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A New Species of () from the Upper Pliocene of West Yunnan, and Comments on Phytogeography and Insect Herbivory

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A New Species of Rhodoleia (Hamamelidaceae) from the Upper Pliocene of West Yunnan, China and Comments on Phytogeography and Insect Herbivory

WU Jingyu1, 2, *, ZHAO Zhenrui1, LI Qijia1, LIU Yusheng (Christopher)3, XIE Sanping1, DING Suting1, 2 and SUN Bainian1, *

1 Key Laboratory of Mineral Resources in Western China (Gansu Province), School of Earth Sciences, Lanzhou University, Lanzhou 730000, China 2 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, CAS, Nanjing 210008, China 3 Don Sundquist Center of Excellence in Paleontology, Department of Biological Sciences, East Tennessee State University, Box 70703, Johnson City, Tennessee 37614–1710, USA

Abstract: In Europe, fossil fruits and seeds of Rhodoleia (Hamamelidaceae) have been described from the Upper Cretaceous to the Miocene, whereas no fossil record of Rhodoleia has been reported in Asia, where the modern species occur. Herein, 21 fossil leaves identified as Rhodoleia tengchongensis sp. nov. are described from the Upper Pliocene of Tengchong County, Yunnan Province, Southwest China. The fossils exhibit elliptic lamina with entire margins, simple brochidodromous major secondary veins, mixed percurrent intercostal tertiary veins, and looped exterior tertiaries. The leaf cuticle is characterized by pentagonal or hexagonal cells, stellate multicellular trichomes, and paracytic stomata. The combination of leaf architecture and cuticular characteristics suggests that the fossil leaves should be classified into the genus Rhodoleia. The fossil distributions indicate that the genus Rhodoleia might originate from Central Europe, and that migrated to Asia prior to the Late Pliocene. Additionally, insect damage is investigated, and different types of damage, such as hole feeding, margin feeding, surface feeding, and galling, are observed on the thirteen fossil leaves. Based on the damage frequencies for the fossil and extant leaves, the specific feeding behavior of insects on Rhodoleia trees appears to have been established as early as the Late Pliocene. The high occurrence of Rhodoleia insect herbivory may attract the insect-foraging birds, thereby increasing the probability of pollination.

Key words: Rhodoleia, leaf cuticle, phytogeography, insect herbivory, Pliocene, Yunnan Province

1 Introduction (Mai, 2001). Within the family Hamamelidaceae, leaf architecture The genus Rhodoleia Champion ex Hooker is one of 31 and anatomical characteristics are helpful for generic genera in the family Hamamelidaceae. The genus classification (Li and Hickey, 1988; Fang, 1990; Pan et al., comprises 7 species (Exell, 1933) or 9 species (Chang, 1990). In this study, based on a detailed comparison of 1973) of evergreen trees or shrubs distributed in South leaf architecture and cuticular features, 21 fossil leaves China, , Thailand, , Malaysia, Sumatra, from the Upper Pliocene in Yunnan Province are and (Zhang et al., 2003). The fossil fruits and identified as Rhodoleia tengchongensis sp. nov. The seeds of several species of Rhodoleia are known in Europe discovery of this new species from Southwest China, as from the Upper Cretaceous to the Miocene (Mai and the only leaf record of Rhodoleia to date, not only Walther, 1985; Knobloch and Mai, 1986; Mai, 1987, provides a valuable opportunity for revealing the leaf 2001). However, no any fossil record of Rhodoleia has architecture and cuticular differences between Pliocene been documented in Asia, and no fossil leaves, wood or fossils and extant species but also improves our pollen have thus far been found elsewhere in the world understanding of the phytogeography of this genus and the * Corresponding author. E-mail: [email protected] (J.Y. Wu); [email protected] (B.N. Sun)

© 2015 Geological Society of China Oct. 2015 ACTA GEOLOGICA SINICA (English Edition) Vol. 89 No. 5 1441 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Pliocene climate of Southwest China. (Shi et al., 2012) and deposition rate (Li and Xue, 1999; -insect interactions have dominated terrestrial Sun et al., 2012), the fossil-bearing deposits studied are ecosystems for over 420 million years (Labandeira, 2006; undoubtedly of the Late Pliocene (3.3–2.8 Ma). Wilf, 2008; Na et al., 2014). The remains of insect feedings on fossil have been widely investigated 3 Material and Methods throughout the Phanerozoic (e.g., Chaloner et al., 1991; Banerji, 2004; Wilf et al., 2005; Prevec et al., 2009), and it The extant leaves for comparison were collected from is generally accepted that insect damage on fossil leaves Kunming and Pingbian of Yunnan Province, Guangzhou can provide abundant information regarding terrestrial of Guangdong Province, and Haikou of Hainan Province. food webs (Wilf and Labandeira, 1999; Labandeira, 2006; To study the leaf architecture, the extant leaves were Carvalho et al., 2014; Donovan et al., 2014). In the present cleared with a 10% solution of NaOH. The experimental paper, the insect damage type and frequency are compared treatments used for the fossil and extant cuticles are well between Rhodoleia fossil and extant leaves, and the described in previous studies (Dao et al., 2013; He et al., specialist herbivores for this genus are discussed. 2014). The fossil cuticles were embedded in paraffin and cut using a Leica RM2255 microtome. The terminology 2 Geological Setting for leaf architecture follows Manual of Leaf Architecture (Ellis et al., 2009), and the foliar cuticle terminology is The fossil leaves were collected from an open-cast that of Dilcher (1974) and Wilkinson (1979). The insect diatomite mine ca. 1 km west of Tuantian Town (24° 41′ damage types are according to Labandeira et al. (2007).

