Tracing ancestral biogeography of Sonneratia based on fossil pollen and their probable modern analogues

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ScienceDirect Palaeoworld 22 (2013) 133–143

Tracing ancestral biogeography of Sonneratia based on fossil pollen and their probable modern analogues Limi Mao a,∗ , Swee Yeok Foong b a

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China b School of Biological Sciences, Universiti Sains Malaysia, Penang 11800, Malaysia Received 19 May 2013; received in revised form 20 August 2013; accepted 5 September 2013 Available online 14 September 2013

Abstract Extant tropical mangrove Sonneratia is assigned in the monogeneric subfamily of Lythraceae. There are still some debates on the early fossil pollen of Florschuetzia, which is well accepted as ancestral to Sonneratia. This paper re-assesses palynological interpretations on the historical biogeography of the genus, based mainly on the updated fossil pollen records of Paleogene through Quaternary and their probable modern analogues. Florschuetzia was extensively documented from the late Eocene to middle Miocene in palaeotropics around the Tethyan region. According to the geological age of the fossil pollen and their morphological assessments, ancestral Sonneratia migrated from the center of origin in southeastern Asia probably during early Eocene, and radiated and expanded northward to China and Japan, southward to Australia, and westward to east Africa. Until the warmer period of the early middle Miocene (Langhian), Sonneratia had the largest geographical range suggested by abundant fossil pollen from southern mainland China and southwestern Japan, out of latitudinal limit of this extant genus. Quaternary glaciations, especially the Last Glacial Maximum (LGM), played a significant role in shaping the current biogeography of Sonneratia. However unequivocal assignments of early Florschuetzia and the associated variants to the evolved Sonneratia remain an issue due to the lack of intensive morphological comparison from different fossil sites. Thus, we examined the evolutionary trends of the extinct genus Florschuetzia towards Sonneratia on the basis of our synthesis on the updated published data and our recent pollen morphological investigation. © 2013 Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. All rights reserved. Keywords: Sonneratia; Florschuetzia; Biogeography; Fossil; Pollen

1. Introduction The well described Cenozoic fossil Sonneratia and its ancestor Florschuetzia include the wood from the Paleocene–Pliocene of southeastern Asia (Ramanujam, 1956; Shallom, 1963; Rao and Ramanujam, 1966; Chitaley, 1968; Awasthi, 1969; Biradar and Mahabale, 1973; Kramer, 1974; Shete and Kulkarni, 1982; Bande and Prakash, 1984, 1986; Lakhanpal et al., 1984; Mehrotra, 1988; Vozenin-Serra et al., 1989; Guleria, 1991; Srivastava, 2008), in the middle Eocene of Libya (Louvet, 1970), in the Oligocene of Austria (Hofmann, 1952) and Japan (Srivastava and Suzuki, 2001), and an exceptional form in the late Cretaceous of Uzbekistan (Shelomentseva, 1992); the root (Chitaley, 1968) and leaf (Ambwani, 1991) from the Paleocene

∗

Corresponding author. Tel.: +86 25 83282245. E-mail address: [email protected] (L. Mao).

of India; and the pollen from the Eocene through Miocene of southeastern Asia (Muller, 1964, 1978; Germeraad et al., 1968; Awasthi, 1969; Graham and Graham, 1971; Guleria et al., 1996; Morley, 2000; Srivastava and Suzuki, 2001; Songtham et al., 2005; Srivastava and Guleria, 2006), in the mid-Tertiary of the Red Sea and Nile Delta (Legoux, 1978; Morley, 2000), in the late Paleogene of France (Gruas-Cavagnetto et al., 1988), in the late Miocene to recent of New Guinea (Khan, 1974), in the middle Miocene of Japan (Yamanoi et al., 1980; Yamanoi, 1984) and China (Lei, 1998), in the late Eocene of China (Lei, 1998; Liu and Yang, 1999), and in the Pleistocene (e.g., Sohma, 1973; Sun, 1991; Zheng and Zhou, 1995; Wang and Zhang, 1998; Zheng and Li, 2000; Kumaran et al., 2005; Rugmai et al., 2008). According to Germeraad et al. (1968) and Muller (1978), the fossil pollen of Sonneratia can be clearly assigned to the extant species from the early Miocene (22.5 Ma). The records of Sonneratia show a gradual change from types referable to Lythraceae and strongly support the evolutionary divergence of Sonneratiaceae

