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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 The genus Rhodoleia Champion ex Hooker is one of 31 genera in the family Hamamelidaceae. The genus comprises 7 species (Exell, 1933) or 9 species (Chang, 1973) of evergreen trees or shrubs distributed in South China, Vietnam, Thailand, Myanmar, Malaysia, Sumatra, and Indonesia (Zhang et al., 2003). The fossil fruits and seeds of several species of Rhodoleia are known in Europe from the Upper Cretaceous to the Miocene (Mai and Walther, 1985; Knobloch and Mai, 1986; Mai, 1987, 2001). However, no any fossil record of Rhodoleia has been documented in Asia, and no fossil leaves, wood or pollen have thus far been found elsewhere in the world
(Mai, 2001). Within the family Hamamelidaceae, leaf architecture and anatomical characteristics are helpful for generic classification (Li and Hickey, 1988; Fang, 1990; Pan et al., 1990). In this study, based on a detailed comparison of leaf architecture and cuticular features, 21 fossil leaves from the Upper Pliocene in Yunnan Province are identified as Rhodoleia tengchongensis sp. nov. The discovery of this new species from Southwest China, as the only leaf record of Rhodoleia to date, not only provides a valuable opportunity for revealing the leaf architecture and cuticular differences between Pliocene fossils and extant species but also improves our 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
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Pliocene climate of Southwest China. Plant-insect interactions have dominated terrestrial ecosystems for over 420 million years (Labandeira, 2006; Wilf, 2008; Na et al., 2014). The remains of insect feedings on fossil plants have been widely investigated throughout the Phanerozoic (e.g., Chaloner et al., 1991; Banerji, 2004; Wilf et al., 2005; Prevec et al., 2009), and it is generally accepted that insect damage on fossil leaves can provide abundant information regarding terrestrial food webs (Wilf and Labandeira, 1999; Labandeira, 2006; Carvalho et al., 2014; Donovan et al., 2014). In the present paper, the insect damage type and frequency are compared between Rhodoleia fossil and extant leaves, and the specialist herbivores for this genus are discussed.
2 Geological Setting The fossil leaves were collected from an open-cast diatomite mine ca. 1 km west of Tuantian Town (24° 41′ N, 98° 38′ E; Fig. 1a), Tengchong County, Yunnan Province, Southwest China. The fossil-bearing diatomites belong to the Upper Pliocene Mangbang Formation (Fig. 1b) which is subdivided into three lithologic units (Ge and Li, 1999; Shang, 2003; Li et al., 2004; Sun et al., 2004). Based on SHRIMP zircon U-Pb dating of volcanic rocks
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(Shi et al., 2012) and deposition rate (Li and Xue, 1999; Sun et al., 2012), the fossil-bearing deposits studied are undoubtedly of the Late Pliocene (3.3–2.8 Ma).
3 Material and Methods The extant leaves for comparison were collected from Kunming and Pingbian of Yunnan Province, Guangzhou of Guangdong Province, and Haikou of Hainan Province. To study the leaf architecture, the extant leaves were cleared with a 10% solution of NaOH. The experimental treatments used for the fossil and extant cuticles are well described in previous studies (Dao et al., 2013; He et al., 2014). The fossil cuticles were embedded in paraffin and cut using a Leica RM2255 microtome. The terminology for leaf architecture follows Manual of Leaf Architecture (Ellis et al., 2009), and the foliar cuticle terminology is that of Dilcher (1974) and Wilkinson (1979). The insect damage types are according to Labandeira et al. (2007). The estimation of the leaf dry mass per area (MA) for the fossil leaves is according to the formula of Royer et al. (2007): lg[MA] =3.070+0.382×lg[PW2/A], where MA is the leaf dry mass per area (g m–2), PW is the petiole width (mm), and A is the leaf area (mm2). 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).
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stored at the Institute of Palaeontology and Stratigraphy, Lanzhou University, Gansu Province, China.