N, 98° 38′ E; Fig. 1a), Tengchong County, Yunnan The estimation of the leaf dry mass per area (MA) for Province, Southwest China. The fossil-bearing diatomites the fossil leaves is according to the formula of Royer et al. 2 belong to the Upper Pliocene Mangbang Formation (Fig. (2007): lg[MA] =3.070+0.382×lg[PW /A], where MA is the 1b) which is subdivided into three lithologic units (Ge and leaf dry mass per area (g m–2), PW is the petiole width Li, 1999; Shang, 2003; Li et al., 2004; Sun et al., 2004). (mm), and A is the leaf area (mm2). Based on SHRIMP zircon U-Pb dating of volcanic rocks All fossil specimens, cuticle slides and SEM stubs are

Fig. 1. Distribution map of Rhodoleia and stratigraphic section of the fossil location. a, The geographic map of fossil site and extant distributions. b, The stratigraphic section through the Mangbang Formation in Tengchong County, Yunnan Province, China (after Ge and Li, 1999; Shang, 2003; Li et al., 2004; Sun et al., 2004). 1442 Vol. 89 No. 5 ACTA GEOLOGICA SINICA (English Edition) Oct. 2015 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags stored at the Institute of Palaeontology and Stratigraphy, and decurrent attachment to midvein. Interior and minor Lanzhou University, Gansu Province, China. secondaries absent. Intersecondaries span more than 50% of the length of the subjacent secondary, occuring at less 4 Systematics and Comparison than one per intercostal area; proximal course is parallel to major secondaries, and distal course perpendicular to a 4.1 Systematics subjacent major secondary (Fig. 2a–i). Intercostal tertiary Order Hamamelidales Griseb. veins mixed percurrent with obtuse angle to midvein and Family Hamamelidaceae R. Brown inconsistent vein angle variability (Fig. 2j, k). Exterior Genus Rhodoleia Champion ex Hooker tertiaries looped (Fig. 2j). Quaternary vein fabric irregular Rhodoleia tengchongensis J.Y. Wu et B.N. Sun sp. reticulate. Areolation shows moderate development. nov. Freely ending veinlets mostly with two or more branches Holotype: FTP–553A (Fig. 2e; Fig. 4c) (Fig. 2j, k). Marginal ultimate venation looped (Fig. 2j). Paratypes: FTP–010A (Fig. 2a, j, k; Fig. 4e, g), FTP– Leaves hypostomatic: Adaxial epidermis ca. 9 μm 010B (Fig. 2b), FTP–315–6 (Fig. 2c), FTP–309–6 (Fig. 2i; thick; cells isodiametric, pentagonal or hexagonal, and 11– Fig. 3c, d; Fig. 4f, h, k, l), FTP–281 (Fig. 2f; Fig. 3b), FTP 25 μm long and 9–18 μm wide; anticlinal cell walls –323–1 (Fig. 2d; Fig. a; Fig. 4a, b, i), FTP–14009 (Fig. straight and developing into a honeycomb, periclinal walls 2g), FTP–14065 (Fig. 2h). smooth (Fig. 3a, c; Fig. 4a). Abaxial epidermis ca. 8 μm Other specimens: FTP–553B, FTP–14016, FTP– thick; cells isodiametric, pentagonal or hexagonal, 12–27 14034, FTP–091, FTP–317–23, FTP–232, FTP–310, FTP μm long and 8–20 μm wide, and each cell covered by a –307–5, FTP–543, FTP–225–21, FTP–504, FTP–135, papilla on the outer wall (Fig. 4b-d); anticlinal walls FTP–304–27, FTP–226–16. straight and honeycombed (Fig. 4a). Stomatal apparatus Type locality: Tuantian Town (N 24° 41′, E 98° 38′), paracytic, randomly orientated and slightly sunk (Fig. 4g– Tengchong County, Yunnan Province, China (Fig. 1A). i). Trichomes occur on both adaxial and abaxial epidermis, Stratigraphy: diatomite beds, Upper Mangbang multicellular and stellate, the trichome base ca. 20 μm Formation. across (Fig. 3a; Fig. 4e, f). Age: Piacenzian, Late Pliocene. Etymology: The name refers to the type locality, 4.2 Comparison Tengchong County. All fossil leaves in the present study share the same leaf Diagnosis: Blade attachment marginal, lamina size architectural characters, such as an elliptic laminar shape, microphyll to notophyll; lamina shape elliptic with medial a leathery texture, an entire margin, pinnate venation, symmetry and basal symmetry, margin entire. Primary obscure 3 basal veins, and simple brochidodromous major venation pinnate, obscurely three basal veins, major secondary veins, demonstrating the closest relationship to secondary veins simple brochidodromous; genus Rhodoleia of Hamamelidaceae (Li and Hickey, intersecondaries occur at less than one per intercostal area, 1988; Zhang et al., 2003). However, the leaves of intercostal tertiary veins mixed percurrent, exterior Rhodoleia are usually confused with those of tertiaries looped. Adaxial and abaxial epidermal cells Rhododendron (Ericaceae) and Distylium pentagonal or hexagonal; anticlinal walls straight and (Hamamelidaceae) with regard to morphology (Zhang et honeycombed. Leaves hypostomatic, stoma paracytic and al., 2003). Fortunately, the cuticular characteristics randomly orientated. Trichomes occur on adaxial and warrant their separation, as the leaves of Rhodoleia abaxial epidermis, stellate and multicellular. possess paracytic stomata and multicellular trichomes; in Description: Blade attachment marginal, lamina size contrast, Rhododendron leaves have anomocytic stomata microphyll to notophyll, 5.6–10.5 cm long and 2.6–5.5 cm and unicellular trichomes (Wang et al., 2007), and wide, L:W ratio 2.2:1 to 1.7:1, lamina shape variable, Distylium leaves usually have undulated cell walls and no usually elliptic with medial symmetry and basal trichomes (Pan et al., 1990). symmetry. Petiole 1.0–2.0 cm long and 1.0–1.6 mm wide