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(Tomlinson, 1986). Recently Graham (2013) synthesized fossil records for the family Lythraceae and rejected some morphotypes of Florschuetzia and Sonneratia that are not compared favorably with accepted family or generic parameters. Thus, it is necessary to re-assess pollen records and the possible associated variants of this genus more prudently. Germeraad et al. (1968) intensively investigated Florschuetzia in Borneo. Of these, some Miocene species can be clearly attributed to the extant Sonneratia, such as F. levipoli attributable to S. caseolaris. Muller (1969, 1978) also investigated extant Sonneratia palynologically and reviewed its fossil record of wood, flowers, fruits and pollen, and concluded that the genus first occurred probably in the early Eocene in Southeast Asia. However, this conclusion does not agree with the earliest Sonneratia-like pollen of Florschuetzia sp. from the late Paleocene deposits in south central France (58.7–55.8 Ma; Gruas-Cavagnetto et al., 1988; Plaziat et al., 2001). Moreover, Florschuetzia sp. pollen was younger than the earliest fossil wood (Sonneratioxylon preapetalum) assigned to Sonneratia from the Deccan Intertrappean Bed, the early Paleocene (67.3–63.8 Ma) of India (Awasthi, 1969). Muller (1964, 1978) and Morley (2000) emphasized the lengthy presence of Florschuetzia and the subsequent appearance of Sonneratia in southeastern Asia, which, however, does not necessarily support a southeastern Asian origin of the genus (Graham, 2013). However, Ellison et al. (1999) asserted that the modern distributions result almost entirely from vicariance events, not consistent with an Indo-West Pacific (IWP) centre of origin for mangrove species and associated gastropods. Considering very few fossils of gastropod were preserved in anoxic, acidic, peaty soils which may rapidly dissolve the calcium carbonate shells (Plaziat et al., 1983), we focus on relatively rich plant fossils in this paper, especially on some well preserved pollen grains. We re-assess fossil pollen records of Florschuetzia/Sonneratia with an emphasis on the historical biogeography of Sonneratia based on the palynological interpretation, and further evaluate the evolutionary trends of extinct genus Florschuetzia towards Sonneratia by reviewing the published fossil pollen data and comparing them with the extant species.

2. General systematics of extant genus Sonneratia and its biogeography 2.1. General systematics of Sonneratia The extant genus Sonneratia belongs to Sonneratioideae (Engl. et Gilg) S.A. Graham, Thorne et Reveal, as one of the monogeneric subfamilies of Lythraceae within the Myrtales validated by Graham et al. (1998). Sonneratia and inland Duabanga were formerly placed in Sonneratiaceae independent from the family Lythraceae, but both of them were assigned in their own subfamily based on morphological and molecular studies on Lythraceae sensu lato (Thorne, 1976, 1981, 1992; Dahlgren and Thorne, 1984; Graham et al., 1993a,b). The phylogenetic analysis of Sonneratia in the Internal Transcribed Spacer (ITS) sequences indicates that the Sonneratiaceae should be included within the Lythraceae instead of a distinct family (Shi et al., 2000). Living Sonneratia consists of around nine species (Fig. 1), including three putative hybrids, namely Sonneratia alba, S. apetala, S. caseolari, S. griffithii, S. × gulngai, S. × hainanensis, S. lanceolata, S. ovata, and S. × urama. It is restricted to mangrove communities, often forming seaward fringing, and some of them have a very restricted range, such as S. griffithii (Fig. 1e, specimen from Herbarium in Prince of Songkla University, Thailand). Species in Sonneratia are notable for their large showy flowers with numerous red or white stamens (Fig. 1) and the berry-shaped fruit seated on a persistent calyx with 6–8 erect pointed lobes (Duke, 2006). They are recognized by the tall conical pneumatophores arising from horizontal roots. Key to these species was described in the early publications (Tomlinson, 1986) and recent illustration books for the field guide (Duke, 2006; Wang and Wang, 2007); Wang and Chen (2002) studied the systematics and biogeography of the Sonneratiaceae in China. However, the systematic descriptions of some species probably need to be revised to take into account their geographical variations, such as S. caseolaris and hybrids of S × gulngai, S. × urama and S. × hainanensis.

Fig. 1. Showy flowers of living Sonneratia and the specimen of Sonneratia griffithii. (a) Sonneratia alba. (b) S. apetala. (c) S. caseolaris. (d) S. × gulngai. (e) S. griffithii, specimen from PSU-Herbarium, Thailand, photo by Jarearnsak Sae Wai. (f) S. × hainanensis. (g) S. ovata. (h) S. × urama, reproduced from Duke (2006). (i) S. lanceolata, reproduced from Duke (2006).

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2.2. Biogeography of modern Sonneratia Sonneratia is an endemic genus in the Indo-West Pacific (IWP) region (Fig. 2), which is the frontal element in the estuary mangrove swamps or tidal inlets and bays from the coastal tropical East Africa to Indo-Malaysia, southern China, New Guinea, Australia, and islands in the Western Pacific (Duke, 2006). Sonneratia grows mostly along the banks of tidal rivers, creeks, and within the sheltered bays of offshore islands and reef cays. It is a typical constituent of mangrove communities throughout its geographical range. Mangrove distributions are influenced not only by long distance dispersal and establishment success, but also by geographical conditions and past changes in these conditions (Duke et al., 1998). Geological and climatic changes have greatly influenced the modern distribution of species and the evolution of mangrove habitat. Mangrove evolution, diversification, and dispersal apparently were accelerated by continental-drift (Duke et al., 1998). The most widespread species in the genus is Sonneratia alba, from East Africa to India and through Southeast Asia (including southern China and Indonesia) to the western islands in the Pacific Ocean including New Caledonia, the Solomon Islands and northern Australia (Fig. 2), mostly at low tidal contours within the frontal stands of downstream, the lower reaches of estuaries and offshore island enclaves in the regions of moderate to high rainfall where tidal ranges exceed 1 m (Duke, 2006). Sonneratia caseolaris occurs frequently in the frontal stands in some upstream estuarine situations subjected to high levels of freshwater runoff, from the west coast of India to southern China and the western islands in the Pacific Ocean, including New Guinea and northern Australia (Fig. 2). Interestingly, the habitat distribution of Sonneratia × gulngai, which is a hybrid of S. alba and S. caseolaris, overlaps those of the parent species in that it is found in mid intertidal, intermediate estuarine situations. Sonneratia ovata prefers a different habitat, usually occurring at the high tide margin in estuaries and is occasionally found on the banks