4 Systematics and Comparison 4.1 Systematics Order Hamamelidales Griseb. Family Hamamelidaceae R. Brown Genus Rhodoleia Champion ex Hooker Rhodoleia tengchongensis J.Y. Wu et B.N. Sun sp. nov. Holotype: FTP–553A (Fig. 2e; Fig. 4c) Paratypes: FTP–010A (Fig. 2a, j, k; Fig. 4e, g), FTP– 010B (Fig. 2b), FTP–315–6 (Fig. 2c), FTP–309–6 (Fig. 2i; Fig. 3c, d; Fig. 4f, h, k, l), FTP–281 (Fig. 2f; Fig. 3b), FTP –323–1 (Fig. 2d; Fig. a; Fig. 4a, b, i), FTP–14009 (Fig. 2g), FTP–14065 (Fig. 2h). Other specimens: FTP–553B, FTP–14016, FTP– 14034, FTP–091, FTP–317–23, FTP–232, FTP–310, FTP –307–5, FTP–543, FTP–225–21, FTP–504, FTP–135, FTP–304–27, FTP–226–16. Type locality: Tuantian Town (N 24° 41′, E 98° 38′), Tengchong County, Yunnan Province, China (Fig. 1A). Stratigraphy: diatomite beds, Upper Mangbang Formation. Age: Piacenzian, Late Pliocene. Etymology: The name refers to the type locality, Tengchong County. Diagnosis: Blade attachment marginal, lamina size microphyll to notophyll; lamina shape elliptic with medial symmetry and basal symmetry, margin entire. Primary venation pinnate, obscurely three basal veins, major secondary veins simple brochidodromous; intersecondaries occur at less than one per intercostal area, intercostal tertiary veins mixed percurrent, exterior tertiaries looped. Adaxial and abaxial epidermal cells pentagonal or hexagonal; anticlinal walls straight and honeycombed. Leaves hypostomatic, stoma paracytic and randomly orientated. Trichomes occur on adaxial and abaxial epidermis, stellate and multicellular. Description: Blade attachment marginal, lamina size microphyll to notophyll, 5.6–10.5 cm long and 2.6–5.5 cm wide, L:W ratio 2.2:1 to 1.7:1, lamina shape variable, usually elliptic with medial symmetry and basal symmetry. Petiole 1.0–2.0 cm long and 1.0–1.6 mm wide (Fig. 2e–g). Margin entire with acute apex angle, acuminate apex shape, acute to obtuse base angle, and straight to convex base shape (Fig. 2a–i). Primary venation pinnate with no naked basal veins, obscurely three basal veins, and no agrophic veins. Major secondary veins 7–9 pairs, simple brochidodromous with irregular spacing, uniform secondary angle to midvein (55–65º),
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and decurrent attachment to midvein. Interior and minor secondaries absent. Intersecondaries span more than 50% of the length of the subjacent secondary, occuring at less than one per intercostal area; proximal course is parallel to major secondaries, and distal course perpendicular to a subjacent major secondary (Fig. 2a–i). Intercostal tertiary veins mixed percurrent with obtuse angle to midvein and inconsistent vein angle variability (Fig. 2j, k). Exterior tertiaries looped (Fig. 2j). Quaternary vein fabric irregular reticulate. Areolation shows moderate development. Freely ending veinlets mostly with two or more branches (Fig. 2j, k). Marginal ultimate venation looped (Fig. 2j). Leaves hypostomatic: Adaxial epidermis ca. 9 μm thick; cells isodiametric, pentagonal or hexagonal, and 11– 25 μm long and 9–18 μm wide; anticlinal cell walls straight and developing into a honeycomb, periclinal walls smooth (Fig. 3a, c; Fig. 4a). Abaxial epidermis ca. 8 μm thick; cells isodiametric, pentagonal or hexagonal, 12–27 μm long and 8–20 μm wide, and each cell covered by a papilla on the outer wall (Fig. 4b-d); anticlinal walls straight and honeycombed (Fig. 4a). Stomatal apparatus paracytic, randomly orientated and slightly sunk (Fig. 4g– i). Trichomes occur on both adaxial and abaxial epidermis, multicellular and stellate, the trichome base ca. 20 μm across (Fig. 3a; Fig. 4e, f). 4.2 Comparison All fossil leaves in the present study share the same leaf architectural characters, such as an elliptic laminar shape, a leathery texture, an entire margin, pinnate venation, obscure 3 basal veins, and simple brochidodromous major secondary veins, demonstrating the closest relationship to genus Rhodoleia of Hamamelidaceae (Li and Hickey, 1988; Zhang et al., 2003). However, the leaves of Rhodoleia are usually confused with those of Rhododendron (Ericaceae) and Distylium (Hamamelidaceae) with regard to morphology (Zhang et al., 2003). Fortunately, the cuticular characteristics warrant their separation, as the leaves of Rhodoleia possess paracytic stomata and multicellular trichomes; in contrast, Rhododendron leaves have anomocytic stomata and unicellular trichomes (Wang et al., 2007), and Distylium leaves usually have undulated cell walls and no trichomes (Pan et al., 1990). Exell (1933) recognized seven species in Rhodoleia, but Vink (1957) reduced them to one species and considered that the variations of this genus are within a polymorphous species: Rhodoleia championii. Chang (1973) argued that there are nine species in Rhodoleia, with six species being endemic to China based on differences in leaf veins, fruits and flowers. To provide a detailed comparison of leaf architecture and cuticular characteristics between fossil
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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.