Exell (1933) recognized seven species in Rhodoleia, but (Fig. 2e–g). Margin entire with acute apex angle, Vink (1957) reduced them to one species and considered acuminate apex shape, acute to obtuse base angle, and that the variations of this genus are within a polymorphous straight to convex base shape (Fig. 2a–i). Primary species: . Chang (1973) argued that venation pinnate with no naked basal veins, obscurely there are nine species in Rhodoleia, with six species being three basal veins, and no agrophic veins. Major secondary endemic to China based on differences in leaf veins, fruits veins 7–9 pairs, simple brochidodromous with irregular and flowers. To provide a detailed comparison of leaf spacing, uniform secondary angle to midvein (55–65º), architecture and cuticular characteristics between fossil Oct. 2015 ACTA GEOLOGICA SINICA (English Edition) Vol. 89 No. 5 1443 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Fig. 2. Fossil leaves of Rhodoleia tengchongensis sp. nov., and the contrastive extant leaves. a–j, l, m, scale bar = 1 cm; j, k, scale bar = 0.3 cm. a, Gross morphology of FTP–010A; b, Gross morphology of FTP–010B; c, Gross morphology of FTP–315–6; d, Gross morphology of FTP–323–1; e, Gross morphology of FTP–553A; f, Gross morphology of FTP–281; g, Gross morphology of FTP–14009; h, Gross morphology of FTP–14065; i, Gross morphology of FTP–309–6; j, Showing brochidodromous secondary veins and alternate percurrent tertiary veins, specimen no. FTP–010A; k, Showing the regular polygonal reticulate fourth veins and branched fifth veins, specimen no. FTP–010A; l, Extant leaves of Rhodoleia championii showing the regular polygonal reticulate fourth veins and branched fifth veins; m, Extant leaves of Rh. henryi, showing brochidodromous secondary veins and alternate percurrent tertiary veins; n, Extant leaf of Rh. henryi. 1444 Vol. 89 No. 5 ACTA GEOLOGICA SINICA (English Edition) Oct. 2015 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Fig. 3. Scale bar = 50 µm. a–d. Cuticles of Rhodoleia tengchongensis sp. nov., under the LM (a, Adaxial epidermis of specimen no. FTP–323–1, notice the stellate trichome; b, Abaxial epidermis of specimen no. FTP–281; c, Adaxial epidermis of specimen no. FTP –309–6; d, Abaxial epidermis of specimen no. FTP–309–6); e, f, Cuticles of extant leaves of Rh. henryi, under the light microscopy (e, Adaxial epidermis; f, Abaxial epidermis). and extant leaves, six extant species of Rhodoleia characteristics are closely comparable with those of extant described by Chang (1973) were selected for the Rhodoleia (Table 1; Fig. 5a–l). However, minor comparison with the Tengchong fossils. differences can also be found between the fossils and most The fossil cuticle displays such characteristics as of the extant species. For example, Rh. parvipetala has pentagonal or hexagonal cells, stellate trichomes, paracytic four regular papillae at two ends of the guard cells on the stomata, and papillae present on epidermal cells. All these inner surface (Fig. 5i), and Rh. macrocarpa displays more Oct. 2015 ACTA GEOLOGICA SINICA (English Edition) Vol. 89 No. 5 1445 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Fig. 4. a, b, d, j, scale bar = 50 µm; c, scale bar = 100 µm; e, f, k, l, scale bar = 20 µm; g–i, scale bar = 10 µm. a–i, Cuticles of fossil leaves of Rhodoleia tengchongensis sp. nov., under the SEM (a, Adaxial epidermis of FTP–323–1, inner surface; b, Abaxial epidermis of FTP–323–1, outer surface; c, Abaxial epidermis of FTP–553, inner surface; d, Abaxial epidermis of FTP–010, inner surface; e, Trichome base of adaxial epidermis of FTP–010, outer surface; f, Trichome base of adaxial epidermis of FTP–309–6; g, Stoma apparatus of FTP–010, inner surface; h, Stoma appara- tus of FTP–309–6, inner surface; i, Stoma apparatus of FTP–323–1, outer surface); j, Section of extant leaf of Rh. championii, under the SEM; k, l, Section of abaxial epidermis of fossil leaves under the LM (k, Showing papillaes and anticlinal walls; l, Showing stomatal apparatus). extrusive papillae and sunken stomata on the outer surface extant Rh. championii and Rh. henryi. However, these two (Fig. 5g). Rhodoleia forrestii and Rh. stenopetala have species have ruglike periclinal walls that differ from those cuticular features similar to those of the fossil leaves, but of the present fossil leaves. As no other fossil leaf has ever these two species exhibit reduced angles between the been reported, a further comparison is limited. The secondary veins and the midrib (Table 1). Regarding leaf comparisons above suggest that no extant species has leaf architectures, the present fossil leaves most resemble architectural and cuticular characters concordant with our 1446 Vol. 89 No. 5 ACTA GEOLOGICA SINICA (English Edition) Oct. 2015 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Fig. 5. Cuticles of extant leaves of Rhodoleia, under the SEM. a, b, d–h, j, l, Scale bar = 50 µm; c, Scale bar = 10 µm; i, k, Scale bar = 20 µm. a, Adaxial epidermis of Rhdoleia championii, inner surface; b, Abaxial epidermis of Rh. championii, outer surface; c, Stoma apparatus Rh. championii, inner surface; d, Adaxial epidermis of Rh. henryi, inner surface; e, Abaxial epidermis of Rh. henryi, inner surface; f, Stoma apparatus of Rh. henryi, outer