Key to mangrove pollen and spores of southern China: an aid to palynological interpretation of Quaternary deposits in the South China Sea

Review of Palaeobotany and Palynology 176–177 (2012) 41–67

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Research paper

Key to mangrove pollen and spores of southern China: an aid to palynological interpretation of Quaternary deposits in the South China Sea Limi Mao a,⁎, David J. Batten a, b, Toshiyuki Fujiki c, Zhen Li d, Lu Dai e, Chengyu Weng e a

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China School of Earth, Atmospheric and Environmental Sciences, The University of Manchester, Oxford Road, Manchester M13 9PL, UK International Research Centre for Japanese Studies, 3-2 Oeyama-cho, Goryo, Nishikyo-ku, Kyoto 610-1192, Japan d State Key Laboratory of Estuarine and Coastal Research, East China Normal University, Shanghai 200062, China e State Key Laboratory of Marine Geology, Tongji University, Shanghai 200092, China b c

a r t i c l e

i n f o

Article history: Received 15 December 2011 Received in revised form 12 March 2012 Accepted 14 March 2012 Available online 23 March 2012 Keywords: mangrove pollen morphology Quaternary marine deposits South China Sea

a b s t r a c t Illustrations of, and keys to, mangrove pollen and spores from extant taxa are essential to studies of tropical Quaternary palynology and palaeoecology of estuarine and marine deposits. In this paper we present a pollen morphological “atlas” and identification keys for most of the mangrove flora of the coastal areas of south China, including an interspecific key to the major mangrove elements Rhizophora and Sonneratia. The morphology of the pollen and spores of 38 species of living mangrove and associated plants is described and illustrated by transmitted light photographs and scanning electron micrographs. These descriptions and illustrations, and the identification keys are presented at an achievable taxonomic level. The keys are open for future development so that pollen of other mangrove and associated plants can be accommodated when available. In their present state they should, nevertheless, aid palynological analyses of Quaternary mangrove and associated estuarine and marine deposits, particularly in the South China Sea and surrounding regions, but also elsewhere in tropical and subtropical regions. © 2012 Elsevier B.V. All rights reserved.

1. Introduction “As cogently noted by Alfred Russel Wallace during his equatorial travels, mangrove forests are crucial occupiers of the boundary between land and sea, being key ecosystems along many tropical and subtropical coastlines” (Alongi, 2009, p. 1). “Mangrove” is an ecological term that refers to a taxonomically diverse assemblage of trees and shrubs that forms dominant plant communities in tidal, saline wetlands along sheltered tropical and subtropical coasts (Blasco et al., 1996). Mangroves prosper mostly in tropical regions as a result of their adaptation strategies, their ecological dynamics being closely linked to changes in sea level. Pollen analysis of mangroves is important for both palaeoecological reconstructions of coastal vegetation and determinations of palaeoenvironment in tropical and subtropical regions (Muller, 1964, 1968; Muller and Caratini, 1977; Woodroffe, 1981; Semeniuk, 1983; Thanikaimoni, 1987; Grindrod, 1988; Baldibeke and Baldi, 1991; Larcombe and Carter, 1998; Chateauneuf et al., 2006; Farooqui and Achyuthan, 2006; Torricelli et al., 2006; Ellison, 2008; Khandelwal et al., 2008; Berkeley et al., 2009; Limaye and Kumaran, in press). Many papers on the succession of coastal ⁎ Corresponding author. E-mail addresses: [email protected] (L. Mao), [email protected] (D.J. Batten), [email protected] (T. Fujiki), [email protected] (Z. Li), [email protected] (L. Dai), [email protected] (C. Weng). 0034-6667/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.revpalbo.2012.03.004

vegetation, ecosystem dynamics and sea-level changes in these regions have been published (Woodroffe, 1988; Mildenhall, 1994; Parkinson et al., 1994; Blasco et al., 1996; Grindrod et al., 1999, 2002; Rull et al., 1999; Jaramillo and Bayona, 2000; Behling et al., 2001; Behling, 2002; Berdin et al., 2003; Behling and da Costa, 2004; van Campo and Bengo, 2004; Yulianto et al., 2004; Ellison, 2005; Kumaran et al., 2005; Scourse et al., 2005; Engelhart et al., 2007; Cohen et al., 2009; Hait and Behling, 2009; Jarzen and Dilcher, 2009; Monacci et al., 2009, 2011; Gonzalez et al., 2010; Barui, 2011; Bian et al., 2011). Specifically in connection with the South China Sea (SCS) and the coastal areas of south China and central Japan, there are a few reports on Neogene and Quaternary mangrove pollen- and spore-bearing deposits (Yamanoi, 1984; Zhou, 1988; Sun, 1991; Zheng and Zhou, 1995; Lei, 1998; Wang and Zhang, 1998), and a mangrove vegetation landscape through Marine Isotope Stage 3 and the Last Glacial Maximum has been reconstructed, based particularly on frequently occurring pollen of the major components of mangroves, Rhizophora and Sonneratia (Zheng, 1991; Sun et al., 2000, 2002; Wang et al., 2008, 2009; Zhang et al., 2011). As for other parts of the world, recent studies based on mangrove pollen data from surface sediments and Quaternary deposits have highlighted their importance for palaeoenvironmental interpretation (Yulianto et al., 2004, 2005; Kumaran et al., 2005; Mao et al., 2006; Li et al., 2008; Urrego et al., 2009, 2010; Proske et al., 2010; Barui, 2011; Bian et al., 2011).

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Effective reconstructions based on palynological analysis depend upon accurate identifications of pollen and spores, and in this respect keys to the products of the extant flora are very valuable (Jimenez-B and Rangel-C, 1997; Chester and Rains, 2001; Rangel-C et al., 2001; Rull, 2003; Willard et al., 2004; Bauermann et al., 2009). Morphological studies have been carried out previously on mangrove pollen from both sides of the Atlantic Ocean (Vezey et al., 1988; Silva and Santos, 2009), the Indian subcontinent, southeast Asia and the western Pacific (Muller, 1969, 1978; Muller and Caratini, 1977; Liu and Tang, 1989; Yamanoi, 2003; Yao et al., 2006; Fujiki and Ozawa, 2007; Mao et al., 2008, 2009; Chumchim, 2010, 2011), but keys to the identification of the palynological products of a wide range of mangrove taxa are not generally available. Hitherto, there has been no effective key to the identification of the pollen and spores of the mangroves of the northern SCS upon which to rely for determinations of specimens preserved in the sediments of the region. The family Rhizophoraceae and Sonneratia dominate tropical mangroves. The Rhizophoraceae, otherwise known as the “mangrove family”, consists of 16 genera and around 120 species of trees and shrubs. Only about 20 species of four genera, the conspicuously viviparous Bruguiera, Ceriops, Kandelia and Rhizophora, are found exclusively in mangroves. Rhizophora is a pantropical genus and a key member of Rhizophoraceae (Duke, 2006). It occurs widely along tropical and subtropical coasts from East Africa across to Asia, the Malay Peninsula, the Philippines, the western Pacific Islands and northern Australia. Rhizophora apiculata is distributed from India and Sri

Lanka across Asia to the western Pacific and northern Australia. It often dominates in mid intertidal, intermediate estuarine situations (Duke, 2006). The distribution of R. mucronata extends from East Africa and India through Asia and Indonesia and again to the western Pacific and northern Australia. It is also commonly dominant in similar conditions (Duke, 2006). Rather less widespread, R. stylosa ranges from the Malay Peninsula and the Ryukyu Islands through Indonesia and Asia to Micronesia, Samoa and northern Australia, and always dominates in mid to low intertidal, downstream estuarine situations (Duke, 2006). Sonneratia occurs throughout the Indo-West Pacific region, i.e., from East Africa to China, through Asia and Indonesia, to New Guinea, the western Pacific and northern Australia (Duke, 2006). The most widespread of all species of this genus is S. alba. Its distribution ranges from East Africa to India and through south-east Asia (including southern China and Indonesia) to the western islands of the Pacific Ocean including New Caledonia, the Solomon Islands and northern Australia. The trees are found mostly at low tidal contours within frontal stands of downstream, lower reaches of estuaries and offshore island enclaves in regions of moderate to high rainfall where tidal ranges exceed 1 m (Duke, 2006). Sonneratia caseolaris occurs frequently in frontal stands in upstream estuarine situations subjected to high levels of freshwater runoff. It ranges from the west coast of India to southern China and again through the western islands of the Pacific Ocean, including New Guinea and northern Australia (Duke, 2006). Interestingly, the habitat distribution of S. × 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,

Fig. 1. A, B, maps showing the location of the research area and the mangrove swamps Dongzhai (a) and Qinglan (b) investigated. C, landscape of the Bruguiera–Aegiceras corniculatum community in Dongzhai. D, landscape of the Sonneratia community in Qinglan. E, F, aerial views (from Google Earth) of parts of the Dongzhai and Qinglan swamps respectively from where pollen material was collected.