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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 described by Chang (1973) were selected for the comparison with the Tengchong fossils. The fossil cuticle displays such characteristics as pentagonal or hexagonal cells, stellate trichomes, paracytic stomata, and papillae present on epidermal cells. All these
characteristics are closely comparable with those of extant Rhodoleia (Table 1; Fig. 5a–l). However, minor differences can also be found between the fossils and most of the extant species. For example, Rh. parvipetala has four regular papillae at two ends of the guard cells on the inner surface (Fig. 5i), and Rh. macrocarpa displays more
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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 apparatus 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 (Fig. 5g). Rhodoleia forrestii and Rh. stenopetala have cuticular features similar to those of the fossil leaves, but these two species exhibit reduced angles between the secondary veins and the midrib (Table 1). Regarding leaf architectures, the present fossil leaves most resemble
extant Rh. championii and Rh. henryi. However, these two species have ruglike periclinal walls that differ from those of the present fossil leaves. As no other fossil leaf has ever been reported, a further comparison is limited. The comparisons above suggest that no extant species has leaf architectural and cuticular characters concordant with our
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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.
5 Discussions 5.1 Phytogeography and paleoclimate
Fossil records of Rhodoleia are well known in Europe from the Upper Cretaceous to the Miocene. For example, the earliest fossil seed of Rh. cretacea was reported from the Upper Cretaceous of South Oebisfelde in Germany (Knobloch and Mai, 1986), followed by a Late Paleocene
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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 (1985) described some fruits and seeds of Rh. bellmannii from the Upper Eocene of White Elster Basin in Germany. Fossil seeds and fruits of Rh. bifollicularis were obtained from the Middle Miocene in Herzogenrath (West German)
and the Lower Miocene in Osieczów (West Poland), which proves the continued presence of this genus during the Miocene in Europe (Mai, 1968, 2001). In Asia, where modern Rhodoleia species occur, Rh. tengchongensis described herein is the only confirmed fossil record of this
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Table 1 Leaf architecture of the present fossil and extant Rhodoleia (after Zhang et al., 2003) Taxon
Shape
Rh. tengchongensis
elliptic
Rh. championii
ovate to elliptic
Width (cm)
Apex angle
Apex shape
Base angle
Base shape
Pairs of major secondaries
Major secondary vein framework
Secondary angle to midvein
Petiole length (cm)
5.6–10.5 2.6–5.5
acute
acuminate
acute to obtuse
straight to convex
7–9
simple brochidodromous
55–65º
1–2
acute
acuminate
acute to obtuse
convex
7–9
simple brochidodromous
ca. 60º
3–5.5
6–9
simple brochidodromous
45–65º
ca. 5
ca. 45º
ca. 3.5
ca. 75º
2.5–4
55–75º
2–4.5
30–50º
3–5
Length (cm)
7–16
4.5–10.5
Rh. henryi
ovate to elliptic
ca. 11
3–6
acute
acuminate
acute
straight to convex
Rh. forrestii
oblong to lanceolate
7–15
2–7
acute
acuminate
acute
convex
7–9
Rh. macrocarpa
elliptic
7–11
3–6
acute
acuminate
acute
convex
8 or 9
Rh. parvipetala
oblong
5–10
2–4.5
acute
acuminate
acute
convex
6–9
4–6.5
acute to obtuse
acute to convex
obtuse
convex
4–6
Rh. stenopetala
ovate
6–10
genus. In addition, the phylogenetic estimation indicate that the divergence time of Rhodoleia was from the Late Cretaceous to the Early Eocene (Qi et al., 2012), which is roughly equivalent to the early occurrence age in Europe. Therefore, the distribution of previous fossil records might suggest that the genus Rhodoleia originated from central Europe, and migrating from Europe to Asia prior to the Late Pliocene. However, due to the inadequate paleobotanical data in East Asia, the origin and divergence pattern of Rhodoleia still need a further research. Extant Rhodoleia trees are distributed in Indonesia, Malaysia, Myanmar, Vietnam, Thailand and South China, ranging from 7º S to 27º N (Zhang and Lu, 1995; Suddee and Middleton, 2003; Zhang et al., 2003). According to the geographic range of Rhodoleia, its climatic requirements appear to be 15–27° C mean annual temperatures (MAT) and 1000–2500 mm mean annual precipitations (MAP) (NMBC, 1983). Hence, the present fossils might also have lived under similar climatic conditions during the Late Pliocene. Indeed, based on both quantitative and qualitative analyses, a Pliocene climate reconstruction for Tengchong flora predicts warm and humid conditions (Tao and Du, 1982; Xu et al., 2004; Wu et al., 2009; Sun et al., 2011; Xie et al., 2012), which is quite consistent with the climate requirements of the genus Rhodoleia. 5.2 Insect herbivory In the past, many paleobiologists (e.g., Huston, 1994; Wilf and Labandeira, 1999; Wilf et al., 2003; Currano et al., 2008; Adams et al., 2010) focused on the diversity of insect leaf feeding in different climate intervals, correlating the insect-feeding diversity with paleolatitude and paleotemperature. On the basis of a more abundant and stable fixed energy supply in low-latitude warm and moist ecosystems, some biologists considered the rate of