surface; g, Abaxial epidermis of Rh. macrocarpa, outer surface; h, Abaxial epidermis of Rh. parvipetala, outer surface; i, Abaxial epidermis of Rh. parvipetala, inner surface; j, Abaxial epidermis of Rh. forrestii, outer surface; k, Abaxial epidermis of Rh. forrestii, inner surface; l, Abaxial epidermis of Rh. stenopetala, outer surface. fossil leaves. Fossil records of Rhodoleia are well known in Europe from the Upper Cretaceous to the Miocene. For example, 5 Discussions the earliest fossil seed of Rh. cretacea was reported from the Upper Cretaceous of South Oebisfelde in Germany 5.1 Phytogeography and paleoclimate (Knobloch and Mai, 1986), followed by a Late Paleocene Oct. 2015 ACTA GEOLOGICA SINICA (English Edition) Vol. 89 No. 5 1447 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Fig. 6. Insect damage types of Rhodoleia tengchongensis sp. nov. Scale bar = 5 mm. a, Hole feeding (DT05). Specimen no. FTP–010; b, Margin feeding (DT12) and hole feeding (DT02), specimen no. FTP–315–6; c, Margin feeding (DT81), specimen no. FTP–226–16; d, e, Margin feeding (DT81), specimen no. FTP–309–6; f, Hole feeding (DT03) and margin feeding (DT12), specimen no. FTP– 553A; g, Margin feeding (DT15), specimen no. FTP–14009; h, Margin feeding (DT13), specimen no. FTP–307–5; i, Margin feeding (DT81), specimen no. FTP–317–23; j, Surface feeding (DT31) and galling (DT80), specimen no. FTP–135; k, Surface feeding (DT31), specimen no. FTP–504; l–n, Surface feeding (DT30), specimen no. FTP–317–23. seed of Rh. hercynica (Mai, 1987). Mai and Walther and the Lower Miocene in Osieczów (West Poland), (1985) described some fruits and seeds of Rh. bellmannii which proves the continued presence of this genus during from the Upper Eocene of White Elster Basin in Germany. the Miocene in Europe (Mai, 1968, 2001). In Asia, where Fossil seeds and fruits of Rh. bifollicularis were obtained modern Rhodoleia species occur, Rh. tengchongensis from the Middle Miocene in Herzogenrath (West German) described herein is the only confirmed fossil record of this 1448 Vol. 89 No. 5 ACTA GEOLOGICA SINICA (English Edition) Oct. 2015 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Table 1 Leaf architecture of the present fossil and extant Rhodoleia (after Zhang et al., 2003) Pairs of Secondary Petiole Length Width Apex Apex Base Base Major secondary Taxon Shape major angle to length (cm) (cm) angle shape angle shape vein framework secondaries midvein (cm) straight Rh. acute to simple elliptic 5.6–10.5 2.6–5.5 acute acuminate to 7–9 55–65º 1–2 tengchongensis obtuse brochidodromous convex ovate to acute to simple Rh. championii 7–16 4.5–10.5 acute acuminate convex 7–9 ca. 60º 3–5.5 elliptic obtuse brochidodromous straight ovate to simple Rh. henryi ca. 11 3–6 acute acuminate acute to 6–9 45–65º ca. 5 elliptic brochidodromous convex oblong to simple Rh. forrestii 7–15 2–7 acute acuminate acute convex 7–9 ca. 45º ca. 3.5 lanceolate brochidodromous Rh. simple elliptic 7–11 3–6 acute acuminate acute convex 8 or 9 ca. 75º 2.5–4 macrocarpa brochidodromous simple Rh. parvipetala oblong 5–10 2–4.5 acute acuminate acute convex 6–9 55–75º 2–4.5 brochidodromous acute to acute to simple Rh. stenopetala ovate 6–10 4–6.5 obtuse convex 4–6 30–50º 3–5 obtuse convex brochidodromous genus. In addition, the phylogenetic estimation indicate leaf area loss to herbivory to be greater in warmer than in that the divergence time of Rhodoleia was from the Late cooler environments (Coley and Aide, 1991; Coley and Cretaceous to the Early Eocene (Qi et al., 2012), which is Barone, 1996; Pennings and Silliman, 2005; Adams et al., roughly equivalent to the early occurrence age in Europe. 2010). According to observations of insect damage Therefore, the distribution of previous fossil records might frequency on fossil leaves from the Early Cenozoic of the suggest that the genus Rhodoleia originated from central Central United States, Wilf (2008) indicated that the insect Europe, and migrating from Europe to Asia prior to the -feeding diversity and frequency increase in variability Late Pliocene. However, due to the inadequate with decreased rainfall. Wu (2009) and Sun et al. (2011) paleobotanical data in East Asia, the origin and divergence had described 28 genera within 20 families of pattern of Rhodoleia still need a further research. angiospermous leaves from the Upper Pliocene of Extant Rhodoleia trees are distributed in Indonesia, Tengchong flora. We examined these fossil leaves, and Malaysia, Myanmar, Vietnam, Thailand and South China, found that among a total of 836 fossil leaves, only 97 ranging from 7º S to 27º N (Zhang and Lu, 1995; Suddee specimens show insect damages. In contrast with the Early and Middleton, 2003; Zhang et al., 2003). According to Cenozoic floras of the United States (e.g., Wilf and the geographic range of Rhodoleia, its climatic Labandeira, 1999; Wilf et al., 2001; Currano et al., 2008), requirements appear to be 15–27° C mean annual the Pliocene Tengchong flora exhibits a remarkably lower temperatures (MAT) and 1000–2500 mm mean annual percentage of insect damages. Based on Climate Leaf precipitations (MAP) (NMBC, 1983). Hence, the present Analysis Multivariate Program, Tengchong during the fossils might also have lived under similar climatic Pliocene experienced