Table 1 List of mangrove species on Hainan Island, China, together with their ecological characteristics and an index to their pollen and spores. Family

a b c

Hernandia nymphaeifolia Pandanus tectorius Nypa fruticans Sonneratia caseolaris S. alba S. hainanensis S. × gulngai S. ovata S. apetalaa Casuarina equisetifoliab Premna obtusifolia Clerodendron inerme Acanthus ilicifolius A. ebracteatusc Barringtonia racemosa Dolichandrone spathaceac Aegiceras corniculatum Excoecaria agallocha Pongamia pinnata Pluchea indica Cerbera manghas Heritiera littoralis Bruguiera gymnorrhiza Bruguiera sexangula B. s. var. rhynchopetala Ceriops tagal Kandelia obovata Rhizophora apiculata R. stylosa R. mucronata Scyphiphora hydrophyllacea Avicennia marina Hibiscus tiliaceus Thespesia populnea Xylocarpus granatum Pemphis acidula Lumnitzera racemosa L. littorea Acrostichum aureum A. speciosum

Identification code (Plate I)

Ecological characteristics

Voucher

Mangrove group (after Tomlinson, 1986)

Life form

HN PT NF SC SA SHA SG SO SAP CE PO CI AI unavailable BR unavailable AC EA PP PI CM HL BG BS BSR CT KO RA RS RM SH AM HT TP XG PA LR LL AA AS

Minor element Mangrove associate Major element Major element Major element Major element Major element Major element Major element Minor element Minor element Minor element Mangrove associate Mangrove associate Mangrove associate Minor element Minor element Minor element Minor element Minor element Mangrove associate Minor element Major element Major element Major element Major element Major element Major element Major element Major element Minor element Major element Mangrove associate Mangrove associate Minor element Minor element Major element Major element Mangrove associate Mangrove associate

Broad-leaved evergreen tree Evergreen monocots (shrub/tree) Monocots/palm Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen tree Conifer-like evergreen tree Broad-leaved deciduous shrub/tree Broad-leaved deciduous shrub Broad-leaved evergreen semi-shrub Broad-leaved evergreen semi-shrub Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen shrub/tree Broad-leaved semi-evergreen/deciduous tree Broad-leaved decidous tree Broad-leaved evergreen shrub Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen tree Broad-leaved evergreen shrub/tree Broad-leaved evergreen shrub/tree Broad-leaved evergreen tree/shrub Broad-leaved evergreen tree/shrub Broad-leaved evergreen tree/shrub Broad-leaved evergreen shrub Broad-leaved evergreen shrub/tree Broad-leaved evergreen tree Broad-leaved evergreen/semi-deciduous tree Broad-leaved evergreen tree Broad-leaved evergreen shrub/tree Broad-leaved evergreen shrub/tree Broad-leaved evergreen tree Perennial herb/fern Perennial herb/fern

IRCJS HN001, Fujiki NIGPAS PT001, Mao NIGPAS NF001, Mao NIGPAS SC001, Mao NIGPAS SA001, Mao NIGPAS SHA002, Mao NIGPAS SG001, Mao NIGPAS SO001, Mao NIGPAS SAP001, Mao KUN 0602505b IRCJS PO002, Fujiki NIGPAS CI001, Mao NIGPAS AI01, Mao unavailable NIGPAS BR001, Mao unavailable NIGPAS AC001, Mao NIGPAS EA001, Mao NIGPAS PP02, Mao NIGPAS PI001, Mao, IRCJS CM003, Fujiki NIGPAS HL001, Zhong NIGPAS BG001, Mao NIGPAS BS001, Mao NIGPAS BS002, Mao NIGPAS, CT001, Chen NIGPAS KO001, Mao NIGPAS RA001, Mao NIGPAS RS001, Mao NIGPAS RM001, Mao NIGPAS SH001, Mao NIGPAS AM001, Mao NIGPAS HT001, Mao NIGPAS TP001, Mao NIGPAS XG001, Mao IRCJS PA004, Fujiki NIGPAS LL002, Mao NIGPAS LL001, Mao NIGPAS AE001, Mao NIGPAS AA001, Mao

Pollen and spore index Morphological key

Illustration

I. Inaperturate II. Monoporate III. Monocolpate/Zonasulcate IV. Triporate IV. Triporate IV. Triporate IV. Triporate IV. Triporate IV. Triporate IV. Triporate V. Tricolpate V. Tricolpate V. Tricolpate V. Tricolpate V. Tricolpate V. Tricolpate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VI. Tricolporate VII. Polyporate VII. Polyporate VIII. Polycolporate VIII. Polycolporate IX. Heterocolporate IX. Heterocolporate X. Trilete X. Trilete

Plate II, 1 Plate II, 2: Plate II, 3 Plate III, 1 Plate III, 2 Plate III, 3 Plate IV, 1 Plate IV, 2 Plate V, 2 Plate V, 1 Plate VI, 1 Plate VI, 3 Plate VI, 2 Liu and Tang, 1989 Plate VI, 4 Wei et al., 2001 Plate VII, 1 Plate VII, 2 Plate VII, 3 Plate VII, 4 Plate VIII, 1 Plate IX, 1 Plate X, 1 Plate X, 2 Plate X, 3 Plate IX, 3 Plate IX, 2 Plate XI, 1 Plate XI, 2 Plate XI, 3 Plate XII, 1 Plate XII, 2 Plate XIII, 1 Plate XIII, 2 Plate XIV, 1 Plate XIV, 2 Plate XV, 1 Plate XV, 2 Plate VIII, 2 Plate VIII, 3

L. Mao et al. / Review of Palaeobotany and Palynology 176–177 (2012) 41–67

Hemandiaceae Pandanaceae Palmae Sonneratiaceae Sonneratiaceae Sonneratiaceae Sonneratiaceae Sonneratiaceae Sonneratiaceae Casuarinaceae Verbenaceae Verbenaceae Acanthaceae Acanthaceae Barringtoniaceae Bignoniaceae Myrsinaceae Euphorbiaceae Leguminosae Compositae Apocynaceae Sterculiaceae Rhizophoraceae Rhizophoraceae Rhizophoraceae Rhizophoraceae Rhizophoraceae Rhizophoraceae Rhizophoraceae Rhizophoraceae Rubiaceae Verbenaceae Malvacae Malvacae Meliaceae Lythraceae Combretaceae Combretaceae Acrostichaceae Acrostichaceae

Species

Species introduced from Bangladesh since the 1980s. Pollen material from the herbarium of the Kunming Institute of Botany. No pollen illustration, but descriptions from the literature included.

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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 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 Peninsular Malaysia, the Riau Archipelago, Java, and Borneo, to Sulawesi, the Moluccas, and Daru Island and Milne Bay in New Guinea (Othman, 1997). Moreover, pollen of Rhizophora and Sonneratia are major contributors to the organic matter preserved in estuarine and marine deposits (e.g., Muller, 1964; Grindrod, 1988; Grindrod et al., 1999, 2002; Mao et al., 2008; Hait and Behling, 2009; Zhang et al., 2011). Thus, it is necessary to differentiate pollen species of both genera if mangrove successions and the evolution of coastal sedimentary environments are to be reliably interpreted on the basis of palynology. In this paper, we present a pollen and spore “atlas” and key to the mangrove pollen and spores of southern China, and a basis for distinguishing species of Rhizophora and Sonneratia. 2. Mangroves of China Mangroves are distributed along the coast of southeast China in the provinces of Guangdong, Guangxi and Fujian, and on the islands of Hainan and Taiwan, extending intermittently from 18 to 27°N (Lin, 1999). The plants concerned are not a single genetic entity, because the types represented in the tidal zone are not all closely related (Duke, 2006). More than 40 species and their associates (including one species introduced from Bangladesh since the 1980s), representing 21 families and 26 genera have been documented, with thermophilic, eurytopic species being the dominant components (Lin, 1999). A decrease in diversity from 37 to 9 species is evident from Hainan Island (18–22°N) to Fujian (23.5–27°N). The existing mangrove area is about 17,800 ha, accounting for slightly more than 0.1% of the world's total. Regrettably, nearly two-thirds of China's mangroves have been lost during the last 40 years (Li and Lee, 1997), largely because of conversion for rice growing, the creation of embankments for aquaculture ponds, and recently, increasing reclamation for urban development (Fan and Liang, 1995; Wang and Wang, 2007). Tomlinson (1986) defined three groups of mangrove plants: major elements, minor elements and mangrove associates. However, satisfactory criteria upon which to distinguish these have not been clearly established. According to currently available records (Wang and Wang, 2007), Hainan Island has the most extensive area of mangroves (Fig. 1) containing the largest number of species in China (Table 1). A total of 29 species of major and minor mangrove elements (from 16 families) occur in our study area, along with 9 species of mangrove associates from 6 families (Wang and Wang, 2007; Table 1). Major elements are Avicennia marina, Bruguiera spp., Ceriops tagal, Kandelia ovata, Rhizophora spp., Sonneratia spp. Minor elements such as Aegiceras corniculatum, Clerodendron inerme, Pongamia pinnata, Scyphiphora hydrophyllacea and Xylocarpus granatum, and mangrove associates such as Cerbera manghas and Hibiscus tiliaceus are abundant along the seashore, immediately adjacent to terrestrial vegetation (Table 1). 3. Material and methods Thirty-seven samples of pollen and spores were taken from flowers and sporangia collected mainly from the natural reserves of mangrove in Dongzai and Qinglan on the island of Hainan (Fig. 1). One sample of Casuarina equisetifolia was taken from herbarium specimens in the Kunming Institute of Botany (Table 1). Lacking suitable examples of pollen of Acanthus ebracteatus and Dolichandrone spathacea, we have relied on the morphological descriptions of Liu and Tang (1989) and Wei et al. (2001) so that our key covers all of the mangrove taxa in southern China.

