e20.5 C, close to 19e21 C at present Huang et al., 2015a), suggesting a strengthening of the precipitation (Zhao et al., 2004). The observed different patterns of temperature seasonality in Yunnan. changes between northern and southern Yunnan might be attributed to the difference in latitude or altitude or both. Northern 8. Conclusion Yunnan clearly had higher latitude than southern Yunnan, which supports a previous interpretation that the late Cenozoic cooling of Based on our integration of published palaeobotanical data from the Northern Hemisphere was more pronounced in higher latitudes Yunnan, our summary reaches six key points as stated below. than in lower ones (Uhl et al., 2007; Utescher et al., 2011). On the other hand, northern Yunnan underwent significant surface uplift (1) Yunnan has a rich Cenozoic plant fossil record which has during the Neogene due to the southeastern extrusion of the Ti- been investigated extensively, particularly over the past two betan Plateau (Zhang and Ding, 2003; Clark et al., 2005), whereas decades, with an increasing number of fossil taxa being re- southern Yunnan remained almost at the same level (Jacques et al., ported. These fossil taxa are important for answering past 2014). The considerable altitude increase probably was the other plant diversity and floral evolution in this region. factor leading to the observed surface temperature decline in (2) Plant species from the Cenozoic of Yunnan are diverse. To northern Yunnan, while the relatively stable elevation in southern date, approximately 386 fossil species belonging to 170 Yunnan may explain the almost unchanged temperature level. The genera of 66 families have been documented. They cover relevant importance of latitude versus altitude in controlling tem- ferns, gymnosperms and angiosperms, of which angio- perature changes, however, is currently unanswerable. sperms are by far the most diverse, including 353 species Apart from this cooling trend, Yunnan has also been affected by grouped into 155 genera of 60 families. In the fossil angio- an aridification since the Miocene. Palaeoclimate reconstructions sperms, Fagaceae, Fabaceae, Juglandaceae, Lauraceae and indicate that environments were humid in Yunnan during the late Rosaceae are among the most diverse families; and Querucs, Miocene, and thereafter a drying trend occurred (Xia et al., 2009; Castanopsis, Acer, Lithocarpus, Cyclobalanopsis and Cinnamo- Jacques et al., 2011; Sun et al., 2011; Xing et al., 2012). For mum are among the most species-rich genera. example, the late Miocene Xianfeng flora revealed a mean annual (3) Most of the families and genera represented in the fossil precipitation (MAP) of 1206e1613 mm, higher than the present- record are still part of the modern natural vegetation in day value of 1011 mm (Xing et al., 2012). This post-Miocene aridi- Yunnan, but some genera have disappeared, possibly as a fication appears to be particularly pronounced in the dry season. result of an aridification and/or extension of the dry season. Various palaeoclimate reconstructions indicate that Yunnan had So far, seven genera are known to have become extinct in higher precipitation in summer but less rainfall in winter during Yunnan, namely Berryophyllum, Cedrelospermum, Cedrus, the late Miocene (Xia et al., 2009; Jacques et al., 2011; Xing et al., Palaeocarya, Podocarpium, Sequoia and Wataria. 2012) and late Pliocene (Xie et al., 2012; Su et al., 2013a; Huang (4) In the late Miocene, Yunnan had three floristic regions: a et al., 2015a). For instance, during the late Miocene the mean northern subtropical zone in the northeast, a subtropical monthly precipitation of the three wettest months was zone in the east, and a tropical zone in the southwest. In the 150e250 mm, while that of the three driest months was less than late Pliocene, Yunnan had two kinds of floristic regions: a 50 mm, suggesting a prominent precipitation seasonality. These subalpine floristic region in the northwest, and two

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Please cite this article in press as: Huang, Y.-J., et al., Cenozoic plant diversity of Yunnan: A review, Plant Diversity (2016), http://dx.doi.org/ 10.1016/j.pld.2016.11.004