a growing season precipitation conditions during the Late Pliocene. Indeed, based on both (GSP) of 1834.3–1901.2 mm (Xie et al., 2012). Therefore, quantitative and qualitative analyses, a Pliocene climate the insect damage frequency of the Tengchong flora might reconstruction for Tengchong flora predicts warm and have been restricted by the plentiful rainfall. humid conditions (Tao and Du, 1982; Xu et al., 2004; Wu The Late Pliocene Tuantian flora consists mainly of et al., 2009; Sun et al., 2011; Xie et al., 2012), which is Lauraceae, Fagaceae, Betulaceae, Hamamelidaceae, quite consistent with the climate requirements of the genus Leguminosae, Myricaceae, Ulmaceae and Juglandaceae Rhodoleia. (Sun et al., 2011). We observed these fossil leaves, and Table 2 lists 11 genera (≥20 specimens) frequently 5.2 Insect herbivory showing insect damages. Royer et al. (2007) established a

In the past, many paleobiologists (e.g., Huston, 1994; method to determine the leaf mass per area (MA) for Wilf and Labandeira, 1999; Wilf et al., 2003; Currano et fossils and indicated that insect herbivory tends to al., 2008; Adams et al., 2010) focused on the diversity of decrease as MA increases. The MA values for our fossil insect leaf feeding in different climate intervals, leaves are also negatively correlated with the frequency of correlating the insect-feeding diversity with paleolatitude insect herbivory (Fig. 7). However, the present fossil and paleotemperature. On the basis of a more abundant leaves of Rhodoleia and exhibit a much and stable fixed energy supply in low-latitude warm and higher percentage of insect damage than that in other taxa. moist ecosystems, some biologists considered the rate of For example, in the present 21 specimens of Rhodoleia, 13 Oct. 2015 ACTA GEOLOGICA SINICA (English Edition) Vol. 89 No. 5 1449 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Table 2 Percentage of leaves with insect damage and estimated leaf dry mass per area (MA) in the late Pliocene Tengchong flora –2 Family Genus Specimen number Leaves with insect damage (%) MA (g m ) Hamamelidaceae Rhodoleia 21 61.9 86.8±4.8 Hamamelidaceae Exbucklandia 30 46.7 112.5±5.4 Juglandaceae Juglans 38 28.9 73.0±6.2 Lauraceae Machilus 29 13.8 116.7±6.4 Lauraceae Cinnamomum 31 9.7 128.4±8.1 Lauraceae Lindera 54 7.4 131.5±8.6 Betulaceae Betula 52 9.6 102.6±7.4 Betulaceae Carpinus 46 13.0 110.6±6.8 Fagaceae Castanopsis 26 15.4 99.5±5.9 Fagaceae Cyclobalanopsis 20 20.0 79.8±4.4 Fagaceae Castanea 24 25.0 89.4±5.1

insects to utilize such resources for supplementary energy. Therefore, the high occurrence of insect herbivory in Rhodoleia may attract insect-foraging birds to increase the probability of pollination. Indeed, studies of modern plant- insect interactions indicate that the behavior of insect feeding is affected by the physical and chemical characters of plants (Qin and Wang, 2001). Feeding behavior depends on the natural selection of insect types, host plant characters and the ecological environment (Jones et al., 1981; Ameixa et al., 2007). For example, the volatile, color, surface, cuticle wax and chemical composition of plants can attract or repel insects (Glinwood and Pettersson, 2000; David et al., 2002; Simon and Hilker, 2005). As insects search for feasible suitable host plants Fig. 7. Correlation between the percentage of leaves with using vision, olfaction and chemical receptors, many insect damage and estimated leaf dry mass per area (MA) insects become specialist herbivores during the process of for the Pliocene Tengchong flora. Each data point repre- sents a taxon mean, which ≥20 specimens are plotted. insect-plant coevolution (Lei and Hanski, 1997; Qin and Wang, 2001; Gripenberg et al., 2008). Based on the leaves (61.9% ) were damaged by insects, including observations of insect feeding in present fossils and extant damage types of hole feeding, margin feeding, surface Rhodoleia, we can conclude that this genus is suitable for feeding and galling (Fig. 6a–n). For comparison, we insect feeding and that the specific feeding behavior of examined herbarium sheets from the Chinese Virtual insects on Rhodoleia, as well as insects and birds, might Herbarium (CVH, http://www.cvh.org.cn/); of 584 have been established as early as the Late Pliocene. observed extant leaves of Rh. championii, 338 leaves (57.9 %) exhibit damages by insects. Moreover, a similar high 6 Conclusions damage frequency can also be discovered in other Rhodoleia species. Thus, insect herbivory of the Pliocene The main outcomes of this study are as follows. (1) Tengchong flora appears to exhibit a prominent selectivity Based on the comparison of leaf architectural and cuticular between insects and some plant groups, such as Rhodoleia characteristics with those of extant leaves, we identify a and Exbucklandia. new species as Rhodoleia tengchongensis sp. nov. from The high frequency of damage by insects in Rhodoleia the Upper Pliocene in West Yunnan. The present fossil might correlate with the attraction of bird visitors. species is the first record of Rhodoleia in East Asia, where Rhodoleia bears bisexual flowers in tight heads and modern species occur, and also a unique record of leaf produces lipid-rich pollen grains and dilute nectar, with a remains documented worldwide. (2) The