All samples were prepared in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, so that the pollen and spores could be examined under both light and scanning electron microscopes (LM and SEM). They were chemically processed according to the method of Erdtman (1969). Each sample was immersed in an acetolysis solution (a mixture of nine parts acetic anhydride and one part sulfuric acid) in a bath of boiling water for 8–10 minutes. After repeatedly washing in de-ionized water until neutral, the residues were mounted on slides with glycerine jelly for observation under a light microscope. Some acetolyzed specimens were dehydrated in an ethanol series and mounted on a stub with adhesive carbon tape, sputter coated with platinum, and examined under a Hitachi S4800 SEM. All pollen and spores were observed and photographed in both polar and equatorial views at a magnification of ×1000 under an Olympus BX51 microscope equipped with an Olympus DP72 camera. Their overall dimensions and other morphological features were measured from photographs using the morphometrics package ImageJ (http://rsb. info.nih.gov/ij/). The values obtained and mentioned in the descriptions of each species are an average of the measurements of at least 20–40 specimens. Both polar and equatorial views are used to illustrate the various morphological features; these are indicated by the abbreviations “P” and “E” respectively with respect to their dimensions in the descriptions. Some of the figures on the plates consist of a combination of two photographs, usually one taken in upper focus and the other showing an optical section. The key below is in two parts: the first is to morphological classes and the second is to characters of the pollen and spores. The former consists of generalized illustrations in the form of graphical icons and class number. The latter comprises class number, brief descriptions of the taxa and plate references. The terminology used follows Punt et al. (2007) and Hesse et al. (2009). Use of this key involves three steps: (1) attribution of the unknown specimen to a particular group of pollen grains or identification as a spore within the “Key to classes”; (2) tentative identification based on the brief descriptions in the “Key to pollen and spores”; (3) confirmation of the identification by comparison with the fuller descriptions provided in the systematic descriptions in Section 5 and the photographs on the plates. To increase the value of the identification guide, we have also added graphical icons of the pollen and spores and an identification code to photographs of flowers, fruits and/or leaves of the plants concerned (see Plate I and Table 1). This should aid field investigations of mangroves. 4. Key to the mangrove pollen and spores There is only one type of spore; hence, we include this with the key to the main morphological classes of pollen. 4.1. Key to classes Grains single, aperturate or inaperturate

Pollen (I–IX)

Inaperturate: grains without apparent apertures

I

Monoporate: grains with only one pore

II

Monocolpate: grains with a single colpus (zonasulcate)

III

L. Mao et al. / Review of Palaeobotany and Palynology 176–177 (2012) 41–67 Grains single, aperturate or inaperturate

Pollen (I–IX)

Triporate: grains with three pores

IV

Tricolpate: grains with three colpi

V

Tricolporate: grains with three colpi within which are usually three pores

VI

Polyporate: grains with more than three pores

VII

Polycolporate: grains with more than three colporate apertures

VIII

Heterocolporate: grains with three colpi and three pores

IX

Grains single, trilete

Spore (X)

Specimens with a trilete suture

X

4.2. Key to pollen and spores I. Inaperturate Echinate, spheroidal, large (mean diameter 91.5 μm) .........................................................Hernandia nymphaeifolia (Plate II, 1) II. Monoporate Microechinate, spheroidal, small (mean diameter 19.2 μm) .................................................................Pandanus tectorius (Plate II, 2) III. Monocolpate/zonasulcate Zonasulcate, echinate tectum, spines longer than 1 μm ...................................................................... Nypa fructicans (Plate II, 3) IV. Triporate 1a. Grains prolate to spheroidal with distinct or indistinct meridional ridge in mesoporium 2 2a. Grains prolate, with distinct mesoporium ridge, pore less than 10 μm in diameter……………….…………………........... 3 3a. Meridional ridges irregularly rugulate, porate fields large, mean length of polar axis 59.5 μm ............……..............………...... Sonneratia alba (Plate III, 2) 3b. Meridional ridges irregularly rugulate, mean length of polar axis 51.8 μm .................S. hainanensis (Plate III, 3) 3c. Meridional ridges variable, usually distorted (twisted), tectum granulate to verrucate over entire grain, mean length of polar axis 41.8 μm ....................................................S. × gulngai (Plate IV, 1) 2b. Grains prolate to spheroidal, with indistinct mesoporium ridge, tectum granulate, elements somewhat larger and less well defined over polar areas, columellate structure indistinct .................................................... S. ovata (Plate IV, 2)

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2c. Grains prolate, no meridional ridges and polar caps psilate........................................................... S. caseolaris (Plate III, 1) 2d. Grains spheroidal, diameter of pore more than 10 μm, tectum sculptured with granules and small verrucae over entire surface of grain….................….. S. apetala (Plate V, 2) 1b. Polar outline triangular, pores crassimarginate, tectum microechinate under SEM……...…Casuarina equisetifolia (Plate V, 1) V. Tricolpate 1a. Large grain (mean 56.6 × 51.5 μm), tectum echinate, surface in between spines microgranulate..………...................................... ...............................….....……..... Clerodendrum inerme (Plate VI, 3) 1b. Small grain (mean 21.1 × 22.7 μm), tectum foveolate to foveoreticulate, wide colpi…................… Premna obtusifolia (Plate VI, 1) 1c. Medium sized grain, tectum foveo-reticulate to reticulate……. .................…Acanthus ilicifolius (mean 41.2 × 31.0 μm) (Plate VI, 2) ..Acanthus ebracteatus (mean 47.3×32.6 μm) (Liu and Tang, 1989) 1d. Tri-syncolpate grain with prominently protruding crassimarginate colpi, coarsely reticulate adjacent to colpi and in subpolar areas …..........................Barringtonia racemosa (Plate VI, 4) 1e. Large grain (mean 55.0 × 48.0 μm), subprolate, tectum reticulate, lumina sub-rounded.......................…………………………… ..................................... Dolichandrone spathacea (Wei et al., 2001) VI. Tricolporate 1a. Pollen grains without endoaperture ............……………………2 2a. Pollen with echinate tectum.……………..…….............. ...............................................…….. Pluchea indica (Plate VII, 4) 2b. Tectum of pollen otherwise sculptured….……..………….3 3a. Pollen with foveolate, foveo-reticulate or reticulate sculpture……....................................................……………..4 4a. Sexine (foveo-) reticulate with granular muri............... ............................................ Avicennia marina (Plate XII, 2) 4b. Sexine foveolate to foveo-reticulate, grains larger than 30 μm .............Excoecaria agallocha (Plate VII, 2) 4c. Sexine foveolate, foveo-reticulate to reticulate, distinctive mesoaperture, pores crassimarginate …..……. Scyphiphora hydrophyllacea (Plate XII, 1) 4d. Sexine finely reticulate, pore small, weakly annulate, slightly elongate at right-angles to colpus, colpi long, extend to polar regions….....…..……… .……………………..….Heritiera littoralis (Plate IX, 1) 3b. Pollen with psilate tectum or with weak or ill-defined sculpture ……………....................................................……5 5a. Pollen larger than 75 μm ………............………. ................................... Cerbera manghas (Plate VIII, 1) 5b. Pollen smaller than 75 μm ……........…..…….……6 6a. Pollen tricolporoidate, small .....................…. ........................... Pongamia pinnata (Plate VII, 3) 6b. Prolate, aperture “cross-shaped” under LM, sculpture finely granulate to mainly rugulate…..... Aegiceras corniculatum (Plate VII, 1) 1b. Pollen grains with equatorially elongated endoaperture …............……………..............................................................…..…….. 7 7a. Pollen grains with continous endoaperture (zonoaperture) .....….….............................................................................….. 8 8a. Prolate to spheroidal, pollen wall distinctly stratified, sexine sculpture mainly foveolate to foveoreticulate……........... Rhizophora apiculata (Plate XI, 1) 8b. Oblate spheroidal, pollen wall less well stratified, sexine scabrate to slightly granulate to irregularly pitted.………………..... Rhizophora stylosa (Plate XI, 2) 8c. Prolate spheroidal, sexine appears to be finely reticulate under LM, but clearly perforated under SEM, endoaperture less distinct…............................................ ...................................................... R. mucronata (Plate XI, 3) 7b. Pollen grains with discontinuous endoaperture in mesocolporium......................................................................................... 9

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9a. Polar axis shorter than 18.5 μm .…..……..………….. 10 10a. Endoaperture indistinct and discontinuous, sexine scabrate to weakly granulate under LM, but seen to be finely foveolate under SEM………… ……………………………Ceriops tagal (Plate IX, 3) 10b. Endoaperture distinct, sexine psilate, scabrate or weakly granulate under LM, scabrate, pitted or finely granulate under SEM....…...……….… 11 11a. Sexine scabrate to weakly granulate under LM, scabrate to pitted under SEM .……..… ................ Bruguiera gymnorrhiza (Plate X, 1) 11b. Sexine psilate to scabrate under LM, scabrate, pitted or finely granulate under SEM.....……Bruguiera sexangula (Plate X, 2) ..................................................................Bruguiera sexangula var. rhynchopetala (Plate X, 3) 9b. Polar axis longer than 18.5 μm, sexine with a rugulate to irregularly foveolate sculpture, endopore often constricted within colporium …………….……………. ............................................... Kandelia obovata (Plate IX, 2) VII. Polyporate 1a. Large grain, echinate, long spines with sharp tips ...................... ....................................................... Thespesia populnea (Plate XIII, 2) 1b. Large grain, echinate, long spines that are constricted just above base and have bluntly rounded tips……....…………... ............................................................Hibiscus tiliaceus (Plate XIII, 1) VIII. Polycolporate 1a. Grains with four or five colpori (tetra- or pentacolporate; more often pentacolporate), colpi shorter than ca. 20 μm...................................... Xylocarpus granatum (Plate XIV, 1) 1b. Grains with four or five colpori (tetra- or pentacolporate; tetracolporate more common), colpi longer than ca. 20 μm………………...…………. Pemphis acidula (Plate XIV, 2) IX. Heterocolporate 1a. Grains small (mean 38.6 × 35.2 μm), but larger than L. racemosa, sexine scabrate to foveolate under LM, more obviously finely pitted/foveolate under SEM…………........…… …......................…………….......Lumnitzera littorea (Plate XV, 2) 1b. Grains small (mean 28.6 × 26.4 μm), smaller than L. littorea, sexine foveo-reticulate, more strongly developed on outer parts of lobes and at the poles.................................... ...............................................… Lumnitzera racemosa (Plate XV, 1) X. Trilete spores 1a. Rounded-triangular in polar view, sculpture of granules and small verrucae of irregular shape, generally slightly larger than those of A. aureum……......…….............…………………. ...............………………..…..Acrostichum speciosum (Plate VIII, 3) 1b. Rounded-triangular in polar view, sculpture of granules and small verrucae of irregular shape, generally slightly smaller than those of A. speciosum…................................................................ ......................................................................... A. aureum (Plate VIII, 2) 5. Descriptions of the mangrove pollen and spores

