2.2. Extant materials and morphological observation

Herbarium specimens of extant Itea species used for comparison were accessed from online data sources such as JSTOR Global Plants (http://plants.jstor.org/) and the Chinese Virtual Herbarium (http://www.cvh.org.cn/). Cleared leaf materials of extant species were collected from the Xishuangbanna Tropical Botanical Garden (XTBG). These leaves were cleared following the protocol developed by Li (1987). Several photographs of cleared leaves of extant Itea species were downloaded from the Smithsonian Cleared Leaf Collection, and their contrasts were adjusted using Adobe Photoshop. All fossil and modern specimens were photographed using a digital camera (Nikon D700). Further, the details of the fossils were photographed using a stereomicroscope (Leica S8APO). In addition, line-drawings and plates were created using CorelDRAW X7. Digital photographs of extant and fossil specimens were measured using ImageJ 1.45s software. The leaf architecture terminology followed Ellis et al. (2009).

3.3. Morphological comparison with fossils and extant Itea species

There are 21 accepted modern species in the genus Itea (International Plant Names Index, https://www.ipni.org/) (Table 1). Most of them (19 spp.) are evergreen (SE Asian & African species) and only one species from Japan (Itea japonica Oliv.) and one species from North America (Itea virginica L.) are deciduous. Moreover, Engler, 1890, Engler, 1928 subdivided the extant Itea species into two sections based on their life forms: Sect. Deciduae Engler and Sect. Sempervirentes Engler.

Sect. Deciduae comprised two deciduous species with ovoid seeds (Itea virginica and I. japonica), while Sect. Sempervirentes comprised the evergreen Asian species with fusiform seeds. This division was consistent until African Choristylis rhamnoides Harv. was transferred into Itea (Kubitzki, 2007). Itea rhamnoides (Harv.) Kubitzki has more or less ovoid seeds but is evergreen. These evergreen and deciduous Itea can be distinguished by their leaf architecture. All Sect. Sempervirentes have scalariform tertiary veins and crenate to serrate teeth, which are stable traits associated with plants residing in a moist subtropical habitat (Plate IVa–g). In contrast, Sect. Deciduae tertiary veins are more reticulate (alternate percurrent, more intersecondaries) (Plate IVh, i) and the teeth are usually serrate. However, I. rhamnoides is much more similar to the deciduous I. japonica of Sect. Deciduae in having acute, serrate, sometimes compound teeth. Its evergreen habitat may be due to its climatic conditions. Morphologically, the fossil leaves from Wenshan clearly belong to Sect. Sempervirentes.

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Plate IV

Leaf architecture diversity of extant Itea species. (a)I. oldhamii (NCLC-W-8918); (b)I. nutans (NCLC-W-8920); (c)I. maesaefolia (NCLC-W-8921); (d)I. yunnanensis (NCLC-W-1133b); (e)I. macrophylla (NCLC-W-8919); (f)I. chinensis (NCLC-3199); (g)I. amoena (NCLC-W-8913b); (h)I. japonica (NCLC-W-8917); (i)I. virginica (NCLC-3198). Scale bar = 1 cm. All the leaves are preserved in Paleoecology Collections, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences.

The leaf shapes of Itea are most commonly oblong to elliptical. This is particularly true for subtropical species at its southern China diversity center. Other leaf shapes are relatively rare and exhibit high ecological correlations. For instance, ovate leaves appear in the temperate I. japonica of Sect. Deciduae and its close African sister I. rhamnoides; obolanceolate and lanceolate leaves only appear in Itea riparia Coll. et Hemsl., Itea tenuinervia S. Y. Liu and Itea amoena Chun, which grow on riverside rocks (Table 1; Plate IV).

The leaf size of Itea also varies to a certain degree, and the leaves of tropical species are larger (e.g., Itea indochinensis Merr., Itea kwangsiensis H. T. Chang and Itea macrophylla Wall. ex Roxb.). Subtropical taxa generally have medium-sized leaves that are 5–15 cm long. Leaves of different sizes, particularly smaller ones, often appear on the same plant (Table 1).

The curved eucamptodromous secondary veins, with a larger single cover area, are often relatively small in number. Most species of extant Itea have an average of only 4–6 pairs of secondary veins, whereas only I. japonica and I. rhamnoides have an average of 7 pairs (Table 1). When leaves have higher numbers of secondary veins, the angles between these veins and the middle veins are smaller (Plate IV).