modern flowering stage from the late winter to spring of the next distribution of Rhodoleia suggests that the genus lives in a year (Zhang et al., 2003; Zhu et al., 2010). Bird pollination warm climate, with an MAT from 15 °C to 27 °C and an in Rhodoleia has been documented by Doctors van MAP from 1000 mm to 2500 mm. Hence, Rh. Leeuwen (1927) and Corlett (2001), and Gu et al. (2010) tengchongensis might also have lived under similar indicated that relative shortages of fruits and seeds during climatic conditions, that is, a warm and humid climate, in winter months can force birds that normally forage on West Yunnan during the Late Pliocene. The fossil records 1450 Vol. 89 No. 5 ACTA GEOLOGICA SINICA (English Edition) Oct. 2015 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags also suggest that Rhodoleia might originate from central ecology in tropical and temperate regions. John Wiley and Europe, and then migrating to Asia prior to the Late Sons, New York, 25–49. Coley, P.D., and Barone, J.A., 1996. Herbivory and plant Pliocene. (3) The Pliocene Tengchong flora shows a defenses in tropical forests. Annual Review of Ecology and remarkably lower percentage of insect damage, which Systematics, 27: 305–335. might have been restricted by the plentiful rainfall. Corlett, R.T., 2001. Pollination in a degraded tropical landscape: However, Rhodoleia leaves exhibit a high percentage of a case study. Journal of Tropical Ecology, 17(1): insect damages, which indicates that this genus is suitable 155–161. for insect feeding, and that the specific feeding behavior of Currano, E.D., Wilf, P., Wing, S.L., Labandeira, C.C., Lovelock, E.C., and Royer, D.L., 2008. Sharply increased insect insects on Rhodoleia was established as early as the Late herbivory during the Paleocene-Eocene Thermal Maximum. Pliocene. Moreover, seasonal food shortages can force Proceedings of the National Academy of Sciences of the birds that normally forage on insects as a supplementary United States of America, 105(6): 1960–1964. energy source. Therefore, the present fossil leaves may Dao Kequn, Chen junlin, Jin Peihong, Dong Chong, Yang Yi, provide a striking glimpse of the coevolution of insect Xu Xiaohui, Wu Jingyu, Xie Sanping, Lin Zhicheng and Sun Bainian, 2013. A new material of Lindera (Lauraceae) of the herbivory, the feeding habits of birds, and pollination late Pliocene from Tengchong, Yunnan and the genus’ interactions. biogeography significance. Acta Geologica Sinica (English Edition), 87(3): 690–706. Acknowledgements David, J.P., Ferran, A., Gambier, J., and Meyran, J.C., 2002. Taste sensitivity of detritivorous mosquito larvae to This work is granted by the National Natural Science decomposed leaf litter. Journal of Chemical Ecology, 28(5): 983–995. Foundation of China (Nos. 41302009, 41402008, Dilcher, D.L., 1974. Approaches to the identification of 41172022 and 41172021), the Foundation of the State Key angiosperm leaf remains. The Botanical Review, 40(1): 1–157. Laboratory of Paleobiology and Stratigraphy, Nanjing Doctors van Leeuwen, W.M., 1927. Vogelbloemen. 3. Rhodoleia Institute of Geology and Paleontology, CAS (No. teysmanni Miq. Trop. Nature, 16: 2–6. 133102), and the NSF EAR-0746105 to YSL. Donovan, M., Wilf, P., Labandeira, C.C., Johnson, K.R., and Peppe, D.J., 2014. Novel insect leaf-mining after the end- Cretaceous extinction and the demise of Cretaceous leaf Manuscript received Apr. 18, 2014 miners, Great Plains, USA. PloS One, 9: e103542. accepted Nov. 22, 2014 Ellis, B., Daly, D.C., Hickey, L.J., Johnson, K.R., Mitchell, J.D., edited by Fei Hongcai Wilf, P., and Wing, S.L., 2009. Manual of Leaf Architecture. Cornell University Press, New York, USA, 190. Exell, A.W., 1933. A revision of the genus Rhodoleia. References Sunyatsenia, 1: 95–102. Adams, J.M., Brusa, A., Soyeong, A., and Ainuddin, A.N., 2010. Fang Yanming, 1990. A study on leaf micromorphology of Present-day testing of a paleoecological pattern: is there really Chinese Hamamelidaceae – stomatal apparatus. Journal of a latitudinal difference in leaf-feeding insect-damage Nanjing Forestry University, 14(4): 30–35 (in Chinese with diversity? Review of Palaeobotany and Palynology, 162(1): English Abstract). 63–70. Ge Hongru and Li Daiyun, 1999. Cenozoic Coal-bearing Basins Ameixa, O., Almeida, L., Gonçalves, A., and Neto, L., 2007. and Coalforming Regularity in West Yunnan. Yunnan Science Feeding behavior of Liriomyza huidobrensis (Blanchard) and and Technology Press, Kunming, China, 104 (in Chinese). L. trifolii (Burgess) adults on bean leaves. Journal of Insect Glinwood, R.T., and Pettersson, J., 2000. Change in response of Behavior, 20(1): 137–155. Rhopalosiphum padi spring migrants to the repellent winter Banerji, J., 2004. Evidence of insect-plant interactions from the host component methyl salicylate. Entomologia Upper Gondwana Sequence (Lower Cretaceous) in the Experimentalis et Applicata, 94(3): 325–330. Rajmahal Basin, India. Gondwana Research, 7(1): 205–210. Gripenberg, S., Ovaskainen, O., Morriën, E., and Roslin, T., Carvalho, M.R., Wilf, P., Barrios, H., Currano, E.D., Windsor, 2008. Spatial population structure of a specialist leaf-mining D.M., Jaramillo, C.A., and Labandeira, C.C., 2014. Insect leaf moth. Journal of Animal Ecology, 77(4): 