pore large, subcircular (ca. 6.4 μm in maximum diameter), nexine finely granulate in the colpi under both LM and SEM. Bruguiera (Rhizophoraceae) Bruguiera gymnorrhiza (L.) Savigny (Plate X, 1) Pollen grains oblate to spheroidal, convexly triangular to circular in polar view, 15.6 (17.9) 20.8 × 16.8 (20.1) 22.5 μm, tricolporate; exine ca. 1.3 μm thick, sexine thicker than nexine, sculpture scabrate to weakly granulate under LM, scabrate to pitted under SEM; aperture slightly protruding, vestibulate, endopore within colpus equatorially elongated, dimensions ca. 2.5 × 1.3 μm, length of colpus ca. 12.6 μm. Bruguiera sexangula (Lour.) Poir (Plate X, 2) Pollen grains oblate to spheroidal, convexly triangular to circular in polar view, 14.9 (16.5) 19.9 × 15.7 (20.3) 21.4 μm, tricolporate; exine ca. 1.2 μm thick, sexine thicker than nexine, tectum psilate to scabrate under LM, scabrate to pitted under SEM; aperture vestibulate, endopore within colpus very slightly elongated equatorially, dimensions ca. 2.1 × 2.0 μm, length of colpus ca. 10.6 μm. Bruguiera sexangula var. rhynchopetala W.C. Ko (Plate X, 3) Pollen grains oblate to spheroidal, rounded triangular to subcircular in polar view, 15.2 (16.4) 19.8 × 16.2 (17.5) 20.6 μm, tricolporate; exine ca. 1.1 μm thick, sexine thicker than nexine, psilate to scabrate under LM, scabrate to finely granulate under SEM; aperture vestibulate, endopore within colpus equatorially elongated, dimensions ca. 2.1 × 1.7 μm, length of colpus ca. 9.5 μm. Ceriops (Rhizophoraceae) Ceriops tagal (Perr.) C.B. Rob. (Plate IX, 3) Pollen grains oblate to subspheroidal, rounded triangular to subcircular in polar view, 13.5 (14.9) 16.2 × 12.6 (13.3) 14.5 μm, tricolporate; exine ca. 1.2 μm thick, sexine thicker than nexine, sexine scabrate to weakly granulate under LM, but seen to be finely perforated under SEM; aperture vestibulate, endopore equatorially elongated and discontinuous in mesocolporium, dimensions ca. 1.6 × 1.2 μm, length of colpus ca. 9.9 μm. Kandelia (Rhizophoraceae) Kandelia obovata Sheue, Liu and Yong (Plate IX, 2) Pollen grains subprolate to spheroidal, subcircular in polar view, 17.2 (21.5) 25.3 × 16.7 (18.2) 21.5 μm, tricolporate; exine ca. 1 μm thick, tectum perforate, sexine thicker than nexine with a rugulate to irregularly foveolate sculpture, but margins of colpi usually psilate; aperture vestibulate, endopore equatorially elongated, dimensions ca. 3.1 × 2.3 μm, often constricted within colporium, length of colpus ca. 14.1 μm. Rhizophora (Rhizophoraceae)

5.1. Major elements Avicennia (Verbenaceae/Avicenniaceae/Acanthaceae) (The Angiosperm Phylogeny Group, 2009) Avicennia marina (Forsk.) Vierh. (Plate XII, 2) Pollen grain tricolporate, subprolate to spheroidal in equatorial view, subcircular in polar view, 23.6 (25.5) 34.8 × 24.2 (28.8) 35.3 μm; exine ca. 3.0 μm thick, sexine thicker than nexine, sculpture appears reticulate with granular muri under LM, but surface of tectum is seen to be more foveolate under SEM; colpi extend to polar regions,

Rhizophora apiculata Bl. (Plate XI, 1) Pollen grains spherical to subspherical, 20.0 (24.4) 28.0 × 19.6 (22.6) 27.8 μm, mostly tricolporate, sometimes tetracolporate; exine ca. 2.2 μm thick, sexine thicker than nexine, sculpture microreticulate to microrugulate under LM, appears more varied under SEM with three main types: perforate, rugulate and reticulate (Mao et al., 2008), but usually perforated to (irregularly) perforate–reticulate; aperture vestibulate with equatorially elongated endoaperture, dimensions ca. 2.4 × 1.4 μm, length of colpus ca. 12.6 μm with finely rugulate membrane.

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Plate I. Photographs of flowers, fruits or leaves with identification codes (bottom right-hand side; see Table 1 for names) and graphical icons (bottom left-hand side) pertaining to the key to classes of the associated pollen and spores.

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Plate II. Inaperture, monoporate and monocolpate/zonasulcate pollen. 1. 2. 3.

Hernandia nymphaeifolia. 1, upper focus showing echinate sculpture; 1-1, 1-2, echinate tectum under SEM. Pandanus tectorius. 2, upper focus showing echinate sculpture; 2-1, optical section showing exine structure; 2-2, echinate tectum under SEM. Nypa fructicans. 3, optical section showing exine structure; 3-1, upper focus showing echinate sculpture; 3-2, echinate tectum under SEM.

Rhizophora stylosa Griff. (Plate XI, 2) Pollen grains subprolate, circular to subcircular in polar view, 19.9 (20.5) 22.7 × 21.3 (22.4) 24.7 μm, tricolporate; exine ca. 1.5 μm thick, sexine thicker than nexine, scabrate to slightly granulate under LM, scabrate to slightly granulate to irregularly pitted under SEM; aperture vestibulate, endopore equatorially

elongated, dimensions ca. 3.1 × 1.6 μm, length of colpus ca. 13.4 μm. Rhizophora mucronata Lamk. (Plate XI, 3) Pollen grains subprolate to spheroidal, outline in polar view subcircular or rounded-triangular, 18.7 (23.8) 26.8×16.6 (20.4)

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Plate III. Triporate pollen (see also Plates IV and V). 1. 2. 3.

Sonneratia caseolaris. 1, equatorial view showing distinct optical section of polar cap and abrupt discontinuity adjacent to equatorial field, with view of sculpture of equatorial region and pore inset; 1-1, 1-2, polar view showing rounded-triangular shape and protruding apertures; 1-3, psilate polar cap under SEM. Sonneratia alba. 2, equatorial view showing distinct meridional ridge; 2-1, optical section. 2-2, polar view showing hexagonal outline with view of polar surface inset; 2-3, psilate polar cap under SEM; 2-4, distinct meridional ridge under SEM. Sonneratia hainanensis. 3, 3-1, polar view in high and mid focus showing hexagonal outline; 3-2, equatorial view showing distinct meridional ridge; 3-3, optical section; 3-4, distinct meridional ridge under SEM.

24.4 μm, tricolporate; exine ca. 1.4 μm thick, sexine thicker than nexine, surface appears to be finely reticulate under LM, but clearly perforated under SEM, perforations less numerous over poles and around equator; aperture vestibulate, endopore equatorially elongated, dimensions ca. 3.0 × 2.1 μm, length of colpus ca. 15.8 μm.

Nypa (Palmae) Nypa fruticans Wurmb. (Plate II, 3) Pollen grains spheroidal, 44.3 (51.5) 56.1 × 36.5 (46.9) 54.3 μm, monocolpate (zonasulcate/annulocolpate); exine ca. 2.5 μm thick,

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Plate IV. Triporate pollen (see also Plates III and V). 1. 2.

Sonneratia × gulngai. 1, 1-1, equatorial views showing distorted meridional ridge (variation subtype); 1-2, optical section; 1-3, polar view showing hexagonal outline with protruding apertures, polar surface inset; 1-4, equatorial view showing granulate to verrucate tectum and meridional ridge under SEM. Sonneratia ovata. 2, equatorial view showing indistinct meridional ridge; 2-1, 2-2, optical sections with surface views inset, exine thicker in polar cap than in equatorial field; 2-3, 2-4, polar and equatorial views under SEM showing hexagonal and elliptical outlines respectively.

sexine thicker than nexine, echinate, spines ca. 3.6 μm high, widening significantly and commonly appearing somewhat swollen close to their base, ca. 3.4 μm apart; surface of tectum between spines foveolate; mean width of colpus 3.9 μm. Sonneratia (Sonneratiaceae)

Sonneratia caseolaris (L.) Engler (Plate III, 1) Pollen grains prolate in equatorial view, triangular in polar view, 40.8 (52.2) 64.6 × 31.5 (41.2) 49.9 μm, average ratio of P/E, 1.27, triporate; exine thickness varies, structurally discontinuous between equatorial and polar regions, thinnest at poles (ca. 2.1 μm), thickest at equator (ca. 2.5 μm); sexine in polar regions (over polar cap) has

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Plate V. Triporate pollen (see also Plates III and IV). 1. 2.