simple brochidodromous simple brochidodromous simple brochidodromous simple brochidodromous
leaf area loss to herbivory to be greater in warmer than in cooler environments (Coley and Aide, 1991; Coley and Barone, 1996; Pennings and Silliman, 2005; Adams et al., 2010). According to observations of insect damage frequency on fossil leaves from the Early Cenozoic of the Central United States, Wilf (2008) indicated that the insect -feeding diversity and frequency increase in variability with decreased rainfall. Wu (2009) and Sun et al. (2011) had described 28 genera within 20 families of angiospermous leaves from the Upper Pliocene of Tengchong flora. We examined these fossil leaves, and found that among a total of 836 fossil leaves, only 97 specimens show insect damages. In contrast with the Early Cenozoic floras of the United States (e.g., Wilf and Labandeira, 1999; Wilf et al., 2001; Currano et al., 2008), the Pliocene Tengchong flora exhibits a remarkably lower percentage of insect damages. Based on Climate Leaf Analysis Multivariate Program, Tengchong during the Pliocene experienced a growing season precipitation (GSP) of 1834.3–1901.2 mm (Xie et al., 2012). Therefore, the insect damage frequency of the Tengchong flora might have been restricted by the plentiful rainfall. The Late Pliocene Tuantian flora consists mainly of Lauraceae, Fagaceae, Betulaceae, Hamamelidaceae, Leguminosae, Myricaceae, Ulmaceae and Juglandaceae (Sun et al., 2011). We observed these fossil leaves, and Table 2 lists 11 genera (≥20 specimens) frequently showing insect damages. Royer et al. (2007) established a method to determine the leaf mass per area (MA) for fossils and indicated that insect herbivory tends to decrease as MA increases. The MA values for our fossil leaves are also negatively correlated with the frequency of insect herbivory (Fig. 7). However, the present fossil leaves of Rhodoleia and Exbucklandia exhibit a much higher percentage of insect damage than that in other taxa. For example, in the present 21 specimens of Rhodoleia, 13
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Table 2 Percentage of leaves with insect damage and estimated leaf dry mass per area (MA) in the late Pliocene Tengchong flora Family Hamamelidaceae Hamamelidaceae Juglandaceae Lauraceae Lauraceae Lauraceae Betulaceae Betulaceae Fagaceae Fagaceae Fagaceae
Genus Rhodoleia Exbucklandia Juglans Machilus Cinnamomum Lindera Betula Carpinus Castanopsis Cyclobalanopsis Castanea
Specimen number 21 30 38 29 31 54 52 46 26 20 24
Fig. 7. Correlation between the percentage of leaves with insect damage and estimated leaf dry mass per area (MA) for the Pliocene Tengchong flora. Each data point represents a taxon mean, which ≥20 specimens are plotted.
leaves (61.9% ) were damaged by insects, including damage types of hole feeding, margin feeding, surface feeding and galling (Fig. 6a–n). For comparison, we examined herbarium sheets from the Chinese Virtual Herbarium (CVH, http://www.cvh.org.cn/); of 584 observed extant leaves of Rh. championii, 338 leaves (57.9 %) exhibit damages by insects. Moreover, a similar high damage frequency can also be discovered in other Rhodoleia species. Thus, insect herbivory of the Pliocene Tengchong flora appears to exhibit a prominent selectivity between insects and some plant groups, such as Rhodoleia and Exbucklandia. The high frequency of damage by insects in Rhodoleia might correlate with the attraction of bird visitors. Rhodoleia bears bisexual flowers in tight heads and produces lipid-rich pollen grains and dilute nectar, with a flowering stage from the late winter to spring of the next year (Zhang et al., 2003; Zhu et al., 2010). Bird pollination in Rhodoleia has been documented by Doctors van Leeuwen (1927) and Corlett (2001), and Gu et al. (2010) indicated that relative shortages of fruits and seeds during winter months can force birds that normally forage on
Leaves with insect damage (%) 61.9 46.7 28.9 13.8 9.7 7.4 9.6 13.0 15.4 20.0 25.0
MA (g m–2) 86.8±4.8 112.5±5.4 73.0±6.2 116.7±6.4 128.4±8.1 131.5±8.6 102.6±7.4 110.6±6.8 99.5±5.9 79.8±4.4 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 plantinsect 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 using vision, olfaction and chemical receptors, many insects become specialist herbivores during the process of insect-plant coevolution (Lei and Hanski, 1997; Qin and Wang, 2001; Gripenberg et al., 2008). Based on the observations of insect feeding in present fossils and extant Rhodoleia, we can conclude that this genus is suitable for insect feeding and that the specific feeding behavior of insects on Rhodoleia, as well as insects and birds, might have been established as early as the Late Pliocene.