757–767. -chewing damage tracks herbivore richness in modern and Gu Lei, Luo Zhonglai, Zhang Dianxiang and Renner, S.S., 2010. ancient forests. PloS One, 9: e94950. Passerine Pollination of Rhodoleia championii Chaloner, W.G., Scott, A.C., and Stephenson. J., 1991. Fossil (Hamamelidaceae) in Subtropical China. Biotropica, 42(3): evidence for plant-arthropod interactions in the Palaeozoic 336–341. and Mesozoic. Philosophical Transactions of the Royal He Yuli, Li Na, Wang Zixi, Wang Haofei, Yang Guolin, Xiao Society London B, 333(1267): 177–186. Liang, Wu Jingyu and Sun Bainian, 2014. Quercus Chang, H.T., 1973. A revision of the hamamelidaceous flora of yangyiensis sp. nov. from the Late Pliocene of Baoshan, China. Sunyatsenia 1: 54–71 (in Chinese). Yunnan and its paleoclimate significance. Acta Geologica Coley, P.D., and Aide, T.M., 1991. Comparison of herbivory and Sinica (English Edition), 88(3): 738–747. plant defenses in temperate and tropical broad-leaved forests. Huston, M.A., 1994. Biological diversity: the coexistence of In: Price, P.W., Lewinsohn, T.M., Fernandes, G.W., and species on changing landscapes. Cambridge University Press, Benson, W.W. (eds.), Plant-animal interactions: evolutionary Oct. 2015 ACTA GEOLOGICA SINICA (English Edition) Vol. 89 No. 5 1451 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

Cambridge, 681. Tanaka, N., Sakio, H., and Qiu Yingxiong, 2012. Molecular Jones, C.G., Hoggard, M.P., and Blum, M.S., 1981. Pattern and data and ecological niche modelling reveal a highly dynamic process in insect feeding behaviour: a quantitative analysis of evolutionary history of the East Asian Tertiary relict the Mexican bean beetle, Epilachna varivestis. Entomologia Cercidiphyllum (Cercidiphyllaceae). New Phytologist, 196(2): Experimentalis et Applicata, 30(3): 254–264. 617–630. Knobloch, E., and Mai D.H., 1986. Monographie der Früchte Qin Junde and Wang Chenzhu, 2001. The relation of interaction und Samen in der Kreide von Mitteleuropa. Rozpravy between insects and plants to evolution. Acta Entomologica Ústředního Ústavu Geologickénho, 47: 1–219. Sinica, 44(3): 360–365 (in Chinese with English abstract). Labandeira, C.C., 2006. The Four Phases of Plant–Arthropod Royer, D., Sack, L., Wilf, P., Lusk, C.H., Jordan, G.J., Niinemets, Associations in Deep Time. Geologica Acta, 4(4): 409–438. Ü., Wright, I.J., Westoby, M., Cariglino, B., Coley, P.D., Labandeira, C.C., Wilf, P., Johnson, K.R., and Marsh, F., 2007. Cutter, A.D., Johnson, K.R., Labandeira, C.C., Moles, A.T., Guide to insect (and other) damage types on compressed plant Palmer, M.B., and Valladares, F., 2007. Fossil leaf economics fossils, Version 3.0. Smithsonian Institution, Washington D.C, quantified: calibration, Eocene case study, and implications. 25. Paleobiology, 33(4): 574–589. Lei Guangchun and Hanski, I., 1997. Metapopulation structure of Shang Yinglian, 2003. Tengchong diatomite deposit and its Cotesia melitaearum, a specialist parasitoid of the butterfly genesis. Yunnan Geology, 22(4): 418–425 (in Chinese with Melitaea cinxia. Oikos, 78(1): 91–100. English Abstract). Li Feng and Xue Chuandong, 1999. Geodynamic setting since Shi Yuruo, Wu Zhonghai, Fan Taoyuan, Tong Yabo and Yang the Cenozoic and its environmental effects in Northwest Zhengyu, 2012. SHRIMP zircon U-Pb dating and Yunnan, China. Geotectonica et Metallogenia, 23 (2): 115– geochemical analysis of the Pliocene volcanic rocks from 122 (in Chinese with English Abstract). Longchuanjiang valley, Tengchong area, western Yunnan Li Haomin, and Hickey, L.J., 1988. Leaf architecture and Province. Geological Bulletin of China, 31(2–3): 241–249 (in systematics of the Hamamelidaceae sensu lato. Acta Chinese with English Abstract). Phytotaxonomica Sinica, 26(2): 96–110 (in Chinese with Simon, M., and Hilker, M., 2005. Does rust infection of willow English Abstract). affect feeding and oviposition behavior of willow leaf beetles? Li Xikang, Tan Xiaohong, Gao Ziying and Yao Jinchang, 2004. Journal of Insect Behavior, 18(1): 115–129. The geological period and sedimentation environment Suddee, S., and Middleton, D.J., 2003. Rhodoleia Mangbang Formation in Tengchong area, Yunnan. Yunnan (Hamamelidaceae), a new generic record for Thailand. Thai Geology, 23 (2): 241–251 (in Chinese with English abstract). Forest Bulletin, 31: 132–135. Mai, D.H., 1968. Zwei ausgestorbene Gattungen im Tertiär Sun Zexuan, Yao Yifeng, Chen Yong and Li Guoxin, 2004. Europas und ihre florengeschichtliche Bedeutung. Analysis on sequence stratigraphy and depositional systems of Palaeontographica B, 123(1–6): 184–199. Mangbang Formation, Upper Tertiary in Longchuanjiang Mai, D.H., 1987. Neue Früchte und Samen aus paläozänen Basin. Uranium Geology, 20(5): 286–298 (in Chinese with ablagerungen Mitteleuropas. Feddes Repertorium, 98(3–4): English abstract). 197–229. Sun Bainian, Ding Suting, Wu Jingyu, Dong Chong, Xie Mai, D.H., 2001. The fossils of Rhodoleia Champion Sanping and Lin Zhicheng, 2012. Carbon isotope and stomatal (Hamamelidaceae) in Europe. Acta Palaeobotanica, 41(2): data of Late Pliocene Betulaceous leaves from SW China: 161–175. Implications for palaeoatmospheric CO2–levels. Turkish Mai, D.H., and Walther, H., 1985. Die obereozänen Floren des Journal of Earth Sciences, 21: 237–250. Weisselsterbeckens und seiner Randgebiete. Abhandlungen Sun Bainian, Wu Jingyu, Liu Yusheng, Ding Suting, Li des Staatlichen Museums für Mineralogie und Geologie zu Xiangchuang, Xie Sanping, Yan Deifei and Lin Zhicheng, Dresden, 33: 1–260. 