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of tidal creeks and rivers on muddy soils inundated only by spring tides. It is scattered in widely separate localities from China and Thailand through the Peninsular Malaysia, the Riau Archipelago, Java, and Borneo, to Sulawesi, the Moluccas, and Daru Island and Milne Bay in New Guinea (Fig. 2). Sonneratia lanceolata occurs at lower tidal contours in the upstream estuarine position. It is relatively unknown beyond Australia, Indonesia, and New Guinea (Duke, 2006; Fig. 2). Sonneratia × urama is the hybrid of S. alba and S. lanceolata (Duke, 1994). This putative hybrid has been reported in Australia, Indonesia, and Papua New Guinea (Fig. 2), essentially reflecting the range of the less common parent, S. lanceolata (Duke and Jackes, 1987). S. griffithii has a restricted distribution along the shores of the Andaman Sea, northward to Bengal and southward to the upper Malay Peninsula, Thailand (Tomlinson, 1986; Fig. 2). 3. Fossil pollen records of Florschuetzia and Sonneratia The genus Florschuetzia has been named in memory of the late Prof. Dr. F. Florschfitz, the founder of palynology in the Netherlands (Germeraad et al., 1968). Florschuetzia is the pollen from genus of several species known mainly from abundant, varied fossil grains in the tropics of Southeast Asia, and also in the Paleocene of southern France (Figs. 3 and 4). There are seven known species of the genus Florschuetzia, namely F. trilobata, F. semilobata, F. levipoli, F. meridionalis from Borneo (Germeraad et al., 1968), F. reticulata from Sulawesi, Indonesia (Sohma, 1973), F. minutes from India (Rawat et al., 1977), and F. claricolpata from central Japan (Yamanoi, 1984). F. reticulata and F. minutes are not accepted based on Graham’s evaluation (Graham, 2013). The former six species do not have a colpate aperture, although colpoid grooves may occur in F. trilobata. However, according to SEM observation by Yamanoi, F. claricolpata is characterized by a distinctly colpate aperture (Yamanoi, 1984; also Fig. 3). More detailed information on this species is presented in the discussion.

Fig. 2. Geographical distribution (in green) of extant genus Sonneratia in the Indo-West Pacific (IWP) region (based on Duke, 2006; Tomlinson, 1986). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

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Fig. 3. Fossil pollen of Florschuetzia, Trilobapollis and Quaternary sub-fossil of Sonneratia. (a) F. semilobata, holotype, early Miocene, Borneo, 23–24 ␮m. (b) F. claricolpata, holotype, middle Miocene, Japan, 25–34 ␮m. (c) Florschuetzia sp. 2, middle Miocene, Taiwan (China), 35 ␮m. (d) F. trilobata, holotype, Oligocene, Borneo, 28–35 ␮m. (e) F. meridionalis, holotype, Miocene, Borneo, 35–60 ␮m. (f) F. levipoli, holotype, Miocene, Borneo, 30–50 ␮m. (g) Trilobapollis ellipticus, ancestral Florschuetzia or variants? Paleocene, Leizhou Peninsula, China. (h) Florschuetzia sp. 1, late Paleocene, France, 26 ␮m. (i, j) Early Pleistocene sub-fossil from Leizhou Peninsula, southern China, Sonneratia sp. 3 (cf. S. alba). (k–n) Late Quaternary sub-fossil from Cambodia, scale bar = 10 ␮m; (k, l) Sonneratia caseolaris in polar view and equatorial view, respectively; (m) S. alba; (n) Sonneratia sp. (cf. S. × gulngai type). Red arrow: mesoporium meridional ridge (pollen diagnostic of S. alba and S. × hainanensis); blue arrow: structurally discontinuous between equatorial and polar regions; light green arrow: pseudocolpus. Photo sources: Gruas-Cavagnetto et al., 1988 (Florschuetzia sp. 1); Yamanoi, 1984 (F. claricolpata); Sun et al., 1980 (Trilobapollis ellipticus); Weiming Wang (Florschuetzia sp. 2); Wang and Zhang, 1998 (Sonneratia sp. 3); Germeraad et al., 1968 (all others except those otherwise specified). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