Casuarina equisetifolia. 1, 1-3, 1-5, upper focus of polar and equatorial views, sexine appears granulate; 1-1, 1-4, vestibulate aperture and crassimarginate pores; 1-2, sculpture is revealed to be microechinate under SEM. Sonneratia apetala. 2, 2-1, optical section and upper focus inset in polar and equatorial views showing exine construction and sculpture; 2-2, equatorial view under SEM showing sculpture of densely distributed granules and small verrucae.

a smooth surface but is granulate to verrucate elsewhere (dimensions 0.3–1.2 μm), with a mean density 1.6 elements/μm 2; pore circular to subcircular, prominently protruding, ca. 7.8 μm in diameter. Sonneratia alba J. Smith (Plate III, 2) Pollen grains prolate in equatorial view, more or less hexagonal in polar view, 51.9 (59.5) 68.8 × 32.1 (44.3) 50.7 μm, average ratio of P/E,

1.35, with distinct meridional ridges extending to polar areas, triporate; exine ca. 2.4 μm thick, sexine thicker than nexine, psilate except for scattered perforations in polar areas, irregularly granulate to verrucate in mesoporial areas with a tendency towards rugulae on meridional ridges (dimensions 0.4–1.4 μm), mean density 1.9 elements/μm 2; pore circular to subcircular, protruding, ca. 9.5 μm in diameter.

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Sonneratia hainanensis W.C. Ko et al. (Plate III, 3) Pollen grains prolate in equatorial view, sub-hexagonal in polar view, 42.9 (51.8) 62.7 × 28.96 (36.6) 47.4 μm, average ratio of P/E, 1.43, with distinct meridional ridges extending to polar area, triporate; exine ca. 3.4 μm thick, sexine thicker than nexine, granulate in mesoporial areas (0.2–1.0 μm), mean density 3.18 granules/μm 2, but elements somewhat larger and more rugulate on meridional ridges; tectum in polar areas psilate apart from a few irregular perforations; pore circular to subcircular, distinctly protruding, ca. 7.7 μm in diameter. Sonneratia × gulngai N.C. Duke (Plate IV, 1) Pollen grains prolate in equatorial view, sub-hexagonal in polar view, 29.3 (41.8) 50.7 × 28.5 (34.3) 41.0 μm, average ratio of P/E, 1.22, with a variable meridional ridge (usually twisted), triporate; exine ca. 2.6 μm thick, sexine thicker than nexine, sculpture of mesoporial areas granulate to verrucate (0.7–2.3 μm), elements closely spaced, larger than in other species of Sonneratia, with the lowest mean density of 0.9 elements/μm 2, somewhat more rugulate over meridional ridge and less well developed over the poles; pore circular to subcircular, protruding, ca. 6.8 μm in diameter. Sonneratia ovata Backer (Plate IV, 2) Pollen grains prolate in equatorial view, convexly triangular to sub-hexagonal in polar view, 34.2 (43.2) 48.8 × 26.5 (34.1) 38.9 μm, average ratio of P/E, 1.29, meridional ridge weakly developed or absent, triporate; exine ca. 2.3 μm thick, sexine thicker than nexine, sculptured with granules in mesoporial areas (0.1–0.9 μm), elements smaller than in other species of Sonneratia, with the highest mean density of 7.8 granules/μm 2, elements somewhat larger and less well defined in polar areas where the cap is perforated; pore circular, protruding, ca. 5.9 μm in diameter. Sonneratia apetala Buch.-Ham. (Plate V, 2) Pollen grains spheroidal in equatorial view, convexly triangular to weakly sub-hexagonal in polar view, 35.9 (46.8) 53.4×32.1 (44.6) 53.3 μm, average ratio of P/E, 1.05, meridional ridge may be faintly discernible, triporate; exine ca. 2.8 μm thick, sexine slightly thicker than nexine, sculptured with densely distributed granules and small verrucae (0.2–1.3 μm; mean density 1.9 elements/μm2) in both mesoporial and polar areas with no clear distinction between the two regions; pores circular, prominently protruding, ca. 11.9 μm in diameter (the largest of all pollen of species of Sonneratia). Lumnitzera (Combretaceae) Lumnitzera racemosa Willd. (Plate XV, 1) Pollen grains subprolate to spheroidal, polar outline subcircularlobate, 26.3 (28.6) 31.6 × 19.3 (26.4) 29.7 μm, heterocolporate (pseudocolpate); exine ca. 2.7 μm thick, sexine thicker than nexine, finely reticulate in equatorial regions, reticulation more strongly developed at the poles under LM, but under SEM the tectum appears more foveolate, fovea larger on the outer parts of the lobes and at the poles; pores within three colpi sub-rectangular, ca. 5.8 × 5.4 μm, both colpi and pseudocolpi (non-functioning “false” colpi) ca. 17.4 μm long. Lumnitzera littorea (Jack) Voigt (Plate XV, 2) Pollen grains subprolate to spheroidal, polar outline subcircularlobate, 35.2 (38.6) 42.6 × 25.8 (35.2) 39.4 μm, heterocolporate (pseudocolpate); exine ca. 2.9 μm thick, sexine and nexine similar in thickness, tectum scabrate to foveolate under LM, more obviously finely pitted/foveolate under SEM; pores within three colpi rectangular, with long axis parallel to the equator, ca. 7.0 × 2.1 μm, both colpi and pseudocolpi (non-functioning “false” colpi) ca. 15.5 μm long.

5.2. Minor elements Aegiceras (Myrsinaceae) Aegiceras corniculatum (Linn.) Blanco (Plate VII, 1) Pollen grains prolate, rounded-triangular in polar view, 18.9 (21.7) 24.7 × 16.5 (17.1) 20.9 μm, tricolporate; exine ca. 1.2 μm thick, sexine thicker than nexine, sculpture finely granular to mainly rugulate; aperture under LM appears cross-shaped because the endoaperture within the colpus is elongated at right-angles to it, ca. 2.3 × 1.9 μm, colpus ca. 16.4 μm long. Clerodendrum (Verbenaceae) Clerodendrum inerme (Linn.) Gaertn. (Plate VI, 3) Pollen grains oblate to subprolate, circular in polar view, 55.3 (56.6) 70.1×45.1 (51.5) 65.5 μm, tricolpate; exine ca. 2.3 μm thick, sexine thicker than nexine, tectum echinate, spines ca. 1.3 μm long, widely and fairly evenly spaced (ca. 4.4 μm apart), surface in between microgranulate under LM; colpi ca. 34.8 μm long, membrane granular with echinae seen under SEM. Excoecaria (Euphorbiaceae) Excoecaria agallocha Linn. (Plate VII, 2) Pollen grains subprolate to spheroidal, circular in polar view, 31.1 (35.6) 41.6 × 30.4 (33.9) 36.9 μm, tricolporate; exine ca. 2.4 μm thick, sexine thicker than nexine, tectum foveolate in polar areas, more foveo-reticulate elsewhere; aperture vestibulate, endopore subcircular to oval, ca. 2.3 μm in diameter, colpi with irregularly granular membrane, ca. 14.5 μm long. Dolichandrone (Bignoniaceae) Dolichandrone spathacea (Linn.) K. Schum. Pollen grains subprolate, circular in polar view, 40.0 (55.0) 65.0 × 38.1 (48.0) 52.0 μm, tricolpate; exine ca. 4.5 μm thick, tectum reticulate, lumina subrounded and distributed evenly over the whole of the tectum; colpi ca. 22.3 μm long (Wei et al., 2001). Hernandia (Hernandiaceae) Hernandia nymphaeifolia (Presl) Kubitzki (Plate II, 1) Pollen grains spheroidal, inaperturate, 56.4 (91.5) 106.3 μm; exine ca. 1.8 μm thick, sexine slightly thicker than nexine, tectum echinate, spines ca. 4.3 μm apart, ca. 3.3 μm long, psilate with bases ca. 2.6 μm wide, commonly somewhat bulbous, rapidly narrowing to a pointed tip; tectum in between spines appears to be more or less smooth under LM but is seen to be microgranulate under SEM. Heritiera (Sterculiaceae) Heritiera littoralis Dryand. (Plate IX, 1) Pollen grains prolate, 19.8 (24.3) 26.9 × 20.6 (21.6) 24.5 μm, tricolporate; exine ca. 1.5 μm thick, sexine thicker than nexine, finely reticulate; pore small, weakly annulate, slightly elongate at right-angles to colpus (maximum diameter ca. 1.9 μm), colpus ca. 13.1 μm long. Casuarina (Casuarinaceae) Casuarina equisetifolia Linn. (Plate V, 1) Pollen grains oblate to spheroidal, rounded triangular in polar view, 21.5 (25.3) 28.6 × 24.6 (30.1) 34.9 μm, triporate or tetraporate

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Plate VI. Tricolpate pollen. 1. 2. 3. 4.

Premna obtusifolia. 1, 1-1, equatorial and polar views showing foveo-reticulate sculpture and wide colpi; 1-2, 1-3, sculpture seen to be foveolate at poles and foveoreticulate elsewhere under SEM. Acanthus ilicifolius. 2, 2-1, equatorial and polar views in optical section with upper focus levels showing apparently reticulate sexine under LM and a long colpus; 2-2, 2-3, tectum is seen to be foveo-reticulate under SEM. Clerodendrum inerme. 3, optical section and mid-focus in equatorial view; 3-1, high focus of oblique polar view; 3-2, showing echinate tectum under SEM, spines widely and fairly evenly spaced, surface in between perforated-microreticulate. Barringtonia racemosa. 4, upper focus of this syntricolpate grain in equatorial view; 4-1, 4-2, different focus levels showing optical sections, crassimarginate colpi and coarsely reticulate sculpture adjacent to them and in subpolar areas; 4-3, showing under SEM syncolpate form, coarsely reticulate sculpture adjacent to strongly crassimarginate colpi and in subpolar areas, and scabrate to psilate tectum elsewhere.