2011. Reconstructing Neogene vegetation and climates to Na Yuling, Sun Chunlin, Li Tao and Li Yunfeng, 2014. The infer tectonic uplift in western Yunnan, China. insect oviposition firstly discovered on the Middle Jurassic Palaeogeography, Palaeoclimatology, Palaeoecology, 304(3– Ginkgoales leaf from Inner Mongolia, China. Acta Geologica 4): 328–336. Sinica (English Edition), 88(1): 18–28. Tao Junrong and Du Naiqiu, 1982. Neogene flora of Tengchong NMBC (National Meteorological Bureau of China), 1983. Basin in western Yunnan, China. Acta Botanica Sinica Climate database of China (1951–1980), vol. 1–5. (Journal of Integrative Plant Biology), 24(3): 273–281 (in Meteorology Press, Beijing, China (in Chinese). Chinese with English Abstract). Pan Kaiyu, Lu Anmin and Wen Jie, 1990. Characters of leaf Vink, W., 1957. Hamamelidaceae. In: van Steenis, C.G.G.J. epidermis in Hamamelidaceae (s.l.). Acta Phytotaxonomica (ed.), Flora Malesiana, Ser. 1, No. 5. Noordhoff, Groningen, Sinica, 28(1): 10–26 (in Chinese with English Abstract). Netherlands, 363–379. Pennings, S.C., and Silliman, B.R., 2005. Linking biogeography Wang Yuguo, Li Guangzhao, Zhang Wenju, You Jia and Chen and community ecology: latitudinal variation in plant– Jiakuan, 2007. Leaf epidermal features of Rhododendron herbivore interaction strength. Ecology, 86(9): 2310–2319. (Ericaceae) from China and their systematic significance. Acta Prevec, R., Labandeira, C.C., Neveling, J., Gastaldo, R.A., Looy, Phytotaxonomica Sinica, 45(1): 1–20 (in Chinese with English C.V., and Bamford, M., 2009. Portrait of a Gondwanan abstract). ecosystem: a new late Permian fossil locality from KwaZulu- Wilf, P., 2008. Insect-damaged fossil leaves record food web Natal, South Africa. Review of Palaeobotany and Palynology, response to ancient climate change and extinction. New 156(3–4): 454–493. Phytologist, 178(3): 486–502. Qi Xinshuai, Chen Chen, Comes, H.P., Sakaguchi, S., Liu Yihui, Wilf, P., and Labanderia, C.C., 1999. Response of plant-insect 1452 Vol. 89 No. 5 ACTA GEOLOGICA SINICA (English Edition) Oct. 2015 http://www.geojournals.cn/dzxben/ch/index.aspx http://mc.manuscriptcentral.com/ags

associations to Paleocene-Eocene warming. Science, 284 Palynology, 155(1–2): 32–41. (5423): 2153–2156. Xie Sanping, Sun Bainian, Wu Jingyu, Lin Zhicheng, Yan Deifei Wilf, P., Johnson, K.R., and Huber, B.T., 2003. Correlated and Xiao Liang, 2012. Palaeoclimatic estimates for the Late terrestrial and marine evidence for global climate changes Pliocene based on leaf physiognomy from Western Yunnan, before mass extinction at the Cretaceous-Paleogene boundary. China. Turkish Journal of Earth Sciences, 21: 251–261. Proceedings of the National Academy of Sciences of the Xu Jingxian, Ferguson, D.K., Li Chensen, Wang Yufei and Du United States of America, 100(2): 599–604. Naiqiu, 2004. Climatic and ecological implications of Late Wilf, P., Labandeira, C.C., Johnson, K.R., and Cúneo N.R., Pliocene palynoflora from Longling, Yunnan, China. 2005. Richness of plant-insect associations in Eocene Quaternary International, 117(1): 91–103. Patagonia: a legacy for South American biodiversity. Zhang Zhiyun and Lu Anming, 1995. Hamamelidaceae: Proceedings of the National Academy of Sciences of the geographic distribution, fossil history and origin. Acta United States of America, 102(25): 8944–8948. Phytotaxon Sinica, 33(4): 313–339 (in Chinese with English Wilf, P., Labandeira, C.C., Johnson, K.R., Coley, P.D., and Abstract). Cutter, A.D., 2001. Insect herbivory, plant defense, and early Zhang Zhiyun, Zhang Hongda, and Endress, P.K., 2003. Cenozoic climate change. Proceedings of the National Hamamelidaceae. In: Wu, Z.Y., Raven, P.H., Hong, D.Y. Academy of Sciences of the United States of America, 98(11): (Eds.), Flora of China, vol. 9. Science Press, Beijing, China & 6221–6226. Missouri Botanical Garden Press, St. Louis, USA, 18–42. Wilkinson, H.P., 1979. The plant surface (mainly leaf). In: Zhu Baozhu, Xie Jinlian, Zhang Fangqiu, Pan Wen, Xu Bin, Metcalfe, C.R., and Chalk, L. (eds.), Anatomy of the Wang Yuxia and Wu Yourong, 2010. Studies on Dicotyledons (2nd edition), vol. I. Clarendon Press, Oxford, morphological structure and flower stage of Rhodoleia plants UK, 97–165. in Guangdong. Journal of South China Agricultural Wu Jingyu, 2009. The Pliocene Tuantian flora of Tengchong, University, 31(3): 16–18 (in Chinese with English Abstract). Yunnan Province and its paleoenvironmental analysis. Lanzhou University, Lanzhou, China (Ph. D. thesis), 119 (in About the first author Chinese with English abstract). WU Jingyu, male; born in 1980 in Shangqiu City, Henan Wu Jingyu, Sun Bainian, Liu Yusheng, Xie Sanping and Lin Province; Doctor; associate professor of Lanzhou University; Zhicheng, 2009. A new species of Exbucklandia He is now interested in the study on paleobotany and (Hamamelidaceae) from the Pliocene of China and its paleoclimate in the Cenozoic. paleoclimatic significance. Review of Palaeobotany and Email: [email protected]; phone: 13893699248.

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