Florschuetzia trilobata in Central Java was first associated with Sonneratia in the middle Eocene deposits of southeastern Asia, but Muller (1981a) viewed it as not quite fully Sonneratia. F. levipoli from the early Miocene of Borneo (ca. 19 Ma) is the earliest fossil pollen directly attributable to living species S. caseolaris, then followed by F. meridionalis from the middle Miocene of Borneo attributable to S. alba according to Muller (1984) and Morley (2000). The Miocene pollen of F. levipoli (S. caseolaris) in Borneo marks the dawn of extant Sonneratia as an obligate mangrove genus, while earlier Florschuetzia trilobata being described from fresh-water and saline deposits (Graham, 2013). The earliest record of Florschuetzia pollen attributable to Sonneratiaceae is reported by Gruas-Cavagnetto et al. (1988) in the late Paleocene of southern France (Thanetian, 58.7–55.8 Ma), but as Graham (2013) pointed out that it is difficult to confirm the Sonneratia-like pollen based on the LM picture of the isolated pollen grains, which are earlier than the later Florschuetzia spp. from Asia (see question marked pollen grain in Fig. 3h and Fig. 4). Zaklinskaja (1978)

reported Florschuetzia in the Eocene of West African; Yamanoi et al. (1980) and Yamanoi (1984) studied the middle Miocene Florschuetzia in central Japan; Liu and Yang (1999) studied the Florschuetzia trilobata in the pollen flora of southern China, which suggests mangrove development in the low area of the Bose Basin since the late Eocene. The frequent pollen record is explained by its current overrepresentation reported in modern pollen assemblages (Caratini et al., 1973). The botanical significance of Florschuetzia trilobata is evaluated according to Germeraad et al. (1968) and Muller (1978, 1981b), as the oldest type, F. trilobata, is linked with an intermediate between Lythraceae and its subfamily Sonneratiaceae. Although it is recorded in the same period in early Miocene as the unambiguous Sonneratia pollen, it has been suggested as an ancestor of the evolved Sonneratia. Germeraad et al. (1968) reported Florschuetzia in assemblages along with Sonneratia and Rhizophora. Consequently it is suggested that F. trilobata was probably produced by a true, but extinct, mangrove plant which was replaced gradually by the extant species in the end of Paleogene and afterwards.

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Apparently, Sonneratia-like pollen of Florschuetzia reported by Gruas-Cavagnetto et al. (1988) from the late Paleocene deposits in south central France (58.7–55.8 Ma) needs to be confirmed (question marked in Figs. 3 and 4), as well as F. reticulata (Sohma, 1973) of the Quaternary and F. minutus (Rawat et al., 1977) from the Eocene of India. Some investigators reported the early-mid Quaternary Sonneratia sp. (cf. alba) in the coastal areas of South China and SCS (Zhou, 1988; Sun, 1991; Zheng and Zhou, 1995; Lei, 1998; Wang and Zhang, 1998; Zheng and Li, 2000) (see also Fig. 3i, j), where it is out of the latitudinal limits for this genus. Impacts of climatic events and consequent sea level changes as a result of the Quaternary glaciations on the tropical mangrove habitats are important in shaping the current distribution range of Sonneratia. In the Holocene deposits, mangrove subfossil pollen grains are preserved as perfect as the living plants’ (Fig. 3k–n). The pollen grains of Sonneratia spp. were extracted from the estuary sediments in the upper Mekong River delta, Cambodia (Li et al., 2012). Table 1 presents detailed fossil information on Florschuetzia and Sonneratia, including some macrofossils.

4. Discussion 4.1. Notes on Florschuetzia claricolpata from Japan and Florschuetzia spp. from southern China Yamanoi (1984) published the fossil pollen of Florschuetzia claricolpata from the middle Miocene of central Japan (Fig. 3b, cf. Fig. 3c from middle Miocene of Taiwan), which is considered comparable to extant Sonneratia alba (also see Fig. 4, top right). Moreover, F. claricolpata accounted for 41% of the pollen assemblage, with other mangrove pollen Excoecaria (12%) and Bruguiera (0.5%) from the same assemblage (Yamanoi, 1984). F. claricolpata is described as heterocolpate, isopolar, porate, and rounded triangular in polar view, which is very close to Lagerstroemia. Yamanoi (1984) discussed morphological overlaps between the two highly similar pollen types. Muller (1981b) suggested that, since some pollen types of Lagerstroemia are similar to Florschuetzia trilobata but have a colpate aperture, these genera are likely to have a common ancestral matrix. The absence of colpi is confirmed in Sonneratia caseolaris and S. ovata with SEM by Muller (1981a). However, pollen grains of S. alba and S. griffithii have a colpal part though it is poorly developed (Muller, 1969, 1981a). To examine the colpi in the extant S. alba, Yamanoi (1984) observed 100 well expanded pollen grains sampled from Semakau Island (Singapore) using SEM and calculated the following frequencies of presence of colpi: distinct (5%), more or less distinct (30%), faint (59%), and absent (6%). These facts and Muller’s phylogenetic view of Lagerstroemia and Sonneratia (Muller, 1981b) suggest that the presence of colpi may be more frequent in the ancestral populations of S. alba than the recent ones. Yamanoi (1984) concluded that F. claricolpata has a definite affinity to Sonneratia and shares more pollen morphological features with S. alba, especially with subtypes D and F described by Muller (1969)