6 Conclusions The main outcomes of this study are as follows. (1) Based on the comparison of leaf architectural and cuticular characteristics with those of extant leaves, we identify a new species as Rhodoleia tengchongensis sp. nov. from the Upper Pliocene in West Yunnan. The present fossil species is the first record of Rhodoleia in East Asia, where modern species occur, and also a unique record of leaf remains documented worldwide. (2) The modern distribution of Rhodoleia suggests that the genus lives in a warm climate, with an MAT from 15 °C to 27 °C and an MAP from 1000 mm to 2500 mm. Hence, Rh. tengchongensis might also have lived under similar climatic conditions, that is, a warm and humid climate, in West Yunnan during the Late Pliocene. The fossil records
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also suggest that Rhodoleia might originate from central Europe, and then migrating to Asia prior to the Late Pliocene. (3) The Pliocene Tengchong flora shows a remarkably lower percentage of insect damage, which might have been restricted by the plentiful rainfall. However, Rhodoleia leaves exhibit a high percentage of insect damages, which indicates that this genus is suitable for insect feeding, and that the specific feeding behavior of insects on Rhodoleia was established as early as the Late Pliocene. Moreover, seasonal food shortages can force birds that normally forage on insects as a supplementary energy source. Therefore, the present fossil leaves may provide a striking glimpse of the coevolution of insect herbivory, the feeding habits of birds, and pollination interactions.
Acknowledgements This work is granted by the National Natural Science Foundation of China (Nos. 41302009, 41402008, 41172022 and 41172021), the Foundation of the State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, CAS (No. 133102), and the NSF EAR-0746105 to YSL. Manuscript received Apr. 18, 2014 accepted Nov. 22, 2014 edited by Fei Hongcai References Adams, J.M., Brusa, A., Soyeong, A., and Ainuddin, A.N., 2010. Present-day testing of a paleoecological pattern: is there really a latitudinal difference in leaf-feeding insect-damage diversity? Review of Palaeobotany and Palynology, 162(1): 63–70. Ameixa, O., Almeida, L., Gonçalves, A., and Neto, L., 2007. Feeding behavior of Liriomyza huidobrensis (Blanchard) and L. trifolii (Burgess) adults on bean leaves. Journal of Insect Behavior, 20(1): 137–155. Banerji, J., 2004. Evidence of insect-plant interactions from the Upper Gondwana Sequence (Lower Cretaceous) in the Rajmahal Basin, India. Gondwana Research, 7(1): 205–210. Carvalho, M.R., Wilf, P., Barrios, H., Currano, E.D., Windsor, D.M., Jaramillo, C.A., and Labandeira, C.C., 2014. Insect leaf -chewing damage tracks herbivore richness in modern and ancient forests. PloS One, 9: e94950. Chaloner, W.G., Scott, A.C., and Stephenson. J., 1991. Fossil evidence for plant-arthropod interactions in the Palaeozoic and Mesozoic. Philosophical Transactions of the Royal Society London B, 333(1267): 177–186. Chang, H.T., 1973. A revision of the hamamelidaceous flora of China. Sunyatsenia 1: 54–71 (in Chinese). Coley, P.D., and Aide, T.M., 1991. Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Price, P.W., Lewinsohn, T.M., Fernandes, G.W., and Benson, W.W. (eds.), Plant-animal interactions: evolutionary
http://mc.manuscriptcentral.com/ags
Oct. 2015