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Plate VII. Tricolporate pollen (see also Plates VIII–XII). 1. 2.

3. 4.

Aegiceras corniculatum. 1, 1-1, optical sections in polar and equatorial views, with inset showing surface sculpture; 1-2, upper focus showing “cross-shaped” aperture; 1-3, 1-4, equatorial and oblique polar views showing colporate aperture and finely granulate to mainly rugulate sculpture under SEM. Excoecaria agallocha. 2, 2-1, optical sections and parts in upper focus in polar and equatorial views; 2-2, 2-4, specimens in equatorial and slightly oblique polar views under SEM showing apertures and foveolate tectum in polar areas, more foveo-reticulate elsewhere; 2-3, upper focus of specimen in oblique equatorial view showing colporate aperture. Pongamia pinnata. 3, 3-1, polar and equatorial views, sexine in upper focus appears faintly microreticulate; 3-2, oblique polar view showing membrane in colpus; 3-3, 3-4, sexine is seen to be irregularly verrucate to rugulate and pitted under SEM. Pluchea indica. 4, 4-1, showing echinate tectum under LM and SEM; 4-2, detail of uneven, perforated tectum and spines under SEM.

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Plate VIII. Tricolporate pollen (see also Plates VII and IX–XII) and trilete spores. 1. 2. 3.

Cerbera manghas. 1, 1-3, upper focus in polar and equatorial views showing weakly sculptured tectum and apertures; 1-1, optical section in polar view; 1-2, 1-4, 1-5, equatorial, polar and equatorial views respectively showing apertures and irregular, finely rugulate to microreticulate sculpture under SEM. Acrostichum aureum. 2, 2-1, trilete spore in distal and proximal views; 2-2, showing granulate to verrucate sculpture, verrucae somewhat irregular in shape and size under SEM. Acrostichum speciosum. 3, 3-1, 3-2, proximal, distal and mid-focus views respectively showing sculpture and optical section; 3-3, showing sculpture of irregularly shaped granules and small verrucae under SEM.

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(triporate more common); exine ca. 1.5 μm thick, sexine thicker than nexine, appears finely granulate under LM but microechinate under SEM; aperture somewhat protruding, vestibulate, pores crassimarginate, thickness of sexine around pore ca. 4.5 μm, pore circular to subcircular, ca. 3.0 μm in diameter. Pemphis (Lythraceae) Pemphis acidula Forest (Plate XIV, 2) Pollen grains prolate to spheroidal, circular in polar view, 40.1 (42.1) 45.7 μm, tetra- or pentacolporate (tetracolporate more common); exine ca. 1.3 μm thick, sexine slightly thicker than nexine, tectum psilate but finely pitted; nexine of colpi microgranulate, pore subcircular, ca. 5.6 μm in diameter, colpi ca. 29.1 μm long. Pluchea (Compositae) Pluchea indica (Linn.) Less. (Plate VII, 4) Pollen grains spheroidal, 17.2 (18.9) 20.5×8.5 (19.1) 22.6 μm, tricolporate; exine ca. 2.5 μm thick, sexine slightly thicker than nexine; uneven tectum echinate and perforated, spines closely spaced, essentially conical, ca. 1.5 μm wide at base and ca. 2.1 μm high; pore circular, ca. 1.7 μm in diameter; colpus comparatively short, ca. 8.3 μm in length. Pongamia (Leguminosae/Fabaceae) Pongamia pinnata (Linn.) Pierre (Plate VII, 3) Pollen grains suboblate to subprolate in equatorial view, circular to convexly triangular in polar view, 16.2 (18.8) 25.6 × 19.2 (21.3) 27.5 μm, tricolporoidate; exine ca. 1.5 μm thick, sexine thicker than nexine, appears faintly reticulate to somewhat rugulate under LM, but irregularly verrucate to rugulate and pitted under SEM; pore circular to subcircular, ca. 3.7 μm in diameter, colpus with microgranulate membrane (nexine), ca. 13.6 μm long. Premna (Verbenaceae) Premna obtusifolia R.Br. (Plate VI, 1) Pollen grains prolate to spheroidal, circular to somewhat lobate in polar view, 18.5 (21.1) 22.2 ×18.4 (22.7) 24.7 μm, tricolpate; exine ca. 2.2 μm thick, sexine thicker than nexine, surface foveolate at poles, foveo-reticulate elsewhere, colpi wide, ca. 2.1 μm at equator, extend to polar areas, membrane (nexine) with a scabrate surface, ca. 13.5 μm long. Scyphiphora (Rubiaceae) Scyphiphora hydrophyllacea Gaertn. (Plate XII, 1) Pollen grains spheroidal, 20.5 (25.2) 29.5 × 23.2 (24.6) 30.8 μm, tricolporate; exine ca. 1.3 μm thick, sexine thinner than nexine, tectum foveolate over poles, foveo-reticulate to reticulate elsewhere; pore circular, crassimarginate, ca. 5.9 μm in diameter, with a mesoaperture in centre of endoaperture, colpi extend to polar areas, ca. 22.1 μm long. (This pollen type is distinguished by the presence of a mesoaperture; Chumchim, 2011). Xylocarpus (Meliaceae) Xylocarpus granatum Koenig (Plate XIV, 1) Pollen grains spheroidal to slightly oblate, quadrangular to polygonal in polar view (more often polygonal), 33.3 (36.1) 39.6 × 35.6 (39.2) 44.2 μm, polycolporate (tetra- or pentacolporate; pentacolporate more common); exine ca. 1.8 μm thick, sexine thicker than nexine, tectum scabrate to microgranulate; pore circular, crassimarginate, wider than width of colpus, ca. 6.5 μm in diameter, colpus short, ca. 15.4 μm in length.

5.3. Mangrove associates Acanthus (Acanthaceae) Acanthus ilicifolius Linn. (Plate VI, 2) Pollen grains prolate, subcircular and slightly lobate to roundedtriangular in polar view, 36.0 (41.2) 54.3 × 26.3 (31.0) 35.2 μm, tricolpate; exine ca. 2.5 μm thick, sexine thicker than nexine, appears to be reticulate under LM but foveo-reticulate under SEM; colpi long, extend to the poles and are almost the same length as the grain. Acanthus ebracteatus Vahl. Pollen grains prolate, 31.5 (38.3) 41.1 × 21.4 (25.2) 30.3 μm, tricolpate; exine ca. 2.5 μm thick, sexine thicker than nexine, finely reticulate, colpi long, extend to the poles. (After Liu and Tang, 1989) Acrostichum (Acrostichaceae) Acrostichum aureum Linn. (Plate VIII, 2) Trilete spores, rounded-triangular in polar view, 49.0 (53.6) 73.5× 64.1 (70.2) 83.1 μm (the length of side × diameter through arm of the trilete suture); exine ca. 3.9 μm thick, sexine thicker than nexine, granulate to verrucate sculpture under LM, granules and small verrucae seen to be somewhat irregular in shape and size under SEM. Acrostichum speciosum Willd. (Plate VIII, 3) Triradiate spores, rounded-triangular in polar view, 42.0 (51.3) 57.5×49.0(60.5)70.5 μm, exine ca. 3.0 μm thick, sexine thicker than nexine, sculpture consists of irregularly shaped granules and small verrucae. Barringtonia (Barringtoniaceae) Barringtonia racemosa (L.) Blume ex DC (Plate VI, 4) Pollen grains prolate, outline circular in polar view, 53.2 (64.2) 70.8× 40.9 (44.6) 46.4 μm, tricolpate (tri-syncolpate); exine ca. 2.2 μm thick, sexine and nexine of similar thickness, coarsely reticulate adjacent to colpi and in subpolar areas, scabrate to psilate elsewhere; colpi strongly crassimarginate, especially in polar regions, ca. 53.4 μm long. Cerbera (Apocynaceae) Cerbera manghas Linn. (Plate VIII, 1) Pollen grains subprolate to spheroidal, circular to subcircular in polar view, 80.2 (85.3) 95.8 × 74.9 (78.6) 82.8) μm, tricolporate; exine ca. 1.81 μm thick, sexine thicker than nexine, irregular finely rugulate to microreticulate sculpture; colpi slightly crassimarginate, ca. 55.1 μm long, with a granular membrane and two oval pores within each, one above and one below the equator, oval pores ca. 10–10.4× 6.2–6.7 μm. Hibiscus (Malvaceae) Hibiscus tiliaceus Linn. (Plate XIII, 1) Pollen grains spheroidal, 104.2 (130.5) 185.9 μm in diameter, polyporate (pantoporate); exine ca. 5.6 μm thick, sexine thicker than nexine, prominent spines scattered over surface of tectum, ca. 19.6 μm in length and widely spaced, ca. 19.7 μm apart; spines psilate, elongate-cone shaped, may be slightly bulbous towards the base before becoming constricted, beneath which the perforated tectum is slightly raised; tectum surface also sculptured with scattered granules; pores ca. 13.6 μm in diameter. Pandanus (Pandanaceae) Pandanus tectorius Sol. (Plate II, 2) Pollen grains ovate-spheroidal, 15.9 (19.1) 22.4 μm in maximum diameter, monoporate; exine ca 1.3 μm thick; tectum microechinate,

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Plate IX. Tricolporate pollen (see also Plates VII, VIII and X–XII). 1.