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than any other species, and that a similar subtype already existed since the middle Miocene. Sun et al. (1980) established genus Trilobapollis of the early Paleogene from Leizhou Peninsula, northern South China Sea (SCS), which resemble Florschuetzia trilobata based on their trilobate-shape, except for the absence of apertures in Trilobapollis. It is speculated that Trilobapollis could be an ancestral type of F. trilobata (Yamanoi, 1984); or it may be a variant of F. trilobata given colpi recognizable under SEM. Sonneratia first appears on the Paleocene island continent of India (Prakash, 1960), earlier than other closely related pollen of the region (such as Santalumidites, Sonneratioipollis, Jugopolis and Florschuetzia) that appeared during Eocene (Venkatachala and Kar, 1968; Venkatachala and Rawat, 1972; Rawat et al., 1977). However, Santalumidites from the Eocene of Australia and Sonneratioipollis, Jugopolis and Florschuetzia from the Eocene of India show no clear affinity with the extant Sonneratia (Muller, 1981a). Therefore, it seems that the distribution range of Florschuetzia was limited along the equatorial regions of Southeast Asia. F. claricolpata from Japan and F. trilobata, F. levipoli, and F. meridionalis from the Pearl River mouth basin, South China (Lei, 1998; Liu and Yang, 1999), together with Trilobapollis from early Paleogene (Sun et al., 1980), possibly belong to an ancestral type of Florschuetzia; all of them were distributed beyond the known geographic range of Florschuetzia, suggesting coastal environment with tropical climate in southwestern Japan and northern SCS during Paleogene through middle Miocene (Yamanoi, 1984). 4.2. Pollen evolution of Florschuetzia towards Sonneratia Florschuetzia is at the base of a complex of emerging pollen types that evolved into pollen forms of Lagerstroemia, Sonneratia, and possibly Trapa and other genera (Germeraad et al., 1968; Muller, 1978, 1984; Morley, 2000; Graham, 2013). The earliest Florschuetzia pollen is reported from the late Paleocene Thanetian (58.7–55.8 Ma) of south central France, which was situated at the southern border of the Tethys (Gruas-Cavagnetto et al., 1988; Plaziat et al., 2001; Graham, 2013). The pollen morphology and pollen evolution of Florschuetzia towards the extant genus Sonneratia are illustrated in Figs. 3 and 4. However, it needs confirmation on whether or not there is an early form of Florschuetzia with no distinctive polar caps, prominent mesocolpal ridges, and the well-defined verrucate equatorial belt of later Florschuetzia species (Graham, 2013). Fossil pollen grains of Florschuetzia are abundant and highly varied structurally in the Eocene deposits from southeastern Asia (Muller, 1981b; Guleria et al., 1996; Morley, 2000). The oldest ones are morphologically more diverse than later ones (Graham, 2013). The oldest species in Asia is F. trilobata, which can be hypothesized as an evolved Trilobapollis ellipticus, which was found from Leizhou Peninsula in the early Paleocene of China (Sun et al., 1980). The species variation and speciation might be triggered by extreme climatic events, such as the Paleocene–Eocene Thermal Maximum (PETM), which might have played a significant role in the early evolution of Florschuetzia. F. trilobata is considered to be the precursor to

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Table 1 Fossil Florschuetzia and Sonneratia (pollen records updated based on Graham, 2013). Fossil name

Organ

Locality

Data source

Remark

Florschuetzia (Extinct), see also Sonneratia Pollen Florschuetzia sp. (as Sonneratiaceae) Florschuetzia trilobata Pollen

late Paleocene middle Eocene to early Miocene

Eocene Eocene early Miocene early Miocene to Pliocene late Miocene to Recent middle Miocene late Miocene to Recent middle Miocene middle Miocene Quaternary

Gruas-Cavagnetto et al., 1988 Germeraad et al., 1968; Muller, 1981a; Watanasak, 1990; Handique, 1993; Lei, 1998; Liu and Yang, 1999; Morley, 2000 Zaklinskaja, 1978 Rawat et al., 1977 Germeraad et al., 1968; Muller, 1981a; Morley, 2000 Germeraad et al., 1968; Muller, 1978; Lei, 1998 Khan, 1974 Germeraad et al., 1968; Muller, 1978 Khan, 1974 Songtham et al., 2005 Yamanoi, 1984 Sohma, 1973

Accepted? Accepted

Florschuetzia minutus Florschuetzia cf. meridionalis Florschuetzia semilobata Florschuetzia levipoli (holotype) Florschuetzia levipoli Florschuetzia meridionalis (holotype) Florschuetzia meridionalis Florschuetzia sp. Florschuetzia claricolpata (holotype) Florschuetzia reticulata

France Borneo, Java, Assam, Thailand, China, Red Sea, Nile Delta India India Borneo, Thailand Borneo, China New Guinea Borneo New Guinea Thailand Japan Indonesia

Sonneratia, including Sonneratioxylon; see also Florschuetzia Sonneratioxylon turonicum Wood late Cretaceous Sonneratia meghalayensis Leaf late Paleocene Sonneratiorhizos raoi Root Paleocene Sonneratiaceae (Florschuetzia sp.) Pollen late Paleocene Sonneratioxylon preapetalum Wood Paleocene (Danian) to Miocene

Uzbekistan India India France India, Thailand, Sumatra

Unconfirmed

Sonneratioxylon aubrevevillei aff. Sonneratia: Sonneratioipollis aff. Sonneratia: Jugopollis tetraporites Sonneratia kyushuensis Sonneratioxylon prambachense Sonneratia caseolaris Sonneratia alba Sonneratioxylon dakshinense Sonneratioxylon dudukurense Sonneratia sp.