ecology in tropical and temperate regions. John Wiley and Sons, New York, 25–49. Coley, P.D., and Barone, J.A., 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics, 27: 305–335. Corlett, R.T., 2001. Pollination in a degraded tropical landscape: a Hong Kong case study. Journal of Tropical Ecology, 17(1): 155–161. Currano, E.D., Wilf, P., Wing, S.L., Labandeira, C.C., Lovelock, E.C., and Royer, D.L., 2008. Sharply increased insect herbivory during the Paleocene-Eocene Thermal Maximum. Proceedings of the National Academy of Sciences of the United States of America, 105(6): 1960–1964. Dao Kequn, Chen junlin, Jin Peihong, Dong Chong, Yang Yi, Xu Xiaohui, Wu Jingyu, Xie Sanping, Lin Zhicheng and Sun Bainian, 2013. A new material of Lindera (Lauraceae) of the late Pliocene from Tengchong, Yunnan and the genus’ biogeography significance. Acta Geologica Sinica (English Edition), 87(3): 690–706. David, J.P., Ferran, A., Gambier, J., and Meyran, J.C., 2002. Taste sensitivity of detritivorous mosquito larvae to decomposed leaf litter. Journal of Chemical Ecology, 28(5): 983–995. Dilcher, D.L., 1974. Approaches to the identification of angiosperm leaf remains. The Botanical Review, 40(1): 1–157. Doctors van Leeuwen, W.M., 1927. Vogelbloemen. 3. Rhodoleia teysmanni Miq. Trop. Nature, 16: 2–6. Donovan, M., Wilf, P., Labandeira, C.C., Johnson, K.R., and Peppe, D.J., 2014. Novel insect leaf-mining after the endCretaceous extinction and the demise of Cretaceous leaf miners, Great Plains, USA. PloS One, 9: e103542. Ellis, B., Daly, D.C., Hickey, L.J., Johnson, K.R., Mitchell, J.D., 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. Sunyatsenia, 1: 95–102. Fang Yanming, 1990. A study on leaf micromorphology of Chinese Hamamelidaceae – stomatal apparatus. Journal of Nanjing Forestry University, 14(4): 30–35 (in Chinese with English Abstract). Ge Hongru and Li Daiyun, 1999. Cenozoic Coal-bearing Basins and Coalforming Regularity in West Yunnan. Yunnan Science and Technology Press, Kunming, China, 104 (in Chinese). Glinwood, R.T., and Pettersson, J., 2000. Change in response of Rhopalosiphum padi spring migrants to the repellent winter host component methyl salicylate. Entomologia Experimentalis et Applicata, 94(3): 325–330. Gripenberg, S., Ovaskainen, O., Morriën, E., and Roslin, T., 2008. Spatial population structure of a specialist leaf-mining moth. Journal of Animal Ecology, 77(4): 757–767. Gu Lei, Luo Zhonglai, Zhang Dianxiang and Renner, S.S., 2010. Passerine Pollination of Rhodoleia championii (Hamamelidaceae) in Subtropical China. Biotropica, 42(3): 336–341. He Yuli, Li Na, Wang Zixi, Wang Haofei, Yang Guolin, Xiao Liang, Wu Jingyu and Sun Bainian, 2014. Quercus yangyiensis sp. nov. from the Late Pliocene of Baoshan, Yunnan and its paleoclimate significance. Acta Geologica Sinica (English Edition), 88(3): 738–747. Huston, M.A., 1994. Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press,
Oct. 2015
ACTA GEOLOGICA SINICA (English Edition) http://www.geojournals.cn/dzxben/ch/index.aspx
Cambridge, 681. Jones, C.G., Hoggard, M.P., and Blum, M.S., 1981. Pattern and process in insect feeding behaviour: a quantitative analysis of the Mexican bean beetle, Epilachna varivestis. Entomologia Experimentalis et Applicata, 30(3): 254–264. Knobloch, E., and Mai D.H., 1986. Monographie der Früchte und Samen in der Kreide von Mitteleuropa. Rozpravy Ústředního Ústavu Geologickénho, 47: 1–219. Labandeira, C.C., 2006. The Four Phases of Plant–Arthropod Associations in Deep Time. Geologica Acta, 4(4): 409–438. Labandeira, C.C., Wilf, P., Johnson, K.R., and Marsh, F., 2007. Guide to insect (and other) damage types on compressed plant fossils, Version 3.0. Smithsonian Institution, Washington D.C, 25. Lei Guangchun and Hanski, I., 1997. Metapopulation structure of Cotesia melitaearum, a specialist parasitoid of the butterfly Melitaea cinxia. Oikos, 78(1): 91–100. Li Feng and Xue Chuandong, 1999. Geodynamic setting since the Cenozoic and its environmental effects in Northwest Yunnan, China. Geotectonica et Metallogenia, 23 (2): 115– 122 (in Chinese with English Abstract). Li Haomin, and Hickey, L.J., 1988. Leaf architecture and systematics of the Hamamelidaceae sensu lato. Acta Phytotaxonomica Sinica, 26(2): 96–110 (in Chinese with English Abstract). Li Xikang, Tan Xiaohong, Gao Ziying and Yao Jinchang, 2004. The geological period and sedimentation environment Mangbang