Most of the evergreen Itea species are irregularly crenate to serrate toothed. In limestone hills, species such as Itea yunnanensis Franch. and Itea ilicifolia Oliv. have teeth that are specialized into spinose. In the temperate deciduous taxa I. japonica and I. virginica, the teeth become serrate. These characteristics of plants might be an evolution indicator for adapting the environment change (drought/cold) (Table 2; Plate IV).

The Wenshan fossil leaves have a smaller size, oblong shape and irregular crenate to serrate teeth with medium density. Comparative morphological analysis of the Wenshan fossils showed that their leaf size, shape and architecture are most similar to the extant Itea omeiensis. The main difference between the Wenshan fossils and I. omeiensis is that the Wenshan fossils have significantly more secondary vein pairs. Therefore, it is treated as a new species (I. polyneura). I. omeiensis is a widely distributed species in the subtropical evergreen broad-leaved forest region in southern China (Fang et al., 2011). In addition, its area of distribution differs slightly from the equally common Itea chinensis Hook. et Aru. Moreover, I. omeiensis is less distributed in the Yunnan plateau region than is I. chinensis, which is characterized by the Sino-Japan floristic region (Table 2).

4.3. Implications from Wenshan fossils

The Itea leaf fossils from the Oligocene Wenshan flora in this study are the oldest occurrence of the genus in East Asia. These are the second confirmed leaf fossils of the genus. The Itea leaf fossils are morphologically similar to extant I. omeiensis of the Sect. Sempervirentes. This fossil record shows that at least in the Oligocene the evergreen Itea was present in southwestern China, which is the center of diversity of the genus today. Moreover, there are many other extant taxa in the Oligocene Wenshan flora that also have the center of diversity in the South East Asia today, such as Fagaceae, Lauraceae, Calocedrus Kurz (Zhang et al., 2015), Exbucklandia R.W. Br (Huang et al., 2017), Ficus L. (Huang et al., 2018a), Mahonia Nutt (Huang et al., 2016a), Burretiodendron Rehder (Lebreton-Anberrée et al., 2015), and the evergreen Ulmus L. (Zhang et al., 2018). Thus, this flora may indicate at least an Oligocene origin for the East Asian flora.

The possible Oligocene origin for the East Asian flora, of which our fossil finding is an example, supports the ‘Tertiary North Hemisphere broad-leaved evergreen forest’ hypothesis (Milne and Abbott, 2002). However, the timing of the development of this biome on different continents may be problematic. According to previous research, some angiosperm taxa endemic to or present in eastern Asia today have a more ancient record in Europe and North America. Manchester (1999), Tiffney and Manchester (2001), Manchester et al. (2009) suggested that East Asia may be a refugium for some formerly more widespread genera rather than a center of origin. Hermsen (2013) also expressed similar views, namely that Itea fits this pattern and should have appeared much later in eastern Asia than in North America or Europe.

However, many fossil flora from the Eocene to Oligocene in southern China (including Wenshan) that have been found and studied in recent years have similar chronological appearances and taxa composition (Shi et al., 2014; Spicer et al., 2014; Quan et al., 2016; Herman et al., 2017; Jin et al., 2017; Linnemann et al., 2018), such as the evergreen Fagaceae (Huang et al., 2018b; Liu et al., 2019), Liquidambar L. (Kodrul et al., 2018), and Camellia L. (Huang et al., 2016b). The geological record of forest flora in East Asia may be much older than previously thought (Linnemann et al., 2018). Therefore, many Tertiary relict taxa have been found in Eocene North America and Europe may not necessarily reflect the origin area.

Although the phylogeny of genus Itea has not been updated, the presence in East Asia of all the different types of groups of the genus (terminal/axillary inflorescence, half-superior/inferior ovary) suggest that East Asia is probably a center of paleoendemism. The origin of the genus may have been in the paleotropics, which were widely spread throughout the Northern Hemisphere during the Paleogene, possibly by the ‘Malpighiaceae route’ (Davis et al., 2002; Jia et al., 2019).

The ecological breadth of Itea is quite extensive. It grows well not only in the understories of tropical rain forests, evergreen broad-leaved forests, and even temperate deciduous forests (Jin and Ohba, 2001), but it is often the dominant species in the shady small tree layer. Moreover, it is also very competitive in open habitats, and often becomes the dominant species in rocky areas in southeastern Africa (e.g., I. rhamnoides) (Van Wyk and Van Wyk, 2013) and in karst areas of southwestern China (e.g., Itea yangchunensis S. Y. Jin and I. yunnanensis) (Fang et al., 2011). Trait variations in Itea may have given these plants the ability to adapt the change of environment in East Asia, Africa and North America.