Wood Pollen Pollen Wood Wood Pollen Pollen Wood Wood Pollen

middle Eocene Eocene Eocene early Oligocene late Oligocene early Miocene middle Miocene Miocene to Pliocene Tertiary late Pleistocene

Libya India India Japan Austria Borneo Borneo India India China, Thailand, India

Sonneratioxylon duabangoides

Wood

Paleocene

India

Shelomentseva, 1992 Ambwani, 1991 Chitaley, 1968 Gruas-Cavagnetto et al., 1988 Awasthi, 1969; Biradar and Mahabale, 1973; Kramer, 1974; Shete and Kulkarni, 1982; Bande and Prakash, 1984; Lakhanpal et al., 1984; Mehrotra, 1988; Vozenin-Serra et al., 1989; Guleria, 1991; Srivastava, 2008 Louvet, 1970 Venkatachala and Kar, 1968 Venkatachala and Rawat, 1972 Srivastava and Suzuki, 2001 Hofmann, 1952 Germeraad et al., 1968; Muller, 1978; Morley, 2000 Muller, 1978 Ramanujam, 1956; Awasthi, 1969; Mehrotra, 1988 Rao and Ramanujam, 1966; Mehrotra, 1988 Sun, 1991; Zheng and Zhou, 1995; Wang and Zhang, 1998; Zheng and Li, 2000; Kumaran et al., 2005; Rugmai et al., 2008 Shallom, 1963; Chitaley, 1968

Pollen Pollen Pollen Pollen Pollen Pollen Pollen Pollen Pollen Pollen

Unconfirmed Unconfirmed Accepted Accepted Accepted Unconfirmed Accepted Unconfirmed Accepted Unconfirmed

Unconfirmed Accepted? Accepted but not all

Accepted Unconfirmed Accepted Unconfirmed Accepted Accepted Unconfirmed Unconfirmed Accepted

Unconfirmed

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Period

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Fig. 4. Tentative interpretation of the pollen evolution from Florschuetzia to the extant genus Sonneratia as proposed by Germeraad et al. (1968) and Muller (1984), also showing fossil pollen of Trilobapollis, possible ancestral Florschuetzia? and interspecific diagnostic of two pollen species of living Sonneratia caseolaris and S. alba. Scale bar = 10 ␮m (SEM equatorial views), 1 ␮m (SEM detailed polar cap), 20 ␮m (LM). More species in this genus, see Mao et al. (2012). Line drawings of Florschuetzia from Graham (2013).

both Sonneratia and Lagerstroemia (Germeraad et al., 1968; Morley, 2000). Florschuetzia trilobata (Figs. 3 and 4) is a subprolate, thick-walled, triporate grain with colpoid grooves and meridional thickenings. The pores are circular and distinct, and the exine is psilate or covered with broken, separate verrucae. Modern Sonneratia and Lagerstroemia pollen are typically triporate and may be three-pseudocolpate (Sonneratia) (Fig. 4, Sonneratia alba) or six-pseudocolpate (see Lagerstroemia Kim et al., 1994) although the prominence of the pseudocolpi varies, as does the exine sculpture in the pollen of both genera. Variants of Florschuetzia approach modern Sonneratia and Lagerstroemia pollen in the development of the colpi and exine sculpture. Early Florschuetzia has been confused with some variants of Verrutricolporites (see Crenea in Graham et al., 1985) in which the colpi were so indistinct as to appearing missing or the typically verrucate exine is reduced to nearly psilate, thus approaching Florschuetzia, except in its smaller size. Morley has speculated that Verrutricolporites, Lagerstroemia, and Sonneratia share an early history with Florschuetzia (Morley, 2000). Florschuetzia trilobata is not present in the Late Cretaceous to Eocene formations of northwest Borneo (Muller, 1968). It

appears in the late Eocene deposits in Assam (Handique, 1993), the Oligocene Kalimantan (Morley, 2000), the Miocene Borneo (Muller, 1981a), and in the mid-Tertiary Red Sea and Nile Delta (Legoux, 1978; Morley, 2000). It occurs with Lagerstroemialike pollen in the middle Eocene Nanggulan Formation of Central Java (Morley, 2000). Florschuetzia trilobata is a component of lacustrine freshwater swamp sediments from the Oligocene in Vietnam, Thailand, and Cambodia, and from the early Miocene of Malaysia and Indonesia (Graham, 2013). In later Miocene, the genus occurs with brackish and salt-water mangrove vegetation, suggesting that Florschuetzia was initially widespread in fresh water in southeast Asia and not restricted to brackish waters or mangrove vegetation as the probable derivative genus Sonneratia is today (Morley, 2000). Florschuetzia by the Miocene coexisted with extinct Sonneratia pollen types according to Muller (1978, 1981b, 1984), and he speculated that it was ancestral to and was eventually replaced by the modern species of Sonneratia in mangrove habitats (Graham, 2013). Muller (1984) provided a diagram comparing the distribution of four species of Florschuetzia through time (Fig. 4,