Formation in Tengchong area, Yunnan. Yunnan Geology, 23 (2): 241–251 (in Chinese with English abstract). Mai, D.H., 1968. Zwei ausgestorbene Gattungen im Tertiär Europas und ihre florengeschichtliche Bedeutung. Palaeontographica B, 123(1–6): 184–199. Mai, D.H., 1987. Neue Früchte und Samen aus paläozänen ablagerungen Mitteleuropas. Feddes Repertorium, 98(3–4): 197–229. Mai, D.H., 2001. The fossils of Rhodoleia Champion (Hamamelidaceae) in Europe. Acta Palaeobotanica, 41(2): 161–175. Mai, D.H., and Walther, H., 1985. Die obereozänen Floren des Weisselsterbeckens und seiner Randgebiete. Abhandlungen des Staatlichen Museums für Mineralogie und Geologie zu Dresden, 33: 1–260. Na Yuling, Sun Chunlin, Li Tao and Li Yunfeng, 2014. The insect oviposition firstly discovered on the Middle Jurassic Ginkgoales leaf from Inner Mongolia, China. Acta Geologica Sinica (English Edition), 88(1): 18–28. NMBC (National Meteorological Bureau of China), 1983. Climate database of China (1951–1980), vol. 1–5. Meteorology Press, Beijing, China (in Chinese). Pan Kaiyu, Lu Anmin and Wen Jie, 1990. Characters of leaf epidermis in Hamamelidaceae (s.l.). Acta Phytotaxonomica Sinica, 28(1): 10–26 (in Chinese with English Abstract). Pennings, S.C., and Silliman, B.R., 2005. Linking biogeography and community ecology: latitudinal variation in plant– herbivore interaction strength. Ecology, 86(9): 2310–2319. Prevec, R., Labandeira, C.C., Neveling, J., Gastaldo, R.A., Looy, C.V., and Bamford, M., 2009. Portrait of a Gondwanan ecosystem: a new late Permian fossil locality from KwaZuluNatal, South Africa. Review of Palaeobotany and Palynology, 156(3–4): 454–493. Qi Xinshuai, Chen Chen, Comes, H.P., Sakaguchi, S., Liu Yihui,
http://mc.manuscriptcentral.com/ags
Vol. 89 No. 5
1451
Tanaka, N., Sakio, H., and Qiu Yingxiong, 2012. Molecular data and ecological niche modelling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphyllum (Cercidiphyllaceae). New Phytologist, 196(2): 617–630. Qin Junde and Wang Chenzhu, 2001. The relation of interaction between insects and plants to evolution. Acta Entomologica Sinica, 44(3): 360–365 (in Chinese with English abstract). Royer, D., Sack, L., Wilf, P., Lusk, C.H., Jordan, G.J., Niinemets, Ü., Wright, I.J., Westoby, M., Cariglino, B., Coley, P.D., Cutter, A.D., Johnson, K.R., Labandeira, C.C., Moles, A.T., Palmer, M.B., and Valladares, F., 2007. Fossil leaf economics quantified: calibration, Eocene case study, and implications. Paleobiology, 33(4): 574–589. Shang Yinglian, 2003. Tengchong diatomite deposit and its genesis. Yunnan Geology, 22(4): 418–425 (in Chinese with English Abstract). Shi Yuruo, Wu Zhonghai, Fan Taoyuan, Tong Yabo and Yang Zhengyu, 2012. SHRIMP zircon U-Pb dating and geochemical analysis of the Pliocene volcanic rocks from Longchuanjiang valley, Tengchong area, western Yunnan Province. Geological Bulletin of China, 31(2–3): 241–249 (in Chinese with English Abstract). Simon, M., and Hilker, M., 2005. Does rust infection of willow affect feeding and oviposition behavior of willow leaf beetles? Journal of Insect Behavior, 18(1): 115–129. Suddee, S., and Middleton, D.J., 2003. Rhodoleia (Hamamelidaceae), a new generic record for Thailand. Thai Forest Bulletin, 31: 132–135. Sun Zexuan, Yao Yifeng, Chen Yong and Li Guoxin, 2004. Analysis on sequence stratigraphy and depositional systems of Mangbang Formation, Upper Tertiary in Longchuanjiang Basin. Uranium Geology, 20(5): 286–298 (in Chinese with English abstract). Sun Bainian, Ding Suting, Wu Jingyu, Dong Chong, Xie Sanping and Lin Zhicheng, 2012. Carbon isotope and stomatal data of Late Pliocene Betulaceous leaves from SW China: Implications for palaeoatmospheric CO2–levels. Turkish Journal of Earth Sciences, 21: 237–250. Sun Bainian, Wu Jingyu, Liu Yusheng, Ding Suting, Li Xiangchuang, Xie Sanping, Yan Deifei and Lin Zhicheng, 2011. Reconstructing Neogene vegetation and