2.

3.

Heritiera littoralis. 1, optical section of specimen in oblique polar orientation showing exine stratification, with high focus inset showing reticulate sexine; 1-1, upper focus of equatorial view showing finely reticulate sexine, long colpi and small pore slightly elongate at right-angles to colpus; 1-2, equatorial view of optical section showing wall layers, thin endexine and weakly annulate pore. Kandelia obovata. 2, 2-1, equatorial views in upper focus showing rugulate to irregularly foveolate sculpture and equatorially elongated pore with constriction structure; 2-2, 2-4, 2-5, showing rugulate to irregularly foveolate sculpture under SEM, margins of colpi in 2-4 unornamented; 2-3, optical section in polar view, with inset showing polar surface. Ceriops tagal. 3, 3-1, upper focus of specimen in equatorial view and optical section in polar view; 3-2, 3-3, showing perforated tectum under SEM.

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Plate X. Tricolporate pollen (see also Plates VII–IX, XI and XII). 1.

2. 3.

Bruguiera gymnorhiza. 1, 1-1, upper focus and optical section of specimen in equatorial view; 1-2, upper focus of equatorial view showing an equatorially elongate endopore; 1-3, equatorial view showing scabrate to pitted sexine under SEM; 1-4, optical section in polar view showing slightly protruding, vestibulate apertures; 1-5, oblique polar view under SEM showing one colporate aperture clearly and scabrate tectum. Bruguiera sexangula. 2, 2-1, upper focus and optical section of specimen in polar view; 2-2, 2-3, upper and mid focus equatorial views; 2-4, showing equatorially elongate endopore; 2-5, 2-6, equatorial and polar views showing apertures and scabrate to pitted tectum under SEM. Bruguiera sexangula var. rhynchopetala. 3, 3.1, upper focus and optical section of specimen in polar view; 3-2, 3-5, 3-6, equatorial, polar and equatorial views respectively showing apertures and scabrate to finely granulate sexine under SEM; 3-3, equatorial view in mid focus; 3-4, equatorial view in upper focus showing equatorially elongate endopore.

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Plate XI. Tricolporate pollen (see also Plates VII–X and XII). 1.

2.

3.

Rhizophora apiculata. 1, 1-1, showing distinct equatorially elongated endoaperture (zonoaperture) with vestibulum (stratified wall is thicker than in R. stylosa and R. mucronata); 1-2, 1-3, high focus and optical section in polar view; 1-4, tetracolporate specimen in mid focus; 1-5, 1-6, specimens in equatorial view showing apertures and irregular foveolate to foveo-reticulate sculpture under SEM; 1-7, specimen in polar view showing apertures and foveo-reticulate sexine under SEM. Rhizophora stylosa. 2, 2-1, high and mid focus of specimen showing distinct equatorially elongated endoaperture (zonoaperture) and vestibulum; 2-2, 2-3, equatorial and oblique polar views showing scabrate to slightly granulate and irregularly pitted sexine under SEM; 2-4, showing “bow-tie-like” aperture; 2-5, 2-6, showing polar views in high focus and optical section; stratification of exine not as distinct as in pollen of R. apiculata. Rhizophora mucronata. optical section in polar view; 3-1, 3-2, high focus and optical section in equatorial view showing less distinct endoaperture and vestibulum by comparison with R. apiculata and R. stylosa; 3-3, 3-4, equatorial and polar views showing perforated tectum under SEM; perforations less numerous over poles and around the equator.

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Plate XII. Tricolporate pollen (see also Plates VII–IX). 1.

2.

Scyphiphora hydrophyllacea. 1, optical section and upper focus inset in equatorial view showing wall structure, crassimarginate pore and foveo-reticulate to reticulate tectum; 1-1, lower focus of equatorial view showing mesoaperture (arrow) and endoaperture (enclosing dashed line); 1-3, 1-4, high focus and optical section in polar view showing wall structure and foveo-reticulate to reticulate tectum; 1-2, 1-5, equatorial and polar views under SEM showing apertures and a tectum that is foveolate over poles and foveo-reticulate to reticulate elsewhere. Avicennia marina. 2, 2-1, 2-3, 2-4, high focus and optical section in polar and equatorial views respectively showing wall structure, and a reticulate sexine with granular muri and large pores; 2-2, 2-5, oblique polar and equatorial views showing colporate apertures and a tectum that is seen to be more foveolate under SEM.

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but in between spines surface appears scabrate under LM; spines ca. 1.0 μm in height; pore ca. 4.2 μm in diameter. Thespesia (Malvaceae) Thespesia populnea (L.) Soland. ex Correa (Plate XIII, 2) Pollen grains spheroidal 74.9 (92.6) 101.3 μm in maximum diameter, polyporate (pantoporate); exine ca. 3.6 μm thick, sexine thicker than nexine, tectum spinose, base of spines consists of raised up perforated tectum bearing scattered granules above which they are essentially psilate to their pointed tips, ca. 11.2 μm in length and ca. 10.6 μm apart; in common with the bases of the spines the tectum between them is perforated and with a granular sculpture; pore ca. 12.5 μm in diameter. 6. Notes on Rhizophoraceae and Sonneratia pollen 6.1. Rhizophoraceae Pollen grains of plants in this family are tri- or tetracolporate, zonorate, oblate spheroidal to subprolate with, according to Erdtman (1969), a finely reticulate sexine that is thinner than, or as thick as, the nexine. Thanikaimoni (1987) described the ectoaperture as long, usually constricted at the equator, and with a wide endoaperture beneath that is perpendicular to the ectoaperture and has irregular lateral borders. Silva and Santos (2009) confirmed that Rhizophora harrisonii, R. mangle and R. racemosa share the characters observed by Erdtman (1969) and Thanikaimoni (1987), except that they found the sexine to be thicker than the nexine in all specimens, and that there was no constriction in the ectoapertural region. They also pointed out qualitative differences between the Rhizophora pollen they examined. According to our observations, the endoaperture of Kandelia pollen is constricted within the colpus. Generally, the four Rhizophoracean genera, Bruguiera, Ceriops, Kandelia and Rhizophora, have the following morphological features in common: subprolate–oblate spheroidal shape, tricolporate apertures with an equatorially elongated endoaperture, and a sexine that ranges from psilate to finely reticulate. Yamanoi (2003) keyed out pollen grains produced by these mangrove taxa to genus level based on equatorial views. The polar axis of the pollen of Bruguiera gymnorrhiza varies from 15 to 18 μm according to him, and the sexine of most grains is faintly and irregularly granulate. The pollen of B. sexangula is somewhat larger (17 b P b 20 μm) than that of B. gymnorriza and B. cylindrica (Pb 15 μm), and the sexine is psilate to scabrate. Grain size varies interspecifically and may even vary within a species. Some biotic and abiotic factors may also lead to questionable or anomalous size measurements. However, Bruguiera pollen grains are uniformly very small and differences between species of the genus are indistinct. It is, therefore, difficult to distinguish dispersed Quaternary pollen grains attributed to Bruguiera, although we have referred its pollen to two groups in the pollen keys. Ceriops pollen grains are the smallest in the Rhizophoraceae family. Their endoapertures are indistinct and discontinuous at the equator, and the sexine is scabrate to weakly granulate and finely perforated. However, their morphology overlaps that of Bruguiera pollen to some extent. It is necessary to examine specimens at high power under an oil-emersion objective in order to distinguish them. Kandelia pollen grains are a little larger than those of Bruguiera and Ceriops; coupled with the constricted structure within the colporium noted above, it is possible to distinguish these from the pollen of other genera within the family. The morphology of Rhizophora pollen has received particular attention because of the evolutionary importance of the parent plants and their palaeogeographic distribution (e.g., Muller and Caratini, 1977; Ellison et al., 1999; Plaziat et al., 2001). Muller and Caratini (1977) reported detailed observations on the morphology of the pollen of six

Fig. 2. Comparison of the size of pollen of six species of Sonneratia. Sonneratia alba has the largest mean size, S. ovata and S. × gulngai the smallest; the mean size of S. apetala shows the closest relationship between polar and equatorial lengths because it is spheroidal in equatorial view. These size differences coupled with the presence or absence of a meridional ridge, variations in the stratification of the polar cap, and the sculptural elements of the sexine are all diagnostic characters.

species of Rhizophora and reviewed fossil records and possible affinities. They also commented on the wide variation in the shape of the pollen and a variable degree of fusion of the endoapertures, which may be relatively short with an irregular termination or completely fused to form an annular zone. Based on a limited number of diagnostic criteria, they differentiated three groups: A, R. mucronata and R. stylosa; B, R. apiculata, R. lamarckii and R. mangle; and C, R. racemosa. This grouping is quite close to ours. R. apiculata can be readily distinguished from R. stylosa and R. mucronata on the basis of its distinctly stratified exine (Plate XI, 1-1) and perforate to perforate–reticulate sculpture over the whole of the surface of pollen grain (Plate XI, 1, 12, 1-5–1-7). However, there is some morphological overlap between R. mucronata and R. stylosa, and our observations agree with those reported previously (Muller and Caratini, 1977; Yamanoi, 2003). Arguably they could be varieties of the same species, but this does not find support in their estuarine distributions in Australia, which do not overlap (Duke, 2006).