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with our update of Florschuetzia claricolpata from Miocene of southwestern Japan, and early Quaternary diverse pollen of Sonneratia added in the diagram). Following the Eocene appearance of F. trilobata in Java, Florschuetzia semilobata occurred in the early Miocene in Borneo (Muller, 1981a), and F. levipoli appeared shortly after in the early Miocene and F. meridionalis in the middle Miocene. Transitional types were also present. Florschuetzia trilobata became extinct by the middle Miocene. Florschuetzia levipoli (Figs. 3 and 4) was considered equivalent to living Sonneratia caseolaris; F. meridionalis (Figs. 3 and 4) attributable to S. alba; Florschuetzia trilobata, F. semilobata, and F. levipoli coexist in the Miocene of Thailand (Watanasak, 1990). Both Florschuetzia levipoli and F. meridionalis occurred in the middle Miocene (ca. 16 Ma) of Borneo (Muller, 1978, 1981a, 1984) and in the late Miocene to Recent of Papua New Guinea (Khan, 1974); F. reticulata is described from the Quaternary of Sulawesi (Sohma, 1973). The SEM images of F. claricolpata from the middle Miocene of Japan (Yamanoi, 1984) show a close resemblance to living Lagerstroemia pollen (Kim et al., 1994; Graham, 2013), but the former accounted for a high percentage (41%) in the pollen assemblage, with other mangrove elements, such as Bruguiera, Excoecaria. Thus, it is unlikely to be Lagerstroemia pollen. According to a recent investigation by Mao et al. (2012), the living Sonneratia has interspecific diagnostics of the shape of optical section, meridional ridge, polar caps and sculptures, unequivocal key to S. caseolaris and S. alba (Fig. 4). Therefore, Florschuetzia reticulata is attributable to S. alba. Morley (2000), with regard to the earliest evolutionary relationships and historical dispersal patterns among Florschuetzia and modern pollen of Sonneratia, Lagerstroemia, Duabanga, and Trapa, envisioned a common ancestral form that originated in the western Tethys region (Graham, 2013). Morley hypothesized that the ancestor of the four modern genera initially diversified as two lineages, one of which remained in the Tethyan Old World and the other dispersed to South America and later dispersed back to West Africa (Graham, 2013). The speculative diagram presented by Morley (2000) clearly illustrates the difficulties in resolving early relationships among the several genera based on the complex fossil pollen record. Although the account is theoretical, the four modern Asian genera of the Lythraceae are monophyletic in molecular phylogeny with Sonneratia and Trapa, and are strongly supported as sister to Lagerstroemia and Duabanga (Graham et al., 2005; Graham, 2013). We outlined the pollen evolution of the fossil genus Florschuetzia toward the extant genus by updated fossil records from possible early ancestral Florschuetzia of the Paleocene to its variants F. claricolpata of middle Miocene, based on the hypothesis by Germeraad et al. (1968) and Muller (1984) (Fig. 4). However, the pollen evolution of Florschuetzia towards Sonneratia needs more fossil data to make a detailed evaluation. 4.3. The historical biogeography of Sonneratia based on palynological interpretation According to Ellison et al. (1999), mangrove taxa, associated gastropods, and the entire mangrove ecosystem originated

around the Tethys Sea, and modern distributions result almost entirely from vicariance events. However, Plaziat et al. (2001) speculated that the Eocene/Oligocene boundary crisis appears to herald a beginning of the biogeographic split between the current eastern (Old World) and western provinces (New World) of mangrove plants. Although the climatic origins of this major disjunction are not clearly understood, their reassessment of Tertiary paleoclimates suggests that the major cooling events of middle Paleocene, end Eocene, and middle Pliocene were influential on the evolution of mangrove floras. According to Plaziat (1975), fossils of gastropods have been used as indicators of plaeo-habitats favourable for the development of mangrove swamps, due to habitat preference for some gastropod genera (e.g., Plaziat, 1984, 1995). Oyama (1950) first interpreted the mangrove environment in central Japan during middle Miocene (around 16 Ma) based on a gastropod faunal assemblage, supported by later pollen investigation (Yamanoi et al., 1980). However, relatively few fossil gastropods can be preserved due to shell dissolution in anoxic, acidic, peaty soils (Plaziat et al., 1983). Sonneratia appears to have colonized Southeast Asia from the northward migrating Indian subcontinent (Ellison et al., 1999). Until the warmer period of early middle Miocene (Langhian), Sonneratia had the largest geographical range suggested by abundant fossil pollen from southern mainland China (Lei, 1998; Liu and Yang, 1999) and southwestern Japan (Yamanoi et al., 1980; Yamanoi, 1984), out of the present latitudinal limit of the genus. Warm climate was also suggested by a fossil fruit wing of Dipterocarpus from the middle Miocene of Fujian in southeastern China (Shi and Li, 2010), because Dipterocarpus today is one of the dominant populations in tropical rainforest of southeastern Asia. The occurrence of Florschuetzia trilobata in the pollen flora suggests some mangrove development in the low area of the Bose Basin in the late Eocene (Liu and Yang, 1999). Lei (1998) found the time of pollen deposition of Florschuetzia levipoli and F. meridionalis in South China was later than that in southeastern Asia from the Eocene to Pliocene, indicating that ancestral Sonneratia probably migrated northwards from southeastern Asia. Based on fossil data (Table 1), we constructed a tentative distribution range of Sonneratia (Fig. 5) for the Eocene and Miocene. Fossil distribution of Florschuetzia/Sonneratia clearly suggests an expansion in middle Miocene, and contraction recently (Fig. 2). In early Quaternary, the tropical warm condition is indicated by pollen records of Sonneratia cf. alba along the coasts of northern SCS, which suggests Sonneratia expanded beyond current latitudinal limits accordingly (Wang and Zhang, 1998; Zheng and Li, 2000). High sea level stands during the warm period maintained the vegetation succession and the structure of mangrove ecosystem. However, sea-level dropped sharply as a result of subsequent glaciations in late Pleistocene, especially the Last Glacial Maximum (LGM); the mangroves and their sedimentation settings failed to keep up with the pace of seawater lowering and lost intertidal habitats. Therefore, the Quaternary glaciations, especially LGM of late Pleistocene (21–18 ka), played a significant role in shaping the current distribution range of Sonneratia in southern China. According to Woodroffe and