climates to infer tectonic uplift in western Yunnan, China. Palaeogeography, Palaeoclimatology, Palaeoecology, 304(3– 4): 328–336. Tao Junrong and Du Naiqiu, 1982. Neogene flora of Tengchong Basin in western Yunnan, China. Acta Botanica Sinica (Journal of Integrative Plant Biology), 24(3): 273–281 (in Chinese with English Abstract). Vink, W., 1957. Hamamelidaceae. In: van Steenis, C.G.G.J. (ed.), Flora Malesiana, Ser. 1, No. 5. Noordhoff, Groningen, Netherlands, 363–379. Wang Yuguo, Li Guangzhao, Zhang Wenju, You Jia and Chen Jiakuan, 2007. Leaf epidermal features of Rhododendron (Ericaceae) from China and their systematic significance. Acta Phytotaxonomica Sinica, 45(1): 1–20 (in Chinese with English abstract). Wilf, P., 2008. Insect-damaged fossil leaves record food web response to ancient climate change and extinction. New Phytologist, 178(3): 486–502. Wilf, P., and Labanderia, C.C., 1999. Response of plant-insect
1452
Vol. 89 No. 5
ACTA GEOLOGICA SINICA (English Edition) http://www.geojournals.cn/dzxben/ch/index.aspx
associations to Paleocene-Eocene warming. Science, 284 (5423): 2153–2156. Wilf, P., Johnson, K.R., and Huber, B.T., 2003. Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous-Paleogene boundary. Proceedings of the National Academy of Sciences of the United States of America, 100(2): 599–604. Wilf, P., Labandeira, C.C., Johnson, K.R., and Cúneo N.R., 2005. Richness of plant-insect associations in Eocene Patagonia: a legacy for South American biodiversity. Proceedings of the National Academy of Sciences of the United States of America, 102(25): 8944–8948. Wilf, P., Labandeira, C.C., Johnson, K.R., Coley, P.D., and Cutter, A.D., 2001. Insect herbivory, plant defense, and early Cenozoic climate change. Proceedings of the National Academy of Sciences of the United States of America, 98(11): 6221–6226. Wilkinson, H.P., 1979. The plant surface (mainly leaf). In: Metcalfe, C.R., and Chalk, L. (eds.), Anatomy of the Dicotyledons (2nd edition), vol. I. Clarendon Press, Oxford, UK, 97–165. Wu Jingyu, 2009. The Pliocene Tuantian flora of Tengchong, Yunnan Province and its paleoenvironmental analysis. Lanzhou University, Lanzhou, China (Ph. D. thesis), 119 (in Chinese with English abstract). Wu Jingyu, Sun Bainian, Liu Yusheng, Xie Sanping and Lin Zhicheng, 2009. A new species of Exbucklandia (Hamamelidaceae) from the Pliocene of China and its paleoclimatic significance. Review of Palaeobotany and
http://mc.manuscriptcentral.com/ags
Oct. 2015
Palynology, 155(1–2): 32–41. Xie Sanping, Sun Bainian, Wu Jingyu, Lin Zhicheng, Yan Deifei and Xiao Liang, 2012. Palaeoclimatic estimates for the Late Pliocene based on leaf physiognomy from Western Yunnan, China. Turkish Journal of Earth Sciences, 21: 251–261. Xu Jingxian, Ferguson, D.K., Li Chensen, Wang Yufei and Du Naiqiu, 2004. Climatic and ecological implications of Late Pliocene palynoflora from Longling, Yunnan, China. Quaternary International, 117(1): 91–103. Zhang Zhiyun and Lu Anming, 1995. Hamamelidaceae: geographic distribution, fossil history and origin. Acta Phytotaxon Sinica, 33(4): 313–339 (in Chinese with English Abstract). Zhang Zhiyun, Zhang Hongda, and Endress, P.K., 2003. Hamamelidaceae. In: Wu, Z.Y., Raven, P.H., Hong, D.Y. (Eds.), Flora of China, vol. 9. Science Press, Beijing, China & Missouri Botanical Garden Press, St. Louis, USA, 18–42. Zhu Baozhu, Xie Jinlian, Zhang Fangqiu, Pan Wen, Xu Bin, Wang Yuxia and Wu Yourong, 2010. Studies on morphological structure and flower stage of Rhodoleia plants in Guangdong. Journal of South China Agricultural University, 31(3): 16–18 (in Chinese with English Abstract).
About the first author WU Jingyu, male; born in 1980 in Shangqiu City, Henan Province; Doctor; associate professor of Lanzhou University; He is now interested in the study on paleobotany and paleoclimate in the Cenozoic. Email:
[email protected]; phone: 13893699248.