6.2. Sonneratia Studies under light and scanning electron microscopes of pollen from five species of Sonneratia were reported by Muller (1969, 1978), who outlined the main differences between normally developed grains. He showed that only in the pollen of S. apetala is the tectum continuous over the entire grain; the polar caps of S. caseolaris pollen show no distinct structure and a meridional ridge is generally absent; and the pollen grains of S. alba have a distinct meridional ridge and are larger than in other species of the genus. Yamanoi (2003) considered that S. alba and S. caseolaris can be differentiated on the basis of the presence or absence of a meridional ridge. Our observations on these three species tie in well with these diagnostic criteria. However, there is some morphological overlap between S. hainanensis, S. alba and S. × gulngai, which causes identification problems. Putative hybrids and variations among Sonneratia species have been documented in south-east Asia (Muller and Hou-Liu, 1966) and Australia (Duke, 1988, 1994), and Muller (1969) reported many subtypes of Sonneratia pollen showing morphological variations. In this study we measured 40 grains for each species of Sonneratia and encountered a wide range in size (Fig. 2), so the characteristics of the tectum, sexine, polar cap and meridional ridge must be regarded as more important than size for distinguishing these pollen types. Mao et al. (2009) recently discussed some subtypes of the pollen of S. × gulngai and grouped six species of Sonneratia pollen into four

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Plate XIII. Polyporate pollen. 1.

2.

Hibiscus tiliaceus. 1, 1-3, composite image of specimen in upper and mid focus showing spinose tectum and granulate sexine, and close-up of aperture, exine and spines respectively; 1-1, whole specimen under SEM; 1-2, 1-5, showing close-up of spinules with rounded tips and basal construction under SEM; 1-4, close-up of perforated tectum bearing scattered granules under SEM. Thespesia populnea. 2, 2-3, composite image of specimen in upper focus and optical section, showing spinose tectum and granulate sexine, and close-up of aperture, exine and spines respectively; 2-1, whole specimen under SEM; 2-2, 2-5, showing close-up of spinules with pointed tips and basal construction under SEM; 2-4, closeup of perforated tectum bearing scattered granules under SEM.

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Plate XIV. Polycolporate pollen. 1.

2.

Xylocarpus granatum. 1, 1-1, polar views of quadrangular and polygonal specimens with crassimarginate pores within colpi, and inset showing surface sculpture; 1-3, equatorial view in both high focus and optical section showing short colpus and crassimarginate pore that is wider than colpus; 1-2, 1-4, showing apertures and a scabrate to microgranulate tectum under SEM. Pemphis acidula. 2, composite image of specimen in equatorial view showing sexine slightly thicker than the nexine and surface as seen under LM; 2-1, optical section of specimen in polar view and inset showing surface sculpture; 2-2, 2-3, polar and equatorial views under SEM showing wide colpi, a psilate but finely pitted tectum, and microgranulate membranes of colpi.

types: A, Sonneratia alba, S. hainanensis, S. × gulngai; B, S. caseolaris; C, S. ovata; and D, S. apetala (Fig. 3). It should be pointed out that some species of Sonneratia are endemic to Thailand, south China (Wang and Wang, 2007) and Australia

(Duke, 2006), each having a very limited geographic distribution. Moreover, the systematic descriptions of some hybrids probably need to be revised to take into account their geographical variation, and observations on their pollen are necessary before a comprehensive

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Plate XV. Heterocolporate pollen. 1.

2.

Lumnitzera racemosa. 1, 1-3, high focus of polar and equatorial surfaces showing reticulate sexine and sub-rectangular pore; 1-1, 1-4, optical sections in polar and equatorial views; 1-2, 1-5 showing colpori, pseudocolpori and sculpture of exine under SEM; the tectum now appears to be more foveolate than reticulate; the fovea are larger on the outer parts of the lobes and at the poles. Lumnitzera littorea. 2, 2-3, high focus of polar and equatorial surfaces, tectum scabrate to foveolate; 2-1, 2-4, optical sections in polar and equatorial view; 2-2, 2-5, showing colpori, pseudocolpori and sculpure of exine under SEM; tectum more obviously finely pitted/foveolate; pores within three colpi rectangular, with long axis parallel to the equator.

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Fig. 3. Diagnostic characters of species of Sonneratia pollen under LM: wall structure in the polar caps, outlines in polar and equatorial view, and mesoporioum meridional ridges (arrows). SC, Sonneratia caseolaris; SA, S. alba; SHA, S. hainanensis; SG, S. × gulngai; SO, S. ovata; SAP, S. apetala. SC and SA show no distinct structure (after Mao et al., 2009).

key to all Sonneratia species and hybrids in Asia and Australasia can be established. Such observations could aid the taxonomic revision. So far, the morphology of the pollen of S. × urama, S. lanceolata and S. griffithii has yet to be documented. 7. Concluding remarks In this paper we have considered representatives of most of the mangrove genera that are found in tropical regions of the world. Our keys to the pollen and spores discussed will aid mangrove palynological analyses of Quaternary sediments in the SCS and coastal regions of south China and elsewhere in the Indo-Pacific region. The morphology of the pollen of a small number of species overlaps, probably rendering them difficult if not impossible to distinguish when found as dispersed fossils. This is inevitable for some taxonomically close species. Further work will be aimed at widening our examination to cover a number of mangrove species that remain to be investigated palynologically. Ideally, pollen and spore descriptions, illustrations and keys to all mangrove species are required, including variations that may be associated with different geographical populations, for palaeoecological analyses of Quaternary deposits associated with mangroves to be soundly based. Acknowledgments This work was funded by the National Natural Science Foundation of China (NSFC, Grants 40971029, 40771072, 41076034) and partially by the National Basic Research Program (973 Program, 2010CB951203). DJB was supported by Chinese Academy of Sciences Visiting Professorship for Senior International Scientists, CAS Innovation Programme (No. KZCX2-YW-QN112) and NSFC (Grant No. 41172011). We are indebted to Mr. C.R. Zhong and Mr. J.H. Chen for their valuable help with our mangrove vegetation survey and pollen sampling in the Dongzhai and Qinglan swamps on Hainan Island. We are grateful to Dr. W.Q. Wang for his attractive photographs of some of the mangrove plants (AC, AL, CE and RA in Plate I). Dr. M. Deng and Prof. Z.K. Zhou are thanked for their help with one specimen examination and sampling of anthers in the herbarium of the Kunming Institute of Botany. We are grateful to Drs. K.Y. Huang and S.X. Yang of Sun Yat-sen University for kindly sending us some

unpublished photographs of Rhizophora pollen, which enabled us to confirm their variation. The following illustrations have been published previously in a book by one of us on the pollen flora of Ryukyu, Japan (TF; Fujiki and Ozawa, 2007, in Japanese): Plate II, 1 (LM and SEM), 2-2; Plate VI, 1 (LM and SEM), 3-3, 4-3; Plate VIII, 1 (LM and SEM); Plate XI, 3-3, 3-4; Plate XIV, 2 (LM and SEM). Permission to include them in this paper has been granted by Akuakora Kikaku, Okinawa. References Alongi, D.M., 2009. The Energetics of Mangrove Forests. Springer Verlag, Heidelberg. xi + 216 pp. Baldibeke, M., Baldi, T., 1991. Paleobathymetry and paleogeography of the Bakony Eocene Basin in western Hungary. Palaeogeography, Palaeoclimatology, Palaeoecology 88, 25–52. Barui, N.C., 2011. Floral diversity of mangrove plants with reference to palaeoenvironment during Holocene in Bengal Basin, India. Quaternary International 229, 89–93. Bauermann, S.G., Evaldt, A.C.P., Branco, S.C., 2009. Pollen and spores atlas of the Cai River Valley, RS, Brazil. Revista Arvore 33, 895–905. Behling, H., 2002. Impact of the Holocene sea-level changes in coastal, eastern and central Amazonia, Amazoniana-Limnologia et Oecologia Regionalis Systemae Fluminis. Amazonas 17, 41–52. Behling, H., da Costa, M.L., 2004. Mineralogy, geochemistry, and palynology of modern and late Tertiary mangrove deposits in the Barreiras Formation of Mosqueiro Island, northeastern Para state, eastern Amazonia. Journal of South American Earth Sciences 17, 285–295. Behling, H., Cohen, M.C.L., Lara, R.J., 2001. Studies on Holocene mangrove ecosystem dynamics of the Braganca Peninsula in north-eastern Para, Brazil. Palaeogeography, Palaeoclimatology, Palaeoecology 167, 225–242. Berdin, R.D., Siringan, F.P., Maeda, Y., 2003. Holocene relative sea-level changes and mangrove response in southwest Bohol, Philippines. Journal of Coastal Research 19, 304–313. Berkeley, A., Perry, C.T., Smithers, S.G., Horton, B.P., Cundy, A.B., 2009. Foraminiferal biofacies across mangrove-mudflat environments at Cocoa Creek, north Queensland, Australia. Marine Geology 263, 64–86. Bian, Y., Jian, Z., Weng, C., Kuhnt, W., Bolliet, T., Holbourn, A., 2011. A palynological and palaeoclimatological record from the southern Philippines since the Last Glacial Maximum. Chinese Science Bulletin 56, 2359–2365. Blasco, F., Saenger, P., Janodet, E., 1996. Mangroves as indicators of coastal change. Catena 27, 167–178. Chateauneuf, J.J., Bauer, H., Cojan, I., 2006. An Avicennia mangrove in the Middle Miocene of the Digne area (SE France): stratigraphic and paleoclimatic implications. Comptes Rendus Geoscience 338, 197–205. Chester, P.I., Rains, J.I., 2001. Pollen and spore keys for Quaternary deposits in the northern Pindos Mountains, Greece. Grana 40, 299–387. Chumchim, N., 2010. Palynology of mangrove flora in Thailand. Unpublished Master's thesis, Chulalongkorn University, Chulalongkorn, 171 pp.

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