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Fig. 5. Geographic range of Sonneratia (late Miocene, 10 Ma): fossil distribution of Florschuetzia/Sonneratia suggesting a range expansion in Miocene, and a recent range contraction (detailed information on the fossil, see Table 1).

Grindrod (1991), sea-level fluctuations are likely to have played a similar role in the biogeography of mangroves particularly in Holocene. Many mangrove species have colonized oceanic islands during the Holocene through successful transoceanic dispersal to these islands. During late Pleistocene and Holocene, estuary succession history of Sonneratia and changes in associated sedimentation settings can be traced and reconstructed based on palynological analysis (Rugmai et al., 2008; Li et al., 2012). 5. Concluding remarks According to previous studies and our assessment, late Paleocene occurrence of Forschuetzia from France is unlikely, and F. trilobata appeared first in Eocene of Java, followed by F. semilobata in early Miocene in Borneo. F. levipoli occurred shortly after in early Miocene, and F. meridionalis in the middle Miocene, with the presence of transitional types. Appearance of F. claricolpata in the Miocene of southwestern Japan suggests the widest geographical range of Sonneratia in history. Florschuetzia trilobata became extinct by middle Miocene. Florschuetzia levipoli was assigned to modern pollen of Sonneratia caseolaris, and F. meridionalis is attributable to S. alba. Fossil pollen record of Sonneratia provides important clues in tracing historical biogeography, especially well preserved pollen grains from the late Eocene to middle Miocene. The modern distribution pattern of Sonneratia might be explained in terms of their origin in the cradle of early angiosperm diversification and their redistribution via migration and range expansion governed by continental realignment (Tomlinson, 1986).

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Range contraction and diversification have been important in American Pelliciera rhizophoreae (Graham, 1976). Comparison of fossil record of Sonneratia with its present distribution suggests a similar range contraction in recent geological epoch. There was a larger distribution range of Sonneratia in middle Miocene according to the well recorded fossil pollen than any other periods. The Quaternary glaciations, notably Pleistocene LGM, played a significant role in shaping current biogeography of Sonneratia. However, fossil occurrence is not sufficient enough to establish high resolution of historical biogeography in more detailed temporal and spatial scale, largely due to sparsely distributed fossil sites and limited data available so far. Consequently, further exploration of fossil materials, including macrofossils (wood, leaf, flowers, and fruits) and microfossils of this genus is necessary to reconstruct historical biogeography in more details. The resolution of pollen observation for Florschuetzia/Sonneratia and their variants should also be improved to determine fossil pollen with high reliability. In pollen morphological comparison in Lythraceae, one should consider geographic variants and/or genetic variation; at the generic level, high resemblance of pollen morphology in Lythraceae may render fossil pollen misidentification based on scanning electronic microscopy (SEM). Ideally, transmission electronic microscope (TEM) and light microscope (LM) in oil objective should be combined in fossil pollen identification. Therefore, early pollen evolution of Florschuetzia towards Sonneratia needs more detailed investigation before a clear phylogenic lineage is reconstructed for this genus in the Lythraceae sensu lato. Acknowledgements This work was funded by the National Natural Science Foundation of China (NSFC, Grant 40971029) and the “Strategic Priority Research Program — Climate Change: Carbon Budget and Relevant Issues” of the Chinese Academy of Sciences (Grant XDA05130401). We are grateful to Prof. Norm Duke for pollen specimens from Australia; Prof. Zhen Li (East China Normal University) for her providing extracted pollen specimens from the Quaternary mangrove peat in the upper Mekong River delta, Cambodia; Prof. Weiming Wang (Nanjing Institute of Geology and Palaeontology, CAS) for his LM picture of Florschuetzia sp. from the Miocene of Taiwan and for his comments on the manuscript. Mr. Jarearnsak Sae Wai kindly helped with a specimen picture and pollen sample of Sonneratia griffithii from PSU-Herbarium, Prince of Songkla University, Hat Yai, Thailand. Prof. Navnith Kumaran and an anonymous reviewer’s comments helped improve the manuscript. References Ambwani, K., 1991. Leaf impressions belonging to the Tertiary age of northeast India. Phytomorphology 41, 139–146. Awasthi, N., 1969. A fossil wood of Sonneratia from the Tertiary of South India. Palaeobotanist 17, 254–257. Bande, M.B., Prakash, U., 1984. Occurrence of Evodia, Amoora and Sonneratia from the Palaeogene of India. Proceedings of the Symposium on

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